Soil Biology as Related to Land Use Practices : Proceedings of the VII International Soil Zoology Colloquium of the International Society of Soil Science (ISSS)


                                                                    PB8t-155251
       Sell Biology as Related to Land  Use  Practices
       Proceedings of the Seventh International  Soil
       Zoology Colloquium of the International
       Society of Soil Science (ISSS)
       (U.S.)  Environmental Protection  Agency
       Washington, DC
       1980
L
                off Commerce
          Technical Information Service

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BIBLIOGRAPHIC INFORMATION
PB81—155251
Soil Biology as Related to Land Use Practices: Proceedings
of the International Soil Zoology Colloquium (7th) of the
International Society of Soil Science (.ESSS) Held at
Syracuse, New York on July 29—August 3, 1979,
1980
PERFORMER: Environmental Protection Agency, Washington, DC.
Office of Pesticides and Toxic Su)stances.
EPA—560/1 3—80-038
Prepared in cooperation with State Univ. of New York ct
Syracuse. Coll. of Environmental Science and Forestry.
Partial contents: Influence of pesticides on soil organisms;
Human waste disposal and soil organisms; Anthrophilic
relationships of soil organisms; Relationships of soil
organisms to agronomic practices and animal wastes;
Influence of mining site modification and rehabilitation of
soil organisms; Effects of silvicu]tural practices on soil
organisms; Human impact on tropical soil ecology; Basic soil
ecology: Nutrient cycling, mioroorganism—faunal
relationships, feeding and reproductive strategieE.
KEYWORDS: *Microorganiams, *Invertebrates •Soils,
*Meetings.
Available from the National Technical Information Service,
Springfield, Va. 22161
PRICE CODE: PC A99/MF AOl
i

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C/EPA
             'jntodStawt
             Cnvironmentil ProMctton
             Offte* Of Pi'«icide
             and Toxic Subiuncet
             WasXiniton, DC 20460
                                      tPA-KC/13-80038
             Toxic SubittiKM
Soil  Biology as Related
to  Land Use Practices
Proceedings of the VII
International Colloquim
of Soil Zoology

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SOIL BIOLOGY
AS RELATED TO
LAND USE PRACTICES
Proceedin s of the VII International Soil Zoology Colloquium of the International Society of Soil
Science (ISSS)
Daniel L. Dindal, Editor
1980
e Organized by the State University of New York, College of Environmental Science and Forestry.
Held in Syracuse, New York USA, July 29 — Augu; t 3, 1979
‘
LITP Published by the Office of Pesticide and Toxic Substances, EPA, Washington, D.C.

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PREFACE
In 1976, at Uppsala, Sweden while attending the VIth Colloquium, I
extended an official invitation from the State University of Naw York
College 0 f Environmental Science and Forestry (SUNY CESF) to coninence
the VIIth International Colloquium on Soil Zoology on our campus. This
Invitation was graciously accepted.
Organizational plans were quickly underway for the meeting to be
held in Syracuse in 1979. From July 29 through August 3 of that year,
135 peoie, interested in various facets of soil biology, met In a
very scholarly and congenial atmosphere. Twenty-seven countries from
around the world were represented with representatives from five
Canadian Provinces and nineteen states from the US on hand.
Being able to organize and take part in such a prestigious con-
ference on our campus has been one of the highlights of my career. And
the interest, cooperation and eager participation by all attendees
helped make the colloquium so successf .jl.
Of course, one 0 f the main values of such an international meeting
Is the timely production of the published proceedings. Through the co-
operation of the Office of Pesticides and Toxic Substances of the USEPA
this objective was realized.
As editor of these proceedings. I compiled and organized the oapers
In a subject-related manner. Most of my editorializing was of a
mechanical nature. A proceedings should be as accurate a reflection of
the papers presented as possible. Therefore, no papers were deleted
even though some readers may feel the manuscripts lack quality. Each
oaper as part of the conference helped to develop the character of the
total meeting and was, for this reason, included.
All particirants were initially given a format to follow in pre-
paration of their papers. In general, most fol1ov ed these directions
very closely for which I am appreciative. Abstracts were optional so
they may or may not be present.
It has been a pleasure dealing with all the participants.
Daniel 1. Dlndal
Syracuse, NY
May 1, 1980
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ACKNOWLEDGMENTS
My appreciation Is extended to the staff of the School of Continu-
ing Education) under the direction of Dr. John N. Yavorsky, for valuable
assistance with all aspects of planning for the meeting facilities,
dining and living quarters and field trip arrangements. As the partici-
pants will recall, the unwavering energy exhibited by Alan L. Hankin was
extraordinary. Also, Dr. John F. Simeone. chairman of the Department of
Environmental and Forest Biology &serves thanks for his he’p, interest
and participation. Bruce G. Stevenson and James I4cflvain were very
diligent In gathering an recording the questions and answers of each
speaker. Jeffrey Waugh volunteered his services as a driver for the
ield trip, and Michael S. Fisher very professionally acted as the
ohauffeurfor the special trips organized for wives of attendees.
Finally, I acknowledge all the invaluable assistance Cf my wife,
Anna Jean Dinial. In addition to her Involvement in the conference
3rganlzation and organizing and guiding the accompanying women’s program
she was truly a major factor behind getting these proceedings compiled
and produced. Publication at this time would have been impossible with-
out her.
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OFFICiAL WELCOME
Donald F. Behrend
Vice President of Program Affairs
SUNY CESF. USA
Good morning and welcome to the Seventh International Soil
Zoology Colloquium. Both Chancellor Wharton and President Palmer join
me In welcoming you to the State University of Net. Y,rk College of
Environmental Science and Forestry.
We are pleased and honored that you have chosen to meet here to
pursue the thene of soil btol gy as related to land use practices.
Th s thene, being followed by scientists from 30 natIons around the
world, may be viewed as a microcosim of our entire College. Thus, In
the CESF we are consciously striving to understand the basis for our
environment, how our environment causes Impacts on us and how we cause
impacts oi it; and, how we can modify our utilization of the resources
provided by our environment in order to maintain its diversity, stability,
and long term productivity.
Soil Is, of course, one of the absolutely crucial elenents of the
system we call our environment. As a practicing wildlife biologist, I
appreciated this many years ago; but in an extremely simplistic way.
Along with many others, I viewed soil as a relatively simple system of
physical and chemical censtltuents which supported plant life which, in
turn, supported, either directly or indirectly, vertebrate animals, and
harbored some troublesorie parasites. Now, thanks to your continuing In-
vestigations, a broad array of scientists, land managers, and policy
makers are fast beco,ninq aware of the complex and fragile nature of the
soil systems which are an integral part of the spaceship earth on which
we are all fel ow journeyers.
I am particularl. heartened j the broad scope of your delibera-
tions this week as evidenced by the . sessions in your program. In
addition to basic soil ecology, a perusal of the program Indicates that
areas from the arctic to the tropics are covered, along with agricultural.
silvicultural, mining, •nd other specific land uses. Additionally, it
Is encouraging to see the critical areas of pesticides and human waste
disposal included In the program. Another topic which needs Increasing
attention is the impact of chemical contamination on soil communities
and the potential role of these communities in decontaminating soils.
It seems to me that the recent recognition of the broader and
more complex role of soil in supporting our environment has set the
staqe for even greater strides in soIl biology. Environmental quality.
agriculture, forestry, non-renewable resource extraction and associated
V

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land reclamation, energy production from biomass (including heat from
decomposition), are some of the areas of study which immediately come
to mind.
Row rapidly you ma.y make strides In these and other areas de-
pends to a large degree on your overall approach. I think It Is
essential that the context you create, the perspective you project
be truly ecological in nature. This will permit you to communicate
more effectively with scientists from other disciplines and with
managers and policy makers. You should also strive to make clear the
relatiorships of basic research to the future application of knowledge
to the probloms of both today and tomorrow. Finally, we must all ijork
together to find timely and effect 4 ve means to communicate the results
of your work to a broad array of audiences.
The program of the Seventh International Soil Zoology Colloquium
clearly indicates that you are well along the way toward these goals
and objectives. I hope that your efforts here this week will be
successful in moving you even farther and faster. And with the con-
tinuing attention of Dr. DIndal, Dean Yavorsky and my other College
colleagues. I am certain that your stay with us will be pleasant as
well as productive.
Again, thank you for honoring us with your visit; and, again,
welcome to the SUNY College of Environnental Science and Forestry.

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TABLE OF CONTENTS
PREFACE i i i
ACKNOWLEDG’IENTS
OFFICIAL WELCOME: Donald F. Behrend v
SESSION I: INFLUENCE OF PESTICIDES ON SOIL ORGANISMS
Moderators C.A. Edwards 1
INTERACTIONS BETWEEN AGRICULTURAL PRACTICE AND
EARTHWORMS
C.A. Edwards 3
ACCUMULATION OF ORGANOPHOSPHORUS INSECTICIDES IN
EARTHWORMS AND REACTIONS OF EARTHWORMS AND MICRO-
ORGANISMS TO THESE SUBSTANCES -
0. Atlavinyté, A. Lugauskas and G. Ki1ikevi iu.s 13
GROWTH OF BASIDIOMYCETES IN THE PRESENCE OF AGP.O-
CHEMICALS
G.J.F. Pugh and M.J. MacDonald 25
RELATION BETWEEN SPECIES LISTS AND TOLERANCE TO
NEMATICIDES
Diana W. Freckman, Lawrence B. Slobodicin and
Charles L Taylor
A PRELIMINARY STUDY OF THE USE OF SOME SOIL MITES
IN BIOASSAYS FOR PESTICIDE RESIDUE DETECTION
Ph. Lebrun 42
EFFECTS OF S]X BIOCIDES ON NON-TARGET SOIL MESO-
ARTHROPODS FROM PASTURE ON STE. ROSALIE CLAY lOAM
ST. cLE’r, QUEBEC
Thomas D. Smith 7 D. Keith McE. Kevan and
Stuart B. Hill .56
EFFECTS ON LINDANE, CARBARYL AND CHLORPYRIPOS ON
NON-TARGET SOIL ARTHROPOD COMMUNITIES
James B. Hoy
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EFFECTS OF CARBOFURAN ON THE SOIL MICROARTHROPO1)
COMMUNITY IN A CORNFIELD
kB. Broadbent and AD. Tomlin 82
INFLUENCE OF APPLICATION C.F A FUNGICIDE AN INSECT-
ICIDE AND COMPOST UPON SOIL BIOTIC COMMUNITY
Yuzo Kitazawa and Talcashi Kitazawa
EFFECT OF TWO HERBICIDES ON THE SOIL INHABITING
CRYPTOSTIGMATID MITES
r. Bhattacharya and V.C. Joy 109
SESSION II: HUMAN WASTE DISPOSAL AND SOIL ORGANISMS ’
Moderator K.H. Domsch 1.19
BIOLOGICAL SUCCESSION IN ARTIFICIAL SOIL MADE OF
SEWAGE SLTJDGE AND CRUSHED BARK
Veilcko Huhta, Veronica Sundman, Eeva tkonen,
Seppo Sive1 , Tuula Wartiovaara and Pekka
Sli lkamaa 1.21
DECOMPOSITION PROCESSES IN SEWAGE SLUDGE AND SLUDGE
AMENDED SOILS
M.J. Mitchell arid S.G. Homer 129
SOIL MICROFAUNA OF OPEN DRAINS IN MID-DEI/FA EGYPT
Mohsei Shoukrv Tadros 139
LEAD AI I’D CADMIUM CONTENT IN EARTHWORMS (LUMBRI CIDPiE)
FROM SEWAGE SLUDGE AMENDED ARABLE SOIL
Caspar Andersen
VERMICO! POSTING ON A HOUSEHOLD SCALE
Mary Appeihof 157
RECLYLTIVATION OF REFUSE TIPS: SOIL ECOLOGICAL STUDIES
W. Broclcmann, H. Eoehler a-d T. Schriefer i6i
SESSION III: ANTHROPHILIC RELATIONSHIPS OF SOIL
ORGANISMS ..
Moderator: Arlan L. Edgar 169
PHYSIOLOGICAL AND ECOLOGICAL AS7ECTS OF THE CCSMO-
POLITAI4I OPILIONID Phalangluin opilio
Arlan L.. Edgar 170
viii

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ACTIVE AND PASSIVE DISPERSAL OF LUMBRICID EARThWORMS
Donald P.. Schwert 18
HORIZONTAL MOVEMENTS IN A NATURAL POPU lATION OF
Fntoinobrya socia IN A LAWN
Elizabeth S. Waldorf 190
THE EFFECTS OF TRAMPLING ON THE FAUNA OF A FOREST FLOOR.
I • MICROARTHROPODS
Irene Garay, Jorge Cancela Da Fr. eca and Patrick
Blandin 200
THE EFFECTS OF TRAMPLING ON THE FAUNA OF A FOREST
FLOOR. I!. MACROARTHBOPODS
Spyros Molfetas and Patrick Blandin 213
SOIL MITE COMMUNITIES IN THE POOREST ENVIRONMENT
UNDER THE ROADSIDE TREES
Jun—ichi Aoki. and Genic1 i Kuriki 226
SESSION IV : . . T .AITIONSHIPS OF SOIL ORGAN Q
AGRONOMIC PRACTICES AND ANIMAL WASTES
Moderator: Pb. Lebrun 233
Reterodera avenae Woll. (NENATODA: TYLENcHIDA) THC
CEREAL CYST NEMMIODE: RELATIONSHIPS BETWEEN ITS POP-
ULATION DENSITY WHEAT GROWTH AND YIELD AND SOIL
VARIABILITY IN SOME SOUTH AUSTRALIAN WHEAT FIELDS
K.E. Lee and J.C. Buckerfield 2 3 ie
SOIL FAUNA IN O VEGETABLE CROPS GROWN UNDER PLASTIC
TUNNELS
Mosben Shoukry Tadros and Abdel—Fattab S.A. Saad 2 l9
BEACH SOIL MICROFAUNA IN lOWER EGYPT
Z4ohsen Shoukry Tadros 257
EFFECT OF NPK COMPLE C FERTILIZERS ON YIELD OF PADDY
RICE AS RELATED TC THE FAUNA AND WATER INFILTRATION
RATE OF SOIL OF THE NILE DELTA
S. E—D. A. Faizy, N. Tudros, S.A. Gaheen and
S. El Krady 263
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THE ABUNDANCE OF SOIL ANIMALS (MICROARTHROPODA,
ENCHYTRAEIDAE, NENATODA) IN A CROP ROTATION
DOMINATED BY LEY AND IN A ROTATION WITH VARIED CROPS
Olof Andrén and Jan Lagerlöf 274
COMPARISON OF MINERAL ELEMENT CYCLING UNDER TILL
AND NO-TILL PRACTICES: AN CPERIMENTAL APPROACH TO
AGROECOSYSTEMS ANALYS IS
Benjamin R. Stinner and D.A. Crossley Jr. 280
EFFECT OF MEADOW MANAGEMENT ON SOIL PREDATORS
A. Kajak 289
INFLUENCE OF AGRICULTURE ON THE OUTBREAK OF WHITE
GRUBS IN INDIA
G.K. Veeresh 301
THE INFLUENCE OF AGRICULTURAL LAND USE PRACTICES ON
THE POPULATION DENSITIES OF Allolobophora trapezoides
AND Eisenia rosea (OLIGOCRAETA) IN SOUTHERN AFRICA
A.J. Reinecke and F.A. Visser 10
THE INFLUENCE OF FARMYARD MANURE AND SLURRY ON THE
EARTHWORM POPULATION (LUMBRICIDAE) IN AMBLE SOIL
Casper Andersen 325
EFFECTS OF HEAVY PIG SLURRY CONTAMINATION ON EARTH-
WORMS IN GRASSLAND
J.P. Curry and D.C.F. Cotton 336
EARTHWORMS AS BIOLOGICAL MONITORS OF CHANGES IN
HEAVY METAL LEVELS IN AN AGRICULTURAL SOIL IN
BRITISH COLUMBIA
Alan Carter, Elizabeth A. Hayes and L.M. Laukulich 344
INFLUENCE OF TRAMPLING OF A HORSE MANADE IN CAMARGUE
ON THE SOIL FAUNA AND THE FAUNA OF CANOPY
Nicole Poinsot-Balaguer and L. Boigot 358
SESSION V: — INFLUENCE OF MINING SITE MODIFICATION AND
REHABILITATION ON SOIL ORGANISMS
Moderator: Dennis Parkinson - 361
RESTORATION OF FUNGAL ACTIVITY IN TAILING SAND (OIL
SANDS)
D. Parkinson 1 S. Visser, R.M. Danielsor. and J. Zak 362
FUNGAL SPECIES ISOLATED FROM THE SENESCENT LEAVES OF
yraudia arundinacea GROWING ON AREAS DISTURBED BY
IRON-ORE MINING ACTIVITIES
M.H. Wong and S.H. Kwan
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RESPONSE OF FIELD POPULATIONS OF TARDIGRADA TO VARIOUS
LEVELS OF CHRONIC LOW-LEVEL SULPHUR DIOXIDE EXPOSURE
J. W. Leethain, T.J. McNary, J.L. Dodd and W.K..
Laur ’ nroth 382
THE EFFECT OF AN INCREASED Ra CONTENT IN THE SOIL ON
SOIL ANIMALS
DA. Xrivolutsk 391
COLLEMBOLA OF REHABILITATED MINE SITES IN WESTERN
AUSTRALIA
Penelope C-reenslade and J.D. Majer 397
EARTHWORMS ON FORESTED SPOIL BANKS
William E. Hamilton and JP. Viminerstedt 409
SESSION VI EFFECTS OF SILVICULTURAL PRACTICES ON
SOIL ORGANISMS ;
Moderators Veikko Huhta +l9
TIE EFFECTS OF HARVESTING PRACTICES ON ORIBATID MITES
AN)MINERAL CYCLING IN A SITKA SPRUCE FOREST SOIL
Alison P. Frater 420
$SMENT OF TOXIC EFFECTS OF T E HERBICIDE 2, 4, 5-T
O THE SOIL FAUNA BY LABORATORY TESTS
H. Eijsackers 427
E1?FECTS F DRAINAGE UPON THE SPIDER FAUNA (ARANEAE)
OF THE GROUND LAYER ON MIRES
Seppo Koponen
STUDIES ON REQUIREMENTS AND POSSIBILITIES DF ZOO-
AMELIORATION OF AFFORESTED ARABLE LAND
Andrzej Szujecki, Stanislaw Mazur, Ja-t Szyszko,
Stanislaw Perlinski and Heriryk Tracz
EFFECTS OF FIRE ON SOIL FAUNA IN NORTH AMERICA
Louis J. Metz and Daniel L. Dindal 450
EXPERIMENTAL STUDY OF THE DIRECT EFFECT OF LITTER
BURNING ON SOIL MICROARTHROPODS IN A DECIDUOUS
TEMPERATE FOREST
Guy Vannier 460
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SESSION VII: HUMAN IMPACT ON TROPICAL SOIL ECOLOGY
Moderatori G.K. Veeresh
EFFECT OF THE ANNUAL BURNINGS ON TESTACEA OF TWO KINDS OF
SAVA AH IN IVORY COAST
Marie-Madeleine Co Iteaux 1i 66
EFFETS A COURT TERME DE LA DEFORESTAT ION A GRANDE
ECHELLE DR LA FORET DENSE HUMIDE EN GUYANE FRANCAISE
SUR LA MICROFAUNE ET LA MICROFLORE DU SOL
J7M. Betech, G. Kilbertus, J. Protth, M.C. Betsch-
Pinot, M.M. Co teaux, G. Vannier and B. Verdier
RELATIONSHIPS OF SOME ISOTOMIDAE (COLLEMBC LA) WITH
HABITAT AND OTHER SOIL FAUNA
Penelope Greenslade and P.J.M. Greenslade k91
FEEDING BEHAVIOR AND FUNCTIONAL ECOLOGY OF TERMITES
OF A TROPICAL SAL FOREST
Udai Raj Singh 507
SESSION VIII: BASIC SOIL ECOLOGY: NUTRIENT CYCLING,
MICROORGANISM-FAtJNAL RELATIONSHIPS, FEEDING AND REPFO-
DUCTIVE STRATEGIES
Moderator: Stuart B. Hill .521
THE FATE OF CATIONS IN BEECH AND SPRUCE LITTERS
INCUBATED situ
G. Parmentier 1 P.. Buidgen and J. Remade 522
ANNUAL CARBON, NITROGEN AND CALCIUM TRENDS IN LITTER
AND SURFACE SOIL OF A MIXED HARDWOOD STAND
Mark F. Tardiff and Daniel L. Dindal 529
KINETICS OF N-K INTERACTION AS RE lATED TO STEM ROT
INFECTION AND WATER HOLDING CAPACITY OF LEAP TISSUES
OF TOMATO PLANTS
S.E-D. A. Faizy
SULPHUR TRANSFORMATIONS IN OXYGEN-LIMITED SYSTEMS:
SOILS SEDIMENTS AND SLUDGES
S.G Hornor 1 7.H. Waugh and M.J. Mitchell 54.8
ON THE INCIDENCE AND DISTRIBUTION OF PARASITES OF
SOIL FAUNA OF MIXED CONIFEROUS FORESTS 1 MIXED LEAP
FORESTS, AND PURE BEECH FORESTS OF LOWER SAXONY
WEST GERMANY
Kurtesh Purrini 561
xii

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IN±’ERACT IONS BETWEEN NEMATODES AND BACTERIA IN
HETEROTROPHIC SYSTEMS WITH EMPHASIS ON SEWAGE
SLUDGE AND SLUDGE AMENDED SOILS
Bonnie I. Abran s and Myron J. Mitcheil 583
USE OF MICROARTEROPODS (MITES AND SPRINGTAILS) AS
VALUABLE INDICATORS OF SOIL METABOLIC ACTIVITY
Guy Vannier 592
THE ROLE OF INVERTEBRATES IN PHE FUNGAL COLONIZATION
OF LEAF LITTER
David A. Pherson
EVOLUTIONARY ASPECTS OF MYCOPHAGY IN Ariolimax
coluinbianis AND OTHER SLUGS
Klaus 0. Richter 616
THE USE OF COTTON STRIPS IN A MICROCOSM STUDY OF
THE ENERGY COST OF A PREDATOR-PREY RELATIONSHIP
J.A.. Springett 637
A NEW TECHNIQUE FOR THE ANALYSIS OF THE DIGESTIVE
TRACT CONTENT IN CARABID BEETLES
G. Benest and Z. Massoud 643
THE GEOPHAGOUS EARTHWORMS COMMUNITY IN THE LANTO
SAVANNA (IVORY COAST): NICHE PARTITIONING AND LAND
UTILIZATION OF SOIL NUTRITIVE RESOURCES
Patrick Lavelle, Boubacar Sow and Roger Schaefer 653
DEVELOPMENT AND FECUNDITY OF THE MANURE WORM Eisenia
foetida (7 nnelida: Luinbricidae) UNDER LABORATORY
CONDITIONS
A.D. Tontlin and J.J. Miller 6
SEASONAL VARIATIONS OP SEC-RATIO IN FOREST GROUND-
BEETLES NATURAL POPULATION
Gil].es Benest and ].P. Cancela da Fonseca 679
INTRODUCTIONS EN SURPOPULATION ET MIGRATIONS DE
LOMBRICIENS MARQUES
Denis Mazaud and Marcel B. Bouch 687
SESSION IX: BASIC SOIL ECOLOGY: SOIL ECOLOGY OF THE ARCTIC
AND DESERTS; STRUCTURE AND FUNCTION OF SOIL ORGANISM
O UNITIES
P.derator: M.B. Bouch 703
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INFLUENCE OF INDIVIDUAL PLANT SPECIES ON THE DIS-
TRIBUTION OF ARCTIC COLLEMBOLA
J.A. Addison 7011
DISTRiBUTION AND DIVERSITY OF NORTH AMERICAN P RCTIC
SOIL ACARI
Valerie M. Behan and Stuart B. Hill 7 17
ASPECTS OF THE ECOLOGY OF ANTARCTIC SOIL FAUNA
WilUam Block 7 1l
DESERT SOIL MICROARTHROPODS: AN ‘r’ - SELECTED SYSTEM
John W. Wall.work . 759
ARTHROPODS AND DETRITUS DECOMPOSITION IN DESERT
ECOSYSTEMS
Walter G. Whitford and Perseu F.. Santos 770
SOIL ANIMAL SPECIES DIVERSITY IN A SEPARATED DUNE
GRASS LAND ECOSYSTEM
Ryszard F. Cykowski 779
DIVERSITY TRENDS AMONG THE INVERTEBRATE LITTER
DECOMPOSEP.S OF A SUBALPINE SPRUCE-F iA SERE: A TEST
OF ODUM • S HYPOTHESES
Lloyd W. Bennett and Richard T. Vetter 785
SYNECOLOGY OF FOREST SOIL ORIBATID MITES OF BELU’J) ;
I. THE ZOOSOCIOLOGICAL CLASSES
Georges Wauthy and Philippe Lebrun 795
POPULATION DYL’IAMIC AND METABOLIC CHARACTERIZATION OF
COLLEMBOLA SPECIES IN A BEECH FOREST ECOSYSTEM
Henning Petersen 806
ACTIVITY OF SOIL BIOTA O IRING SUCCESSION FROM Ot’ FIELD
TO WOODLAND
A uyan acfadyen 8 4
SESSION X: CLOSING
Moderator: Daniel L. Dindal 847
‘r’ WORMS AND’K’ WORMS: A BASIS FOR CLASSIFYING LUMBRICID
EARPHWORM STRATEGIES
J.E. Satchell - 848
xiv

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SOIL FAUNA STUDIES FOR SOLVING PBOBLEMS OF 310-
GEOGRAPHICAL CONNECTIONS
MS. Ghilarov
LIST OF PARTICIPANTS 871
LIST OF ADDITIONAL ‘CONTRIBUTORS 878
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SESSION I: INFLUENCE OF PESTICIDES ON SOIL
ORGAN ISMS
Moderator: C. A. Edwards
Rotham.cted Experime ta1 Statiot
Harpeuden. England
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INTERACTIONS BETWEEN AGRICULTURAL PRACTICE AND
EARTHWORMS
C. A. Edwards
ollnimcSd Exp.rimrnffil SMI ,on
‘iarpi’nde,, England
INTRODUCTION
There are earthworms in most agricultural soils in both
temperate and tropical regions, althocgh the species may differ
in different parts of the world. The conversion of natural
forest or prairie into a regularly cultivated system involves
considerable changes in the soil as a habitat so that Species
that can withstand repeated soil disturbance and a relatively
limited supply of orjanic matter, are favoured at the expense of
those that cannot.
Since the publication of Charles Darwin’s book, ‘The
Formation of Vegetable Mould Through the Action of Worms’ (1881),
there have been many reports that earthworms are important in
hreakinç down plant organic matter and incorporating it into soil,
forming soil aggregates and improving soil stricture, aeration and
drainage. There have also been reports that earthworms improve
mineral availability and general soil fertilit) (Edwards and
Lofty, 1977, 1979). Nevertheless, there has been relatively little
discussion as to how this is achieved nor how tha various forms of
agricultural practice affect earthworm poFulation’i an , conversely,
how earthworms influence the growtn of crops. Work on these
subjects has been in progress at Rothamsted since 1961 .nd this
paper summarizes some of the main findings of this programme and
zelates them to the requirements of modern agriculture.
METHODS
The field experiments in which the influence of agricultr ral
practice on earthworm populations have been assessed, all in ol e
small plots (ranging from five metres square to 30 m x 10 m) usually
replicated four times. The experimental cultivations, strawburning,
arid applications of fertilizers and pesticides to these experiiv.ents
have all followed normal agricultural practice and used recommended
doses nd timing of treatments.
E rthwurm populations were assessed on the basis of four
half metre square quadrats per plot (usually a total of 4 m 2 /
for four plots). On to each quadrat, 9.2 1 of water containing
50 ml formaldehyde were poured gradually from a watering can and
the earthworms coming to the surface of the quadrat removed and
3

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stored in 5% formalin until they could be weighed and ident fied
to species.
The effects of pesticides an:i fertilizers on earthworms and,
in particular, uptake of chemicals into earthworm tissues have also
been assessed in 1abora ory box tests. These tests have involved
setting up cultures of ten earthworms (usually Lumbricus terrestris
1. or Allolobophora caliginosa Savigny) in medium clay loam
sterilized soil, contained in boxes 25 cm square and 40 cm deep,
kept at 25% moisture content and 15°C (Edwards, 1979). To assess
the effects of fertilizers and ,esticides, the ch€micals were mixed
thoroughly into the soil before the worms were added; the boxes
were dismantled and mortality assessed at I — 2 weekly intervals.
Some experiments have irvolved the inoculation of earthworms
into field sites to study their effects, and to do this the
earthworms were spread evenly over the surface of small plots and
covered with a large polythene sheet for 24 hoL’rs until they had
burrowed into the surface soil. There was virtually no atera]
migration from these small plots and very good survival of the
worms.
REFULTS A4D DISCUSSION
1. Effects of pesticides
The literature on effects of pesticides on earthworms has
already been reviewed thorough’.y (Davey, 1963; Edwards and
Thompson, 1973; Edwards and Lofty, 1977) and will not be con-
sidered here, except where results disagree with those obtained at
Rothamsted.
Pesticides can kill earthworms and can also accumulate in
worm tissues. Moreover, earthworms can move pesticides absorbed
in their tissues from the soil surface into deeper soil where most
of the pests live, thereby often increasing the effect iv ness of
the pesticide. Some pesticides are degraded within tJo tissues of
earthworms; for instance, even the most stable pesticide, DDT
becomes degradea to DDE in earthworms (Edwards and Jpffs, 1974).
Fortunately, most pestacides do not kill earthworms at
normally recommenoed doses, which makes it even more difficult to
have some assessment 0 r the relative toxicity of different pesti-
cides to them. rhe relative toxic.i.ty of a wide range of pesticides
to earthworms is summarised in Table I which is sri overall assess—

-------
TABLE 1 LATJVE TOXICITY OF PESTICIDES TO EARTHWORMS
Chemical Use Relative toxicity to
earthworms
Chioropicrin Wematicide * * * * *
D—D ‘I
Methyl bromide ft * * * * *
Methem sodium U * * * * *
Aldicarb I ’ * * *
Dazomet *
Thionazin * I’
Methomyl Ut * *
Chiordane Organochiorine * * * *
insecticide
Endrin
Heptachior * * *
Di T 0
Dieldvin 0
Aidrin 0
BHC (lindane) 0
Phorate Orga 1 .opho phate * * * * *
insecticide
Parathion * * *
Fonofos II * *
Trichiorphon
Fenitrothion 0
Tetrachiorvinpos 0
Disulfoton (I
Malathion 0
Menazon 0
Ch].orfenvinphos 0
Carbaryl Carbamate * * * * *
insecticide
Carbofuran 1 * * * * *
Benomyl Carbamate * * * * *
funcjicide
Thiophanate methyl U * * * * *
Carbendaiim * * * * *
Methiocarb Carbamate * * *
molluscicide
Simazine Herbicide *
Cyanazine ‘I * *
Chiorthiamid *
DNOC *
Benzoylpropethyl 0
Linuron U U
Monuron 0
Peraquat 0
Dalepon tI 0
Triallate 0
S
5

-------
* * * * Extremely toxic
* * * * Moderately toxic
* * * Intermediately toxic
* * Slightly toxic
* Very slightly toxic
o Non—toxic
ment based on both laboratory end field tests. Most nematicides
tend to be broad—spectrum biocides and are therefore to varying
degrees toxic to earthworms and, in particular, the fumigant
nematicides chioropicrin, 0 — D, methyl bromide and metham sodium
are vory toxic to worms. Of the organocnlo ine in-scticides,
only chlordane is very toxic to earthworms with endrin slightly
less so, but these paticides are readily abwrbed from soil into
earthworms’ tissues, so that there can be as much as ten times
the concentration of the chemical in the tissues as in the
surrounding soil.
Organophosphate insecticides seem to be the least toxic
pesticides to earthworms, only phorate being very toxic with
parathion rather less so. Only small amounts of organophosphate
insecticides ru taken up into earthworm tissues. All of the
carbamate pesticides seem to be relatively toxic to earthworms.
Most herbicides are not directly tc i c to earthworms (only the
triazines being slightly toxic) but herbicides have very consider-
able indirect effects on earthworms by &anging the surface
vegetation which ultimately provides SOt? organic matter.
Earthworms are considered to be sufficiently important
test organisms for the British Pesticide Safety Precautions Scheme
(linked to the registration scheme: to require pesticide firms to
provide earthwoi m toxicity data (Edwards, 1978).
2. Effects of fertilizers
Fertilizers, either organic or inorganic, are applied to
most agricultural crops. In some long term experiments at
Rothamsted, the same fertilizers have been applied annually to
plots of grass, root crops or wheat since the 1340’s, in what are
teru ed the ‘Classical experiments’. Fluctuations in the earthworm
populations in these plots and in other shorter term experiments have
demonstrated clearly how fertilizers effect numbers. In all
expeciments, populations increased after application of dung or fish
meat. and other organic fertilizers. The deep-burrowing species
LLambricus terrestris increased, particularly. Balanced mineral
t rtilizers containing N, P, K, P s and Ng have cat sed slight
ir.creases but large doses of amwonium nitrogen have decreased earth-
worm numbers significantly probably because such treatment increases
soil acidity (Fig. 1). These cor c1usions have been supported by
6

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kO.
uther species
Lumbricus tex’rpstris
[ ] H
30 -
p. I
ra1G
c4
Nitrogen level
FIGURE 1. EFFECTS OF NITROGEN (AMIIONIIJM SULPHATE) ON EARTHWORM
POPULATIONS (N 1 = 48 kg/ha, N 2 96 kg/ha, N 3 = kg/ha)
data from other workers (Edwards and Lofty, 1975b). Other nitro-
genous fertilizers, particularly calcium nitrate (‘nitro—chalk’),
and the addition of lime to soil, favour the build—up of most
species of earthwori .
More recently, sewage sludge, sewage cake, animal slurries
and waste from breweries have been used as organic fertilizers and
our results have shown that although some of the raw forms may
kill a few earthworms they usually increase populations, evertually
quite considerably. Unfortunately, there can be some uptake of the
heavy metals Pb, Zn and Cd into earthworm tissues from the sewage
materials.
3. Effects of cultivations
Grassland tends to contain more earthworms than arable land,
but it is not certain whether this is due to regular disturbance of
the habitat by cultivation or to lower levels of soil organic
matter in ploughed fields. An experirr.ent at Rothemeted investigated
the effects on earthworm populations of ploughing up old grassland
and using either the maximum or minimum additional cultivations
before reseeding to gre8s; the effects of doing this once were
compared with those of repeating the cultivations annually.
During the first two seasons, the overall earthworm populations
L
7

-------
iticreased in all the reseeded plots compared with the unculti-
vated ores but most of the increase was of the shallow-working
species; with repeated reseedin. , populations, particularly of
the deep-burrowing species, began to decrease. The conclusion
was that many species of earthworms could withstand repeated
cultivations but populations decreased as the organic matter
content of the soil fell.
Investigations into the impact of cultivations on earth-
worm populations have been given new impetus by the practice
known as ‘direct drilling’ in England and ‘no-till’ farming in
the U.S.A. This involves killing an existing crop with a broad—
spect:un herbicide and reseeding directly with a special drill
that drops the seed into a slot cut in the soil. This is becamin
more popular since 1973 because of considerable savings in energy
and labour and also because it minimizes soil erosion; in England
half a million hectares of crops are currently sown this way.
Investigations at Rothamsted on 24 field ex ’eriments and in a
field survey have shown that populations of deep-burrowing species
such as L. terrestris and Allolobpphora longs tend to build up
spectacularly iith repeated direct drilling, although the effects
on numb€rs of shallow—working species are much less (Edwards, 1975;
Edwards and Lofty, 1975a). Some of the changes in earthworm
populations in two long term experiments ate si.mmarised in Figure 2.
‘gGoo
5O0
300
200
100
B.
ir L _
Deepoburrowing app. Sha11ow. working app.
FIGURE 2. RELATIVE CHANGES II EARTHWORM POPULATIONS RESULTING
FROM DIRECT DRILLING
A. Boxworth
1760
3730
7th
year year year year year
8

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and
present.
Other experiments in both field and laboratory have shown
that earthworms are important in promoting the root growth of
direct drilled cereals by providing suitable tunnels and spaces
lined with available nutrients in the relatively compacted soil.
Moreover since some earthworm burrows go deeper than tne plough
pan, rcots penetrate deeper than in picughed soil.
Th.zs, it has been established that the greater the intensity
frequency of cultivations generally the fewer earthworms are
4. Strawburnin9
The practice of burning straw in cereal fields after harvest
is common in Fr i1.and, about 50% of all cereal straw being currently
disposed of in this way. The effects of etrawburning on earthworm
populations has been investigated since 1974 at Rothamated. In
one long—term experiment, the effects of chopping straw and spread-
ing it evenly over some plotb were compared with doing the same and
burning the straw, baling and removing the etraw, and leaving the
sir .iw in uwathes over the rows nd burning it. The burning or
removal of straw had little effect on earthworm populations in the
ftrst year, a slight effect after the second tresiment but, by the
third and fourth years, populations of the deep—burrow nq
L. terrestris had decreased dramatically, and to a lesser ext ent
so had those of the shallow-working A. caliginosa . By contrast,
burning favoured populations of Allolobophora cTilorotica (Savigny)
(Figure 3) (Edwards and Lofty, i 79J ,
FIGURE 3. THE EFFECTS OF STRAW DISPOSAL ON EARTHWOV POPULATIONS
(after three successive yearij
9

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4
There seems little doul.t that the :‘rtual burning had little effect
on earthworms but that populations of those species dependent upon
the availability of surface organic matter were soon aEfected.
5. Rotations
There is very li 4 tle evidence on the influence of rotetions
un earthworm populations. However, the data that have been
accumulated at Rothamsted, indicate that earthworm populations tend
to build up under continuous cereal cropping much more than in
three or four course rotations involving such crops as beans,
potatoes, oil seed rape or fodder crops. This is presumably because
the cereal stubble and roots, which constitute about 50% of the
total biomass of the crop gus any straw ‘eft on the field, add
greatly to the oil organic matter upon which many species of earth-
worms depend.
6. The management of earthworm populations for maximum
agricultural benefit
The conr nsus of evidence is that earthworms improve soil
structure, fertility, organic matter decomposition, aeration and
drainage. Their importance increases with the current tendency
towards minimal or zero cultivation. If this is accepted, there is
a strnng case for a programme of earthworm management aimed at
encou ag.i.ng practices which favour the build-up of earthworm popu-
lations and avoidance, as far as possible, of practices which are
harmful to them.
The various agricultura] activities which influence earth-
worms are illustrated in Figure 4. Not all affect earthworm
populations equally. In order of importance, they are probably:
addition of organic matter, minimal cultivation, strawburr.ing,
continuous cereals, use of pesticides toxic to earthworms and use
of inorganic fertilizers. We have enough experimental data on most
of the parameters in this model to be able to define the optional
agricultural practices necessary to encourage maximum earthworm
populations.
ACKNOWLEDGEM NT5
I should like to thank J.R. Lofty, B.A. Jones, A.E. Whiting
and 3. Bater for their extensive assistance in these investigations.
10

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FIGURE 4.
MODEL FOR ThE MANAGEMENT OF EARTHWORM POPULATIONS
ADDITION OF
ORGANIC M&T ER
\
SOME NORGANIC
FERTILIZERS PARTICU ARL
LIME AND CALCWI NiTRATE
/
SOME NITROGENOUS
FERTILIZERS
PARTICU.ARLY
AMMONILPI SULPHATE
STRAbIBUFd4ING
OR
REMOVAL
1
LITTLE OR NO
CLLTIVATION
1’
/
_Li i 11I III CEREALS
LARGE EARTHWORM POPULATIONS FMIOUR
SOIL FERTILITY AND PLANT GROWTH
\
USE OF SOME
PESTICIDES
PARTICULARLY
BENZ L’1II ZOLE
FLPIGICIDES
HEAVY
CULTIVATIONS
FACTORS ThAT
fl 1CREASE
EARTHWORM
POPULATIONS
FACTORS ThAT
DECREAS Z
EARThWORM
POPLLATJJONS
4
/
1].

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REFERENCES
Darwin, C. 1881. The ro ation of Vegetable Mould through the
.jction of Earthworm3. Pub. John Murray, London 326 pp.
Davey, S.P. 1963. Effects of chemicals on earthworms: A
review of the literalure. Special Science Report.
U.S. F.ash and Wildlife Service 74, 1.
Edwards, C.A. 1975. Effects of direct drilling on the soil
fauna. Outlook onAQri.cI.I1t. .i _ ulture 8, 243—244.
Edwards, C.A. 1979. Tests to Assess the Effects of Pesticides
on Beneficial Soil Organisms. In: Tests for the
Ecological Effects c:F Chcm caJs. Pub. Erich. Schmidt
Verlag, Berlin 249—253.
Ec wards, C.A. and Jeffs, K.Z. 1974. The rate of uptakr of DDT
from soils by earthworms. Nature_(London) 247 (5437),
157—158.
Edwards, C.A. and Lofty, J.R. 1975a. The influence of
cultivations on soil animal populations. In: Progress
in Soil Zoology. Proc. 5th mt. Cangr. Soil Zoology
Prague. Pub. Junk, Amsterdam 399-407.
Edwards, C.A. and Lofty, J.R. 1975b. The Invertebrate Fauna of
the Park Graqs Plots. 1. Soil Fauna. Rothamsted Report
for 1974 , Part: It, 133—154.
Edwards, C.A. and Lofty, JR. 1977. Bioiogy of Earthworms. Pub.
Chapman and Hall, London 333 pp.
Edwards, C.A. and Lofty, J.R. 1979. The Influence of Arthropods
and Earthworms upon Root Growth of Direct Drilled Cereals.
3. Applied Ecol . 15, 789—795.
Edwards, C.A. and Thompson, A.R. 1973. Pesticides and the Soil
Fauna. Residue Reviews 45, 1—79.
I
12

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ACCUMULATiON OF ORGANOPHOSPHORUS INSECTICIDES
IN EARTHWORMS AND REACTIONS OF EARTHWORMS AND
MICROORGANISMS TO THESE SUBSTANCES
0. Atlavinyté, A. Lugauckas and “G. KiIikevi ius
•I.151it iite of Zocilopy and Parasitotogy
InsiiIute of Botany
R.s,arch Institide of Forealry
Lit hwinian SSR
INTRODUCTION
Aooording to Zdwards, Lofty (1973), many authors
have investigated the effect of peaticidea on earthworms
and the accumulation of pesticides in the organism of
earthworms. Many pesticides that get into the soil are
detrimental to earthworms. Ftlrst and Ronnenberg (1974)
mention several pesticides that are being used against
rodents and are pernicious to earthworms. Ruppe]. and
Laughlin (1977) analyzed what effect on the organism of
earthworms had the pesticides usually applied against no—
matodee. Thea. authors have observed that the pesticides
are less harmful to earthworms if thn A Rubstaflees get
into tne soil in the form of pellets Rnd not in the form
of dust. Th. also established that organophoaphorus pes-
ticides are less injurious than the carbomatic ones.
Organophosphorus insecticides are used rather wide-
ly, but their effect on the useful fauna such as earth-
worms as well as on the soil microorganisms is littis
known.
The aim of our investigations was to elucidate the
effect of organophosphorus ineeotiotdea on the aotivity
of earthworms, on their survival, the accumulation of or—
ganophosphorus insecticides in the organism of earth-
worms, the densities of soil mio oorganisms and the spe-
cific composition 0 microscopic fungi.
METHODS
Investigations were carried out in 1977—1978; they
were performed in a field (200 m 2 ) and in a wood (on 0.25
and 12 m 2 plots) both unfertilized and fertilized by
leaves and green lupine. LeaTos and lupine were put in
nylon net sacks; inseoticides were inserted there too
mixed with the soil. Some part of the investigations a
performed in pots which contained 3 kg of soil and had
30 or 50 g of straw or 12 g of leaves and 15 or 20 earth-
worms (control i ontained no earthworms).
Investigations were done with 3 repetitions. The
following insecticides were investigated: anthio, benso—
phosphate (phosalons), phosphamids, ohlorophoa, zeta-
tione. (The doses of insecticides are indicated In
le 1).
13

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The following media were used for the cultivation
microorganisms: meat peptone agar (MPA), starch am-
monia a ar (aLA) and beer mash agar (BMA). The number
of microorganisms per g a’n of absolutely dry soil. The
amount of insecticides in the organism of earthworms
wa calculated following the spontaneous removal of earth
f:rom their intestine.. Minced earthworms were treated by
acetone and analyzed by means of the chromatographio de-
vice eTevet_5R with thermionic detector; the procedure
was repeated twtoe.
RESULTS
1. The effect of org nophosphorua insecticides
on the activity of earthworms and their survival.
Anthio, bensophosphate and ohiorophos decreased
the survival of earthworms in the pots by 33 to ii6 per
cent a& compared with the survival of earthworms with-
out ins ot oides. Straw mineralization proceeded more
slowly when pots with earthworms contained also insecti—
cide5 (with the exception of ohlorophoe).In the variants
with insecticides earthworm aotiv .ty was also weuker and
earthworms had lass effect on the intensity of straw mi—
neralz zation. In the variant with phophamide (5 mg per
1 kg of soil) earthworms did not survive and straw mine—
raliz *tion proceeded there more slowly by 32.8 per cent.
Harmfulness of anthio depended on its amount In the soil.
Little doses of anthio (0.7 mg per 1 kg of soil) did not
decrease the survival of earthworms (Table 1).
During experiments performed in the wood uhemica].s
(viz. chlorophos 20 and 30 days from the insertion in
the soil and bensophosphate 30 and 60 days from its in-
sertion) had a delaying effect on the earthworm migra-
tion to the corresponding organic substance.
2 • The accumulation of organophosphorue ineeoti—
cides in the organism of earthworms.
At the beginning of the experiment metathione in
the soil was 2.0 p.p.m., but following 20 days from the
beginning of the ex9eriment we found in 1 kg of soil
0.2 mg of metathione reaid ae-and almost the same amount
in the earthworms (in Eieen g roeea 0.2 p.p.m. and in
qlobophora caliginosa 0.3 p.p.m. At the beginning of
the experiment beozophosphate in the soil was l5;lSOp.p.m.,
after 65 days the residue of benmophosphate in the earth-
worms Lumbrioum r’ibelljas was found 4.8; 2.7; 2.9 p.p.ni.
(tne oorrespon ing amount in the soil was 1.7; 8.2;
20.7 p.p.m.). Earthworms were investigated in the wood
where they oould freely immigrate and emigrate and
therefore tL.eir life period ira the experiment might be
different.
We have found almost the same amoun ;s of dimethoate,
14

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Table 1. EFFECT OF ORGANOPROSPHORUS INSECTICIDES ON THE
ACTIVITY AND SIJRVIVAL OF ALLOLOBOPHORA CALIGI—
NOSA (in the pots)

Unrotten straw (0)
Variants and the in variants rt 0 m
duration of experiments survlva.
control with (0)
earthworms
I Iay—Ju1y 1976 (65 days)
lithout chemicals 40.4 32.2 89.0
Phoaphamide (5 p.p.m.) 73.2 7 1.ii —
Benzophosphate
(150 p.p.m.) 60.0 56.2 55.0
June—August 1977
(75 days)
Without chemicals 27.6 16.0 95.0
Benzophosphate
(150 p.p.m.) 30.3 21.0 48.0
Chiorophos (80 p.p.m.) 15.6 13.0 60.0
April—September 1978
(130 days)
Without chemicals 15.0 11.3 86.5
An hio ci. , p.p.m.) 14.3 14.6 43.0
Anthio ç12.0 p.p.m.) 38.6 36.0 —
&nthio (1.5 p.p.m.)
(155 days) 9.7 5.1 40.0
Without chemicals
(155 dayS)X 75.0
AuthiO (0.7 p.p.m.)X 75.0
July—AugUst 1978 (60 days)
Without ohemio 1a 33.3 31.6 73.5
Anthio (200 p.p.m.) 34.0 32.3 42.0
August—September 1978
(30 days)
W 4 thout ohemioala 88.5
Anthio (200 p.p.m.) 45.0
x — fertilized wit i leaves
__ — unfertilized
15

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the metabolite of anthic, in the organism of AUolobop p—
.1.jg1nos as in the soil (0.4 p.p.m. and 1.7 p.p.m.
respectively; and 0.4 p.p.m.; 0.6 p.p.m. in earthworms
and the same amounts in the soil). When bigger amounts
of anthio were put in the soil (200 p.p.m.) we have
found 7.4 mg of this chemical per 1 kg of soil and
5.8 rng o earthworms following 30 days and 3.2 mg per
1 kg o ’ soil az d 1.0 mg per kilogram of earthworms £0].—
lowing 80 days from the beginning of the experiment .Theae
data give us sufficient ground to assume that depending
upon the time the amount of dimethoate, the metabolite of
anthio, both in the earthworms and in the soil is decreas-
ing. A slight amount of anthio was found in the soil(0.1;
0.3 p.p.m.), in the organism of earthworms there were de—
teoted only tracks. (Table 2).
Apart from this the aooia’nulation of Insecticides
in the organi3m of earthworms does show that on th one
band earthworui accelerate soil purification of these
harmful substances and on the other hand earthworms pro-
long the harmful effsct o pesticides when these inver-
tebrates are consumed by birds and other animals.
3. The effect of earthworms and the insecticide
anthio on densities of microorganisms.
It is well established that earthworms act posi-
tiveLy on the delelopment of microorganisms in the soil
(Atlavinyté, Lugaiskas, 1973; At1avinyt , 1975; Brtlsb—
wits 1959; Ghilarov, 1963; Kozlovskaja, 1969; Went,
19635. In analyzing the present results of these inves-
tigations one may clearly see that earthworms In this
case too did stimulate the development of microorganisms.
In almost all the variants of our investigations micro-
organisms have oonsiderab .y multiplied in the soil due to
the favourable role of earthworm activity. It has been
noted that the densities of aotinomyoetee and microsco-
pic fungi increased when the insecticide anthio was adde .1
to separate variants of our experiment. It may be seen
more obviousLy In the variants without earthworms. The
effect of anthio on microorganisms partly depends on its
amount and the duration of its action. Earthworms baire
decreased the effect of anthio on mioroo:ganisms( b!.e 3).
4. The change in specific composition of fungi
dueto the effect of earthworms and the insecticide an—
thio.
The results of our investigations have shown that
earthworms and the insectiolde anthio are powerful eco-
logical factors that influence the change in specific oom—
position of soil fungi. Owing to these factors the sue-.
cession of microscopic fungi In the soil takes place. Ge—
nerall.y the composition of microscopic fungi in the soil
iS rather constant and changes but litt e. Moat often tim
same species of fungi are found in all the samples of
soil of the same type. It is rarely that dominant ape—
16

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Table 2. RESIDUES OF ORGMWPHOSPHORUS INSECTICIDES AND THEIR ACCUMULATION IN THE ORGANISM
OF EARTHWORMS
=
Amount of
Surface insecticides Residues of ineectici.äes, The upeclea of
Duration
Insecticides of expa— in the sot]. .P.m . earthworms
inveeti— riments, at the beg .n—
gation, ning of tbe in the In tha
days experiments, 8011 earthworms
p.p.m.
Metathion 200 20 2.0 0.2 0.2 Lisenia rosea
0.3 Alloloboplipra
caliginosa
l . a
Ben ophosphate 12 65 15.0 1.7 4.8
rj e hue
12 65 150.0 20.7 2.7
• 0.25 65 150.0 8.2 2.9 p
• inthepot65 1700.0 n 5.6 “
•1 31
Anthio ” 65 140.0 .7 1.4 Ahlolobophora
cahiginosa
31 31
155 0.7 0.4 0.4
155 1.5 o.6 ” 0.6”
80 200.0 0.1 1.0”
3.2
30 200.0 0.3 t.
7.4 5.8
— Dimethoate, the metabohite of anthio, found In the earthworms and the soil.
n — not InveBtigated; t — track

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Table 3. EFFECT OF EARTHWORMS AND THE INSECTICIDJ ANTHIO
ON THE DENSITIES OF MICROORGANISMS IN THE SOIL
UNFERTILIZED AND FERTILIZED BY STRAW AND LEAVES
(1978)

- Unrot- Densities of microorganisms
ar± ts a a the tan (in thousands per 1 g Df soil)
ox erimet ts MPA SAA BMA
April—September
(130 days)
Control ].5.O 1 )4.8 427.0 67.4
20 earthworms 11.3 362.6 600.0 76.9
Control + 1.5 mg
of anthio per
1 kg of soil 14.3 172.4 780.0 298.8
20 earthworms +
1.5 mg of
anthio per 1kg
of soil 14.6 400.0 621.2 70.6
20 earthworms +
0.7mg of anthio
per 1 kg of
soil (150 days) 321.4 535.7 95.2
July—September
(60 days)
Control 33.3 800.0 12’e. O 119.6
15 earthworms 31.6 420.0 2043.0 150.5
Control + 200 mg
of antbio per
1 kg of soil 34.0 472.5 1208.8 87.9
15 earthworms +
200 mg of anthlo
per 1 kg of soil 32.3 1068.2 1931.8 125.0
15 earthworms +
200 mg of antbio
par 1 kg of
soil (80 days) 31.3 1101.1 1180.0 78.7
August—Septemb r
(30 aaya)
20 earthworms 483.6 714.3 142.9
20 earthworms +
200 mg of anthio
per 1 kg of
soil 160.0 750.0 181.8
* — fertilized with leaves
* w -• unfertilized
18

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des of fungi. would chnage in the soil. As we see from
Table 4, however, the specific composition of dominant
fungi did change very much owing to the affect of earth—
worms and the insecticide anthio. Due to the above—men-
tioned reason the formerly formed as ociation of soil
fungi disintegrate, their functional activity is impair-
ed and new favourable conditions appear for the intensive
development of other fungi species the activity of which
was earlier inhibited by the development of former domi-
nant species of fungi.
Table . EFFECT OF EARTEWORMS AND TEE INSECTICIDE ANTEIO
ON THE DISTRIBUTION OF DOMINANT MICROSCOPIC
FUNGI IN UNFERTILIZED SOIL AND THE SOIL PERTIL
LIZED WITH STRAW AND LEAVES (1978)

Variants and The num—
the duration bar of Dominant species
of experiieents species
Apr il—September
(130 days)
Control
20 earthworms
Control + 1. mg
of anthio per
1 kg of soil
20
18
29
Hormiaotis candida v.Höhnel.
num rosaum (Oud.) W.Gams
T iohoderma hamatum (Bon.) Bain.
Tvir idUPOr ax S F. Gray
Siopula iopsis fusca Zaoh
lenicillium subleteritium Biourge
P. oaneeoens Sopp
T iiTi kii Zal.
sterile
Mortier’311a candelabrum v.Tiegb
at LeM I n1er
M. humus Linuem 1
U alpine Peyronel
Trioho erina hamatum (Bcn.) Bain
T. viride Pars. ax S.F.Gray
Acremonlum (v.Bayma)W.Gama
Peniotilium purpuro enum StoU
P. nigricans (Bai.n. )-
luteurnZukal
T miczytiskil Zal.
sarium redolens Wr.
M. voelia steriii.a
Penioillium lanosum Westi.
P. capeulatuth Rapir at Fe nnell
P. goai.ewsicii Zaleeki
!io oderma tride Pers.ex
.F.Gray
othecium verrucaria Difmar
Cladoaporium herbaruin Link ax Fr.
Altarnarie ai t (Yr.) Ke s].
19

-------
Table 4 (Ctd.)
====================== ========—======
Variants and The nuin—
the duration bar of Dominant species
o:f experiments species
Oospora laotis (Free.) Saoc.
verti I1lium album (Preuss)
Pidopliczko
Mycelia stariLia
20 earthworms + 2]. Mortierella vinaoea Dixon—Stewqrt
1.5 mg of anthio Penicillium cyolopium Westi.
per 1 kg of soil P. odlowekit Zale8k
o euoron tanuissimum (Peck)
Hughes
Acremonium roseum (Oud.) W.Gams
Wui6r plumbeus Bon.
Nycelia eterilia
Brown ex
Smith
20 earthworms + 17 Aspergi.Llus niger v.Tiegham
0.7 mg of authio Mortierella humilis Liunem.
per 1 kg of soil Gotytriobum macroaladum (Saoc.)
(150 daye)* Hughes
Penicillium roseo—purpurogenum
Dierckx —
P. oapsulatum Rapo at Fonnell
ggdlewslcii Zaleski
eb3.1om ces javanicus Brown ax
Smith
Mycelia eterilia
Ju1y— eptember
(60 days)
Control 32 Triohoderma viride Pars. ex
S.F.Gray
T. iamatum (Bon.) Bain.
Wnioilh1um restriotum Gilman at
Abbott
P. godlewekit Zaleski.
ncephalaetrum racamosum Conh
ax chraet.
Mortierella llgnioola (Martin)
Game at Moreau
Cephalosporium
Humicola fuscoatra Traaen
Glioola ium a].bum ( Preusa ) Patch
Papularia phaerosperma (Pars.)
V .Hbbnel
Oldiodendron tenuisaimum (Pock)
Hughes
15 earthworms 22 Mucor cLrcinelloides v. 1egh.
Ab5idia inoea Lendn.
20

-------
Control + 200 mg 19
of anthto per
1 kg of soil
15 earthworms +
200 mg of anthio
per 1 kg of soil
Acremonium stxicturn W.Gama med.
Trichoderma virid.e Pers. ox
S.F. Gra
Panioillium godlewekil Zale ski
P. purpurogenuw Stoll
P simplicissimum (Oud.)
caneeoens Sopp
restri& üm Gilm&ri et Abbott
Actinomucor £ oaue (Hars)
Naumov
Miacor humilts Naumov
Mortierella alpina Peyronel
M. ii loola (Martin) Game et
oreau
Trioboderma bamatuin (Ben.) Bain
Penloillium reetric turn Gi man et
‘bbbtt
P. purpuresoens (Sopp) Raper.
ooumbens Worn
I adb 5porum berbaruin Link ox Pr.
30 Aspergillue tua Pros.
Btizopue oligosporus Saito
penioiiUum o41ewakii Zaleski
P. oyaneum ( Bain. etsart ) Biourge
i iambans Thom
oor p umbeua Bon.
M. 6ir Ine]ioides v.Tiegh.
emonium roseum (Oud.) W.Gams
Mycelia ete t1ia
16 Penioilhium godlewakil Zaleeki.
7 ffere Jensen —
Y eubleteritium Biurgo
T oorylopb.i].lum Dierokx
jorotrioum olivaceum Fr.
! rrichoderma fl! vrde Rifal
Myoelia steri]ia
16 Mortiorella o1 cepha1a Coern.
Sporotrioburn oiivaoeuin Fr .
enioi11ium r !! Ew Gilnian et
- w-
p. decumbens Thom
P. javanIo v. Beyn a
pfia1osporum ourtipes Saoo.
Acremontum roseum (Oud.) W.Gams
Table 4 (Ctd.)
Variants and The nurn-
the duration ber of Dominant species
of experiments species
15 earthworms +
200 mg of anthio
per 1 kg of soil
(80 days)
August—September
(30 days)
20 eartbwormsU
21

-------
Table 4 (Ctd.)
= ==a====== ===== ======== :.=
Variants and The num—
the d*aratjon ber of Dominant species
of experiments species
Mucor riseo—oohraoeus Naumov
er ha
20 earthworms + 19 Penicillium deoumbens Thom
200 mg of anthio P. piscariüm Westi.
per 1 kg of soil sub1ater Ltium Biurge
T simpllcisslmum (Dud.)
IiOmastiXcereaU s (Karst.)
Dickinson
Paeoilomyces javanicuin Brown ex
Smith
Mycehia sterilia
it was noted that earthworms and caproliths pro-
duced by them stimulate the development of the fungi M9—
corales . In the variants with Garthworms there was an in-
crease in the development of such genera of sot], fungi
as prt1ers1la, Mucor, Actinmucor, Absidla, Rhizopus .
In the soil fertilized by 8traw the fungi of the
genus Trichodernia ( . hamatum , .viride, .aureovirjde
and others) and also some ,epresentatlves of the genus
Peni.cillium ( . psulatum, 7.godlewskil, .p pj ,pgernz )
developed more Intensely.
Due to the affect of anthio sterile mycelluni of
fungi increased in the soil samples; when sown Into nu-
tritive media under normal laboratory conditions this
myoelium did not produce organs of reproduction, Mean-
while in separate oases the sterile myoel um copiously
produced and excreted into the environment its enzymes
and acids. Separate strains of the sterile niycelium when
acted upon by special means acquired capacity to produce
organs of reproduction. But the latter strains of fungi
and their organs of reproduction differed greatly from
the standard strains of the same species of fungi. Thus
it was established that the insecticide anthio may have
a negative effect on the development of separate species
of fungi and limit their distribution in the. soil. How-
ever, not all species of fungi react equally sensitively
to this chemical. Some species of the fungi belonging to
the genus Penicilhiuni under the effect of anthio Inten-
sify their activity and become very competitive (P. god—
lewskii, ,. canescena , ,.mIrczy’nskii).
SUMMARY
Organophosphorus inseoticid e, such as anthlo, ben—
zophosphate (phosalone) and chiorophos, have decreaded
22

-------
the urv1Va1 of earthworms up to 46 per cent. Anthio,
benzoph05P 1 t0 weakened the activity 0± earthworrcs and
slowed the mineralization of organic sub tauce . The
following residues of accumulated insecticides were
found jn the tissues of earthworms: 0.2 to 0.) p.p.m. of
metathione, 2.7 to 5.6 p.p.m. of benzophosphate and 0.4
to 5.8 p.p.m. of diinethoate, the metabolite of anthio,
per 1 kg of earthworms.
The effect of the insecticide anthio on the densi-
ties of various mioroorganisms in the soil is rather dif-
ferent and depends on the amount of insecticide and th
duration of its action. The insecticide anthio produces
the succession in the species of microscopic fungi in as—
eocj.ation alraa&y formed. A positive effect of this in-
secticide W& noted on some Lungal species of the enus
eaic1U1J&j! • g&l wffikii, 2. canescens , 2.mirozynakil.).
But due to the effect of anthi i, some other species of
fungi lose their ability to form organs of reproduction.
Therefore an increase in the amount of sterile mycelium
in the oi3- is noted.
Earthworms and their metabolitea had a positive
effect on the densities of microorganisms and stimulated
the development of the fungi Muoorale3 . Due to these in-
vertebrates the representatives of the enara Mortierel —
ia, Mucor, Absidia, Rhizopus have become more abundant.
The activity of fungi of the genus Triohoderma 15
intensified in the soil fertilized by straw.
LITERATURE CITED
Atlavinyté 0. and Lugauskas A, 1973. The Effect of Lum—
briOidae on the Soil Microorganisms. — In: “Soil
organisms and primary production”. — Ann.zool. —
6col.aflim., Nwn.h.sêr.71, 7, 73—80.
Atlavillytê 0., 1975. Ecology of Earthworms and thel! ef-
fect OD the fertility of Soils in the Lithuanian
SSR. Vilnius, 202 p.p.
Brilsewitz G., 1959. Untersuobungen tiber den ,influss des
RegeflWtIr O8 auf Zahi, Art und Leistungen von Mik—
roorganismefl 1w Boden. — Archly Z.Mikrobiologie,
33, 1, 58—82.
Edwards c.A. and Lofty J.F., 1972. Biology of Earthworms.
London, 283 pp.
FUrst L., Ronnenberg R., 1974. Einfluss von Bloziden auf
daB Bodenleben. “Garten org.”, 4, 109.
Ghi].arov M.S., 1963. On the interrelations between soil
well1ng Invertebrates and soil microorganisms.
23

-------
In: — Soil organisms, Amsterdam, North—Holland
Publ.Co., 255—259.
Koziovakaja L.S., 1969. Der Einfluaa der Exkremente von
Regenwttzmen auf die Aktivieruug der inikroblellen
Prozesse im Torfboden. — Pedobiologia, 9, 1—2,
l58—l61 .
Ruppal R.F., Laughlin Cb.,W., 1977. Toxicity of some soil
pesticides to earthworms. “J.Kana.Entomol.Soc”,
50, 1, 113—118.
Went J.C., 1963. Influence of earthworms on the number
of bacteria in the soil. — In: Soils organisms,
Amsterdam, North Holland Publ.Co., 260—265.

-------
GROWTH OF BASIDIOMYCETES IN THE PRESENCE OF
AGROCHEMICALS
C. J. F. Pugh and M. J. MacDonald
Uui eruIy of Asloii
UK INTRODUCTtON
The role of memi rs of the Basidioxny .etes in a ecomposition
proce sees has been st .died by relatively few researchers. The abil-
ity of many soil Basidiomycetes to break down lignin, noted by Fa].ck
(1923, 1930), is common in many wood-destroyers. On the other hand,
Meith (1925) remarked that the mycorrhiza forming Ba3idiomycetes are
incapable of utilizing cellulose or lignin but depend for their
nuti-ition on carbohydrates derived from their host trees. It was
subsequently shown by Norkrans (1950) tha even some of the mycorr—
hizal fungi are capable of decomposing at least cellulose.
L1ndeberg (1944, 1946, 1948) studied the ability of soil in-
habiting Basidiomycetes to decompose litter and its main constit-
uents, cellulose and li nin. In addition, Norkrans (1944, 1950),
Nikola (1954& and Fries (1955) i&icated that the ability to decom—
pose these constituents is very coiwn n among soil fungi. The most
active litter decomposers have been found among the genera of
Marasmius. , ycena, Olitocybe, Col]ybia, C].avaria and stropharia. , and
many wood destrc ying fungi fow d on decaying trees have decomposed
litter effectively in vtro: Ax,niUari. . mellea and species of
F) mmy a, Itypholoma., Phoiota and Polyporus (Lindeberg, 1946; Mikola,
1954a).
Thus the Basidiomycetes in soil represent a physiologically
heterogeneous group and in order to determine their role in the soil,
thorcug i investigations into the physiology of individual species are
needed. The course of litter decomposition, includ.ing its speed and
intermediate and final products, depends on three main factors
i) the physical and chemical properties of the litter, ii) the
environmental conditions and iii) the organisms themseives. The fac—
tore in turn are interdependent. The significance of each individual
factor in the decomposition of litter or wood is a matter for invest-
igation. In addition, with the rapid escalation in biocide usage in
agricultural and forestry ?ractice. it is urgent that we evaluate the
pressures which these cumpounds e rt on the fungi responsible for
decompr sition processes. Biocides are considei’ed to be indispensable
aids in agricultural, horticultural and forestry practices, and a
vast array of chemicals are applied directly to soil. Other agro—
chemicals enter the soil as run—off from treated aerial systems, or
from drifting sprays.
Dvring the course of studies on soil fungi, members of the
Basidiomycetes have often been overlooked because 0± difficulties
25 L

-------
of isolation and identification. thesters (1949) referred to “the
secret of the higher Basi.diomycetes”: Warcup (1959),with his hyphal
isolation technique, showed that Basidiomycetes can be recovered from
the soil, and Warcup and Talbot (1962) were able to identify several
species. However, these isolated studies give only a sisal ] indica-
tion of the work still to be done: other approaches, such as the
cultivation of myceita from sporophores, en .ble cultural studies to
be carried out.
In the present study, three non—tnycorrhizal species (235M,
ç prinus comatus and Cyathus stercoreus) , two known mycorrhizal spe-
cies ( Boletus t s and Pa d].lus involutus) , and Phallus
impuchcus , a species of uncertain status, have been used to investi-
gate the basic physiclogy and the reaction of each to the presence of
agrochemicals. In this way comparisons can be made of the abilities
of the nutritionally lifferent species under a range of environment-
al pressures.
MATERIALS AND METHODS
Species
The ft.ng]. used in this study include: two species isolated
from sporophore tissue, Coprinus comatus growing on a grass lawn,
and Phallus impudicus growing among mosses in deciduous woodland; an
unidentified Basidiontycete isolated from leaf litter of
tenuis , designated 235M; two known mycorrhizai species, Boletus
variegatus and Pa.,dflus involutus (supplied by Dr.P.Marnn, Institute
of Terrestrial Ecology, Edinbui ) and the non-4nycorrhizal fungus
C.yatbus st rcoreus (supplied by Dr. P. Blakeman, Aberdeen).
Media
All species were maintained on a modified Hagein malt agar
(HMA) (Modess 1941) and contained per litre of distilled water:
Glucose, log; NHAC]., O.5g; MgSO .7H 2 O, O.5g; malt extract agar
50g; Fe 013(1% s ].ution), 10 drops.
The basic liquid medium (BIll) contained per litre of distill-
ed water: Glucose, lOg; NH 1 01, O.5g; MgSO .7H 9 O, O.5g; KH 2 POA,
O.5g; malt extract 20g; Th! min, 1 mg; mi r3eIeinents (after ‘
Lilly and Barnett, 1953), 2m]..
Inocuk. for liqu d cultures were cut from the growing edge
of petri plate cultures on EMA. These inocula were transferred t
the flasks and floated on the surface of the culture medium, All
flasks were incubated as standing cultures.
Chemicals
Herbicides; Maxide 36 (as maleic laydrazide) — active ingred-
ient (a.i.) 36% (w/v) 1,2-dihydro—3,
6-pyridazyzaedione
26

-------
Paraquat — a.i. 25% (w/v) 1,1t .dimethyl_4,4?_
bipyridinium.
Fungicide: Verdasan — a.i. 2.5% (w/l) phenyl mercury acetate.
The field application rates of the agrochemicals are as follows:
Ilazide: .pprox. 4000 ppm
Paraquat: approx. 80U ppm
‘.‘erdasaxi.: approx. 20 to 80 ppm
Effect of temperature on growth rate
Petri plates containing about 20 cm 3 of IIMA were inoculated
with a 5 mm disc cut from he 9 rgtn of colonies grgwing on HMA.
Plates were incubated at 5 , 10 , 15°, 200, 25°, 30 and 350 0.
The colony diameters were t .Jcen as the mean of two diameters at right
angles to each other. Five replicate plates for each temperature for
every fungus were used. Extension growth rates were calculated dur-
ing the log phase of growth.
Dry weight increase
flasks containing 20 in]. BIll were inoculated with the tost fun—
gi and incubated at their optimum temperatures. Three replicate
flasks for each consecutive sample for each fungus were used. For
dry weight analysis flasks were removed, the inycelia harvested and
dried to constant weights.
Effect of agrochemicals on growth
Appropriate amounts of herbicide stocks were added to BIM to
give final concentrations of 500, 1000, 2000, 3000, 4000 and 8000 ppm
(a.i.) for Mazide, and 5, 10, 25, 50, 100 and 250 ppm (ai. for Para—
quat. Flasks were autoclaved for 15 mm and 15 psi. Appropriate
amounts of Verdasan stock solution were added to cooled sterile BIll
to give final concentrations of 0.1, 0.25, 0.5, 0.75, 1.0 and 2.5 ppm
(a.i.). Bill without agrochemical addition was used as control. Five
replicate flasks for each concentration of agrochemic il for every
fungus were used, and dry weight analysis performed as above.
RESULTS
Effect of temperature on growth rate
The results are summarised in Figure 1 arid i dicate the opti-
mum growth temperatures. All six species grew at 5 C, the lowest
tempel-ature used. Four of the species investigated showed growth
between 20° and 25°C (Basidiomycete 23514, Coprinus comatus , Boletus
and Phallus impudicus). Paxi].].us involutus showed a lower
optimum temperature, around 20°C, while Cyathus stercoreus had its
optimum near 30°C.
In general, the two mycorrhizal species ( P.involutus and
B.variega sJ and P.impudicus did not grow above 30”C, whereas the
other three non-.mycorrhizal species g ew above this temperature.
27

-------
10
5
10
8
6
4
2
l0
$
6
4
2
3
2
6
4
2
6
4
2
Ilus invoIu i
vari• hj
, çIu’i tm p,d, T
5° Id’ i? Q 0 5O 3QO 3?T.mp
FIG I .EFFECT OF TEAVfIA1URE ON MYCILIAL EXTBJSION
TE OF SIX SASIOIOMYCETES ON HMA.
C,
3
I
12 16 20 24 28
do s
•Soudc,’i c.t. M23501oI.fus vorI.g.Ius
OC a liu. ltrcoreus £Pa*iIli Involutu,
UCoprinvi c nvtvs APhsIIus u’pudlcin
PiG 2. GROWflI OF SIX SPECIES IN LIQUID MEDPJM AT THEIR
OPTIMJM TEMP AflJ1ES
(U
70
60
I
I
10
8
I I . I

-------
Dry weight increases
The three non-inycorrhizal species, 2394, C. comatu9 and
C,stercoreus , showed relatively higher growth rates than did
P.involutus , i!M s and P.impudicus (Table i).
TABLE 1 • C’rowth rate (mg dr ’ wei ht/24 hr) of
Basid.iomycetes at their optimum temperature
for growth.
Basidiomycetes 23514 33.50 Bolec.us variegatus 6.25
Cyathus stercoreus 9.38 ! 11us involutus 4.50
Coprinus comatus 7.67 Phallus impudicus 3.25
In addition, it is evident from P gure 2 that not only were
growth rates slower in the two mycorrhizal species arid P.impudicus
but the lag phase of growth was, in general, considerably longer.
Conversely, those specius with a shorter lag phase also showed a
faster growth rate.
Effect of agrocheniicals on growth
The effects of the agrochemicals on the groi.th of the six
Basidiomycetes are shown in Figures 3, 4 and 5. In general the
fungi were relatively tolerant to Mazide at the concentrations used:
only Phallus impudicus was inhibited at concentrations above 1000
ppm. Paraquat and Viidasan showed some similarities in their eff-
ects on growth at the concentrations used: 2391 and Coyrinus £ atus
were more tolerant than the other species. Boletus variegatus azir
Pa d].lus involutus were least tolerant, being inhibited at 5 ppm of
Paraquat and 0.1 ppm of Vexdasan. Cyathus stercoreus and. Ph ii1us
impudtcu s showed growth patterns similar to the mycorrhizal species
in the presence of Paraquat, but both wc-rc more tolerant than these
species to Verdasan.
DLS CUSS ION
In earlier studies on Basidiomycetes, most have been found to
be mesophi.lic in their temperature requirements. Three mycorrhiza]
species of Bo].etus studied by NoUn (1925) showed opt.iiwm growth at
25 C, while lWcola (1948) found a slightly lower optimum for species
of Anani ta and Lactarius . Norkrans (1950) found hat n corrhizal
Tricholcma species had optima within the range 18 to 30 C, while
)la ’x (1969) showed that Pisolithus tinctorius grew best at 30 to
35 C. L iiho (1970) reported the teiuperature 0 ma d.mum for eight
strains of Pañflus involutus to be about 30 C, with all strains
being killed at 32°C.
Of the various wocd-destroying I ymenomycetes studied by
Humphrey and Siggers (1933) and BjBrkman (1946) belonging to the
29

-------
60
id ycIts
1 1rir r
I I I I I
CON 5 10 25 50 100 250
Cciicnt,ation PPM
FIG 4. EFFECT OF PARAQUAT ON GROWTH
40
10
60
Cyallius sIercor.u,
60
Poxillui Involutiq
40
20
Boktu, vorisgalu.
Capil. ui w’ tui
fli ir’,
Cyathus stsrcoiaul
Paisillus hlvolukji
60
40
20
60
40
20
CON 0.1 0.25 0.5 0.75 1.0 2.5
Conc.nt.clon P M
FIGS EFFECT OF VE1 SAN ON GROWTH
Phallus irpudicus
UoI.Ius or.IpuIuI
If’ Phsltui iipdfcui
I — rfi — . I I
asldlomyc.ts 235
M
60
40
Ccprssis Cir’%It%4
Iir
kiIdIaiuiyc. e 23514
60
40
‘ . 5 )
0
5
E
a
I
a
ri.r
÷
ErYirir
60
Piiiillus ;nvolussjs 0
14-, 20
I iI 1L....z. .... L
-I .
±
60
40
20
60
40
20
rkithn
60
Bolspj s VOn 5 ltuI
20’
________-
60
PhaIIu ‘‘Dudcjs
20 —
CON 500 ‘000 2000 3000 100C 8000 FF1.
FIG 3 EFFECTOFMAZIOEON 3 OWTh

-------
genera Polyporus, Sterewn aug Por g , the great majority have
growth at temperatures of 28 C or higher. On the other hand, several
Mycena species grew best at 20°C (N. Fries, 1949). Treschow (194.4)
found the coprophile Psalliota bispcra to grow best at a temperature
range between 20° and 27”C with the optimum at 24°C. The coprophi]ic
species of Coprinus investigated by Rege (1927) showed a hi i opti-
mum of 30° to 35” 0 while L.Fries (1956) foufld various species to grow
‘nest at 300 to 35 C with good growth at 44 C in one species.
In the pre sent study, the six species used were also me so—
phi]ic, with Cyathu:; stercoreus showing the h ghest temperature
range. All six species e:thibited growth at 5 C, and. there were indi-
cations that Cop inus comatus could probably grow quite well at lower
temperaturSs. Me].in (1925) found that three species of Boletus grew
well at 10 C and two of them continued to grow at 6°C, while Lobanow
(1960 repgrted that the temperature minimum of mycorrhizal fungi
was 1 to 5 C. However, temperature requirements can depend on the
origin of the strains used: Moser (1958k) showed that the min mum
for a strain of P.involutus isolated 0 from a 0 va].].ey was 20 to C,
whereas a mountain strain grew at —2 C to 4 0.
Soil inhabiting Basidiomycetes have long been regarded as
slow growing organisms. However, Basidiomycete 235 ) 1 is exceptionai
in showing a rate of growth comparable with many non—Basidiomycetes.
Phallus iinpudicus and the two inycorrhizal species tested were not
only slower groving than the other non-mycorrhizal fungi, but they
also showed a much longer lag phase. Further studies are in hand
to see whether the growth rate can be used as a criterion for dis.-
tinguishing between inycorrhizal and non-mycorrhi zal fungi.
In the presence of the agrochemicals used, there were again
some differences in the tolerance shown by the mycorrhizal and non—
mycorrhizal species. With the exception of PhaU ijnpudicus the
i ycorrhizal species were less tolerant than the non-mycorrhizal
species to the three chemicals used. At field concentrations, all
species except Phallus impudicus were tolerant to Mazid.e. With
Paraquat and Verdasan, however, all of the test fungi were inhibLted
below the field application rate.
The behaviour of Phallus impudicus indicates many similarities
with the known inycorrhizal Boletus variegatus and. Pa aUus involutus .
However, Cx-ainger (1962) described it as growing saprophytically on
leaf mould and decayed wood, while Trappe (1962) reported it as a
possible mycorrhizal species.
Thus, the use of these agrochemicals could have more delet-
erious effects on myr orrhizal activity than on decomposition in
general. This could be particularly important in those marginal
situations where higher plant growth is dependent on inycorrhizal
associations.
31

-------
LITERATURE CITED
BjBrkman, E. (1946) On lagringsr8ta i inassavedgardar och dess
forebyggazide. (English Summary).. Medd. frar Stat. Skogsforskn.
Inst., Stoclcho]m.
Chesters, c.a.c. (1949). Concerning fungi inhabiting soil.
Trans. Br. Mv’col. Soc., 32(2): 197—216.
Fa].ck, R. (1923). Erireiterte Denkschrift Uber dis Bedeutung der
Fadenpilze für die Nutzbarmachung th’r Abfailstoffe zur
Baumer hrung liii wa]de und (Iber die Noglichkeit einen
nachtraglichen pi].zlichen Aufschlie ssung des Trockentorfs.
rkol. Unters. u. Ber., !: 38—72.
Faick, R. (1930). Nachweise der Huniusbildung und Humuszehrung durch
bestinun Arten h rerer Fadenpilse im Wa]iiboden. Forstarchiv.,
6: 365—377.
Fries, L. (1955). Studies in the physiology of Coprinus . I. Growth
nibstances, nitrogen and carbon requireinent . Sv.Bot.Tidskr.,
42: 475—535.
Fries, L. (1956). Studies in the physiology of Coprjnus. . II.
Influence of pH, metal factori and temperature. Sv.Bot.
Tidskr., 50:1.
Fries, N. (1949). Culture studies in the genus Mycena . Sv. Bot.
Tidskr., 43: 316-342.
Grainger, J. (1962). Vegetative and fructifying growth in Phallus
impud.icus . Trans. Br. Mycol. Soc., 4 (1): 147—155.
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32

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I
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33

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RELATION BETWEEN SPECIES LISTS AND TOLERANCE TO
NEMATICIDES
Diana W. Freckman, ‘ Law•ence B. Slobodkin and ***Charles E. Taylor
Un,r,rsikv of Califoniia—Riprr , ,de
SUNY Stont, Brook
• Un, er.Itk of Californro—Rnyrs,tfr
USA
INTRODUCTION
One body of ecological theory ass2rts that the physiological
properties of the individual organisms in a collection are related to
the n nnber of species in that collection. Slobodkin and Sanders (1969)
have suggested the possibility that where there are many species in a
community some degree of species packing (MacArthur and Levins, 1967)
has occurred, and that each individual from a collection containing many
species may be expected to be less tolerant of perturbation than each
individual in a collection with smaller numbers of species involved. In
this sense, a community comprising a large number of “tightly packed”
species should be l2ss stable than one consisting of a smaller number of
‘ loosely packe4” ones. Most investigators from their own experience can
think of systems which seem to confirm (or, perhaps, deny) the previous
sentence, but this involves selection of evidence and does not constitute
a test.
We wanted data which constituted objective samples of clearly
comparable communities, which were accessible to collection and perturbation,
but which had not previously been subjected to extensive analysis from the
standpoint of our hypothesis. We therefore chose to study neuiatodes.
Nematodes were chosen to test the hypothesis bec.iuse they are an
integral part of the seil fauna, and may be either harmful as parasites
of plant roots or beneficial in decomposition processes. It is also of
economic importance to know how nematode communities in thc soil will be
affected by a pesticide perturbation.
Our sampling procedure was one routinely used in soil nematology.
From each location we had a list of organisms present and relative
abundance data. For discussion of the significance of such lists see
Botkin et al. 1979, Maguire et al. 1980.
The perturbation was the application of an agx icu1tura1 nematicide
to a sample of living organisms in the laboratory. Since the hypothesis
relates to the properties of individuals, the perturbation need not be
performed in nature. It might be argued that extraction itself is a
perturbation which preselects for differential response to nematicides
but this seems far fetched.
3Lf

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METHODS
In this study seven localities were identified; four of these could
be considered species—rich in nematodes. These were all in the botanical
garden at the University of California, Riverside. We considered these to
be a sample of “tightly packed” neinatode communities. The other three
communities were normaily stressed by dryness and we Dxpected to find only
a few species of nemaLodes. These were located in a native coastal sage
scrub community on a nearby ecological area, also on the 11CR campus. Soil
samples were taken at the base of the plant (near) or at the plant canopy
(far). The localities were: Botanical Gardens — (a) . Juglans pyriformis near,
(b) J. pyriforinis far, (c) .7. hybrid near, (d) 3. hybrid far; Sage Scrub -
(e) bare ground, (f) Ambrosia duinosa near, (g) A. dumosa far.
Soil samples were taken in the spring of 1977, the nematodes
extracted, and the genera found in the first approximately one hundred
individuals examined from each site were recorded. One hundred hand
picked live nematodes from each site were placed into a solution of
nematiclde, 250 ppm 1,3 — dichloropropene. The time to 50% immobilization
was determined. (funnobilization is used as a criterion of the effectiveness
of a nematicide because the actual death point of a nematocie is difficult to
determine from visual observation). Solutions were examined for immobilized
neinatodes every 5—6 minutes and at the termination of the 5—minute interval
after immobilization had exceeded 50 , a differential count was made of the
first one hundred mobile animals encountered. This was repeated on scp rate
samples, March 21 and March 22, 1977, so that two measures were
made from each community. For statistical purposes they were treated as
independent samples.
. ESULTS
The 1 st and number of ne’natode genera found in each sample before
and after treatment axe shown in Tables 1 and 2. As expected, the mean
number of genera found in each sample from the Botanical Gardens were
greater than those in the coastal sage scrub (10.4 vs. 5.5). A median test
showed that more species were lost f rum the species—ric garden communities
than from the species—poor scrub areas (4.9 vs. 3.0) (X 7.87, df = 2,
P<..05). However, there were more genera there initially to lose; the
proportions of the genera lost in the two areas (.39 va. .27), while in the
same di ection , was not significantly different when tested 1 ith a median
test CX = 1.17, df 3, P>.7).
It should be recognized that the number of species present is but
one measure of community structure. Lewontin (1969) has stressed that
community stability should be measured in a variety of ways. A way to do
this is to compare the vectors of the specic’s composition before and after
treatment. Prior to treatment with nematicides each population can be
epresented by a vector = (P 1 , P 2 — 1, where the
components represent the proportion of each genus In making up the sample.
35

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TABLE 1. Namatode genera present in soil sample. before and after treatment with a nematicida.
DAY 1
Location A B C D B V C
Beforc At te’ Before After Before After Before After Before After Before After Before After
specir a 13 6 11 6 12 7 11 6 5 5 7 4 7 5
Acrohelea + + + + + + + + + + + + + +
Acrobeloides + + + + + + + + + + + + +
_____ + + + +
Diptheropbora +
D itylenchua + + 4 +
Doryla nue + + + + + + + + 4 4 + + + +
fle..otdogy +
Merliniua + + + + +
Nonhyetera
Paraphelenthue + + p + + + + + 4 + + + + +
Para ty lenchua + + + + +
Pratylenchus 4 + + 4 + +
Prts.atolathuj + 4
Pailenchu . +
Quinsulctua +
Ithabditis + + + + 4 + + +
‘ richodorus + +
Tykenchorhynchu . + 4 + +
Tylenchue + + + + +
! Lp n! m a p + +

-------
DAY 2
Location A B C D B P C
Before After Before After Before After Before After Before After Before After Before After
species 14 11 14 9 13 7 12 9 8 6 7 3 8 5
Acrobelee + $ + + + + + + + + + + + +
Acrobeloidea + + + + + + + + + + + + +
Aleimus + + + +
Aphelenchoides + +
Cervidellus + +
p erophora + + +
Ditylencinis + +
oor1a1! t + + + + + + + + + + + +
Herlinius + + + + + + + + +
Monhystera + + + + +
Pei aphe1enchus + + + + + + + + +
Pari ty1enchus + + + + + + + +
Plectue + + 4 + + + + + + + + +
Prerylenchug + + + + + +
Priematolaimus + + +
Pailenchue
Bhahditis + + I. + + + + +
Trichodorus $
encherhynchua + +
Tylenchus + + + + + +
+ + + . +

-------
Table 2
Number of neinatode genera present in soil samples before and after treatment with a nematicide,
Number of Genera
Location
Species—rich Average
coinmuniLie D y 1 ft Day 2 ft Day l/Day2
(Botanical B fore After Loss in Before After Loss in Ave Ave ft
Gardens) nematicide nematiclde Change genera nematicide nematicide Change genera change loss
A 6 —7 —.54 14 11 —3 —.21 —5 —.37
B 1]. 6 —5 —.45 14 9 —5 —.36 —5 —.40
C 12 7 —5 —.42 13 7 —6 —.46 —5.5 —.44
D 11 6 —5 —.45 12 9 —3 —.25 —4 -.35
Ave 11.75 6.25 —5.5 —.465 13.25 9 —4.25 —.32 —4.87 —.39
Species—poor
(Sage Scrub)
E 5 5 0 0 8 6 —2 —.25 —1 —.1.2
F 7 4 —3 —.43 7 5 —2 —.29 —2.5 —.36
C 7 5 —2 —.29 8 5 —3 —.38 —2.5 -.34
Ave 5.66 4.66 —1.66 —.24 7.66 5.33 —2.33 —. 1 —3.0 —.27

-------
After treatnicut, the communities would be changed to a new vector of
co.apositions (h). (We have used proportionate abundance because
absointe species ab’mdance could not be estimated).
Community stability can be measured in a number of ways. We
chose to measure Euclidean distance between the position vectors before
and after tteatment. A more stable community should be moved less. We
also detcrmined the angle between the vectors PA and P . A more stable
community should be moved through a smaller an e by ttce neniaticide.
The Euclidean distance in n—space, where n is the number of genera prior
to treatment, and the ang]e between community vectors before and after
treatment are compared (Table 3).
There was a greater effect on the more species—rich communities.
The nematicide moved the species—rich communities an average distance of
.90 genera, whereas .he species—poor communities were moved a distance of
only .57 genera. This difference was significant by a Mann-Whitney U—test
(U6, P<.0l). The angles through which the communities were moved also
differed significantly (U=7.5, P<.05) with the species—rich communities
being again more affected.
These data suggest that species—packing is an important determinant
of community stability. It suggests also that the mathematical theories
of community stability may be helpful for better understanding the effects
of pesticides on plant and animal communities.
Tab .p 3
Stability of species—rich and species—poor nematode communities. Stability
is measured by the resistance to change in species compositioi ver.tors by
treatment with a nematicide.
Euclidean dIstance between vectors Differences in angles between vectors
before and after nematicide - before and after nematicide
Location
Botanical Gardens Day 1. Day 2 Ave. Day 1 Day 2 Ave.
A 0.87 0.63 0.75 30 37 33.5
3 0.88 1.29 1.1 52 80 66
C 0.74 1.01 0.87 43 61 52
D 0.74 l.OL 0.90 43 63 53
Ave 0.80 0.99 0.90 35.25 60.25 51.12
Sage Scrub
E 0.46 0.66 0.56 26 39 32.5
0.52 0.35 0.44 30 20 25.0
0.96 0.45 0.70 57 26 41.5
Ave 0.65 0.49 0.57 37.7 28.3 33.0
L

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DISCU3SION
There has developed an extensive and polemical literature on the
relation between species packing and environmental stability. Thich
discussion has foiussed on whether or nor particular environments ought
to be thought of as more or less stable dnd on various definitions of
stability. In addition there has been concern as to statistical problems
in the determination of diversity. These p’oblems remain unresolved.
Obviously the stability of the environment must be viewed from the stand-
point of particular organisms. What cot.stitutes perturbation in one kind
of organism will not in any way disturb another. Aluo most measures of
species diversity are subject to various interpretations.
The Slobodkin—SandeTs (1969) formulation of the role of stability
in contributing to diversity asserts that there exists a relation between
the number of species and the physiological properties of the inaividual
organisms in collections of organiws made in nature. This connection is
not obvious. It might, for example, be asserted that if one kind of organism
in a particular place is particularly sensitive to some envirotuLental event
then others in the same place might share that sensitivity but this assertion
would say nntbing about the number of species to be c pected in that place.
Perhaps the most significant aspect of the Slobodkin—Sanders formulation is
that it atti znpts to explicitly rationalize a connection between physiological
properties of individual organisms and properties of assemblages of species
in which they are found. Testing detailed aspc.cts of the Slobodkin—Sanders
theory would require an e iornous amount of time and effort in studying
several ecosystems. In the absence of general agreement on clear
definitions of stability and ambiguity as to the relative merits of
different diversity measures such tests would still be equivocal. We
have not attempt’ed this — rather we asked the simpler question — whether
we can demonstrate any relation at all between the number of species in
a collection and the physiological properties of the individual organisms.
In the absence of such a relation any attempt at rationalization of
species diversity in terms of biological properties is suspect.
‘We used an unnatural perturbation, the nematicide, to avoid the
possibility that we are mimicking a natural event which the organisms
might not find perturbing. Ou choice of statistical procedure was
dictated b ’ our desire to use as much of the information in our data
as possible, and to minimize the role of special distributional functions.
If we had studied a we .l understood community we would legitimately
be subject to the criticism th”t we had chosen either the community or
the perturbation because of prior knowledge of how the organisms would
respond. Our choice of organisms was motivated by our desire to approach
as closely as possible a blind test of the simple hypothesis that there
was in fact a relation between length of species lists atd physiological
properties.
40

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The fact that we did show that the longer species—list sample3 were
more sensitive than the shorter does not by any means demonstrate
universal validity for the Slobodkin—Sanders argument. It does demonstrate
a specific prediction of the formulation; using our criteria or diversity
and for statistical difference, the hypothesis was confirmed. This of
itself is of significazu e in light of the assertion by Abele and Walters
(1979) that the hypothesis is a tautol.,gy, i.e. is untestable.
ACKNOWLEDGMENTS
This work was suppo ted in part by NSF grant in General Ecology.
We wish to thank Arnold Be: 1, Department of Nemato gy, University of
California, Riverside. I or his valuable assistance.
LITERATURE CITED
Abele, L.G. and K. Walters. 1979.. The stability—time hypothesis:
Reevaluation of the data. M. r. Natur., 114:559—568.
Botkln, D., S. Golubic, B. Maguire, B. Moore, 1 1.3. Horowitz, and
L.B. S]obodkin. 1979. Closed regenerative life support
systems for space travel: Their development poses fundamental
questions for ecological science. (COSPAR) Life Sciences and
Space Research, 17:3—12.
Lewontin, R.C. 1969. The meaning of stalility. Brookhaven Symposia
in Biology, 22:13—24.
MacArthur, R.H., and R. Levine. 1967. The limiting similarity,
convergence and divergence of coexisting species. Amer. Natur.,
101:377—385.
Naguire, B., L.B. Slobodkin, H.3. Horowitz, B. Moore, and D.3. Botkin.
1980. A new paradigm for the examination of (closed) ecosystems.
In John Giesy (ed.), Symposium on Microcosms in gjica1 Research .
Technical Information Center, U.S. Dept. of Energy (In press).
Slobodkin, L.B., and R.L. Sanders. 1969. On the contrib ition of
environmental predictability tu species diversity. Brookhaven
Symposia in Biology, 22:82—95.
41

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A PRELIMJN Ry STUDY OF THE USE OF SOME SOIL MITES
IN BIOASSAYS FOR PESTICIDE RESIDUE DETECTION
Ph. Lebrun
Unsvrrsihg of Lcuvain
B,Ig ,upn
INTRODUCTION
Our objective In this paper is to analyze the methodology of bio-
assays principally In relation to the detection of toxic residues of
pe ’ tic1des through soil fauna. In this sense, our conception is in
accord with that o Ruztcka (1973): “The determination of pesticide
resIdues by bloassays Is based on the measur ent of growth, death or
some other physiological (or ecological) change in animals, plants or
microorganisms.” The concept of bioassay derives from that of the blo-
indicl’Itor. A bioindicator Is in all biological parameters, qualitative
or quantitative (measured at individual, population or comunity level)
likely to indicate the particular life conditions corresponding either
to a given state, to a natural variation or to an envIrormtental pertur-
bation. Thus, In the sense of the naturalists, this definition
includes the more restrictive terms of indicator or characteristic
species. The actual revival of these old conccDts conies especially
from actual needs co’icerning ecological evaluation, quantification of
their biologicel value and ecosystem quality. In this context, and by
referring to soil ecosystem, the problem of bloassays becomes more and
more essential for soil biology and necessitates certain adjustinen s.
On the other hand, as of now a distinction should be made between bio-
assay and screent no. Screening is based principally on the comparison
of direct nortality induced by various molectles on whatever species,
either noxious or norm-target. On the contrary, by definition, bioassay
refers to standard organisms taken as a measure of reference . In addi-
tion, we do not foresee the direct repercussion of pesticides In the
field GF the consequence of their use on soil organisms. These aspects,
which constitute a global approach and not strict bloassays, have been
synthesized by several authors throughout the past few years (Edwards,
1973a, b; Thompson and Edwards, 1974; Matsumura, 1975; Brown, 1977).
OBJECTIVE OF BIOASSAY TECHNIQUE
The objectives of bloassays, in the restricted sense of the term,
can be classified Into four categories:
1. The study of the perststance in function of the behavior
of pesticides such as mobility and influence of external
factors on the blocactivity.
11 .2

-------
2. The comparison of molecular analogues In the perspective
of proposing a compatible choice with ecological Impera-
tives in the sense of minimizing destructive effects on
envirorunent.
3. Demonstration of secondary effects;
a. the Induction of resistance,
b. demecological (population level) such as
influence on the fecundity of non-target
species, or biocenotical modifications
such as biomagnlflcaticn, and
c. the Indication of teratologic effects.
4. The detection and measure c? biological residual activity
of pesti’ides;
a. either with Iabcratory experiments (absolute
bloactivity), or
b. from field samples (relative bioactivity).
We are essentially developing the latter objectives, but we can briefly
gi e a few samples concerning others in the context of soil biology.
RESEARCH REVIEW
Behavior of Pesticides
As Lichtenstein (1966) and Edwards (1973b) recalled, the bloactivity
of soil pesticides depends on a number 0 f factors, such as the chemical
characteristics of the molecule, the type of treatment, the type of soil,
the organic matter content, clay content, acidity, the temperature and
water Content of the soil, the type of vegetation or crop. Interesting
studies carried out by Read (1969, 1971, 1976) by Harris (1969, 1972,
1973) by Harris and Sans (1972) by Griffiths and ith (1973) on crickets,
flies and r.utworms have pointed out the Importance of these factors on
the real biological activity of insecticides. Among soil fauna. some
species of colleuboles, especially Folsomia candida . have been studied
within this view, mainly by Thompson anJ re (1972), Thompson (1 73)
and by Tomlin (1975, 1977a, b). Here are two examples of these studies.
The first (Table 1) shows that the bioactlvity, and thus the hazardous
effects of pesticides, can vary considerably depending upon the species.
In the second example (Table 2) it Is the type of soil and particularly
the organic matter content which p’oves to be a criterion equally deter-
minant. This Is already proof c i t e superiority of biological analysis
versus chemical analysis since for equivalent concentrations of pesti-
cides the effects expressed in total bioactlvity vary in very large pro-
portions. In both cases, the chemical analysis would have lead to a
simple equivalence of activity.
43
L

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Table 1. Comparative Bloactivity of Some Insecticides
on 2 Co11e ibo1an species (after Tomlin, 1975)
Insecticide
Bioaetlvity (% mortality)
Onychiurus jiistl Folsomla
porter candida
Counter. t ‘at:
0.05 ppm 9% 100%
01 ppm 73% 100%
0.5 ppm 96% 100%
Carbofuran at:
0.5 ppm 0% 15%
0.1 ppm 0% 100%
0.5 ppm 0% 100%
1.0 ppm 35% 100%
Table 2.
Influence of Soil Type on the B1oact vity
of Technical Chiordane (Target: Crickets)
(after HarrIs, 1972)
SOIl Type
% Organic Matter CL 50 (ppm)
Sand
0.5 0.46
Clay
27.8 6.56
Muck
64.6 18.82
Comparison of Pesticides
The comparison of the effects of analogues pesticides is one of the
most positive aspects of bloassays because soil ecologists can recoimiiend
or Impose the least prejudicial molecules in the edaphic environment
(Table 3). The three pesticides mentioned are, in principle, equivalent
as to their capacity of crop protection. This comparison reconinends not
44

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Table 3. Bloactivity of some Carbainate Insecticides
on Lumbricus herculeus (from Lebrun and
Klein, In pre.)
A ld1carb’
Carbofuran
CL 5
(5 hours of
0
inmiersion)
Toxicf y
Rotlo
1 : 1
3.6 : 1
2.9
10.6
ppm
ppm
Thiphanox
26.8
ppm
9.2 : 1
only to make a choice as to the less harmful compound, but also It
encourages studies directed at select’ng pesticides less and less toxic
for the faunal deconiposers. In this aspect, the study by Tomlin (1377b)
is very interesting (see Table 4). It Is obvious, Indeed, that the first
benonyl Is more compatible with ecological demand than the other, and
with benonyl itself.
Table 4. Toxicity (mortality %) of Soil Application
of Benomyl and two Analogues to three
species of Springta lls
Concentration In SoIl
5
Benouiyl
ppm 10
Analogue 1
N-methyl carba-
moyl -benzimidazoIe
Analogue 2
N-methyl carba-
moyl -imf dazol e
ppm 5 ppm 10 ppm
5 ppm 10 ppm
Onychiurus justi
porterl
ILypogastrura annata
Folsomla candlda
40
40
100
100
100
100
0 0
0 0
0 0
0 100
0 100
0 100
Demonstratl3n of Seco’rtdary Effects
Soil ecologists are quite concerned about the secondary effects of
pesticides due to the very slight mobility and the very long persistance
of pesticides in the daphic environment If compared, for example, with
aquatic envlromient (Thompson and Edwards, 1974). Contrary to the studies

-------
on noxious Insects (Read, 1965; Rajak et al., 1973), few works have been
dedicated to resistance and modification of fecundity induced in soil
mlcroarthropods. As an example of demecological effect, one can men-
tion the work of Gregoire-Wibo (1978), conducted with Folsomla candida ,
which showed that the selective pressure Induced by cat furan affects
the fecundity already after three generations of the species. As far
as the blocenotical aspects are concerned, numerous studies have been
realized directly in the field to study prey/predator relationships
(for example Sheals, 1956) or modifications of the conmiunity structure.
These works extend beyond the frame of this presentation and cannot, by
their nature, be considered as real bioassays. On the other hand, from
an ecological point of view, the work conducted by Popp (1970) on the
oribatid Hermannia convexa is a model study. Popp combined laboratory
and field experiences in order to consider all the problems of con-
tamination and the transfer of pesticides. In this manner Popp (1970)
showed that mite dejectlons treated with reduced doses of dieldrir 1 were
extremely toxic (their bloactivity was tested on Daphna ) and could be
the beginning of an important contamination of decoaiposer trophic
chains of the soil.
A PROPOSED RESEARCH DIRECTION
Detection aid P easure of the Residual Bioactlvity
Let us now approach the bioassay concept in the more restricted
sense. The general scheme presented In Figure 1 Illustrates the differ-
ent methodological steps and compares the two possThle approaches of
bioassays (the physiological and ecological approach) with usual chemi-
cal approach. In all three cases, the problem remains the same, that is
the detection and the quantification of residues and their possiole
activity on the tested fauna. Chemical analysis will certainly provide
the most complete answer depending ppon the techniques used such as
spectrophotometry S—UV, S-IR, S—F) and chromatography (TIC, GLC, LLC).
One will obtain the exact spectrum of the parent compound, of its
metabolites and of the hydrolized products. This information, however,
as complete as it may be, does not clarify anything as far as the bio-
logical influence of the various toxicants. In fact, the knowledge of
effects due to all combinations of concentrations between parent compound,
nietabolites, and hydrolized products would be necessary to provide the
real value of the bioactivlty. Besides, the variability of measures, as
well as the difficulty in establishing techniques, make it so that the
chemical analyses are restricted to very punctual problems.
Concerning biological assays, the information obta ed is reversed
as it Is the bloactivity on which the attention is focused and not the
chemi’al composition of the residues. However, the physiological
approach and the ecological approach do not provide the same information.
Only the ecological approach proiides the actual toxicity of samples of
the soil which are tested. As it appears in the figure, thIs technique
gives a very rapid diagnosis that 1 often very precise as to the quality
of the environment. After having established the tolerance of a sensitive
species to one or anotner toxicant, we then put experimental populations

-------
PIIYSIOL%ICAL A CN
(sopWisTIcaTID)
smus wiTh ouuiwON . PisTiclil AWi
WillOWS CONCINIIATION$.
ItU WITH wumumis PUTICIDI AlsO swus mm isumoos PISIICIW w
PIllOWS COICIwTIATIsOII. PIllOWs COIICUITIATICU.
& 1
1iNAl. DT*WTICN. AL IXTWACTION.
I I
TI,L S-IN I MICIOCO CONT IINATION
SLC ST UTRACT
U.C SF (Wit. SIT CONTACT S P000 ...).
Sic I
[ L J±i L J
PAITITION Ii - PAJ4PIT CiSsOOWiD. I JIfMMI
— NIT,AOUTES. NESPONSS OF flIPISIPIITAt POPui..A’iON. DIWECT SISPONPI CF IXPUIMIIIIAL
NTRNSLTRI PIOSSJCTS, POPILATION.
____ ‘p
/ci,t .
cowm SON WITH $T*I SI Clvi
(PONVIONSLY UTASLIlvU
ON0OsOs& .
UTUODUTISI TO SUPPOIU me-
ACTIVITY.
Hr H 1
— / .i (J _____________
CIsO*IIOW WITH STMSAPI CUPYS
(PaIVuOusI.y i$TMLIIIIIO).
IXTUPVLATICI ii ILSIM.
CONWSTRATI OI.
CsOsO* lION WITH STONOAPI INVI
(PPIYIDUS .v (ITONLIISCS).
‘p
LXTIAPC.ATICN TO IOUIYA4 .LNT
CCNC SISTHA TICN’.
Fig. 1: COMPARISON OF METHOLOGICAL STEPS AND APPROACHES TO BIOASSAYS.
LCOL%PCAL OPPRO ,
(Il u ic?)
47

-------
in contact with tested pedological samples. Following the mortality in
the experimental population, we deduce the concentration by extrapola-
tion in a given produce In terms of total toxicants. This type of bio-
logical trial, initiated by Sun l957, 1963) and Gupta (1973), has
already been put into practice with edaphic Collemoba (Thompson, 1973;
Thirumurthi nd Lebrun, 1977; Thirmurthl, 1979). The advantages of this
method in comparison to others are presented In Table 5, which points out
the number of repetitions possible and the relative price of the
analysis.
An example of bioassay using the physiological approach was realized
with the colleubole, Folsomia candida , as given in Figure 2. The biolog-
ical activity was followed In two plots, one at a dose of 2 kg Al/ha and
the other at a dose of 10 kg Al/ha. With the standard curve (previously
established), the temporal evol ution of the residues could be observed.
The residues were determined by dilution of the soil samples only for blo-
activities reachtn2 100% murtality. This example shows one of the great
interests n the use of rnicroaithropods as an Instrument to measure and
diagnose the quality of soils, as well a the evolution of residual
toxicity. As also proved by a parallel study on field populations, they
c n restore themselves approximately 24 weeks after the treatment at a
dose of 2 kg Al/ha.
DISCUSSION AND CONCLUSIONS
According to Matsuniura (1976), dOne of the most important considera-
tlcns In the analysis 0 f residues Is assessment of their potential damage.
It Is urifDrtunate that biological and biochemical assessment have not
been rea’y extensively applied to the field of residue analysis”. In
fact, the development of bloassays runs up against several difficulties
of which the main ones are, according to Ruzlcka (1973), the choice of
species of reference, and a lack of specificity of living material in con-
parison to chemically different pesticides. These two difficulties are
extrcanel.y related because discrimination between the residues of two
rnole ules can n1y be done by using two different species, one being
sensitive to the first pesticide and resistant to the other, and in-
versely for the other species. “In essence, bioassay animals are
selected on the basis Of high pesticide sensitivities and by the ease with
which large numbers of them can e reared” (Matsumura, 1976). Froo this
point of view, it is essential to point out that because of its great
diversity the scil microfauna present a large reservoir of species pre-
senting the properties of very good biolndlcators ( sensu JenkIns, 1972).
Due to the diversity in feeding habits, behavior, optima and ecological
tolerance of soil mlcroarthropods, they represent variable and sensi-
tive living forms which can be largely used In bioassays. Now, as we
have already pointed out for soil animals, only certain species of
collenboles are actually used In L’loassays. The necessity to measure
the effects of residues In a more precise manner either In the soil
(T mlin, 1977a) or In vegetal tissue (Pree and Saunders, 1973) could be
encountered by diversifying the living material.

-------
TABLE 5 : COMPARATIVE ADVANTAGES OF CHEMICAL AND BIOLOGICAL WAYS
CHEMICAL WAY
PHYSIOLOGICAL APPROACH
BIOLOGICAL WAY
ECOLOGICAL APPROACH
-ABSOLUTE
AND CONC
CHEMICAL
ENTRATION.
COMPOSITION
—ABSOLUTE (POTENTIAL)
BJOACTIVITY.
-RELATIVE (ACTUAL)
B IOACTIVITY,
KIND OF INFORMATION
-SUPPOSED
BIOACTIVITY.
-GLOBAL CONCENTRATION.
-EQUIVALENT CONCENTRATiON.
COST
j 1 fr
‘•
TIME SPEPTS
LONG
INTERMEDIATE
SHORT
NUMBER OF POSSIBLE
REPLICATES
LITTLE
INTERMEDIATE
LARGE

-------
CARBOFURAN
PERIOD IN WEEKS
FIg. 2: ECO-TOXICOLOGICAI. EVOLUTION OF CARBOFURAN RESIOtES TESTED
foleomia candida (After THIRUMURTI4I and LEBRUN 11B77)
- A- -j --
FI9.3TOXICITY OF ONE INSECTICIDE
AND ONE MITICIDE ON PERGAHASUS NORVEGICUS
(L4 )-( PRF JMINARY UNPUBLISHED RESULTS)
(MORTALITY AFTER 48h1
50
0.7 1.0 1.2
logo (ppm)
2.7 3.0
log (] (ppm I
O 2KG Al/HA
110KG Al/HA
RESIDUES
BIOLOGICAL ACTIVITY
E 22!
0.
0.
2
2
4
4
U
‘I’
w
C
4n
4
0
4
U
I .
0
-a
SO
I
I .
0
25 U4
S
0
0
0.
6
0
L
‘I
I

-------
Some preliminary tests have been performed in this sense on
Oribatidel of the genus Dainaeus ( onustus and clavipes ) (mycophagous
species) and on gamasids of the species Pergamasus norvegicus (preda-
tory species). The Initial resulted obti ined (FIgure 3) show that
with carbofuran the range of sensitivity Is already very good, with-
out attaining the ranse of 0.1 to 1 ppm, such as is generally recom-
mended (Sun, 1957). On the other hand, the resistance of Pergamasus
norvegicus to an ac tr1c1de, which is very active on tetranychids and
oribatids, seams to invalidate the usually formulated criticism of
non-specificity of biological material.
In conclusion we can only strsss the development of bioassay
methodology by using soil fauna. Table 6 suninar1z s the character-
istics and qualities which should be sought after in the future for
the species test, as well as for the diversification and the adjust-
TABLE 6. Use of microarthropods in bloassays -
trends for the future
QUALITIES OF TIlE TESTED - SPECIES
- High sensitivity
— Specificity to one (or a few number) pesticide
— Use of wild popUlation (from untreated fields
as forests)
- Reaction homogeneity (use of one sta 1s)
— Easy mass rearing and manipulation
QUALITIES OF THE MEASUREMENTS
— Simultaneous use of contrasting species (trophic
levels, taxonomic status)
— Ecological approach (actual bioactlvlty)
— Need of continuous watch
ment of an instrument for precise and reliable measures. In this view
one must point out that the qualities of chosen species shall be en-
countered in the highest specialized species of which one different
stasis will be selected. As far as the quality of assays, one must
still stress the determination of the actual bloactivity which can only
be estimated through an ecological approach. Finally, one must stress
that what could b2 t .e most Important Is the need to continually con-
trol the biological quality and thus the maintenance of soil fertility.
51

-------
LITERATURE CITED
Brown, A.W.A. 1977. Ecology of pesticides J. Wiley, New York.
525 pp.
Edwards, C.A. 1973a. Envirormiental pollution by pesticides. Plenum
Press, London. 542 pp.
Edwards, C.A. 1973b. Pesticide residues In soil and water. Pages
409—458 in C.A. Edwards (ed.). Environmental pollution by
pesticides. Plenum Press. London.
Gregoire-Wibo, C. 1978. Effete du curater sur la fecondite et Ia
survie de Folsomla candida (Insecte-Collminbcle). Med. Fec.
Landbouww. Rijksuniv., Gent. 43(2):569-580.
Griffiths, D.C. and C. Smith. 1973. The insecticidal activity of
diethyl and dimetPiyl analogues of azlnphos, bromnophos, carbo—
phenothion and parathion on glass surfaces and in soil. Pestic.
Sd. 4:335—342.
Gupta, D.S. 1973. LieGe of bioassay In the residue analysis of
insecticides. Pages 215-228 j S.P.R.A. (India).
Harris, CR. 1969. Laboratory studies on the persistence of biologi-
cal activity of some Insecticides In soils. J. Econ. Entomol.
62:1437—1441.
Harris, C.R. 1912. Factors influencing the biological activity of
technical chlordane and some related components in soil. J.
Econ. Entomol. 65:341-347.
Harris, C.R. 1973. Behaviour and persistence of biological activity
of HCS-3260 (AG—chiordarie) In soil under laboratory conditions.
Proc. Entom. Soc. Ont. 103:10—16.
Harris, C.R. and W.W. Sans. 1972. Behaviour of heptachior epoxide
in soil. J. Econ. Entomol. 65:336—341.
Jenkins, D.W. 1972. Development of a continuing program to provide
Indicators and indices of wildlife and the natural envirormients.
Smithsonian Institution, Ecology Program. Washington, D.C. 20560.
165 pp.
Karg, W. 197$ , Milben as Indikatoren zur Optinlerung von Pflarizen—
schutzmassnalinen in Apfel itensivanlogan. Pedobiologia 18:415—425.
Lichtenstein, E.P. 1966. Persistence and degradation of pesticides
in the enviroirent. Scientific Aspects of Pest Control. National
Academy of Sciences, Washington, D.C. 221-230.
Marshall, T.C., H.W. Dorough and HE. Swim. 1976. Screening of pesti-
cides for inutagenic potential using Salmonella typhimurlum Mutants.
Agri. Food Chen. 24:560—563.
52

-------
Matsignura, F. 1976. ToxIcology of Ins ctlcides. Plenum Press. New
York. 503 pp
Poppe, E. 1970. Effects of dteldrln tHEOD) on a moss mite Hennannia
convexa CL. Koch (Acari: Oribatel). Z.f.Angw. Ent. 65:117—130.
Pree, D.J. and hL. Saunders. 1973. Bloactivity and translocation
of carbofuran residues in mugho pine. En. Ent. 2:262—267.
Rajak, R.L,, N. Ghate and K. Krishnamurthy. 1973. BIoassay technique
for resistance to malathion of stored product Insects. Inter-
national Pest Control (Nov.—Dec.) pr. 11-16.
Read D.C. 1965. Methods of testing Hylmnya root maggots for insecti-
cides resistance. J. Econ. Entomol. 58:719-727.
Read, D.C. 1969. Pers1stenc of some newer Insecticides in mineral
soils measured by bioassay. J. Econ. Entomol. 62:1339—1342.
Read, D.C. 1971. Bioassays on the activation and deactivation of some
new insecticides In a mineral soil and absorption of toxic components
by rutabagas. J. Econ. Entomol. 64:796-800.
Read, D.C. 1976. Comparisons of residual toxicities of twenty-four
registered or candidate pesticides applied to field microplots of
soil by different methods. J. Econ. Entomol. 69:429—437.
Ruzicka, J.H. 1973. Methods and problems In analysing for pesticides
residues in the environment. Pages 11—56 InC.A. Edwards (ad.).
Environmental poI 1 ution by pesticides. Plenum Press, London.
£heals, J.G. 1956. Soil populations studies. I. The effects of culti-
vation and treatment with Insecticides. Bull. Ent. Res. 47:803-822.
Sun, Y.P. 1957. Bioassay of pesticide residues. Adv. Pest. Control.
Res. 1:449—496.
Sun, V • P. 1963. BIoassay insects. Pages 399-423 in Anal yti cal Methods
for Pesticides and Food Additives. Academic Press, London.
Thirumurthi, S. 1979. Environmental toxicology of carbofuran In a
grassland ecosystem. Linpubi. Ph.D. Dissertation. University of
Louvaln. 113 pp.
Thirumurthi, S. and Ph. Labrun. 1977. Persistence and bloactivity of
carbofuran in a grassland. 4ed. Fac. Landbouww. Rijksuntv. Gent
42(2):1455—1452.
Thompson, A.R. 1973. Persistence of biological activity of seven
Insecticides In soil assayed with Folsomla candida . J. Econ.
Entomol. 66:855—857.
EL

-------
Thompson, AR. and CA. Edwards. 1974. Effects of pesticides on
nontargert invertebrates In freshwater and soil. Pages 341 .346
In Pesticides in Soil and Water, Soil Science Society of
iiier1ca. Madison, Wisconsin.
Thompson, A.R. and F.L. Gore. 1972. Toxicity of twenty-nine imectl-
cides to Folsomi a candida : Laboratory Studies. J. Econ. Entomol.
65:1255-l!6
Tonlin, A.D. 1975. ToxIcity of soil applications of insecticides to
three species of springtalls ( Collembola ) under laboratory con-
ditions. Can. Ent. 107:769-774.
Tomlin, A.D. 1977a. Culture of soil animals for studying the
ecological effects of pesticides. Pages 541-555 in Crop Pro-
tection Agents. N.R. McFarlane (ed.). Academic Wess, London.
Tomlin, A.D. l977b. Toxicity of soil applications of the fungicide
benoinyl and two analogues, to three species of Collenbola. Can.
Ent. 109:1619-1620.
QUESTIONS and COMMENTS
H. EIJSACKERS : Don’t you fear a change in genetical
composition after mass rearing for a long time, so the species
ui der study may not be representative anymore for the “wild”
species selected at the start of the project?
Ph. LEBRUN : I agree with you but the laboratory strains
could be characterized and isolated. On the other hand, for
our strains, we regularly regenerate (in the genet cal sense)
the strains by adding some wild individuals directly coining
from the field.
C.A.EDWARDS: Do you have any evidence for resistance
developing when the same culture is exposed to a pesticide
at intervals?
Ph. LEBRUN : Yes it is the case as Dr. Gregoire has
shown on the Fol’omia candida population treated with carbo-
furan at LC 5 After three generations th fecundity i
increasing nong intervals.
A.J. REINECKE : it is a well Xnown fact that males and
fei- 1 ales of many species react differently in bio-assays. In
some soil microarthcopods sexual dimorphism develops at a
fairly late stage which should be taken into account. Did
you find the same persistent differences between the two
sexes in their reaction to pesticides?

-------
. LEBRUN : In the case of Folsomi candida the problem
is very simple as that species is a parthenogenetic one.
The sexual discrimination is practically impossible on
Oribatid mites. In the gamarid group, where the 5exual
differentiating is always possible, I observed no differences
in reactions to pesticides.
However, in most cases, the sex is determined after
the death of animals.
.55
II

-------
EFFECTS OF SIX BIOCIDES ON NON-TARGET SOIL MESO-
ARTHROPODS FROM PASTURE ON STE. ROSALIE CLAY
LOAM, ST. CLET, QUEBEC
Thomas D. Smith, D. K,ith McE. Kevan and Stuart B. Hill
Macdonald Cam pu McGill U ir rciIy
Canada
INTRODUCTION
Soil inhabiting ir.s ct pests have always been more
difficult to control than their above ground cc.unterparts.
Some relief was achieved, however, with the introduction
and use, often overuse, of DDT in the mid nineteen-forties
and of cyclodiene biocides in the e.rly nineteen-fifties
(Harris ct al. 1.967). From that time onwards, synthetic
organic biocides have impinged on both living and non-living
parts of the environment (Figure 1) (Kevan, 1955; 1962;
Rudd, 1964; Edwards, 1969; 1973; 1974; Gillett, 1970;
Guyer, 1970; Mills and Alley, 1973; Butcher, 1976; Wallwork,
1976; McTaggart—cowan, 1977; and Hill, 1979).
OBJECTIVES
Concern for possible detrimental effe-ts of b!o - ide
use led to the establishment of a field tLial to measure
and suggest significance of changes in population densities
of non—target soil mesoarthropod species, primarily Acari,
in moderately intensively managed, cattle—grazed pasture on
Ste. Rosalie c1 y—loam B 0 j1 The study site was on the
farm of Mr. J. Martineau, :-t . Clet, Soula ige Co., Quebec.
MATERIALS 3 ND I . ETHODS
The bioci s 1 ‘ sq d for the present study were single,
separately app1:- . perationa1 dosages of diazinon,
fenitrothion, ma, methoxychior, carbaryl and
mexacarbate (Table 1). Experimental design was a linear
random arringement of pairs of like treatments having 00
magnetic azimuth and being perpendicular to prevailing
winds.
1 Names of biocides are fra ’ Spencer (1973).

-------
Applicatien of b1oc de tc soil.
—--..-.p. Direct move,ient of biocide into sphere from
application source.
b . physical t nmport and degration of biocide.
, 1ogicat degradation of biocide.
Retirn oF modified biocide.
1 Modified from Robinson (1973).
Ti are 1: Stheim ofbiocide transport with!n the biosphere .
57

-------
TABLE 1: Sources and application rates of biocides.
Biocide Application rate 1 (kg/ba) Source
ORGAROI’HOSPHATE
diazinon 0.89 Commercial
fanitrothion 0.28 CIBA—GEIGY
malathion 0.20 Commercial
CHLORINATED
HYDROCARBON
inethoxychlor 1.60 Commercial
CARBANATE
carbary’ l 1.10 Commercial
mexacarbate 0.14 CIBA—GEIGY
1 Based on manufacturer’s label
for best
all purpose control;
Fenitrothion and mexacarbate based
for control of spruce budworm, New
on single
Brunswick,
application rate
1969.
Insecticides were applied on 23 June, 1971, and samples
collected on 21, 24 and 29 June, 6 and 20 July, and
17 August, 1971. Soil mesoarthropods were extracted in
a modified Kempson, Lloyd and Gelardi (1963) infra-red
extractor (Hill, 1969 and Behan, 1972).
ANALYSIS OF DATA
Since we were more interested in finding, than in not
finding significant differences among popu1 tion densities
and dry—bioniass values of soil inesoarthropod species from
treated and control plots, we used a two—way analysis of
variance and Duncan’s Multiple R nge Test (Duncan, 1955;
Steel and Torrie, 1960; Chew, 1976a, b; 1977) (Tables 2 and
3).
Population densities and dry—biomass values were com-
pared with those of pre-spray and/or control treatments
(Figure 2).
58
.&. -_;,-__ —

-------
TABLE 2. AnalysiS of data.
Group Populaticn r:y
Density Blc ass
Total soil mesoa!thTOPOdS 1
ZoophagOus soil vleHoarthropOda 1
Phytophagous soil mesoarthropods 3.
Zoopha us Acari 1 1
Phytophagous Acari 1 1
Aca ri 2 1 1
“c ther” soil inesoarthropods 2 1
Two—way analy3iS of variance and Duncan’ a Multiple Range test.
2
Rarer
taza azcludled.
Data
not detern ined.
CONCLUSIONS
1) Number of species, population densities and dry—biomass
values of non—target soil mesoarthropods, were affected
by the biocides used in this study, often in several ways.
2) Use of suprageneric groupings of soil mesoarthropods
would have masked changes caused by biocides at the
species or life—stage level.
3) Greatest reductions in population density and Acari
dry—bioiuass normally occurred within two days after
biocide app]Lcation. Delayed reductions in population
density and dry-biomass of phytophagous Acari occurred
from one to two weeks after application of methoxychior;
and of population density of zoophages from one to four
weeks after application of mexacarbate. A persi stent
reduction of zoophagous Acari dry—bioniass occurred from
12 hours to two weeks after spraying mexacarbate.
59
a

-------
TABLE 3a. tffects of iocidea on soil mesoarthropod density and dry
bicinasa according to Duncan’s Multiple Range Test*.
POPULATION DENSITY DRY BIOM&SS
1) No significant difference among treatments:
GROUP 3 GROUP ’
Phytophagous soil mesoarthropods 2 Acari
Zoophegous Lean
Hexapoda 2
Entoinobryidae Mesostigmata
Sininthunidae 2 Hypoaspis angusta
Staphylinidae 2 2 Rypoaspis similisetae
Diptera larva 1 Neo)ordensia levis
Acari Prostigmata
Zoophagous Lean ! leorchestes formicor nn
upodes voxencollinus
Me sostigmata
) lacrocheles merdarius Onibatei
Brachychthonius j ugatus
Prostigmata
Speleorches tee formicor m
T.mpanipes hystricinus
Eupodes voxencollinus
Coccorphagidia n.sp.
Hauptmannia op.
Oribatei
Ti ture Onibatei 1.
Imentuxe Oribatei 2
2) All biocide treatments significantly greater than control treatment :
Collembola Mesostignata
Orychiunidae Rhodacarellus silesiacus
Mesostiginata Onil ,atei
Rhodacarell.us sil. siacus Tectorepheus velatus
Oribatei Oppia zn nus
Tectocepheus velatus
Oppia minus
A1l biocide treatments significantly less than control treatment :
Xe908tigmatd Proatigmata
Tnichouropoda obscura Bakerdania blumentnitti
Prostigm*ta
Bakendania blume”tnitti
* Ste. Rosalie clay loam pasture, St. Clet, Quebec; Data for all sample dates
from 21 June to 17 August, 1971.
60

-------
Rexapoda
2
Eo lentoi idae
Aphidee
Acari
Phytophagous Acari
Proetignata
Tarsonemue randsi
Oribatei
Brachychthouius jugatus
Scheloribatee pallidulus
Hexapoda
Thripidae
dia., car.
car.
car., dia.
car., fan., max.,
dia.
sal., mel., sex.,
f en.
dia., sex., car.,
sal., fan.
trol treatment .
Mesos tigmata
Trichoaropoda obscura
Macrocheles inerdarius
Ololaelqe aelinicki
Dendro.Laelape etrenzkei
dia., car. sex.,
w.sl., fen.
sex., car., dia.,
f en.
met., sex.
met., sal., die.
dia., fen., sex.
TABLE 3b.
(4) Some biocida treatments signif
POPULATION DENSITY
DRY BIOM&SS
GROUP
Significant
Biocide
Treatment
GROUP
Significant
Biocide
Treatment_
s nt1v erea tar than
4r .PIIloflf !
Acari
Phytophagous Acari
Prostigmata
Tareonesue randsi
2 rhaidia n • ep .
(5) h{ (d treatments sLgnIfI
Total Boil mesoarthropods
sal.,
car.,
Rflt lv
car.
sex.
lees than eoii
dia.,
met.,
max., sal.,
f en.
Mesoetigmata
I ypoaepis angusta
dia.,
niex.
dia.,
met.
fen.,
met.,
fen., car.,
met.
sex.
max., sal.,
car.
Proetigmata
Nanorcheetes collinus
Scutacarus lapponicus

-------
TABLE 3b (Continued)
Uypoapis similisetae
Ololaelaps selinicke
Ameroscius corbiculus
Cheirosetus borealis
Asc i i bicornis complex
Neojordensia levis
Dendrolaelaps strenzkei
! us crassipes
lapponicus
car., met.,
mex., fen.
f en.
fen., mel.,
.aal. , mex.,
mel., met.,
car.
fen., sex.
met., fen.,
nez.
)fen., die.
met., Dial.
7mex car.
.ma l.
7dia., car.
4inex., fen.
7dia., car.
(mex.
,‘dia.
mex.
.
POPULATION DENSITY
- -..
DRY IOMASS
Significant
Biocide
Tr atment 3
c ou

Signifkant
Biocide
i:reatme&
fen.,
sal.
let.
met.,
let.,
nez.
car..
net.
f en.,
nez.,
car.,
car.,
die.,
dia.
inst.
met., mel.
Prostigmata
sphagiieti
O ibatei
Oppie].].a nova
(6) Some biocide treatments sLgnif
Coccotydaelous krantzi
complex
I!!’.!P! aphagneti
Oribatel
Oppialla nova
r _ less (C) than control treatment :
Nesostiguiata
Ameroseius coribuculus
Cheiroselus borealis
Aeca bicornis complex
dia., nez., met.
dia., met., sal.
cantly areater (;) c
Hexap ode
llypogastruridae
Proetigmata
Nanorchestes collinuo

-------
POPULATION DENSITY
- DRY MOM S5 -
CR0
- - —
Significant
fliocide
- —
o ou
— — -. -
Significant
Biocide
atasut
3 Abbreviation for insecticide
dia = diazinon
f en fenitrothica
mel — malathion
met methoxychior
car carbaryl
mex mexacarhate
fee., mex.
car., dia.
?met., mal., fen.
Cmex., die, fen.
car, met.
TABLE 3b. (Continued)
met.
die.
Scutacarus lapponicus
Astigmata
ryrophagus dimidiatus
Rhizoglyphus rotundatus
Oribatei
Trichoga].uiana n. sp.
Groups in phylogenetic order.
Dry biomass values not determined.
treatment
!!!z ue craeaipea
!R!! SUB lapponicus
ProsLigmate
Hauptmannia ep.
Astigmata
Rhizoglyphus rotundatus
1
2
‘fee., die., max.
mex., fee., die.
car., met.
I .

-------
PI RE 3. 7 equsnciss of n b.r of occurroncss wh.n population
donahty of vail .onoarthropod. and dry biosaus of
soil Acarl var. lover than in control., folloviog biocide
tTaa sat. Sts. Rosalie clay Loan pasture, St. Clot,
P,Q, (23 Jon. to 17 August, 1971).
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66

-------
LITERATURE CITED
Behan, V. 1972. The effects of urea on acarina and other
nrthropods in Quebec black spruce ( Picea inariana Mill.)
humus. M.Sc’. Thesis, McGill University. 175 pp.
Butcher, J.W. 1976. Pesticides and Soil Arthropods. Pages
254-275 in KUhnelt, W. (Ed.) Soil Biology — with speciaJ
reference to the animal kingdom. Faber and Faber,
Londo ,, U.K.
Chew, V. 197 . Uses and abuses of Duncan’s Multiple Range
Test. Proc. Fla. 3tate Hortic. Soc. 89: 251—253.
Chew, V. 1976b. Comparing treatment means: a compendium.
Hortscience. 11: 348—357.
Chew, V. 1977. Comparisons among treatment means in an
analysis of variance. Data Systems Application
Division, Agric. Res. Sexy. U.S. Dep. Agric., Beltsvi].le,
Maryland, U.S.A. pubi. No. 1977—0—228—258. 64 pp.
Duncan, D.B. 1955. Multiple Range and Multiple F—tests.
Biometrics, 2: 1—42.
Edwards, C.A. 1969. Soil pollutants and soil animals. Sci.
Jim. 220: 88—98.
Edwards, C.A. (Ed.) 1973. Environmental Pollution by
Peeticides. Plenum Pr., London, U.K. 542 pp.
Edwards, CA. 1974. The effects of pesticides on soil
organisms. Natl. Res. Counc., Canada, Ottawa, 5
December, 1974. Castette taped seminar.
Gillett, J.W. (Ed.) 1970. The Biological Impact of Pesticides
on the Environment. Environmental Health Science
Series. No. 1. Proc. Symp. Oreg. State Univ. Corvallis,
OregDn, U.S.A. 1969. 210 pp.
Guyer, D.E. (Ed.) 1970. Pesticides in the Soil: ecology,
degradation, and movement • mt. Symp., Mich. State
Univ. 1970. East Lansing, Michigan, U.S.A. 144 pp.
Harris, C.R., avec, H.J. and Mukerji, M.K. 1967. A new
look at old prok 1eins; the need for a modern evaluation
of old soil insect problems. Proc. North Cent. Branch
Soc. Am. 22: 47—52.
67

-------
Hill, S.B. 1969. Ecolocyy of bat guano in Tamana Cave,
Trinidad, W.I. Unpublished Ph.D. Thesis. Univ. West
Indies, Trinidad. : :o pp.
Hill, S.D. 1978.. Agricultural chemicals in soil. Pages
18—53 in Beveridge, D.M. (Ed.) Chemicals in Agriculture:
Problems and Alternatives. Proceedings of a Seminar.
Fort. Qu’Appelle, Sask. 1977. Can. Plains Proc. 5.
Kempson, D., Lloyd, M..and Ghelardi, R. 1963. A new extractor
for woodland litter. Pedobiologia 3: 1-21.
Kevan, D.F.McE. 1955. Soil Zoology. Butterworths, London,
U.K. 512 pp.
Kevan, D.K.McE. 1962. Soil Animals. Witherby Ltd., London,
U.K. 237 pp.
McTaggart-Cowan, P.D. 1977. Fenitrothion. The Long term
effects of its use in forest ecosystems. Current
Status. Associate Committee on Scientific Criteria for
Environmental Quality, Nat. Res. Counc. Canada,
Ottawa, Ont. Pubi. NRCC/CNRC No. 15389. 19 pp.
Mills, J.T. and Alley, B.P. 1973. Interactions between
biotic components in soils and their management practices
in Canada: A Review. can. 3. Plant Sci. 53: 425-441.
Robinson, 3. 1973. Dynamics of pesticide residues in the
environment. Pages 459-513 in Edwards, C.A. (Ed.)
Environmental Pollution by Pesticides. Plenum Pr.,
London, U.K.
Rudd, R.L. 1964. Pesticides and the Living Landscape. Univ.
Wis. Pr., Madison, Wisconsin, U.S.A. 320 pp.
Spencer, E.Y. 1963. Guide to the chemicals used in crop
protection (6th edn.) Supply and Services, Printing
and Publishing, Ottawa, Ont., Agric. Can. Publ. 1093.
542 pp.
Steel, R.G.D. and ‘ orrie, J.H. 1960. Principles and
Procedures of Statistics. McGraw-Hill. New York, N.Y.,
U.S.A. 431 pp.
Wallwork, J.A. 1976. The Distribution and Diversity of
Soil Fauna. Academic Pr., London, U.K. 355 pp.
68
*IL _ - —-

-------
QUESTIONS and COMMENTS
. BENGTSSON : Rave you tried to analyze the mechanism
of interaction between the different species used and the
pesticides considering the dicferent biological characteristics
of the species and the chemical characteristics of the pesticides?
HILL : I have only examined this on pap r in relation
to various reviews of the literature that bear on this sub-
ject. fly preliminary ideaa have k.aen published in the Pro-
ceedings of the Fourth North inerican Forest 50318 Conference
(Hill, S.B., L.J. Metz and M.H. Farrier, 1975. Soil meso-
fauna and Silvicultural Practices. Pages 3]9 to 135 in B.
Benio and C.H. Win9et (eds.) Forest Soils and Forest Land
Management. L aval Univ. Press, Quebec) in relation to the
mechanisms by which fertilizers might affect soil utesofauna
in coniferous forest soils. Some of these are likely to be
similar to the mec anisms involved in pesticide effects.
FAIZ : Please give the reason for the delay
action of some ir ecticides on density of soil fauna and
whether it is due to physiological reasons related to the
fauna itself or due to a chemical and/or physical process
going on in the soil.
HILL : I suspect that most delayed effects operate
via the food chain and via (initiaily)sublethal effects that
influence behavior and reproduction. Which of these is most
important will vary from one species and one habitat to another.
I(.H. DOMSCH : Do you know any confirmed field observa-
tions on reduced organic matter degradation following pesti-
cide application at reconuttended rates?
S.D. HILL : No. I am, however, familiar with several
farmers that I respect, who claim that such relationships exist
at an economically significant level. There are, of course,
various litter i ag studies that have supported such conclusions.
Dr. Satchell mentioned Dr. B.N.K. Davis’ work on effects of
pesticides on rate of organic matter decomposition. There was
no significant difference and displaced millipedes were re-
placed by others. I believe that we should examine such short-
term observations with caution as substitute species may have
qualitatively dLfferent functions (e.g. that have a bearing
on rate of release of certain trace minerals) whose effects
may not become clear for 5. 10 or more years.
C.A. EDWJ RDS : I noted that you list Rhodacarellus sileacus ,
as a species that increases in nun ber due to biocides. As
this is a well—known predator, how do you explain these in-
creases in numbers? Are they due to hyperpredation?
69

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.. HILL : I do not know the answer. Certainly hyper-
pcedation is one pos8ibility. Reduced competition and in-
vasion from adjacent areas or movement upwards from the pro-
file below the emptied depth would be other possibilities.
I 8uspect that . sileacus would be reduced in arable soils
in which pesticides would move rapidly and penetrate the
deeper soil layers. Our study site was a pasture on clay—
laom soil so that vert distribution of pesticides would
be more limited.
70

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EFFECTS ON LINDANE, CARBARVL, AND CHLORPYRIFOS ON
NON-TARGET SOIL ARTHROPOD COMMUNITIES
James B. Hoy
Uniuers.ty of Cahforn,a—Bnbfrv
USA
INTRODUCTION
In an effor to ieduce losses of high—value pine trees in camp-
grounds, parks and dooryards, lindane is used as a protectant spray in
localized but heavy applications. The toxicity of lindane (and certain
other insecticides) to bark beetles has been established (Lyon, 1971;
Smith, Trostle and McCambridge, 1977). However, lindane’s operational
efficacy has been challenged Dahlaten, 1976). and suspected environ-
mental side effects have resulted in a rebuttable presumption against
reregistration by the U. S. Environmental Protection Agency. Should
reregistration be denied or failures prove widespread, possible alterna-
tives to lindar . include carbaryl end chiorpyrifos (Lyon, 1971; Smith
et al. 1977).
Concern that spiash and drift of bark beetle sprays disrupt the
soil arthropod community directly under sprayed trees resulted in a
cooperative research agreement between the U.S • Forest Service and the
University of California. The ultimate concern is that a change in the
arthropod community will affect litter decomposition and nutrient re-
cycling. Although the i”aportance of microarthropods in litter decom-
position is ‘tot well understood Harding and Stuttard (1974) concluded
that it is greatest in pioneer and mor soil;. The microarthropods
disintegrate litter, which increases the surface area for fungal attack,
and they mix the organic and mineral components of the soil (Edwards,
Reichie and Crossley, 1977).
The scudy of lindane began in 1978 in a mature pL ,e plant.atic’n
( Pinus ponderosa Lawson). and a comparison of the effects of lindan!,
carbaryl and chlorpyrtfoa as initiated in 1979 in a stand of niature
ponderosa pine forest.
METHODS
The initial study of liudane was started in 1978 at the U. S.
Forest Service Institute of Forest Genetics, Placerville, California at
800 m elevation. Plots 3 m in diameter were sprayed with lindane at
either of two rates, 1.13 g/ui 2 or 11.3 g/m 2 . The latter rate was 10
times the base rate which one might expect under a tree to which lindane
carefully and legally was applied. The higher ate was to neure an
effect and to simulate an over—zealous pp1ication. Spray plot application
71
— - .. - —... - - -. . —

-------
rates were established on the assumption that 10 percen.. of the volume
applied to a tree fell as splash or drift, and that 80 percent of that
fell within 1.5 m of the center of the Lree. Residue analyses of soil
under treated trees confirmed the model.
One d y priur to spray plot treatment and at 3, 9, 21, 45, 93,
141. and 381 days post—treatment soil cores were taken f om the 11
replicates of each treatment. During 1978 2 cores 32 cm x 7.6 cm deep
were taken from each plot, however the last samples (at 381 days) were
20 cm 2 x 5.1 cm deep, 3 per plot. xtraction of the arthropods over a
4 day period followed Price’s method (1973). All data analysis was of
c.rnnposite data from each plot.
In 1979 the following treatments were randomly assigned to 49
plots in the Challenge Experimental Forest, Challenge, California:
chiorpyrifos at 5.22 gIn 2 , 6 plots; chiorpyrifos at 26.1 gun 2 , 6 plots;
lindane at 1.57 g/m 2 , 6 plots; lindane at v.83 gIn 2 , 6 plots; carbaryl
at 5.22 g/m 2 , 6 plots; carbaryl at 26.1 g/ m 2 , 6 plots and 13 controls.
These application rates were based on refined estimates of residues under
trees treated in routine operatt. ns.
I
Statistical analyses were analysis of variance following Little and
Hills (1978), the Games and Howell t—mcdification (Keselman and Rogan,
1978) and Kendall’s tau following Chent (1 63).
I would like to acknowledge the taxonoinic services of Drs. Roy A.
Norton and Douglas W. Price and No. Barbara Wi]son tor identifications
of the Cryptostigmata, Prostig’aata and Mesostigmata, and Collembola,
respectively. Drs. Michael I. Haverty and C. .1. DeMars gave me helpful
suggestions during the preparation of this paper. Funding for the re-
search was provided by the U. S. Forest Service, Cooperative Research
Agreement FS—PSW #50 and #68.
RESULTS
For the sake of clarity, only pretreatment and 45, 141 and 381
post—treatment data will be presented, and that as a percentage reduc-
tion below concurrent controls. Furthermore, only those taxa that were
well represented will be diBcussed.
The general effects of lindane applied in the pine plantation can
be seen in Table 1. The Collembola were reduced to a highly significant
degree under the high application rate arter 141 days and at both the
high and low rate 381 days after application. Contrariwise , the
Prostiginata were reduced to a highly significant degree after 45 days
at both rates, showed strong signs of recovery after 141 days, and were
very abundant 381 days post- treatment where the high rate was used • The
Mesostigmata showed moderate (but not significant) reductions prior to
381 days, at which time there was an increase over control numbers in the
low rate plots and a highly significant reduction in the high rate plots.
The Cryptostiginata were reduced during all three periods, either
sign Lficantly or highly significantly in all but one case. The category
72

-------
TABLE 1. Percent reduction (increase) of arthropød groups following
application of Lindane at two spray treatment rates, 11 plots/treatment
45 days 141 days 381 days
1.13 11.3 1.13 11.3 1.13 11.3
glm 2 g/m 2 aim 2 g/ n a 2 g/na 2 gi n a 2
Collembola 53 47 20 82 ’ 87 96
Prostigmata 40 62 12 23 23 (204)
Mesostigmata 38 53 25 57 (56) 85
Cryptosti-gm ta 52 67 34 79
Othert 16 25 58 89 44 70
Double underlining indicates statistical significance at the 1% level
(single underlining, the SZ level) following transformation of counts to
Log (N+1).
which included all other arthropods showed the greatest effeci..s after
141 days, but with a stri&ing effect at the high rate even at 381. days.
The Collembola, most abundantly represented by the Entomobryidae
and the Onychiuridae, showed a wide range of responses to lindane. The
dramatic and lasting reduction of the Entomobryidae and the erratic re-
ductions of the Onychiuridae, as well as the effects on other families
as illustrated by Table 2.
The effects of linda’ie on the Prostigmate are given in Table 3 by
families. The first five families show the most dramatic effects. All
but the Tydeidae were severely reduced. The very abundant Tydeidae were
eventually overabundant by 241 percent.
The Cryptostigmata offer the greatest opportunity to see the
effects of lindane on the community as a whole. With 10 species (see
Table 4) abundant enough for analysis of variance, a wi.de variety of
responses were found. Aph .lacarus acarinus (B’ rlese) and Eobrachv—
chthonius ep. were severely affected. A progressive reduction was
vi.denced by Sphaerochthoniue sp. and Eramaeus ep. However, Schelori—
bates ep. seemed to rabound from a slight initial reduction to over-
abundance. Overall, after 381 days, all but Sche].oribatee sp. were
greatly reduced at the high rate and most were greedy reduced at the low
rate.
Three quantitative measures of community structure ere applied to
the cryptoatigmatid data; 1) mean number of species per plot, 2) the
complemented Simpson’s index, 3) Kendall’s tau. The latter statistic is
a rank correlation method advocated by Ghent (1963). but seldom used.
It has the advantage that paired data are used, thereby preserving
information content lost by the more widel, used Simpson’s index or the
information theory indices.
73

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ThBLE 2. Percent reduction (increase) of Colleinbola following
application of lindane at two spray treatnent rates, 11 plots/treatment
45 days 141 days 381 days
1.13 11.3 1.13 11.3 1.13 11.3
g/m 2 g/m 2 g/m 2 g/m 2 gun 2 gun 2
Zntomobryidae 74!’ 99 86 100 91 99
Isotomidae 70 41 50 96 35 88
Onychiuridae 15 39 (57) 43 83 97
Poduridae 28 16 33 74 77 63
Double underlining indica..es statistical uignificance at the 1% level
(single underlining, the 5% level) following tr nsformation of counts to
log (N+l).
TABLE 3. Percent reduction (increase) of Proetigmata following
application of lindane at two spray treatment rates, 11 plots/treatment
45 days — 141 days 381 days
1.13 1.1.3 1.13 11.3 1.13 11.3
g/m 2 g/m 2 g un 2 g/m 2 g/m 2 gIm 2
Nanor hestidae 82 130 87 100 86 97
= == = =
Eupodidae 92 86 89 96 96 100
= = = =
Tydeidae 30 54 (2) 2 24 (241)
Bde l lidaa 81 97 66 96
=
Cunazidae 85 j QQ .
Cryptgnathidae 45 4 (3) 41 81 21
Raphignathidae 37 46 76 38
Caligonellidae 16 62 34 70 36 53
Stigmaeidae 38 (22) (25) (260) 30 25
Double underlining inc Lcatea statistical significance at the 12 level
(single underlining, the 5% level) following transformation of counts to
Log (N+1).

-------
TABLE 4. Percent reduction (increase) of Cryptostigmata following
application of lindane at two spray treatment rates, 11 plots/treatment
- 45 days 141 days — 381 days
11.3 1.132 11.3 1.13 11.3
g/ 2 g/m 2 g/m g/m 2 g/m 2 g/m 2
Aphelacarus a,’
acarinus 79— 99 97 99 97 99
= = =
Sphaeroch-
thonius sp. 6 12 25 71 73 85
Eobracny—
thonius sp. 96 97 95 100
Epidaniseus sp. (117) 60 38 93 65 98
Eramaeus sp. 64 84 75 99 89 100
= — = = =
E. stiktos 58 91 51 94
- =
Autogneta sp. 56 38 54 87 52 98
ei1a nova (200) 66 9 53 9 78
Schelori—
bates ep. 36 49 (108) 45 (172) (160)
Zachvatkini—
bates sp. 92 98 81 100
Double underlining indicates statistical significance at the 1% level
(single underlining, the 5% level) following transformation of Counts to
log (N+l).
Pretreatment samples provide data on species richness and hetero-
geneity as well as do concurrent controls (Table 5). A slight decline
occurred in mean number of species per plot in the low rate plots, and a
sharp decline in the high rate plots. Species diversity as measured by
Simpson’s index was very uniform prior to spray treatment, and was
slightly depressed in the control plots at 141 days (late summer). At
the low rate Simpsoa’s iudec changed very little until the 381 day
sampling. However, at the hi& rate there was a steady decline throughout
the post—treatment sampling.
Rank correlation of the abundances of the cryptostignatid species
between controls and the two spray treatments are given in the last two
columes of Table 5. Note the difference in the two statistics prior to
spraying. Th.are was a relatively slight decline in the correlation in
the comparison with low rate plots and a dramatic decline in the high
rate plots.
75

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4
t
r
TABLE 5. Cryptoatigmatid species richness, heterogeneity and species rank correlation arranged
according to four sampling periods and three treatments
Richness fleterogeneity
Rank Correlation
(Mean species per plot) (Complemented SimpRon’s)
(Kendall’s tau)
Cuntrol Control
vs. 2 VS• 2
1.13 g/m 11.3 g/tn
1.13 11.3. 1.132 11.32
Control g/m 2 g/m 1 Control gun g/m
1 day pre—treatment 10.5 10.7 9.5 .86 .88 .87 -’
.66 •74 ’-”
45 days poet—treatment 12.8 11.6 8.2 ’ .87 .82 .69
.57 .33
141 days post-treatment 11.6 9.6 4.4 .7 .73 .51
.61 .47
381 days post—treatment 11.6 8.5 4.]. .89 .28 .28
.46 .26
A’ Double underlining indicates statistical significance at the 1% level
level) folloving transformation of counts to log (14+1).
(single underlining, the 5%
.
b/
— Fiducial, limits not set,

-------
Comparison of the effects of lindane, carbaryl and chiorpyrifos on
soil arthropods un er pine is in progress in a mature forest setting.
The fauna is more diverse than in the plantation study described above,
but the abundances of giien species are lower. Table 6 reflects this
situation, for in it are listed only the 6 cryptcastigmatid species that
were abundant enough for analysiL of variance. After 40 days it appears
that chiorpyrifos had a relatively slight effect, that lindane had a
strong negative effect. and carbaryl had a mixed, but often positive
effect. At the same time chiorpyrifos had strong and statistically
significant effect on the miscellaneous arthropods and the prostiginata
as a group, while neither lindane nor carbaryl had a significant effect.
Much of the effect on the Frostigmata was the r.2sult of the sensitivity
of the Tydeidae. The Ne oatigznata were aurprisingly rare during this
time.
DISCUSSION
Years may pass before soil fertility problems resulting from
persistent pesticides use in forests become evident as was pointed out
by Thompson and dvards (1974). That is the underlying thought for thid
discussion.
Interpretation of a body of data arranged by taxonomic categories
should not be done line by line. Nor should the traditional 52 level of
significance be rigidly imposed on data from species that are notorious
for contagious distributions, data transformation notwithstanding.
Comparison between the lindane experiment and th€ Chiorpyrifos—
lindane—carbaryl experiment is probably justified despite 7.6 cm core
depths in one, and 5.i cm depths in the other. However, the single
point in time and reduced replication in the second experiment prevent
that data from standing alone.
Lindane effects
A long—term effect by lindane on all major groups is evident.
Therefore, annual applications of lindane for bark beetles would certainly
cause a continuous depression in the numbers of most species, and hcy
would probably have a cumulative effect.
The contrasting effects of the two application rates on the
Prostigmata, for which the Tydeidae hold the stat’..stical explanation,
moat likely has a biological explanation in the Mesostigmata data. The
average density of mesostigs increased in the low rate plots after a
year had gone by, but density was still declining in the high rate plots.
Although all of the mesostig data were sparse, there was a strong sugges-
tion of a phytoseild explosion relative to earlier levels, A differen-
tial effect of Lindane on predaceous mesostigs seems tc explain the
tydeid numbers.
The ongoing and increasing effect on the Collembola seems quite
straightforward. Family differences through time could be explained by
‘ /7

-------
TABLE 6. Percent reduction (increase) of Cryptostigmata 40 days
following application of three materials at two rates each, 13 control
plots, 6 each of spray treatment
chiorpyrifos lindane carbaryl
5.22 26.]. 1.57 7.83 5.22 26.1
g/m 2 gin? g/m 2 g/m 2 g/m 2 g/mZ
• Joshuella ap. 19 43 80 79 64 (176)
Eramaeus SF. 38 65 90 100 61 41
Carabodes ep. (149) 52 100 44 94 71
Scheloribates sp. 1 42 34 65 57 6 (239)
Scheloribates Bps 2 5/ 81 89 98 (121) 63
Neoribates Bps 14 40 84 96 (314) (218)
Total 30 63 82 85 16 (153)
Cryptostigmata
78

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1) downward movement of rebidues, 2) seasonal movement of the collein—
bo].ans, 3) community dynamics. I would expect that a combination of the
last two is moat likely.
Quantitative analysis of community structure, as affected by
lindane, wcs limited to the cryptostig component of the soil coimnunity.
For the cryptostigs there was greater depth of data and identification
to species. “Direct species counts, while lacking theoretical elegance,
provide one of the simplest, most practical, and most objective measures
of species r .chness” (Peat, 1974). Using that measure I found very
slight differences in counts among the plots before treatment and
declines in richness at both spray treat rates throughout the study,
whereas the index remained high in the concurrent control plots.
Simpson’s index, as oppobed to the Shannon index and others based
on information theory, is most sensitive to changes in the abundant
species (Peet, 1974). 1 have made the conscrvttive aanuinption that the
more abundant cryptostigs are more important to community structure and
fertility than the uncommon species. With one exception, Simpson’s
md - . .. . ranged from 0.86 to 0.89 in the pie—treatment and concurrent control
plots. At 381 days both spray rates had a i index of 0.28 pointing to a
long—term decline of population heterogeneity following lindane
application.
Rank corre1’ tion of the abundances of species proserves information
content by keeping species names associated with items in the frequency
distributions from each treatinert. This is done by neLther the Shannon
index nor Simpson’s index. The overall trend of correlations was a
decline over time. The ei nificance of the slight upturn for both
application rates at the 141 day point is uncertain. It may reflect a
greater sensitivity or some aspect of conmiunity structure not measured
by Simpson’s index • However, by this meas’.re there is also a change in
counity 3tructure.
Chiorpyrifos and carbaryl effects
The effect of chiorpyrifos and carDaryl on the cryptostigs 40 days
after application are quite different from each other, and from .indane
(Table 6). Chiorpyrifos seems to have a limited negative effect, and
carbaryl a very mixed effect. The greater number of positive effects
and only moderate negative effects caused by the high application rate
of carbaryl than caused by the lower rate, suggest that there may be a
general increase of prey because of predator mortality. Yet the slot’
reproductive cyci.e of the cryptostigs would require fortuitious timing
of the applications for this to show up in just 40 days. Until the fall
season’ a collections are in this question will be left unresolved.
COBCLUSIONS
Lindane residues bad a pronounced, lasting and increaaimg effect on
the soil fauna through 381 days. The effects include changes in total
numbers and in the counity struc:ture. The two altArnate materials,
ch].orpyri±os and carbaryl, have very different effects on the dominant
group, the cryptostigmata, at 40 *ys post—treatment.
79

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LITERATUR2 CITED
Dahisten, D. L. 1976. Lindane: An undesirable approach to bark beetle
control. Pages 16—21 in T. W. Koerber, ed. Lindane in Forestry
• . . A Coutinuin Controversy. USDA For. Sexy. Gen. Tech. Rapt. PSW—14.
Edwards, C. A., D. E. Reichle, and D. A. Crossley, Jr. 1977. The rote
of soil invertebrates in turnover of organic matter and nutrients.
Pages 147—172 in W. J. Mattson, ed. The Role of Arthropods in
Forest Ecosystems. Springer—Verlag, New York, N. Y.
Ghent, A. W. 1963. Kendall’s tau coefficient as an index of similarity
in comparisons of plant or animal cosinunities. Can. EntolAol. 95:
568—75.
Harding, D.J.L.. and R. A. Stuttard. 1974. Microaethropods. Pages 489—
532 in C. H. Dickinsor. and G.J.F. Pugh, eds. Biology of Plant
Litter Decompositi.n. Academic Press, London.
Keselman, Li. J., and J. C. Rogan. 1978. A comparison of the modified
Tukey and Scheffe methods of multiple comparisons of pairwise
contrasts. J. Amer. Stat, As oc. 7Z: 47-52.
Little, T. M., and F. J. Hills. 1978. Agricultural Experimentatton.
John Wiley and Sons, N. Y., 350 pp.
Lyon, R. L. 1971. Contact toxicity of 17 1nse ticides applied topically
P0 adult bark beetles. USDA For. Serv. gas. Note PSW—249.
Peat, R. K. 1974. The measurement of species diversity. Ann. Rev.
Ecol. Syst. 5: 285—307.
Price, D. V. 1973. Abundance and vertical distribution of microarthropods
in the surface layers of a California pine forest soil. Hulgar4ia
42: 121—48.
Thompson, A. B., and C. A. Edwards. 1970. Effects ‘f pesticides on
non—target invertebrates in fresh water and soil. Pages 341—386
in V. D. Guenni, ad. Pesticides in Soil and Water, Soil Science
Society of America, Madison, Wis.
S’nith, R. H., C. C. “rostle, and W. F. McCambridge. 1977. Protective
spray tests on three species of bark beetles in the western United
States. J. Econ. Entomol. 70: 119—25.
80

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QUESTIONS and COMMENTS
G. EENGTSSON : Using diversity indicies, e.g. Simpson’s
for describing changes in species composition (nuiflber,
diversity) might be obscured by changes in evenness which the
indicies have not been developed to describe. Fitting data
to models for species abundance distribution is another de-
ductive method. Why do you p:efer to use indicies in cnis work?
J.B. HOY : I chose Simpson’s index because it emphasizes
the more abundant species and Kendall’s rank correlation method
because it retains information content lost by the other
methods. Should there be inversions in the ranks Kendall’s
tau will detect changes missed by the index. I cannot discuss
the fine points of the Shannon index, but have re2.ied on Peet’s
(1974) review.
. GOULD : Were any of the increases in abundances sig-
nificant statistically?
J.B . HOY: Only the tycieids. They increased by 241%, a
figure that was significant it the 5% level.
81

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fl k4’ p. -_ n- 1-.
EFFECTS OF CARBOFURAN ON THE SOIL
MICROARTHROPOD COMMUNITY IN A CORNFIELD
*A B. Broadbent and A. 0. Tomlin
University of Gurlpli
‘Agrscidlsirr Ctrnada
Cn ,rnda
I NTRODUCT ION
Carbofuran, a carbamate insecticide, was introduced in 1967 by
the Niagara Chemical Division, F.M.C., under the trade name Furadan(R).
Granular carbofuran, applicd in-row at corn planting, is used
extensively in Ontario for control of the northern corn roo worm,
fliabrotica lo gicornis (Say).
Although the acute toxic effects of carbofuran to earthworms
have been well documented (Stenersen, Gilman and Vardanis 1973; Tomlin
and Gore 1974). its effect on the beneficial soil microarthropod
community is not well understood. The important role of these micro-
arthropods in the decomposition prccess of organic matter has been
re ,ieweo by Edwards, Reirhie and Crossley (1970) and Edwards (1974).
Any agricultural practice, including the use of insecticides, which
interf es with the composition of the decomposer community or shifts
its component lopu1ations’ equilibria may result in reduced litter
decomposition which could affect soil fertility.
Thowpson and Edwards (1974) have reviewed the effects of pesti-
cides on non-target soil fauna. Martin (1978) has reported the
effect of cari,ofuran (2.24 kg ..i./ha) on soil arthropods when applied
as gratu..les to the surf :e of a New Zealand pasture.
As part of a s u- y to determine the effect of carbofuran on the
decomposer community, soil cores were taken in a cornfield and the
resident microarthropods analyzed in the laboratory for population
differences due to carbofuran treatment.
MATERIALS AND METHODS
The experimental site was a plot (120 x 40 m) of sandy loam soil
in a 12 ha field of continuous corn under regular tilla e and management
at the Arkell Research Station, near Guciph, Ontario. Soil cores (5 cm
82

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diam.x 15 cm deep) were taken randomly from within the rows of a
carbofuran 10 G row-treated (1.12 kg a.i./ha, the recommended rate in
Ontario) and a control plot in the cornfield. In 1977, 10 soil cores
per treatment were taken at 4, L6 and 24 weeks after planting/treatment
day (May 10); in 1978, 12 cores per treatment were taken at 2 weeks
pre-treatment, at treatment day (May 23), and at 2, 6, 10, 14, 18 and
22 weeks post-treatment.
Microarthropods in the soil cores were extracted in the laboratory
by modified Tuligren funnels as described by Ton Iin (1977). Extraction
was completed in 72 hours with the animals being collected in glycerol:
ethanol:water (5:70:25). The arthropods were subsequently counted and
identified to family level for Collembola and suborder for Acari, using
a dissecting microscope. The numbers of specimens for each of these
major taxa from treated and control plot cores were subjected to anilysis
of variance or each sampling date. Logarithmic transformation of the
data was used to stabilize the high variance due to contagious distri-
butions of most of these arthropods.
RESULTS AND DISCUSSION
The proportions of the component populations of the soil arthropod
fauna in the cornfield during the growing season are shown for 1977
(FIGURE 1) and 1978 (FIGURE 2). More than 90% of the arthropods recovered
from each sampling date were mites and springtails. The predominant
genera of Acari and Collembo]a identified frcnn the cornfield are listed
in TABLE 1.
TABLES 2-7 (Appendix A) summarize the effects of carbofuran on
rious components of the soil arthropod fauna on successive sampling
dates in 1977 and 1978.
Differences between the control and treated cores were nor consistent
over the sampling period or between years. The total number of a;thropods
per core differed significantly (P<0.01) on only one sampling dat in
1977 (9 June, 4 weeks post-treatment) and one date in 1978 (25 October,
22 weeks post-treatment). On both these dates the number of arthropods
in the treated plot was approximate1 twice the size of that in the
control.
The myriapods. predominantly pauropods, symphylids, and dipiopods
comprised consistently less than 10% of the total arthropod population,
typically 2 to 5 per core except on September 1, 1978 when 12 per core
were recorded for the control plot. On that date the mean number of
pauropods per core in the control was 4.5 times greater than in the treated
plot.
83

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4 16 24
WEEKS POST TREATMENT
O COLLEMBOLA
• ACAR1
F’lJ MYRIAPODA & INSECTA
C CONTROL
T CARBOFURAN TREATED
lK I/1 o
(MAY 5,1977)
FIGURE 1. Proportions of the component populations of soil micro-
arthropods in control and carbofuran treated plots of
Arkell cornfield 1977.
OCOLLEMBOLA
! ACARI
MYRIAPODA a
INSECTA
C CONTROL
I CARBOFURAN
TREATED
IKq aL/ha
(M 23,t978)
FIGURE 2. Proportions of the component populations o soil micro-
arthropods in control and carbofuran treated plots of
Arkell cornfield 1978.
I
CT CT CT
I-
z
w
a-
C C CT CT CT CT CT CT
-20 2 6 10 14 18 22
WEEKS POST TREATMENT
‘Ii

-------
----—-
- -—-..-.-..—. -- -— ___
TABLE 1. The major famili s and geflera of Acari and Collembola
recovered fro the Arkell cornfield soil.
ACARI FAMILY GENUS
PROSTIGMATA
Pygmepho idae B k erda ia
Tarsoneinidae Tarsonemus
Scutacaridae Scutacarus
Nanorchestidae Speleorchestes
Tydcidae Tydeus
Eupodidae Eupodes
MESOS7I MATA
Asci.dae Arctoseius
Ascidae Pr amase1 lus
Rhodacaridae Rhodacarel lus
Digainasellidae Dendrolaelnps
Laelapidae Hypoaspis
Parasitidae Pergamasus
CRYPTOSTIGMATA
Oribatulidae Scheloribates
Oribatul idae Zygoribatul a
Oppiidae Oppia
Oppiidae piella
Tectocephidae Tectoc epheu5
ASTIGMATA
Acaridae Acarus
Acaridae Rhizoglyphus
COL LEMBOLA
Isotomidae Isotoma notabilis Schaffer
Iaotoinidae Proisotoma minuta (Tul lb erg)
I sotomidae Fol somides p rvus Fol soni
Entomobryidae Lepidocyrtus cyaneus Tul lb erg
Entomobryidae Pseudosinella sp.
Onychiuridae Onychiurus arinatus(Thllberg )
The pterygofe insects, mainly larvae of Diptera and Coleoptera,
were consistently less than 4 of the total arthropod populaticrI
(1 to 2 per core). No differences due to treatment were observed,
partiadarly as no corn rootworin population was found in the cornfield.
The n’ajor differences observed between the control and treated plots
involved the Acari rnd Collembola; the most obvious difference was the
larger prostigniatid mite population in the treated plot. This increase
was made up largely from the mite Bakerdania sp. (Pygmephoridae) which
85

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— —.-rs -f t .. — —
occurred in consistently higher numbers after carbofuran treatment
(at 4 weeks in 1977 and 2 an 6 weeks post.-treatnent in 1978). By
16 and 18 weeks post-treatment, in 1977 and 1978 respectively, this
mite had sho vn a significant (PcO.OS) decline in population in the
treated compared to the cor .crol plot.
The mesostigmatid mites (predominantly predacious) showed a
significant decline (P
-------
— - — —
,•e.- - l- ’—- - ‘-ft. .,. .••. — . - - —
ilartin r.oted that nearly all the species most affected by . hofuran
inhabit the Utter and surface Jayers of the soil. Future .-tudies should
include division of the soil core into hori. ons before e’.Lraction and
analysis, as well as study of carbofuran penetration i tro the soil.
CONC LUS IONS
The overall results of this soil microarthTopod survey are difficult
to interpret Although fluctuations in variou’ component populations
were observe. due to treatment thexe is no suFstantial reduction in thc
total fauna c r its composition by autumn. Mcre drastic popuiation
fluctuations can be expectec’ from the eff3cts of cultivation and the
addition of organic manure (Edwards and Lofty 1969). It is therefore
concluded that at current approved applicntion rates, carbofuran had r.o
observable long term detrimental effects on the niicroarthropod decomp,ser
comn nity. hence, it is conside cd unlikely that a significant effect
on litter decomposition in the cornfield soil occurred.
ACKN0WLEDC 4ENTS
The authors ac1 ’ow1edge financial support from the National
Research Council th ough Dr. C. R. Ellis, University of Guelph, and the
Ontaric Pesticides Advisory Committee, and gratefully acknoi 1edge the
technical assistance of P. Vander Deen and J. Miller. We also thank
Prs. E. E. Lindquist and W. R. Richards of Biosystematics Research
Institute, Agriculture Canada, Ottawa, Canada for identification of
Acari and Collembola respective. y.
Contribution No. 765, Research Institute, Agriculture Canada,
London.
87
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APPENDIX A
TABLE 2. Mean number of maj’r arthropod ta, a per soil core (n=l0)
in a carbofurr’ treated (T)(May 5) and control (C)
Plot of Arkell cornfield 1977
Weeks Post-treatment
4 16 24
(9.6.77) (2.9.77) (28.10.77)
C T C T C T
TOTAL
ARTHROPODS 69.1 131 •4** 84.5 53.5 52.5 67.1
ACARI 39.6 111.4* 48.7 22.4* 21.8 21.1
( .OLLEMBOL 25.6 16.4 31.9 27.9 25.9 39.9
MYRIAPODA 2.1 2.1 2.4 2.0 3.2 4.7
I 1 4SECTA 1.8 1.5 1.5 L2 1.6 1.4
Significant difference * P
-------
.1 3tC &fl—... — —— — ——
TABLE 4. Mean number of Colleqitola per soil core (n=l0) in a carbofuran
treated (T)(May 5) and control (C)
plot of Arkell cornfield 1977
Weeks Post-treatment
4 16 24
(9.6.77) (2.9.77) (28.10.77)
C T C T C I
COLLEMBOLA 25.6 16.4 31.9 27.9 25.9 39.9
ISOTOMIDAE 10.0 l.7** 13.2 7.3. 12.9 24.2
ENTOMOBRYIDAE 8.5 9.2 11.6 15.4 10.5 11.3
ON?CHIURIDAE 6.0 5.4 6.1. 4.b 1.9 3.9
SMINTHURIDAE 0.8 0 0.7 0.6 0.5 0.5
PODURIDAE 0.3 0.1 0.3 0 0.1 0
Significant difference - PcU.0l
89
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TABLE . Mean number of major arthropod taxa per soil core (n-12) in carbofuran treated (T)(May 23) and
control (C) plot of Arkell corncield 1g78.
Weeks Post-treatment
2 6 10 14 iS 22
(9.6.78) (6.7.78) (3.8.78) (1.9.78) (28.9.78) (25.10.78)
C T C T C T C I C T C T
TOTAL
ARThROPODS 100.0 105.2 133.7 127.3 145.1 153.7 186.2 198.8 118.1 99.9 73.4 146.7**
ACARI 65.5 82.4 95.4 110.7 116.2 116.7 136.2 158.5 70.7 !Q.9 39.4 64.2*
XILL.EMB0LA 28.0 17.6 30.8 10.8* 19.7 33.4 32.0 33.6 40.0 42.8 30.7 774**
MYRIAPODA 2.5 1.8 2.4 1.3 5.2 2.7 12.4 3.7 4.8 4.6 1.9 4.2
INSECTA 3.9 3.4 5.1 4.5 4.0 2.9 5.6 3.0 2.6 1.6 1.4 0.9
Significant difference - PcO.05; ** PcO.01
TABLE 6. Mean number of Acari per oi1 core (r.=12) in carbofuran treated (T) (May 23) and
control (C) plot of Arkell cornfield 1978. j
Weeks Post-treatment
2 6 lii 14 18 22
(9.6.78) (6.7.78) (3.8.78) (1.9.78) (28.9.78) (25.10.78)
C T C T C T C T C T C T
ACARI 65.6 82.4 95.4 110.7 llb.2 116.7 136.2 158.5 70.7 5(1.9 39.4 64.2*
PROSTIGMATA 49.8 73.2 49.6 74.7 76.7 78.7 113.4 127.9 57.4 32.6* 28.2 41.3
MESOSTIGMATA 13.0 6.2* 33.6 26.5 37.9 30.0 17.8 16.9 10.0 3•5* 5.0
ASTIGMATA 2.4 2.1 0.3 2.7 0.8 1.3 2.4 1.4 1.2 0.5 1.4 2.8
CRYPTOSTIGMATA 0.4 0.9 1.9 6.8* 0.8 6.7** 2.6 12.3 2.1 14.3* 3.3 15.1**
I’
Sigrificant difference - * P.cO.05; ** P0.01
-------
TABLE 7. Mean number of Collenibola per soil core (n=12) in carbofurai treated (T)(May 23) and
control (C) plot of Arkell cornfield 1978
Weeks Post-treatment
2 6 10 14 18 22
t9.6.78) (6.7.78) (3.8.78) (1.9.78) (28.9.78) (25.10.78)
C T C T C T C T C T C T
OLLEMB0LA 28.0 17.6 30.8 l0.3 19.7 33.4 32.0 33.6 40.0 42.8 30.7 77•4**
ISOTOMIDAE 21.2 7.8 18.2 5.1* 10.4 6.9 9.8 8.2 13.1 6.4 7.9 24.8
EN1 M0BRYIDAE 3.8 6.9 3.4 3.7 4.6 21.2* 10.4 15.4 17.7 15.9 9.2 30.2**
0NY HIURIDAE 2.0 2.1 7.2 2.0 4.5 5.3 11.2 10.0 8.8 20.2** 12.9 21.3
SMINThIJRIDAE 0.5 0.7 0.1 0 0 0 0 0 0.2 0.3 0.6 1.0
PODURIDAE 0.5 fl 1 1.9 0 0.2 0 0.6 0 0.2 0 0.1 0.1
Significant difference - * P<0.05; ** P
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LiTERATURE CiTED
Edwards, C. A. 1965. Effects of pesticide residues on soil invertebrates
and plants. Fifth Symp. Brit. Ecol. Soc. pp. 239-261. Ecology
and the Industrial Society. Oxford: Blackwell.
Edwards, C. A. 1974. Macroarthropods. Pages 533-554 in C. H. Dickinson
and 6. .1. F. Pugh (Eds.), Biology of Plant Litter Decomposition.
Academic Press, London.
Edwards, C. A. and J. R. Lofty. 1969. The influence of agricultural
practice on soil micro-arthropod populations. Systematics Association
Publication No. C, The Soil Ecosystem. pp. 2.7-247.
Edwards. C. A., D. E. Reichie and D. A. (rossley, Jr. 1970. The role
f soil invertebrates in turnover of organic matter and nutrients.
Pages 147-172 in D. E. Reichle (Ed.), Ecological Studies, Analysis
and Synthesis Vol. 1. Springer-Verlag, Berlin.
Martin, N. A. 1978. Effect of four insecticides on the pasture eco-
system. VI. Arthropoda dry heat-extracted from small soil cores,
and conclusior 1 s. N.Z. Journal of Agricultural Research 21: 307-319.
Stenersen, J., A. Gilman and A. Vardanis. 1973. Carbofuran its
toxicity to and metabolism by earthworm ( Lumbricus terrestris) .
J. Agr. Food Chem. 21(2): 166-171.
Thompson, A. R. and C. A. Edwards. 1974. Effects of pesticides on
nontarget invertebrates in freshwater and soil. Pages 341-386
W. D. Guei 1 zi (Ed.), Pesticides in Soil and Wate. Soil Sci. Soc.
Am. Inc., Madison, Wisconsin.
Tomlin, A. D. 1975. Toxicity of soil a p1ications of insecticides to
three species of springtails (Collembola) under laboratory conditions.
Can. Ent. 107: 769-774.
Tomlin, A. D. 1977. Pipeline construction- impact on soil, micro- and
mesofauna (Arthropoda and Ai nelida) in Ontario. Proc. Ent. Soc.
Ont. 108: 13-17
Tomlin, A. D. and F. L. Gore. 1974. Effects of six insecticides and a
fungicide on the numbers and biomass of earthworms in pasture.
Bull. Environ. Contam. Tox. 12(4): 487-492.
QUESTIONS d COMMENTS
M. S. GflIL BOV : How do you explain the increase of
some groups of microarthropods after the insecticide treatment?
In our experiments with DDT dusting of natural coniferous
forests in Siberia. the observed effect of a temporary de-
crease of collembolan population density followed by a great
fncrease in population was related to the suppression by
treatment of predators (Mesostigmata and Coleoptera).
A.B. BROADBENT : I can only hypothesize at this time.
io reasonable explanations are: firstly the suppression
of predators (particularly Mesostigmata) gave rise to an
increase in their prey (particularly Prostigmata and
92
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Collembola) arid secondly, due to the very toxic effect of
carbofuran to earthworms, and therefore the presence of a
large biomass of dead worms, plus all the food in the soil.
not consumed by these worms, a larger population of sapro—
phagous animals was suppo’ted. The latter hypothesis was
proposed by Martin (1978).
! : The speaker has concluded that because no
reduction in total fauna or its composition was observed
by autumn, therefore there were no long—term detrimental
effects on the microarthropod decomposer community due to
carbofuran reatment. When in fact, an increase in pop-.
u_ation of certain groups vas observed 22 weeks post—
treatment in 1978, can it still be concluded that no detri-
mental effects on the community or its litter decomposition
processes occurred? As ecologists, we mustn’t assume that
“more is better.” Would the speaker please comment.
AS. BROADRENT : Since no reduction in the populations
of saprophagous animals, in particular, was observed by
late season, I have concluded that no long—term detrimental
effects on the community or litter decomposition processes
occurred after carbo ur n treatment • This rather tenta ive
conclusion is supported by data from a litterbag study con-
ducted concurrently in the same plots. The rates of cornleaf
decomposition were monitored and we found that although a
lag in response was observed initially, by autumn no dtfference
in rate wac noted between carbofuran treated and control plots.
C.A. EDWARDS : ‘ollowing mention by the speaker of the
effect of carbofuran on organic matter breakdown, I should
like to comment that Dr. J.F. McBrayer and I investigated
the effects of phorat.e on corn litter breakdown in an
Indiana field and found a significant depression in decompo-
sition rate aft . .reatment.
9,
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INFLUENCE OF APPLICATION OF A FUNGICIDE, AN
INSECTICIDE, AND COMPOST UPON SOIL BIOTIC
COMMUNITY
Yuzo Kitazawa and Takashi Kitazawa
Umoersrly of Occupahiovuil and Ear,rnnmen Sal Health
Japan
INTRODUCTION
Soil fauna and soil flora constitute soil biotic community or
edaphon. Herbivorous and fungivorous animals consume leaf and woody
litter, furt i and humus and eject large amount of fecal pellets giving
rise to the crt.unby structure of the soil. These bring about the break-
down of dead plant bodies, mixing of them with soil, increase and
ma.ntenance of porosity, aeration and water capacity of the ;oil, which
are closely related to the increase and maintenance of t• . microbial
activity. Predation by microbivorous animals is related to che control
of microbial numbers and increase in net microbial production. Movement
of soil fauna facilitates the dissemination of bodies and spores of
microbes. Thus the soil fauna plays a catalytic role against microbial
activity and is related to the increase and maintenance of soil fertili-
ty.
The purpose of the present study is to pursue the changes in soil
fauna and soil microbes in the experimental field where insecticide,
fungicide and compost are supplied singly and in combination. This
study was made in joint research with Prof. Takai and his - oup of the
University of Tokyo, who engaged in the subjects other than soil fauna.
METHODS
Six kinds of experimental plots were set up in the experimental
-------
field of the Faculty of AgricuLtur.’ of the University of Tokyo as shown
in TABLE 1. Grasses and herbs in the plots were removed. Compost, a
TABLE_1. Experimental plots. —
Year
April 1973 May 1974
to to
March 1974 December 1977
A Control
Control B Compost 3 lcg.nr 2
Plots C TPN 40 ppm
SUC 10 ppm D T BHC 10 ppm
‘Aidrin 10 . TPN 40 pm +TBHC 10 ppm
F Compost + TPN 4’ ’BHC (Same Conc.)
fungicide TPN (Daconil) and an insecticide TBHC were supplied singly or
mixed to the plots in the amounts shown in TABLE 1. The size of a soil
sample core for small Arthropoda was 20 cm 2 in suri ce area, 5 cm deep
and 100 cm 3 in volume. Ten of them were taken from each pl.ot in 1974,
and in 1975 and afterwards five soil cores were taken from carefully
stirred 3500 cm 3 of soil taken from five places in each plot. Extrac-
tion cf animals with Tullgren funnels was continued for 48 hours. A
soil core for small hygrophilous animals such as £nchytraeidae, Netnatoda
and Rotif era was (2.5 cm x 2.5 cm x 4 cm) — 25 cm 3 in volume. Ten of
them were taken from each plot in 1974 and 1975 and afterwa. ds five were
taken from above stirred soil. Extraction of animals with Baermann
funnels was continued for 48 hours.
The survey of soil macrofauna was made only once in 1977 at the
end of the period of experiment by hand sorting, because the area of
the experimental plot was so small that each survey may injure the plot
so much and cause the decrease in density and biomass which are detri-
mental for this study. Number of taxonomic groups (families and orders)
and of individuals of macro—herbivores and macro—predators in 40500 cm 3
of soil in each plot were counted.
95
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I ESULTS
Main taxonomic groups extracted were Cryptostigmata, other Acari,
Collembola, Diplura, Enchytraeidae, Nematoda and Rotifera (Bdelloidea).
Besides these, Diptera larva, Protura, Syuiphyla and Tardigrada often
appeared in sma1 i. numbers. The numbers of these exonoinic groups were
smaller than those in the soil of forests in Tokyo. It was noticeable
that Pseudoscorp±onida, Isopoda. , Myriapoda, Copepoda and Turbellaria
were lacking in the experimental plots. Changes in numbers of extracted
animals are shown in APPENDIX A to F. Numbers of taxonomic groups and
those of individuals of macro—herbivores and macro—predators are shown
in TABLE 2. From the data shown in APPENDIX and TABLE 2, the following
TABLE 2. Number of taxonomic groups and individuals of
soil macrofauna. (Nov. 31 to l l917 I
A
Control
B
Compost
C
TPN
D
VBHC
E
‘i .B
F
CT.B
Number oi
Macro—
taxonomic
herbivores
4
1U
1
4
1.
5
groups
Macro—
predators
Total
inacrofauna
5
10
10
22
3
4
4
8
0
1
3
8
Number of
Macro—
indivi—
herbivores
10
71
3
14
6
29
duals
Macro—
predators
Total
macrofauna
44
55
134
207
25
28
7
21
0
6
6
35
results could be introduced.
Changes in numbers of small soil animals
Control plot (A )
Densities of soil animals of the control
those of the forest soils in Tokyo in general.
about one tenth of that of the latter. But the
plot were lower than
Number of Nematoda was
patterns of seasonal
96
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--
changes in numbers are similar to those seen 1 n natural soils of lokyo
districts. In the sun er of 1975, the air temperature was unusually
high and the precipitation was small. The soil of the jdot was very dry
and numbers of soil animals reduced.
Compost plot (B )
Numbers of all six main animal groups, namely Collembnla Cryptn-
stigmata, other Acari, Enchytraeidae, Nematoda and Rotifera increased
indicating marked influence of the supply of compost.
Fungicide plot (C )
After three years continuous supply of PN, numbers of a!1 of the
sLx main groups were diminished. Especially remarkable was the diminu-
tion in hygrophilous animals as Encbytraeidae, Nematoda and Rotif era.
Insecticide plot (D )
Numbers nf Arthropoda, namely, Cryptostigmata, other Acari and
Collembola were reduced. But the insecticide effect of TBHC on Collein—
bola seemed to dIsappear after six months from the time of supply.
Numbers of Enchytraeidae, Nematoda and Rotifera did not decreas but
increased though this tendenc was not clear in Neniatod.a in 1976.
According to the study of Yang and Takai, The amount of 1BHC had re-
duced to 30 to 10 2 after one.year from the supply to the soil.
TPN + TBHC plot CE )
All of the animal groups were remarkably influenced by the
combined use of these fungicide and insecticide. Especially small
Arctropoda were almost destructed by continuous combined supply. Ac-
cording to the study of Yang and Takai, the rate of decomposition of
TPN and rBHC was reduced in this pLot. In this experimental plot, an
insecticide Aldrin was supplied in May 1973. A part of it changed to
Dieldrin, and 75 to 90 2 of them remained till one year later. It seems
that there was influence of thede two compounds on decrease in animals.
Compost 1- TPN +Y 3HC plot (F )
97
-------
In 1974. numbers of Collembola, Enchytraeidae, Nematoda and
Rotifera became larger than those in olot E, and in 1975 the same trend
w s seen in Netnatoda, Enchytrae dae and though less remarkable in Col—
lembola, suggesting the existence of fuzwtion of compost to reduce the
detrim nta1 effect of TPN andYBHC. But in 1976 this trend was seen
only in Nematoda. It seems that in this plot the detrimental effect
of three ye. rs combined use of TPN,TBHC and of Aidrin used in 1973
exceeded the easing effect of supply of compost.
Changes in numbers of soil macrofauna
At the end of four years e,rperiment, numbers of taxonomic groups
of soil macrofauna was the largest in the compost plot, followed by the
control plot and the least in the combination plot of TPN at d1’BHC as
seen in TABLE 2. It is also noteworthy that tbe number in F plot ex-
ceeded that of the plot E and C, suggesting the easing effect of supply
of compost. Numbers of individuals of macrofauna was also the largest
in the compost plot, followed by the control plot, the least in the plot
of coinbimation of TPN andT8RC. And the number in F plot exceeded
that of E, C, and D. Thus the patterns of changes in numbers of Taxo—
nomic groups representing the degree of community diversity and of
individuals were almost the same.
DISCUSSION
The results of the experiments indicated that there were detri-
mental effec.ts of continuing and combined use of TPN and $BHC agniast
all of the soil fauna, and that the supply of TPN generally redu..ed
numbers of small a.. 6 d large soil animals, ‘ hi1e the supply of xBBC did
not reduce the numbers of Enchytraeidae, ematoda, Rotif era, but
increased them. The supply of compost increased all the groups of the
soil fauna concernec , and eased .he detrimental effect of the supply of
combined TPN and TBRC to some extent. These general trends were a1 eady
98
-------
recognized in 1974, the first year of the period of this study, and some
discussions were made (KitEzawa and Kitazawa 1975)
The “elation between changes in numbets
of soil fauna and those of microbes
The changes in numbers of microbes, soil respiration and dehydro—
genase activity in the soil of the same experimental plots were studied
(Takai and ‘Lang 1975), (Takai 1977). The relations between changes in
numbers o soil suna and those of soil microbes were taken into con-
sideration. The results in soil microbes axe &ummarized. as followsi
Compost plotj
The supply of compost increased numbers of fungi, total bacteria
and gram—negat ve bacteria to some extent, and also incriaac9d rates of
soi) raspiration and dehydrogenase activity of the soil.
TPN plot (C )
The supply oi TPN decreas ed numbers of fungi and spore—forming
bacterIa, but ineieased numbers of total bacteria, especially remarka-
bly increased those ,f TPN—resistant gramu—negative bacteria. It de—
creased rates of soil respiration and dehydrogenase activity o the
soil.
B}IC plot (D l
No marked influence of supply of r BHC upon numbers of microbes,
soil respiration and dehydrogenase activity was recognized. However,
tie centinuous use of it increased numbers of gram-negative bacteria a
little.
TPN + BHC plot (E )
The joint supply of TPN and P BHC decreased numbers of fungi.
But it increased the number of total. bacteria a little and increased
markedly that of gram—negative bacteria.
99
-------
Compost + CPN + BKC plot (F )
The joinc supply of compost, TPN and IBHC eased the decreasing
activity of TPN to the number of soil fungi and soil respiration rate,
and accerelated the increasing effect of TPN and (BRC on the nembers of
total bacteria and gra’n—negative bacteria.
The relations among effects of compost, TPNI fBi on numbers of
soil fauna, soil microbes and rates of soil respiration and dehydro—
genase activity in the soil, were diagrammatically summarized in FIGURE
1.
More precise reports on microbes, microbial activity, decoiiip si—
tion and residue of che itical compounds will be published soon by Takai,
Wada. Yang and Mukai.
SUNM&RY
The effects of compost, a fungicide TPN, and an insecticide
TBHC, supplied singly or combined, on numbers of soil animals were
studied for four years, and the changes in them were discussed in rela-
tion to the changes in numbers of soil microbes, ate of soil respi-
ration and dehydrogenase activity in the soil which were studied in the
same experimental plots by Takat and others. The outline of the results
were diagrammatically summarized in FIGURE 1.
100
-------
APPENDIX A. Numbers of small soil animals extracted with Tullgren
funnels. No.11.00 cm 3 with S.E. Compost, fungicide and insecticide were
supplied on 15 and 16 May, 1974.
1974 £1MAY 2OMAY 1JUNEJ1SJUNEI 1SJULYJ I9SEPT.I 6DEC.
I Co1lemboJ
A
B
C
D
E
F
88±2.0 27.0±39 217±3.6 7.3±1.2
88±2.0 19.3±2.4 25.8±22 20.4±3.3
111±2.23 67±2.4 a6j23 2.9±0.8
35±1.35 4.0±0.7 13±0.8 0.5±02
2.0±1.05 2.6±0.9 0 0 )
2.0±1.05 0 0.2±0.13 1.2±0 6
Crypto t _ . . . ,
83±1.6
11.2±2.1
P7±0.8
46±1.5
2.0±’ .7
88::3.3

10.8±3.8
19.3±33
12±0.3
39±1.2
22±0.8
13±3.5
9.9±3.7
180±3.4
10.4±26
20.8±42
10.6±34
36.2±17
A
B
C
D
E
F
9.3±1.1
63±1.1
9.0±1.5
0.
0.1±01
0.1±0.1
1.5±0.5
1.7±04
1.3±0.5
0
0.1±0.1
0
2.5±07
2.1±1.0
1.5±0.4
0.1±0.1
0.5±0.5
0.1±0 1
1.7±08
19±0.9
1.2±0.9
0
0
0__—
1.5±0.5
19±0.2
0.7±0.3
0.1±0.1
0
0
10.6±4.9
15.1±2.4
1 2±0.8
0
0
0
1.5±0.4
2.0±0.7
0.5±0.3
0.5±03
0
0
Other Acarl.
A
B
C
D
E
F
03i3.0
10.8±3.0
7.9±1.5
- 0
0.5±0.3
0.5±0.3
18±0.5
2.0±0.b
2.3±0.6
0.3±0.1
02±0.1
0.1±0.1
3.B±ft7
12±0.9
1.6±0.4
0.3±0.2
0.1±01
0.1±0.1
2.9±0.6
45±0.7
1.5±04
0
0
0
2.1±0.7
50±0.8
1.4±0.7
0.3±0.3
0
0.2±0.2
4.8±1.0
135±1.5
2.4±0.6
0.3±0.2
0.3±9.2
0
36±0.8
3.8±0.4
0.8*0.4
0.1±0.1
0.1±0.1
0
fliplura
A
B
C
D
E
F
0.3±0.2
0.3±0.2
0.6±0.3
0
0
0
0.2±0.1
02±01
0.1±9.1
0.1±0.1
0
0
0.2±0.2
0.1±0.1
0
0
0
0
0
0
0
0
0
0
0.2±0.1
0.2*0.1
0
0
0
0
0
03±9.2
9.3±9.2
0
0
0
0
0
0
0
0
0
101
-------
APPENDIX B. Numbers of small soil animals extracted with Baermann
funnels. No./25 cm 3 with S.E. Compost, fungicide and ins ctitjde were
supplied on 15 and 16 May, 1974.
: 974
1l) iAy 2OMAY IJUNE I ISJUNEI 1SJULIYIIQSEPT.I 6DEC.
A
B
C
D
E
F
- F dae — -
52±0.8 12±0.4 2.1±0.8 0.6 ft2 2.1±0.6 09±0.3 [ 0
52±0.8 27±0.7 2.2±05 1.8±0.1 4.0±0.9 09±0.6 0
32±10 L3j0.6 0.7±03 0.8±0.4 0.1±0.1 0.2±0.1 0
4.4±0.8 34±05 45±07 7.2±2.7 8.8±14 2.3±0.4 0.3±0.2
39±1.1 1 6±0.7 1.6±0 5 2.8±0.7 1.5±0.4 32±1.3 0.1±0.1
39±1.1 14±0.8 1.1±05 41±15 ±Li.... !±l 4 1..±04
en .atoda
A
B
C
D
1
F
39.2±84
39.2±8.4
532±9.4
315±44
24. ?±45
242±45
114±14.0
658±69
77.6±106
46.1±94
957±134
230±4.2
44.8J:?.3
49.5±6.2
51.9±9.4
611±10.6
28.0±50
746±201
453±4.0
506±6.5
317±6.8
31.0±2.4
14.9±40
29.9±5.2
32.7±4.4
397±43
138±51
204±2.8
157±2.4
442±61
84.6±14.7
228±39.5
21.2±4.7
42.8±6.2
62.1±22.1
547±b.2
1 5 1j237
194±19.1
49.6±116
llu±10.4
52.5±131
126±143
oLifera
A
B
C
D
E
F
1.5±04
1.5±0.4
0.1±0.1
0.2±0.1
1.6±0.9
1.6±09
2.7±0.7
1.0±0:3
0.1±0.1
1.9±07
0.2±01
— 0 —
1.2±0.4
1.5±07
0
1.9±0.6
0.4±0 3
0.4±0.2
0.2±0.1
0.1±0.1
0
0.3±02
0
C
0
0.3±0.2
0
0.2±0.1
0
0
0.9±0.3
16±1.1
0
2.8±0.7
0 3±0.2
0.6±0.3
2.6±0.8
6.2±1.2
0.1±0.1
6.1±1.0
0.1±0.1
2.6±1.3
irdigrad
A
B
C
D
E
F
0
0
0
0
0
0
0
0
0
0
0
0
0.1±0.1
01±01
0.2±0.1
01±0.1
0
03±0.2
0.2±0
0.4±0.2
08±0.3
0
0
0
0
0
0
0
0
0
0.2±0.1
0
0
0
o
0.1±0.1
0
0
0.1±0.1
0
0
0
102
-------
— — 1 ..r..fll flmWW ._.. W fl’C — - - - - — -
APPZNDIX C. Numbers of small soil animals excracted with Tuligren
funneLs. No.1100 cin with S.E. Compost, fungicide and insecticide wer
supplied on 7 May, 1975.
1975
2MAY ( I2MAY 9JUNE 21JLJLY I 3SEPT. 2NOV.
Cc ,l lembola
A
2±0.4
1.6±0.5
30±1.1
0.6±02
0
4.0±0.7
B
7.6±2.1
1 34±31
7.2±1.1
2.8±1.0
0
1 5.2±2.6
C
1.6±05
02±0.2
02±0.2
0
0
7.2±32
D
2.6±07
10±0.5
1.4±0.5
18±08
0
12.6±1.6
E
0.6±0.4
1.0±0.3
0.1±0.4
02±02
02±0.2
1.4±05
F
7.0±1.0
12±0.2
t6± 0 6
1.4±0 6
0.4±0.4
7.0±1.3
Cryptos j Jnata
A
7.2±1.4
10.0*0.9
5.4±07
1.2±04
0.6±0.6
17.0±32
B
12.4±0.8
138±07
6.8±1.9
36±1.0
0
32.8±1.6
C
1.2±02
0
0.2±02
08±06
0
0.8±04
D
0
0
0
0
0
32±0.7
E
0
0.2±02
0
0
0
0
F
0
0.2±0.2
0
0
0
0
Other Aca’-
I
—.
A
2.6±1.1
( 0.4±0.8
.4±1.5
1.2±06
4 4±1.5
32±0.6
B
6 8±08
17.4±31
1 1.4±24
94±10
1 0±0.3
38±0.9
C
22±08
32±09
1.0±0.6
0.6±0.2
0
0.8±0.4
D
0.6±0.4
0.8±04
1.2±0.4
1.6±0.7
32±04
38±1.6
E
0
0.2±02
0
0.4±0.2
0
0
F
1.2±04
0
0
0.2±02
2.0±0.6
0.2±02
‘inlura
A
0
0.2±0.2
0
0
0
0
B
0.8±06
0.2±0. 2
0.2±0.2
0
0
0
C
0.2±0.2
0
0
o
0
0
D
0
0
o
0
0
0
E
0
0
0
0
0
0
F
0
0
0
0
o_
0
103
-------
APPENDiX 0. Numbers of small sail animals extracted with Baerinann
funnels. No.125 cm 3 with S.E. Co’np,st, fung±cide and insecticide were
supplied on 7 May j975 .
1975 2MAY 12MAY I 9.IUNE 2SJULY 3SEPT. 2NOV.
chvLrae
da.e
_________
A 0
B 02±0.2
c 0
0 0.4j0.2
E 0
F 1.0±0.0
0.4±0.2
02±02
0
02±0.2
0
0.2±0.2
0.6±0.4
2.0±0.6
0
1.0±0.8
0.2±0.2
1.8±0.6
0
04 04
0
0
0
0
0
0
0
0
0
0 1
0
0.0±0.4
0
0.2±0.2
0
0.4±0.2
—
Nematoda
-
A 183±19.7
B 822±404
C 124±86
0 181±27.0
E 384±4.0
F 214±158
114±27.7
321±29.1
144±22.0
155±10.7
47.8±85
172±22.3
916±2.4
376±2a6
70.6±12.9
79.0±10.5
546±7.7
162±12.7
119±117 29.2±2.2
399±2 .5 183±181
232±54 14±0.4
178±87 70.0±65
806±55 15.0 4.4
593±314j 337±2 4.2
203±9.4
478±535
32.2±4.4
109±14.1
95.0±5.8
534±5.2
(otifera
A 1.3±0.6
B 1.4±05
C 0.2±02
D 2.0±06
E 0.2±0.2
F 0.6±0.2
10±0.7
3.0±0.6
0
30±1.3
0
06±0 4
4.0±1.1
90±0.6
02±0.2
34±0.8
0.2±0.2
0
0.8±05
5.4±09
02±02
2.6±0.4
0
0
04±0.4
08±0.4
0
04±0.2
0
0
18±1.5
7.0±1.5
0
2.8±08
32±2.7
2.2±1.0
___
rd g ad
- —
A 0
B 0
C 0
D 0
E 0
F 0
0
0
0
0
0
0
0
0
0.4±0.2
0
0
0
0
0
0
0
0
0
0
0
0
02±0.2
0
0
02±02
0
0
0
0
0
10 1 e
-------
- — -..‘. —. .--.-. ——
APPENDIX E. Numbers of small soil animals extracted with Tuligren
funne]s. No.1.OO c m 3 with S.E. Compost, fungicide and insecticide were
supplied on 15 May. 1976.
IOMAY 1 2OMAY I i JUNE 21 3 liLY I 12NOV._
o1lembola
23.0±2.6 84±15 232±4.2 6.4±13 6.0±0.6
26.0±1.3
14.6±1.0
D 65.2±36
E 1 31±1.0
F 10.2+1.4
10±1.7
08±0.4
36±09
0.2±0 2
02±02
268±2.2
04±0.2
82±0 9
04±04
— 0.2±0.2
17.4±2.3
1.2±08
4.2±16
0.2±0.2
1.4±0.8
315±4.0
172±38
1 82±2.9
38±0.7
11.0±2.2
“rv tostia m
ta
A 660±12.4
B 352±6.1
C 6.0±2.0
D 6.8±15
E 0
F 1.2±04
26.4±38
260±2.9
1.8±0.6
04±0.4
0
0
76.4±105
600±6.4
1.0±0.3
50±0.9
1.0±0.6
0.8±06
80±17
246±1.7
0
2.2±0.9
02±02
0
184±32
230±30
0.2±0 2
28±0.6
0
0.3±0.3
Other Acari
A 82±0.5
B 6. 1±1.2
C 58±14
D 18j05
E 1.0±05
F’ 1.8±0.6
3.2±02
14±11
1.0±05
0.8±04
0
0.4±0.2
21 2±32
380±0.6
1.8±0.5
0.4±04
2.0±08
08±0.4
2.0±03
14±5.7
0.8±00
04±0.2
0
0
124±11
143±1.3
1.4±0.7
4.0±00
14±09
0.8t03
—
A 0.2±0.2
B 0.2±0.2
C 0
D 0.2±0.2
E 0
F 0
oz±0.
0
0
0
0
0 —
0
0
0
0
0
0
a
0
0
0
0
0
0
0
0
0
0
1O5
-------
APPENDIX F. Numb Tt of small soil animals extracted with Baerinann
funnels. No./5 . m 3 with S.E. Compost, fungicide and insecticide w ire
supplied on 15 Ma.,, 1976.
1976
IOMAY ZOMAY 15JUNEt 2IJULY1 )2NOV.
Enchyt ran ” e
A 0.8±0.5
B 10±1.0
C 1.0±0.5
D 0.8±0.5
E 1.0±0.6
F 0.4±0.2
1.0±0.5
22±0.6
0
22±15
0
0
1.8±0.7
21.8±28
0
0.0±1.4
0.2±0.2
0.2±0.2
0.4±0.2
40±06
0
1.8±0.4
0
04±0.2
0.2±0.2
0.6±0.2
0.6±0.4
0.6±04
0.2±0.2
22±0.5
Nemat oda
A
B
C
1)
E
F
216±41.2
357±71.2
170±14.5
300±23.9
153±83
324±29.7
189±20.8
366±244
92.0±16
155±60
54.0±4.5
125±0.8
401±191
720±54.3
108±171
185±11.9
562±15
270±9.9
169±238
4Y7±211
40.2±63
89.4±6.4
110±1.0
121±1 0.5
436±33.9
303±388
644±16
166±15
60.2±7.0
207±20.7
Rotifera
—
A
E
C
D
E
F
4.5±18
11.8±2.2
1.0±0.8
2.6±06
0.2±0.2
1.8±0.5
28±0.9
226±4.2
2.6±18
6.4±0.8
04±0.4
2.0±1.8
2.8±1.5
282±43
0.8±0.6
10.2±3.0
4 6±3.7
2.0±1.3
50±1.2
10.8±6.3
60±3.2
80±1.3
3.4±2.9
0.2±0.2
3.6±1.3
10.4±30
1.2±0.b
62±12
0.2±0.2
2.4±0.5
ardigrada
A
B
C
D
E
F
0
0
0.2±0.2
0.2±0.2
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
o
0
0.4±02
0
0
0
o
106
-------
(+) ACCEREi ATE. INCREASE (-I iNHIBIT. REDUCE
(±) (+) OR (-). NO INFLUENCE
FIGURE 1. The relations among effects of compost, TPN and KBHC on
numbers of soil fauna, soil microbes, rates of soil respiration and
dehydrogenase activity in the soil. (Kitazawa, Yang, Wada, Takai 1975.
From Takai 1977)
I. .
0
..
-------
ILTERSI’tJRE CITED
Kitazawa, 7 and T. Kitazawa. 1975. Effer.ts of manure, an insecticide
gBHC, a fungicide TPN on numbers of soti mesofauna. Abstracte of First
Franca -Japanese seminar on soil zoology. 11—16.
Takai, Y. a d S. Yang. 1975. Changes in soil wicrof Iota when supplied
with compost, insecticice and fungicide. Effects of incorporation of
chemical substance into the soil ecosyste 1 o. Annual report of 1974.
16—19. (In Japanese)
Takai, Y. 1977. Effects of incorporation of chemical substance into
the soil ecosystem. Annual Report of the Co—operative Research.
Environment and Human Survival. Ilittist. Educ. Cul. 276—285. (In
Japanese)
108
-------
• EFFECT OF TWO HERBICIDES ON THE SOIL INHABITING
CRYPTOSTIGMATID MITES
T. Bhattadiarya and V. C. Joy
Vwa BhariIi Urnvt’rsity
India
INTROD(JCTIO ’l
Herbicides administered for the elinination of unwanted plants in the
agroecosysteins may unintentionally upset the balance of the ecosystem by
affecting the sensitive nontarget soil animals like cryptostigmatid mites.
Effects of these chemicals on the soil fauna have been rec ntly reviewed
by Rijsackers and ver der Drift (1976). Notwithstanding this, very little
information is available to date regarding the influence of weedicides on
the nontarget fauna of the soil in t -opical countries like India. Here the
use of these chemicals is gaining momentum, with the development of modern
agrotechnical measures following a “grow more food” campaign. This communi-
cation deals with the possible ill effects of two herbicides, Nitrofen
(2,4 - dichiorophenyl - 4 - nitrophenyl ether) and Propanil (3,4 - dichloro-
propion anlilde), which are of very common use in India, on the community
structure, species diversity and density of cryptostigmatid mites, under
field and laboratory conditions.
MATERIAL AND METHODS
A rabi crop (early October to February) of a dry cultivatable variety
of pacidy, “Pusa - 2 2 l , was raised for the experimental purposes in three
small highland plots with laterite soil. All the normal agricultural
manipulations wure employed simultaneously in the plots except for the
application of herbicides in the two treated plots. S 4 ngle applications of
tne herbicides, Nitrofen (Tok, E—25) and Propanil (Stam, F-34), were made
in the lowest agricultural doses recommended for general weed control in
paddy crops in India by Mukhopadhyay and Bhattacharyay (1967). Nitrofen
at the rate of 2 kg’ al/ha was sprayed as a pre—emergence h rblcide, while
Propanil was used for post-emergence weed control at the rate of 3 kg. ai/ha.
Details regarding the maintenance of the crop, soil samplings, extraction
and identification of the fauna are being published elsewhere (Bhattacharya
and Joy, in press). The field experiment was conducted from the month of
September 1977 to February 1978, and soil samples were collected at fort—
nightly intervals.
Analysis of the data obtained from the field experiment were made
with respect to the relative abundance and frequency after Dindal (1977),
and density and species diversity of cryptostigmatid community. The latter
was compared with the help of Shannon and Weaver index (Shannon and Weaver,
1963). A comparison of the cryptostigniatid density as a whole and of the
dominant species (frequency>50%), between the treated and untreated plots
was made and thei - statistical significance was checked with the help of
‘tw’ test (Lord, Pages 120-122, quoted in Snedacor and Cochran, 1947).
Percentile deviation of the density 0 f these groups In the treated plots,
in relation to that of the untreated plot was also estimated.
109
-------
The dominant species encountered In the field experiment were subjected
to .he same doses of the two herbicides under laboratory conditions. A known
number of live cryptostigmatid mites of the same age group and size, reared
for the purpose under laboratry conditions, was placed in special treatment
cells c’lntaining sterile soil sprayed with the herbicide solution. Details
of th .. rearing techniques are given elsewhere (Bhaftacharya, Joy and Joy,
1978). Untrea’ed control cells were also maintained in th! laboratory and
the mortality of the mites in both the sets was estimated after 7 days.
RESULTS
Field experiment
The overall density of all tile cryptostigmatid species collected from
the untreated (UT), Ilitrofen treated (T 1 ) and Propanil treated CT 2 ) plots
is given in Figure 1. In all, 11 species were encountered in the UT p’ ,ot
while there were nine each in the T 1 and T 2 plots.
Rel ati ye Abundance and Frequency
Scheloribatesaiblalatus and Qp ia nodosa were the two dominant species
in all the plots (Table 1). Their dominance was more prominent in the treated
plots prior the the herbicide applications. Figure 2 shows the degree of
response by different cryptost gmatid species to the herbicide. Both S.
albialatus and 0. nodosa became subdominants after Nitrofen application while
only S. albialatus lost its dominant status as a result of Propanil treatment.
Parop Ja sp.ind Archegozetes longisetosus which were subdomjnants in thc T 1
1ot became occasional and rare respectT iiy, while Galumna sp. and Cosmoch-
thonius emmae remained unaffected. In the T 2 plot most Uthe species
renamed unaltered In their status after the herbicide treatment.
Species Diversity
The analysis of the cryptostigmatid community according to the Shannon
and Weaver index (Table 2) shows that there is no significant change in the
species diversity after the application of Nitrofen (t=O.198), while the
Propanil treatment signifantly shifted the diversity of species (t=4.52,
P < 0.05).
Table 2: A COMPARISON BETWEEN THE SPECIES DIVERSITY OF
CRYPTOSTIGMATID COMMUNITY CEFORE AND AFTER THE
HERBICIDE TREATMENT.
HERBICIDE
N
S
H’
i
S. E.
N ITRO FEN
Pre-treatment
100
8
1.66 56
+
0.0682
Post-treatment
96
7
1.65517
+
0.0613
PROPANIL
Pre-treatment
Post-treatment
111
161
9
8
1.82685
1.40540
+
+
0.0692
0.057
110
-------
Pbroppio sp.
Figure 1. OVERALL POPULATIO1 DENSITY OF THE
SPECIES IN THE EXPERIMENTAL PLGTS.
c±
D(Sche oflbatessp)— -(Sd)
0(Opposp. ) - - (Sd )
Sd( ropçiosp. ) - (0 )
Archegozete5Sp )- - ( R)
0(Gdumnosp. ) —10)
O(Cosmochthori sssp) - ( 0)
R( PiIo tetla sp.)
R(Eportatuka sp.)
T Mjcmzetes sp.
re2
DIFFERENT CRYPTOSTIGMATID
D( Schdaibates sp4 —(Sd;
Figure 2. RESPONSES OF THE DIFFERENT CRYPTOSTIGMATID SPECIES TO THE
HERBICIDE APPLICATION IN THE TREATED PLOTS.
111
111 orib es ______
..I ______
________ L
25 Opposp 54. Epoñ xâ sp.
I r i _
1O G rnosp.
.I ____
0 — 5
1 A egozets p, 1
____ 5
5.1. Atab eUo sp
Sf — Cryptac i W
2UTP t •T 1 PIot •T Pt t
Agurel -
P trofen
Propanit
Pre treat. POst treat.
Pre treat. Pbgt treat
D(Oppiosp. ) - (D )
0(POropp sp. ) - - (0 )
R(A the ojetessp)— -(R)
R(Pdobot Io5p. ) - —(R )
R(Cosniov tith u sp.) ( R)
(R) ——Q iicrozetessp.)
(0 )- —Sd(Galumnasp.)
(R)Eporibatuto sp.)
-------
Table 1: RELATIVE ABUNDANCE AND FREQUENCY JF THE
CRYPTOSTIGMATID SPECIES IN THE EXPEkIMENTAL
PLOTS
40% Subdominant
10% Rare
30 to
10 to
I
50% Subdominant
30% Occasional
inq’
UT T i_________ T 2 ____________
SPECIES Pre- 4 .reat.
RI
F
Pre-treat.
RA F
5.0 20.0
RA ___ F
0.5 3.5
0.3 1.7
Post-treat.
RA F
7.3 10.6
Post- reat.
F
3.6 9.5 1.2 5.1
Cosmochthoni us eninae Ben ese
Cryptacarus dendnl setosus
Bhatta harya, Bhaduri and
Raychaudhuri
Z Archegozetes longisetosus Aoki
Microzetes auxillaris Grandjean
ppia nodosa Hauner
Paroppia sp.
Paralamellobates bengalensis
Bhaduri and Raychaudhuri
Gal umna sp.
portibatula sp.
Sche1orjbj tas albialatus Hanmer
Pilobat 1la sp.
13.0 46.7 1.0
- - 12.5
28.1
30.2
33.0
12.0
2.1
17.0
36.2
17.0
73.3
40.0
3.6
3.6
18.9
17.1
6.2
1.9
41.4
6.4
0.3
13.9
2.7
23.0
3.5
13.8
12.1
48.3
13.8
1.7
40.0
5.2
62.1
6.9
0.6
6.2
46.0
4.4
2.6
18.0
71.8
12.8
6.7
6.7
66.7
23.8
10.0
6.7
76.2
9,5
10.0
1.0
25.0
1.0
26.7
6.7
66.7
6.7
RA - Relative abundance: > 40% Dominant
10.4 11.9 12.6
- - 7.2
10.4 38.3 31.5
- - 1.8
18.6 38.5
10 to
22.4
0.6
F = Frequency:
46.2
2.6
> 50% Dominant
-------
N = Number of Individuals
Number of Species
H’= Shannon and Weaver Index in log e
Comparison Between the Densities
The fluctuation in the densities of cryptostigmatid population as a
i hole and of the two dominant species under consideration (frequency> 50%),
in the three plots at various intervals of sampling are given in FIgure 3.
Table 3 shows that both Nitrofen and Propanil significantly decreased the
density of cryptostigmatid mites as a whole after their application.
Table 3: Values of ‘tw’ test between different iptervals of
sampi ing in the experimental plots.
SAMPLING CRYPT0STIG tATA
OCCASIONS UT T i T2
- tw tw
I vs. II 0.285 0.222 0.688 ***
II vs. III 0.207 —+0.395 * 0045
III vs. IV 0.117 0.222 —+0.420 **
IV vs. V 0.225 0.149 0.271
V vs. VI 0.123 0.143 0.261
VI vs. VII 0.354 * 0.157 0.148
VII vs. VIII 0.222 0.096 0.123
VIli vs. IX 0.393 * 0.372 * 0.571 ***
* P< 0.05 The a’rows indicate the
** P < 0.02 stage at which herbicide
*** P <0.01 was treated
TLrning to the dominant species, it was noted that both the herbicides
depressed the population levels of S. albialatus and 0. nodosa on their
application (Table 4). However, the effèct was more astic and statistically
significant in the case of Nitrofen, for both the species.
Table 4: A comparison between the densities of the two dominant
specle of Cryptostigmata In Untreated and Treated plots
after the herbicide application.
SPECIES
(ii
140./Sample
T 1
tw
UT
No./Samp
12
le

tw
Scheloribates
7.6
1.4
0.614
***
7.3
6.0
0.121
albialatus
Oppia nodosa
19.3
3.9
0.441
*
21.0
12.3
0.231
** P . 0.02 *** P < 0.01
113 I
-------
Figure 3. CHAI4GES IN THE DENSITY OF THE TOTAL
AND OF THE TWO DOMINANT SPECIES.
2CO
2
SwnfJriç OCCQSIO.5
8
9
I
I
a
CRYPTOSTIGMATID MITES
FIgure 4. RELATIVE PERCENTILE DEVIATIONS IN THE DENSITY OF THE TOTAL
CRYPTOSTIGMATID MITES AND OF THE TWO DOMINANT SPECIES IN THE
TWO TREATED PLOTS IN IELATION TO THE UNTREATED PLOT.
U. k
13
IKX k Oi øcw

i . i . I oec. ‘ Jan. I Feb. 1
1977 1978
---UTpsot *T $@t —.O—T 2 pbt
Cryptc6t n a
th LU 1
20C
theb b sP.
I
H
Q— .
3 4 .5 6 7
-------
An analysis of the percentile deviations of the densities of
Cryptostig.nata in toto and of the two dominant species in the two treated
plots, in relation to those of the untreated plot at various intervals of
sampling (Figure 4) also Indicated that Nitrofen has more adverse effect on
the nontarget organisms under field conditions.
Laboratory experiment
Results of the experiment conducted in the laboratory (Table 5)
reveaied that the agricultural dose of Nitrofen killed all the individuals
of S. albialatus a d 0. nodosa within 7 days, while that of Propanhl killed
all the speciiiiëiis of 0. n dö a; about 6.5% of the total S. albialatus were
still alive within that period. On the other hand, in the untreated control
cells all the individuals of S. albialatus and 0. nodosa remained active
after 7 days and iany of these cells cantained newly laid eggs.
Table 5: EFFECT OF THE AGRICULTURAL DOSES OF HERBICIDES ON NO
SPECIES OF CRYPTOSTIGMATID MITES UNDER LABORATORY
CONDITIONS.
SPECIES
R
N
A
‘!L
R
L
11 A
T i
I D
R
L..J2__
N A I
D
I
D
0. nodosa
S. albialatus
20

250 2 O
220 j 220
-
-
-
-
18

180 -
200-
- 180
;‘-
18

180

-•

-
!
1’30
UT - Untreated control cells R - Replications
- Nitrofen treated cells N - Number of Individuals
T 2 - Propanhl treated cells A - Active
I — Inactive
D - Dead
DISCUSS I ON
Findings of this investigation indicate that the single dose application
of Nitrofen and Propanil can affect the density and diversity of cryptostigmatid
mites in a c addy ‘field. Experimental evidences further suggest that these
herbicides have a direct killing action at least on the two species under
consideration. Adverse effect of herbicides like Shell WL 19805, Paraquat,
2,4-0 and Simazine, on the soil inhabiLing cryptostigmatid mites has also
been shown by Edwards (1970), Edwards and Lofty (1975) and Prasse (1975).
Edwards (1970) showed that the Sehil WL 19805 had less adverse effect on the
cryptostigmatid mites when the plots were rotovated after spraying, than in
plots with the herbicide left on the soil surface. It is known in the
case of i4ltrofen, that it should not be incorporated in soil but placed as
a thin layer on the soil surface (Brian, 1976) and that the herbicidal
activity of this chemical s rapidly lost if incorporated with the soil
115
-------
(Iiukhopadhyay, 1972). Edwards a ,d Lofty (1975) while comparing tho density
of cryptostigmata in Paraquat treated, direct drilled plots with those in
ploughed ones, said that the forner has less impact on the number of soil
animaic. Similarly Prasse (1975: observed that the herbicide Simazinc
significantly decreased the number of the cryptostigmatid mite, Tectocepheus
velatus (Michael) in up to 10 cms of soil, while 24-D could not produce
any significant decline. It seems that both ploughing and herbicide
application done in the same plot can decrease the population of nontarget
orga iisms of soil.
COtICLLJS ION
I
It may be concluded that the herbicide Flitrofen had more adverse
effect on the cryptostiginatid mites compared to Propanil in field conditions.
Experimental evidences under laboratory conditions suggest that these weedicides
have a direct knock-down effect at least on cryptostigmatid mites like 0.
nodosa and S. albialatus .
LITERATURE C 1ED
Bhattacharya, T. and V. C. Joy. (in press). Chaiiges in the abundance of
sot! inhabiting Acari of.a paddy field in response to the application
of two herbicides. ‘roc. All India Symp. on Pesticide Residues in
the Environment. Bangalore. 1978.
Bhattacharya, T. , V. C. Joy and S. Joy. 1978. Studies on the effect of
temperature cm the development of Oppia noaosa Hanvner (Acari:
Cryptostigmata: Opplidas). Entomon 3(2): 149—155.
Brian, R. C. 1976. The history and classification of herbicides. Pages
1 - 54 in L. J. Audus (ed). Herbicides; Physiology, Biochemistry,
Ecology. Vol. 1. Academic Press, London. 608 pp.
Dindal, D, L. 1977. Influence of human activities on oribatid mite communities.
Pages 105 - 121 In D. L. Dindal (ed). Biology of Oribatid Mites. SUNY
Coil. Envlronm. Sd. Forestry, Syracuse, NY. 122 pp.
Edwards, C. A. 1970. Effect of herbicides on the soil fauna. Proc. 10th
Weed Control Conf.,’ 1052 - 1062.
Edwards, C. A. and J R. Lofty. 1975. The influence of cultivation on soil
animal populations. Pages 399 - 401 in Jan Vanek (ed). Progress
in Soil Zoology. Dr. W. Junk, B. V. Piibl. and Academia, the Hague
and Prague. 630 pp.
Eijsaekers, H. and J. van der Drift. 1976. Effects of the soil fauna. Pages
149 — 174 in L. J. Audus (ed). Herbicides; Physiology, Biochevinstry,
Ecology. V i. 2. AcademIc Press. London. 564 pp.
-------
Mukhopadhyay, S. K. 1972. Herbicidal action of the we killers available
in India. Pesticides, April 1972: 11 - 14.
Mukhopadhyay, S. K. and S. P. Bhattacharyay. 1967. Weed control In upland
rice by chemical and cul tural methods. Proc. mt. Symp. Plant
growth substances,: 503 —507.
Prasse, J. 1975. The effe:t of the herbi:ides 2,4-D and Simazin on the
coenosi of Collembola and Acari i u arable soil. Pages 469 - 480
in Jan Vanek (ed). Drogress in Soil Zoology. Dr. W. Junk, B..V.
Pubi. and Academia, the Hague and Prague. 630 pp.
Shannon. C. E. and W. Weaver. 1963. The mathematical theory of communication.
Univ. Illinois Press, Urbana, ill. 117 pp.
Snedacor, G. W. and W. G. Co:nran. 1947. Statistical Methods. 6th ed.
Oxford and IBH, Calcutta. 593 pp.
ACKNOWLEDGMENTS
The authors arc grateful to Prof. A. B. Das, Iead, Department of
Zc logy, Visva-Bharati for facilities. Thanks are also due to the CSIR,
lew Delhi for granting a research fellowship to VCJ.
117
-------
SESSION II: HUMAN WASTE DISPOSAL AND
SOIL ORGANISMS
Moderator: K. H. Domsch
Agricultural Research Center
Braunschweig. West Germany
119
-------
BIOLOGICAL SUCCESSION IN ARTIFICIAL SOIL MADE OF
SEWAGE SLUDGE AND CRUSHED BARK
Veikko Huhta, Veronica Surtdman, ‘Eeva Ikonen. ‘Seppo SiveLä,
wTuula Wartiovaara and Pekka Vilkamaa
tlniversily of jyodskyl
Univrrssly of Helsinki
F,n!and
The pre5ent paper summarizes the main results of a 3—year study
dealing with the biological processes that occur durinq the
humification of municipal sewage sludge, Witil particular reference
to the use of sludge as artificial soil in environmental building.
The types of sludge used for the experiments were 1) digested sludge
from a biological—chemical plant (activated sludge process with Fe 2 SO
precipitation), 2) activate sludge (=1 without digestion, but lime
and ferric chloride added), and 3) limed sludge from a chemical plant
(lime content ca. 50 % of dry matter). These were dried to ca 20 %
dry matter content and mixed I to 1 (vol) with crushed pine or spruce
bark. The test plots were established on a small parcel of Field
from which the topsoil had been r 9 moved. The materials were applied
in squares ca 25 cm deep end I I in in area.
The principal study objects were: I) uncomp sted digested sludge
and bark, 2) uncomposted activated sludge and bark, 3) uncomposted
limed sludge and bark, and I.) digested sludge and bark after 1 year’s
compost Ing. These were compared with 5) dIgested sludge alone, 6)
crushed bark alone, 7) compost made of digested sludge and bark, 8)
cultivated field soil, 9) garden grassland soil, and 10) forest soil.
The variables measured were: physical and chemical properties of
ttie test materials, contents c ’ heavy metals in soil and vegetation,
production of the vegetation, total numbers of bacteria, numbers of
Ciostridia, Streptomycetes, Protozoa, and glucose—fermenting bacteria,
length of fungal hyphae (Sundman & Sivel , 1978), numbers of specific
groups of microbes ;ndlcat;ng the nitrogen metabolism and hygienic
state of the materals, nitrification and dehydrogenase activity,
oxyge. consumption, cellulose degradation, numbers and biomasses of
groups and species of Invertebrates, total animal biomass and changes
in the animal communities.
In fresh mixtures of sludge and bark the microbial activity was
very Intens,. Numbers of clostrldk and glucose—fermenting bacteria,
indicating anaerobic processes, were highest soon after the establishment
of the experimental plots. Biological activity, measured as oxygen
consumption or cellulose degradation, was most intense during the
first growing period (Figure 1).
Numbers of denitrifying and nitrate-reducing bacteria remained high
in uncomposted materials thrc’ugtsout the study period. Nitrification
activity was low in the beginning but Increased in the second and third
years.
121
-------
FIGUPE I. Degredation of cellulose in 90—day periods
consumption of oxygen (bottom) In the different materials
Symbols used:
V . .VII..IX T ’
1975
(top) 1 and
tested.
digested sludge and bark,
activated sludge and bark,
L ‘ limed sludge and bark,
C — composted mixture of digested sludge and bark,
S — digested sludge alone,
B — bark alone,
T — tillage used as reference.
D = uncomposted mixture of
A— U II
‘V’ ‘VII.
1976
Ix’ ‘‘V’’ III’’ IX ’
I I 1977
C
S
0
‘I ,
In
0
4J
.
LA
L
B
I
1975 1976 1977
uv’J-
5O
5
4
3
2
1
0
- S
D=D *=B
P
T
T
I
122
-------
Flying insects (Coleoptera and Diptera), and phore ic nematodes
and mites (t4esostigmata, Prostigmata, Asti3mata) transported by them
colonized fresh mixtures of sludge and bark in a few days and reproduced
rapidly. These early groups became less numerous as the materials
aged. Collembola prop gated dense populations within a few weeks
and retained an importønt position through all stages, while Oribatei
were among the late colonists (Figure 2).
The animal community during the early stages of succession can be
described as typical for dung and related accumulations of easily
decomposable organic matter. This “dung community” changes relatively
rapidly into a less specialized “compost Community”, and gradually
further Into a community of generalist soil dwellers (Figure 3).
However, even in the oldest material tested, a composted mixture of
digested sludge and bark in the third year after application, the
animal community differed con5iderably from that of the adjacent rable
soil.
Of the fresh mixtures examined, that of activated sludge and bark
showed the highest biological activity and harbored the greatest
animal biomass. The mixture of digested sliadge showed the lowest
activity and biomass, and that of limed sludge took an intermediary
position (Figure 4). Enchytraeidae and Lumbricidae were almost absent
during the first year in the mixtures containing digested and limed
sludges, while Enchytraeldae were especially numerous in that with
activated sludge. Digested and limed sludges were obviously harmful
or toxic to these groups, a fact verified for earthworms by culture
experiments.
Compostng strongly promoted the biologicai processes in the
materials tested. After one year’s composting the mixture of digested
sludge and bark attained a degree of stability which was not
achieved by the uncomposted mixture even in the third growing season.
High nitrification activity characterized the compostad mixture in
comparison with the uricomposted ones.
In the mixtures of digested sludge and bark the processes
proceeded more rapidly than in either of the ccmporent materials
alone. Bark alone differed from the sludge ,naterials in its
biological properties: fungal hyphae were e3pecially abundant (Figure 5),
and the animal community contained some characteristic species, the
Enchytraeidaedominating In the faunal blomass.
In addition to the compost ing, freezing in winter was shown
to improve the hygienic state of the sludge—containing materials:
numbers of fecal coliforms, which remained high through the first
growing season, had dropped to practically zero by the next summer
(Figure 6). Fecal streptococci, on the other hand, were not affected
by low winter temperatures.
123
-------
G NI Nl
N
C
l Ni e
op — 0 —
rPC)
-. a c
a a — .
< F,’
— p. .,
a j
n —op
U,
a 0

D 0
..
-i Oj(a
OCD ‘a’ (N
1* - UI UI
a
a- —o
a
m
UI
000..4
a a..
mm
—‘rIfl
C,
—•. a
(Q 0 ,•r -‘
c u. a a
-‘ -im
CD 0 — —
a a.
0
—•m
N UI a.
Ort
CD r.
—
(N
— >3
< a-
a 0
C D- ,—
UI 0 1 01
a
ENCHYTRAEIDAE
-------
FIGURE 3. Changes in the
Coflernbola in an uncomposted
(relative abundances).
Hypogastrurl manubriatis
Piolsoloma mInute
Isotoma tigrina
O/o Lsp docyrtus sp
communities of Nematoda (top) and
mixture of digested sludge and bark
Isotoma viridis
Hypogastrura dsrtlculata
others
: 12 .5
Pelodeca ap
‘eiodera c i chitwoodi
Rhsbdiljdie pp
Diploscapter coronets
Aph Ienchoididae spp
Rhabditis o ycorca
Panagrolai rnus r,gjdsjs
Aphelenchoides bicaudatus
-------
umol 02 cm . h 1
25
DDO D
V.’ - 1 V11’ ‘IX’
FIGURE 4. Oxygen consumption (left) and average animal bloniasses
in uncomposted mixtures ef activated (A), limed (L) and digested (D)
sludge and bark in the first growing period (1975 for 0, 1977 for A
and L).
FIGURE 5. Lengths of fungal hyphae in different materials tested.
For methodical reasons the data for 1975 are not quantitatively
comparable with those for 1976 an 1977. Symbols as In Figure 1.
W i
‘I
A
2C
1C
LUMBR CIDAE
ENCKYTRAEIDAE
MACROARTHROPOD*
M,CR0ARTHI OPOOA
NEMATODA
A L D
1976
126
-------
FIGURE 6. Total numbers of feca coliforms In different materals
tested. Symbols as in Figure 1. (The survey of A and L was started
In 1977).
127
3
0
sc
‘ S I
I-
E
C
C I
0
-------
The Mesostigmata showed good ability to differentiate between
the different substrates: the initial conmiunities in the thr,e kinds
of sludge were almost totally different, and even the oldest material
tested shared no cormon dominants with the adjacent arabic soil. The
Coliembola proved to be least specialized: the communities of the
different fresh materials were almost identical, and those of aged
mixtures showed the greatest similar:ty to the control community.
Succession was observed not only in he ordinary test plots, but
also In the reference plot established on arable soil. After
remaining untreated for the survey period, it showed increasing
biological activity and animal biomass from year to year (Figures 1
and 2).
The zoological part of the investigation will soon be published
In greater detai (Huhta, Ikonen & Vilkamaa, in press). The micro-
biological part is in preparation. A report of the whole project
has already appeared in Finnish (Huhta et at. , 1978).
LITERATURE CITED
Hubta, V., Sundman, V., Ikonen, E., Slvel , S., Wartiovaara, T. &
‘ilkamaa, P. 1978. J teliete—kuorirouheseosten maatumisen biologia.
- Jyväskyl n yliopiston biologlan laiLoksen 1.iedonar .toja 11:1—124.
Huhta, V., Ikonen, E. & Vilkamaa, P. (in press). Succession of
Invertebrate populations In artificial soil made of sewage sludge
and crushed bark. — Acta Zool. Fennica.
Sundman, V. & Sivel , S. 1978. A comment on the membrane filter
technique for estimation of length of fungal hyphae in soil. — Soil
Bio . Biochem. 10:399-401.
QUESTIONS and COMMENTS
.B. QMSCH : Are there any significant correlations
between the plant production on those different plots and
soil biological parameters tested’
V. HUHTA : We tried to find out correlations between
different factors with the aid of factor analysis and canonical
correlation analysis, but the result was poor because the
materials tested differed from each other in many respects,
several factors being highly intercorrela’ced.
H. EIJSACKERS : Have you any explanation for the toxicity
of digested and treated sludges on Lumbricidae and Ency-
traeidae, perhaps from heavy metals?
!. HUHTA : We made some preliminary tests on the pOsBible
effe&t of heavy metal content, oxygen deficiency and the Fe 2 SO 4
used for precipitation, but we could not find any single factor
responsible for the toxicity.
128
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DECOMPOSITION PROCESSES IN SEWAGE SLUDGE AND
SLUDGE AMENDED SOILS
M. J. Mitchell and S. C. Homer
SUNY CESF
USA
An understanding of decomposition processes in both natural and
anthropogenic systems is necessary for maximizing productivity and
minimizing deleterious environmental impacts. An important category
of anthropogenic systems is associated with the treatment of waste-
water. These facilities are used for the maintenance of water quality
and also demonstrate the importance of decomposition both within the
systems themselves and by their interactions with surrounding axJas,
including urban and agricultural comswiities.
The two major outputs of a given wastewater treatment facility are
the treated effluent and the residual solid, defined as sludge. ,The
characteristics of the effluent and especiall:’ the sludge vary greatly
since the sewages themselves and the treatment processes differ both among
and within these facilities (Mitchell et al, 1978; Somoers, Nelson and
Yost, 1976). Important variables Include the concentration of various
human pathogens, heavy metals, organic constituents and inorganic nutri-
ents. Although the major objective of wastewater treatment is the re-
moval or elimination of these components from the effluent, the effi-
ciei y of this process depends on the design of each treatment facility
which may utilize some combination of primary (physical settling of
solids), secondary (decreasing organic constituents by biclogical proces-
ses) and tertiary (removing dissolved inorganic and organic substances)
treatment (Eckenfelder and O’Connor, 1961). 1.5 treatment facilities
have become more effective in this removal process, there has been a
concomitant increase in the residual sludge which now amounts annually
to about six to seven million dry metric tans in the United States
(Harrington, 1978). The decomposition and resultant stabilization of
this material are major factors which affect its management.
During secondary treatment, both activated sludge and trickling
filters are used to stabilize and reduce the organic constituents of
sewage. The actual function of these systems has been detailed else-
where (Curds and Hawkes, 1975; Hawkes, 1963; Mitchell, 1978). In addi-
tion, the sludge, which is produced from this secondary as well as from
primary and tertiary treatment, needs further processing which may in-
clude dewatering, aerobic and anaerobic digestion and disinfection.
Ultimately this sludge must be managed by either disposal or further
utilization. If the sludge is incinerated or dumped in the ocean, air
or water pollution may occur and thus the latter disposal practice is
being discontinued (Bastian, 1977).
In contrast, the deposition of this sludge on land has a variety
of potential benefits including its use as a soil conditioner and ferti-
lizer due to its organic constituents ..nd elevated levels of inorganic
129
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nutrients including nitrogen and phosphorus. However, as mentioned pre-
viously, sludges may contain heavy metals, such as cadmium, and human
pathogens which can endanger public health if they contaminate water
supplies or enter the food chain (CAST, 1976; Loehr, 1977; Love,
Tompkins and Galke, 1975). To maximize the utilization of sludge as a
soil amendment, its decomposition processes must be delineated since
they partly determine organic matter stabilization, heavy metal availa-
bility, pathogen inactivation, minera1i. ation and even odor production.
Some of the major factors which will affect the decomposition and stabi-
lization of sludge are availability of an organic energy source, con-
centration of electron acceptors, moist’ire, temperature, inorganic
nutrients, pollutants, and various biotic components. The importance of
each of these factors ‘dli be d1cussed with regard to wastewater treat-
ment, in general, but eitphasizing decomposition of sludge and sludge
amended soils.
Organic energy source availability
Wastewater solids have a high proportion of labile organic consti-
tuents which are removed in varying amounts during the treatment process.
!f the resultant sludge is digested anaerobically, the organic mattur of
the raw sludge, which ranges from 60 to 80%, is reduced to between 40 and
60% (Bolton and Klein 1 1971; Eckenfelder and O’Connor, 1961; Hawkes ,
1963). The production of methane by anaerobic metabolism depends on the
availability of labile organic fractions such as acetate, the amount of
which decreases as stabilization progresses (Mah et al. 1977). The
methane produced by this process may be 5ubsequently used as a fuel.
For aerobically digested sludges, the organic matter reducticn is
less and after digestion it may still constitute 62-75% of the solid
residuals. The major portion of this organic matter is probably de-
rived from microbial products (Daigger and Grady, 1977).
Another mode, which has been recently employed for furthering
sludge stabilization, is composting in which the organic matter of raw
sludge can be reduced about one-third under thermic and aerobic condi-
tions (Epstein and Willson, 1975). As in all couiposting processes the
rate of decomposition decreases rapidly as the organic matter stabilizes
and humification occurs (Gray and Biddlestone, 1974).
If drying beds are used for sludge dewatering, the decomposition
and humification cont .nues within these systems. Regardless of whetnex
the sludge is derived from anaerobic or aerobic digestion, both anacro .
bic and aerobic decomposition occur. Anaerobic decomposition, as indexed
by methane production, predominated in the early drying phase of an acti-
vated sludge due to abundant labile organic fractions and low oxygen.
With a residence time of two weeks in these drying beds, an additional 2%
reduction of the org inic matter occurred during the sumner at tempera-
tures ranging from 11 to 28C Mitche1l, Hornor and Abrams, in review).
When sludge is applied to soil the decomposition rate is also de-
pendent on the degree of stabilizaticn. For example, an aerobically
digested sludge lost 48% organic matter in contrast to three anaero-
bically digested sludges, which lost from 28 to 36% organic matter over
130
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• _... ....__.—cyrrwS’ . . — - — —— —_ —_ fl —
-- -
168 days when added to a mineral soil in a glasshouse (Mitchell et al.,
1978). In microcosms and a sludge amended agricultural soil, organic
matter losses of anaerobically digested sludges were 20% over S months
(Miller, 1974) and 60% over 7 years (Hinesly et al., 1977), respectively.
Since sludge decomposition and stabilization are biologically
mediated, the rate of those processes is an index of the activity of
various organisms. The importance of these orga’ isms in aerobic and
anaerobic digestors has been reviewed previously (Curds and Hawkes,
1975; Mitchell, 1978). With increasing sludge stabilization there is
a parallel decrease in total viable bacteria (Miller, 1974; Mitchell
et al., 1978). Similarly, in sludge drying beds and sludge amended
soils there is a fauna! succession which is probably due to changes in
food resources as well as in the physical and chemical environment.
Major endemic faunal components associated with this succession include
nematodes, enchytraeids and arthropods (Huhta , Ikonen and vilkpm , 1977;
Mitchell et al., 1978, in review). Furthermore, the addition of
oligochaetes, such as Eisenia foetida (Say.), into sewage sludge will
hasten sludge decomposition and their activity depends on both the age
and type of sludge (Mitchell et al., 1977, 1978, in review; Mitchell,
1979).
Electron acceptor availability
There is a general trend during sludge stabilization from an ex-
cess of electron donors to an excess of electron acceptors. One of the
major objectives in the activated sludge process and aezobic digestion
is the maximization of the concentration of oxygen which serves as the
terminal electron acceptor in aerobic respiration (Eckenfelder and
0’ Connor, 1961). In contrast, anaerobic digestion uses the products
of fermentation, organic acids and carbon dioxide, as electron acceptors
and converts them into methane and carbon dioxide (Crowther and Harkness,
1975). Therefore, the rate of methancigenesis is limited by the availa-
bility of precursors such as acetate (Mah et al., 1977).
Within sludge drying beds the availability of electron acceptors
is a major factor in determining the rate of decomposition and whether
aerobic or anaerobic decomposition will predominate. The rate of oxygen
diffusion into sludge is highly dependent upon its moisture content as
will be di5cusscd below. It has also been shown that the addition of
an alternate electron acceptor such as nitrate stimulates carbon dioxide
evolution (Mitchell, Hornor and Abrams, 1980). Similarly, for composted
sludge, it is generally necessary to use forced aeration to msintain a
surplus of oxygen necessary for this aerobic process (Epstein and Wilison,
1975).
When sludge is added to soil, it serves as a rich source of
electron donors and thus may deplete oxygen and alternate electron
acceptors and cause a depression of Eh and an increase in anaerobic
microbial metabolites. For example, Taylor et al. (1978) found that
131
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raw sludge produced a m’ch larger proportion of methane in the soil
atmosphere than anaerobically digested sludge which would have less
electron donors due to its increased stabilization. A general conse-
quence of a depressed Eh a d anaerobic conditions is the reduction of
decomposition due to the lower metabolic efficiency of anaerobiosis.
In addition, some of the reduced compounds may be toxic tc microflora,
invertebrates and higher plants and there may be a depression of carbon
flux and mineralization, although certain nutrients such as phosphate
may become more available (Buckinan and Brady. 1969; Patrick and
Delaune, 1977; Skinner, 1975). Among these reduced compounds various
malodorous sulfu. ’ gases may also be produced which may restrict the
application of sludge to land (Hornor, Waugh and Mitchell,this volume). In
addition, the Sb will affect the avai abi1ity of certain heavy metals
such as cadmium (Binghaun at al., lSI76). It should be emphasi ced that
the consequences associated with anaerobic microbial metabolism are not
exhibited if the sludge is stabilized and proper application rates and
soil conditions are maintained.
Oxygen availability will also affect the functional role of the
faunal components. Nematodes, which are abundant in sludge drying beds,
can survive anoxic conditions and be active at a p02 of 7000 dyne cnr 2
(Abrams and Mitchell, 1978). In contrast earthworm respiration is de-
pressed at a p 02 of 53200 dyne cur 2 (Johnson, 1942). This effect was
shown indirectly in a sludge drying bed wh ure the presence of earth-
worms d d not affect the rate of decomposition until aerobic catabolism
predominated. In addition, a depression of Eh was associated with high
mortality of earthworms which ba’ been eviously introduced into the
sewage sludge (Mitchell et al . , in review). In general, the role of
various faunal components during sludge decomposition nay be linked to
their oxygen needs and Eh tolerance.
Moisture
During the treatment of wastewater itself, the amount of water
present does not affect the decomposition process except as a determi-
nate of the concentration of the various inorganic and organic con-
stituents. However, in drying beds the moisture content has major
importance. Because of the low solubility of oxygen in water, a sludge
or a sludge amended soil with a high moisture content and elevated meta-
bolic rate will be rapidly depleted of oxygen, the results of which
were discussed previously with regard to electron acceptors.
With increased drying, oxygen availability increases, but there
is a concomitant decrease in metabolic activity. Within certain thresh-
olds, moisture content is directly proportional to decomposition rate.
Similarly, as has also been documented for soils, when sludge has been
rewetted, the metabolic activity is enhanced (Mitchell, 1979; Mitchell
et al. in review). The importance of moisture in affecting the de-
composition of sludge amended soils has been shown indirectly in a
glasshouse study Lu which organic matter loss was greater, due to a
higher nolature regimes than under natural L.2A covdjt1 ua (J!jnaa ly
et aL 1977; Mitchell at al., 1978).
132
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The general importance of moisture for maintaining the activity
of both the microflora and the fauna has been well documented for soils
and it can be assumed that similar relationships would be found in
sludge amended soils.
in all decomposition processes, the effect of temperature is
marked. enerally, the rate of metabolism increases with toinperature
within upper and lower limits which are dependent upon the constituent
an as’ temperature tolerances. Within anaerobic sludge digesters
30 to 35°C is considered as the optimal range for both organic matter
stabilization and methane production (lahoff, ! Iller and Thistlethwayte,
1971). Temperatures of activated sludge and trickling iiters are close
to ambient although they may be somewhat lower in simmer and higher in
winter and their activity is thus closely coupled with ambient condi-
tions. Seasonal changes in their characteristics may be partly d!.le to
these temperature fluctuations (Curd5 and Ham tes, 1975). In composted
sludge, the temperature ranges from ambient to 80°C (Epstein and
Wilison, 1975).
Oxygen consumption of activated sludge taken from a drying bed
exhibited an exponential relationship to temperature and a Qio of 2.94
over a 5 to 30°C range. This value is within the range found for soils
and aquatic sediments (Mitchell, 1979). Temperature not only directly
affects microbial end faunal metabolism, but also affects population
growth and Interspecific interactions between the fauna and their
microbial food resources (Abrams and Mitchell, this volume; Mitchell,
1979).
Although the effect of temperature on decomposition in sludge
amended soils has not been studied in detail, it is widely recognized
that low temperatures, especially below freezing, may limit the applica-
tion of sludge in winter. Furthermore, the general effect of tempera-
ture on decomposition of sludge amended soils has been demonstrated by
Miller (l974 using microcosms in which the temperature regime was
directly related to decomposition rate.
Other nutrients and pollutants
Because there is a high concentration of inorganic nutrients,
such as nitrogen and pho piwru.c, these constituents do not generally
limit sludge decomposition and their presence is one of the major benefi-
cial attributes of sludge as a soil amendment. Moreover, the minerali-
zation rates of these nutrients will affect heir availability to higher
plants and determine in part the potential for ground water contamina-
tion (Koterba, Hornbeck and Pierce, 1979; Riekerk, 1978). However,
both organic (e.g.. phenols) and inorganic (e.g., heavy metals) con-
stituents, depending on their concentration may interfere with sludge
decomposition and stabilization by their deleterious impact on the
biota (Hayes and Theis, 1978; CASTJ 1976; lahoff et al., 1971). Such
pollutants, along with pathogans, if present in sludge, may limit its
I”
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utilization a , a soil amendment because of potential toxic effects to
both. plants and animals, including man (Burge and Marsh, 1978; CAST,
1976; Harrlr.gton, 1978; Williams, Shenk and Baker, 1978).
Biota
The overall role of the microflora and invertebrate fauna in
wastewater treatment is well documented (Curds and Hawkes, 1975; Hawkes,
- 1963) and recent studies have established basic information on their
roles in sludge and sludge amended soils (Huhta et al, 1977; Mcllveen
and Cole, 1977; Mitchell, 1978, 1979; Mitchell et al 1978, 1980, in
review; Varanka, Zablocki and liinesly, 19Th). The importance of the
biota in wastewater and sludge has been alluded to in previcus sections,
The biota should be considered as a series of functional units
which maximize nutrient and carbon flux. An excellent example of
the interactions between these units is exhibited by the synergistic re-
litionships between protozoa and :heir bacterial food sources in acti-
vated sludge where protozoa feedi g stimulates the metabolic activity of
the bacterial populations. The iriportance of similar interactions in
sludge drying beds and sludge aneuded soils has been demonstrated for
endemic nematodes and bacteria (Mitchell et al. 1980; Abram and
Mitchell, this volume) as well as introduced macroinvertebrates such
as Sisenia foetida (Brown, Swift and Mitchell, 1978; Mitchell, 1978,
1979; Mitchell et al,, 1978, 1980, in review) 1 The importance of
these interspecific interactions has also been shown by the introduction
of an ectomycorrhizal fungus into sludge amended soil which resulted in
accelerated tree growth (Berry and Marx, 1976).
Decomposition and maximizing sludge utilization
Both wastewater treatment and sludge management rely on maximizing
beneficial f nctiona1 relationships among the biota and their chemical
and physical environment. It must be clearly recognized that these re-
lationships are major factors in determining the efficiei’cy of the
treatment process and the subsequent utilization of sludge as a soil
amendment. By minimizing those components such as heavy metals a . d
undesirable processes such as the production of toxic compounds, the
utilization of wastewater treatment and sludge management as a mechanism
for soil reclamation and nutrient conservati n may be fully realized.
LITERATURE CITED
Abrams, B.I. and N.J. Mitchell. 1978, Role of oxygen in affecting
survival and activity of Pelodera punctata (Rbabditidae) from
sewage sludge. Neinatologica 24i456-462.
Abrans, B. I. and N.J. Mitchell • This volume, Interactions between
neniatodes and bacteria in heterotrophic systems with emphasis
on sewage sludge and sludge amended soils.
134.
-------
Bastian, R . K, 1977, Municipal sludge management: EPA construction
grants program. Pages 673-689, in R,C. Loehr (ed.). Land as
a waste management alternative. Arbor Science, Ann Arbor,
Mich.
Berry, CR. anci Dli. Marx. 1976. Sewage sludge and Pisolitnus
tincterius ectomycox’rhizae: their effect on growth of pine
seedlings. Forest Science 22:351-358.
Binghain, F.T., A.L. Page, R.J. Mahler and T.J. Ganje. 1976. Cadmium
availability to rice in sludge-amended soil undcr “flood” and
“non-flood” culture. Soil Science Soc. Amer. 3. 40:715-719.
Bolton, R.L. and L. Klein. 1971. Sewage treatment, basic principles
and trends. Ann Arbor Science, Ann Arbor, Nich. 256 p.
Brown, B,A., B.L. Swift, and M.J. Mitchell. 1978. Effect of Oniscus
asellus feeding on bacterial and nenatode populations oT e
sludge. Oikos 30:90-94.
Buckman, 11.0. and NC. Bra y. 1969. The nature and properties of
soils. Macmillan Co., New York. 453 p.
Burge, W.D. and P.B. Marsh. 1978. Infectious disease hazards of land
spreading sewage wastes. 3.. Environ. Qual. 7:1-9.
Council for Agricultural Science and Technology. 1976. Application of
sewage sludge to cropland: appraisal of potential hazards of
the heavy metals to plants and animals. CAST Rep. No. 64, Ames,
Iowa. 63 p.
Crouther, R.F. and N. Harkness. 1975. Anaerobic bacteria. Pages 65-91.
inC.R. Curds and H.A. Hawkes (ed.). Ecological aspects of
used-water treatment. Academic Press, New York.
Curds, C.R. and H.A. Hawkes (ed.). l97 . Ecological aspects of used-
water treatment. Academic Press, New York. 414 p.
Daigger, G.T. and C.P.L. Grady, Jr. 1977. A model for the biooxidation
process based on product formation concepts. Water Research
11:1049-1057.
Eckenfelder, W.W. cind P.3. O’Connor. 1961. Biological waste treatment.
Pergamon Press, Oxford, 298 p.
Epstein, E. and G.B. Willson. 1975. Composting Raw Sludge. Pages
245-248 in Proceedings of the 1975 NationaL Conference on
Municipal Sludge ManagemeIit and Disposal, USS.E.P.A., Information
Transfer, Inc. Rockville, Maryland.
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F
Gray, KR. and A.J. Biddlestone, 1974. D composition of urban waste.
Pages 743-775, in C.H. Dickinson and G.J.P. Pugh. Biology of
plant litter decomposition. Vol. 2, Academic Press, London.
Harrington, Ltd. 1978. Hazardous solid waste from domestic wastewater
treatment plants. Environ. Health Persp. 27:321-237.
Hawkes, H.A. 1963. The ecolog) of waste water treatment. Perganion
Press, Oxford. 203 p.
Hayes, T.D. and T.L. Theis. 1978. The distribution of heavy metals in
anaerobic digestion. J. Water Pollut. Control Fed. 50:61-72.
Minesly, T.D., R.L. Jones, E.L. Zeigler and J.J. ‘ler. 1977. Effects
of annual and accumulative a np1ications of sewage sludge on the
assimilation of zinc and cadmium by corn (Zea mays L.). Environ.
Sci. Technol. 11:182-188.
Hornor, S.G., J’.H. Waugh and M.J. Mitchell. This volume. Sulfur trans-
formations in oxygen limited systems: soils, sediments and sludges.
Huhta, V., E. Ikonen and P. Vilkamaa, 1977. Animal succession in arti-
ficial soil made of sewage sludge and crushed bark, Pages
573-577, in U. Lohmn and T. Persson (eds.), Soil organisms as
components of ecosystems. Proc. 6th Tnt. Coil. Soil Zool., Ecol.
Bull, CStockholm) 25.
Imhoff, K., U. MUller and D.K.B. Thistlethwayte. 1971. Disposal of
sewage and other water-borne wastes. Ann Arbor Science Publ.
In., Ann Arbor, Mich. 405 p.
Koterba, t’LT., J.W. Hornbeck and P.. . Pierce, 1979. Effects of sludge
applications on soil water sulutions and vegetation in a northern
hardwood stand. J. Environ. Quality 8:72-78.
Johnson, M.L. 1942. The respiratory function of the haemoglobin of
the earthworm. J. Exp. Biol. 18:266-277.
Loehr, R.E. (ad.), 1977. Land as a waste management alternative, Ann
Arbor Science, Ann Arbor, Mich. 811 p.
Love, G.J., E. Tompkins and W.A. Gaike, 1975. Potential health impacts
of sludge disposal on the land. Pages 204-213. in Proceedings
of the 1975 Municipal Sludge Management and Disposal, U.S,E. P.A.,
Information Transfer, Inc., Rockville, Maryland.
Nab, R.A., D.M. Ward, I .. Baresi and T.L. Glass. 1977. Biogenesis of
methane. Ann. Rev. Microbiol. 31:309-341.
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Mcllveen, W.D. and H. Cole, 1977, Influence of sewage sludge soil
amendment on various biological components of the corn field
ecosystem. Agriculture and Environment 3:349-361.
Miller, R.H. 1974. Factors affecting the decomposition of an
anaerobically digested sewage sludge in soil. J. Environ.
Qual. 3: 376—380.
Mitchell, M.J. 1978, Role of invertebrates and microorganisms in
sh..dge decompcsition. Pages 35-50 in R. Hartenstein (ed.)
Conference proceedings on utilizatio f soil organisms in
sludge manogement. SUNY, CESP, Syracuse, ?ew York.
Mitchell, N.J. 1979. Functional relationships of ma roinvertebrates
in heterotrophic systems with emphasis on sewage sludge
decomposition. Ecology, in press.
Mitchell, N.J., R. Hartenstein, B.L. Swift, E.F. Neuhauser, B.I.
Abrams R.M. Mulligan, B.A. Brown, D. Craig and D. Kaplan.
1978 • Effects of different sewage sludgez on some chemical
and biological characteristics of soil • .7. Environ. Qual.
7: 551—559.
Mitchell, M.J., S.G, Hornor and b.I. Abrams. 1980. Utilization of
microcosins in studying decomposition processes in sewage sludge,
in press. LnJ.P. Geisy (ed.). Microcosins in ecological re-
search,
Mitchell, M.J., S.G. Mornor and 3, 1. Abrains. In rev. Decomposition
and gas flux rates in heterotrophic sewage sludge drying beds
and the effect of the earthworm, Eisenia foetida (Oligochaeta) .
J. Environ. Qual.
Mitchell, M.J., R.M. Mulligan, R. Hartens’cin un l EP. Neuhauser.
1977. Conversion of sludges into “topsoils” by earthworms.
Coinp. Sci. 18(4):28-32.
Patrick. W.H. and R.D. Delaune. 1977. Chemical and biological redo.
syJtems affecting nutrient availability in the coastal wetlands,
Geoscience and Man. 18:131-137.
Riekerk, H. 1978. The behavior of nutrient elements added to a forest
soil with sewage sludge. Soil Sci. Suc. urn. J. 42:810 - 1316.
Skinner, F.H. 1975. Anaerobic bacZ.eria and their activities in soil.
Pages 1-1.9. in N, Walker (ed.). Soil Microbiology. Haisted
Press, New Yo E.
Sounners, L.E., D.W. Nelsoi aid K.J. Yost. 1976. Variable nature of
chemical composition 9 sewage sludges. 3. Environ, Qual. 5;
303-306.
13?
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Taylor, J.M,, E, Epstein, W.D . Bu ge, 1t,L , Chaney, J.D, ?denzies and
L.J, Sikora, 1978. Che itica1 and biological phenomena observed
with sewage sludges ii simulated soil trenches. J. Environ.
Qual. 7:477-482.
Varanka, M.W.,, Z.M. Z b1ocki and T.D. Hinesly. 1976. The effect of
digested sl’ dge on soil biological activity. J. Water Pcllut.
Control Fed. 48:1728-1740,
Williams. ?.H. 3.5. Shenk and D,E. Baker. 1978, Cadmium accumulation
by meadow voles ( Microtus pennaylvanicus ) from crops grown on
sludge-treated soil. J. Environ. Qual. 7:450-454, -
QUESTIONS and COMMENTS
FAIZY : How do you explain the positively
linear relationship between 02 consvntption and moisture content
in sludge? I believe that the increase in moisture (100 to
300%) might eventually lead to anaerobic conditions.
M.J. MITCI LL : Sludge has much higher moisture holding
capacity than mineral soils. We have found that aerobic
catabolism may predominate even when sluda’3 is 300% moisture
on a dry weight ba8is. Under conditions of high oxygen de—
inand and low oxygen diffusion anaerobic conditions are pro-
duced.
138
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SOIL MICROFAUNA OF OPEN DRAINS IN MID-DELTA EGYPT
Mohsen Shoukiy Tadros
Tanta University
Egypt
INTRODUCTION
In Egypt during the last ten years, a project was
established to replace the normal open drainage system to
tiles, in the whole valley. To execute this project,
machinery had to deepen the ordinarily used drains and
dredge the accumulated residues from the bottom of the
drains, placing it on one or both sides of the ditches
making a huge mound of wet soil. This process had been
done previously, but on a limited scale during a specific
period of winter time.
This soil—like residue is used in brick factories, or
for filling in around house foundations. It is also used
on a large scale as an organic fertilizer following its use
as an animal bedding material.
Organic fertilizers usually do not contain poisons in
toxic concentrations. Gases and heat released during their
decomposition may be translated into behavioral responses
among soil fauna. In addition, these organic fertilizers
provide additional habitat space and food which supports
micro- and mesofaunal organisms. High percentages of the
total soluble salts associated with them may be harmful
to plants.
Many investigators dLscussed the relation between ferti-
lizer and soil, Allison (1966), Foster (1968), Behan (1972)
and Bebrend (1973). Others reviewed forest fertilization
or the role of soil organisms in organic matter decomposition
(Baule et al. 1970, Bengeton 1971, Weetman 1973, and Mitchell
1978.
In Egypt, Hafez (1939) who described the insect fauna
of the dung. Later on El-Xii.l (1957, 1958) investigated some
ecological factors responsible for faunal fluctuations.
139
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Tadros (1965, 1976, 1978) discussed the vertical and hori-.
zontal distribution of oribatids and more ecological factors
responsible for fauna populations.
This paper briefly reviews tue following objectives:
a) to determire the most prevalent fauna species of dredged
mud from the bottom of the drains through a 12 months
period.
b) to find if there is any difference in faunal distribution
in the accumulated drain residues, compared to the native
fauna in the same district.
c) to find if the prepared organic fertilizer is harmful
to animals, when using it as bedding in their sheds,
or harmful for plantations in fields.
METHODS AND MATERIALS
Location of the Study
Two villages near the Faculty of Agriculture were chosen
for this experiment. They were about 8 km (5 mi) andil km
(7 mi) from the city of Kafr E1-Sheikh. An ordinary open
drain was running beside these two villages. Its upper
margin was about 3 in; its bottom was 1 in wide, while its
depth was about 2 m. From the muddy hill, established from
the machinery deepening process in that drain, a 16 km
(10 mi) plot war. cho5en. This hill was about 2 in high. At
the beginning of investigation, the site was ne r1y all
composed of wat muddy soil. From the third month onward
it was drier and some weeds grew scattered n it.
This characteristic soil, is known to be heavy, black
and becomes full of cracks when dry. comprising big masses
of soil. The percentage of total soluble salts is also
reasonable in that sort of soil.
Techniques
It was arranged to take samples at three levels (top.
middle aLd bottom) from the previously mounded soil residues
cast from deepen i.ng the drain. Samples were taken every two
weeks until the third month, then monthly until the end of
investigation. At every amp1ing date 30 cylinders were
collected. 10 from each examined level representing 10
1 .o
-------
_I
replicates from each. Some soil samples were also tested
to find some essential soil properties. More samples were
also taken from the prepared organic fertilizer. The
sampling arid extraction precedures were just the same
described by Tadros et al. (1965).
Extracted Fauna
RESULTS AND DISCUSSION
The extracted fauna was found to fall under two cate-
gories, Insecta and Acarina. The first group representec
individuals from the orders, Collembola, Thysanura. Hymeno—
ptera, Homoptera and Coleoptera, but owing to the fact that
springtails comprised the majority of insects they were
considered as separate sub—groups. Acarina comprised moss
mites and soft bodied mites.
Total Fauna Encountered
At the beginning of experiment, no fauna existed in
mud, but from 2 wke until 12 mos the extracted fauna in-
creased (Figure 1).
15
Is
14
Ii
10
2
S
0
6
4
0
1
0
1 2 3 4 ’S 6 7 5
H 0 N T H
FIg.(1): Ptaans of total fauna
1 l
9 10
S
-------
It is clear that a peak occurred in the third month, with two
other lesser peaks occurring after ]½ and B iso. These re-
sults may be due to high water content and to anaerobic
circumstances in the first samples, but when the soil began
to dry, organisms began to creep into it. The last peak
occdrring in the eighth month may be due to the scattered
growing weeds at that time that gave a suitable atmosphere
in which some fauna could flourish. On the otF r hand, the
low percentage of other Eciunal forms during that period may
be due to the low relative humidity in soil due to its
dryness after that long period.
Vertical E.’istribution of Fauna
It was found that most of the fauna (40.9%) were in
the lower level while in the middle, 31.8% of the fauna,
and in the upper level, the minority of 27.3%. These re-
suits may be due to the drying by the sun and wind evaporation
cf water occurring more rap d1y in upper regions. Also,
individuals immigrate to lower regions in demand for moisture.
Faunal Groups
Springtails were found in enormous numbers in the soil.
They are the base of soil animal food chain (William 1942).
They can occur in all types of soil and under various vege-
tative cover. This group is abundant in all moist and
fairly moist soils to unknown depths (Jacot 1940).
In this investigation, the springtails comprised (25.42%)
of the whole fauna, while all other insect orders (32.20%).
Acarina was a prevalent order in this type of soil (42.37%).
Comparing the percentage of coLlembolans to insects, the
former comprised 44.12% of the insects. This result supports
the prior findings of Williams and Jacot.
Faunal Groups, Vertical Levels and Months
It was clear (Table 1) that only slight differences
occurred in the 3 vertical levels tested. Insecta and
Acarina tended to flourish in the middle and lower regions
of soil cast residue mound during all times of the experiment
(Table 2). These results may be attributed to the moisture
in these two regions. It was clear from the same table that
springtails were affected by both microclimatic and soil
factors. This result appeared in the fluctuation of its
numbers over time and in the different vertical strata.
lie2
-------
Table 1: PERCENTAGES OF ‘IdREE MAIN FAUNA GROUPS AT 3
VERTICAL LEVELS EXTRACTED FROM MUD DREDGED
FROM A DRAIN
GROUPS
UPPER
MIDDLE
LOWER
MEAN -
OLLEMBO
LA
25.92
24.87
25.92
25.57
flISECTA
29.62
36.5.1.
27.16
..
‘l.O9
ACARINA
45.06
39.15
46.91
43.70
The a ithor attributes this result to the sensitivity of
this group to many ecological factors.
Prepared Organic Fertilizer
Data in (Tables 3 & 4) indicates that total soluble
salts (TSS) soil residues from the drain was 3.75 nun hos/cm,
or rather, nearly a salty soil. It is also known, that
Kafre El—Sheikh soils are somewhat alkaline, so a decrease
of TSS occurred when preparing the organic manure, because
of the acidity of urine and faeces of animals when using it
for bedaing. The percentage of both Collembola and Insecta
was low in this manure when compared with that from cast
drain soil; this result indicates that such acidity is not
preferred by Insecta. On the other hand, Acarina flourished
in manure and nearly doubled giving an impression that that
environment was pr2ferable to them.
Considering the numbers of microflora obtained (Table 4),
it was obvious that Bacteria, Fungi and Actinomycete counts
increased in the cast drain residues when compared with
ordinary cultivated soil. This is due to the change in soil
acidity, but this increase was only for a short time for
a decrease was observed when preparing the organic fertilizer.
The high percentage of organic matter comprising the manure
may be also considered, The increase of nticroflora was
fo .lowed by an increase of microfauna that depends upon
microflora. This result was obvious from the table, for
fauna became nearly five times greater when compared with
that occurring in cast c’rain soil.
It, therefore, is not suitable to use this prepared
organic matter as an organic fertilizer, for it appeared
143
-------
Tabls 2s ERTMCTED PMIAL 0 vPB P uI E SOUI STEATA OVER M l MlRUAL PERIOD (no. In asaii.)
—
0
Lnnocta
carina
—
0,4
0.2
0
i:t
L.O
—
0.8
1.4
o.ij 0.0
i.oj
0,3
0.1
0.6
0.1
0.3
1.1
0. 5
1.2
0.7
1.:
13.
0.2
1.4
0.1
C1 .4
0.1
0.3
0.0
0.3
0,2
0.0
0.1
•7.6
11.6
0.5
0.7
4


aaoup
CoIlsabolo
—


ith
0
—


—
04
—
PERIOD IN I OUT II3
0.1
0.5
i
I
1.61 13
0.2
0.1
—
0.4
0.7
—
1.2
0.0
rr r —ir rir
0.0
—
0.0
0.0
0.0
0.3
6.7 0.4
ot. Fauna
-
o
0.9
1.5
2,7
2,7 4,9
0.6
0.8
1.8
2.4
3.3.
1.3
13
03
03
0.5
0.4
25.°
1..
•
Icc4letnboln
aecta
o &c jna
.r
lot, 10Ufl2
—
—

—
0.4
—
.6
0,5
—
1.2
0.0
—
1.2
0.0
—
0.0
0.7
—
0.2
—
0,5
0.0
—
0.0
(,.0
—
0.0
_
0.1
—
7.4
0.5
o
0.4
0.3
24
0.8
0 . 8
0,7.
1.1
0.0
0.4
0.2
0.0
0.1
0.2
0.4
11.0
0.7
o 0.9 5,3
3.8
1.7
2,5
2.0
1.2
1.5
1.0
0.9 1,5
2.9
1,0
0 ,7
0.9 1,6 30.2
1.9
o11or bo1a
—
0
—
0.0
—
0.0
0.5
—
1.7
—
0.3
—
4.9
1.4
—
0.7
0.0
0.0
—
0.4
—
0.0
—
0.0
—
0.0
—
0.0
—
0.2
—
10.1
—
0.6
liwecta
3
0.0
0,5
0,0
0.5
0.5
1.8
0.9
0.4
0.2
0,2
1,2
1.2
0,1.
1.3
0.9
0.9
10.6
0.7
.carzna
t;F W In
F—
0
0.7
0.4
1.8
13
0.7
8.3
0.9
0,5
0.2
0.1
0.0
0,1
0.0
0.4
0.6
1.4
10.2
13.
•
—
2,5 7.1
—
0.0
—
7.9
—
8.9
17,6
—
5.2
—
4.9
—
4.6
43
5.2
11.6
2.1
.9
4.5
95.0
5,9
-------
Table 3: MEANS AND PERCENTAGES OF 3 MAIN EXTRACTED FAUNA
GROUPS IN PREPARED ORGANIC FERTILIZER AND CAST
DRAIN SOIL
GROUPS ORGANIC FERTILIZER
Mean/sampl2
-_a_________
COLLEMBOLA 0.23 22.60
CAST
DRAIN SOIL
Mean
0.50
sample!
-
%
—
25.51
INSECTA
2.30
22.77
0.63
32.14
ACARINA
7.57
74.95
0.83
42.35
Table 4: MICROFLORk AND MICROFAtJNA IN
WITH ‘ iWO SOIL PROPERTIES
that it contains a high percentage of
to both soil or plants, especially if
once in somewhat alkaline soils. It
sensitive animals for the same reason
TSS that may be harmful
it is used more than
injury may also affect
discussed.
IVTAL
10.1’)
1.96
THREE APPLICATIONS
-
-
-
pH
Total
means
gm
soil
‘ acteria
Fungi
Actino-
Total
Soluble
mycetes
Microfauna
Salts
Mean %
CONTROL 7.56
1.11
2 x io6
1.17x10 5
2.5x10 5
3.66 23.28
CAST DRAIN
SOIL RESI-
DUES 6.20
3.75
.

12 x 10
4
4.5xlO
4
3.75x1O 1.96 12.47
ORGANIC
FERTI- 6.65
2.60
6
6 x 10
5
2.3x10
5
2.5x10
10.10 64.25
.LIZER
—
U
l11 5
-------
SUNM RY
An ezaluation of fauna existing during a year in
dredged and mounded muds from an open drain was researched.
As this soil is transferred to organic fertilizer when
using it as an animal bedding in their sheds, fauna was
also estimated in it, plus accompanying soil cultivated
with ordinary crops. Soil properties that were suggested
to affect fauna, was also estimated.
The results indicated that no fauna was present in the
mud residues until the third month. Extracted fauna was
found to fall under two orders: Insecta and Acarina. 3pring—
tails comprised a reasonable fraction of insects. It was
suggested that this type of soil is not preferable in use
as an organic manure especially in the somewhat alkaline
soils with high water table. On the other hand, this soil
can be used in brick factories or filling up house foundations.
ACKNOWLEDGMENTS
The author wishes to express his sincere gratitude to
Dr. S. Masha]., Department of Botany at the Faculty of
Agriculture, Tanta University for estimating microflora
counts recorded in this investigation. Thanks are also due
to Miss E. El—Wakil, Mr. E. Khalifa and Mr. S. Mashali from
Soils Department for their aid in soil analysis included in
this research.
REFERENCES CITED
Allison, F.E. 1966. The fate of nitrogen applied to soils.
Adv. Agron. (18): 219—258.
Baule, H. and C. Pricker. 1970. The Ecrtilizer treatment of
forest trees. BLV. Munich: 259.
Behan, V. 1972. The effects of urea on acarina and other
arthropodes in Quebec black spruce ( Picea mariana ,
Mill) hinuus. Proc. North Amer. Forest Soil Conf.,
Laval Univ. Quebec (1973): 110—135.
-------
I
Behrend, D.F. 1973. Wildlife management—forest fertilization
relations. In Forest Fertilization Symp. Proc: 108-110.
Bengsto. . G.W. 1971. Trends in forest fertilization. Pages
27-77 Searching the Seventies. WA. Muscle Shools,
Ala.
El-Kifl, A.R. 1957. The soil 3rtbropod fauna in a farm at
Giza, Egypt. Bull. Soc. Entom. Egypte XLI: 231—268.
________ 1958. The arthropou fauna of the Egyptian farmyard
manure. Bull. Soc. Entom. Egypte XLII: 477—500.
Foster, A.A. 1968. Damage to forests by fungi arid insects
as affected by fertilizers in forest fertilization.
Pages 42—46 j Theory and Practice. WA, Muscle Shoots,Ala.
Hafez, M. 1939. Some ecological observations on the insect
fauna of dung. Bull. Soc. Fouadler. Ent. XXIII: 241—287.
Jacot, A.P. 1940. The fauna of the soil. Quart. Rev. Biol.
XV: 28—79.
Mitchell, M.J. 1978. Soil of invertebrates and microorganisms
in sludge decomposition. Pages 35-50 a. Eartenstein
(ed) Conf. Proc. of Utilization of soil organisms in
sludge management. SIJNY CESF. Syracuse. NY.
Tadros, M.S., A.K. Wafa and A.H. El—Kifl.. 1965. Ecological
studies on soil oribatei in Giza region. Bull. Soc.
Entom. Egypte XLDC: 1-37.
_______ Abdel-Fattah and S.A. Saad. 1978. Structure and
activity relationships in herbicides on soil microfauna of
e tonfie1ds. Pages 1134-1140 Proc. mt. Symp. On
Crop Protect. Gent, Belgium.
Weetman, G.F. 1971. Effects of thinning and fertilization
on the nutrient uptake, growth and wood quality of
upland black spruce. Pulp and Paper Inst. Can. Woodland
32: 18.
William, E.C. 1942. M i ecological study of the floor fauna of
Panama rain forest. Bull. Chicago Acad. Soc. VI (4): 63.
1 i7
-------
LEAD AND CADMIUM CONTENT IN EARTHWORMS
(LUMBRICIDAE) FROM SEWAGE SLUDGE AMENDED ARABLE
SOIL
Caspar Andersen
Royal Veterinary and Agnc elI’.raI University
Denmark
ABSTRACT
From 1976 to 1978 a research programme has been carried out
in order to investigate the uptake of the metals Lead and Cadmium
in eat thworms from sewage sludge amended arable soil. Two types of
sewage sludge were used in the experiment. One with a low metal con-
tent and one with a high metal content, derived from an industrial
area of Northern Copenhagen. Additionally was studied Lwnbricus te —
restrie L.,1758,frcm the garden of The Royal Veterinary and Agricul-
tural University in central Copenhagen with heavy Lead pollution from
automobile nission. Metal content was measured in whole earthworm
tissue, waste bodies from the posteriormost region, gut walls, soil,
sewage sludge and earthworm casts. In general Lead is not concentra-
ted in earthworm tissue, whereas Cadmium is strongly concentrated.
AikaZobophora ionga Ude,1886, seems to exploit the sewage sludge—
N supply very extensively. Frequencies of the individual species
from the sewage sludge treated plots were compared to plots receiv-
ing slurry and farmyard manure.
INTRODUCTION
As a result of the increasing interest paid to the recycling
of waste water and sewage sludge in agricultural practice, a great
effort has been done to study the uptake of heavy metals in crops for
hucnan food. In this connection there is also a need to study the gen-
eral impact of these metals on the soil life, because good soil con-
ditions and plant growth as revealed by several investigations are
intimately associated with soil life.
Dindal, Schwert and Norton, 1975, found that waste water irri-
gation caused r shift in soil fauna biomass towards earthworms and a
general decrease in species diversity. Earthworms are preyed upon by
a great number of animals and may become a potential source of pollu-
tion for these in an increasingly polluted environment. &etz, Best
and Prather, 1977, found highly increased Lead levels in starling kid-
ney and liver from urban environments.
In the present study is reported on uptake of Lead and Cadmium
in earthworms from sewage sludge amended soil and the influence on
species composition. The up•.ake of these metals was also studied in
L. terrestria from the garden of The Royal Veterinary and Agricultu,.-
al University (RVAU) in central Copenhagen, adjacent to a main street
with intense automobile traffic. The investigations were supported
by the Danish Research Council, SJVF.
148
-------
METEO13 and MATERIALS
Sampling and treatment
Earthworms for metal analysis were sampled in sewage sludge
experiments performed at Askov Research Station, Southern Jutland,
in June and October 1977. Two types of sewage sludge ‘were used. 1)
one with low metal content and 2)one with a high metal content, in-
dicated in Tables 1 to 3 by (L) and (H) respectively. Material for
metal analysis was obtained by digging. Material for species and bi.o—
mass determination was extracted by the formalin technique using 0.5
m 2 sampling quadrat. Eight sampling units were taken per treatment,
which also include a 0—treatment. The sewage sludge was given in
amounts equivalent to 30 tons sand free dry matter/ha, and contains
approximately 1000 kg N/ha. the following species w. re obtained:
A. l.onga, A. caliginosa Savigny, 1826, A. roelaa Savigny, 1826, A.
ohiorotica Savigny, 1828, and £wnbi’ioua terreetrie.
Material of I. terr astris was sampled by the formalin extrac-
tion technique in the RVAU—garden at stations in, 20, 30, 40 and 50
metres from the side of a main street with intense automobile traf-
fic.
Preparation of samples and extraction
From the sewage sludge experimeut were taken subsamples of
earthworms containing from 10 to 35, depending on size. Lead, Cad—
mium and Calcium were extracted from worms, sewage sludge, soil and
casts of A. 1 onga by vet digestion in nitric—perchtoric ..tcid with
subsequent analysis by atomic a’osorption spectrophotoinetry (An4ersen,
1979 in press). From A. longa waste bodies located in the coeloinic
sacs of the posteriormost region were isolated by dissection. Like-
wise gut wall material was isolated from behind the gizzard in A.
ionga and A. rosea. Metals from waste bodies and gut material were
extracted by wet digestion in 1 ml nitric—perchloric acid (4:1) in
test tubes glaced in an alumigium block heated on a hot 0 plate, 3
hours at 80 C, 2 hours at 110 C and 1 to 2 hours at 180 C for evap-
orating most of the extracting solution. After cooling metals were
quantitatively transferred to test tubes with glass stoppers in 3 x
1 ml 2N 1* 103 diluted (1:20) in double deionized water. Then were ad-
ded 1 ml Na—citrate buffer and 1 ml 1% DDDC (Diethylainmonium.N.N.
diethyldithiocarbaminate) in xylene, an organic conipexbi—der. The
solution was shaken for not less than 2 minutes, with oubsequent
analysis by AAS.
Yron. the RVAU-gardeit material of worms and soil were taken six
subsamples per station for metal analysis. Each subsample of worms
contained from 3 to 5 mature individuals. Soil pH was determined in
Cad 2 .
RESULTS
Metal content of worms and soil from the sewage sluc ge experi-
ment is given in Table 1. In Table 2 is given metal content in A. ion—
149
-------
— —— . aJ sa.%- I — —
ga casts, sewage sludge and the top 5 cm soil (soil/sewage sludge)
mixture from the experimental field. Data in Tables 1 and 2 are corn—
biv 1 from June 1977 and October 1977. Number of subsamples are from
2 to 7 except in A. rosea 0—treatment, and A. ohiorotica where there
was only material for one. Neither was there sufficient material for
analysis of A. caliginoca and A. chior’otica from the 0-treatment. In
Table 3 is given metal content in waste bodies and gut wall material.
Whole body and gut wall material was isolated from material fixed in
42 formalin and stored for one year in 70% alcohol. Lead and Cd con-
tent in the storage liquid was neglectible, 60 ppb Lead and 9 ppb Cd.
In Table 4 is given Lead, Cadmium and Calcium content in £. terre—
etrie and soil, including soil pH from the RVAU—garden. In Figure 1
number and biomass of earthworms from the sewage sludge experiment
are given. It is seen that L. tez’reatris is also included here, but
material for nicital analysis was insufficient. The reason for this is
that L. terreetris is difficult to obtain in sufficient numbers for
ar alysis by digging. In Figure 2 Lead is plotted against Calcium in
L. ter?estris from the RVAU—garden. It is seen that there is a weak
correlation between Lead and Calcium cor.tent r = 0.5113. p < 0.01.
y = 0.0035 x + 0.9106. There was no correlation between Cadmium and
Calcium content.
TABLE 1 . Askov Research Station. Metals (ppm dr.w.) in earthworms
and soil.
A.
Z.onga
A.
rosea A. chiorotica A. caligino a
Soil
Pb
Cd
Pb
Cd
Pb
Cd
Pb
Cd
Pb
Cd
Treatment
0 3.8 11.8 3.2 26.9 — — — 15.3 0.29
SLUDGE CL) 4.6 5.7 4.7 10.9 4.6 10.9 6.4 6.9 23.2 0.65
SLUDGE (H) 5.9 9.2 5.5 19.6* 5.8 16.2 9.2 1C.9 3S.9 0.99
*$ignificantLy higher than sludge CL).
TABLE 2 . Aslccv Research Station. Metals (ppm dr.w.) in casts
of A. longa, sewage sludge and soil.
SLUDGE CASTS SOIL —
Pb Cd Pb Cd Pb Cd
Treatment -___________________
O — — 13.2 0.14 15.3 0.29
SLUDGE (L) 396 14.6 45.0 0.53 28.2 0.65
SLUDGE (H) 2425 25.0 105.0 1.60 40.0 0.99
iso
-------
I
TABLE_3. Askov Research Station. Metals (ppm dr.w.) in A. Zonga
— waste bodies and gut wall, and A. roeea gut wall.
.4. longa A. longa A. rosea
WASIE BODIES CUT WALL CUT WALL
Pb Cd Pb Cd Pb Cd
Treatment
0 60.0 15.4 31.4 16.1 12.0 16.1
SLUDGE (H) 89.2 12.9 31.6 15.0 23.7 15.0
TABLE 4. kVAU—garden. Soil pH. Metals (ppm dr.w.) in L. tar—
reetria and soil. 10 to 50 metres from the roadside.
SOIL
1. terrestria
p 1 1 — Pb Cd Ca
Pb Cd Ca
Metres
10 6.93 203 1.04 25300 23.7 21.0 5000
20 7.08 179 0.76 23000 13.3 30.8 3000
30 7.21 148 0.72 24000 18.9 32.5 4700
40 7.40 66 0.29 24000 7.2 29.1 2900
50 7.28 90 0.45 16100 8.9 12.5 4500
DISCUSSION
Prom Figure 1 it is seen that number and biomass per in 2
high for the species A. longa and L. terre.. trie. L. terreatria is
primarily a f eerier on dead leaf material, but will to a high degree
also feed. on the sewage sludge. When these data are compared with
plots rcceiving farmyard manure with approximately the same nitrogen
content (1000 kg N/ha) (Ande sen in press) it is also seen that the
number of L. terreetrie is slightly lower, but biomass higher and
that the proportion of adult biomass is very high compared to the
condition in farmyard manure. In slurry both number and biomasa of
L. terreatria are very low. It may therefore be concluded that sewage
sludge suppresses reproduction in this species. In A. longa the pro-
portion of adult biomass is much smaller. Apparently this species is
not a surface feeder as L. terree ris, but nevertheless appears to
have a preference for particulate organic matter, and becomes do . i—
mating in sewage sludge. In farmyard manure treated plots it is
likewise seen that the number of biomass of .4. lon ’a is greater than
in slurry treated plots, which fits well with this interpretation.
From Table 2 it is also seen that casts of A. Zonga contain coneider—
able amounts of Lead and Cadmium coir axad to the content of the sew-
age sludge treated soil. It is therefore cor. luded that A. 1 .onqa ac-
tively locates and eats the sewage sludge.
Upon dissection it is seen that tn the posteriormost 10 or
more segn*rnts in A. Zonga the coelomic sacs were densely packed with
waste material. These waste bodies on microscopic examinati.,n appear
151
-------
A. Biomass of Earthworms.
1111
ffflr
1Z34 12345
5 tL) S(H)
11
1 .i4
SW
1
12 i 45
PT ’
FIGURE 1 . A. Biomass g/m 2 in June 1977 of the Earthworms: 1)A. longa,
2)A. al iginoaa, 3)A. roeea, 4)A. ohiorotica, 5)1. terx e—
str 8 from the following treatments. 0 — zero—treatment.
S(L) — sewage sludge with low metal content.
high metal content. FI!M - farmyard manure,. 1000 kg N/ha.
SLU Slurry 1000 kg N/ha. The N content of sludge was
approximately 1200 kg N/ha.
152
• Adults
D T.oEatures
30
20
10
0
No. /m 2
S(L)
S( 11 )
150
100
SLU
B. Number of Earthworms.
50
-------
FIGURE •
ppm
40
30
20
10
Pb
Regression of Ca against Pb content in the Earthworm Lwn—
bz’icua tezrestrie from the garden of the Royal Veterinary
and Agricultural Unive:3ity, Copenhagen 1 adjacent to a
main street sampled at distances from 10 to 50 metres
from street. The correlation coefficient r = o.5113 is
weakly significant p < 0.01 at n = 29.
153
.
.
.
.5
.
.
.
S
y = 0.0035 x + 0.9106
r = 0.5113
S
ppm Ca x 1000
5 10
-------
to be surrounded by a znembraneous structure and can easily be drawn
out of the coelomic sacs with a nea.dle. The waste bodies posscss a
very heterogeneous structure and have a Lead content which is extraor-
dinarily high compared to the content of the worm in toto. (Table 3
and 1; 90 ppm Lead versus 6 p 1 mO. The origin of these waste bodies
is not clear, but they may represent transformed nephridia, which is
now being investigated. Material of L. terrestria also possesses such
waste bodies. In L. ternetris there appears to be a number of smal-
ler packages in the last five to eight coelomic sacs as oppnsed t
A. longa where two or three large waste bodies fill up the entirE
space of the coelomic sacs in the ten posteriormost segments. Metals,
however, were not analysed it s L. terrectria waste bodies, but as seen
from the better :eproduction in A. jonga this species may be more ef-
fective in inmebilizing harmful substances in this way. This phehome—
non may be part of a i x evolutionary strategy in especially A. Zonga,
being more dependent on processing large quantities of soil than L.
terr estria, and therefore more exposed to pollution of any kind. The
posterior end may be easily lost and regrown, and harmful substances
accumulated in this way may be eliminated. The number of such waste
bodies present may also be age—dependent. The occurrence of waste
bodies in other species has not been investigated.
High concentrations of Lead and Cadmium were also found in the
gut wall from A. Zonga and A. rosea. But the difference in Cadmium
content between gut wall and whole animals inclusive waste bodies was
not so great as the differences in Lead content.
A. rosea, Table 1, is seen to concentrate Cadmium from the er
ternal medium with a factor 100 from untreated soil, but only with a
factor 20 from soil receiving sewage sludge with high metal content.
In A. ionga Cadmium is also concentrated mostly f to m tt3ated soil,
concentration fsctor 60. It thus appears that - . •r’ i . nrively
strongly immobilized in sewage sludge compared .... s .
This is consistent with other invefligations sh w3...g tS Cd 1..
strongly adsorbed to litter and decomposed r lant mate :ix (Somers.
1978) and humus (Tyler, 1972). In individue.ls from soil treated with
sewage sludge with a high metal content, CadmIum content is higher
than in individuals from soil treated with sewage sludge containing
less metal. This is seen in all species. However, variation between
subsamples is very great. and only in the case of A. rosea the dif-
ference between the two tçpes of sewage sludge was significant. (Tab-
le 1). This great vakLat on may be caused by .ineven age distribution
in the subsamplec.
In 1. ten- :atrie frnm so i. polluted by automobile traffic in
the RVLU—garden mc-ta content in general is highest (Table 4) close
to the strd ’t. Pro, Table 4 it is seen that soil pH is increasing
from 6.93, tcs trou toe street, to 7.40 at 40 metres’ d s—
tance, however, wLth a irop to 7.28 at 50 metres’ distance. Soil Ca
is generally high and the low pH values closest to the street may
be ascribed to acid pollution from the motor traffic.
Calcium content in 1. terreetrCe was analysed, because Calcium
metabolism and Lead content may be associated. Recent studies have
shown that the -hloragosomes of the chloragog tissues in L. terra—
atria (PrentØ, 1979) may play an impcrtant role in Calcium metabo—
lisi in this species, p H regulation and ionic and osmotic regulation
-S
-------
of the body fluids. A regression of Lead against Calcium in the RVAU
material showed a weak correlation between Lead and Calcium content
r = 0.5113, p < 0.1)1. Figure 2. Studies by Ireland (1975) have also
indicated this re1 ttionship. His studies were made in highly polluted
Calcium deficient soil, and at soil pH values well below 5. Therefore
the correlation under nearly neutral conditions will not be so strong.
In the RVAIJ—garden the earthworms seem to have unlimited access to
Calcium, but in the worms living closest to the street some Calcium
must have been used in stabilizing the internal milieu. pH of blood
and coelontic fluid is supposed to be slightly alkaline. pH 7.3 t i
7.4 (Drewes and Pax, 1974). This increased Calcium turnover will t ien
result in an elevated Lead level. The activity state of the worms may
also play a role in determining content of metals. In material of L.
terreatris from the RVAU—garden Calcium content was higher and Lead
content lower during reduced activity in December 1977 compared to
levels in active worms sampled in June 1978 (Andersen, 1979). but
mechanisms by which earthworms maintain salt and water balance under
normal conditions cf partial dehydration in the soil are little stud-
ied (Oglesby, 1978).
From the foregoing discussion it is seen that the uptake pattern
of heavy metals in earthworms is a complicateâ matter and may vary be—
twe3n species. Also different external factors are very impurtant,
notably soil pH and cjncentration of Calcium, including different food
sources of the earthworms. With respect to the q.aestion of earthworms
being a source of contamination for other animals it seems clear that
various birds and small maamals ±eedim.g on earthworms living in sew-
age sludge treated soil will be subjected to ingestion of consider-
able amounts of Lead from t e gut content, and also Cadmium concen-
trated in the tissue of the worms. Therefore communities being asso-
ciated with recycling of sewage sludge should be further studied.
1 .5
-------
LITERATURE CITED
Andersen, C. 1979 (in press). Cadmium, Lead and Calcium content, num-
ber and biomass in Earthworms (Lumbricidae) from sewage sludge
treated soil. Pedobiol. 19(6:00).
Andersen, . (in press). The influence of farmyard manure and slurry
on the earthworm population (Lumbricidae) in arable soil. VII
International Colloquium on Soil Zoology. Syracuse.
Dinual, D.L., D. Schwert and R.A. Norton. 1975. Effect of sewage
effluent disposal on coimnunity structure of soil invertebrates.
In 3. Vanek (Ed.). Progiess in soil zoology. Prague:419—427.
Dreves, C.D. and R.A. Pax. 1974. Neuromuscular physiology of the
longitudinal muscle of the earthworm Lwnbrz:cuc terreati’ia. i.
Effect of different physiological salines. 3. Exp. Biol. 60:
445—452.
Getz, Lowell L., L.B. Best and M. Prat.her. 1977. Lead in urban and
rural song birds. Environ. Pollut. 12(3:235).
Ireland, M.P. 1975. Metal content of Dendrobaena rzbida (Oligochae—
ta) in a base metal mining area. Oikos 26(11:74—79).
Oglesby, L.C. 1978. Salt and water balance. In P.3. Mills (Ed.).
Physiology’ of Annelids. Academic Press:555—658.
PrentØ, P. 1979. Metals and phosphates in the chioragosomes of
Lwnbricus terrestrie and their possible physiological signif-
icance. Cell and Tissue Res. 196:123—134.
Somers, G.F. 1978. The role of plant residues in the retention of
Cadmium in ecosystems. Enviren. Pollut. 17:287—295.
Tyler, C. 1972. Heavy metals pollute nature, may reduce productivi-
ty. Ambio 1:52—59.
QUESTIONS and COMMENTS
N. BEYER: Would you expect that cadmium concentrations
in earthworms would increase with time, as the organic matter
is gradually broken down after an application of sludge?
C. ANDERSEN : Yes there is a possibility that Cd may
become mobilized if the sewage treatment is interrupted.
S.G. RUNDGREN : In fact the concer tration of lead is
much higher in specific organs. We have made several analyses
of organs showing that there is a concentration and inagni-
ficatio of lead in organs such as cerebral ganglion and
reproductive tissues -
C. ANDERSEN : Yes we have also pursued this possloility
but are unfortunately not able to present any results at
this time.
j . VOSE-LAGERLtJND: Do you think you can use the Cd-
level in earthworms as a reliable indicator on Cd—pollution
in general? Will this be an inexpensive method in the future?
C. ANDERSEN : This is a possibility but further studies
are needed on the dynamics of cadmium with respect to local—
i.zation in specific compartments of different species of
earthworms.
15b
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VERMICOMPOSTING ON A HOUSEHOLD SCALE
Mary Appeihof
Kalamazoo Nah.rr Cm l ,, Inc.
USA
INTRODUCTI Or
The organic component of household garbage contri-
butes to increased loads in solid waste disposal operations
and, through garbage disposals, in wastewater treatment
plants. Either form of disposal, burying in landfills or
flushing it down the drain, wastes potentially valuable nu-
trients for plant growth. Gardeners who compost recognize
the value of recycling these organic wastes. During winter
months in colder areas, however, many “composters seek other
ways to dispose of their garbage because they cannot get to
their compost piles through the snow. Previous work by the
author (unpublished, and Appelhof, 1974) has shown that two
pounds of earthworms can process a pound of garbage a day.
This figure is supported by Roy Hartenstein’s work with se-
wage sludge (Hartenstein, J978) and Ronald Gaddie’s work with
larger quantities of worms on city refuse (NEWSWEEK, 1976).
This project was designed to demonstrate that house-
hold garbage can be roadily composted indoors during the win-
ter, using earthworms to process the garbage and convert it
to humus. An experiment was set up to determine whether it
was feasible tc carry this out on a larger scale than that
of a single household.
MATERIALS AND MEIHODS
Three wooden bins were constructed of 3/4 inch ply-
wood: two single family bins (SPB 30.5 x 61 x 91.5 cm (1 x
2 x 3 ft) and one multiple fa ily bin (MFB) 30.5 x 76.5 x
245 cm (1 x 2½ x 8 ft). One-half inch holes were drilled in
the bottom for aeration. Bins were placed on legs with cast-
ers for convenience.
Shredded cardboard bedding (WORM CHOW from Worm World
Denver. Colorado) was soaked in water, wrung Out by hand,
and placed in the MFB and SFB A to a level of approximately
20 cm. Newspaper shredded by hand, soaked in hot water,
and wrung out was used in SFB B to determine whether this
readily available material could also be used as a bedding.
157
-------
Redworms ( E&senia foetida ) donated by the Southwestern
Michigan Worm Growers Association were used as follows: 9 kg
(20 ibs) in the MFB, and 0.9 kg (2lbs) in each SFB.
Household garbage from six low income famijies was bur-
ied weekly for 14 weeks; two families used the two SFB’s, four
to six families the MFB. pH was tested using pH paper (Hydri-
on Vivid 6-8 range , ‘icroessential Laboratories). Moisture was
determined empirica4ly by squeezing a handful of bedding. A
stre im of water or definite sogginess at the bottom was felt
to be too wet, extreme dryness on top, too dry. Burlap used
to cover the bedding reduced excessive evaporation of moisture
and curtailed undesirable odors. Bins were watered as needed.
Participants weighed and buried the garbage, tested p11, check-
ed moisture, and watered the bins.
A spectral analysis of the bedding for nutrient value
was obtained, and a sample was taken of the completed compost.
Worms were separated from the compost and bedding to be weigh-
ed on week 16. Compost and worms were distributed among the
participants during week 17.
RESU LTS
The amount of garbage buried per week and pH of the bed-
ding are shown in Table I. In the MFB, a total of 78.2 kg was
buried over a period of 14 weeks, averaging 5.58 kg/wk, or
1.35 kg (2.97 lb)/family/wk. Of the SFB’s, one received a tot-
al of 30.8 kg, averaging 2.3 kg (5.3 ib), the other a total of
TABLE I. pH OP BEDDING AND AMOUNT OF GARBAGE BURIED PER WEEK
MULTIPLE FAMILY BINS SINGLE FAMILY BINS
SFB A SFB B
Week kg garbage # Lam. pH kg garbage pH kg garbage pH
1 3.4 5 6.9 1.3 .o .s 6.6
2 5.1 5 6.6 5.6 6.6 2.2 6.0
3 8.4 5 6.6 3 ,9 1.5 6.9
4 7.z 5 6.3 2.0 6.4 1.7 7.4
5 6.5 5 6.4 1.5 6.9 2.3 7.6
6 8.4 4 7.4 1.6 7.0 1.4 7.2
7 5.3 4 6.8 1.8 7.4 1.5 7.4
8 7.0 4 6.9 2.1 7.6 1.5 7.6
9 5.4 3 6.8 0.8 7.0 2.2 6.8
10 4.2 4 7.4 7.2 1.4 6.4
11 7.1 4 7.0 5.6 7.1 2.7 7.6
12 3.5 3 6.8 2.6 7.2 1.4 7,4
13 3,9 3 7.2 2.0 8.0 2.1 8.0
14 2.8 4 7.2
Total 78.2 58 30.8 25.4
Mean 5.58/wk 1.35/fam/wk 2.37/wk 1.95fwk
158
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25.4 kg, avo aging 1.95 kg (4.3 ib) per week. pH of
the bedding ranged from 6.3 to 8.0.
Considerably less garbage (1.35 kg/fam./wk) was bur-
ied in the multiple family bin than in either of the two SFB’s
(2.37 and 1.95 lcg/wk).
Initial and final weights of worms, total amount of gar-
bage buried, and compost obtained appear in Table II.
TABLE II. AMOUNTS OF GARBAGE BURIED, COMPOST OBTAINED, AND
WORMS USED (kg)
MFB SFB I SFB B Total
Garbage buried 78.2 30.8 25.4 134.4
Compost 76.8 16.0 23.2 116.0
Initial worms 9.0 0.9 0.9 10.8
Final worms 2.25 1.05 0.79 4.09
Total wet weight of worms and compost was 116 kg. Con-
tributing to this weight was the original bedding (weight un-
known), and 134.4 kg garbage. Whereas bins were originally
set up with 10.8 kg worms, only 4.09 kg were harvested. The
presence of many you ig worms and capsules in the bedding in-
di.cated that reproduction did take p1a ..e.
Types of garbage buried were lettuce, cabbage, celery,
beet greens, citrus rinds, banana peels, cereals, beans, bread,
egg shells, moldy leftovers, apple and potato peels, and over
40 different kinds of kitchen garbage. Meat scraps and bones
were not generally included, although on at least one occasion
chicken bones were buried.
On a qualitative basis, shredded newspaper appeared to
provide a sstisCactory bedding, although it dried out more
readily on top and was more difficult than shredded cardboard
to prepare.
DISCUSSiON
This work served to demonstrate to the participants
and to thousands of others that earthworms can effectively con-
vert household garbage to compost, indoors, within a four
month period, and with almost no objectionable odor. Partici-
pants, all members of low income families, were able to dis-
tinguish and separate acceptable organic materials from unac-
ceptable materials such as rubber bands, foil, plastics. They
were also able to comprehend the need for and maintain the rig-
ors of weekly trips to the Kalamazoo Natnre Center to weigh
1S9
-------
the garbage, check pH, and water the bins. One motivation
for their continued enthusiasm and participation was the fact
that each participant would receive a share of th compost to
use in her garden and/or on houseplants.
There i3 no question that, combined with the wirk of
microorganisms, molds, fungi, and other decomposers, the gar-
bage is effectively processed by earthworms. How much they
can handle, or how much a given quantity of worms requires to
maintain its biomass is still unknow i. The great reduction
in biomass in this experiment (greater than one-half) may be
attributed to inadequate nutrition. The experiment was de-
signed assuming that each family would contribute about 450
g garbage/day, or about 3 kg/wk. The results show that less
than half this amount was fed to the worms. Whereas six
families could have buried garbage in the MFB, only four did;•
since these four contributed less than half the expected
amount, the worm biomass far excoeded the mass of food to eat..
The original worm population did reproduce--many cap-
sules and young worms were seen in the bedding. The greater
nutritional needs of this larger population were most likely
not met, and may further explain why biomass was reduced so
drastically. Other possibilities are that worms were dying
from toxic conditions created in the beds from their OWTI
castings, lack of calcium in the environment, and lack of
soil.
CONCLUSIONS
Household garbage from six low income families was ef-
fectively converted by 10.8 kg redworms ( Eisenia foettda )
to worm castings and compost over a 16 week period. The ave-
rage amount of garbage buried/family/wk was 1.6 kg (3.5 ib),
for a. total lf 134.4 kg (298 lb) over 14 weeks. Both shred-
ded cardboard and newspaper served as satisfactory beddings.
Wet weight of the compost produced was 116 kg. Further work
needs, to be done to determine optimum worms/garbage/bedding
ratios.
LITERATURE CITED
Appeihof, Mary. 1974. “Worms--A Safe, Effective arbage Dis-
posal”. ORGANIC GARDENING AND FARMING MAGAZINE. Aug.65-69.
Hartenstein, Roy. 1978. “The !4bst Important Problem in Sludge
Management As Seen by a Biologist”. In: Conference Proceed-
ings: Utilization of Soil Organisms in Sludge Management.
Syracuse, NY. June, 1978. 2-8.
NEWSWEEK. 1976. “Worming Away”. June 21. 67-68.
160
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RECULTIVATION OF REFUSE TIPS: SOIL ECOLOGICAL
STUDIES.
W. Brockmann, H. Koehler and T. Schriefer
UmveTssty B,rmen
We Germ riy
Many problems arise with the recultivation of a refuse tip and its
preparation for later coniuercial or public use. They are related to
the underlying material (garbage etc.), to the new artificial topo-
graphy of the dump and to the undeveloped soils of the refuse tip cover.
In order to find a basis 1:cr ecological recultivation measures on refuse
tips, soil ecological studies on test sites in the vicinity of Bremen, FRG,
have been undertaken (temperate climate, precipitation 728 mm/yr 1 . average
temp. 9°C). Three selected studies are presented, two as prelimin3ry re-
ports.
The Influence of methane on the immigration to refuse tiDs by Lumbricids
Research site and methods
Six waste dl5posals, controlled tips as well as uncontrolled uncovered
tips were examined with special reference to the earthworm fauna.
The fonnalinmethod according to Raw was used (Raw, 1960). Sample squares
were 0.25 and 0.125 m 2 . The biotop study was done during April and June 1978.
Soil air conditions were measured with Dräger.GasspUrgerät Mod 21/31.
Two sites of different age (3 yrs and 5 yrs after covering) on the same
refuse tip were Investigated in respect to immigration mechanisms nut of
the surrounding habitats.
Results and discussion
Pi gure 1 shove the state of immigration, the abundance, the vegetation
cover and the soil-air conditions. Lumbricus rubell us and Dendrobaena
octeedra (south exposition) are the important colonizing species on this
covered waste disposal. Horizontal — and deep burrowers are unimportant.
Elsenla tetraedra was frequently found in the zone of percolating water.
The immigration speed is about 4 rn/yr towards the tipplateau.
On the covered waste disposals the Immigration of the soil cover by
earthworms Is hindered by bad soil aeration.
161
-------
nd ind
,o. ‘0 .
v I
_________ ‘° ‘ \‘ r 7 . L
c i - _ - _ -. -— — - 0 LL __ .I ’ #--.-..——
covered in 1975
FIGURE is Imigration of Lumbricids on two sites of different age
(3 and 5 years after covering) on the same refuse tip
slope. Graphs from top to bottom: State of insnigration,
abundance, vegetation cover, soil—air conditions, soil-
moisture (F) and soil-activity.
The study has shown, that eartlw.orm-inmiigration is affected by
0 2 —concentrations below 15 col% and C0 2 -concentrations of more than
6 voiX (15 cm depth).
Methane and carbondioxyd production from the underlying waste force
out the atmospheric oxygen even of upper soil layers (Tabasaran, 1976).
Damage on the vegetation was observed when 0 2 -concentratlons were less
than 15 vol%.
Li.,
0. . ,
D ’vb
‘I , ’ ,. . ’
Vot% >JO% >30% 0,
10 °
covered in 973
m
i6z
-------
The correlation analysis shows both high significance between
0 2 -concentration and vegetation cover as well as between 0 2 -concentra-
tion and abundance of earthworms. It is not known whether the immi-
gration is hindered directly by the bad soil aeration or indlrcctly by
the absence of plant cover.
The influence of soil cultivation and compaction on the
Enchytraeid community (prel. rep.l
Introduction
The negative effects of soi I compaction on terrestrial invertebrates
are evident (Wilcke, 1963). In field and laboratory investigations on
soil animals (Acari, Collembola, etc.) a decrease in numbers was found
when compacting clay grassland soil (Aritajat et al., 1977). This report
shows preliminary results of field experiments on Enchytraeidae after
mixing and com ,acting clay grassland soil. The transported and disturbed
soils of wasts tip covers are characterized by destruction, drainage and
compaction of the habitat the soil fauna lives in. These factors may cause
difficulties in recolonization and erection of a terrestrial ecosystem of
high stability.
Research site and methods
Preinvc.st 1 gatlons ware done in July and August 1978 on a clay grassland
soil within an area of 8 x 24 m. For treatment this range was splitted into
three equal test plots (64 in 2 ) on the 16.9.1978. Plot 1: remained untreated.
Plot 2: soil was loosened down to 15-18 cm by rotary cultivation. Plot 3:
treated like plot 2 and once compacted with an UNIMOG tractor (1.01 kp/cm 2 ).
Samples were taken randomly at intervals of two weeks and one, three, six
and nine mcnths after the treatment. Twelve soil cores each with 20 cm 2
surface and 15 cm depth were examined from the three test plots and divided
intc 5 cm layers. These 100 cm 3 samples were extracted in an apparatus
functioning according to the method of O’Connor (O’Connor, 1962).
163
-------
Results and discussion
Results ( FIGURE 2 ) are means of 12 samples. The distribution pattern
shows aggregation, typical for Enchytraeids (O’Connor, 1971). 14 days after
the treatment significant density decrease is observed on plot 2 and 3.
Compared to the control-plot 1 the compacted plot is marked by a continuous
decrease of abundance (up to 90% in June 1979) throughout the Investigation
period.
A correlation between compaction of soil and decrease in numbers of
Encnytraeids on the experimental plot is obvious. Correlation studies be-
tween the reduction of Enchytraeids and the volume of macro-pores (>50u)
are in progress.
Seasonal Variation of Ihe Abunclonce of ENCHYTRAEIDS
m 2
do. of
•xomw ,othr
p..
g
0
I . ,
ii
Otilveated s l mbod sail mixed a d compacted soil
FIGURE 2s Abuy,dance of EnchytrOIidO of tr diffr.nt ?t•osmsnt of ths iou (,nson of 12 i Is 1.
16’e
-------
On plot 2 the original abundance has nearly been reached 9 months
after the treatment. High precipitation and high soil humidity during the
study period (Sept. 78 — June 79) as well as an increase of soil pores
> 50 i for about 55 % has promoted the fast regeneration of Enchytraeids.
The usual dry suimner months with rapid evaporation of water from the
bare soil surface and the high soil temperature on the treated plots may
cause additional negative effects on the remaining fauna. Further comparative
investiçjations on the terrestrial invertebrates will be of high interest for
the probler of recultivating refuse tips. In such places the abiotic and
biotic conditions in general are even worse than on the described test
sites.
Comparison of the soil mesofauna of a dump with an adjacent meadow with
special reference to Acarl and Coilernbola (prel. rep.) g
Introduction
One of the problems concerning the recultivation of waste disposals is
th.. relatively undeveloped soil fauna of the cover. he colonization from
the surrounding habitat is controlled by the physical soil conditions and
by the dispersal power of the colonizing species. For a zoological soil
diagnosismites are very useful, since their abundance is enormous (up to
2 io6 ir d/m 2 in the ;tudied grassland) (Strenzke, 1952).
Research site and methods
A marshland clay grassland adjacent to a dump near Bremen, Fed.Rep.Ger.,
has been investigated since Feb. 1978 monthly. A simultan&ius study on both
sites, dump and meadow, started in June 1979. Genercliy, 12 samples.of
20 cm 2 surface and 15 cm depth were taken and cut into cylinders 5cm deep
(100 cm 3 ). These samples were treated in a modified Macfadyen Canister
Extv actor (Ilacfadyen, 1961), 4 days in ‘umid regime (up to 35°C), the
following 6 days in thy regime (up to 60°C). The organisms ro collected
in picric acid and then transferred to an alcohol—glycerin mixture (Voigts,
Oudem ns, 1 O6), for counting under a binocular microscope.
Thr abiotic data are from June 79, the biotic data from June 73 (meadow)
and June 79 (dump).
L 6 3
-------
Results and discussion
The characteristics of the two sites are:
Grassland: full vegetation cover ( Alopeccurus pratensis, Festuca rubra),
well developed humus, high perce.itage of clay (sand ‘ 15 %), high
moisture (‘ 50 %), low pH (4.0 — 4.5). Refuse site: well developed pioneer
vegetation ( Cirsium arvense, Artemisia vulgaris, Tanacetum vu qare, Poa
div. spec.), little or no humus, sand with some clay, low moisture (< 15%),
medium pH (6.8 - 7.3).
As shown in table 1, the abundances especially of the Acari differ
strongly on both sites.
Tab. 1: Abundances (ranges) of Acari and Colleinbola of meadow (June 78)
and dump (June 79); md/rn 2 x IO 3 , o-15 cm depth.
Meadow Dump
Acari
- 168.4
-
1837.6
4.4
-
72.8
Collembola
68
-
119.2
7.6
-
70
In the meadow, the abiotic conditions are very favorable for oribatids
(Strenzke, 1952). Here they represent nearly 60% of the mite community. On the
disposal site, however, oribatios in addition to being slow colonizers fird
suboptimal abiotic conditions, which is reflected by their low abundances
(Karg. 1962b, 1967;Fig. 4). Gamasids and Tyroglyphids, both highly mobile
species with high dispersal power through phoresy make up the major fraction
of the Acari community (Stammer, 1962). A predator-prey relatiociship between
these two groups has been suggested by Karg (1961).
The trophic structure of the Acari and Collembola communities of the
two investigated sites are very similar. The relative abundances of decom-
posers (Collembola and mites without Gamasids) In relation to predators (Ga-
masids) are comparable (meadow: 90/10; dump: 85/15, Fig. 5). This suggests
that trie two years old plot on the dump has recovered a certain stability.
Further studies on the structure o the communities are under progress.
166
-------
I ”.
60
JPil Meadow
£0
H Dump
20
ORIDATIDS
Fig. 1: Coinpos1tk n oc the mite communities of meadow :nd Uump.
1’
Carnivores (Gamasids)
Phyto- ar4 detritophages (Collembola
and Acarl w/o Gamasids)
Fig. 5: Trophic structure of the acari-collembola community of
meadow and dump.
Literature c te
Aritajat, U. et al., 1977. The effect of compaction of agricultural soil on
soil fauna. Pedoblol. 17, 262-282.
Karg, W.., 1961. Ukologlsche Untersuchungen an edaphischen Gamasiden
(Acarl, Parasitlforines). Pedobiol. 1 77-98.
- 1962. Das Verhältnis von biocbnologischen, autökolo-
glschen und n’orphologlschen Arbeitsmethoden In der Bodenzoologie.
Abh. Ber. Naturkundemus. GUrlitz, 37, 179-188.
- 1967. Synökologische Untersuchungen von Bodenmilben aus forstwirt-
schaftlich und landwlrtschaftlich genutzten Böden. Pedobiol. 7, 198-214.
167
GAMASIDS OTHER
50
H
MEADOW DUMP
-------
Macfadyen, A., 1961. Improved funnel type extractors for soil
arthropods. J. Anim. Ecol. 30, 171-184.
C ’Connop, F.B., 1962. The extraction of Enchy raeidae from soil.
InMurphy,P.W. (ed) Progress ir’ Soil Zoology, London,
279—285.
- 1971. The Enchytraeidae. — In Burges, A. & Raw F. (eds)
Soil Biology, London-New York, 259-322.
Raw, F.,1960. Earthworm population studies. A comparison of sampling
methods. Nature, July 16/1960, 257
Stammer, H.J., 1962. Beiträge zur Systematik u. Dkologie mittel—
europ 1scher Acarina. Leipzig.
Strenzke, L., 1952. Untersuchunqen Uber die Tiergemeinschaften des
Bodens: Die Oribatiden und ihre Synus en in den Böden
Norddeutschlands.Zoologica, Stuttgart, 37, 104, 172 pp.
Tabasaran, 0., 1976. 0berlegung n zum Problem Deponiegas. MUll und
Abfall 7, 04-210.
Voigts, H., A.C. Oudemans, 1904. Zur Kenntnis der Milbenfauna von
Bremen. Abh. naturw. Ver. Bremen, 18, 1-253.
Wilcke, D.E., 1963. Untersuchungeri Uber den ElnfluB von Bodenverdlchtungen
auf das tierlsche Edaphon landwi rtschaftl ich genutzter F1 chen.
Z.f.Acker— und Pflanzenbau 118/1-44.
168
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SESSiON III: ANTHROPHILIC RELATIONSHIPS OF
SOIL ORGANISMS
Moderator: Arlan L. Edgar
Alma College
Alma. Michigavi USA
169
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PHYSIOLOGICAL AND ECOLOGICAL ASPECTS OF THE
COSMOPOLITAN OPILIONID, I’halangium opilio
Arlan L. Edgar
Alma C illege
USA
I NTRODUCT ION
The daddy longlegs Phalangluin oçflio L. is probably the
best known member of order Opiliones ( Ph iangida). It was
known to Aristotle. mentioned by Robert Hooke and was the only
opilionid species named by Linnaeus (Savory, 1962). Many medieval
naturalists made recognizable Illustrations of it. rhe species has
been recorded from many parts of Europe, North and Central Asia,
Asia Minor. North Africa and Nor..h America (Spoek, 1963). For.ter
(1947) reports that it is the only non-endemic opilionid in New
Zealand. Indeed, one may conjecture that this wa the species
that prompted the coninon names “harvestman” ar,d ‘reaper” of the
group in England and France, respectively. The most descriptive
name, daddy longlegs, possibly was given to P. opllio in America
although coninon woodland spe .fes of Lelobunum have longer legs and
smaller bodies and also may be the basis for this term.
Perhaps the main reason for our familiarity with P. opillo is
its occurrence around mans disturbance of nature. Typicil habitats
include roadsides, fence rows, lawns, gardens, edges of fields and
foundations of buildings (Clingenpeel and Edgar, 1966; Sankey and
Savory, 1974). These relatively exposed locations are not used
oi’dinarlly by other opillonids except by a few lo’ig-legged forms
In matin season and occasional populations of Opilio parietinus
(De (eer, In late fall.
The majority of species in any opilionid fauna are under some
kind of cover. They may bc in forest shade, near the grGund under a
vegetative overlayment, in fallen litter interstices or in the soil.
Why then is P. opillo different? Why Is there little overlap in the
habitats of P. opilio and virtually all others?
LIFE HISTORY AND DEVELOPMENT
Most woodland opihlonid species reach adulthood in late sumner,
then mate, oviposit and die in the fall. A few mature in early
sinimier and produce eggs that hatch In the fall. In the former, the
species pass the winter as eggs while the latter overwinter as
Ininatures. In both cases there is one generation each year.
Phalangiuni opihlo exhibits a third pattern. Wintering over occurs
170
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both as eggs and immatures. Hatching occurs in the spring and also
in mid summer whe , the winter juveniles reproduce. Oviposition is
done both in mid surmner and in late fall. Thus mature adults may be
seen during a large portion of the summer and fall in temperate
latitudes since two populations of ad jlts are produced each year.
PhalanQium opi1io is more noticeable in the fall than any other
time. When man is preparing shrubs and perennials for winter,
harvesting crops and garden produce in anticipation of frost P. opillo
adults are fully mature. They exhibit considerable movement; mating
behavior is easy to observe. Clutches of yellow eggs may be encountered
tinder rocks and solid debris at building foundations and vegetative
borders. The cue of declining seasonal temperatures apparently
stimulates the species to mate and oviposit.
Egg development requires a cold diapause in several species
(HoIm, 1947). Without it Opillo parietinus development goes to the
blastoderm stage and stops. Embryonation of P. opilio egr s proceeds
at a rate controlled by temperature but without the necessity of a
cold period. As a consequenre. it can be considerably more exploita-
tive of its environment than diapausal species. P. opillo is able
to utilize favorable environmental condttions to maximize population
size.
Opilionid eggs are very susceptible to dessication and fungal
attack. Eggs whose development has been terminated both by evaporative
fluid loss and mold colonization have been recovered in nature. Any
phalangid species that withstands a broader moisture regime during
egg development will have a reproductive advantage. In laboratory
incubations P. opilio eggs have tolerated greater relative humidity
fluctuation and resisted n ld growth more successfully than the
woodland species, Lelobununi longipes Weed, found frequently in
contiguous habitats. Eggs of tF e two species incubated side by side
in the laboratory reacted differently at both very high humidities
and low ones. Yuan and Edgar (unpublished) observed that eggs c’f
P. opilio develop and hatch with greatest success in an atmosphere
of 94 to 98% RH. Klee and Butcher (1968) hatched P. opllio eggs
on a substratum of styrofoam in 1/8” dia. holes approximately 3/4”
deep in an a nosphere of 75-90% RH. The relative humidity around
the eggs probably was much higher, however, since the styrofoam blocks
were “kept moist”.
Young P. opilio survive more successfully ira labratory
colonies than do other species. The general hardiness of eggs and
young of P. opillo , along with the life history characteristic of
several stages of development in a population at all times, appear
to be major factors enabling this species to survive the disturbance
of man.
17 1.
-------
HABITAT ANALYSIS
The open, relatively exposed habitat of Leiobunum vittatum (Say)
is as similar to that of P. pi1io as may be found in the Great LaIes
Region. Leiobunum vittatum is widely distributed in the northeastern
United States. The spectrum of environments where it has been found
ranges from the trunks of pulus growing in sand dunes to the edge
of a quaking mat bog. It apparently adapts readily to new conditions
and tolerates severe physical extremes. This species frequently
inhabits vegetative burders and ecotones from dense forest to open
fields where there is exposure to sun and relatively free air movement;
however, it is not abundant around man’s disturbance. Of all the
non—anthrophilic opilionids it occupies a habitat niost like that of
P. çpjlio in terms of temperature, light and relative humidity. For
This reason the habitat of P. p.ilio is compared with that of L.
vittatum and occasionally, for contrast, with woodlana specieso
Lelobunum and with a sometimes companion of P. oplIlo, QpiIio parietinus .
• In order to explore the habitat preference as well as the
vertical distribution of the various optutonid species, a number of
localities were visited and at each locality, organisms were collected
at three separate strata (ground layer, understory, uppercanopy). For
each stratum at each locality, both the abundance of organisms and
the density of cov r were estimated on a scale of 1 (sparse) through
5 (dense). Thus, after sampling was complete, it was possible to
compare the relative abundance of the opilionid species in relation
to the cover density in each of three height strata. The abundance-
cover profile (Figure la) atteripts to coinbfne a visual estimate of
both the relative abundance of the opilionid spectes and the density
of Its associated vegetative and other shade producing cover (Edgar,
1971). Data from 42 sites are combined In Figure la. A weighted
percentage abunda ice of organisms in each vegetative strata is plotted
versus increasing cover density (sparse = 1; dense = 5). Details of
how the percent abundance was weighted and of the other calculations
may be seen on p. 41 in Edgar (1971).
Dense grass, other ground layer vegetation and foundations ot
buildings, support the highest populations of P. piuio . The sum of
abundance-cover densities 3, 4 and 5 in grouncflayer accounts for 84%
of total. In other strata, P. opilio is high when shrubs and brushy
vegetation are very sparse ( 1+2 = 94 ) . The characteristic upper
canopy seldom is dense to moderately dense (1+2 76%) when supporting
high populations of P. oplllo . In the majority of instances there are
no tiees (1 53%) present where P. opillo is in greatest abundance
(rigure la).
The habitats of most opihionids can be characterized not only by
density of vegetative cover but also by dominant tree species of the
upper canopy. For P. opilio the unusual categories “buildngs,” and
“grass’ need to be added. Figure lb indicates that buildings were the
most frequent dominant “upper canopy” In 43% of thc- sites where P.
ooiIto was collected. Maple and elm canopies were dominant but l2ss
frequently so. Above average abundances of P. opil io were encountered
172
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— ..t n.fl’ — — ..-_ _—r__•___ —. — ——— —v— -.- ——— —
in aspen, grass and around buildings. This species was never or
seldom collected in everal dominant canopy species. Since very few
collections of P. opilio were made where aspen was the dominant upper
canopy this high abundance value may be considered mainly the result of
small sample size (Figure ib).
=
I
% .

--- K
+1.5
U
.l.o I
O
C
0
a
-1.0.!
0
Maple Elm h ce r Ash bI kMI$ Bldg. w°”
FIGURE la & b. (a) Abi ndance-cover profile plotting weighted
percent abundance of Phalanglum pilio* versus Increasing cover density
(I = sparse; 5 = dense), and (b) Relative occurrence and abundance of
Phalangium o ilio in the major canopy groups. Under5tory cover, when
associated with buildings was assigned a value of 1. **percent of
collection sites. (Modified from Edgar, 1971)
901 • Upper canopy
I £ Under tory
aol • Ground layer
* 40.
8
30
20
IC
0
45.
40
Ca)
35.
3o
Mean - 2.52
*
15
I C
5 ,
=
-
173
-------
By comparison the habitat in which Leiobunutn vlttatum (Figure 2a
and b) Is most abundant is characterized by moderately dense to dense
upper canopy (3+4+5 = 80%) and ground layer vegetation (3+4+5 = 86%).
Understory is sparse (1+2 = 46%). All groups of dominant canopy species
are colonized by 1. vittatum (Figure 2b) with no group supporting a
population density clearly greater than any other group.
50
40
*30
a
C
C
U
I-
l
20
l0
(I
30
25
20
*
*i 15
lo
S
0
FIGURE 2a & b (a) Abundance—cover profile plotting weighted
abundance of Lelobunum vittatun * versus increasing cover density
(1 = sparse; 5 = dense), and (b) Relative occurrence and abundance
of Leiobu,ium vittatum In the major canopy groups. **percent of
collection sites. (Modified from Edgar , 1971).
• Upper canopy
A, Underetory
• Ground layer
I
LU)
2
3
C
a
0
E
C
0
cedar birch
Cb
Misc
174
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The abundance-cover profile of the forest opilionid, L. longipes
shows how comparatively protected it is from moisture and light
extremes (Table 1). Lelobunum lon9ipes has a three strata total of
267 (300 possible) as compared with 220 for L. vittatum and only 122
for P. opilio . This suggests that shade Is ense and the soil is at
lea&E mesic to support this density of vegetative cover where
1. longipes is most abundant. The non—anthrophilic, ecotonal L.
ittatum is found most abundantly in close proximity to rather dense
vegetative cover. The anthroph le, P. opllio , has a stratal total
dramatically lower than both L. vittatum and L. longipç .
TABI.E 1. A comparison of habitats of three opillonids using
cover-abundance profiles of Edgar (1971)
1) Species, 2) A
ssociation with man
and 3) Habitat
Stratimi
1)
2)
3)
Leiobunum
•Iongipes*
Non—anthrophilic
Protected
Leiobunum
vittatum
Non-anthrophilic
Ecotonal
Phalangium
opilio
Anthrophilic
Exposed
Upper canopy
3+4+5 = 97
3+4+5 = 80
3+4+5 = 24
Understory
3+4+5 = 96
3+4+5 = 54
3+4+5 = 14
Ground layer
3+4+5 = 74
3+4+5 = 86
3+4+5 = 84
267
220
122
*Edgar, 1971, Figure 6, p. 44
On the basis of habitat analysis alone P. opilto and L. ! .‘ittatum
might be expected to be more able to withstand env ronmental extremes
than L. longipes . Further, P. opillo should have additional physiological
and/or bihavioral attributes over L. vittatum to exist successfully in
its physically harsher environment.
PHYSIOLOGICAL ECOLOGY
Light and activity
In a light gradient both male and female P. opilio occupy a zone
of higher intensity than two other opilionid species (Figure 3),
Leiobunwi Qplitum Weed and L. vittatum , which are round in habitats
contiguous with that of P. QpJiio in Michigan (Clingenpeel and Edgar,
1966). The order of dark-to-li fIt preference is predictable on the basis
of the usual habitat of each species. The habitat of L. politum is
typically denser and supplied with a more constant source of moisture than
175
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L. vittatum , and likewise, L. vittatum occupies a more protected
position in relationship to sunlight than does P. oplio .
: P
20 •‘ ‘• \ MALES LVITTATUM
‘° L.POLrTUM
z __________________
< 0 TV
P OP1LIO
• 52 20 FEMALES
• •kM10 12 2PM.4 5 5 ID 12
TIME OF DAY
FIGURE 3. Light intensity preference of three species of
phalangids In a light gradient. Dots Indicate the location of
individuals in a light gradient.
In nature, males are generally more conspicuous. This Is borne
out in the laboratory gradient by the fact that the males of all three
tested species generally were found in a higher light Intensity than
f nales (Figure 3).
From these data there appears to be no c sns1stent reaction to
light on the basis of time of day. However, another study (Edgar and Yuan,
1968) indicated that there is more activity by both sexes of P. opllw
during dusk and darkness and relative Inactivity in daylight tFigure 4).
Periods of virtually no activity closely parallel times of the day
when light intensity Is the greatest. Ninety percent of total activity
occurred between 6 p.m. and 6 a.m. In its natural, relatively exposed
habitat this activity pattern should allow P. opilio maximum conserva-
tion of body moisture since It avoids daily thuperature extrenes and
is most active when ambient humidities are the highest.
176
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>
I-
U
4
F-
z
L i i
1 .)
L i i
RM.
FIGURE 4. Averaged activity of Phalangiuni opillo in nornial
The general pattern of inactivity during daylIght and activity
during darkness is seen in several species of Lelobunum and P. pj3io
(Edgar and Yuan, 1968). Activity was measured in the laboratory by
tallying the number of times the animal walked the length of an activity
chamber. DUring periods of activity, approximately 6 p.m. to 6 a.m.,
P. oplhlo is conspicuously more active than all seven species of
Leiobunum tested (Table 2). It travelled 25 tImes more distance than
the ecotonal L. vittatun and forest L. longipes . This considerably
elevated activity level suggests that P. oufflo does not have to depend
on imobihity and seclusion for protection against its enemies but
rather can move about more freely in search of food, mates and protecHon
from the deleterious aspects of its physical environment.
25
— FEMALE
$—MALE
AM.
6-9 9-12 12-3
light.
3-6 6-9
177
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TABLE 2. Comparison of mean total activity per day by Phalanglum
pp ilio , and seven species of Leiobunu in normal 1ig’ t. (Modified from
Edgar and Yuan. 1968)
O.
L.n1
L.c. 3
L.ve. 4 L.no. 5
L.p. 6
L.vi 1
L.1 8
d
568*
449
109
26
40
31
17
17
555
317
58
54
16
13
28
27
Mean
561
383
83.5
4fl
28
22
22.5
22
Activity
Ratio
25.5
17.3
3.8
1.8
1.3
1
1
1
1 Phalangium opillo , 2 L• iobunum nigripes , 3 L. calcar ,
4 L. ventricosum , 5 1... nigropal i , 6 L. politum , 7 L. vittcitum , ,,
8 t. longipes
*Number of trips from one end of chamber to the other for all
individuals tested.
Relative humidity and survival in dry air
Opilionids in a humidity gradient appear to select higner
humlditie after a short period of orient .tion (Todd. 1949; Clingenpeel
and Edgar, 1966). Few species have need of a particular relative
humidity within 12 to 15 hours of deprivation from food and water. As
time passes and body water is depleted, they appear more sensitive to
moisture levels in the air and this is expressed by movement into
higher humidities (Edgar, 1971).
Corr.parative survival in a humdity gradient should indicate
something about both the hardiness of a species to withstand the
extremes in its environment and hardiness in relationship to other
species tested. In this respect P. opilio is comparable to 1. vit tatum
and both are much more tolerant to desiccatthn than 1. politum
(Clingenpeel and Edgar, 1966).
An extension of this measure of comparative hardiness is survival
in dry air. Adults of both sexes placed in dessication chambers live
varying periods of time. Rate of loss of water, and percent loss of
body weight are factors which affect survival time. The anin ils
surviving longer lose water slower and/or are able to withstand greater
weight loss before death. Among four spades of Leiohunum , including
L. vittatum and . politum referred to earlier, 1. vittatum survived
more than twi:e as long as the other three; P. op1li Thurvived 13% longer
than L. vittatum (Eigar, 1971) (Table 3). Considering all three
criteria, survival time, percent body weight loss and rate of body
178
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I
weight loss, .. op l1o out performed the four Leiobunuin species tested
on all counts except one (female 1. vittatum lost body weight slightly
slower than female P. optU ) .
TABLE 3. Response by five op 4 lionid species in dessication
chambers (modified from Edgar, 1971)
- —— — — __ =-t = ==— —
Survival Body wt. loss 1 Rate of body
Species time (hrs.) ( per cent) wt. loss (%/hr. )
0” - -
1. politum 18.4 38.6 40.0 44.6 2.76 1.36
L. longipes 25.1 59.1 36.7 38.1 1.67 0.83
L. calcar 37.0 47.5 43.5 45.6 1.33 1.0
L. vlttatum 56.4 116.1 43.7 48.9 0.81 0.48
P. opilio 75.6 120.0 48.3 57.6 0.72 0.52
1 ca1culat d at time of death.
Temperature tolerance
Given access to a range of temperatures, opilionids might be
expected to spend the most time in a narrower range that represents
conditions they encounter in nature. Results obtained from several
species having access to a temperature gradient for a period of several
hours appear to bear this out (Figure 5). Six opilionid species in
such a situation show mean values which appear to accurately reflect
the degree to which they are exposed to temperature influence from the
sun and evaporative cooling. The mean temperature values for Leiobunum
vitattum and P. opillo were substantially higher than three woodland
species of Leiobunum and suggest that both re well adapted to higher
sun ner temperatures. In contrast, 0. parietinus is often found on the
shadea side of cement walls where usually the humidity Is high and the
substrate is cool. Its mean temperature preference of 19.70C is to be
expected and lends further authenticity to the temperature mean for
P. opillo .
179
I
-------
Ms n
UI °C.
vjflptuiii 27,9
p3.9
*LLL 27.6
s2L z 24.2
24.3
p!!1.’;nvI 9.7
FIGURE 5. Mean temperature preferences of six species of
phalangids, based on location in a temperature gradient at successive
half-hour intervals. Limits of gradient are indicated by cross lines
at ends of time bars. Each point is the mean of 3-5 values (from
Edgar, 1971).
SUMMARY
Phalang jjjo has been reported from widely separated
regions of the world and probably is the best known species in order
Opillones. It is anthrophilic, being associated with mans disturbance
in gardens, lawns, roadsides, building foundations and fields. The
occurrence of other opilionids around man probably is incidental to
their search for food, shelter or mates.
More than one life history stage of P. o 1110 exists at a time
and the eggs develop to hatching without a col iapause. Both eggs
and young are more hardy than other species In laboratory manipulations.
Compared with that of associated opIlionids the habitat of
P. oplllo Is more exposed to broad extremes of light Intensity and
moisture. The density of vegetative cover is low. Trees seldom are
as important as grass and buildings for shelter.
In laboratory experiments involving light, water and temperature’
the performance of ,, optlio matches what would be predicted on the
basis of the natural environment of the species. It chooses higher
light intensities and temperatures, survives longer in dry air and moves
about more than associated species.
Phalangium opilio appears to be well adapted for survival around
man.
S
a
I
180
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LITERATURE CITED
Clingeripeel, L.bI. and A.L. Edgar. 1966. Certain ecological aspects
of Phalangiurn opilio (ArthropoJa: Opiliones). Papers Mich.
Acad. Sci. Arts Letters. 51:119-126.
Edgar, A.L. 1971. Studies on the biology and ... ;ology of Michigan
Phalangida (Opiliones). Misc. Pubs., Mus. Zool., Univ. Mich.,
No. 144, pp. 1-64.
Edgar, A.L. and H.A. Yuan. 1968. Locoinotory activity in Phala g um
jjio and seven species of Lelobunum (Arthropoda: Phalangida).
Bios. 39(4) :167—176.
Forster, R.R. 1947. The zoogeographical relationships of the New
Zealand Opiliones. The New Zealand Sd. Cong. 233-235.
Hoim, A. 1947. On the development of Opiuio parietinus . Deg. Zool.
Bidr. (Jpps., 25:409—422.
Kiee, G.E. and J.W. Butcher. 1968. Laboratory rearing of Phalangium
opilio (Arachnida: Opiuiones). Mich. Entomol., 1(8):275—278.
Sankey, J.II.P. and T.H. Savory. 1974. British harvcstrnen. Synopsis
of the Br tish fauna, Plo. 4. Academic Press, 1—76.
Savory, T.H. 1962. Daddy Long Legs. Scientific American, pp. 3—9.
Spoek, G.L. 1963. The Opilionida (Arachnida) of the Netherlands.
Uitgegeven Door Het Rijksmuseum van Natuurlijke Historie te
Leiden, No. 63, 1—70.
Todd, V. 1949. The habits and ecology of the British h .tvestnzen
(Arachnida, Opiliones), with special reference to those of
the Oxford District. J. Anim. Ecol. 18(2):209-229.
QUESTIONS and COMMENTS
M. . GEt LABOV : In what meaning do you use the term
“survive desiccation” — ability to lose water and survive.
or being protec-ted from water loss. (According to ny and
L.M. Semenova’s data the epicuticle of . opilio is very
thick especially on tergites).
A.L. EDGAR : I don’t have histologic data to Indicate
exoskeletal thickness or waxiness of the c;aticls. In fact,
the question could be asked ,hether death occurs from desic-
cation (water loss) or from suffocation. The answer to that
is likewise not known specifically for the opilionids tested.
181
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ACTIVE AND PASSIVE DISPERSAL OF LUMBRICID
EARTHWORMS
Donald P. Schwert
North Dakota State University
USA
INTRODUCTION
Gates (1972), through the cooperation of the United
States Bureau of Plant Quarantine, accumulated considerable
evidence to suppo-t his hypothesis that the lunibricid fauna
of northern North America represents principally species
introduced there and distributed within the continent by man.
Of the 3400 earthworm specimens seized by inspectors from
Imported plants during a 15-year period, nearly 1600 were
lumbricids, representing 16 species. Because man ’ of these
species, in addition t’ other lumbricids, are Iiolarctlc or
even “ osmopo1i a ”” (sic Gates 1972) in distribution, it is
easy to follow Gates’ (1970. 1972, 1976a) reasoning that the
present range of each reflects their transport to other
regions by man. For North America, alone, Gates (1976b)
lists 24 lumbricid species as Uexotic I the source continent
of most of these lunibricids presumably having been Europe;
transpert to North America was probably accidental, such as
earthworms trapped In ship ballast or among the roots of
imported plants.
In North America today, the dense distribution across
the continent of many of these “exotic” lumbricids (e.g.
Lumbr’tcue terreatri a L., L. ru llue Koffmelster, Aporrea-
todea spp., Oatolas ion spp., and others) precludes the
determination of the place(s) and time(s) of their introduc-
tion. Indeeu, fossil evidence (Schwert 1979) indicates that
at least one of these widespread “European exotics,” Den ro—
drilus rulidue (Savigny), was inhabiting North America over
10 000 years ago, certainly well before the arrival of
European settlers. The limited distribution of some other
“exotic” lumbricids In North America, however, clearly
indicates the general region, f not the exact time, of
their introduction to this continent. A population of the
European luinbricid Aporreatodea icterica (Savigny), now well
established in the region of an arboretum In southern Ontario,
Canada, probably originated from trees imported to the site
from England in 1971 (Schwert 1977). The limited distribu-
tion, outlined by Reynolds (1976) 1 f Lumbric?a feetivus
(Savigny) within the Saint Lawrence watershed of eastern
North America, appears to represent a species introduced to
182
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that rc . gion in one or more isolated localities decades or
perhaps centuries ago and since slowly expanding its range
outward from the valley.
Unfortunately, Gates and others have probably relied
too much on ma as the agent respo”sible for the present
lumbricid distribution In northern No th America. Certainly
while beirg a major, if not the primary, influence on earth-
worm distri utior ,. mar cannot claim responsibility for the
total distribution. We now know that endemic earthworms,
Including geophagous species, often densely inhabit the
northern Appalachians and even some deglaciated areas of the
continent; given so many thousands of years since deglacia-
tion “to eat their way” (sic Gates l976a) over these moun-
taIns 9 it is not surprising to find the endemic lumbricids
Birnastos or Eiasnoides throughout the state of Pennsylvania
and even into New York and Massachusetts.
The seemingly sedentary nature of earthwcrms is mis-
leading. In northern North America, most lumbricids are
remarkably active throughout the spring and autumn, and, in
the southern regions, winter. Whether one accepts or re-
jects Gates’ premises on their present distribution, the
wide and dense distribution of many of these species across
North America have benefited from their extraordinary
abilities at nat ral dispersal. Of the three to be men-
tioned, one is an active mechanism, while the other two
involve passive dispersal through other natural agents.
All three are in ,eed of further investigation, and addi-
tional mechanisms probably exist.
STREAM DRIFT
The moist lowlands adjacent tc streams and lakes are
often idea’ habitats for many ,pecles of Lumbrtcldae. Sig-
nificant activity of these earthworms at or near the surface
occurs when temperature, moisture, and light conditions per-
mit. Inevitably, many individuals are washed into these
waterways Ir ia surface runoff resulting from rainfall and
snowmelt or from mass movements of soil during erosion, and
they can potentially be transported long distances down-
stream. Bouché (1972) noted that several species of earth-
worms inhabit only particular drainage basins in France and
hypothesized that stream drift was probably an important
factor In Influencing their distribution. Ward (1976)
applied a similar hypothesis to explain the recolonization
of a riffle area by the lumbrlcid EieenieZia 1etrru dra
(Savigny) in a Colorado stream. Although adult lumbricids
can remain submerged in aerated water for prolonged periods
(Roots 1956; Edwards and Lofty 1972), the mortality rate of
183
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Individuals must be high during stream transport due to
predation and physical battering. Nevertheless, live lum-
bricids can be frequently seen 3fl stream bottoms, and the
potential value of this drift to the dispersal of the spe-
cies involved must be considerable.
During an ar.alysls of a small stream in southern
Untario, Canada, Schwert and Dance (1979) recovered over
300 lumbricid coco ns from drift sar. ples. Of the total,
92% were found to contain ,perm and albumen or some stage
in the development 0 f the embryonic mass; these we e be-
lie ed, therefore, to be viable and potentially capable of
hatching. From identification of the cocoons, they were
found to represent at hast six geflera of Lumbrlcidae, afl
of them common to that region.
The small size and tough, s iheroidal outer wails of
these cocoons are, unlike the adult worms, ideally suited
for long and rigorous transport downstream. Their palat-
ability to fish Is unkno n, but presumably low. Roots
(1956) demonstrated that cocoons, such as those of the lum-
bricid Allolü ophoz’a chZorotica (Savigny), could success-
fully hatch while submerged, with the young also undergoing
normal growth in a submerged environment. From the remark-
ably high viability of the stream drift cocoons, their
successful hatching could, likewise, be expected in areas of
a stream where the cocoons had been deposited near the mar-
gin or in the bottom sediments of pools. Consequently, these
transported species would become established in lowland areas
downstream of their original source.
Since this study, numerous cocoons have been isolated
from other streams in Canada and the United States, and this
phenomenon appears to be widespread. Further investigation,
however, wll be needed to determine the degree in which such
dispersal may have actually influenced lumbricid distribu-
tion.
MASS EMERGENCE
In northern North America and Europe. the mass emer-
gence of lumbricids during periods of heavy rainfall or dew
is a common, yet poorly studied, phenomenon. Such emergences
were first described by Darwin (1881) and were subject to
casual analysis by Friend (1924). Because this occurrence
is more often witnessed in areas affected by human civiliza-
tion, the deaths of often hundreds of thousands 0 f Individ-
uals stranded on drying streets and sidewalks have led to
popular conceptions that the dying earthworms were Ill,
poisoned, or drowned. Lankester (1921). Merker (1926, 1928),
1811.
-------
Nishida (19.5l) and others, in search of a more scientific
explanation, proposed that through chemotaxis the worms are
forced to the surface as the oxygen supply to the soil Is
cut by rain saturation; Shiraishi’s (1954) experiments failed
to demonstrate t .is. Doeksen (1967) proposed that similar
types of “migrations” observed in wet, foggy greenhouscs
result from behavioral changes in the worms resulting crow
increased hydrogen suiphide concentrations in the soil.
.. vendsen (1957), without seeking a chemical factor to explain
surface activity, proposed that some species actively search
for food sources during rain; in his experiments, he noted
that several luinbricid sr ecies aggregated to dung through
movements at or near the surface during moist conditions.
However precipitlLtion actually triggers such surfac-
ing, these mass emergen:es are so predictable in occurrence
and so massive in scope, usually affecting several species
at one time, that an anditional hypothesis may be proposed
with respect to the foflowing two points:
1) Mass emer nces occur primarijj during periods of
cool, moist ieatner. Friend (1924T noted emergences
in England occurring only during the autumn, winter,
and spring months. In North America, soil tempera-
tures taken at a 3-cm depth during ernergences in
Ontario, Canada and in North Dakota, U.S.A. have
ranged from 2° to 9 C. When soil temperatures rise
above this range, as in the summer months, this
phenomenon rarely occurs. A notable exception to
this behavior is L. terrea*rle , which is known Lo
surface for food and mating throughout the summer
months.
2) Before human civilization, the original habitats
of the Lumbricidae were primarily forests and forest
meadows . Unfortuna iTy, as prev ously note 7 most
observations of mass emergences have been in urban-
ized areas, where the earthworms are trapped by man-
made structures and quickly killed by desiccation and
sunlight. This surfacing phenomenon, however, also
occurs on the forest floor, where the surfaced
individuals are protected from desiccation, sunight,
and large predators by the tree canopy and by litter
cover. During periods of cool litter temperature and
sufficient moisture to permit respiration, the lum—
bricids may enter the litter and migrate through it
rapidly and for long distances without the need to
burrow. Contrary to popular belief, surfaced individ-
uals can rapidly re-enter the soil in areas where it
Is sufficiently porous.
With this combination of proper soil temperatures
sufficient moisture from fresh precipitation, protection from
185
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sunlight and predators, and the loose litter medium for
enhanced mobility, free and rapid surface dispersal can
occur in relacive safety. Such a behavioral response is
advantageous to the species involved as it: 1) no longer
limits the active outward dispersal of geophagous species
to burrowing a’:tlvity; 2) decreases population pressure
during periods of peak reproduction and, therefore, food
and space competition in areas o high earthworm density;
3) rapidly expands the range of the species ir’volved;
4) enhances the possibility of genetic exchange among
scattered populations of a species. The direction of
dispersal movement appears to be random, even on sloping
surfaLes, and inevitably many individuals are washed into
streams, potentially to colonize downstream areas.
In northeastern and nnrthcentral North America,
nearly all of the established species of Zumbrieu3, Eieenia
A 1 olo both oi’a, Octolci ions Apor3 ’ectodea, D6nd?o7 zena, and
Dendrodriiza can be observed surfacing during preper condi-
tions at cool times of the year. Several species of Bimas—
tos are, likewise, known to surface. Sub-aquatic Lumbricidae
inhabiting saturated environments, such as Eisenoide3 l ’nn—
bergi Michaelsen and Eieenielia tetraedx ’a are, as would be
predicted, unaffected by the precipitation tri qer.
TRANSPORT BY OTHER ANIMALS
No published records apparently exist of earthworm
individuals or their cocoons accidentaly being transported
by birds or mammals. Cocoons could be carried substantial
distances if trapped in mud on birds’ feet. Live inoividuals
carried by predaceous birds are, from observat on, occasion-
ally dropped in midflight and could potentially reburrow.
Certainly some of the irtriguing earthworm records 0 f James
R. Philips (unpublished data, personal communication 1973 -
1975), such as Immature £umrc a terr itrio apparently
established in a kestrel (FaLco eparverizw 1.) nest position-
ed on a tree l 4 mb 6 m above the forest floor, are attribut-
able to avian transport. Whether such passive transport has
profoundly affected earthworm distribution is impossible now
to determine; in all probability, it has been of marginal
significance.
SUMMARY
Although a number of lumbriciu species now inhabiting
North America were Introduced there by man, human transport
cannot alone account for their remarkably widespread estab-
lishment across the continent. Rather, many Lumbricidae are
186
-------
- ‘fl ¼1P - --
capable 01 rapid dispersal through active or passive means
other than by burrowing or by man. Dependent upon seasonal
conditions, random movement of some species, often ‘ n a mass
scale, occurs at or near the surface during periods of rain-
fall or of heavy dew; atmospheric and soil tem ,eratures
appear to be key factors In determining periods and size of
such movements. Downslope dispersal of the Lumbricidae is
facilitated by stream drift, especially durinci the cocoon
stage in which up to 9O may remain viable after drifting
ofter’ considerable distances. Avian transport of individ-
uals is a small, but po entia11y siqnlficant mechanism of
nassive dispersal.
LITERATJRE CITED
Bouché, M.B. 1q72. Lombriciens de France, écoloç ie et
syst€matique. Inst. Nati. Rech. Aqron. Paris. 617 pp.
Darwin, C.R. 1881. The formation of vegetable mould throuqh
the action of worms, with observations on their habits.
Murray, London. 326 pp.
Doekse,i, J. 1967. Notes on the activity of earthworms. V.
Some causes of mass migration. Meded. Inst. Biol.
Scheik. Onderz. Landbouwgewassen. 353:199-221.
Edwards, C.A. and J.R. Lofty. 1972. Biology of earthworms.
Chapman and Hall, Ltd., London. 283 pp.
Friend, H. 1924. The story of British annelid3 (Oligo-
chaeta). Epworth Press, London. 288 pp.
Gates, G.E. Miscellanea megadrilogica VII. Mega-
drilogica I(2):l-14.
Gates, G.E. 1072. Burmese earthworms - an introduction to
the syctematics and biology of megadrile oligochaetcs
with special reference to soutneast Asia. Trans. Amer.
Philos. Soc., Philadelohia. 62(7):I-3 6.
Gates, G.E. 1976a. More on earthworm distribution in North
America. Proc. Biol Soc. Washington. 89(40):467-476.
Gates, G.E. 19Thb. More on oligochaete distribution in
North America. Megadrilogica 2(l1):l—6.
Lankester, E.R. 1921. Earthworms drowned in puddles.
Nature 107:329-330.
187
-------
Merke,-, E. 1926. Die Empfindllchkeit feucht—hautlaer here
im Licht. II. Warum kommen Regenwiirmer in Wasser1 chen
urn und warum velassen sei bei Regen ihr Wohnrohr?
Zool. Jahrb. 42:487-555.
Merker, E. 1928. Warum kommen die Reoenwi rmer bei Regen
aus de n Erdreich, und warum sterben sie in Wasserlächen?
Ber. ser.ckenb. naturf. Ges. 58:361-366.
Nishida, V.A. 1951. Zur Fraçie liber die Auslösenden Faktoren
des Auskriechens des Regenwurms bel Regenwetter. J.
Fac. Hokkaidô Univ., 6th ser. 10:23—32.
Reynolds, J.W. 1976. Die blogeografie van Noorde-
Amerikaanse erdwurms (Oligochaeta) noorde van Meksiko.
II. Indikator 8(1):6-20.
Roots, B.!. 1956. The water relations of earthworms. II.
Resistance to desiccation and immersion, and behaviour
when submerged and when allowed a choice of environment.
J. Exptl. Biol. 33:29-44.
Schwert, D.P. 1977. The first North American record of
Aporrectodea iaterica (Savigny, 1826) (Oligochaeta,
Lumbricldae), with observations on the colonization of
exotic earthworm species in Canada. Can. J. Zool.
55(1) :245-248.
Schwert, D.P. 1979. DescriptIon and significance of a fos-
sM earthworm (Oligochaeta: Lumbricidae) cocoon from
postglacial sediments in southern Ontario. Can. J.
Zool. 57(7):1402-1405.
Schwert, D.P. and K.W. Dance. 1979. Earthworm cocoons as
a drift component in a southern Ontario stream. Can.
Field-Nat. 93:180-183.
Shiraishi, K. 1954. On th chemotaxis of the earthworm to
carbon dioxide. Tóhoku Univ. Sd. Rep., 4th ser.,
20:356-361.
Svendsen, J.A. 1957. The behaviour of lumbricids under
moorland conditions. J. An m. Ecol. 26:423-439.
Ward, J.V. 1976. Lumbricid earthworm populations in a
Colorado fountain river. Southwest. Nat. 21(1):71-78.
188
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QUESTIONS and COMMENTS
M.S. GHILAROV : The cause of emergence of earthworms
on the surface is the deficiency of 2 after heavy rains in
stmuuer in the soil. In spring after melting of snow earthworms
don’t emerge on the surface, whereas after spring flooding
they don’t die off, but. after s* mi er floodings of rivers
they do perish. These facts were shown still in the 20’s by
Berciemisher and Clietyrkina. Certainly emergence on soil
surface after sunmter rains allows the active dispersal and
mixing of population; this has been stressed already e.g. by
erel and by Xvavadze.
Passive dispersal along slopes by rains is described by
Atlavinyte, whereas in arid territories of Central Asia earth-
worms in natural conditions are known only along river benches
(and subsequently along irrigation channels. So previous data
of soviet zoologists are in accordance with your conclusions
and support them.
. TOMLIN : There are examples of . terrestris rising
and dispersing after rainf ails in July and Augus (3 cm soil
temperature 12°C) though greatest emergence admittedly occurs
April-June and Sept-Oct. I particularly refer to the Windsor
Airport situation. I disagree that j . terrestris dispersal
is limited to “cool” soil temperatures.
D.P. ScRWERT : Of all the peregrine species discussed,
only Limibricus terrestris regularly feeds on the surface.
Surface feeding for this species does occur in mid—summer.
when soil temperatures are greater than 9°C. I am surprised,
however, at learning of a mid—summer mass phenomenon causing
problems at Windsor.
A. CARTER : To what degree does the availability of areas
for shelter affect the amount of earthworm movement after heavy
rains? In flat grassy areas (city lawns), soil may become
readily water—logged and earthworms have no hwmnocks for shelter.
h.P. S RWERT : I have no quantitative information on which
to answer this question. For reasons that I have just out-
lined, however, we could expect that the lack of shelter in
such areas would le&d to proportionally far greater mortality
than in forests.
C. . EDWARDS : You give the impression that the surfacing
of earthworms after rain is confined to Lumbricidae in cool
weather. It is common in hot weather in the tropics by
Eudrilidae and Megasco].ecidae.
D.P. SCaWERT : I’m aware that other families do surface,
however, I am not certain whether the same behavioral response
for tropical sartbworms is involved.
D. MAL lOW : What studies, if any, have been done on rates
of movement by itimbricid worms. ,ith regards to their enter-
gences during fall and spring rainf ails?
D.P. SCEWERT : At this time, I know of no such studies.
My own research efforts in Nc.rth Dakota are inhibited by low
earthworm densities and limited rainfall in this part of the
continent. 1b9
-------
HORIZONTAL MOVEMENTS IN A NATURAL POPULATION OF
Entomobrya socia IN A LAWN
Elizabeth S. Waldorf
Louisiana State University
USA
Horizontal movements within a population, or mixing, are of general
interest in both population ecology and population genetics. In spring—
tails in addition tc affecting individual activities and population para-
meters, movements influence the dispersal of microorganisms.
As a part of a study of Entomobrya soda in southern Louisiana, I
have examined horizontal movements in a natural population. This epigeic
sp. ies is accessible for sampling and abundant in lainis composed pri-
marily of St. Augustinegrass ( Stenotaphum secundatuni (Walt.) Kunze).
Using sticky plates as snares I have captured the animals entering an
area of lawn. Thase data have been compared with estimates of population
density obtained by suction sampling at about the same dates.
METHODS
Square plates of plexiglass 25 cm on each side were generouqly
coated with TamglefootTh, a fruit tree grease. Placed flat in one area
on the lawn, these captured insects that alighted on them. Two experi-
mental designs were utilized. Initially 6 plates coated on both sides
were set out at 10 AM. At 4 hour intervals thereafter one was recovered
until the last was retrieved at 10 AM the following day. This procedure
was followed from mid—April to mid—May 1978. As no Entomobrya were col-
lected on the lower plate surface and more replicates were needed, a
second design was substituted. Three plates coated on only the upper
surface were distributed, retrieved 2 hours later and 3 new plates set
up. To reduce the stimulating effect of disturbance, I did not step
closer than 40 cm to a plate. This procedure was followed for 24 hours
on six dates from May through mid—July 1978 (Table I).
Animals captured were counted, the samples from the first procedure
pooled, all (700) individuals were measured, and the presence or absence
of gut contents (visible through the translucent body wall) was recorded.
For comparison, standard samples were collected with a household
vacuum cleaner with a filter fitted over the nozzle. The filter was moved
over the wire screen within a wooden frame (19.3 cm X 30.4 cm) to collect
a sample. Four sites were sampled between 4 PM and 6 PM on the dates of
sticky plate captures or near to them (Table 1). Estimates suggest that
this method removes about .7 of the Entomobrya present, that is, it is
about lOX efficient. The data were utilized without correction, Animals
were measured and the presance or absence of gut contents was determined.
190
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RESULTS
Individuals that moved hor 4 zontally were of large body size.
Figure 1 depicts the numbers in four sizc classes with the general popu—
lation shown below the lines and mixers above. Mixers represer&.ed about
the upper 50% of the size range of the population present. Large animals
dominated even in mid and late June when juveniles were numerous. Thii i
s zggests that most were adults, dfl , because female springtails tend to
be larger than males, that many were females.
The translucent body of Entamobrya in preservativc allowed the
presence of absence of gut contents to be recorded • in Figure 2 the frac-
tions empty are illustrated by bars with dots for immigrants and b s with
slanted lines for the general population. Of the mixers about twice as
many had empty guts as animals of the same size fro—i suction samples. As
fasting characterized the interval preceding and following ecdysis, the
data suggest that many of the izunigrants were near the time of ecdysis.
For Tomocerus minor and Orchesella cincta , DeWith and Joosse (1971) found
that locomotor activity increases immediately after ecdysis.
TABLE 1. Numbers of Entomobrya soda caught on sticky plates and in
suction samples. Two standard errors are given in paren-
theses.
Immigrants Standard Ppulations
Total — Suction —
on x/day Sample Total x per Sample
Dates Plates in 25x25cm Dates Catch (49,132 nmi 2 )
15 Apr. 5 1.4 8 Apr. 109 27.2S (25.25)
20 Apr. 9 2.6 23 Apr. 116 29 (9.2)
10 May 38 10.8 9 Nay 209 52.25 (44.6)
25 Nay 86 25.7 (3.5) 31 May 576 144 (29.6)
5 Jun. 129 43. (17.6) 5 Jun. 491 122.75 (53)
15 Jun. 64 21.3 (7.8) 13 Jun. 149 37.25 (20.3)
21 Jun. 79 26.3 (8.1) 21 Jun. 334 83.5 (53.4)
1 Jul. 224 74.7 (6.5) 29 Jun. 660 165 (96.5)
18 Jul. 66 22 (2.5) 18 Jul. 299 74.75 (28.1)
The numbers of animals moving horizontally varied with several
factors. First, time of day was a determinant producing a daily pattern
of movements. For all sa* ie dates there was a bimodal pattern with
maximum mixing between 9 to 11 AN and 5 to 9 PM (Figure 3). The two
dates (5 June and 1 July) with morning iigration extended to 1 PM were
the only two with overcast skies. A diurnal rhythm of horizontal activity
has also been described from pitfall trap data on Smithurides malmgreni .
19].
-------
FIGURE 1. The body
(shcwn above
the lines).
category.
z
0
U
‘I.
size distribution of animals that moved horizontally
the lines) and the general population (shown beneath
The numbers are the numbers of individuals in each
15 JUlIE
<.14 .142S.2S S 
-------
- •Y • • .-’ -
FIGURE 2. ?Lie fraction of empty animals among the mixers (shown as bars
with dots) and among the general population (shown as bars with
diagonal lines). The numbers give sample sizes.
HEAD LENGTH (IN MM)
3
£0
31
25 MI.1
21 JUNE
52
12
208 k’ 1 14
2
0
U
I
JULY
18 JULY
63
32
30
L6L1
49
.I4 2S .2$i3$ ) 3S ,14 25 .26i38 >.31
193
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FIGURE 3. The average numbers of imeigrants (entering area 25 cm X 25 cm)
at various times of day. The descriptive LermS refer to cloud
cover; th number; on the right are the total animals trapped on
that date.
E
U __________________________________________ _______________________________
N
K
U
N
4
w
4
2
w
I-
z
&1I
2
U I
(3
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UI
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25-26 MAY sunny
10
:
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F 1
t: 1 ki
I 1
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i ri
86
..
.•
Ii
•
H
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5-6 JUNE .v.r ait
129

I5I6JUNE sunny
:
i
i:•
1
. ...
p: . 64
21-22 JUNE sunny
79
1 2 JULY overcast
10

i;
:
WJuIhuL 1 u
224
1 19 JULY Sunny
GO
•:
5.7
7.9
a-il iii 13 3 5
noon
9.11 11-I 1 3 3—5 5.7 7.9
nudrnght
TIME OF AV
19 e
-------
... .-•—.— — I ‘Iets , ,flaa.fl.m9 ,r ..
Working in West Greenland, Kristenseu and Vestergaard (1975) found only
one peak of activity per 24 hours during the day. Bowden, Haines and
Mercer (1976) report that climbing by Collembola above the substrate
occurs primarily between 5 PM and 10 All, an int rval that includes both
the maxima of I. socia .
Season, temperature and population dens!ty influenced the numbers
of mixers per day. Figure 4k illustrates th fraction of the animals
present that moved horizontally on different dates. There is an upward
trend from April to June. The same figure depicts the 6 PM air tempera-
tures. Temperature is significantly correlated with the fraction of
mixers Cr .1892; P = .03). The points in Figure 43 show the observed
relation between the number of mixers on the vertical axis end population
density on the horizontal axis. Again there is a significant positive
correlation (r = .8787; P = .0018).
Because as the seasons advance both the temperature and population
density increase, it is of interest to determine which exerts the effect
on mixing. By a maximum r—square improvement procedure, density was
found to account for 77.2 percent of the variation. The linear equation
T —5.93 + .303X, illustrated by the line in Figure L., best describes
the relation between the number of mixers and population density.
The average number of mixers per day (per 25 cm x 25 cm) ranged
from a minimum of 1.4 on 15 April (the first sampling date) to a maxi-
mum of 74.7 on July (Table 1). These are associated with estimated
population densities in the same area of 35 on 8 April and 165 on 29
June. Thus from 4 to 45% of the animals present are estimated tc have
moved per day.
The pattern of nix big by !• socia in the days after rainfall is
presented in the upper half of Figure 5. The vertical bars show plus or
minus two standard errors of the means. Two significant peaks of mixing
follow rainfall. In SE England, Bowden, Haines and Mercer C 1976) found
that the number of climbers increased after rainfall. Earlier work on
! socia has demonstrated the synchronizing effect of rainfall on molting
and periods of fasting (unpublished except an abstract; Waldorf . 1978).
The fractions of empty animals from suction samples collected through
the warm periods of 1978 and 1977 are shown for successive days after
rainfall in the lower half of Figure 5 • The fractions of pharate animals
of the same body sizes are represented by the vertical bars. There are
peaks of fasting at two days and at four day after rainfall (Waldorf.
unpublished). Since I know of no laboratory evidence for fasting except
preceding and following ecdyses (see for example, Thibaud 1?uS. 1916),
this suggests that two molts follow rainfall. The peaks of mixing oc—
curing 1% and 4¾ days after rainfall coincide approximately with the
timing of molting. The absence of data for the fraction of mixers at
two days and four days after rainfall might account for the differenc,s.
The general similarity of these graphs supports the idea that animals
mix about the time of ecdyses.
195
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FIGURE 4. A)illustratea 6 PM temperature and the fraction of mixers on
suce .eeive sample dates. The points in B) represent the relation-
ship observed between number of mixers and general population
density. The equation is illustrated by the line.
I
U i
‘C
2
0
I-
U
U.
NO. IN SUCTION SAMPLE
196
-------
5
K
z
0
I-
U
4
I ’
C
E
e
p.
S .
z
0
I
4
5 -
z
0
I-
DAYS AFTER RAINFALL
FIGURE 5. The relationship of the fraction of mixers, the fraction empty
and the fraction pharate to the timing of ranfall (R). The ver-
tical bars show plus or minus two standard errors of the mean.
The fractious empty are for large animals from 20 va m collection
dates in 1978 and 21 in 1977. The numbers give the sample sisea
in which pharate animals were observed.
R 2 4W
2 4 10
I
-------
DISCUSSION
The failure of the lower surfaces to catch s aringtails is evidence
that locally the grease has a repellant effect. Those animals trapped
probably come from outside the range detectable by their chemoreceptors.
This suggests that all jumped onto the traps either spontaneously or
following stimulation. Consequently, the numbers caught estimate imm-
igration front beyond a minimum distance and underestimate the total
numbers entering the area which would include Lhose that walk in.
The data on the general population from 2he suction samples also
underestimates the actual density. The unknown correction factor should
take into account factors that influence sampling efficiency and those
that influence the number of animals present. Because both the measures
of mixing and density err in the same direction, the ratio of the two is
more accurate. As the suction samples include many individuals, neither
the distribution of gut contents nor the distribution of body sizes viU
be altered substantially by further increase.
The data indicate that immigrants are adults near the time of ecdyses.
As a consequence of its empty gut, the lighter weight immigrant might
travel further. The new microhabitat will provide a different foot supply
and affect reproduction. Both the immigrants and residents have access
to new sources of gametes with the advantages that genetic variation con-
fers. Females of Sinella curviseta in laboratory culture cannot retain
sperm through the molting process; they pick up sperm and oviposit early
in certain intermolts (Waldorf,1971). If E. socia is similar and conditions
are favorable, by moving near the time of ecdysis many female immigrants
can immediately utilize sperm from new associates to oviposit.
Some euedaphic springtai. have diurnal cycles of vertical movements
(Leuthold, 1961). My preliminary observations suggest that these characterize
Entomobrya socia . Individuals were not visible to an observor at 4 P14, but
were visible ‘when the habitat was next eiamined at 7 PM. The time of t.pward
movemant coincides with a peak of horizontal immigratiou. After moving up-
ward some animals tend to move laterally. Horizontal movements occur in in-
tervals between periods of Lemperature extremes and in tiiues that avoid the
low air humidity characteristic of mid—afternoon (2 to 4 P14).
Population density was the primary variable that influenced the
number of mixers per day. The linear relation depicted in Figure 4B
suggests that below a density of about 20 individuals per sample (49,000mm 2 )
no mixing occurs. In two years of population sampling this density or a
lower density characterized from January through March of both years and
July through December of 1977 (Waldorf, unpublished).
More data on mixing would allow an evaluation of the ecological re-
lation of mixing to population density. How does the fraction o mixers
vary with increasing population density?
198
-------
By synchronizing molting, rainfall ind2rectly affects the timing
of most mixing. It tends to synchronize imnig ation. The bloom of
bacteTia that follow rainfall posskbly supplement the diet and acc-
elerate the breakdown of other organic foods. As a consequence imm-
igrants might be more likely to find an abundance of available food.
CO 2 experimentally introduced stimulates increased horizontal movement
in epigeic species (Joosse and Kapteijin,1968). Since a burst of CO 2
is generated by microbiol activity shortly after rainfall, natural
O2 might stimulate the peak of mixing following rainfall.
SUMMARY
Ihen individuals of K. socia that moved horizontally in thcir
natural habitat were compared with individuals of the general population.
the mixers .ere found to be of large body size and more likely to have
empty guts. The numbers of mixers varied through the 24 hour cycle with
maxima at 9 to Ii AM and 5 to 9 PM. The number per day was dependent
primarily on population density. Two peaks of mixing occur in the days
following rainfall; these coincide approximately with peaks of fasting
end moltir.g in the general population.
LITERATURE CITED
Bowden, 3., I.E. Haines and D. Mercer. 1976. Climbing Collembola.
Pedobiclogia 16:298—312.
DeWith, H.D. and E.N.G. Joosse. 1971. The ecological effects of
moulting in Collenibola. Rev. Ecol. Biol. Sol 8:111—117.
JoosseE.N.G. and .1.11. Kapteijn. 1968. Activity—stimuLating phenomena
caused by field—disturbance in the use of pitfall—traps.
Oecologia 1:385—392.
Kristcnsen, R.M. and . Vestergaard. 1975. Dognaktivitet under
arktiske soerbetingelser has springhalen Smiuthurides malsgreni
Tullberg (Colleinbola). Entomologishe Meddelelsi, 43:21—32.
Leuthold, R. 1961. Vergleichende Untersuchungen der Tierwelt yen chiendener
Wiesenboden iz oberbayenischen Raum, unter besonderer Berucksichtigung
der Colleabolen. Z. angew. E:it. 49:1—50.
Thibaud, 3.—M. 1968. Cycle d i tube digestif bra de l’intermue ‘ hez
lea Hypogastrunidae (Colleinboles) epiges et cavernicolea. Rev.
Ecol.. Biol. Sol 5:647—655.
Thibaud, 3—11. 1976. Relations chronologiques entre lea cycles du tube
digestif et de l’appareil genital ions de l’interwue des Insectes
Collemboles. Rev. Ecol. Blob. Sob 13:191—204.
Waldorf, E.S. 1971. The reporductive biology of Sinella curviseta
(Collembola:Entomobryidae) in laboratory culture. Rev. Ecol. Biol.
Sol 8:451-463
Waldorf, E.S. 1978. Rainfall, ecdyais and fasting in a natural population
of the springtail, Entomobrya socia . Bull. Ecol. Soc. Amer.
59:116 (Abstract). —
199
-------
THE EFFECTS OF TRAMPLING ON THE FAUNA OF A FOREST
FLOOR.
I. MICROARTIcROPODS
Irene Garay, Jorge Cancela Da Fonseca and Patrick Blandin
Ecole Nonnale Superieure
France INTRODt CTION
Perigrban forests have an important social function
as recreation ateas . However, soil structure and .iifc:,espe—
cially, are sometimes seriously troubled by trampling effec-
ts. So, it i of importance to have ecological indicatort
able to give us information on the evolution of a disturbed
edaphic ecosystems
To appreciate pollution effects, investigations have
been carried out not only on Lichens and Bryophytes (Gilbert
,1970), but also on Macrofauna (Novakova,1969; Gilbert,1971)
,and Microarthropods (Lebrun,1976; Bolle et.al.,1977) . On
the other hand, a limited number of studies have been concer-
ned with trampling effects in forests (Liddle1975).
The atm of the present study is to analyse the ela—
tionship between Nicroarthropods and 5O i uodifications un-
der trampling influence . According to its role n soil dj—
namics and its high specific richness and density,studie3
of this fauna may give a more precise and complete infc’.ma•-
tion on the perturbation level,than any abiotic factor of
the ecosystem
Study area
The work was carried out in a section of the Fontai—
nebleau Forest. near Paris, which is frequently visited by
tourists . The area is located along a road,in front of a
parking lot, and is used for picnics and recreation. Trees
are beecbes (Fagus silv’atica L.), and oaks (Quercus sessi—
1ifZo .a Smith); near the road there are also a few pines
(Pious silvestris L.).
METHODS
Soil analysis
Three parameters were distinguished: humidity,orga—
nic matter and porosity. Sampling was made 0 along give rows
parallel to the road and 10 m. apart.Row n 1 was at 5m from
200
-------
- - -
the road and under the pine trees, In each row fiye cilindri-
cal sample units were taken (diameter 5 cm.). Where a l’olor—
ganic horizon (U) existed,it vas ‘emoved
Each a mple unit was immediateiy weighed and it9 he—
igth was measured; after drying at 85 C to constant ve gth,
humidity ias calculated. The organic matter was measured by
the Anne method on the fine particles (less than 2 mm.). De-
bris greater than 2mm in diameter was weighed in order to es-
timate the total amount of or 6 anic matter. Estimation of po-
rosity was made according to Duchaufour (1960). As the soil
lies on eolian sand, the rea’ soil density was calculated
from the sand density, corrected by taking into account the
total organic matter concentration
Xicroarthropods sampling
The Microarthropods sampling realized on the 9th Ja-
nuary 1978, was made along six rows parallel to the road and
lOm. apart,except for the sixth row which was only 5m. away
from the fifth. In each row, five sample units were taken
(diameter 5cm.). The L and F layer as well as 5cm. of soil
wire separated
Microarthropoda were extracted in a high gradient ex-
tractor. After extractior, litter was dried at 85C to cons—
iant weigth. The soil was treated as before in order to me—
sure the organic matter concentration
RESULTS
Station ca-racteristics
Results concerning the soil are summarized in figure 1,
tables 1 and 2. As there are pines and patches of grass along
the road, the border row (row 1) is not comparable to others:
here the soil shows a mor humus (figure is). For this reason,
results from this row are not taken into account in the co-
rrelation analysis
The most distinctive parameter of each row is humidity
(gee table 1). It is well correlated with porosity and the a—
mount of soil organic matter as well as the total organic ma-
tter (table 2)
Porosity presents a threshold at the level of row four
in which it reachs a normal value (53 to 65%) obtained for the
same substratum in the Fontainebleau Forest (Faille,1977).
However,for those normal values of porosity the eon—
centration of soil organic matter is significantly higher.
201
-------
HO _____
sii XXY’ A13 B
Tc i
Li LJi
a) The Border (Row J) b) High Degradation
Zone (Row 2)
Humidity 18.5±3.6* Humidity = J7.2±0.9*
Porosity — 57.4±3.0* Porosity 45.6 2,J*
Soil Organic + Soil Organic +
Mattel = 4.7 -1.3* Matter — 2.5—0.5%
(Row 3)
Humidity — J5.7±J.7*
Porosity = 47.9 2.J%
Soil organic ÷
Matter — 2.9—0.3
2 3
5-7.
11
18-19
40.
57.
cm
L
±1
LLL
-1--I-
All
A12
61
Bf
C) Transition Zone
(Row 4)
.4.
A
B
C
Humidity = 24.3;3.8t
Porosity 57.6-2.4%
Soil organic +
Matter 4.1—0.7%
17.
32.
42.
57.
c l i i
I!
LJ LJ ..
— —0—
0
— . ---
A12
A13
Cl
C?
C3
jjjj ‘:
d) Mosaic Zone (Accu-
riuii’tion spots)
(Row 54.
Humidity = 34.7;J2.0 %
Porosity = 58.2—4.2%
Soil Organic +
Matter =
A
FIGURE 1 . Soil profil8 — Humidity,porosity and level of or-
ganic matter.
-------
in row 5 than in row 4 (figure lcd) .Values for row 4 are lo-
ver than the usual ones for a n od r humus in the Fontaineble—
au Forest : 4.7X (Robin,1971)
TABLE 1 - Comparison ot numidity,porosiz.y and organic
matter concentration between the rows (R) . Nonparametric U—
test. O:no significant; :signi icant; 4:very significant.
R 1 R 2 R 1 R 3 R 1 P R 2 R 3 R 2 R R 2 R 5 R 3 R 4 R 3 R 5 R 4 R 5
Humidity
44
44
44
44
44
44
4
44
44
44
Porosity
44
44
0
0
4
44
44
44
44
0
Soil Orga-
nic Matter
44
44
0
0
0
-
44
44
44
44
44
-
Total 0:9 5-
nb Matter
. .-
••
Q
44
44
44
44
0
TABLE 2 - Correlations between humidity,porosity and
organic matter . a = a—error . The estimates ver mada from
the raw data . n = 20
Soil Organic Total Organic Porosity
Matter
Matter
(% of soil dr
( of soil dry
( )
weigth)
weigth)
Humidity
r = 0.94
b = 0.14
r = 0.96
= 0.27
r = 0.82
b 0.47
(* of soil
a = 0.87
a =—0.26
a 42.19
dry weigth)
j6
a=
a jo_8
a =
Porosity
r=0.83
0.21
r=0.85
b = 0.4)
( )
,____________
a =—7.26
a = ioT —
a = J3 82
— a jo
According to these observations,four different situa-
tions can be distinguished
i) The border (row one); somewhat comparable to rows
4 and 5 for porosity and concentretion of organic matter but
with a different humus type (figure la).
Li) The high degradaticn zone (rows two and three) ;
with a porobity lower than normal , a very low concentration
203
-------
TABLE 3 — Estimates of the densities (md/rn 2 ) by rows and ,y group of Microarthropods
2 D 2
The relative errors (er.) were estimated from : S + from Berthet et al.(1970) 1
2 2,2 2 2 é D K 2
D L.2 ., or D .L.. according to the relation between ,E and a and the values of k
I ii
(Elliot,1971) . High relative errors are due to the extremely low densities and to the
proportion of zeros in the sample-units
N
Row)
Row2
Row3
Row4
RowS
Row6
Prostlgmata
3,107 f26
560 209
560 ± 209
3,107 626
12,783±4,774
12,783±4,774
Ac .tridiae
6,987 867
6,987 867
6,2)3 944
6,987 ± 867
25,668±5,260
10,084±2,9)4
Gamas Ida
Uropoda
0
0
0
0
),630— 552
#
1,630-552
Gamas Ida Pa-
rasitodea +
Zarconjdae
7)3 185
0
0
1,120 7)2
6,264±2,389
6,264±2,389
COllembola
rthrop1eona
1,767 ± 759
1,767 759
),767 759
11,204±5,175
65,648±2(3085
65,648±24085
Co.Llembola
Sympliypl eons
9,167±2,052
998 ± 218
J,73) 594
1,732 594
306 ± 249
306 ± 249
Oribat lda
775 ± 286
775 ± 286
775 ± 286
775 286
24,995±9,921
24,995±9,92)
-------
of organic matter and a high reduction of water content . The
absence of F layer indicates that the organic matter cycle is
upset . In factleaves are swept out from this zone during win-
ter and spring and accumulate at the level of row 5 according
to the microtopography . The low values of organic matter con-
centration correspond with the profiles: the A 11 horizon is mi-
ssing in row 2 (figure ib) and a A 11 horizon of only 1—2 cm is
observed at the level of row 3 . Tfiis zone presents a layer o
0.5—1 cm of “ery leached sand between litter and soil . Some
further drillings demon8trated other abnormalities in the pro—
files,aa superficial recasting of sand and leaching patches
iii) The transition zone(row four),with a very thin F layer.
The porosity is normal . The low concentration of organic matter
and a discontinuity,represented by a shallow layer (0.5 cm) of
leached sand between the F layer and the A 11 horizon,suggest
that the organic matter cycle is disturbed (figure id)
iv) The mosaic zone (row five) . This is a patchy zone
and we have chosen for sampling places where a cumu1ation exists.
The litter can raach a depth of 7 cm or more . The porosity is
normal but the organic matter cozacentratlon is very high: 5.9
* 1.5% (figure Id)
The mlcroarthropod communities
Quantitative and qualitative characterization
Results are summarized in table 3 and figure 2 . A com-
parative analysis of the different rows shows that the micro—
arthropod groups appears or increase in density in passing from
the high degradation zone (row 2 and 3) to the mosaic zone (row
5 cud 6) . However Collembola Symphypleona have a different pa-
ttern . In effect,their abundance decreases towards the mosaic
zone in which they are almost absent • In addition,this group
is significantly more abundant in the border row (U—test, 0.028)
The Acaridiae,98% of which belong to the Tyroglyphidae,
present the maximal density in row 5 (U—test, =O.028)
The density and presence or absence of the different
groups allow to distinguish four Microarthropod communities.
These correspond to the soil zones described before (figure 2).
1.) The border community (row one) is chara’ terized by
mphypleona and the Acaridiae (41% and 31% of the total
205
-------
0 OSTUIMTA
0
o
• G A1 N s
o
20S 0*TIDA
hi
n
I
i -

I l
hi
10*1
L
I0*
I
lOWS
I
FIGURE 2 Densities (histograms) and relative abundances
(circles) of Microarthropoda in the different rows of sam-
ples . Circle surfaces are proportional to the square root
of the total density in each row
I I
7 ORIBAT1DA species 20 ORIBAT1DA species 131 ORIBATIDA species
‘SQ I
I I
I I
I 10 -
noFlayer, __)
-a I
I I
I I
LEAVES-LITTER (L+F) cmØ
FIGuRE 3 . Relation between the numbers of Collembola—Orib —
tida (L+F) and the dry weigth of extraction leaves litter
• , 2
o row 3
• row 4
0 rowS
*rowS
0
-S
I I .
US
10
* *
4
0
0
* *1
I
206
-------
density respectively) and by the absence of the Gamasida Uro—
poda . Oribatie a and Arthropleona are present, but in very low
numbers
ii) The high degradation zone community (rows two and
three) . In this zone,the total density of Microarthropods is
ten times less than in the mosaic zone . The community can be
characterized by the dominance of Acaridiae (63% of the total
density) , by the absence of Gainasida (both: Uropoda and non—
Uropod ) and by the very low density of Oribatida: 775* 286
ind./m
iii) The transition zone community (row four) . In this
zone the Microarthropod density is twice that of the previous
zones . Arthropleona are dominant (45% of the total densit ”),
while the relative abundance of Acaridiae decreases (28%)
this is also the case for Oribatida and Symphypleona . Gamasi-
da non-Uropoda are present
iv) The mosaic zone community (rows five and six) . The
only significaist difference between the two last rows concerns
Acai idiae densities (U—te8t,u O.OO5) . The other Microarthro—
pods have similar densities in the two rows . Arthropleona re-
presents 47.8% of the total density in row 5 and 54% in row 6
The density of Ozibatida is about 32 times highe: than in other
zones and their relative abundance is 18% and 20.5% in rows 5
and 6 respectively . Gamasida llropoda are present
Relationships between Microarthropods, litter and soil
organic matter
Table 4 shows that the total number of Microarthropods
in each core sample is significantly correlated with the litter
(L + F), dry weigth and also witi; the organic matter concentra-
tion in the soil . This is not surprinsing, inasmuch as the or-
ganic matter and the litter are not independent (r=0.43 ; a0.O1).
However, the correlation between litter Microarthropod’s
number and the amount of litter is significantly higher than the
correlation between the soiljicroarthropod’s number and the or-
ganic matter r 1 >r, ; a=10 (see table 4) . This is also true
for Collembola and O ibatida alone
In a protected forest area the soil Microarthropods are
independent of the soil organic matter (Garay,uupubliahed data).
This is also observed,in a very different ecosystem,by Santos,
De Pree and Whitford (1978), but they found a dependence between
Mi roarthropods and the amount of litter . So, other parameters,
d1ffere t from the organic matter concentration,remain to be
found n order to explain the distribution of soil Microarthro—
pods
20?
-------
____ .,.....dt..r ,___.__,.__a._____.______.. ——
TABLE 4 — Correlations
amount of litter, and between
tration of organic matter, in
between Microarthropods and the
Nicroarthropods and the concen-
the core—samples. u a—error
ME
croarth
pods
pods
Oribatida -
Collerabola
by
level
:
by
core-sample
by level
(L+F) or
soil
(L+FI and soil
(L#F) or soil
Litter LI-F
‘g)
n = 25
= 0.84
b = 0.57
a =49.48
a = jo6
r 2 = 0.55
b —72.42
a -32.59
=
r 3 = 0.86
b —41.88
a =41.5)
=
Soil organic
Matter
= 24
r 4 = 0.37
b =23.94
a =39.J7
a 0.08
—
= 0.54
b —71.32
a =-)J.00
a = 0.t)
r 6 = 0.4)
b =21.75
a =47.7)
a = 0.05
Nevertheless, in our disturbed area, a more detailed
observation of data shows a threshold phenomenon in the tran-
sition zone: when the organic matter concentration is less
than 4.8Z , the number of Microarthropods is low and only for
higher values of organic matter concentration the presence of
aggregates may be observed
Litter Accumulation and Microarthropods
In figure 3,representing the relationship between li-
tter dry weigth per core—sample and number of litter Cohen-
bola and Oribatida,two dotted lines parallel to the 1—axis
diferenciate three sets of points.The first line corresponds
to the maximum amount of litter when there is not F layer_
(1.49bg) and the second one corresponds to the value X = L+F.
L+F was estimated from the value of the Jenny coeffi-
cient K,given by Lemee and Bichaud (1973) for an indisturbed
area with the same substratum and the same vegetation
K = L = 0.38
and
25 = 0.905g
where is the amount of L layer in the core—sample number i.
Thus, L+F 2.38g
208
-------
Most of the points corresponding to the high degradation
zone (rows 2 and 3) are included in the first sat of points,whi—
le most of the points of row 6 and 5 are respeetively included
in the second and third set of points . The transposition bet-
ween points of row 5 and 6 is due to the fact that litter co-
ming frcsm the high degradation zone accnmulates in the normal
region near the trampling area (row 5) . However, a point of
high accumulatiov exi3ts in row 6 due to microtopographic con-
ditions: the an unt of litter is 6.4 g and there are 407 Collem—
b31a and Oribatida
The ab ve results demonstrate that the number of Microar—
thropods is correlated with the amount of litter . Considering
only the Oribatida, their core-sample number (litter and soil)
is also significantly co 5 related with the corresponding litter
quantity: r=0 71 (e= 10 ) . It is therefo’e of interest to
study the specific composition of this group in order to compare
the different categories of samples characterized in figure i.
In the samples taken from the high degradation zone and
represented between the Y axis and the line x = 1.496g,7 species
have been found in very low density : Carabodes labyrinthicus
(Michael), Cam.isia horrida (Hermanu), Tectocepheus sarekensis
Tragardb, Phthiracarus nitenc CNicolet ), Achipteria coleoptrata
(L.), Chamobates pusillus (Ber) and Chamohates incisus
i n the samples represented between x = l.496g and x —
2.38g, 20 species have been found The Oppidae are represente4
by Oppiella inscuipta (Paoli), Oppiella minus (Paoli) . The
Brachychthoniidae by Brachychthonius impressus Moritz,Liochthn—
nius simplex (Forsslund) and LiochthOnius of. tuxeni (Forsslund).
The Suctobelbidae by Suctobelbella sarekensis (Forssl ind), Suc—
tobelbella at. perforata (Sttenzke) and Suatobelbella subcorni—
gera (Forsalund)
In the samples corresponding to litter accumulation,31
species were identified . Among them there arc 3 species of
Oppidae: 0. insatzlpta, 0. minus, Oppiella - VS (Oudemans); 9
species of Brachychthoniidae: B. impressus, Brachychthoziius
bimaculatus Willmann, Brachychochthonius suecicus Forsslund,
Brachychochthonias cf. jacoti (Evans), BrachychochthOnius ros—
tratus (Jacot), L. tuxeni, Liochthonius horridus (Selinick),
Liochthonius brevis (Michael), Paraliochthonius piluliferus
Forsslund; and 5 species of Suctobelbidac: S. cf. sarekensis,
S. . . f. perforata, S. subcornigera, Suctc’beLbella intermedia
(Willmann), Suctobelbc.Zla nasalis (Forselund)
The accumulation places are characterized by an impor—
209
__________________ I
-------
- .--—.--- - -
taut increase of specific richness, which is mostly due to
species generally considered as microphytophagous . This fact
suggests that the trophic conditions can be modified by li-
tter accumulation -
CONCLUS IONS
A comparative analysis of Microarthropod patterns in tae
study area allows us to classify them according to their reac-
tion to perturbations indu...ed by trampling
Three groups may be distinguished : i) The first group
includes species whicit seems tc be opportuuist This is the
case of Acaridiae Tyroglyphidae, a family comprising spocies
living in different environments a stored foods,human and
animal habitats, agricultural soils treated with pesticides
(Rarg, 1979) . Some Prostigmata ar eq4ally found in the high
degradated zone and are thus capable of ltving in extreme con-
ditions, but usually in small numbers
ii, A second group incl’idcs species belonging to Symphy—
pleona and Ortbat.ida aaapted to open spaces where the micro—
climate shows imçortant variations: some Symphypleona are known
for their abilIty to live in open environments thanks to various
morphological and physiological adaptatic.is (Betsch,Betsch and
Vannier, 1979) . Thisis also true for Oribatida like Camisia
horrida , Carabodes lab yrinthicus and Tectocepheus sarekensis
which we have not only found in the degradated zone of the Stu-
dy area but also in the parking lot . These species are known
for their ability to live in environments showing extremely Va—
riabic conditions
iii) The third grcup consists of species whose absence
or low densities in the disturbed zones express arious sensibi—
lities to trampling : a) a first set includes very sensitive spe-
cies which only exist where porosity,soil organic matter and li-
tter structure are normal These specieB belong to Uropoda and
the Oribatida: Oppidae, Suctobelbidae and Brachichthoniidae which
are mainly microphytophagous living in hu’2u 5 layer . b) another
set is formed by less sensitive species capable of surviving in
an environment partia]ly modified by trampling . This is the
case of Arthropleona and Gamasida non—Ut opoda . The number of
these predators is normally correlated with that cf Collembola
which are their potential preys (Blandin et.al.,in press)
210
-------
— — h-’ %.‘f V .
These observations allow us to propose the use of Mi—
( rLarthropoda as indicators of trampling damage . In particu—
l —,this co 1d be of practical usefulness for the evaluation
of the threshold beyond which these damages are irreve sible.
Taking into account thE. overall quantitative and qua-
litative changes undergone by the community of Microarthro-
pods,precise indications could be obtained . The quantitati-
ve variations of a single species — or category— do not al—
low to draw definitive conclusions, although these could be
ptovided by the comparative study of species hav’ng differ-
ent sensibilities . It is therefore the whole community w i—
ch could be a good ecological indLcqtor of the trampling im-
pact -
ACU 0WLEDGM1 NTS
This research was supported by the )linistere de l’En—
‘jironnement et du cadre de Vie, Grant N 0 77136 . W thank
Mrs. M.—D.Pilot for kind help in pedologic studies and u.S.
Molfetas for useful discussions end help with the manuscript.
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lanzenschutzmaznahmen In Apfelintensivanlagen.pedobjo logja.
3d 18 (5) , 415—425
Lebrun, Ph.,1976 . Effets ecologiques de 1* pollution atmos—
pherique sur les populations et communautes de microarthropo—
de cortlco].es (Acariens,Collemboles et Ptertgotes) Bull.Ecol.
ti, 4 • 417—430
Lemee,G. et Bichaud,N. ,1973 . Recherches sur lea ecosystemes
des reserves biologiquea de la foret de Foutaineblesu . It
Decomposition de la litiere de fenilles des arbrea et l 4 bera—
tion de bioelements . OEcol.Plant. • 8(2) , 153-174
Liddle, M.J. .1975 . A selective review of the ecological e—
ffects of human tramp1i- gon natural ecosystems . Biol.Conse-
rv. 7(1) • 17—36
Novacova, E. .1969 . Influence aes polliitions industrielles
sur lea communauteg animales et l’utilisatiou des animaux
comma bioindicateurs . Air Pollution—Proceedings of the First
European Congress on the influence of air polluti,n on Plants
and Animals .Wageningen,1968 , 41—48
Robin,A.M. ,1970, .Contribution a l’etu ie du processus de
podzolization sous foret de feullius . Science du Sol , 1 ,
63—83
Santos,P.P.,De Pree,E. and Whitford,W,G.,1978. Spatial dis-
tribution of litter and Microarthropods in a Chihuahuan de-
sert ecosystem , J.of Arid Environment 1, 41—48
212
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THE EFFECTS OF TRAMPL!NG ON THE FAUNA OF A FOREST
FLOOR.
II. MACROARTHROPODS
Spyros Molfetas and Patrick Blandin
Ecole Norm tsk S4per,eure
France
INTRODUCTION
Based on the observation obvious to any biologist, that envi—
roninental conditions quite clearly determine the living beings pre-
sent, one may conversely seek to describe the physical environment
through the organisms that inhabit it. In fact, ecologists constan-
tly amploy different organisms as indicators, in order to characteri-
ze certain situations or phenomena which are difficult to approach
directly.
In aquatic environments, the use of estimates of quantitative
and qualitative changes in animal communities as bioindicators in the
examination of certain alteration factors (water pollution) is highly
applied. On the contrary in the case of terrestrial environments the-
se methods are still in the research stage (Novacova, 1969 ; Gilbert,
1971 ; Liddle, 1975 ; Lebrun, 1976).
The position of animals in the trophic sequence of ecosystems
accounts for an ability of integration greater than that of vegeta-
tion. This should motivate research of .!cological indicators in order
to detect, define, and measure the levels of global perturbation in
ecosystems.
Since January 1978 we have been engaged in a research project
on the Macroarthropods community as indicator of evolutionary tenden-
cies in suburban woodland areas. This work sEeks to define multispe—
cific groups, able to provide precise indicai ons on the state and
evolution of suburban forestrial environments. In particular we con-
centrate our interest on the effects of trampling on the Maeroarthro
pods of the woodlands floor which are subject to a high frequentation
rate.
The forest of Fontainebleau. situated 60 km away from Paris,
was chosen for our investigations, as it supports particularly heavy
visitation rates. The foreb! attracts 9,000,000 visitors per year
i.e. an average of 25,000 visitors per day (S.A.R.E.S., data for
1969). For s&anpling area, it was chosen a 0.2 ha woudland section.
The average altitude is 100 m. The regions mean annual temperature
is 10.1°C and the mean annual rainfall 697 mm. Some characteristics
of temperatures and rainfalls annual repartition are presented in
figure 1. The section’s canopy consists of Fague silvatica L. with
some O ercus aeeailif2ora Smith, lofty trees. Six Pii zw a ?. ipcatrita
L. are along bordering road. There is no ground vegetation.
213
-------
FIGURE 1. Average monthly temperatures in °C and rainfall in nun
in the Fontaineb].eau region (data from Mét€orologie Nationale).
Tn 4 Tx
FIGURE 2. Average monthly visitation rates in the parking lot in
of the study area (data from the observation of the number of vililcies
during week ends.
J FMAMJ J A SO ND
Number of
Vebic I. e
IF MAMJ JASON
214
-------
-— -... ,a,.n flr’w S ..S..fl tWP ...eran . S W SI V c’t ea -
An important reason for the choice of this area was that a
parking lot is situated in front of this section, from the other side
of the road. So the frequentation rates were expected to be higher
than the average values of Fontainebleau as it is known that most vi-
sitors frequent particular areas which offer certain conveniences
(parking lots, easy access). People also, do not leave their vehicles
more than 100 in behind, thereby remaining within very limited arLas
(Baillon, 973). Researches in forestrial environments on the influ-
ence of trampling in vegetation, have pointed out that in such zones
the tourist impact and th? degradation of soil and vegetation ire con-
siderable (Fal].inski, 1973 ; Littel, 1974).
Annuals litter evolution
Litter’s evolution was followed by pictures every week from
January 1978 to January 1979. In the end of November the floor is co-
vered from the leaves fallen c 1 iring Autumn. Progressively under the
wind’s influence and as the soil is subsided, leaves accumulate more
or less in certain places according to the inicrotopography. So during
January and February, only in the background of the section we can
observe an undisturbed litter which shows three distinct layers :
1) The L layer formed by leaves which fell during the previous
Autumn.
ii) The F layer which consists of partly decomposed leaves.
iii) The H layer which consists of amorphous humus.
In Spring, three zones parallel to the road can be recognised:
i) The first is almost nude, but however wth small spots of
accumulated litter. It will be called from now on zone of high degra-
dation.
ii) The transition zone corresponds in the area where litter
accumulates in wide spots, but some places remain nude.
iii) The last zone seems to be relatively undisturbed showing
an abundant and permanent litter.
Frequentation of the stud7 area
All throughout 1978, the i umber of vehicles in the parking lot
area, was observed and frequentation rates of the section were esti-
mated. The histogram traced from these data, points out the biinodali—
ty of frequentation with two maxima, during March—April and October
(figure 2). a finding that corresponds to the general frequentation
of the forest of Fontainebleau.
METHODS
After a preliminary sampling in June 1978, it was decided
to do series of r.mples every three months, starting from Novem—
ber 1978. The preliminary sampling pointed out the existence of a
certain gradient in the spatial distribution of Macroarthropods.
Thus, we decided to collect samples along four rows parallel to the
215
-------
- - -
road and ffceen meters apart. Seven sample units were taken in each
Row. Samples w9re limited by a 25 x 25 cm metal frame inside wnich
litter was collected. Samples in February and May, for the first two
Rows, were ollected in spots where litter was accumulated and not in
the cotnpletly nude soil. Litter was kept in paper bags, and back in
the laboratory was put in Beriese—Tullgr. n funnels with light as heat
source for fifteen days, adequate duration for the extraction of all
the Macroarthropods (Geoffroy, 1979). Animals were collected in re—
cipientc cOntd]ning Salycilic Acid.
RESULTS
Results are summarized in tables 1, 2, 3 and figures 3, 4, 5,
6, 7, 8, 9, 10. A complete absence of certain groups of Macroarthro—
pods such as Isopods, Pseudoscorpions and Opilions, everywhere in tha
area, is observed. An extremely low presence of other groups such as
Diptera, Diptera larvae, Coleoptera, Coleoptera larvae and Millipedes
are observed to exhibit important densities, unless in certain pe—
t-iods and usually in the background of the section (figures 5, 6, 7,
8, 9). On the other band, the Spiders and Centipedes are present, but
in low densities and not throughout the whole sampling period Cf igu—
es 3, 4).
TABLE 1. Estimates of the densities (inc ./m 2 ) by Rows and by
groups ot Macroarthropods in November sampling. The relative errors
D 2 1 S
(er) were estimated from re 1w + , Berthet and Gerard, 1970 ;
22 2 E.J —
D 2 = tS or D 2 = !: according to the relations betweeni and S 2 and the
nx
values of K (Elliot, 197]). Great relative errors are due to the ex-
tremely low densities. one individual per Row ; two individuals
per Row.
ROW1 ROW2
216
ROW3 ROW4
Spiders
10.3 ± 6.2
er : 60 %
10.3 ± 6.2
er : 60 Z
22.9 ± 19.0
er : 83 Z
48.0 ± 16.0
er : 33 %
Centipeds
Millipedes
3.4 ± 2.7
er : 79 Z
0
3.4 ± 2.7
er : 79 2
12.2 ± 7.5
er:61%
11.4 ± 9.9
er : 86 2
12.2 ± 7.5
er:61%
12.2 ± 7.5
er 61 2
12.2 ± 7.5
er:612
Diptera
20.0 ± 8.2
er:41Z
20.0 ± 8.2
er:41Z
20.0 ± 8.2
er:412
20.0 ± 8.2
er:412
Coleoptera
Dipt.
65.1 ± 15.8
: 24%
377.1±274.3
65.1 ± 15.8
r : 24 2
379.0 ± 84.0
125.7 ± 30.5
er : 24 Z
379.0 ±
25.7 ± 30.5

84.0379.0 ± 84.0
Larvae
er : 73 2
er : 22 2
er : 22 2
er : 22 2.
Col.
Larvae
97.6 ±
er : 16%
15.5’97.6 ± 15.5
I er : 16 2.

97.6 ± 16.5
er : 16 2
97.6± 15.5
er : 16 2
Ants
a
4.1±2.4
er : 592
4.1±2.4
er: 59%
-------
md/rn’
30
10
o
nd/rn’
1$,
.30,
S
AVERAGE DENSITY (iM./ 2 )
(scUd re tang1e) AND MA!
ROWI ROW2 ROW3 R0W4
FIGURE 3. SPIDERS
tu
ROWI ROW? ROW3 ROW4
FIGURE 5. DIPTERA
IN NOVEM R (b .ack rectangle), FEBRUARY
(eiapty rectangle) FOR youR PAR LLEL ROWS.
217
FIGURE 4. CENTIPEDES
1
I
md/rn’
410
3 10
270
SO
0
•1
ROWI ROW2 ROW3 ROW4
FIGURE 6. DIPTERA
I
0
ROWI R0W2 ROW3 ROW4
1
LARVAE
-------
AVERAGE DENSITY (tnd./s 2 ) IN NOV M R (black rectangle), P! BRUARY
(solid rectangle) p AY (eapty rectangle) FOR ThE YUJR PARALLEL ROWS.
FIGURE 7. COLEOPTERA
FIGUL E 8. COLEOP1ERA
Ind/m
25
20
1$
I0
$
NOWI ROWZ
ILl.
*0W3 R0W4
FIGURE 9. MILLIPEDEs
FIGURE 10. ANTS
ISO
0
o o
ROWI ROWS ROW3 ROW4
20
md/rn ’
ROWI ROWS ROWE ROW4
I.
LARVAE
ROWI
ROWS
ROW4
218
-------
- 71 —. .&tI ?e . _ flhlP4tc .tfl—. - _ -
TABLE 2. Estimates Q t ia densities (iM.fzn 2 ) by Rows and by
groups of Macroartbropods in February sampling.
A one individual per Row (Scven sample units) ;
* *two individuals per Row (Seven sample units).
ROW1 ROW2 ROW3 ROW4
Spidersj
Cent ipeds
3.8 ± 2.2
er: 7Z
* * —
3.8 ± 2.2
- er:577.
0
3.8 ± 2.2
er:57Z
0
13.7 ± 12.0
er:87Z
6.9 ± 3.9
er:56 2
Mihipe
des
o
a
*
9.1 ± 7.4
er_: 81_7.
Diptera
0
10.2 ± 7.1
er 69%_
10.2 ± 7.1
er:69Z
20.5 ± 15.1
er: 73%
Coleoptera
9.1 t 7.0
er: 76%
43.4 ± 27.6
er :63%
70.0 ± 23.6
er: 33%
96.0 ± 42.4
er: 44%
Diot.
Larvae
Col.
Larvae
Ants
1G9.0 ± 45.8
er : 27 7.
114.2 ± 29.9
: 26 7.
169.0 ± 45.8
er : 2’ 7.
114.2 ± 29.9
er : 26 7.
33.0 ± 140.0
er : 32 2
153.0 ± 38.3
er : 25
433.0 ± 140.0
er : 32 2
169.1 ± 62.3
: 367.
a
a
0
0
TABLE 3. Estimates o the densities (indi/m 2 ) by Rows and by
groups
o Nacroartbropods in Nay sampling.
* one
**two
individua3 par Row (Seven sample units) ;
individuals par Row (Seven sample units).
RQW1
RQW
ROW3
ROW4
Spiders
a
0
0
6.8 5.9
86 2
Cent ipeds
0
a
0
o
MiIIipede
0
C
*
**
Diptera
* *
0
70.7 ± 10.9
er:15Z
70.7 ± 10.9
er:132
Coleoptera
33.1 ± 8.8
er:267.
56.0 ± 21.4
er:38%
56.0 ± 21.4
er:382
33.1 ± 8.7
er:262
Dipt.
64.0 ± 25.1
64.0 ± 25.1
112.0 ± 29.6
112.0 ± 29.6
Larvae
er ; 39 7.
er : 39 7.
er : 26 7.
er : 26
Col.
Larvae
55.5 ± 18.8
r:33Z
55.5 ± 18.8
ez:33%
55.5± 18.8

82.2 ± 13.2
jjj_
Ants
0
8.5 ± 3.5
er:41 2
4.]. t 2.4
er:5az
23.0 ± 1.5.8
219
-------
Quantitative and qualitative characteristics
Results of non parametric U—test comparizon between different
groups and Rows La the three periods of sampling, are summarized in
table 4. The values of U-test comparizon of all the groups densities
beb een Rows one and four ire highly significant. AU the groups show
much higher ave-age densities in Row four than in Row one. )!illipades
and Ants are not even pres nt in Row one in any sampling period. On-
ly in the case of Diptera, Di,tera Lai?vae and Coleoptera Larvae in
November sampling were the deflsities practically the same, between
these two Rows (figures 5, 6, 8).
In the intermediate area bet .’een Rows one and four, the diffe-
rences in the group average densities. seem to be not so clear. No
difference in the densities between Ro two and Row three for almost
all the groups, could be observed (Millipedes, Spiders, Diptera, Dip
tera Larvae and Coleoptera Larvae in November sampling, Diptera in
February and Coleoptera adults and Larvae in Nay sampling). Some
groups, also, have densities not significantly different, between
Rows one and two (Coleoptera in November’s sampling, Diptera Larvae
and Spiders in Nay’s sampling), as veil as between Rows three and
four (Coleoptera in November, Diptera Larvae in February, Diptera
adults and Larvae in May).
Thus, we see that the main distinction existing between the Ma-
croartbropod densities is this between Rows one and four. In the in—
termed late R4VS the groups -except from tie predators— have similar
densities.
The Macroarthropod communities
Taking into account the groups present and absent in each. Row,
and their relative abundances, three Nacroarthropod cciumuni ties could
be distinguished, corresponding more or less direct ly to the intensi-
ty of perturbation.
In the first zone, corresponding to Row one, the commrnity is
characterized by the complete absence of Millipedes and Ants (figures
9, 10), by the partial absence of Spiders, Centipedes and Diptera, and
by a very important reduction of all the Macroar’iiropod densities. The
dominant group is the Diptera Larvae.
The second zone (Rows ttio and three) • is situated at an inter-
mediate distance from the road. The community here is characterized by
the appearence of the groups not existing in the previous zone. Never-
theless the densities of the Macroarthropod community in this zone an.
:elatively low, lower than those in Row four. The groups of predators
still existing in the section, seem to be most affected, shoving the
lowest relative abundance. Diptera and Coleoptcra Larvae are still the
dominant groups.
The thi d Macroarth opod community corresponds to the last sam-
pling zone (Row four). Litter here is abundant with a vertical struc-
ture during winter corresponding to the three layers previously des-
cribed. The perturbation of this zone by trampling seems to be negli-
gible. Dcnsities of certain groups such as Spiders and Centipedes are
five and nine times respectively bigher that those in the first zone.
220
-------
TABLE 4. Non parametric U—test coniparizon between Rows and different groups for all
the sampling periods. Level of significance : 0.05.
• non significant ; * significant ; * * highly significant.
NOVEMBER FEBRUARY
- R R R 2 R R 3 R 4 %R R 1 R 2 R 1 R 3 R,R R 2 R 3 R R 4
MAY
R 3 R 4 R R
R 1 R 3 [ R R
R R 3
R,R 4 1 R 3 I
Spiders
•**********•
•**.****
Centipedes
•
**********
•
•
**
****
•
•
1
Millipedes
******
•
•
•
•
•
**
•
**
•
•
•
•
•
•
•
Diptera
I
•
I
I
I
I
******
•
****
•
********
•
Dsptera
Larvae
•• •• •.**o***•
Coleoptera
•
******
•
•
******
a
********
•
•
**
•
Coleoptera
Larvae
•
1
• • • • • •

**I******l •
— — — — —
******** •
—
• • • • •
— — — —
•
•
* •
*******
— — —
1 Ants
‘
***
—
—
-------
A preliminar comparizon between the densities of Macroartbropods in
this zone and those of a non trampled, similar forest floor was made.
(Station Biologique de Foijuif, E.N.SI, situated 20 kin south of our
study area, unpublished data). This comparison points out that almost
all the groups from the third zone of our study area have lower den-
sities than tL,se of the practicly non trampled floor. Nevertheless,
Coleoptera have in all the sampling periods much higher den5ities
than those of Foijuif.
However the composition of Macroarthropod community in this
third zonc appears not to differ significantly from this of the non
per turbated floor.
Seasonal variations of the Macroarthropod communities
In the end of November lLtter is formed over the study area as
an homogenous layer of leaves. This litter is rapidly inhabited by
many groups (Tabic 1). Although litter is hoinogenously distributed,
a certain gradient between Rows can be easily observed, for Spiders,
Centipedes, Ants and Coleoptera. Other groups such as Diptera adults
and larvae, CoJ.eoptera Larvae, ang even Millipedes seem to be unaf-
fected i thin period. During winter, with the litter’s accumulation
in th less trampled on places, the influence of perturbation is
clearest in all the groups, which show progressively increasing den-
sities from Row one to Row four. During Spring the ilitensity of tram-
pling reaches its maximum (figure 2). The composition of the Macro—
arthropod community in Zones one and two is completely different from
February to May samplir (Tables 2 and 3). Thus, Spiders, Millipedes,
Ants and Diptera are c.’inpletely absent from Row one and two while
they show low densities i Rows three and four. Centipedes are absent
from all the area.
The predator populations
The previous discussion focused on the spatial and temporal va-
riations of the structure of I4acroarthropods community under the in—
flueuce of perturbations 3 rn’uced by trampling. We observed that the
predators are affected the most, their densities respondingalinost di-
rectly to the intensity of perturbation factors. Spiders and Centipe-
des are practically the only predators remaining in the area. The den-
sity of Spiders increases progressivly from Row one to Row four. The
number of species present, also follows this pattern in November’s
sampling, we found only one species : Leptypzw2tes fiavipea in Row
one, two species, Tiso Vi79w28 (31.), Tlzeridiwn vittatio’t C.L. Koch in
Row two, and five species, Centt’a,nerita’ conoinna, (Th.) Leptyphrintea
minutas, 31., Tieo vag za , Leptiphantes flavipes 31., Centromenue
aequalis C.L. Koch,in Rows three and four.
The study of Centipedes shows that the Litbohiomorph. do not
appear all over the study area. Only one species of Geophilomorph.
Schendyla neinorenais C.L. Koch, was found in the first and the se-
cond zone, while four different species (three immatures and a Bi’o—
ohygeophi lies t2’yncorwn Meiriert, were found in the third zone (Row
four).
These results show the important relation which may exist bet-
ween certain perturbation factors and the specific richness of the
predator communities in the soil ecosystem.
222
-------
CONCLUSIONS
The study of the Macroarthropod coiwuunities of a trampled on
forest soil, focuse on certain aspects of their structure. First of
all we wish to underline the complete absence of certain functional
groups such as Pseudoscorpions and Cpilions, whose the role as preda-
tors is important for the coimnunity. Also, the absence of the espe-
cially important for litter’s decomposition group of Isopoda, is
remarquable. The reasons of disappearence of these functionally and
taxonomically very different groups, have to be identified. However,
other predator groups such as Spiders, Centipedes and Ants are pre-
sent in much lower densities than in non trampled on zones. The sam-
pling by Rows, pointed out that their numbers and specific riciriess
increase when the perturbation in the floor is less important Cf igu—
res 3 and 4). Studies in ecosy5tenis of different structures, also
show that th& predators arc always affected the most (Novacova, 1969;
Littel, 1974 ; Van Ploeg and von Wijngaarden, 1975).
From the other hand, groups such as Diptera and Coleoptera seen
to be no affected directly, showIng howev. r certain gradients in their
densities corresponding to t.he intensity of perturbation.
Thus, Nacroarthropods, which, do not show the same preferences
in habitat and nutrition, do not react in the same way, in trampling.
Through the study of these reactions and the ). :roarthropod conmuni—
ties modifications, it will be possible to measure the effects and to
characterize the impact of perturbation induced by trampling.
ACKNOWLeui jr . zr.ni.n
This research. was supported by the Ministère de l’Environne—
merit et du adre de Vie under Grant n°7713 6 . Mr Christophe T. and
Ceoffroy 3.—J. for the Spiders and Centipedes determination and also
Caray L. for kind help in statistical interpretation are greatfully
acknowledged. Thanks to Niovi Lynghiari and C. Lionel—Marie for edi-
torial work and manuscript typing.
LITERATURE CITED
Baillon, R, 1! 73. Relations entre statut socio—culturel et Er quen—
tation de Ia Lorat. Ecole Polytechnique, Paris A.102.1273.
Berthet, P. and Gerard, C., 1970. Note sux l’estiination de la densi—
té despopulations dapb.iques. Pages 189—193 in Methods of study in
soil ecology. Proceedings of the Paris Symposium. Ecology and Conser—
vation, llnesco, 1970.
Elliot, J.lL, 1971. Some methods for the Statistical Analysis of
sample of benthic invertebrates. !reshwater Biological Association
Scientific Publication N 25 148 p.
Paliriski, J.B., 1973. Reaction of field layer in forest coijununities
to trampling in the light of experimental studies.Phy±ocenosis, 2
(3), 205—217.
Ceoffroy, .T..L, 1979. Les peuplenents de Cbilopodes at de Diplopode.s
d’une Cb2naie—Cbarinaie (Station Biologique de Foljuif). de
3e cycle d’Ecologie, Univ. Paris 6, 179 p.
223
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Gilbert ,O.L, 1971. Some indirect e fects o air pollution on bark li-
ving invertebrates. J. Ecol., 8, 77—84.
Lebrun, P., 1976. Effets écologiques de L’ pollution atmosphérique sur
lee populations at conununaués de Microarthropodes Corticoles (Aca—
riens, Collemboles at Ptéry otes). Bull. Ecol., t. 7 (4), 4174 O.
Liddle, N.J., 1975. A selective review of the e’ological effects o
human tra npling on natural - cosystems. Blot. Conserv. 7, 17—36. -
Littel, A., 1974. Betredingsonderzoek in een duinvallel : effecten op
mesofauna en vagetatie. Verkenningen van het Instituut voor Nilicu
Vraagstukken Vri3e Universiteit, Amsterdam. Serie B, No 5.
Novacova, E., 1969. Influence des pollutions industrielles sur lee
coinmunaut e animales et l’utjlisation des animaux come bioindica—
Leurs. Air Pol].ution—Procee ings of the First European Congress on
the influence o air pollution on plants and animals. Wag sn.
Ploag, S.W.F. van der and Wingaarden, W.K.., van, 1975. The influence
of trampling on Spiders. Prcc. 6th mt. Arach. Congr. Leiden, 1975.
QUESTIONS and COMMENTS
G. KLE : Did you find any physically damaged or dead
larger macroarthropods in the heavily walked over areas in
Row 1 or Row 2, that appeared to be injured by being stepped on?
MOLFETAS : The damages, in individuals with a length
of 5 nun is very difficult to be identified. In any case,
our method was not the hand sorting sampling but the ex--
traction in Berlese—Tuligren, so that the already dead animals
could not be extracted.
. . SNIDER : In casual sampling near the established
rows, did you frequently find isopods? What was (were) the
species?
. MOLFETAS : During the whole sampling period we have
never found any isopods in this section. Nevertheless in
adjacent section of the forest, with similar vegetation
structure, but not trampled, we can find easily “normal”
densities of isopods. The same happens also with the control
(Station Biologique de Foijuif).
B. STEVENSON : The presence of undisturbed litter appears
to be important for a stable macroarthropod community. Does
the importance of this litter habitat for arthropods rest
primarily in its structure, energy or food value, or effect
on soil-litter microclimate?
S. MOLFETAS : The structure and function of the macro-
arthropod communities in the soil, is related with th litter’s
structure, because it is in the same time the habitat and
the food factor, for the decomposers, which are the prey of
predators’ populations. So the abundance of litter, determines
224
-------
I
more or less the ntacroarthropods’ densities.
K. RIVETER : No mention was made of pulmonate mollusks
in your study: Is this an indication they were never observed
an therefore not present in the Forest of Fontainbleau?
S. MOLFETAS : Three slugs were observed during the study
and therefore slugs were not considered as important indicators
of trampling effect.
225
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SOIL MITE COMMUNITIES IN THE POOREST ENVIRONMENT
UNDER THE ROADSIDE TREES
Jun-ichi Aoki and **Genichi Kuriki
Yokoliama National University
“Toltokn Dental Univrrsily
Japan
INTRODUCTION
In the central part of large cities wholly laid with
asphalt, we can see soil surface only around roadside trees.
The areas of about 1 X 1 m suare are mostly naked or covered
by poorly grown weeds and the soil is very firm almost with-
out organic layer. Such an environment seems to be one of
the most unsuitable places to live for most of soil animals.
The present study was carried out in and around Yoke—
hama City to ascertain whether soil mites inhabit such an
environment or not and, if they do, what kind of species or
group of mites can live there and how the soil mite communi-
ties differs from those of green area.
METHODS
The city of Yokohama is located south of Tokyo and
the secor d largest city of 2 Japan, having a large population
of about 2,752,000(6454/km ). The sampling was made in May,
1978 at 18 points in three serieses along the Route 16(Pig—
ure 1). The series A was taken from soils around roadside
trees in the urban area near the center of Yokohama City.
The series B was also taken around roadside trees, but in
the suburban area outside the city. The series C was taken
in green areas in and outside the city, namely in parks or
groves situated not so far from the Route 16. At each point
ten samples of 100 cc soil were taken by the sampler of 5
X 5 X 4 cm from around ten trees.
RESULT AND DISCUSSION
The five groups of soil mites
An unexpectedly large number of soil mites were col-
lected frori any of the three different environments. They
226
-------
Figure 1. A ap showing the sampling points along the oute 16.
A 1 —A 6 :Urban roadsides(in the city). 8 i 35: Suburban
roadsides(outside the city). C 1 — C 7 :Green areas.
901_ \
1x
20
10
I ’
W I
H
I
. .
Figure 2 Change in average density of the five groups of soil
mites in the three different environments.
a
URIA$ SU3VRBAN
DsIDg ADUDE
GRE SN
227
-------
-fl -—fl - -
were classified into five taxonomical groups — Gamasida,
Oribatida, Actinedida, Tarsonemida and Acaridida. As shown
in Table 1 and in Figure 2 the densities of Gainasida and
Actinedida were not so clearly different among the three
different environments, though their average numbers become
slightly higher from the series A to C. However, a distinct
tendency of increase in number of Oribatida was observed in
the green areas(series C) compared with the suburban(series
B) and urban roadsides(series A). The average density of
Oribatida in the green areaa was about three times as high
as that in the urban roadsides.
On the contrary, the densities of Acaridida and Tar—
sonemida were highest in the urban roadsides and lowest in
the green areas. The tendency was especially striking in the
case of Acaridida, its average density in the urban road-
sides being 100 times as high as that in the green areas.
A similar tendency was observed in the coi q.arison
among relative abundaneies(Z) of the major groups •3f soil
micro—arthropods including Collembola(Figure 3). The average
density of Oribatida was 30.92 in the green area, but it
decreased to 23.6% in the suburban roadsides and was reduced
to only 5.62 in the urba.. roadsides. On the contrary, Acari-
dida occupied only 1.52 in the green areas, 9.82 in the sub-
urban roadsides, but strikingly increased to 48.92 in the
urban roadsides. Tarsonemida showed a tendency somewhat
different from that of the actual density, reaching to the
highest percentage(16.3%) in the suburban roadsides. Rela-
tive abundancy of Collembola was highest in the green areas
(34.6%), but not so strikingly decreased in the roadsides
(25.1% and 20.02).
The population of Acaridida was mostly composed of a
single species, Tyrophagus putrescentiae (SCHRANK ), which is
known in Japan as a famous pest of stored foods and “tatami”
(straw mats). The species is a]5o found is forest soils of
Japan, but always in very low density. The mites of Tarsone—
mida mostly consisted of several unidentified species of the
families Scutacaridae ajtd Pyemotidae. These two groups of
soil mites, Acaridida and Tarsonemida, seem to prefer en-
vironments under heavy human impacts and may be considered
as “anthrophilic” animals, while Oribatida as a whole may
be called “atithrophobic” animals.
In natural forests of Japan or in places under light
human impacts, the order in abundancy of the five groups of
soil mites is usually Oribatida> Gamasida Actinedida >
Tarsonemida Acaridida. It was proved that this order was
converted in environments under heavy human impacts as
Oribatida> Tarsoueuiida = Acaridida> Gamasida Actinedida
in the suburban roadsides or Acaridida > Tarsonemida > On—
228
-------
Table 1. Denaity(number/5x5x4 cm 3 ) of the five differcut groups of soil mites
in urban roadside(A), suburban roadside(B) and green area(C) of Yokohama.
Sampling point
Gamasida Actinedida Oribatida Acaridida Tarsoneinida
Total
,
. ‘
.



Al Yamashita—cho
£2 Tauruma
A3 Sengen—cho
£4 Miyata—cho
AS Hodogaya
A6 Kamihoshikawa
3.6 5.0 5.6 26.3 1.9
2.8 1.2 11.8 104.1 20.4
8.6 11.9 17.3 218.1 34.6
0.9 3.2 2.0 36.8 15.4
5.7 4.2 6.0 181.8 28.1
2.6 0.7 8.0 26.2 11.0
42.4
140.3
290.5
58.3
225.8
48.5
Average
4.0 4.4 8.5 98.9 18.6
134.3
I

#‘


B1 Minaini—Machida
B2 Kami-Tsuruina
B3 Fuchinobe
B4 Sagainihara
B5 Minami—Hashimoto
2.3 1.7 13.8 0.1 1.6
12.1 3.0 10.4 13.8 5.6
4.6 4.5 8.5 21.8 11.4
6.8 11.6 35.6 8.6 14.6
0.9 5.7 6.1 0.1 12.7
19.5
44.9
50.8
77.2
25.5
Average
5.3 5.3 14.9 8.9 9.2
43.6
-

Cl Sankei—en
C2 Sankei—en
C3 Yokohama Station
C4 Yokohama Natn. Univ.
C5 ICami—Kawai
C6 Sagamihara
Cl Sagamihara
8.6 7.9 15.3 2.5 0.1
10.1 15.3 45.4 0,3 1.6
10.5 9.8 24.9 1.2 5.9
4.3 12.4 23.2 0.4 7.2
3.2 6.1 11.9 1.6 0.1
8.6 15.1 39.1 0.7 1.9
1.9 7.3 20.2 0.1 0.4
34.4
72.
52.3
47.5
22.9
65.4
29.9
Average
.7 10.6 25.7 1.0 2.5
46.6
-------
Figure 3. Cou arison among relative abundancies of soil micro—
arthropod groups in the three different environments.
A: Urban roadsides, B: Suburbdn roadsides, C: Creen areas.
The blank .reas indicate the total percentage of the other
uuc o—arthropods including the remaining mitec, araneids,
crustaceans, myriapods and the other insects.
A B
______ Tarsonemida
Collembola
batida — Actinedida — Gamasida in the urban roadsides.
The average density of total soil mites was highest
in the urban roadsides, being about three times as high as
that in the suburban roadsides or the green areas. Before
our investigation, we supposed that the mite density would
be very low in the urban roadsides and never expected such
a. high density which was attributed to a great number of
acarid mites.
Analysis of Oribatid communities
As stated above, Oribatida as a whole was found to
be “anthrophobic” animals. But, are they all anthrophobic ?
To elucidee the problem, the species composition of Oriba—
tida ras investigated a each sampling point.
A total of 91 species of Oribatida were found, 22
species from the urban roadsides, 37 sp cies from the sub-
urban roadsides a ’ d 76 species from the green areas. A part
of the species showed characteristic pattern of appearance
in relation to environmental difference as shown in Table 2.
Oppia tokyoensis AOKI, Oribatula sakamorii AOKI and Eremulus
sp.B of the “group 1” were more frequently found in the
roadsides(A and B) and considered to be “anthrophilic”
species. Oppia tokyoensis had been described from the soil
under roadside thicket in the central part of Tokyo(AO I ,
230
C
______ Acc ridjda
Ori tida
-------
Table 2. Groi iing of the oribatid species accordi:.g to their appearance in the three dikferent
environments. The figures in the table indicate the degree of average density/tOO cc soil
divided into five classes — 1:0.1—0.9, 2:1.0—1.9, 3:2.0—2.9, 4:3.0—4.9, 5:5,0—14.6.
Grot p
Oribatid species
Urban
roadside
Suburban
roadside
Green area
A1A2A3A4A5A6
B1B2B3B4B5
c1c2C3C4C5C6C7
1
Oppia tokyoensis AOKI
Oribatula aakamorii IOK1
Eremulus sp.B
2 1 1 1 1 5
1 4 1
1 2 1_—
1 4 1 4 1
1 1
3 1.
1 2
2
2
Cultroribula lata AOKI
Netrioppia sp.A
Fiaeiceph us clavatus ( OKI)
Microzetes auxiliaris GRANDJEAN
Eremobelba japonica AOKI
Multioppia brevipectinata SUZUK
Gymnobates sp.
Eohypochthonius crassise tiger AOKI
3 1 5 4 5
3 2 1 1 3
1 1 1 1
1 1 j
1 2 2 1
2 1 1
1 1 1
1 1 1
3
Bypochthoniella iuinutissima BEBLESE
Machuella ventrieetosa IIMMER
Eohypochthonius parvus AOKI -
Rhysotritia ardua (C.L.KOCH)
Oppiella nova (OUDEMANS)
1
1 2
1
1 1
1 1
1
1 1 1
1 1 1
1 1 1 1
1 1 1 1
1 1 1 1 1 1
1 5 1 3 4 2
4
Tectocepheus velatus (MICHAEL)
Oppiasp.33
Oppiasp.1
Quadroppia quadricarinata (MICHAEL)
2 1 2 1
255141
11 1
2 1 1
1 3 2 4 1.
53214
111 1
1 3 1
3 1 4 1 1 3
131
1 1111
1 1 1 1
Average total number
5 12 14 2 6 8
13 8 7 32 6
21 13 36 20 11 37 11
Total species number
5 10 14 6 9 6
13 8 13 26 11
22 20 31 26 19 24 20
-------
1974) and Oribatula sakamorii had been collected for the
first time in a greenhouse of melon fruit(AOKI, 1 7O) oud
was later found from poor secondary grasslands and farms.
But, such species are rather exception . among the
oribatids. Most of the oribatid species dc not like to in-
habit poor soil environments under heavy human impacts. The
species of “group 2” and “group 3” in Table 2 are normal in
this sense, inhabiting only or mostly the green areas. The
species of “group 4” are non—selective inhabitants which
appeared evenly in the three different environments.
CONCLUSION
According to our expectation, the mite group Oribati—
da decreased in number in the suburban roadsides and more
strikingly in the urban roadsides. Gamasid and Actinedida
showed a similar tendency. It is incorrect, however, to say
that all the soil mites decrease in soils under heavy human
impacts. Acaridida and Tarsonemida were more abundant in
the roadsides than in the green areas, reaching to the high-
est number in the urban roadsides which seem generally to
be the poorest environment for soil animals. We may call
these groups of mites “anthrophilic”. Even in Oribatida a
few species were found to be anthrophilic.
LITERATURE CITED
AOKI, J. 1970. A new species of oribatid mite found on melou
fruits in greenhouses. Bull. Natn. Sci. N t is. Tokyo
13 581—584.
AOXI , J. 1974. A new species of oribatid mite found in the
middle of Tokyo. Bull. Natn. Sd. Mus. Tokyo 17 283—
285.
232
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— — -, a- . !aflWW
SESSION IV: RELATIONSHIPS OF SOIL
ORGANISMS TO AGRONOMIC PRACTICES AND
ANIMAL WASTES
Moderator: Ph. Lebrun
University of Louvain
Lou ain-Ia-Neuve, Belgium
233
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Heteroder avenae Woll. (NEMATODA: TYLENCHIDA), THE
CEREAL CYST NEMATODE: RELATIONSHIPS BETWEEN ITS
POPULATION DENSITY, WHEAT GROWTH AND YIELD, AND
SOIL VARIABILITY IN SOME SOUTH AUSTRALIAN WHEAT
FIELDS
K. E. Lee and j. C. Buckerfield
CSIRO
South Australitu
INTRODUCTION
The cereal cyst nematode, Heterodera avenae Woll., also known as
the oat cyst nematode, infects the roots of cereals and many other
graminaceoua plants in many parts of the world (see Meagher, 1977).
In Australia it is widespread in the southern cereal-growing areas of
South Australia, Victoria and New South Wales. Because wheat is the
most widely grown and economically the most important cereal crop in
southern Australia that is par’asitised by H. avenae , much work has
been done there on the effects of this nematode on wheat growth and
production (Davidson, 1930; Millikan, 1938 a,b; Wallace, 1965;
Meagher, 1968; arry, Brown and Elliott, 19711; O’Brien and Fisher,
19711; and others).
In South Australia about two million bee tares are sown to
cereals each year, and about 50 to 60% of this area is sown to wheat;
cereal production provides an annual gross income of about Aust. $210
million, or about 30% of the total value of farm production in the
state (data from Leonard (1978) for the five years 1972—3 to 1976—7).
Cereals are sown after rains in late autumn, ana hatching of H. avenae
in t.he soil is apparent]y controlled by falling soil temperatures and
increasing soil moisture, so that the infective larvae are active in
the soi.]. in large numbers when cereal root growth begins.
Second-stage larvae emerge from cysts in the ooil (mainly in the top
lOom), and enter the seminal roots of wheat plants close to the
growing tip. They may survive only a few weeks in the soil unless
they are able to gain entry to a root (Davies and Fisher, 1976).
Hatching and emergence of larvae continue into winter, until about the
end of July, and larval entry into roots continues into August.
Following tnfeotion, the plant oroduces giant cells (syncytia)
at the infection point, and the larvae feed on the contents of these
cells. The mechanism that incites development of syncytia is not
understood, and would repay careful investigatIon, because the larvae
are dependent on their formation for their further development, and an
understanding of their genesis and growth might lead to a better
understanding of the effects and possible control of some plant
parasitic nematodes. Growth of the infected root tip ceases, and the
root branches above the infection point. In cases of very heavy
infection, the new root tips are infected, and this
-------
may be repeated, with further branching, producing a “knotted” system
of short branching roots.
Larvae develop within the root to becorte dults. Adult females
are spherical and remain within the root, protruding slightly onto the
root surface; adult males are worm-like and emerge and move along the
root surface, and after locating and fertilising the females, they
die. After tertilisaticn the body of the female becomes progressively
more distended with eggs, developing into a white ovoidal projecting
body, about 0.5mm in diameter, on the root surface. This stage is
known as the “white cyst”, though it is really the living female; it
• is firmly attached to the root and is easily identified. As the
plants mature the females die, but their outer cutioles remain to form
brown “cysts”, each containing from abou’ 100 to about 60D eggs. The
“oysts” remain in the upper layers of the soil, and in the next autumn
and winter about 50 to 60% of the larvae emerge. Eggs that do not
hatch in the first yea. may remain viable, to hatch in subsequent
years; “cysts” may contain viable eggs for 10 years or more.
Counts made of “white cysts”, at about the flowering stage of the
plants, are generally ao. epted as a reliable measure of infestation
rate in assessing the effects of B • avenae on plant growth and grair
yield (e.g., Southey, 1956; Meagher and Brown, 197k). tn our 1971 and
1978 sampling, which provided the data used in this paper, we accepted
“white cyst” counts as a valid basis for assessment of’ the possible
effects of H. avenae on wheat growth and yield, and all estimates of
H. avenae populations in this paper are so based. Because we have
been unable to demonstrate any consistent relationship between this
measure of infestation and plant growth and yield data, we have
extended our sampling in the 1979 season to include estimates of
“cysts” and larvae in soil, and of larvae and “white cyst” numbers in
plants from seed sc ing to harvest.
Many authore have concLuded timt H. avenae reduces plant vigour
and grain production, and efforts have been made to reduce its
apparent effects by breeding resistant or tolerant varieties, use of
nematicides to reduce neiuatode populations, &nG thus infection rates,
and crop rotations deai ned to deprive the nematode of a suitable host
or one or more years between cereal crops (see review of Kort,
1972). Much recent work in South Australia and Victoria has compared
nematicide—treated wheat plots with non-treated controls and baa
attributed increased growth and yield in the treated plots to control
of B. avenae (e.g., Rovlra, 1978).
H. avenae is highly aggregated in its distribution and population
density varies widely wJtbin small areas. We have taken whole
farmers’ wheat fields as sampling sites, and have designed our
sampling programme to cope with the variability in H. aveuae
populations, wheat growth and yield, and soils so that we can make a
statistically—based assessment of the relationships between them.
235
-------
We have not interfered with normal farm practice nor introduced any
experimental treatments, but have attempted to sample the fields,
which are the units of the farmers’ cropping syste . By sampling at
the same points in these fields in successive ct’ops of wheat through a
crop rotation cycle we also hope to learn whether the patterns of
nematode aggregation and any effects they may have on wheat growth are
consistent from crop to crop.
Severe “patchiness”, i.e. patches of yellowing and stunted growth,
in cereal crops has long been associated with patchy infestation by H.
avenee in southern Australia and elsewhere (Davidson, 1930;
Hicldnbotham, 1930; Duggan, 1961; Meagher, Brown and Rovira, 1978).
Similar “patchiness” is also attributed to other diseases and to
variability in nutrient or water availability, related to patterns of
soil variability. There is little quantitative data that would relate
H. avenae infestations directly to patchy growth, so we included in
our study a wheat field Io own to be heavily infested with H. avenae ,
and with severe “patchiness”.
METHODS
In the 1977 season three wheat fields were selected, at Coonalpyn,
Bute and Calomba, in South Australia. On these fields, whose areas
were approximately 3Oha, 0ha and 1 01m respectively, stratified—random
sampling grids (50 points per field) were established, and samples of
wheat plants (10 £n a row per sampling point) were taken when H.
avenae was at the “white cyst” stage (flowering stage of the plants)
and again at harvest. Soil cores (to im depth) were taken at each
sampling point (50 cores per site), soil profiles were described and
soil samples were taken for analysis.
The fields sampled in 1977 were not sown to wheat in 1978. Two,
at Coonalpyn and Calomba, have been sown to wheat again in 1979, and
sampling is in progress at exactly the same points.
In the 1978 season we sampled a wheat field at Moorlands, in South
Australia, that was known to be heavily infested with H. avenae , and
which displayed extreme “patchiness”. On a transect approximately
200m lo ig there were three “good-growth” patches and four
“poor-growth” patches; sampling points were selected on the transect
mid-way across each of these seven patches. Ten adjacent plants along
a row were collected at flowering stage from each sampling point; nine
weeks later, immediately before harvest, a further 10 plants were
collected from each of two adjacent rows at the same sampling points.
For all samples, “white cyst” counts and a range of plant
characteristics were measured on each plant at the first sampltng; at
the second (harvest) sampling all measurements were repented on each
plant, except cyst counts and root measurements, which are not
236
-------
practicable when the plants are mature • The ten plants from each
sampling point, at each st.mpling time, were dried and ground for
chemical analysis, separating grain from straw at the second sanioling.
For the H. avenae cyst øounts and all plant measurements we aimed
to collect sufficient data such that the standard errors of means
should be no more than io of tile means. Although 500 pjants were
collected at each of the Coonalpyn, l3ute aniA Calomba sites, it was
found that, except at the Calomba site, 300 sets of measurements were
adequate for “white cyst” c ounts and measurement of seminal root
length. At the CalomL site, 63% of plants sampled had zero counts
for “white a ysts”, so the cyst counts were not suitable for
statistical analysis.
RESULTS
In our treatr ent of the data, we aimed to identify:
a. the effects of H. avenae on Ci) plant mortality, (ii) plant
growth, and (iii) grain yield;
b. variations in the above, related to soil variation;
c. within—site and between—site variation in neinatode
populations and their relationships to the above.
Some of the basic data from the aites at Coonalpyn, Bute and
Caloinba are st m ,’ised in Table 1. The 1977 growing season was
unusually hot and dry, and g”ain yields were low throughout the South
Australian cereal—growing areas. When plants are under mo2sture
stress, it is believed that they are more likely to suffer severe
d ’n ige from H • avenae infestation. than when they have
adequate moisture for growth (Barker and Olthof, 1976).
Tables 2 and 3 list correlation coefficients between data sets for
Coonalpyn and Bute respectively. Where correlations include “white
cyst” counts or seminal root length only those 300 plants for which
data were obtained are included • For correlations between
measurements made at the first and second sampling times, means of ten
plants at each sampling point were used, because the plants sampled at
the second sampi:.ng were not the same plants as at the first
sampling. For the numbers of plants sampled correJation coefficients
> oao.25 are statistically significant (P43.05), but it must be
appreciated that at this level only about 6% of the variance is
accounted for. T..evels of significance of the correlation coefficients
are given in the tables.
Twelve subdivisions of principal profile forms (classification of
Northeote, 197J1) were recognised among the soils at the 50 sampling
points at the Coonalpyn site. Of these, 16 were solodic soils (Dy
soils in Northcote, 1 971$) and 18 were sandy calcareous soils with
gradational texture profiles (Go soils in !Iorthcote, 197k). Taking
these two groups separately, “white cyst” counts in the Dy soils were
2 7
-------
TABLE 1. leterodera avenae “white cyst” counts and some other
measurements made on wheat plants n three South Australian
wheat fields in 1977. (All means ± S.E.)
(n.s.d. — no significant difference between means)
Locality
Coonalpyn
Ruts
Calomba
“Vhite cyst” counts (300 plants)
Mean no./plant
Range
68 .9±3.6
0—32 1 1
51.7±2.7
0—286
3.75±0.78
0—158
Inter—plant spacing (500 plants)
Mean at first sampling (am)
Mean at second sampling (cm)
7.13±0.lI1)fl,s.d.
7.31±0.28)
hl.12±O.23)n.s .d.
11.71±0.311)
5. 38 ±O.27)n,a.d.
5.08±0.27)
Shoot height (500 plants)
Mean at first sampling (cm)
Mean at second sampling (øm)
36.8±0.37
‘15.6±0.110
27.7±0.72
32.7±0.1 13
31 1.5±0.81
37.7±0.37
Shoot dry weight (500 plants)
Mean at first sampling (g)
Moan at second sampling (g)
0.92±0.011
39.85±2.53
0.32±0.02
6.62±0.38
1.27±0.06
18.15±1.09
Seminal root length (300 plants
Meanat first sampling Corn)
1301.5±57.9
377.2±23.0
668.3±38.5
Nodal riot length (300 plants)
Mean at first sampling (cm)
65.11±2.7
15.0±1.6
60.0±2.5
Gr ; Yield (500 plants)
Yield (g/m of row)
Estimated total yield Ct/ha)
211.11±1.8
1.2
8.1±0.7
0.110
111.8±0,9
0.71
Farmer’s Yield Ct/ha)
1.0
0.35
0.60
I
-------
“White cyst”
count
Sea. root
penetration
Plant
spacing
TABLE 2. Correlation coefficients between some measurements of wheat plants
and H. avenae “white cyst” counts, sampled at flowering (first sampling)
and at harvest (second sampling) of the plants, at Coonalpyn,
South Australia, in 1977.
‘Pearson’s correlation eoeffioient, significant at pcO.05,
P<0.001.
“significant at PcO.01, “significant at
00
1J
IA 1l
I i — ’
•11
U.
U)
0.01 0.58”
—0.59”
-O
0.02 0.16
0.22” 0.52”
0.27’ 0.13
0.01
Shoot
height
0.39’
—0.23
00
.r4
II
Shoot dry
weight
0.115 1
—0.23
I
Grain
yieli
O. 6*7
0.36”
-0.05
0.29
—0.16
—0.07
0.83”
0.97”
Plant
spacing
Shoot
height
Shoot dry
weight
Seminal
root
length
Nodal
root
length
“White
cyst”
count
Plant
spacing
Shoot
height
Shoot
dry
weight
First Sampling
Second Sampling
-------
TABLE 3. Correlation coefficients between some measurements of wheat plants and
H. avenae “white cyst” un, sampled at flowering (first sampling) and at harvest
(second sampling) of the plants, at Bute, South Australia, in 1977.
“White cyst” —0.02
count
0.25’
0.21 1 *
0.21$’
Shoot
0.69’”
height
Shoot dry 0.52”
weight
Grain
yield
O.68 **
0.59”
—0.21
0.52”
0.36’
0.00
0.86”
0.92”
Plant Shoot
spacing height
I
Shoot
dry
weight
Seminal
root
length
Nodal
root
lengtl
“White
cyst”
count
Plant
spacing
Shoot
height
Shoot
dry
weight
‘Pearson’s correlation coefficient, significant at PC0.05, • significant at PcO.01, “significant
at P<0.001.
00
4 J
,I, .,.4
9
—0,13
0.14 1 4”
Sen. root -0.02
penetration
0 Oil
Plant
spacing
0.25’
0 • 05
0 • 02
•r4
I
First aair ling
Second sampling
-------
much lower (mean 59.2 ± 5.6 per plant) than in the Go soils
(inean=9 1 .6 ± 5 .11 per plant), and this difference is significant
(PcO05), but the mean grain yields were 227 ± 2.8 and 23.2 ±
3.2g/m or row length, and these means are riot, significantly
different. At the Bute site six primary profile forms were recognised
at the 50 sampling points, and of these 35 were sandy calcareous o .ls
with gradational texture profiles (Go soils). Moan “white cyst”
counts per plant in the Ge soils were 1e8.5 ± 2.8, compared with 53.0
± 7.5 for all other soils and 51. ± 2.7 for al]. 50 sampling
points, while mean grain yield was 9.1 ± O.8 fn of row length,
oompared with 8.1 ± O.7g/m of row length at a l 50 sampling points.
In none of these pairs of figures is there any significant difference.
Some results for the “patchy” wheat field at Moorlands are
presented in Table Zj• “White cyst” numbers per plant in the
“poor-growth” patches were about 11 times ,those in the “good—growth”
patches, and this difference was significant (PC0.001). Shoot dry
weight per plant in “poor—growth” patches was about half that in
“good—growth” pa ohes, and this difference was significant
(PcO.05). The total length of the seminal roots per plant at the
flowering stage was much greater in the “poor—growth” patches than in
the “good—growth” patches, and this might best be interpreted as a
reflection of a difference in soil fertility between “poor—growth” and
“good growth” patches, with the plants in the “poor growth” patches
being forced to explore a greater volume of soil to obtain nutrients
because of love” fertility than in the “good—growth” patches. It is
of interest that there were much greater r.umbers of H. avenae cysts on
the longer roots in the “poor-growth” pate es than on the shorter
roots in the “good-growth” patches, and that the difference in root
length was significant (P<0 .05); in both sets of plants seminal root
length was pos 1 .tively correlated with numbers of “white cysts” and the
correlation coefficients were significant (PcO.0O1). Figures for
grain yield in good— and poor-growth patches are not easily
interpreted. It is not possiblo to make correlations for those data
on a plant—by—plant basis, as with other data in Table 11, because the
plants taken at harvest were not the same individuals as those taken
at flowering, so only the mean values at each sampling point ox the
plant and nematode data can be used and the data sets are very small.
However, taking the mean values for grain yield in g/plant, the plants
in the “good-growth” patches apparently produced about twioe as much
grain as those in the “poor-growth” patches, and this difference was
significant (PcO.05), but in neither case was the grain yield
significantly correlated with mean “white cyst” counts for adjacent
plants at flowering stage. If the grain yield is recalculated as g/m
of row length, which gives an indioa ion of the real-world production
of the crop, the mean yield in “good—growth” patches was no longer ‘
significantly different from that of the “poor—growth” patches; at the
same time, the yield in both sets of plants now became negatively
correlated (P.cO.O01) with “white cyst” counts previously made on
adjacent plants at flowering stage, and the correlation apparently
accounted for a high proportion of the variance.
24].
-------
TABLE 1$. fletepodera averiae : 3eminal root “white cyst” counts and some other measurements
fror. wheat plants in good and poor—growth patohea of a wheat field at Moorlands,
South Australia, in 1978
Good—growbh patches
Poor—gruwth patches
All plants
Seminal root “white cyst”
counts (no,/plant)
Mean ± 3.8.
(Range
5.1111±1.13
(0—80)
4
Cr )
Mean ± 3.8.
(Range)
60.811±11.29
(111—133)
r
Cr )
Mean ± 3.8.
(Range)
36.69±3.98
(0—133)
4
Cr )
Shoot dry weight Cs)
a. at first sampling
b. at second sampling
1.91±0.23
(0.13—5.35)
5.66±0.119
(0.30—18.71)
0.48’
(0.28)
—0.1(
(0.011)
0.77±0.08
(0.10—2.75)
2.60±0.27
(0.08—13.211)
0.18
(0.03)
0.01
(0.00)
1.28±0.13
(0.10—5.35)
3.93±0.29
(0.08—18.71)
—0.311”
(0.11)
-0.27’”
(0.07)
Seminal root length at
sampling (cm)
1102.7 ±63.2
(57—1937)
0.56”
0.31)
803.0 ±75.9
(1011—2060)
0.5 11”
(0.29)
637.11 ±511.8
(57—2060)
0.61 ”
(0.37)
Grain yield
a. g/plant
b. g/meter length of
row
2.17±0.18
(0.29—8.16)
36.33±7.99
C20.11—53.92)
—0.69
(0.118)
—0.99”
(0.98)
1.10±0.11
(0—4.30)
21.92±5.67
(13.52—111.28)
—0.21
CO.0 1 1)
0.81 1 ’
(0.71)
1.57±0.11
(0—8.16)
28.10±5.113
(13.52—53.92)
—0.75’
(0.56)
0.26
(0.07)
I
tiPearson ‘a correlation 2oeftloient for correlation with seminal root “w’il.te cyst” counts
‘:Correlation coefficient significant at Pc0.05, “significant at Pc0.01; ‘ significant at Pc0.001.
-------
Dj.SCUSSION
Sampling involves destruction of the wheat plants, and it must
therefore be assumed that measurements made on plants taken at the
flowering stage (first sampli ig) can legitimately be compared with
adjacent plants taken at harvest (second sampling). That this
requirement has probably been met in this investigation is indicated
by the significant positive correlations between shoot height and also
plant dry weight at the first sampling and these same measurements
made on plants at the second sampling (Tables 2 and 3).
There is no evidence that H. avenae caused significant plant
mortality; if it did, there should have been a significant negative
correlation between “white cyst” numbers per plant and spacing between
the plants (Table 1), and thin was not apparent either at the first or
at the second sampling (Tables 2 and 3). C,rain yieli does not
correlate with plant spacing within the limits of spacing found in the
fields we sampled; within practical limits, plants that are more
widely spaced apparently grow larger and produce more grain than more
closely spaced )lants (see Tables 2 and 3).
At the Coonalpyn site there was a significant negative correlation
(Table 2) between “white cyst” counts and plant dry weight at the
flowering stage, and this may be interpreted as indicating that H.
avenae causes a check to early growth of the plant. No such evidence
was available at Bute (Table 3), and at neither site was there any
evidence of this effect by toe time the plant: were mature.
There was a significant negative correlation between “white cyst”
counts and grain yield at Bute, but no such relationship was shown by
the Coonalpyn data. “White cyst” counts ranged from zero to several
hundred per plant (a very heavy infestation) at both sites, so it was
possible to examine a wide range of possible interactions. Two nets,
each of 50 plants from five sampling points, along lines at right
angles to each other across the middle of the Puts field, were
examined separately. In one of these sets of five points mean “white
cyst” counts were 75.7±7.5 per plant and in the other set they were
68.0±10.28 per plant (no significant difference). Grain yield in
the two sets was 8.7±1.11 and 5.3±0.6g/m of row length respectively
(no significant differenoe). However, the correlation coefficients
for the relatIonship between “white cyst” count per plant and grain
yield per plant were respectively —0.81 and +0.88, and these resulis
are significant (PC0.05 and PC0.01 respectively). It must be
concluded that in at least one, and perhaps in both oases, these
correlations do ‘iot reflect cause and effect relationships.
At Coonalpyn, Bute and Moorlands (tables 2,3 and 11) we found
significant positive correlations between total length of s minal
roots and “white cyst” counts on the seminal roots, i.e., the more
roots the more “white cysts”. The principal effect of H. avenae nn
plant growth and yield i.e generally claimed to derive from the
stunting of the seminal roots, which reduces their depth of
penetration in the soil, resulting probably in reduced water and
243
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nutrient uptake by the plant, and eventual reduction in yield. In
addition to measuring the total length of the seminal roots, we also
measured the seminal root penetration, i.e., the length of the longest
seminal root 1 on all plants at the flowering stage, when we also
counted the number of “white cysts” on the sane sets of seminal
roots. There was no significant correlation between this measure of
seahir)ai root growth and seminal root “white cyst” counts at Coonalpyn
or Bute, the only sites where we were able to make statistically
reliable estimates (r0.13 and -0.05 respectively). The same
correlation was done separately for Go and Dy soils at Coonalpyn,
where Go soils had much higher “white cyst” counts than Dy soils, but
again there was rio significant correlation (r=—0.Q2 and 0.1Z
respectively). Also, despite the much higher “ h!te cyst” numbers of
plants growing in Go as compared with those growing in Dy soils, the
mean root penetration at flowering stage for p] aflts on Go soils was
l’I. 1 $±O.6cm and on Dy- soils 13.8±0.6cm: and these means are not
significantly differ-ant. This is not to deny that H. avenae
infestation may result in reduced seminal root penetration into the
soil, because there is much evidence that it does so (e.g., Holdeman
and Watson, 1977L It is more likely that variation in depth of
penetration of se’iiinil roots is due to a number of factors, including
variations in soil type, micro-topography (influencing Boil moisture),
fertiliser application, and probab)y many other things, and that ij •
avenae infestation level, except in extreme cases, is not the most
important factor, or even a very important factor, in regulating the
depth of seminal root penetration in the overall picture of a farmer’s
wheat field. The depth of seminal root penetration was significantly
positively correlated with shoot dry weight, total seminal root
length, and Length of nodal roots at f’loweriig stage, at both
Coonalpyri and Bute, and also with shoot height at that stage of growth
at Cocnalpyn (Tables 2 and 3); it is apparently a fairly significant
tnd cation of the general health of’ the plant at that stage. When the
mean seminal root penetration at flowering stage was compared with
grain weight at harvest of plants from the same sampling points there
was rio significant correlation at Coonalpyn (r=-0.02 for grain yield
per metre of row length, r=—0.0 I for grain yield per plant), but at
Bute there was a significant positive correlation (r:0.52** and
r=0.il6 respectively). Apparently the plants at Coonalpyn, which
eventually grew much larger (about six times the weight) and yielded
about three times as much grain as those at Bute (Table 1), bad
recovered trcto the early check to growth, while those at flute had not
recovered.
Data from Coonalpyn indicate that a contrast in Boil types may be
reflected in a significant difference in “white cyst” counts, as the
sandy caloareous (Go) soils bad higher counts than the solodic (Dy)
soils. The difference may be due to different texture and drainage
charauter’istios of the soils, affecting ]arval motility and survival,
but we have so evidence to support this, and it may be that in another
season, with different weather conditions and soil moisture
relationsbtps, the effect would be different. Despite the differences
-------
in soil and related differences in H. avenae “white cyst” numbers at
Coonalpyn, there was no significant difference in grain yield between
Go and Dy soils; the farmer’s cultivation and fertiliser practices
must have over-ridden any differences in soil fertility between the
two groups of soils.
CONCLUSIONS
The work reported here represents results from orz]y one season’s
work, and some very simple statiatioa3 analyses of the data. This
year (1979) a more comprehensive study is in progress, at the same
sampling points, at the Coonalpyn site. At this site the B. avenae
population and its relationship to the wheat plants and to soil
variation is being fGllowed from the date ,,f sowing of the wheat right
through the season until harvest. At the Calomba site sampling
similar to that in the 1977 season is being repeated. It may be that
significant damage is done to plants by H. avenae at an early stage,
and that we did not recognise this from our 1977 sampling, wbieh began
at the flowering stage, or the “white cyst” stage of H. avenae ; if
this is so our conclusions from the 1977 season may be invalid, but so
too will be most of the conclusions of previous workers on the effects
of H. avenae on the growth and yield of cereals, since nearly all the
work that has been done in the past has been based on “white cyst”
counts as a valid measure of the H. averiae population, as related to
cereal growth and yield.
When we haie data for this season, and have completed chemical
analyses of soil samples and of plant samples from the 1977 and 1979
samples, we intend to apply multivariate statistical methods to the
data to try to quantify the contribution of H. avenae cyst, larval,
and “white cyst” population densities to an array of factors that
appear to influence the growth and yield of wheat plants.
On the basis of our results so far we conclude that, at least in
southern Australia conditions:
1 • there iB no evidenoe that H. avenae cauaes significant mortality
of wheat plants.
2. H. avenae may adversely affect wheat plant growth at an early
stage, but the plants are capable, given reasonab].u conditions for
growth later in the season, and even when infestation rates are high,
of recovering so that the effect is no longer evident at harvest.
3. the major direct effect of B. avenae observed by previous workers
in southern Australia and elsewhere is a reduction of the depth of
penetration of the seminal roots of affected cereal plants. We have
shown that reduction in depth of seminal root penetration resulted, at
our sampling sites, in reduced plant growth, at least at an ear].y
stage and perhaps through to harvest, but even in wheat fields that
were very heavily infested with H. avenae there is no dvidence that
this nematode was a o ’itioal, or even a significant factor in
regulating the depth of seminal root penetration on the scale of
245
-------
variability that is founil in a farmer’s wheat field, with an area of
30 to 0ha.
. the sampling methods we used and the data we obtained 2hou].d be
adequate to detect reductions in plant growth and grain yield of more
than about 10 over—all. No suob effects that could be attributed to
H. avenae infestation were apparent in our results,
5. our results conflict with those of much recent work in southern
Australia, especially the results of plot trials that have measured
the response of wheat plants to the application of rieznaticides, and
have attributed the measured improvements in growth and yi. ld to
control of H. averiae (e.g., Brova, Meagher ard Mc3wain, 1970; Meagher,
Brown and flovira, 1978).
Nematjcjdeg are broad-spectrum biooides, whose effects on non-target
organisms, and, for that matter, directly on plant growth, are often
drastic, and in the context of ‘ork in southern Australia are
virtually unknown. We conclude f’rcm our results that field
experiments that compare neinaticide—tr’eated plots with non—treated
plots and rely for their assessment solely on comparisons of plant
survival, growth, weight, and grain yield at harvest ara not capable
of’ testing so specific an effect as that of a particular nematode (
avenae ) on wheat growth and yield.
6. difference in soils may significantly infiLance lcvels of nematode
infestation on plant roots, but such differences in infestation levels
were not reflected iii final grain yield in out’ experiments.
7. “patchy” growth, which is common in southern Australtan wheat
fields, may possibly be due to H. avenee infestation, but our evidence
shows that in a particularly severe example that we investigated,
although mean H. avenae populations were much higher and grain yield
was much lower in “poor—growth” than in “good-growth” patches, it wi.s
not possible to show any significant causal relationship between H.
avenae “white cyst” numbers and plant performance; there is no doubt
that high “white cyst” numbers and poor plant performance were
co-variants, but they were not directly related.
8. an interesting philosophical question is r’ ised by the results we
have obtained. Here is a soil—inhabiting animal that, for most of its
life cycle, is a parasite of the roots of cereal plants, in our case
wheat plants, and we can show that at an early stage of growth of the
plants the depth of penetration of their roots may be inversely
related to the rate of infestation of the roots by the parasite.
Reduction of early root penetration may affect the final grain
production of the plant, though it seems that the plant, given
reasonable growing conditions later in the season, may recover so that
the effects of reduced root pen€tration at an early stage do not
influence the final grain yield. On the scale of- wheat fields of 30
to 4Oha many environmental factors that affect final wheat yield are
variable, and there are factors other than leveL of H. avenae
infestation that affect the depth of root penetration. How then are
we to assess the effects of a parasite of wheat roots, that is known
to be very discontinuously distributed on the scale of a wheat field,
and whose only known harmful effect is to reduce the depth of roof
penetration at an early stage of growth, in terms of eventual yield of’
2 i6
-------
grain. We believe that this can be done realistically by regarding
tne problem as one of interactions withir. an ecozystem comprising the
population of H. avenae , wheat plants, and 30113, each of which is
affected to varying degrees by many factors (see also Wallace, 1978).
To make some kind of approximation to a model of such an ecosystem it
is necessary first to design a sampling programme that is capable of
estimating relevant attributes of the populations and variability
within them, with an acceptable level of eonfidence, and then to use
statistical methods t3 a ess the relationships between the levels of
H. avanae infestation and oth w factors that may determine the
performance of wheat plants. This is what we are attempting to do,
using methods that have been success fully used in many studf en of soil
animal populations, and applying them to a problem that involves
parasite/host relationships in an agronomic context.
ACKN0 1L EDG 1 TS
We should like to thank Professor H.R. Wallace for his interest in
anc advice on this work, and for his constructive criticism of the
manuscript.
LITERATURE CITED
Barker, K.E. a..id Olthof, T.H.A. 1976. Relationships between -iematode
population densities and crop r 5pon3es. Ann. Rev. Phytopath. 14
327—353.
Barry, E.R., Brown, R.H. and elliott, B.R. 1974. Cereal cyst nematode
( Heterodera avenae ) in Viotoria: influence of cultural practices
on grain y Aelds and nematode populations. Aust. .J. Exp. Agrio.
Anim. Huab. 14 : 566—571.
Brown, R.H., Meagher, J.W. and McSwain, N.K. 1970. Chemioal control
of the cer l oyst ne’natode ( Hetcrodera avenae ) in the Victorian
Malice. Aust. J. Exp. Agrio. Anim. Husb. 10 172—173.
Davidson, J. 1930. Eelworms ( Heterodera schachtii Schm.) in cereals
in South Australia. .1. Dep. Agric. S. Lust. 314 : 378-385.
Davies, K.A. and Fisher, J.M. 1976. Factors influencing the number o
larvae of Heterodera avenae invading barley seedlings in vitro
Nematologiea 22 : 153—162.
Duggan, J.J. 1961. The effect t cereal root eelworm ( Heterodek’a
major , 0. Schmidt) on Its hosts. Irish .1. Agric. Res. 1 : 8—17.
Hiokinbothani, A.P.. 1930. Eelworm and “No Growth” patches. J. Dept.
Agric. S. Austr. 314 : 386—392.
Holdeman, Q.L. and Watson, TJ.. 1977. The oat cyst nematode
Heterodera avenae Wollenweber, 1924, a root parasite of cereal
crops and other grasses. State of California Dept. of Food and
Agriculture. Slpp. Sacramento, California.
Kort, J. 1972. Neniatode diseases of cereals of temperate climates.
In J.M. Webster (ed.) “Economic Nematolog3r”. Academic Press,
London.
2L 7
-------
Leonard, B.E. 1978. South Australian tear Book. No. 13 : 1978.
Australian Bureau of Statistics, South Australian Office.
Meagher, J.W. 1968. The distribution of the cereal cyst nemator e
( Heterodera avenae ) in Victoria and its relation to so .l type.
Lust. J. Exp. Agric. Anim. Husb. 8 : 637—6110.
Meagher, J.W. 1977. World dissemination Cr the cereal-cy3t nematode
( Eeterodera evenae ) and ita potential as a pathogen of wheat. J.
Nematol. 9 (1) : 9-15.
Meaglier, J.W. and Brown, R.H. 19714. Mieroplot experiments on the
effect of plant hosts on populations of the cereal yst nematode
( Heterodera avenae ) and on the subsequent yield of wheat.
Nematologica 20 : 337—3I$f .
Meagher’, J.W., Brown, R.H. and Bovira, A.D. 1978. The effects of
cereal cyst nesatode ( Heterodera averaae ) and Rhizoctonia solani on
the growth and yield of wh)at. Lust. J. Agrio. Res. 29
1127—1137.
Mill ikan, C.R. 19!Sa. Eelwor’m .Heterodera schaohtii Schmidt) disease
of cereals. Journal of Agriculture, Victoria. September 1938 :
l452_1168.
Millikan, C.R. 1938b. Eelworm ( ieterodera sobacbtii Schmidt) disease
of cereals - Part II. Journal of Agrioulture, Viotoria. Ootober
1938 : 507—520.
Northoote, IC.H. 19711. A Factual Key for the recognition of Australian
sol.Ui. CSIRO Rellim Press, Adelaide.
O’Brien, P.C. and Fisher, J.M. 19711. Resistance within wheat, barley,
and oats to Heterodera avenae Woll. in South Australia. Lust. J.
Exp. Agric. Anim. Husb. 111 : 399-11011.
B,vira, A .D. 1978. Assessment of yield losses in wheat due to eerea
cyst nematocJe ( Heterodera avenae ) by the use of seleotive
chemicals. In: “Epidemiology and crop loss assessment” (R.C.
Close et al. , eds). Proc. A.P.P.!. Workshop, Lincoln College, New
Zealand, 1977. pp. 27—1 to 27—5.
Southey, J.F. 1956. National survey work for cereal root eelworm.
Nematologioa 1 : 61— 1.
Wallace, H .R. 1965. The ecology and control of the cereal root
nematode. J. Lust. Inst. Agric. Sd. : September 1965 : 178-186.
Wallace, H.R. 1978. The diagnosis of plant diseases of complex
etiology. Ann Rev. Phytopathol. 16 : 379—1102.
21 18
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SOIL FAUNA IN TWO VEGETABLE CROPS GROWN UNDER
PLASTIC TUNNELS
*Moshen Shoukry Tadros and ‘Abdel-Fattah S. A. Saad
Tiznta University
Helwan University
Egypt
INTRODUCTION
In Egypt, Hafez (1939, 1947) investigated the insect
fauna of dung. El—Kifi (1957, 1958) recorded soil, fauna
under various vegetations and so:ne soil types. Tadros (1965,
1967, 3.974, 1977, 1978) surveyed tho fauna under some crops,
green lawns, and fallow field ii some districts, and recorded
the effect of some ecological factors responsible for fauna
fluctuations.
In association with a trial to harvest tomatoes, either
as seedlings or fruits in the cold season in Egypt and to
produce cucumber fru3.ts in the early season, the following
investigation was carried out with the following obj ctives;
1) To compare the fauna under plastic tunnels with that of
the open air sites in the same area.
2) To find out the effect of growing two vegetable ccops
(tomato & cucumber) on soil fauna either under the same
previous tunnels when they were covered by plastic in
the cold season, or uncovered afterwards.
3) To compare the fauna found under a tomato crop grown
under plastic tunnels with that grown in the open air.
4) To investigate the effect of some fertilizers, plant
spacing and some cucumber plantations on soil fauna.
M TERIALS Mm METH
The . experiment was carried out at the horticulture farm
in the Faculty of griculture at Kafr El-Shei1 h, 130 km to
the northeast of Cairo. Two parcels of land, each of 250
square metres, were selected f3r this purpose. It was planned
to cover these two plots by a plastic covering in the shape
of a tunnel by the aid ‘f iron bars fixed to the soil during
the cold season. The tun 1s were supplied with doors for
-------
the control of both temperature, relative humidity and to be
a way of controlling pest infestation if possible.
The first tunnel was cultivated with 21 species of
tomato. P!ants were grown on wires tied to tunnel tops.
Every species was replicated 4 times, namely 48 plots over
all the area. In every plot 16 plants were cultivated.
Every two plants were 40 cm apart.
The second tunnel was d videa into equal parts. The
front was cultivated with 7 c’icun ber species (Pecador,
Belair, Kobus mix, Fakor mix, Fablo mix, Nicracross and
Mirella). Each species was replicated 4 times (32 plots).
In every plot 7 plants were cultivated at 40 cm apart. The
rear part was cultivated with only ons species of cucumber
but differed in spacing (20 or 40 cm)and fertilization (NPK)
that was added at 3 rates to the plot.
Samples were taken by the same way described by Tadros
(1967), and extraction took place for 48 hrs in batteries of
modified Tullgren funnels. The experiment lasted for 6 mo,
beginning in November and ending by May of the same year.
RESULTS P ND DIb
COVERING EFFECTS
Total Fauna
It was c:L ar from the data that covering the soil with
plastic createri a suitable environment in which both plants
and fauna flourished. Fauna nearly doubled in soil cultivated
with cucumber species (35.87% to 64.13%) and was enhanced
in fert.ii ed tzo atn r ts (from 26,88% to 73.12%). This
result may be due to the suitable environmental factors of
tern;-.. :tire anc relati.ve humidity (RH).
The numbers in Table 1 indicated that the cover raised
both air temperature about 2°C and soil temperature about
1.5°C (at 5 cm deep) over that of the open air. It was also
clear that the covering raised the RH about 0.3%. This
variation in both temperature and RH may be a direct or
indirect cause for the faunal increase under tunnels.
250
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1: TEMPERATURE AND RH (MZAN S) DURING COLD SEASON
UNDER PLASTIC TUNNELS AND IN THE OPEN
Temperature RB
MONTHS - —
Under plastic In open Under plastic In open
January 15 C. 13.2 C. 84% 78%
February 15.2 C. 12.7 C. 76% 74%
March 15 C. 13.0 C. 78% 74%
- U
This result was confirmed in the second tunnel cultivated
with tomato. The data indicated that fauna doubled under
cover (32.40% to 67.60%).
Soil Fauna Present
Four groups of tuna were extracted, namely Insecta,
Myriapoda. Acarina and Oligochaeta. Acari’ a was further
subdivided into two groups, Oribatei and th soft-bodied
acarines.
The percentages presented in Table 2 show that the
closed atmosphere caused the soil insects to flourish more
abundantly than those in the open, since they increased
about 3 times (from 73.82% to 26.18%, respectively).
251
Table 2: EFFECT )F COVERING ON MAIN FAUNA GRCUPS
Covered Uncovered
CLASSES —
Mean % Frequency Mean % Frequency
INSECTA 299.25 73.82 106.10 26.18
MYRIAPODA 13.00 72.22 5.00 27.78
ACARINA 14.50 40.63 21.75 60.00
OLIGOcRAE1’A 0.50 100.00 0.00 0.OG
Total 327.25 —— -— 132.85 —— ——
-------
-..w... -€.raa ._.. — -
Myriapoda gave the same result as insects, (72.22% to 27.87%).
The Acar’na were not so much affected in these two different
atmospheric zones (60% to 40.65% in open iersus covered).
The authors attribute these results to the fact that this
group penetrE.tes to more than 30 cm deep (Tadros et al. 1965).
Hence acarines flourish under different microcliinatic strata
of temperature • RH, amount of organic matter and vzater table;
they were not affected so much by these limits. Earthworms
were found to flourish under the covered area (100%) only
due to the very suitable environmental conditions offered
under closed atmosphere. The agricultural operation- such
as har’owing and irrigating) carried out in uncovered plots
may be the maui reason for the escape or the death of earthworms.
SPECIFIC CROP EFFECT
The difference in cultivated vegetabie crops seemed to
affect soil fauna differently (Table 3). Fauna flourished
under cucumber plantations either under tunnel or in the
open. On the other hand, they did not flourish under tomato
plants. We attribute this to the differences in types of
root systems or to the various root metaboli am secretions
of the two selected plants (Tadros et al. 1965).
Table 3: SOIL FAUNA (MEANS) IN TWO VEGETATIONS, UNDER TUNNELS
ANI) IN TNE OPEN AIR
Vegetations Covered Uncovered
Cucumber Species (8) 212.13 118.63
Tomato Species (12) 37.05 17.76
OTHER AGRICULTURAL EFFECTS
Fertilizer
As indicated in Tabie 4 it waz obvious that the higher
the quantity of fertilizers added, the lower the percentage
of fauna obtained. This may be attributed to the direct
effect of fauna nutrients and acidity, or on the other hand,
the fertilizers or their impurities may have been toxic to
microflora.
The fertilizers added in this experiment (ammonia) make
2 .52
-------
- Pfl ..,a Cfl.. .. ..___.— —
the soil more acid, increa ing fungal growth ( i11 et al.
1975) and consequently increasing fungal feeding fauna.
Data showed such a raptd decrease in fauna ntuubers. We
attribute this fact to the toxic effects of such fertilizers,
or to the immigration of organisms deeper in soil immediately
after fertilizers applicatior 1
Table 4:
EFFECT
UNDER
OF FERTILIZATION RATIO (NPIC) ON SOIL FAUNA
TUNNELS
Spacing
Fertilization ratio
(A) High (3) Medium
Mean % Mean
(C) Low
Mean %
I —
20 cm
50.75 31.42 52.50 32.50
58.25 36.08
40 cm
42.50 17.89 72.75 3o.6:i
12.25 51.48
Total
93.25 23.37 123.25 31.49
160.05 45.24
Spacing
Total fauna. It was clear from Tables 4 & 5 that the
cioser the plants were planted, the more the fauna flourished
either under tunnels or in the outer atmosphere. Thia result
as more clear under tunnels. This may be due to suitable
environments offered by root systems as food, shelter or
suitable aeration.
Table 5: EFFECT OF SPACING ON TOTAL FAUNA IN CUCUMBER I
SPACING COVERED UNCOVERED
20 cm Mean 248.75 83.00
62.07 56.08
40 cm Mean 152.00 65.00
37.93 43.92
253
-------
I C
90
70
90
I0

20
10
• Soil faunal groups. The numbers as illustrated in
Figure 1 indicated that nearly all groups tended to flourish
with aggregated plants, except with Acarina. The variance
in some groups was so clear such as with the insecta and
Oribatei. This result may thus show that both insects and
Oribatei prefer soils planted with aggregated plants. The
importance of oribatids is known in raising soil fertility
owing to the role it jlays (Tadros, 1967). Oribatei (probably
organic matter feeder) flourish in soils of aggregated plants,
while other acarines are not so much affected owing to their
mode of living and feeding.
-‘jilt
Fig(1) The effect •f spaciflg on fiuna
,ou s
It was obvious from Table 4 that aggregated plants (at
20 cm apart) did not affect fwna so much at tne different
rates o fertilizers. This may be due to the sufficient
food in the soil, by these nearness of plants and perhaps
by the unsuitable chemical environment occurring in soil
after adding these fertilizers. With plants at 40 cm apart,
Fertilizers & Spacing
— 20cm.
=40 cm . ’
I 0
a
3. -J
U I p 0
S ft 0 U P F s
254
-------
the higher the quantity of fertilizer added, the lower the
f3una obtained. This last result shows that spacing would
perhaps give a way for the root system to grow and hence
for the fauna to flourish.
Cucumber Species
The data indicate that the differences in fauna between
the B selected cucumber species were small, but fauna x—
tracted under the Kobus-mix was higher (18.29%) than the
others, with Fakormix ranked second (14.74%). The other six
species ranged between 10—12%. These slight differences
may be due to the differences in root system form that
creat s a suitable environment in which fauna may flourish.
This last result was assured when finding the yield highest
in Kobus reaching 2.15 Kg/rn 2 and least in Sirella reaching
0.80 Kg/rn 2 .
SUMMARY
On examining the effects on soil fauna by covering the
soil during the cold season in Egypt with p1asti tunnels
our data showed that this new atmosphere was more suitable
for both fauna to flourish and plantations to grow.
iIO vegetables were grown under tunnels, namely cucumber
and tomato, in order to produce their fruits for early market
or to produce tomato seedlings in the cold period of the
year. The mean of extracted fauna under cuc .ut ber was higher
than that under tomato.
This experiment indicates that the higher rates of NPK
lessened faunal percentages, while the aggregation of plants
raised faunal percentages. There were some differences be-
tween the extracted groups in accordance with these two factors.
The fauna was not much affected by the two vegetative species.
REFEPENCES CITED
El—Kifi. A.H. 1958. The soil arthropod fauna in a farm at
Giza. Bull. Soc. ent Egypte 41 (1957): 231-268.
— . Soil arthropod fauna of an onion field, with an
evaluation to extraction methods used. Bull. Soc. ent.
Egypte 42: 388-409.
255
-------
Hafez, M. 1939. Some ecological observations on insect fauna
on dung. Bull. Sco. Fouad ler. ent. Egypte 23: 241-287.
__________ 1947. Further additions to the dipterous fauna
of dung in Egypt with some biological observations.
Thid 31 (1947): 307—312.
sill, S.B., L.J. Metz & M.H. Farrier, 1975. Soil mesofauna
and silvicultura]. practices. Pages 119-135 B. Bernier
& c.R. Winget (eds). Forest Soils and Forest Land Manage-
ment. International Scholarly Books Services, Portland
Ore, and ibrairie Vuibert, Paris.
Tac ros, M.S., A. Wafa & A.R. El-Kifi. 1965. Ecological studies
on oribatids in Giza region. Bull. Soc. ent. Egypte
49:1—37.
__________ and A.H. El-Kifi. 1967. The mite fauna of a green
lawn at Giza. Thid . 51:153—251.
__________ F.F. Mehiar & M.M. El—Kadem. 1974. Studies on
some factors affecting the population density of
oribatids in Egypt. 2nd Egt. Pest Cont. Cong. Alexandria.
pp. 517—531.
__________ G.N. Rezk & A.E. Hazem. 1974. The correlation
between the pexcentage of both organic matter and
microflora with the vertical distribution of soil
oribatids in Shoubra E1—Xhima region. 2nd. Pest. Cont.
Cong. Alex. pp. 471-479.
___________ 1975. Ecological studies on soil oribatids in
Kafre E1-Sheikh region (ABE). Bull. Zool. Soc. Egypt
27: 85—89.
__________ 1976. The role of soil fauna in the decomposition
of organic matter. zool. Pnz. Jena. 196 (5/6): 347—356.
___________ 1978. Effect of some herbicides on soil fauna.
3rd Pest Control Conference. Am Shame Univ., Cairo.
pp. 341—345.
__________ and LA. Saad. 1978. The distribution of soil
microfauna on drainage banks. 4th Conf. of Pest Control,
NRC. Cairo, pp. 227—232.
256
-------
--
BEACH SOIL MICROFAUNA iN LOWER EGYPT
Mohsen Shoukry Tadros
Tanta Uir,v r ity
Egy
INTRODUCTION
It was of great interest to investigate the coil
fauna on the seashore to get an idea about this new area
especially in a town where the Faculty of Agriculture at
Kafr E1-Sheikh is situat ’d. The selected town for this
investigation is Baltim; t is situated about 135 km north-
east of Kafr El-Sheikh and about 245 km to the north of Cairo.
Investigators working on seashore soils include
Luxtor. (1964, 1966) who made a series of ecological inves-
tigations oi the salt marsh acarina in southern Wales.
Webb et al. (1971) worked on cryptostiginata occurring in a
sandy heathland soil in southern England. Fujikawa (1972)
recorded the results on the zonal changes of oribated fauna
in vegetation of the Ishikari seaabc re near Sapposo, Japan,
and Cancela de Fonseca (1975) studied the colonization of
fresh litter by aid of ima. algae and fungi in two soils
of a beach forest in France.
In Egypt, there are no records about the seashore fauna.
and therefore, the present investigation was planned to learn
about the horizontal and vertical distribution of species
either in non—cultivated or cultivated areas from plots beside
the seashore and away from it.
METHODS ND TECHNIQUE
The research area was situated on a peninsula between
the Mediterranean Sea and Borolos Lake. Cultivations were
not grown regularly in the area, but one finds green plots
beside sandy ones owing to the nature of the soil itself
and to the total suspended solid content.
Samples were taken during the winter from six plots
257
-------
representative of a horizontal distribution of the whole area.
These plots were scattered either close to the sea or about
0.8 kin (0.5 nti) away iron it. Three types of samples were
taken, the first from plots close to the sea and never culti-
vated, the second from plots like the first but cultivated
with ordinary field or vegetable crops, while the third was
from orchards, some near the seashore and others 1.6 km (mi)
away from se shore. The winter crops on the second plot type
were beans, wheat and alfalta. Pious was the only plant grovzn
in the orthards.
The sampling procedure was discribed by Tadros et al.
(1965) and was representative of the vertical distribution
of the soil. Samples we]e taken of the disturbed sc.LJ. layer
(0—20 cm) and undisturbed layer (20—40 cm) below. Extra
samples were also taken from a plantation beside the seashore
arid away from it for about 2 km to represent the horizontal
distribution. Extraction for 48 bra took place using batteries
of modified Tuligren funnels.
RESUIJ1 S ND DISCUSSION
Extracted Fauna Groups
From six plantations in the test area 10 different
organisms were extracted; they were all arthropods and belong-
ing to three classes, Acarina, Tnsccta and Myria oda. Some
species of Chelontida were collected. Col1emb ,1ans were the
prevalent species extracted from all the tested fields
followed by Glycophagus destractor (Shrank). These results
are similar to the findings of Dinda]. and Metz (1975).
Total Fauna and Cultivations
It appears that alfalfa and beans were the crop lands
most preferred by so.1 fauna while tomato was the least
(Figure 1. Table 1). Tauna were also present in fallow
fields but iii low percentages, e tcept for the Acariria (82.35%).
This result may be due to the crop residues left on that soil.
Microflora work on the cast residues decomposing it to a grade
which is favorable to microfauna. This process on cultivated
lands happens without any human assistance. The different
percentage of faunal group fluctuations in the six tested
plots plus the uncultivated area may be due to the nature of
258
-------
— —. — — . — —.— — ,. 4.•_...#,...,. •.. __._ ,_ ,____
TEST
ITES
iiN .N\
FAUNAL
,
a)
i
I.
‘ .4
!4.4 41
Ui 101 41
41

,k 1 1 Li
Id ._‘
“4
g ‘-4 0
r41 I d
INSECTA
71.73 58.75 41.87 25.65 46.43 17.65 60.00
ACARINA
20.14 41.26 67.22 74.35 53.35 82.35 40.00
MYRIAPODA
3.53 0.00 4.55 0.00 0.00 0.00 0.00
Table 1: PERCENTAGE S OF THREE FAUNA GROUPS OCCURRING IN
UNCUIIPIVATED AND FALLOW LAND AND FIVE PLANTATIONS
Bulk
Density
g/cm
Water
content
%
Porosity
%
pH
Organic
matter
%
Total
Fauna
%
Uncultivated
land near
seashore 1.54
0.94
41.62
6.77
0.02
0.50
Cultivated sea-
shore land with
crops 1.72
1.62
35.02
7.60
0.90
95.60
Cultivated
land with
ficu 1.22
6.00
54.02
7.58
0.88
3.90
Table 2: ANALYSIS OF SOME IMPORTANT PARAMETERS OF THE CHOSEN
SOIL NEAR THE SEASHORE
259
-------
.
RCCU.EMBOLA
INSECTA
so SOFT ACARINA
70 M0SS MITES
MYR IAPO0A
TOT. FAJJMA
‘o.
50
40. h
o 30 . ,i N I
3.
11 1 LII
SEANS ALFALFA FICUS WHEAT TOMATO FALLOW UNCULTIV.
Fig.(1): Numbers fl percentages important hurlS coups iri jive
plantations, fallow I. un-cu1ti ated airs.
the different root systems of those plantations.
Bulk density; water content, porosity, organic matter
and pH differed between sites (Table 2). The uncultivated
land, close to seashore had a relatively high porosity, low
wate’ content and low percentage of organic matter that pre-
vents some fauna groups from occurring. In the soil of culti-
vated seashore lands the Insecta were the most prevalent
taxori. The percentage of organic matter and porosity had a
clear effect on the faunal distribution.
Main Fauna Groups & Cultivations
Acarina was the prevalent group in four of the seven
tested sites (Figure 1) • while the Insecta dominated the
three remaining areas. This result is due to either spring..
tails or Coleoptera occurring at high rates in alfalfa, wheat
and in the uncultivated area. Myriapoda were present only
in legume crops. This result may be due to the trophic
characteristics of these animals for they eat fungi and
decomposed orgmic matter that may be offered at high rates
in the rhizosphere of the leguminous plants.
260
-------
The Vertical and Horizontal Distribution of Fauna
About 70% of the fa ma was extracted from the upper
layer (0-20 cm) of the soil surface (Figures 1 and 2).
This result may be due to the characteristics of sandy soil,
its porosity, and the amount of organic matter within it,
resulting from its cultivation with crops. Also, most soil
fa ina are fungivorous or organic matter feeders and those
conditions are more prevalent in the upper soil strata.
In measuring fauna horizontal distribution (Figure 2)
it was clear that the peak occurred in plots which. were about
420 in from the sea. This fact may be due to total soluble
salts and needs further investigation.
a
C
a
S
E
.5 40C -
C
3OO.
0
204060 10 2 3X 400 900 200Dm.
Distinci horn tho I
FIq(2): Nor zontol dIstribut Sfl •f totsi I una
SUMMARY
Seven plots of land ranging from the seashore inland
were selected to deterzuine soil microf&una occurring within
it. These plots were situated in a peninsula between the
Mediter .anean and the big Borolos Lake. In this new area
ordinary crops and orchards were grown up in only some
scattered plots.
All extracted organisms were arthropods. Acarir.a was
a prevalent group in four out of the seven examined planta-
tions. On the other hand, Insecta flourished in the unculti-
-ated plots, while Myriopoda was c,xtracted only in soils
cultivated with legume crops • It was found that high percent-
261
-------
ages of fauna flourished in the upper soil layer. The author
attributed this distribution to: presence of plantations,
water content, porosity, pH, and faunal interactions with
microflora in the rhizosphere.
REFERENCES CITED
Cancela da Fonseca, J.p. 1975. Observ3tions preliminair s
sur la colonisation par les microorganismes et par
Les niicroosthropodes de la litiere fraiche de deux
sols d’une Eetraie (Foret de Retz). Pedobiologia 15:
375—381.
flindal, D.L. and L.J.. Metz. 1977. Co unity structure of
collen bola affected by fire frequency. Pages 88-95
in W.J. Mattson (ad). The Role of Arthropods in the
Forest Ecosystem. Springer—Verlag, NY.
Fujikawa, T. 1972. Oribatid fauna in several differeut
vegatations along Ishikari seashore, Appi. Ent. Zool.
7(3): 173—176.
Luxton, 14. 1964. Acarologia, Fasc. hs.: 172—182 CR ler
Cong mt d’Acarologic (1963).
- 1966. Acarologi 8: 163—174.
______ 1972. Studies on the oribatid mites of Danish
Beech Wood soil. Pedobiologia 12: 434-436.
Tadros, M.S., A.K. Wafa & A.H. El—Kifi. 1965. Studies on
soil oribatids in Giza region. Bull. Soc. ent. Egypte
49(1): 1—37.
Webb, N.R. & G.W. Elnes. 1971. The structure of an adult
population of Ste nacarus magnus (Nic.), Cryptostigmata.
Proc. 3rd mt. Cong. Acar., Prague (1971):135-137.
262
-------
EFFECT OF NPK COMPLEX FERTILIZERS ON YIELD OF
PADDY RICE AS RELATED TO THE FAUNA AND WATER
INFILTRATION RATE OF SOIL OF THE NILE DELTA
S. E-D. A. Fa zy, M. Tudros, S. A. Gaheen and S. El Krady
Uiiivrr ity of Toulo
Egypt
Abstract :
Several ecological factcre have been changed after the building
of the Aewan Dam (1963) • The annual. rate of K—replenishment
of Fgyptian aoila must have been reduced as a result of the
sharp decrease (97%) in suspended matter (largely K-bearing
mineral.) in the Nile river. Therefore, field experiments
were conducted an the alkali saline a1 Luvia1 (55% clay) soil
of Kafr El Sheilth . to test the effect of MI 4 . •a pellets,
NP and NPK viking ship complex fertilizer (from Norsk Hydro,
as.) co grain yield of tiø paddy rice cultivara (Giza 172
and 1R579) as well as soil fauna (insects • acarina and
colleabola) and rate of vertical infiltration of water. The
results showed that the yield of cv. 579 was significantly
higher with NPX- (454.g/nii 2 ) than NP— (346.g/m 2 ) or N— trea 4 ” ’tts
(3D8.g/m 2 ). Similar trend was observed with cv. 172. The
yield of rice grains increased hyperbolically with increasing
density of colleabola up to 140/kg) further Increase in
colleabola to 320/kg soil did not affect the yield. The
density of acarina increased hyperbolically to 24/kg with
increasing the dry weight yield of roots per bill. The grain
yield as well as the density of coll bola were negatively
correlated with the infiltration rate bicb varied from 0.1
to 1.3 am/mm. In different treatments. At a constant N,
the density of insects was found to decrease (from 20 to 4/kg)
wi.th increasing K level • thi, decrease was observed with cv.
579 but not with cv. 172.
263
-------
Introduction :
For thousand of years f ioathng of the Nile river resulted n
the deposition of suspended K—rich city into the soils. The
process provided Eç ypt with an untapped source of K-
repleniabmant . The warm Mediterranean climate prevailing
in this area as well as the constant availability of irri-
gation water • provided elements for a very Intensive
agricultural systee, producing two to three crops annually.
About 97% of the suspended matter (Helal and Rasheed 1976)
was last after the construction of the Aewan Dam (1963). About
one fourth of the annual consumption of P was last as a
result of the construction of the Dam (Balba • 1979). Whilst
th€ dThsolved K in Nile water was unaffected by the Dam,
about 91% of the annual deposition of K into the soil was
lost (Balba 1979). This situation may be aggravated by the
present consumption of very high rates of N in relation to
P with virtually no K. Mcanwhile EH 4 -N fertilizers were
found to inhibit K uptake (Faizy, 1979) from the soil solu-
tion (Grimmee, 1974) • On the other band the susceptibility
of plant. for fungus infection was highly increased at low
K and high NH 4 —N fertilizc. ion (Faizy, 1973). The physio-
logical, Morphological and phenoligical changes which were
usually induced following fertilization were found to
affect the population dynamics phytophageous insects
(Bogenschutz and Konig, 1976). A decrease in the density
of soil fauna .as reported following fertilizat’on (Ronde,
1957 and Beckan, 1972). Soil physical properties, such as
high compactnaas and low per ability • were found to have
a determinable effect en soil fauna (Wileke, 1963).
Since NPE compound fertilizers have naver been used In
Egypt it was therefore a e of the objectives of th 4 .a study
to compare the effect of straight N fertilizers with that
of NP and zv
-------
compound fertilizers on the yield of two paddy ric cultivare
as well as their influence on the density of soil fauna and the
response of soil fnsecta to different rice cultivare. The
relationship between water infiltration rate and density of
collambola and grain yield was investigated.
Materials and Methoda :
Two paddy rice (Oryza Sativa) cultiva:s IR.579 (indica, lang—
grain) and Giza 172 (Japonica. short—grain) were cultivated
(June — October 1978) in Kafr Bi Sbeikh.
The seedlings were trannplanted on July, t tellering the
equivalent of 50 Kg of N per acre of different straights as
well s NP and NPK viking Ship Complex fertilizers (Norak
Hydro a.s.. Oslo. Norway) were to field plots (3 x 3.Sis) using
the two cultivars in a rancbmized split plot design with three
replicates. At harvesting, straw and grain yields were air
dried, divided and wei ied. Th. least significant difference
was estimated by the t-test according to Speigel (1972).
The soil used was of the a’luvial sodic type with 55% clay,
2% carbonates and a pH of 8.2. The soil ha a relatively hi
ground water table (1 meter from surface 1 • By the end of the
growing season and after drying off the fielda, the water
infiltration rate was meaanred by the uble—ring infiltro-
meter. according to Gaheen and Njos (1978). At the same time
soil samples from the rhizu phere were tahen • Piom these
samples soil fauna were extracted, counted and differentiated
according to Tudros at al. (1965).
z6
-------
Results and Discuapion :
The qffect of different fertilizer trea m .nts on grain rice
yields (table 1) was such that the yield of cv. 579 was
genarally higher than that of cv. 172. However, with the tvo
varieties the yield was genarally, significantly, higher with
the NPX than the NP or N trea ’ ts. This result suggested
that K was a limiting factor for rice prodi tion In Egypt.
Ameonium sulfate was found to decre ass rice grain yield
(Helal, 1975). On a similar soil a significant increase in
yield of corn (Nafadt and Gobax, 1975 and Faizy, 1979) and
seed cotton (Paizy, 1979) were reported with K-fertilizers.
With the t cultivars of rice, the highest yield was obtained
with the 21 7 14 grade. Indicating that unlike in cotton where
the highest yield was obtained with a fertilizer having an
N/K 2 0 ratio of 1 or less (Faizy, 1979), In paddy rice the most
suitable N/K 2 0 ratio was 1.5 (Ismunadji et al. 1973).
The grain yield as well as the density of soil fauna was
higher with urea super granules than ordinary urea (Becham,
1972). indicating that the slow rate of urea granule diaaolution
was more favorable. Alternatively, the increase in the density
with the 23 23 - than the 20 20 - seemed to be due to the high
rate of water soluble P of the former than the latter grade.
It was of interest to note that the density Cf collembola was
positively correlated with th. grain yield (fig 1). The yield
increased hyperbolically with increasing collembola and leveled
o ! at abont 70 c ollembola/5OOg soil. The density of collembola
was & imilarly related to the dry weight of roots (fig 2).
These observations suggested that the density of collenbola
might be taken as a biological test for soil productivity
(Buckle, 1921, and Brauns, 1955). The dry weight at root of
266
-------
Table 1: The grain and straw yield as well as the density of total
fauna of t o rice cultivara as affected by different
fertilizer treatments.
Figures followed by same letter are not significantly different at
L.S.D. of 1 and 2 are 95,4 and 90.4. respectively.
I
I
-K
+K
0 K 0
25 2

( 4)2504 — —
t hea — —
Grain q./aq.m
T’ T cv.579
Straw 2 g./sq.Tn
1
cv.172 cv.57
rotal fauria/500g
soil
cv.172 cv.579
315.3bc
308.0 c
f 4T •
526.7 f
611.7e
754.7 d
646.7e
164.

30.
76.
Urea — —
aranule a
20 —
2 5i

355.7 b
327.7bc
69476e
C
851.7 c
620.7 e
74.
26.
99.
38.
23 23 —
239.7 c
TTT
611.7 e
656.7 e
44.
42.
20 U. 11
34.7 C
357.3 b
663.3 e
539,3 f
43.
36.
[ 5 15 15
237.7 c
3T757ób
715.Ode
713,3de
54.
18.
25 7 7
J34.4 b
376.Oab
723.3 d
990.0 b
161.
64.
11 14
45,7 b
390.O b
1 e
691,Ode
94.
166.
21 7 14
109.3ab
TT a
.099.3 a
93.
70.
L.S.D.
11.5
‘ T
116.2
—
—
-------
a.
U I
4OC
m
a I.
iK c t 579
+ K . 172
- Kcv.579
- Kc. 172
80 160
de (ty or collembola/500g.
fig. 1. The relationship between the rice grai.i yield and
density of collambola for the t rice cultivar ,.
T e o ashed vertical line represents the limit of
r€sponae of collembola to yield increase.
v. c i ,
120
thisik ot coflenbola/500g.
ftg. 2. The relationship between dry wei rit of roots and
density of collembola in rhizoephere of t rice
cult vara.
I
a
I
0
Cv. si
268
-------
the t rice varieties were also hyperbolically re1ate to
the density of acarina (fig 3).
The rice grain yield as well as the density of collembola
were negatively correlated with the water infiltration rate
(fig 4). In contrast to Wilcke (1963). this surprising
result might be due to the high salinity of the soil, which
might have caused ao subsurface cracks upon drying
(Russell, 1972).
At a constant N supply (50Kg/acre), K and P ere increased
(from 14 to 50Kg/acre) with different NPK grades (table 1).
The influence of this i icreaae on the density of insect
population was such that .th cv. 579, the density decreased
(fig 5), whereas with cv. 172 the density increased (fig 6).
This striking difference suggested that soil insects were
not only related to species (von ndem, 1974) but were also
a function of the cultivar. It was therefore tentatively
suggested that the insects might have been either feeding
on root-parasites or the root itself of cv. 172; whereas
with cv. 579 which was found to have a high response to K
fertilizers (von Uexkull. 1976). This K might have given
the cv. 579 a thicker and harder root cell walls or a low
palatability (xengel, 1976, Ismunadji. 1976, and Troildenier
and Zebler, 1976) and thus rendering it more invu1 ierab1e
to invasion of parasite and soil insects.
With the different fertilizer treatmanta, the acarina made
up about 10% of the total density of fauna. This percentage
was vary low wh6n compared to that (45%) reported for the
acarina of a bar soil from the same area (Tudros. 1975).
This differer e might be mainly due to water submergence
and the resultant reducing conditions which are usually
induced in paddy rice f±elds.
269
-------
fig. 3.
E
: 2
a,
200t
a
I.
• Cb .Pv
• C I7
WUteratLon cm/m n.
fig. La. Relationship between grain yield of two ri ce cul-
tivars and water infiltration rate.
fig. Lb. Relationship between d isity of collnbola in
rhizosphere and water infiltration rate for two
rice cultivars.
c . r t
c v.
2
de,s(ty of acarula/5 009
The relationship between dry wv ight of roots and
lensity of acarina ‘n rhizoaphere of two rice
Cu iti vars.
• . .
• CV.(7*.
S
I. •
• S .. U
•
120
S
I
I
U
S
8 1.2
LnfLlteráUon crvØnin.
r.
270
-------
50 K 2 0 tg./acre
fig. 5. Density of insects per 500g. of rhizo ipbere soil
as affected by variation in K- and P- at a constant
N—f ertiliz at a.
50 KO Kgy cre
Kg ./acre
fig. 6. Density of insects per 500g. of rhizosphere soil
as affected by variation in K- and P- at a constant
N-fertilizers..
C
1o.
op. cr
0 I 0 I
-------
References :
1. Balba A14. (1979). a. Environ. Qual. 8:153—156
2. Becham, V. (1972). M.Sc. Thesis. McGill Universi.ty
p. 175
3. Bogenscbutz, H. and E. Konig (1976). Potash Rev.
Subj.23, 49th suite 6/7 p.15
4. Brauns, A. (1955). Neves ardtiiv F. Niedersachsel.
ag. (113):1—18.
5. Buckle, P. (1921). Ann. App. Biol. 8:135—145
6. Faizy S.E-D.A. (1978). Proc. mt. Arid Land. Conf.
of Plant Resources, Texas Tedi Univ. (in print)
7. Faizy, S.E—D.A. (1979). Agron. Abet., p.170
8. Faizy, S.E—D.A. (1979). Proc. 14th Co lloq. mt.
Potash Inst., (in print)
9. Gaheen, S.A. and A. Njos (1978 . Scient. Reports
Agric. Univ. Norway no. 88:1—11
10. Grinmie, H. (1974). Proc. 10th mt. Potash Inst.,
113—18
11. Helal, N.E. (1975). Egypt. J. Soil Sci., Special
I,sue, 75—83
12. Helal, N.E. and M.A. Rasbeed (1976). Egypt. a.
Soil sci. 16:1—8
272
-------
— . .- — .-
13. Isinunadji. 14. (1976). Potash Rev. aubj. 23. 49th
suite 6/7 p. 17—19
14. irnnunadj. M. L.N. Hakim, I. Zulkarnaini and F. Yazawa
(1973). Contribution Central Res. Inst. Agric.
Bogor, No. 4, 10
15. Mengel. K. (1976). Potash Rev. subj.. 23, 49th suite
6/7 p. 17—19
16. Ronde, G. (1957). Foratwiss caitbi. 76(3/4):95—126
17. R ssel1, E.W. (1961). Soil Conditions and Plant Growth,
9th editn, Longmane. Lonthn, p.378
18. Speigel. 14.R. (1972). Theory and Pz b1 na of statis-
tics in 51 iinita. McGrow & Hill, New York., p.188
19, Trollendenier, G. and E. Zehler (1976). Potash Rev.
subj.23. 49th suite 6/7 p.6
20. ‘Pudros. M.S.(1975). Bull. Zool. Soc. Egypt. 27:85—89
21. Tudros, M.S., A. Wafa, and A.H. El—Kifl (1965).
Bull. Soc. Ent. Egypt XLI:231—268
22. von Emdem, H.P. (1974). Peat Concrol and its ecology.
Edward Arnold. Lonthn
23. vc Uexkull., H.R. (1976). Aspects of Fertilizer use
in n edern high yield rice culture. mt. Potash
Inst. Dull, no. 3
24. Wi3 .cke, D.E. 1963). Z. Acker—u. Pf. Bau 118:1—44
273
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THE ABUNDANCE OF SOIL ANIMALS (MICROARTHROPODA,
ENCHYTRAEIDAE, NEMATODA) IN A CROP ROTATION
DOMINATED BY LEY AND IN A ROTATION WITH VARIED
CROPS
Olof Andr n and Jan Lagerlöf
cu’, i,.I, L bitt yr.JI ,, ill Ay ii ,iIhi,ai S i tin, r
.‘J;L l•lIi’
The of fe ts of different cropping systems on the abundance of soil fauna
is studied as a part of the project:
“Ecological systems in arabic land” at the Swedish University of Agricul-
tural Sciences.
This is a preliminary feport from a soil fauna investigation in an a ri-
cultural field trial, located in As near Ostorsund in central Sweden,
where a crop rotation dominated by icy (short-term gras 1and) is
compared with a rotation with varied crops. The trial was started in
1955. The experimental plots measure 19.0 in x 6 . .q in and arc replicated
in two blocks. All crops in both rotations are grown every year, so it
is possible to study all years in a rotation at the same time.
(See table 1.)
Crop rotation 1 represents a farm with dairy cattle whore all crops arc
used on the farm as forage and large amounta of farmyard manure arc pro-
duced. Crop rotation 2 represents a farm without cattle t here all crops
are sold and n farmyard manure is available.
Tablel. Long-term field etpvrlriient with different cropping Systems at ns. noar I Sterstind in entral Swede,,. Soil
fauna investigations were carried out in the tr atiiient• undeiHred.
CROP ROtATION LROPROTATICN2
Iortii,zatioi , kg x ha 1 Uertil ,2aj ,on I g ha
Crops —— Crops - - - - — - - -- —-. —--—— -
II P K ramyard manure i. P K Farmyard marjre
Barley under own Barley undersowii
c€1rTeLm mture 10 3’, 60 30 m IC wT1TTijF 30 25 bO
Lny. year 1 90 .. - - fa llow 30 —.
Lay, ye 2 90 1!. 60 AuLuii ,i- uw, , rye 50 25 81)
Ley. year 3 91) 15 60 15 25 ,‘a
Le . year 4 90 IS -- 30 z Potatoes 10 1’ 35 260
90 :s 40 —- Carrots i 35 14L
46C 95 220 60 a It. 3 300 145 5110
.. ‘ -I.
-------
2-
The soil of the experimental site is a clay ]‘am with about 7 00 organic
matter. The p 1- 1 of water extract is about 5.9. In 1966 investigations
showed differences in soil physical properties crcatcd by the different
crop rotations (Uãkarwson 1968). The mean porosity was significantly
higher (p < 0.05) in rotation 1 than in rotation 2 when barley undersown
with icy mixture was growi (54.4 arid 49.9 00 by volLune respectively).
Analyses for orgai ic carbon in 1972 showed a hi3hcr levol in rotation 1
than in rotation 2 (3.68 and 3.26 0 by weight respectively).
The soil fauna samplings were carried out iii Sep cmbcr 1977. To compa c
the crop rctations, samples were taken in barley undersown with by
mixture in both rotations. To compare the five year old icy in crap
rotation 1 with the succeding barley iatdcrso ’n with icy mixturc. the five
year old icy was also sampled.
The fauna groups studied were:
Microarthropoda : only Collembola and Acari arc discussed here. Other
arthropcd groups were also recorded but their abundance was to low to be
measured accurately with the smuili sample units used. Collemboki arc
classified as one group. Acari have been divided into the suborders
Me ostignata, Prosti ata, Astigmata and Cryptostigmata. Among the
M sostignata only the cohort Gamasina wa found.
Exichytraeidae : this group has not been divided further taxonomic:aily
Nematoda : this group has been divided into ecological feeding groups
after Banage (1963), (figure 2).
Sampling for Microarthropoda was mad’ with a cylindrical soil corer with
a diameter of 33.5 nun. The sampling depth was 0-10 cm. 20 sample units
wore taken in each treatment, 10 from each plot. The animals were extrac-
ted with a high gradient canister extractor (i4acfadyen 1961) further
developed at the Mols laboratory in Denmark (Pcrsson & Lohm 1977,
Petersen 1978). Sampling for Enchytraeidae was performed with a cylindri-
cal corer of 5. , nun diameter. The sampling scheme was thc same as for
Nicroarthropoda. The ar.ii.ials were extracted with a modified Bacrman
üamel method described by Otonnor (1962). Samples for nematodes were
taken with a soil borer of 20 nun diameter to a depth of 20 cm. 30 random
samples from one plot were pooled. 4 pooled samples were taken in each
treatment. The nematoc 1 cs were extracted according to the method descri-
bed by Seinhorst (Southey 1970). The microarthropods and enchytracius
were counted under a stereo microscope (5 - 40 X) and arithmetic means,
standard errors, ANOVAs and Duncan’ s tests werc compuLed with BMDP
computer programs from UCLA, U.S.A..
The results from the Fnchytraeidae and Microarthropoda investigations
are shown in figure 1. Generally speaking the different soil animal
groups show a tendency of decreasing abundance as folluws:
Five year old by in crop rotation 1. > Barley undersown with iey mix-
ture in crop rotation 1. > Barley undersown with ley mixture in crop
rotation 2. The results from the nematodc investigation show the same
pattern as the Microavthmpoda, although the differences are not signi-
ficant (figure 2). The distribution between the ecological feeding
groups is constant with a majority of plant md fungus feeders.
275
-------
Individua ls
600 (X)
50000
40000
30000
Figure 1
Enchytrasidae aM principal groups a
in the field eaperimert
at As. near Ostersund
Individuals rn- 2 . 0 —10cm depth
4a significantly different from barley
undersown with Icy mixture in crop rOtation 1 (p’O 05)
Mean of 20 sample units per treatment
N
at
20000
1000u
Scan
.%rari
Scar.
-------
md m 2
7 10 - PL = Pt nt and fungus feeders (Tylenchida)
Mc MicrobiaL feeders (Rhabdit ,da.Monhysterida.Araer 1aurnuda)
6 .i06 Ms = MisceLLaneous feeders (DoryLaimida)
P = Predators (Mon nchidae)
5.106 U = Unidentified nematodes
4.106
3.106
2.106
106 — — __________ —
Pt Ms 1 Li PL 4 Ms 4 U Pt 4 Ms 4 U
Mc P Mc P Mc P
Five year old Ley. BarLey unc r— BarLey under—
Crop rotation 1. sown with Lay sown with Ley
mixture. mixture.
Crop rotation 1. Crop rotatu’ n 2.
Figure 2.
Nematoda of dltferent eco’ogicaL feeding grc ups in the fieLd
experiment at As near Ostersund. Individuals -m 2 ,
0 —20 cm depth. Means of 4 pooLed sampLes are shown with their standard errors.
It is not surprising that the old ley has the greatest abundance for
most of the groups studied. The soil has not bcen ploughed for five
years, the surface has been constantly covered with vegetation and a
great root biomass has developed.
Li barley undersown with ley mixture in crop rotation 1 the abundances
of Coilembola, Gamasina, Cryptostigmata and Enchytraei ae are signifi-
cantly lower than in the five year old ley by which it is preceded in
the rotation. ProF ibly ploughing is the main factor involved. Similar
effects of plough.ing have been reported from other investigations
(Edwards & Lofty 1969, Ryl 1977. Collernbola are reported to recolonise
rather quickly after plougiung while Gainasina and Cryptostigmata are
slower (Sheals 1956) probably due to longer generation time. The Acari
group Astigmata shows a higher abundance in barley in rotation 1 than in
the other treatments, especially the deutonymph stage, hypopus. The
Astigmata seem to have derived advantage from the decaying roots nd
litter resulting from the ploughing of the icy. The addition of farmyard
nure is probably also important, as earlier experiments show (Marshall
1977).
277
-------
Barley in crop rotation 2 has low -ibundances for most soil animal groups
ii.vcstigatcd. The mite group Prostigmata ts an ObV.LOUS CXCeI)tiOn, with a
ir an abundance four times higher than in thc other treatments. A]most
all Prostigii ta found here belong to the 3uperfanhily Tarsoneiridjc,
small forms measuring areund 0.3 mm or less in body length . These small
n 1 itcs i hich a e fungivores, plant feeders or insect associates seem to
have a greate’ chance to exploit the soil in crop rotation 2 than other,
larger forms which might hav difficulties bccause of the low I)OrOSitY,
the changing environment with soil cultivatioii every year and the less
st 1 L’1e humidity and temperature conditions than in crop rotation 1. The
scarcity of competitors and predators probably give this group a better
chance of suivival in this treatment than in the others.
The authors would like to express their gratitude to the staff of the
Division of Nematology, S %edish University of Agricultural Sciences for
t’tc extractic n and analyses of the nematele samples.
REFERENCES
Banage, t .B. 1963. fhe ecological importance of free—living soil
nematodes with special reference to those of noorland soil.
- J. Animal Ecology 32(1):133—140.
Edwards, C.A. & LoFty, J.R. 196g. The influence of agricultural practice
on the soil microarthropods.
- In: Sheals, J.C. (Ed). Systeinatics Assoc. Pubi. 8:237-247.
HJkansson, I. 1968. Markfysikaliska stud er i ett växtföljdfbrsök pA
As den 15—16 juli 1966.
- Rapporter fran jordbeaibetning avde1ningen, Sverig s lant-
bruksuniversite -, Uppsala, Nr 8, 13 pp.
i’Iacfadyon, A. 1 961. Improved funnel type extractors for soil arthro-
pods.
— J. Anim. Ecol. 30:171—184.
?1arshall, ‘.G. 1977. Effc cts of manures and fertilizers on soil fauna:
a review.
- Commonwealth Bureau of Soils, spec.publ. 3, commonwealth
Agricultural Bureaux, England, 79 pp.
OConnor, F.B. 1962. The extraction of Enchytracidae from soil.
- In: Murphy, P.W. (Ed.). Progress in soil Zoology. The Hague,
279—285.
Persson, T. & Lohm, U. 1977. Energetical significance of the Annelids
and Arthr pcds in a Swedish Grassland soil.
- Ecol. Bull. (Stockholm) Nr 23, 211 pp.
Petersen, H. 1978. Some properties of two high grbdient extractors for
soil wicroarthropods and an attempt to evaluate their ex-
traction efficiency.
- Nat. Jutlandjca (20):95-122.
278
-------
Ryl, B. 11)77. Enchytraoids on rye a .1 potato fields in ‘rure% .
— ELO1. Pol. 25(3):51.-529.
Sheals, J.G. 1956. Soil population stud.es. 1. The effects of cultiva-
tiori ard treatmc nt with insecticides.
— Bull. Ent. Re:. - 7:8O3—822.
Southev, J.F. 1970 (Ed). Laborator’ methods for work with ilant and
scil nematodes.
— \1..’LS.S. tech. Bull. 2, ed., London.
279
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COMPARISON OF MINERAL ELEMENT CYCLING UNDER TILL
AND NO-TILL PRACTICES: AN EXPERIMENTAL APPROACH
TO AGROECOSYSTEMS ANALYSIS
Benjamin R. S’inner and D. A. Crossley. Jr.
Univen.zy of Georgia
USA
The sofl fau ia. of cultivated agronomic systems is notoriously
lirproverished, suppc rting low populations of 5011 arthropods In compar-
ison with uncultivated, natural forest or grassland ecosystei’ (Edwards
and Lofty, 1969; 1973). Tillage practices can cause appreciable
disruption of soil structure and biological conuiiunlties (Allison, 1973).
Cultivated soils also show large decreases in organic matter compared
to untilled soils (Brady, 1974). Typical modern agricultural techniques
replace naturally occurring soil structure and function with a virtually
sterile medium for culture of a single crop species at high density.
It is ironic that much of our knowledge of physical and chemical pro-
perties of soils, and even microbial properties, is derived from studies
of such highly modified systems. Knowledge of soil zoology is more
nearly based upon studies of undisturbed systems.
In the past decade several developments have crnverged to promote
au increased interest in soil zoology of agronomic systems. One develop-
ment is the utilization of an ecosystem viewpoint, empnaslzing holistic
approaches (Harper, 1974). A major catalyst has been the use of nutrient
cycling as an integrating paradigm for evaluating whole ecosystems per-
formance and response to disturbance (Borniann and Likens, 1967). The
interactions of major ecosystems processes (primary production, consump-
tion, decomposLion and abiotic processes) have been evaluated using
nutrient flows, in a variety of natural or managed ecosystems, as evi-
dent by several papers at this symposium. Another development has been
the increasing adaption of minimum tillage or no-tillage agronomic prac-
tices (Perelra, 1975). Whatever their other benefits, reduced tillage
practices result in richer soil biota, Including invertebrates (Edwards
and Lofty, 1973; House, 1979). Increased awareness of the inportance
of niycorrhlzal associations for some crop systems has suggested that
tillage practices might be modified. Increasing costs of energy for cul-
tivation and chemical amendment, aid awareness of the need to reduce
sediment and chemical pollution of waterways, are additional considera-
tions leading to reduced cultivation practices. In any event, reducing
tillage allows soil biological components and processes to operate in a
manner similarly to those in undisturbed ecosystems.
In this paper we give an overview of a research project which is
attempting to integrate the approaches of agrcnorqy and ecosystem ecology.
We are attempting t.o apply methodologies and approches of ecosystem study,
in particelar nutrient cycling, as a means of evaluating performance of
agronomic systems. Specifically, we are comparing structure, function
and nutrient dynamics in a set of no-tillage and conventional plots.
280
-------
— — — —— — .
No-tillage or minimum tiliage farming excludes or reduces
plowing and smoothing the soil priot’ to planting (Phillips and Young,
1973). Seeds are planted in the residue from the previous crop. The
only disturbance to the soil is the narrow cut for the seed currow.
Special planti’ig equipment is used for this operation. Conventional
tillage usually entails six or more trips across the field (plowing,
disking, planting, cultivating at least once, herbiciding anu harv t-
ing). No—tillage requires only one trip ea’h for planting, herbicidiv’g
and harvesting, and thus is eiergetically more efficient than conven-
tional tillage. Important benefits from no-tillage practices are
conservatl ., 1 i of soil and water resources. Also, as described above,
perturbation of soil structure is suI stantially decreased. However,
there are some disadvantages to no-tillage: Weed problems can be
severe, although companion planting can reduce weed growth (Phillips
and Young, 1973). Some studies (Musick and Petty, 194) have shown
increased insect problems in no-tillage. Still, no-tillage farming
is increasingly popular.
The research project described here is currently in its second
year of development, ano is tne joint effort of several ecologists at
the Ur.iverslty of Georgia. Results given here are fragmentary and pre-
liminary, but representative. Data are presented on plant growth, de-
composition, soil niicroarthropods and nutrient leaching. Other infor-
mation on canopy consumers, soil, fertility, microbial processes, soil
mlcroarthropods and chemical transformations is not yet ready for re-
portir . .
The foundation for our experimental approach is the general
hypothesis that no-tillage practice leads to nutrient and energy con-
servation. Biotic and abiotic components of soil, left undistu’bed,
are organized into a well-defined structure, with the result that
nutrient cycling reduces loss of nutrients from the system. This para-
digm is supported by watershed studies (Bormann et al. 1974; Waide and
Swank, 1976) s ..wing that in forested areas (hi jhly structured systems)
Internal cycling greatly exceeds throughput. Plowing once or twice
ycarly is a major perturbation which destroys the soil system’s struc-
ture and function, ana recycling of nutrients becomes minimal. Conven-
tionally tilled farm land is in essence kept in a very early succession-
al or imature state by man-induced subsidies. No-tillage farming allows
soil structure to develop. Biotic components remc.in relatively undis-
turbed and therefore the no-tillage system should have more of its
recycling processes intact.
EXPERIMENTAL DESIGN AND METHODS
Horseshoe Bend is a 40—acre tract of land located in Clarke
County, Georgia. The area is an alluvial flood plain adjacent to the
Oconee River (Barrett, 1968). The crop system we are using consists of
eight ¼ acre plots, bordered on two sides by an old-field. As of flay,
1978, the area which is now the crop system was in old-field vegetatiot.,
not having been cultivated for 12 years. In May, the area was cleared
of vegetation to ground level. Eight experimental plots, randomly
-------
selected, received either conventional plowing or no-ti 1 lage treatment.
Following staiidard fertilizer applications, atrazine was used as a .re-
emergence herbicide. Grain sorghum was planted using a no-till planter.
In the fall of 1978. both till and no-till plots were planted in winter
rye which was conseque itly mowea and chopped in the spring of 1979.
Sorghum was again planted. Through_ t, we have used standard cultural
recommendations for sorghum in the Georgia piedmont.
Both above and belcw ground sorghum biomass was sampled at two
week intervals using three 1-rn 2 quadrats randomly located in each of
the eight plots. Plant material was oven-dried to constant weight for
biomass determination, ground, and subsampled for nutrient measure, ents
utilizing a plesma emission spectrograph. Grain production was evalua-
ted from similar 1-.m 2 collections made at the time of harvest.
Litterbag techniques were used to measure rates of decomposition
(Crossley and Hoglund, 1972; Edwards and Heath, 1963). Litterbags con-
taining weighed crop residue were randomly distributed ever the soil
surface of each treatment soon a ter planting. Five bags per plot were
randomly collected at approximately two week intervals. The residue
was oven-dried to constant weight in order to calculate loss of materi-
al, grc’ind and retained for n itrient analysis.
Soil microarthropods were sampled by extracting them from soil
cores (5 cm ala, by 5 cm deep) on a modified Tuligren apparatus (Mer-
chant and Crossley, 1970). Teii random cores were taken from each
plot at two week intervals. The soil mnicroarthropods were also sampled
prior to plowing and planting. Gross counts by major taxonomic groups
made on these samples are flaw ava 4 lable, arid more detailed analysis of
the faunal structure is continuing.
Because the experimental area is flat with minimal or no sur-
face run-off, the major loss of nutrients is through the downward
movement of ground water. Porous cup Tysimeters (Soil Moisture Corp.)
were used to measure the concentration of nutrients (f4H4, N03, P K,
Na) at a depth of 50 cm. Ths measurement is considered to represent
loss concentration, since the area of nutrient uptake by sorghum is
generally above 50 cm. The lysirneters were sampled approximately every
two weeks. The ground water was analyzed for ammonia and nitrate nitro-
gen t ing colorinetric techniques. Cation and phosphorus determinations
are teing made with a plasma emission spectrophotometer.
RESULTS AND DISCUSSION
The results of these studies obtained so far confirm the
advantages of no-till practices over conventional tillage. Only
results from the s”-mer of 1978 are available, ard these results
cover but a few of the process—level measurements.
Primary production in no-till and conventionally tillage plots,
as revealed from harvests of sorghum, produced nearly identical plant
blornasses by the end of the growing season. Figure 1 shows that sorghum
282
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FIGURE 1. Above-ground biomass of grain sorghum in conventionally—
tilled (CT) and no-tillage (NT) experimental plots, Horseshoe Bend
Experimental Area, Athens, Georgia. 1978.
T, ,‘
.0’ NT
I00
iO
S
1%) in
in
4
0
S
U
0
S.
U
-a
I-
z
ug)
9°
— —
‘ \
%
\
‘
S
4— —
——S
3•J if) .
JULY
at F, ——
,w al__ I
CT
FIGURE 2. Retention of dry weight by litter confined in small-mesh
bags placed in conventionally-tilled (CT) and no-tillage (NT)
experimental plots, Sunmier, 1978.
0
/
/
1
/
0
/
I
1
JU E JULY AUGUST SEPTEMBER
-------
growth in no—till plots initially lagged behind growth in cultivated
plots. Leaf formation and heading time also lagged behina in the no-
till plots. A significant factor may have been the slower root devel-
opment in no—till plots, which itself may heve been influenced by an
early-season drought. As Figure 1 shows, at the end of summer sorg-
hum biomasses were similar in conventional and no-tillage systems.
Biomass of weeds was higher in the no-till plots in the first weeks
samples, but thereafter weed blomasses were similar for the two treat-
ments.
Weight loss by plant residue, as measured by litterbag techni-
ques, is illustrated in Figure 2. In each treatment weight loss was
slow, but increased abruptly in late sunmer. Litter confln d in bags
in the no—till plots lost weight more rapidly than that in the con-
ventional tillage treatment; but final percenta9es of litter remain-
ing were similar (Figure 2). The pattern of weight loss and decompo-
sition of surface litter during the winter season may be of greater
significance than results for the summer growing season. Total decom-
position might be expected to proceed more rapidly under cultivation,
since surface litter becomes incorporated into the mineral soil.
However, the ameliorating effects of surface litter on abiotic micro-
climatic factors in no—till systems may negat9 this Influence of cul-
tivation, at least in some years.
Populations of soil microarthropods in conventional, no-till
and old—field plots showed an initial decline followed by an increase
later In the summer (Figure 3). Very low values obtained for micro-
arthropod populations in cultivated plots during June or July (about
1000 per in’), but these nurrbers increased dramatically following July
rains (Figure 3). A complete analysis of soil nhicroarthropod respon-
ses to tillage practices in these plots has been developed (Weems, in
preparation) ar.d will be presented elsewhere. Similarly, pitfall
trapping has been used to compare populations of sur’ ace—dweliing mac-
roarthropods in these tillage comparisons (Blun’berg, 1980).
While we are attempting to develop input-output budgets for
several major nutrients, we are placing particular emphasis on nitro-
gen fluxes and transformations. Reid et al. (1969) suggested that
nitrogen regimes are principally functions of immobilization and re—
mineralization rates, processes largely mediated by microbial activi-
ties. While large gaseous fluxes of nitrogen occur in soil systems,
leaching losses may be appreciable as well, particularly in the humid
southeastern United States (Nelson and Uhiand, 1955). Figure 4 shows
nitrate nitrogen concentrations in lysimeter collections at 50 cm
depth in conventional and no—till plots. During the last half of the
summer, nitrate concentrations in groundwater were significantly higher
in the conventionally tilled plots. These data suggest that no—tillage
practices retard nitrate loss via leaching. Further evaluation must
be based on gaseous transformations as well as leaching losses.
Figures 1 - 4 are illustrative of the types of research data
being collected In this field experiment. We emphasize the phenomena
-------
FIGURE 3. Total microarthropods in top 5 cm of conventionally-til1ed
(CT), no-tillage (NT) and old—field (OF) soils, Horseshoe Bend
Experimental Area, Sumer, 1978.
25
ow
I ’
I’
I
I
I
2
I
15
U.
(I .
2
2
U
I-
2
w
U
2
0
U
5
, CT
0
1
\
0
C NT
JULY S.’ TEMCER JULY AUC’JST SEPTEMBER
FIGURE 4. Nitrate-nitrogen concentrations in groundw .ter collections
from porous cup lyslmeters at depths of 50 cm in soils of conventional-
ly-tilled (CT) and no-tillage (NT) plots, Suniner, 1978.
•1
NT
OF.
CT
I
I
I
I
1
0
,
I • _•
MAY
-------
pertaining to the soil constitute the major differences between
the experimental systems. A generalized overview ccnslders nutrient
inputs and outputs in ccntrast with internal nutrient dynamics in
these systems. The principal nutrient input for both sy&tems is the
fertilizer subsidy. Harvest of crops is a major nutrient output,
but so are leachng and (for nitrogen) gaseous losses. ihe regula-
tion of the latter nutrient export is a function of the soil system
and is mediated by soil biological communities. It appears from
our results to date, that the more intact soiis of no-tillage agro—
nomic systems should prove to be more conservative of nutrients.
AC KNOWLEDGEMENTS
We are reporting the team efforts of a nunber of scientists,
students and others interested in the changing face of American
agriculture. We gratefully acknowledge the contributions of all of
them, especially Drs. Eugene P. Odum and Robert L. Todd. Institute
of Ecology, University of Georgia. We are especially grateful to
Dr. A. Kumura, M . Greg Hoyt, Ms. Anne Kirther, Ms. Georgianna May,
and Mr. Danforth Weems, for the use of their previously unpublished
data. Support for this research was provided by the Department of
Entomology a’id the Institute of Ecology, University of Georgia.
Research on populations and activities of soil arthropods was sup-
ported by a contract (DE-A509-76Ev00641.) between the Department of
Energy and the University of Georgia (D. A. Crossley, Jr.).
LITERATURE CITED
Allison, F. E. 1973. Soi1 organic matter and its role in crop
production. Elsevier, New York. 637 p.
Barrett, G. W. 1969. The effects of an acute insecticide stress
on a semi-enclosed grassland ecosystems. Ecology 49: 1019-
1035.
Blumberg, A. V. 1980. Comparison of soil surface arthropod popu-
lations in conventional tillage, no-tillage and old-field
systems. MS Thesis, University of GeorgIa. 96 p.
Bormann, F. H. and G. E. Likens. i967. Nutrient cycling. Science
155: 424-429.
Bormann, F. H., G. E. Likens, 1. 6. Siccama, R. S. Pierce and
J. S. Eaton. 1974. The export of nutrients and recovery
of stable conditions follcwing deforestation at Hubbard
Brook. Ecol. Monogr. 44: 255-277.
Brady, N. C. 1974. The nat ire and properties of soil. (8th ed.,.
MacMillam, New York. 639 p.
Crossley, D. A., Jr. and M. P. Floglund. 1962. A litterbag method
for the study of microarthropods inhabitating leaf litter.
286
-------
Ecology 43: 571-573.
Edwards, C. A. and J. W. Heath. 1962. The role of animals in
the breakdown of leaf mate ials. p. 76-84 in Drift,
J. Van der and J. Doeksen eds.), Soil Organisms. North
Holland, Amstrrdam. 453 .
Edwards, C. A. and J. R. Lofty. 1969. Agricultural practice and
soil microarthropods. in Sheals, J. G. (ed.), The Soil
Ecosystem. p. 237-247. The Systematics Association,
London.
Ethards, C. A. and J. R. Lofty. 1973. The influence of culciva-
tion on soil animal populations. p. 399-407, in Vaneck, J.
(ed.), Progress In Soil Zoology. Proc. 5th mt. Coil. Soil
Zool. The Hague: W. Junk and Prague: Acddemia.
Harper, J. L. 1974. Agricultural ecosystems. Agro—ecosystems.
1:1-6.
House, G. J. 1979. Carabid beetle abundance diversity and
seesonality in conventional and conservation tillage
cropping systems. MS Thesis, Univ. Georgia. 59 p.
Merchant, V. A. and D. A. Crossley, Jr. 1970. An inexpensive,
high efficiency Tuligren extractor for soil microarthropods.
Jour. Georgia Ent. Soc. 5:83-87.
Musick, C. J. and B. G. Petty. 1974. Iiisect control in conserva-
tion tillage systems. In Convservatimlillage, A Handbook
for Farmers. Soil Conserv. Soc. America. 52 p.
Nelson, L. B. and R. E. Uhiand. 1955. Factors that Influence loss
of fall-applied fertilizer and their probable importance in
different sections of the United States. Proc. Soil Soc.
Amer. 19: 492—496.
Pereira, H. C. 1975. Agricultural science and the traditions of
tillagi. Outlook on Agric. 8:211-212.
Phillips, S. H. and H. M. Young, Jr. 1973. No—tillage farming.
Reiman Assoc., Milwaukee. 224 p.
Refi, A. S., G. R. Webster and H. R. Krouse. 1969. Nitrogen
movement and transformations in soil. Plant Soil 31: 224-237.
t4ajde, J. B. and W. 1. 5,: ik. 1976. Nutrier 4 cycling and the
stability of ecosystems: implications for forest management
in the southeastern U. S. p. 404-424 in America’s
Renewable Resource Potential for 1975: The Turning Point.
Nat. Cony. Amer. Soc. For. Proc. 1975.
287
-------
QUESTIONS and COMMENTS
F. GOULD : Did you monitor weeds?
B.a STINNEI : Yes, we did. Biomass of weeds was
higher in no-till plots in the first samples we took. By the
end of the aunmter, the weed bion ass in conventional tillage
was just as high as in no-tillage.
E. WALDORF : Was insecticide applied in your conven-
tional tillage? If not, how does this compare with agricul-
tural practice?
B.R. STINNER : No, we didn’t apply ax y insecticide.
This woul not be unusual for grain sorghum in our area.
C.A. EDWARDS : We have also found fewer attacks by
atemborers in no—till systems -
The slow initial growth you reported was a normal
response. We have always found slower initial root growth
under no-till but later in the season root growth catches
up and overtakes that in ploughed soil.
I am not so sure about the nutrient situation.
In England we often have to add extra nitrogen to no-till
crops and less of other nutrients.
288
-------
E’FECT OF MEADOW MANAGEMENT ON SOIL PREDATORS
A. Kajak
Poli k Academy of &ICnCC
Poland
The thesis of this ontributiou is that meadow mnY ge —
ment is usually followed by a decrease, in the aburn nce of
invertebrates, predators being most heavily reduced as compa-
red with other trophic groups. This refers both to the pre-
dators occurring aboveground and to the predators inhabiting
soil and. soil surface.
In unuttlized ecosystems, or in those extensively
utilized, the abund Y1ce of invertebrate R1’ (m ls is closely
correlated with available food supply. There is a relation-.
ship between the amount of organic matter dying over the
year and the biomasa of saprophb.ges [ fig. 1J. There is also
a relationship between the biomaas of saprophages and the
biomass of predators j ig. J. The regression describing
this relationship has been calculated from data on 12 eco-
systems ajak, 1977). There is also a relationship between
the rate of dead matter input and. the predator biomass in
an ecosystem, although the bio’ ee of predators in a given
area is extremely sin U / o - 4 f, as compared with the
amount of dead. organic natter. Neverthele ss, the abu1 Rance
of predators depends on the amount of this matter. Both the
average bio1n 8 of predators an the average biomass of
aaprophages are a function of dead. matter input.
A regression of the average Rnnnal invertebrate
biomass on the nnnal input of dead plRnt material was
calculated. The functions were verified by the 1yais
of varIance on the basis of P statistics. The value
of F obtained from the empirical data is higher then the
theoretical P at the level 0.01 for all the functions
[ fig. I and. 23.
In intensively utilized ecosystems these relation-.
ships are disturbed. The number of predators is extremely
small in relation to food supply in such ecosystems.
When axia].yaing this problem, such factors as “ bers,
biomass, ant lobomotory activity of predators were conside-
red. Author s own observations were used anil the literature
data.
I am going to start with a vex actual problem
analysed by a. group of research workers of the Institute
of Ecology, Po1ei ti, for some years, namely with the problem
of the effect of mineral fertilizers on a meadow ecosystem.
The meadow was fertilized only with main macro—
elei euta — NPK, at a rate of 680 kg • ha • As a result,
289
-------
‘4,
/
a
10 1000
Litt.r input (g drywt m- 2 yr- 1 )
Fig.1. Rilationship bitweon litter input and saprephag.
(..A )or predator (s. fl biomass.
100 10000
biomau (mg dry wt . -2
b•tween saprophag. and predator
•,
,..
‘ 100000,
IT
• I.
/
.1
.
S..
1000
0
E
o
.0
I-
0
a
0
a:
S
.
S
10
S
S
Sapropitag.
Fi g.Z. R•Lat ion ship
blomass.
290
-------
the soil was acidified. [ PH KCI 5—5.6 in the ci ,ntrol
plots, while 4.5-4.8 in the fertilized. plotsJ. There were
some losses in the exchangeable Ca and Mg and d.ecceaae in
sorption capacity in the soil (Czerwiñski an Praoz 1978].
At the same time some changes occurred in the liv. ug part
of the ecosystem. The yield increased, plant species and.
their chemical coraposition being changed. This was followed
by an increase in the number of pbytophagous insects living
on green plant parts. The biomass of soil fauna decreased
for all the trop aic levels. The biomasA of predators,
however, dropped most, by more than 6(Y in the third year
of fertilizer application, while the biomass of saprophages
and phytophages dropped by about 2C . Tbus the proportion
of predators decreased in relation to the total biomass
of invertebrates. tab. 1J.
Tab. I
Effect of fertilizing on soil meso — and. macrofauna
Trophic
groups
Mean biomass . d.wt. • m —
-
Control plots
Fertilized plots
reo.a ors
Herbivores
Sapropi ages
Total
Predators/Total
in%
O. 7
2.05
26.85
29.47
2.00
O.’19
1.11 .9
23.09
211.77
1.00
after Andr e3ewska, 1976, Ma]o.alec, 1976; Nowak 1976;
Olechowioz 1976; Pçtal, 1976; Wasile’wske, 1976;
Zyroxnbka—&ldzka, 1976, Kajak 1977.
However the total number of predators was not affected,
only the proportion of small size an m ls increased in
the carnivore level. ab. aJ.
The number of such small arthropods as Stepbylin.tdae
increased, while the number of larger predators such as
Carabidac and Chilopoda decreased.. At the same time, the
average body weight of an individual increased in the
group of predators of small size, aM - d.ropped. in the
group of large ones. (Tab. 3).
In the community of spiders, which are anim la of
intermediate size as compared with the groups earlier
discu ssed., p0 significant changes in the density were
observed cab. 23, only the proportion of particular
species was changed. In the fertilized plots the heaviest
species declined, [ Tarantula pulverulenta /Cl/, T pcho _ sg
n%rioqj Q Koch, Pardosa pa].uatria /L/J, while an increase
in number was observed in the species of small body size,
! gona jj& Bi., ç ipalpi& /Wid../, Centomerita
bicoloF7Bl.J (Tab. J.
291
-------
Tab. 2
Effect of fertilizixl€ on density and bioniasa of p ’edatory arthropods
-
Siall ani a1s
Numbero find’ai 2
Control plot 1 Fertilized plots
—--
a gdwta 2
Control plots Fertilized plots
Stapbylinidae in.
Etap1qli idae
larvae
1973
1974
1973
1974
110.5
69.7
96.0
54.2
142.2
84.6
139.4
58.1
26.5
20.1
8.3
3.2
4ô.3
39.9
14.4
6.8
N
Large a ” ls
-
—
Araneae
Obilopoda
Carabidae iii.
-
1973
1974
1973
1974
1973
1974
-
37.?
35.4
61.3
86.5
3.01
5.46
--—
73.7
28.8
10.3
68.8
1.71
5.58
—
106.7
34.0
25.1
179.2
53.3
88.5
71.5
19.7
4.3
79.5
22.9
134
Total
1973
1974
309.4
251.3
367.3
247.9
220.0
325.0
161.4
159.3
-------
Tab. 3
ilean individue] wei ht
! e thod
1973 soil
1974 cores
1973 1 i soil cores
1973 0,97 quadrz te
1974 0,79 r!cthod
197k 13,!! soil cores
1975 2L1.,2 pitfall traps
— - - - -
ni owt
SrnalJenirne1s Ye
Staphylinidae im.
Carabidae 1arv e
0,24
-‘ r%V1
‘J
0,37
0,10
Large animals
.Areneae
Carabidee
2,85
2,00
17,7
35,1
-------
C2 ic. :
fecL ji o
I —u
— .- ‘— . - —
- - -.-
- .
i.cl
I ‘ri
It,
I r a
I0
I ,Q
ho
I ‘ r i
‘ C l ]
I (0
f4 )
IF I
IC )
gH
N
C- W I . •bf,I 1
S W%..LJ’..• ,•,
‘brc’ . uJ t’ c r’ ; •.
—.- i. t- —“ ,
:OC tt
Cc:’ .ro:.urU,z
_.ri ;o:c: •_‘itCif: - ,
? •‘.ci’c - :-q .J: .
I . ...J
I ,— i.
I ‘‘ .- ‘ •
., I I,
I i— t —

I ‘ I ‘I I
I ;
- -
I,
I , —
-------
The species of intermediate size were subject to smallest
changes aob natha degeer Sund/.
There—fore, in treated plots two processes occur at
the same time - changes in the body size an si in numbers.
[ Tab. 2, Tab. 33. In the group of large an inals there was
a decrease in the average body weight and in numbers, while
in the group of small predators an Q pposite situation was
observed. Mean density of predators is similar in treated
and untreated areas. nab. 2].
A decrease in the body size implies that ai i inals with
a higher metabolic rate generally also with a shorter life
cycle became more tinportent. As a result, the biomass turno-
ver increased .. Also the diet of predators must be shifted
towards smaller prey. The decrease in the proportion of
predators as such is one of the mechanisms of speeding
up the rite of matter cycling akubc7vk, Kajak 1997);
a decrease in the size of Lndividuals must have similar
consequences.
An accelerated. matter cyclii g can compensate for
losses in the mitrients leached from the ecosystem because
of increasing acidification, or removed from the ecosystem
with increasing yield and. not restored beca ase only a
limited number of nutrients is supplied with fertilizers.
A similar tendency bo a ti1 ini-nishing of the body size of
a imels, as observed in ferti].ized meadows is also
characteristic of crop fi Lds, as compared with natural
and. se i — natural ecosystems.
The changes in the biomass and. species composition
of predators in. the fertilized plots were associated with
a decrease ifl their mobility. Less &i imals were caught by
pitfall traps. As far as the number of predators did. not
drop we can a,ssume that the difference in the number of
individuals trapped is a result of decreased locomotory
activity of arth.ropods. cab. 2 and. 5).
Tab. 5
Effect of fertilizing on locomotory activity
of predatory arthropods.
Eumber of md per trap. 211th — 1 1
Control plots
Fertilized, plots
— Araneae
Poxmicidae
Carabidae
11.77 ± 0.40
1.19 2 0.111.
0,81 0.07
5.16 2 0.18
1.20 ± 0.11
0.35 ± 0.06
after Ka ak, 1977
295
-------
Similar methods as applied in the analysis of the
effect of mineral fertilizing were used to ex uine the
effect of organic fertilizers in the form of sheep m vnIre
on an ecosystem. This treatment was followed ‘by a oompl te
chRnge in the vegetation oo nposition and by a raise in
yield, as it is the case when mineral fertilizers are
ap lted. The basic difference is that the input of orgax.io
fertilizers was followed by an increase in the biomass of
soil fauna, including pbytophages and saprophagos. The
biomaaa of predators, instead, dropped, though not so
marked13r as after the application of mineral fertilizers
/Yy about 20%] / ab. 67. Tho proportion of predators to
the total biomass of soil fauna decreased cona 4erab]. y,
as it was one...fifth of that in unfertilized plots.
The size of iirn 1 did not diminish , however.
The ‘ 1yaia of the effect of grazing on predators
will be based on data frc.m American prairies. These were
long—term studies, tbu it is possible to follow longi teria
effects of enclosing large areas to exclude them front
grazing. My ecosystem components were analysed there,
from which only soil fauna dill be discussed hero.
Andrews et al. [ 1974.3 estimated energy flow through short
grass prairie ecosystem in the Colorado state. There was
compared, among others, respiratory energy loss of three
consumer levels in heavily gra ed (1 ateer/4 .8 ha for
180 day9 and ungrazed areas.
Gr tzing was o lowod by a decrease in the energy used
for respiration by £nvertebrate -‘als. And again predators
were more afZected than other trophic groups • The energy
flow through the trophic level of predators dropped almost
by half in the grazed prairie, while the amount of energy
used by pbytophages and sapro hages decreased by only
a little more than 20$ L ab. 7 47.
A similar concinsion can be drawn from the studies
conducted in prairies of different types /Lewis 1971J.
The average bioniass of predators in different prairies was
higher for ungrazed sites, although, for exeYnpl.,pbyto_
phages showed an opposite tendency (Tali.? B].
A negative effect of mowing on the m aber of preda-
tors is convincingly illustrated by Southwood and Ien
[ 19673. According to these authors, pbytop agoua species
tended to be more abundant in the out grass land while
both predatory a” ’ eaprophagous species are in the most
cases reduced in Immbers. They have also shown that
mowing is followed by a decrease in the proportion of
predatory species in groups of f ]- with large food
spectrum such as Acarixia, Coleoptera, and Heteroptera
LTab. 7.
296
-------
Tab. 6
iff eat
Of V’i11!iD. b ,
penning sheep on soil neso— a,ad inaorofa ’n .,
Trophia group
Mean biomasa / g d vt m 2 /
Control
tear after m puring
Predators
Berbivorea
Saprophagea
Total
Predatora/ Total
in%
0.15
0.28
4.50
4.93
3.0
0.12
0.92
20.60
21.64
0.6
- --
--
aZter Deio v, Laja -i r , £‘ç e L 1 •,’*, Wasi1ewá a 1974, Nowak
Tab. 7
Effect of grazing b cattle on aotivit and bionass
of belowgrouxad invertebrates.
Respiration koal • n’ 2 p.r 180 ds a
Jngrazed
Read].
grazed
rngrazed/ ReaVil
grazed
Herbivores
Saprophagea
Carnivores
22.8
16.2
3.9
17.4
12.5
2.1
1.31
1.30

S.L. yf’I
angrazed/ grazed
1970
1972
Herbivores
Carnivores
0.8
1.7
0 .3
1.9
— —
-
——
sr er j. ew,.a , Ba1)afl.tei.
Grassland Biome flata Bank 1972
eruer An ewa
S
297
-------
Tab. 8
Per cent of predators in total number of individuals
out meadow
uncut meadow
Acarina -
Coleoptera
lieteroptora
19.0 32.0
8.4 20.0
17.0 22.G
I
after Southiwood, iden 1967
Summing up, it may be concluded that meadow management
is usually followed by a decrease in the proportion of
predators in the ecosystem, and by a reduction in the biomass
of predators. Their bioinaas is reduced even in the case when the
treatments aDplied. cause an increase in plant bioinass and
in he oten ial food resources Ce.g. organic fertilizers).
The riim ’ ls nR1,ysed above are po].yphagous predators with a
relatively long life cycle. Stenophagous predators
ji.g. parasitesJ were not pnalysed here, it is even possible
that their activity can compensate to some extent for the
deficiency of po].yphagous predators. The data available
seem to indicate, however, that the reduction of predators
affects the functioning of one of the mecnanisms of number
‘egulation. Another important consequence is the accelera-
tion of decomposition rate as it seems that Boil predators
inhibit the rate of tnese processes jja jak and Jakubczyk
1976, 1977].
So far pest outbreaks in meadows have been rare as
compared with other ecosystems such as forests and crop
fields. It seem , however, that the intensification of
agricultural treaments enhnnoes pest outbreaks also in
meadows,
One of the characteristic features of grasslands
is the retention of organic matter in soil h unue decompo-
sition processes being generally less rapid thnn
production. As a result of the intensification of manage-
ment these processes seem to be shifted towards a higher
decomposition rate, this maki ig grasslands similar to
crop fields,
298
-------
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oloraentc of tha . )roc’uction in cever&i -2as1]ric euwiron—
— :-o1. )Ol. 23: 45 —4 1
L.owt’ 1 : •i. 1573 — ii ,rreo oa’ . ortiiizcitios on et 4 rtnori.u;
_ C o’ct r soil ; o; o un . coii.,onontz. — _ OL. cccl. $uU. 2:
1 5—2O7.
Olecaowicz n. 1973 — T. n effcct o .ii teru1 £ort-tJJt.in’c on
incect coz.nunitj of tue aerbauc ifl C ]dOWfl neocow — Pol.
ecci. Ztu1. 2: 129—136.
299
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P ta1 J. 197 /4. — .àna1ys .s of a sheep pasture ecosystem in
the Pienin mountains /the Carpathians/. XV. The effect of
pastu$e mana ement on ant population — Ekol. pol. 22: 679—
92.
Pc ta1 J. 1976 — The sffect of inera1 fertilizing on ant
populations in movm ueadows — Pol. ecol. Stud. 2: 209— 213.
Souihwood T.R.E., &tden von H.P. 1967 — A comporison of the
fauna of cut 8nd ur-cut grasslands — Z. angew. entomol. 60:
188—198.
Wasi1ews :a L. 1974 — Analysis of a sheep pasture ecosystem
in the Pieniny mountains fthe Cerpathians/. XIII. Quantita-
tive distribution, respiratory metabolism and some sugges-
tions on predation of nematodes — Ekol. p01. 22: 651—668.
Wasilewska Ii. 1976 — The role of nematode in the ecosystem
of a meadow in Warsaw environs — Pol. ecol. Stud. 2: 1 7—
156.
yroniska—Rudzica H. 1976 — Response ‘.f .Acarine—Oribatei 3n1
other r.iesofaune oi1 components on nii eral fcrti1izin -.
Pol. ecol. Stud, 2: 157—182.
QUESTIONS and COMMENTS
TADROS : What kind of traps were used in this in-
vestigation for determining soil fauna activity?
SZUJECKI I feel I am unable to answer questions
since it is not my work.
S.B. HILL : Did Dr. Kajak examine the influence of time
of application of the various management practices on soil
fauna. My experience is that timing is critical with respect
to both beneficial (intended) and harmful (unintended) effects.
A.J. SZUJECKI : I cannot answer for Dr. Kajak but you
are quite right; it is important.
3C0
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INFLUENCE OF AGRICULTURE ON THE OUTBREAK OF
WHITE GRUBS IN INDIA
C. K. Vecresh
Unn’ersily of Agricu DM701 5(,encr5
India
INTRODUCTION
Every fanner In India is aware of white grubs but seldom thinks
they would cause injury to his crops. The danger Is realized only when
the crops suddenly start wilting. Such plants are easy to pull up and
a white grub can often be scooped up from the soil under the plant. The
fanner then thinks that all white grubs are his enemies, although a small
percentage of this large group of scarabaeids are phytophagous and the
rest are either coprophagous dung feeders or litter inhabitants. Thus
the farmers are often hesitant to apply compost and farmyard manure in
which many white grubs live, because they think that the white grub prob-
lem In the cultivated field is Introduced with farmyard manures. Not
many realize that the white grubs develop Into the beetles that swarm In
dusk after the prenonsoon showers.
The white grub problem Is worl”-wide, mostly in lawns, turf and
grasslands, but in India extensive dair.age is caused to cultivated crops
in addition to lawns and turf. White grub damage to cultivated crops
reported from outside India Is mostly on sugarcane (Nungomery. 1948;
Mautia, 1935; Wolcott, 1935; Jepson, 1956). In India, no crop is free
from the ravages of white grubs, except under puddled conditions
(Veeresh, 1977).
The seriousness of the problem of white grubs to cultivated crops
was not realized until 1956, when a serious outbreak of white grub was
reported on sugarcane in Dalmianagar, Bihar (Anonymous, 1956) although
early records of white grub damage to crops In India were a’,ailable
(Sharp, 1903; Fletcher, 1919; Beeson, 1919; Anstead, 1919; Isac. 1919;
Stebblng, 1899). If the number of publications on white grubs in India
Is any indication to the magnitude of the problem now and before two
decades, certainly the problem has increased In the last two decades. Be-
fore 1960 there were On ’ twelve publications on this subject compared to
more than two hundred . .ences,avai1able now. Realizing the Importance
of white grups In I .”i ‘ ..,lculture, the Indian Council of Agricultural
Research constituted a cuninittee of experts in 1974 to covi Ider the prob-
lem and to suggest corrective measures (Anonymous, 1974). Large scale
campaigns against white grubs have been launched in the States of
Karnataka (Veeresh, 1974), Maharashtra (Raodeo et al., 1976) and Rajastan
(Yadava et al., 1978). The ICAR Scientific Panel of Entomology and Nmna-
tology has suggested an All Inlia Coordinated Research Project on white
grubs, io be taken up in the sixth five year plan.
301
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Perhaps for the first time a single pest has drawn the attention of
the whole country. So far there has been no single effective solu-
tion for the problem of white grubs in this country and every year
damage by the pest Increases. An attempt was made to assess the
factors responsIble for the sudden increase in the white grub inci-
dence. With the evidence available a change in agricultural practices
seems to have a major Influence favouring the outbreak of this other-
wise ubiquitous Insect, in the last two decades when the practices of
traditional agriculture gradually gave way to modernization.
METHODS
Data has been collected for over t%velve years on the incidence
of whlti grubs ..nder different agroclimatic conditions in India both
by personal visits and through coirvnunlcation. kesporise to a quarterly
white grub newsletter, Issued from the Department or Entomology,
University of Agricultural Sciences, Bangalore since 1974, provides
Informatlor. needed to a.;sess the causes for the outb,eak of white grubs
in this country. Observations were made on major species of white
grubs occurring In different agroclimatic condltic.ns, like coastal
belts, heavy ratr fall plantation districts of western ghats, peninsular
India, Northern plains and upper Simla Hills. And also the relation of
outbreaks to temperature, moisture, humidity, rainfall, soil types.
food preferences, natural enemies and cultivation practices were studied.
One species under each agroclimatic zone was selected for ob-
servation. They Include Leucopholls coneophora Bl. (coattal belt and
low lying areas of western ghat slopes), liolotrichia nilqlria Arrow
(heavy rainfall plantation districts of western gt ãts), Holotrichia
serrata F. (Deccan plateau), Holotrichi a consangulnea Bl. (Northern
plains) and Holotrichia sp. (upper Shill Hills). ‘Fill observations were
recorded under the fc.llowlng four categories:
1. ADULT: emergence, mating, food preference, fiiglt range,
and egg laying
2. LARVA: food habit, migration, effect of moisture
3. PUPA
4. NATURAL ENEMIES OF WHITE GRUBS
At a site selected atMahadeswarapura, Mandya District, about 130
kilometers from Bangalore, observations were made for the pest outbreak,
in relation to changed pattern ef agriculture in an area of over 200
hectares, where there was no incidence of the pest before lrrigatiLn
facilities were created after which the cropping p .ttern was changed.
302
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RESULTS
ADULT
Emergence
Leucopholls coneophora nerged only after the heavy rains for 3-4
weeks of monsoon in the laterite soils of western ghat slopes and
coastal region. Holotrichia nilglria nerged twice a year, although it
has an annual life cycle; the first was In April-May after the pre-
monsoonshowers and the second time was during post-monsoon period in
October-November when there was rain after several days of sunshine.
Holotrichia serrata emerged imnedlately after the premonsoon rains in
March-April Th South India and up to early July In Northern plains de-
pending on the occurrence of rain. H. consanguinea found emerging in
June—July, when the premonsoon rains occurred, as it confined to the
plains of Northern India. All the species emerged In dusk around 1930
hrs except L. coneophora which emerged an hour early in cloudy rainy
weather. Other species were not active during rainy windy days.
fiat I nq
Mating occurred above ground on host plants or on some trees In
all the species except L. coneophora w iich mated on the ground IniTledlately
after emergence and went back to the soil after some time. Other species
remained active on clear nights till dawn and fed on preferred hosts.
Food Preference
Adults of L. coneophora did not feed on any plant nor were they
found resting on lants. H. nilgirla did not show special preference to
any plant although was found resting on several plants. II. serrata and
H. consaniulnea have definite liking for neem ( Azadiracta 1nd1ca and
zizyphus ( Zizyphus jujuba L.) among nearly 30 host plants on which they
can feed.
Flight Range
L. oneophora did not move more than a meter from the place of
emergence. It walked faster than many other chafer beetles. H. nilgiria
was capable of flying long dstance and was attracted strongly to light.
H. serrata and H. consanguinea were also attracted to light, but they
are not capable offlylng long distance. Marked and released . serrata
beetles were recovered from light source at 660 m from the place f
emergence, whereas they did not go beyond 150 m to preferred host trees
in one night flight. More than 90% of the beetles were confined to
within 50 in radius, If the preferred hosts were available at the place
of emergence.
Egg Laying
All the species laid their eggs at a depth of five to eight cm
Irrespective of soil type and climatic conditions. Eggs were individually
laid In earthen cells. Normally eggs hatched in 10 to 18 days but eggs
may not hatch arid remain viable under dry conditions, up to a month in
the case of H. serrata , after which the eggs hatched In presence of
moisture. if there was moisture four days after laying, the eggs hatched
303
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in 10 to 12 da, but the young ones did not come out of the earthen cell
even up to 120 da until the surroundings got enough moisture, when the
larva continued to lead nomal life.
LARVA
Food Habits
The first stage larva of all the species fed on organic matter,
unless they encountered roots. Only from the second instar, the grubs
went In search of roots and their distribution confined to the root
zones. 1. coneophora were found mostly under coconut and arecanut
Araca catechu ) plantations as they needed a larger quantity of roots.
A t ugh they are polyphagous, they were seldom encountered in grass,
turf or under small plants, but had equal preference for tuber crops.
The grownup larva reached up to 10 cm In length. H. nilgiria could feed
on woody plant roots but were cornonly encountered under coffee plants.
H. serrata and H. consanguinea fed on a variety of plant roots except
under puddled conditions. More grubs of H. serrata were attracted to
onion, french bean and groundnut than sovjhum, inaile, guard and garlic.
Migration
There was no horizontal migration in the case of k. coneop hora and
H. nilgirla as they generally were found in dense roots and favorable
soil conditions. Holotrichia serrata was found to move a maximum of 6 m
under row crops anTiip to a meter In lawns from hatching to pupation.
In sandy loam soils the larvae moved a longer distance compared to red
soils and black soils with more percent of clay.
Vertical migration was m ximum in the case of L. coneophora and
H. nhlgirta In laterite soils. Although eggs were laTd at a depth of 5
to 8 cm the grubs were found to go up to 2 in before pupation, depending
on the level of moisture in laterite soils during stainer. The other 2
species pupated at depths varying from 20 cm in the Deccan Plateau in
the case of H. serrata to 1 m in H. consanguinea . Similarly, In upper
Simla Hills at altitude above 3000 m Holotrichia species went up to. 1 m
depth.
Effects of Moisture on Larva
Complete saturation of soil for more than 6 da was detrimental to
grubs of H. serrate . In laterite soils grubs were not affected by con-
tinuous rain for several days, as there was enough aeration. A con-
tinuous wet seasop for nearly 2 mo during the monsoon in west coast and
western ghats, did not affect the normal activity of L. coneophora and
H. nhlgirla . However H. serrata did not thrive well under this con-
dition but had more chances of overcoming prolcnged drought c3ndltion In
the plains. The young larvae of this species did not come out of the
earthen cell for up to 4 mo un er drought condition and revived activity
Ininediately when moisture was available. H. consanguinea , found In the
range of 20 to 40 cm under normal conditions, but went deeper in sandy
304 .
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loam soils up to 1 in depth during sumner as was found in Punjab.
Under Inundation resulting from continuous rain for a couple of days,
the larvae came to the surface of soil and exposed the abdomen,
dipping head and abdominal tip Into the soil until the water receded
when they went back to the soil.
PUPA
The pupal period of all the species of melolonthids listed have
ranged from 2 to 3 wk. Pupation generally started in December -January
In majority of the species but k. coneophora pupates In March-April and
early May. in this case the adult life Inside the soil was short com-
pared to Holotrichia spp. which spends Its life as an adult inside soil
in the puPil cell for up to 6 mo, in some cases.
The depth at which pupation occurred depended on the type of soil
and species Involved. L. coneo hora pupated at depth ranging from 1-2
m In laterite soil. H. nilgirla nupated at depths ranging from 30 to
100 an. H. consanqulnea usually pupated at depths around 30 cm but It
was not unusual to find pupae at depths up to 1 m In sandy—loam soils.
Natural Enemies
Ve?y few parasites and predators were recorded on either adults
or grubs. Toads ( Bufo melanostictus ) feeding on adults and crows
( Corvus splendehs ) on grubs were the main predators.
The Insect parasites include Tiphilds and Scolilds but at no time
were they found to be abundant enough to check the white grubs.
The fungal pathogens Netarrhlzium anlsopllae and Beauveria
brongnlartii were found attacking all the stages of the pest. M.
anlsopliae was mostly found In the coastal belt during the monsoon when
high humidity and high temperature prevailed. B. brongniartii was
found to attack all the stages of the Insect 1n ’lud1ng grub, pupa, and
adult in tne transitional belt of high rainfall and low rainfall area.
Up to 5% of the grubs were found to be infested with bacterial diseases
under all situations.
DISCUSSION
There are nearly 200 specIes of white grubs In the sub-families
Melolonth lnae, Rutelinae, Dynastinae and Cetonlnae of the family
Scarabaeldae which are economically Injurious to crops in India either
In their adult stage or in larval stage or both. The genus Holotrichia
( Lachnosterna ) alone has more than 120 species known to occur In India
(Frey, 1971), causing injury to plants mostly in their larval stage.
Not all known species have become pests although their feeding be—
hav 4 our is similar to that of the highly injurious species. The most
widely distributed and destructive species are j. serrata and j.
consanqulnea . Both these are quite similar In their biology and be-
305
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haviour. H. serrata is found throughout India whereas H. consangulnea
is restricted to the northern part of India. These two species have
assumed the status of national pests of crops In the last two decades
In Thdla. Some of the factors responsible for the outbreak of this
pest in relation to agriculture fs discussed here.
Up to 20 years ago, traditional agriculture closely followed
the monEcon pattern in this country. Adults of white grubs May-
beetles or June bugs) also became 3ctlve after the premonsoon rains.
The annual life cycle of :.he pest started with egg laying after the pre—
monsoon rains when preparatory cultivation also started. During tillage
operations like ploughing, harrowing and sowing, grubs were reduced to a
minimum due to predation by birds or injury. But with the shift In the
cultivation practices brought about by the introduction of high yield-
ing varieties of artificial irrigation In the early sixties, the avail-
ability of food changed for white grubs and the time of tillage.
White grubs are found In all situations where plant growth is
pc ssible except under puddled condition. There was a balance in nature
in their population level when they were subsisting in uncultivated area.
Wfr.hex x n of cultivated area, in the last 25 years, which has almost
doubled the cultivated land to 167 million hectares, most of their habi-
tat has been encroached upon. During the same period irrigation was
extended from 18% to 25% of cultivated land. Consequently, growing crops
do not depend on the monsoon and the sowing is done much earlier than the
onset of rains. The problem of white grub was more severe in areas where
there was a standing crop at the time of adult emergence. For example.
sugarcane is tradittonally planted during December—January. At the time
of egg laying in May—June the crop is half grown with no possibility of
dIsturbing the soil to expose the young ones for predation. Moreover,
the injury is noticed only after 2 to 3 mo when the grubs are fully
grown and conditions are favourable even for chemical control. Similar
situations are encountered in the case of other crops like maize,
sorghum, groundnut and vegetables (Veeresh, 1977) whIch are grown as
relay crops whenever artificial Irrigation Is available.
Report of severe outbreak of white grub (H. seratta)wasx ozted n
Mahadeswarapura, Mandya District, karnataka during 1974-76 iii an area of
200 hectares. The pest was not encountered in the magnitude before in
the living memory of the farmers of that area. Analysis of the situation
revealed that the area was mainly cultivated with the help of rains before
1970. In the early l970s, several Irrigation weVls were dug and growing
crops almost round the year was started. Sugarcane became the major crop
followed by sorghum and maize. The pest which was at low population
levels confined to low lying areas, suddenly found a new situation where
it could multiply and establish unharmed. In 2 to 3 yrs, it Increased
to a population level of 40 to 60 grubs per square meter. In the year
1976, a total of 1.4 millIon beetles were collected in this 200 hectare
area. This was one of the few instances ud1ed where shift in agriculture
was the cause for the pest outbreak.
There was no report of a y damage due to white grups from upper
Simla Hills of Himachal Pradesh at altitudes ranging 2500 to 3000 m prior
306
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to the Introduction of potatoes from the Central Potato Research In-
stitute, Simla which evolved varieties to grow at high altitudes.
The area under potato was extended to hitherto uncultivated areas.
White grubs which were lurking In small numbers suddenly found the
proper soil conditions with plenty of food during their larval period.
Now the cultivators have to be content with only 60 to 80% of good
tubers, the others scooped out by the grubs are either discarded or
sold at very low prices.
The widespread distribution ot white grubs is most man-made.
The studies on the behaviour and biology revealed that the adults
have a limited flight range; less than 660 m from the place of øner—
gence. The larval migration Is almost nil In many cases but then can
go up to a maximum distance of 6 ii depending on the types of crops or
types of soil. Although the adults of Holotrichia have some hosts on
which they feed by preference If available within a short distance
from their place of emergence, they d not go in search of hosts over
a very long distance. The widely distributed species H. serrata and
H. consangutnea are attracted to light at the time of emergence. Per-
haps Increased transport systems In the recent past might have helped
to some extent to carry the beetles at dusk from the place of their
emergence to wi1.,fe ted areas. It is convnon to see the incidence of
white grubs greater on road side fields and in farms with electric
lights.
Ircreased use of inputs like fertilizer and pesticides also has
helped to increase the Incidence of white grubs. According to Box
(1935) the white grubs disappeared as such after the giant toad ( Bufo
mar1n sj was introduced to Puerto Rico but reappeared after the de-
cline of toads due to a depleted food supply as a result of wide-
spread use of pesticides. Modern agr1 .ulture In India, too, depends
more on inputs like Irrigation, fertilizer and pesticides to grow high
yielding varieties. Their effect n the natural enemies of white grubs
is not yet known but the pest is on the Increase. This might be due to
depleted natural enemies. In recent years. white grtb In endemic areas
in I4aharashtra and Rajasthan have been covered with insecticide sprays
on host trees of adult beetles for the control of white grubs (Raodev
et al., 1976; Yadava et al., 1978). At several places, birds were
noticed dead after eating these beetles. In a survey made In Nandad
dIst’ict of Maharashtra to find out the causes o? severe outbreak of
white grub in that area, several farmers were complaining that they have
not been seeing the crows following their plough at the time of plough-
ing as they used to be some years back. No one was able to give the
reason for the same.
Some species are restricted to a particular region, as for ex-
ample; L. con phora and H. nflqirla are found in the heavy rainfall
track oT liTájiijreglon an i at hTgh altitudes, respectively. Both
thr1v well on laterite soils whereas H. serrata although present In
these regions has not oeen able to estiblish as a major pest as It
cannot manage to live In the lateritic soils.
307
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CONCLU IONS
From the results obtained during the course of thEse observa-
tions, It can be concluded that man—made situations have helped the
pest to multiply and spread despite weak innate ability to migrate
and disperse. Adult dispersal is mostly localized, unless it is
aided by external agencies. The larval migration is negligible ex-
cept where the roots are sparse; then they may move a few meters.
Both adults and larvae have few natural enemies. Heavy mortality
occurs only In situations where the Infested soil Is disturbed re-
peatedly and grubs are exposed to predators or Injured. Lands kept
under crops at the time of egg laying that provide roots with adequate
and continuous moisture with least distrubance of soil during larval
period will favour the buildup of the pest. Bringing uncultivated
area under crop, extending Irrigation to unirrigated areas, relay
cropping, and pesticides have contributed favourable conditions for
the pest outbreak.
ACKNOWLEDGMENTS
The author Is Indebted to the Indian Council of Agricultural
Research and the University of Agricultural Sciences, Bangalore for
the financial assistance to enable me to present this paper in the
Seventh Internatioral Colloquium on Soil Zoology.
LITERATURE CITED
Anonymous. 1956. IISR News letter 2:1—4.
Anonymous. 19,4. White grubs scientists nmiet. Pesticides VII !:
pp. 60.
Anstead. R.D. 1919. Insect pests of South India and their control.
Rept. Proc. Third Entomol. Ntg.,Pusa 1:329-330.
Beeson, C.P.C. 1941. The ecology and control of forest iflsects of
Indian and the neighbouring countries. Publ. Forest Res.
Dvn. Govt. of India. p. 358.
Box, R.E. 1953. The history and the changing states of some Neotro-
pical insect pests of sugarcane. Trans. mt. Cong. Entoinol,
9:254-259.
Fletcher, T.B. 1919. Annotated list of Indian crop pests. Rept.
Proc Third Eritomol. Mtg., Pusa. 167-168.
Frey, G. 1971. Keys to the Indian & Ceylonese species of the genus.
Holotrichia Hope (Coleoptera—Melolonthldae). Ent. Arb. Mus.
Frey 22:206—225.
308
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Isac P.V. 1919. Some recently noted South Indian Nelolcnthldae of
Economic importance. Rept. Proc. Third Entomol. Mtg., Pusa.
1028—29.
Jepson, W.F. 1956. The biology and control of the Sugarcane chafer
beetles in Tanganyka. Bull. Ent. Res. 47:377-397.
Mautla, L.A. 1935. The sujarcane white grub Lachnosterna ( Phytalus)
Smithi Arrow in Mauritlus. Pr c. V. Coii . mt. Soc. Sug. Cane
Tech., BrIsbane. 436-445.
Mungomury, R.W. 1948. The use of BHC in controlling white grubs in
Queensland. Proc. 15th Cong. Queensland Sugarcane Tech. pp.
35-42.
Raodeo, AeK., S.V. Deshpande. A.D. Putani and G.G. Bllapete. 1976.
A large scale campaign for the control of white grub. PANS
22:223-226.
Sharp, 0. 1903. Lamelllcorn Coleoptera from the Nilgirl Hills. Ann.
Nag. N. HIst. 11:15.
Stebbing, E.P. 1899. InJurious insects of Indian forests. Govern—
inent of India Press, Calcutta. p. 52.
Veeresh, G.K. 1974. War against white grubs. Curr. Res. 3:87-88.
Veeresh, GK. 1977. Studies on the Root-grubs In Karnataka. UAS
Monograph series No. 2. P. 87.
Wolcott, G.N. 1935. The white grub problen In puerto rico. Proc.
V. Cong. mt. Soc. Sug. Cane Tech. Brisbane. 445-456.
Yadava, C.P.S., R.C. Sexana, R.K, Mishra, N.N. Dadheech and P.S. Poonfa.
1978. Integrated control of white grubs. White gr . bs News-
letter. 2:23-26.
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THE INFLUENCE OF AGRICULTURAL LAND USE PRACTICES
ON THE POPULATION DENSITIES OF Allolobophora Ira pezoides and
Eisenja rosen (OLI OCHAETA) IN SOUTHERN AFRICA
A. J. Reinecke and F. A. Visser
Po?chefst room Unwirsslv
South A:r,ra
INTRODUCTION
As soon a soils are utilized for agricultural purposes
it is generally accepted by many soil biologists that a decrease
in the number of soil organisms as well as species diversity
will follc.w (Evans & Guild, 1948; Graff, 1953). According
to Ghilarov (1973) very few members of the soil community
can survive the destructior. of soil structure resulting from
cultivation. Earthworms are affected in various ways by
cultivating practices depending on the species and frequency
of cultivation (Edwards & Lofty, 1973). The latter authors
recorded increases in the numbers of certain species. They
presunied that a modest amount of cultivation provides better
soil conditions for earthworm burrowing. Allolobophora
calicinosa was favoured most in the long run by cultivation
practices. In later studies the same authors (Edwards & I fty .
1977) found that earthworm populations have been consistently
larger in uncultivated plots than in cultivated ones with
L. terrestris populations particularly favoured by lack of
cultivation. For this species, in particular, decreases of up
to 400% were recorded while cultivation decreased populations
of other species of earthworms much less.
The influence of chemical fertilizers on the soil fauna
has not yet been studied extensively since the woric of Duerell
(1959) and Slater (1954). Artemjeva & Gatilova (1973) com-
pleted a long term investigation in Russia and con-luded that
chemical fertilizers such as anunonium sulphate, superphosphate
and potassium chloride have a direct negative effect on the soil
microorganisms, depending on dose of application (and of
course, relative composition) — These authors are convinced that
the nature of the effect of a mineral fertilizer is also deter-
mined by the type of plant cover. Zajonc (1973) also concludes
that high doses ot ] .ovosice niter affects earthworm numbers
adversely.
310
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The present investigation was undertaken in irrigation
soil in South Africa as part of a wider survey to evaluate the
position of the endemic and introduced earthworms in agricul-
tural soil in the Mooi River irrigation area (Visser & Reinecke,
1977). The irrigation area houses various earthworm specie5
of which Allolobophora trapezoides has the highest population
density followed by Eisenia rosea with the widest distribution
in the area.. The purpose of this study was to demonstrate
the collective influence of some agricultural land—use prac-
tices on the earthworm fauna.
METHODS
Research was conducted on two adjacent sampling sites
(A and B) of SOm x lOOm in the Mooi Rivcr irrigation field
nee Potchefstroom (27°4’E and 26°47’S). Medicago sativa
(luzern) had been established three years previously. The
particular spot proved to have the highest population densities
for . tra ezoides and . rosea in the irrigation area (Visser
& Reinecke • 1977). The maximum crop yield for the field was
1,91 kg, m 2 in 1975. The two adjacent sampling sites were
carefully selected and analysed faunistically, physically
and chemically to ensure the closest posbible similarity.
Therznographs were erected on the sampling sites to measure
soil temperatures at a depth of 15 cm during the research
period. Rainfall was measured with a conventional funnel-
type rain gauge. Random soil samples were taken from both
sites for chemical analysis. Conductivity (Soujoucos-method)
and ph (KC1-inethod) were also determined. Physical descrip.
tions were obtained for soil samples from both sites. The
hydrometer method was used to analyse particle size before
classifying textural classes (Townsend, 1973). Complete pro-
file descriptions were provided by pedologists from the P.U.
for C.H.E. at Potchefstroom. Measurements of soil pF (Lavelle,
1971) for both sites were obtained With the aid of a membrane
press (plate extractor). Soil moisture content was determined
every second week with the aid of an Ultramat moisture meter
using soil samples taken at a depth of 15 cm..
To determine the number of samples to be taken from each
site, a preliminary survey was undertaken. Southwood’s (1966)
formula was employed to determine the number of samples re-
quired to calculate the mean density (at 95% confidence level)
311
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within 20% of the actual mean density. From this survey
five samples proved adequate. However, eight were taken from
each site over a period of 3.5 months from October 1974 to
December 1975 after a preliminary evaluation in September
1974. The samples were taken at random using tables for ran-
dom distribution. These eight soil samples of 25 cm 2 were
taken every second week from each of the sau pling sites.
This sample size proved practical (Zicsi, 1958; At lavinyte,
1964; Tsura, l9 75; Reinecke & Ljungstrom, 1969) and statis-
tically reliable.
Earthworms were extracted from the soil samples by hand-
sorting on a field table. Samples were taken to a depth of
40 cm and sometimes deeper, depending on soil moisture condi-
tions. The collected worms were kept alive on moist filter
paper. !siomass determinations were un eitaken on live worms
after no more castings were excreted. Satchell (1969), Madge
(1969), Block & Banage (1968) and Nordstrom & Rundgren (1972)
have shown that preserved specimens could lose as much as 25%
of their body mass.
Site B was disturbed physically as a result of cultivation
practices. Crop rotati ,n took place and a NPK—fertilizer was
applied. This happened in October 1974 and again in August
of the following year. Site A was left undisturbed through
the whole of the research period. The application of these
land—use practices to site B took place shortly after it be-
came cle’r that the two sites were, for all practical purposes,
qualitatively and quantitatively identical.
The results of the survey were subjected to a variance
analysis programme BMDP2V by die Computer Centre, P.U. for
C.H.E. using an IBM 370’125 computer.
The tolerance of A. trapezoides for the various components
of a NPK-fertilizer was investigated by subjecting batches of
mature worms to various concentrations of commercial potassium
chloride, superphosphate and urewn separately. The aim was to
gain a provisional insight into their susceptibility for the
various components in order to draw some conclusions on the
possible role of fertilizers as disturbing factor operating
in site B. Eight batches of 15 worms each were kept in glass
jars at concentrations of 200 ppm through to 40)0 ppm KC1 for
10 hrs in a controlled environment. Worms were thereafter washed
and placed on wet filter paper in petri dishes. They were
investigated for mortality after 24 hrs. The same procedure
312
-------
was repeated with ureum and superphosphate. Provi iona1
conclusions axe mentioned in the discussion of this paper.
n in depth blo—assay is presunt].y being undertaken by J.R.
Kriel and the senior author at this institute.
RESULTS
Comparison of Two Sampling Sites
Strictly identical soil profiles were obtained for both
sampling sites. The A horizon (ortic) (0—34 cm) had a sand
loam texture, apedal structure with high porosity. B2l was
neokutanic (35-66 cm), sand loam but structurally less devel-
oped. Earthworm burrows were predominantly in A 1 , somet lines
in B 21 and very rarely in B 2 . A complete analysis is given
by VLsser (1978). The physical properties of the soils from
the two sampling sites are compared in table I.
The chemical propertles of t) e soils from the two sam-
pling sites are compared directly before and after site B
was cultivated and a 2:3:4 fertilizer applied (5,3w; 8%P;
10, 7%K) at 200kg/ha (Figure 1). From the figure the similarity
in the chemical make—up for the more important ions before
cultivation can be clearly seen. After cultivation and
fertilizer application soils from site B differed prominently
in respect of K—coi:tent. Phosphorus almost doubled from 34
before to 70 p.p.m. after fertilizer application. The organic
matter content remained the same and no fine analysis of ni-
trogen content was undertaken.
A comparison of the moisture conditions prevailing in the
two sampling sites during the course of the investigation is
illustrated by Figure 2. From this figure it can be seen that
the available soil moisture conditions differed only slightly
between sites A and B. The pF values are also indicated.
Quantitative Changes in Sites A and B
From the start of the survey in September 1974 the earth-
worm fauna of the two sites were quantitatively fairly siini-
lar. This remained so until October 1974. Site B was first
cultivated the second week of October. The mechanical dis—
333
-------
1.ABLE I.
Comparison of the physical properties and soil moisture
of the soils of sampling sites A and B at various depths.
mean ± SE
% moist.at kPa
33 1000
Site
Depth
Conduc- pH %
&
Text
org.
(cm)
tivity
(p5)
Silt
Clay Sand Class
mat.
0-35
A
B
7,3 15 11 74 Sim 742
1500
35—65
082
7,2
15
14
71
Sim
7,01
6,6±1,3
65—90
7,1
14
20
66
Sim
6,62
90-110
7,0
15
18
67
Sim
4,10
0—35
7,2
16
8
76
Sim
6,37
35—65
0,79
71
17
11
72
SIm
7,21
7,2±0,2
65—90
6,9
1
19
68
Sim
5,43
90—110
7,0
18
15
67
Sim
3,21
5,6±1,4 4,4±1,3
5,6±1,5 4,7±0,6
-------
SITE A
Before After
200-
1K
100-
L JW
SITE B
Before After
205
4 ini
0
FIGURE 1. The concentration P arid K in the soils from sites
A and B before and after cultivation and fertilizer
application (2:3:4 at 200 kg/ha) had ta)cen plact in
site B. No significant change occurred in respect
of Ca, Mg and Na content during the period.
315
-------
SITE A
— — — — — — — — — — — — — — — — — — — — — — — — — — — — — — U
— — — — — — — — — — — — — — — — — — — — — — — — — — — — — — U
I — — — — S — — — — — — — — — — — — — — — — — — — — — — — I
SITE B

— — ,— — — — — — — — — — — — — — — — — — — — — — — — — — —
— — — — — — — — — — — — — — — — — — — — — — — — — — — — — a
I — _ — — — — — — — — — — — — — — — — — — — — — — — — — — — — a
OCT 74
FIGURE 2;
SAMPLING PERIOD
A graphic representation of the moisture conditi.oris
in sites A and B during the sampling period.
‘U
U,
2.5
3.0
4.2
I1
0.
5-
25
3.0
4.2
DEC 75
316
-------
turbance to a depth of. approximately 25 cm was accompaniea
by the application of a NP.Lc.—fertilizer (2:3:4) at 200 kg/ha.
soil analysis in the area undertaken afterwards by a local ferti-
lizer company lead them to recommend 1:4:0 combination at
200 kg/ha.
An immediate effect was observed, most probably caused by
the combined effects of mechanical and chemical disturbances
(including crop rotation). This was revealed by population
estimates for both species (Figure 3). There was a dramatic
decrease in the population density in site B. These popula-
tions only regained their original peaks in March and May with
a maximum peak of 182 worms/rn’ in May for both species. The
worms in the undisturbed site (A) reached a population density
exceeding 600 worms/rn 2 in mid-April. Both sites experienced
a drop in numbers in June and July. These, however, correlated
well with low rainfall data (Figure 3) and relatively low
moisture conditions which prevailed on both sites. The seine
quantitative overall difference is revealed by t ie bioinass
figures for both species in both sites (Figure 4). The fluc-
tuation patterns were basically similar for both sites.
Variance analysis (Visser, 1978), not represented here,
confirmed a highly significant difference (at the 1% level)
for the population densities of the earthworms in the two
sarpling sites. Comparison of the numbers of j veni1e worms
from the different sites were not very revealing and no major
differences in reproduction rates were detected. It was,
however, possible that the reproduction rate (as deducted from
cocoons production and the number of juveniles sampled) of A.
trapezoides was slowed down to a lesser extent in site B than
that of E. rosea . From this and the fact that A. trapezoides
was numerically affected to a lesser degree by the chemical
and physical disturbances of the hnbitat it is concluded that
this species seems to bc more tolerant of changes in the hab-
itat. This seemingly higher adaptability to disturbances may
also correlate with the ability of this larger of the two
species to migrate deeper down into the soil where it is less
adversely aff3cted by superficial changes in the upper soil
layers.
317
-------
SITE A
SITE B
FIGURE 3.
Graphic representations of the changes that occurred
in the population densities of Allolobophora trapezoides
and Eisenia rosea in sites A and B. Seasonal chan-
ges in rainfall, soil moisture content and tempera-
tures are also given. All measurements and samples
were taken at two—weekly intervals.
SAMPLING PERIOD
318
-------
FIGURE 4.
Histograms showing the seasonal changes in popu- .
lation density and biornass for . a ez ides and
E. rosea in sites A and B.
c l
E
V i
E
I-
0
V i
Vi
0
E
0
-o
Oct74
SAMPLING PERIOD
Dec 75
319
-------
DISCUSSION
The overall effect of the land-use practices on the
earthworm population densities of the two species for the
period under consideration, is clearly revealed by the present
investigation. Although this phenomenon is not new, it at
least nrovides a scientific basis as far as effects on these
earthworms are concerned.
Trials to assess the relative roles of crop rotation,
fertilizer application and cultivation separately are at
present under way. Indications are that KC1 fertilizer in
its commercial formulation only causes mortality in A. trape—
zoides at extremely high doses. These doses are much higher
than those measured in Site B of the present investigation.
It seems to be the same with superphosphate, thu application
of which is accompanied by a lowering of pH to levels beyond
the normal tolerance limits of the earthworms.
A possible synergestic effect could also operate between
the various fertilizer components when applieñ in coutbination.
This merits investigation as well as the invluer.ce of soil
type on possible toxological effects. Tong term trials can only
revc.al whether the possible negative influence of fertilizers
mentioned in the literature is of a short duration only.
The relative roles played by each component of the collec-
tive land—use practices can not be assessed from the present
field studies. However, destruction of soil structure as a
result of cultivation cannot be ignore’s as a major factor in
destroying earthworm populations. Minimal or zero cultivation
of agricultural land is being increasingly adopted as stand-
ard practice in many countries (Edwards & Lofty. 1977) with
exceptionally good results and without any noticeable negative
effects on the soil fauna. The physical soil environment and
the destruction of its structural make-up may still prove the
major contributing factor in eliminating or decreasing earth-
worm populations in agricultural soils.
In southern Africa endemic species are almost without
exception absent from agricultural fields while the “common
field worms” are either Ailolobophora trapezoides or Eisenia
rosea . but usually both. Laboratory trials and efforts to rear
endemic species are extremely sensitive to changes in the
320
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physical environment as well as various forms of physical
disturbances. It is common knowledge amongst farmers in
many parts of southezn Africa that endemic ear-thworins origi——
nally occurring in the soil, will disappear completely soon
after a new agricultural land is cultivated. Du Plessis
(197a) is convinced that the sensitivity of the endemic fauna
for habitat changes and the human land--use practices in South
Africa are leading to a destruction of natural populations.
This contention seems to support the idea of Ljurigstrom (1972)
that man is playing a major role in exterminating the endemic
earthworm fauna.
ACKJ’TOWLED( 4ENTS
The authors are indebted to the South African Department of
Agricultural Technical Services for financial assistance and
to prof. P.A.J. Ryke for his useful comments and the facilities
placed at our disposal.
LITERATURE CITED
Artemjeva. T.I. & F.G. Gatilov i. 1973. Soil microfauna
changes under the influence of various fertilizers.
Pages 463-468 jfl J. Vanek (ed). Progress in Soil
Zoology. Czechoslovak Acad. Science, Prague.
Atlavanyte. 0. 1964. Distribution of earthworms (Lumbricidae)
and larvae of insects in the a oded soil under cultivated
crops. Pedobiologia 4: 245—250.
Block, W. & W.B. Banage. 1968. Population density and bio-
mass of earthworms in some Uganda soils. Rev. Ecol.
Biol. Sol. 5,3:515—521.
Doerel. E.C. 1950. Was sagen die Regenwurmer zur Minerald—
ungung. Deutsche landw. Presse, 4,1.
Du Plessis, S.F. 1978. ‘n Ondersoek na die verspreiding en
taksonomie van die Microc]iaetinae (Oligochaeta) in Suid-
Afrika. Unpublished thesis. Potchefstroom University
for C.B.E.. South Africa.
321
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Edwards, C.A. & J.R. Lofty. 1973. The influence of culti-
on soil animal populations. Pages 399—407 in 1. Vanek
(ed). Progress in Soil Zoology. Czechoslovak Acad.
Science, Prague.
Edwards, C.A. & J.R. Lofty. 1977. The influerce of inverte-
brates on root crops grown wiUi minimal or zero culti-
vation. U. Lohm & T. Persson (eds). Soil organisms
as components of ecosystems. Proc. VI Internat. Soil
Zoology Colloquium. Ecol. Bull.:NFR25 Stc kholin.
Evans, A.C. & W.J. Mc.L. Guild. 1948. Studies on the rela-
tionships between earthworms and soil fertility. V.
Field populations. Ann. appi. Biol. 35,4:485—493.
Ghilarov, M.S. 1973. General trends of changes in soil
animal populations in arable land. Pages 31—39 in J.
Vanek (ed.) Progress in Soil. Zoology, Czeckoslovak Acad.
Science, Prague.
Graff, 0. 1953. Investigations in soil zoology with special
reference to the terricole Oligochaeta. Z. Pf 1. Ernahr.
Dung. 61,72—77.
Lavelle, P. 1971. Etude demographique et Dynamique des popu-
lations de Millsonia p na1a (Acanthodrilidae—oligochetes).
Unpublished thesis. Univ. Paris, France 88p.
Ljungstrom, P.-0. 1972. Introduced earthworms of South Africa.
On their taxonomy, distribution, history of introduction
and on the extermination endemic earthworms. Zool. lb.
Syst. 99:1—81.
Madge, D.S. 1969. Field & Laboratory studies on the activities
of two species of tropical earthworms. Pedobiologia
9:188—214.
Nordstrow, S. & S. Rundgren. 1972. Methods of sanpli q lum—
bricids. Oikos 23:344—352.
Reinecke, A.J. & P.O. Lungstrom. 1969. An ecological study
of earthworms from the banks of the Mooi River, Potchef—
stroom, South Africa. Pedobiologia 9:100—Ui.
Satchell, J.E. 1969. Methods of samoling earthworm populations.
Pedobiologia 9:20-25.
322
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Slat6r, C.S. 1954. Earth orrns in relation to agriculture.
U.S. Dept. of Agric. Res. Service Circular.
Southwood, T.R.E. 1966. c1ogical methods. Menthuen & Co.
London. 391p.
Tsura, S. 1975. Seasonal variations of nun ber and biomass of
earthworms in grassland. Pages 223-228 j J. Vanek (ed).
Progress in Sos). Zoology. Czechoslovak Academy of Science,
Prague.
Townsend W.N. 1973. An introduction to the scientific study
of the soil. Edward Arnold Ltd. London. 209p.
Vis’er, F.A. 1978. ‘n Bio—elcologiese ortdersoek na die terres—
triele Oligochaeta in die Mooirivierbesprc’Ciings-gebied.
Unpublished thesis. Potchefstroom University for C.H.E.,
South Africa.
Visser, F.A. & A.J. Reinecke. 1977. The earthworms of the
Mooi River irrigation area in Potchefetroom, South Africa
Oligochaeta: Lumbricidae, Acanthodrilidae, Microchaetidae
and Ocnerodrilidae) P. Cent. pir. Biol. exp. 9:95-108.Jaca.
Zajonc, I. 1973. Variations in meadow associations of earth-
worms caused by the influence of nitrogen fertilizer and
lizer and liquid-manure irrigation. Pages 497-503 j
3. Vanelc (ed). Progress in Soil Zoology. Czechoslovak
Academy of Science, Prague.
Zicsi, A. 1958. Freidlanduntersuchungen zur kenntnit der
Empfindlichkeit einiger Lumbricideri-Arten gegen Trocken-
pexioden, Acta.. Zool. Hung. 3:369—383.
QUESTIONS and COMMENTS
G. KLEE : Did you notice any bird predation of earthworms
of freshly plowed soil in your study plots?
INEcKE: Due to the depth of ploughing very few
earthworms were found on the surface directly after ploughing
and no bird predation w s noticed. If limited bird predaticn
did occur, the effect could hardly account for the drastic
changes in the population densities.
323
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.7.E. SATCHELL : Could the reduction in earthworm popula-
tions after cultivation have been caused by reduction of
their food supply?
.J. REINEC’KE: This could be a possibility although the
fairly homogenous distribution of organic material in this
soil and the earthworm’s ability to move about should rule
out lack of food as a direct cause. Structural changes in
the soil as a result of cultivation may however still retard
normal mobility and feeding.
. A • FAIZY $ I want to know your opinion regarding the following
statement “Nigh dressing c! N-fertilizers only will reduce the density
of soil fauna. However with a high dressing of a balanced NPIC-fertjljz3r,
the density of soil fauna might not be reduced.”
.L. REfliWK s The application of N-fertilizers are usually accomp n1 ad
r a decrease in pH which is harmful to earthworms. A high dressing of
balanced fertilizer will probably not reduce the fauna when the N-component
is relatively low. I do not know of any available data to support the
idea that the presence of (say) P and K would have a synergistic effect.
32
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THE INFLUENCE OF FARMYARD MANURE AND SLURRY ON
THE EARTHWORM POPULATION (LUMBRICIDAE) IN ARABLE
SOIL
Casper Andersen
Roytti Vthrinary tu,d Agricvltural Unw rsily
Den
ABSTRACT
Earthworms were i ampled spring and autumn in the years 1976 to
1978 by formalin extraction and handsorting. Farmyard manure and slur-
ry were given in the following quantities; 50 and 100 tons/ha each
year, 200 tons/ha each second year and 40C tons/ha each fourth year.
In this way both short term and long term effects were studied. Earth-
worms were identified, sorted into classes and measured as to biomass
(fixed material).
The two types of manures greatly influenced the frequencies of
individual species. Farmyard manure favours all species especially
AlZô obcphora ?.onga Ude, 1888, whereas by slurry treatment A. onga is
outnumbered by AlZol.obophora caUginoaa Sauign . 1826. The greatest
‘opulation densities are recorded by 100 tons/ha/year to 200 tons/ha
/second year, for both types of manures. Following application of 400
tons manure/ha a sharp decrease in population size is seen. Two years
after application of this amount of manure, the population seems to
have recovered. Population size, however, is influenced by climatic
conditions.
INTRO ICTION
Over the past years a great number of studies has been carried
Out Ofl the importance of earthworm3 in arable soil and the influence
on earthworms of mechanical treatment, straw incorporation, green ma-
nuring and animal manure, some of which are cited here: (Barley and
Jennings, 1958; Dunger, 1969; Edwards, 1975; Edwards sri Lofty, 1976;
Graff and Kuhn, 1977; Leger and Milette, 1977; Rogaar and Boswinkel,
1978; Schwerdtle, 1969; Sharpley and Seyers, 1977; Seyers, Sharpley
and Keeney, 1979; and Wilcke, 1962).
Studies on animal manure have mostly been concerned with the
traditional semisolid farmyard manure (FYM). However, with the intro-
duction of modern technology into husbandry it has become more conve—
iient to collect faeces and urine from the livestock in tanks, stored
a a liquid suspension — slurry, which is spread on the fields as a
manure or as simple waste. This practice may, however, result in the
spreading of pathogens, and slurry has also been shown to be toxic
to earthworms under certain conditions (Currey, 1976).
In the present study is reported on the influence of high dos-
ages of slurry and PIN on earthworms under field conditions. Thus in-
vestigations were carried out in the period 1976 to 1978 on Askov Re—
325
-------
search Station, SouthertL Jutland, Denmark, and were supported by the
Danish Research Council, S.JVF.
METHODS and MATCRIALS
The soil type ef the experimental fields of Askov Research
Station is a sandy loam with a weakly developed eluvial horizon below
the ploughLig layer (Andersen in press). Samples were taken in the L
— field, which is under conventional tillage with wi!lter ploughing,
normal preparation of secdbed in spring and a yeary rotati3r 1 of ce-
reals, sugar beets and grass.
The experiments with farmyard manure and slurry were started
it 1972. Farmyard manure and slurry are given to the plots in the fol-
lowing amounts: 50 and 100 tons/ha each year, 200 tons/ha each second
year and 400 tons/ha each fourth year. Thesc amounts are equivalent
to 250, 0O, 1000 and 2000 kg N/ha, calculated from Nenmiing, 1976. A
control was included, receiving NPK fertili :er, 80 kg N/ha. In Decem-
ber 1976 all the above mentioned levels of manures were given.
Earthworms were sampled by the forir.alin method from a 0.5 m 2
sampling quadrat. 2 x 10 litres 0.4% formal.in solution was used per
quadrat. Formalin extraction was supplemented by top soil handsorting.
Sampling was performed in spring, April to M y, and in autumn, Octo-
ber, at presumed maximum activity of earthworms. There were four
plots per treatment of approximately 70 m 2 size. Two sampling unite
were taken per plot, yielding a total of eight sampling units per
treatment. The standard error of the mean by this number is between
10 and 20%. Sampling was made in October 1976, April 1977, October
1977 and October 1978. (I) and (II) in Table and 2 refer to April
and October respectively.
Biomass of earthworms was determined on specimens fixed iv 4%
formalin stored in 70% alkohol. No allowance was made for gut content
and weight loss in the storage liquid. The earthworms were sorted in-
to: 1) mature worms with clitellum present and 2) worms without cli—
tellum present.
Five species of earthworms were commonly found and identified
(Stöp—Bowitz, 1969) as A. Zonga, A. caUginosa, A. i’osea Savigny,
1826, A. ehl otiaa Savigny, 1826 and twnbricus ter2’eBtpia L. 1758.
As cc A. cal ginoa2 material from Fyn collected simultaneous-
ly with that of Askciv makes it probable (Cat’ s, 1972) that the Askov
material of A. oaliginoaa should be referred to as AlioZoboph ra tur—
gzda Eisen, 1874, and the Fyn material to A. tubsrcuiata Eisen, 1874,
the latter being consistently larger than A. tirgida. Probably also
A. trapezoidea Duge6, 1828, may be found in the Askov material.
RESULTS and DISCUSSION
Table 1 and 2 show the total number and biomass of earthworms/
m 2 per year, including the NPI( fertilizer control, while in Table 3
the combined effect of all years is given for the respective levels
of manures and in Table 4 correspondingly for the different species.
326
-------
a
TABLE 1. Total biotnass, g/m 2 of earthworms, at different levels of farmyard manure and slurry, collected in
October t976, April 1977, October 1977 and October 1978. Askov Resca ch Station.
FARMYARD MANURE SLURPY
76 h7 78ii 76it
CONTROL 13.2 22.6 22.0 17.3 13.2 22.6 22.0 17.3
50 t 11.6 14.5 25.2 41.5 11.4 19.6 23.8 40.1
100 t 23.5 23.2 37.3 39.7 13.1 26.4 34.1 35.4
200 t 15.2 27.7 41.1 38.1 10.8 19.7 22.1 34.0
400 t 12.0 21.6 32.8 39.6 9.0 19.1 19.1 39.2
TABLE_2. Total number of earthworms/rn 2 . Other data as in Table 1.
FARMYARD MANURE SLURRY
7611 _____ 78ir 76 77 fl 7811
CONTROL 101.1 122.9 150.8 131.3 101.1 122. 150.8 131.3
50 t 43 ..O 119.0 242.7 228.9 126.9 118.0 291.6 255.8
100 t 216.4 148.7 294.1 214.4 153.4 135.4 385.4 272.8
200 t 178.0 209.4 284.8 228.8 150.0 140.5 352.0 282.4
400 t 128.3 117.6 176.9 452.9 132.9 78.6 144.8 383.3
-------
The combined effect of the two types of manures was tested
by Students t—test to each other and to the control receiving 80 kg
N/ha.
Along the same lines Figures 1 to 3 shu the individual, effect
of manuring on the five collected species.
A. longa is favoured by FYM with a number per m 2 , which is sig-
nificantly above the number found in control plots, while slurry re-
duces the number of A. Zonga to a remarkable degree (Table 2). The
high number of A. Z.ongcz found in FYM compared to control plots is
caused by an increased reproductivity (Andersen in prep.). Thus there
appears to be a fast turnover of juvenile A. longa in FYM probably
influenced by the mechanical treatment, preventing a greater propor-
tion of the juveniles to reach maturity.
L. tcrr stri.a, the second, large species, is only found in low
numbers. This species also benefits from the FYM, and biomass here as’
well as numbers are signifi’ antly above controls. Because of its very
large size it yields 19Z of the total biomass in F M. As in A. Zonga
number is reduced by slurry t—eatment.
Both A. ionga and L. terre8trie possess well defined openings
of their burrows and on application of slurry this will infiltrate
the burrows and either kill some of the worms in the burrows or force
them to the surface, where they may perish, which has often been ob-
served in the field. The other three species, which do not possess
well defined openings of their burrows are not expc ed to the direct
influence of slurry to the same extend. Juveniles which in general
are closer to the surface than adults will also suffer more from the
direct act!on of the slurry.
A. caUginoaa is the dominating species oy number in both FYM
and slurry, including control. This species is greatly favoured by
slurry as well as FYM treatment, where numbers are significantly
above controls (Table 4). The most marked inf].ucence is seen in slur—
ty, where the biomass is significantly above both FYM and control.
The biomass in FYM is not significantly different from that of con-
trol plots.
A. Zonga and A. caUginosa seem to vary inversely as to number,
and the ressons for this are, 1) that A. caUginoea is less exposed
to the direct influence of slurry as explai ed above, 2) that . ion—
ga and A. caiiginoaa show different food preferences. Both species
ingest considerable amounts of mineral soil, but besides A. Zonga
seems to prefer the more particulate (more or less decomposed plant
debris) organic matter of FYM. which is not found in similar condi-
tion in slurry. A. Zonga has also been shown actively to seek up par-’
tides and clods of sewage sludge incorporated into the soil (Ander-
sen in press). A. calzginoaa on the other hand is a consumer of humus,
which may fit well with a soil where growth of bacteria and other mi-
croorganisms has been stimulated after the application of slurry (Fi-
gures 1 to 3).
A. rosea and chiorotica seem not to be greatly influenced by
the two types of manures, and data for these two species have there-
fore been combined in Table 4. Biomass in both slurry and PYM plots
328
-------
No. /m 2
50 t
CONTROL
EThJ
12345
-n -i
A. FIN
100 t
Th
12345
200 t
12345
Influence on individual earthworm spe’ies of
different levels of manure. A. Farmyard ‘nanure,
B. Slurry. Number/rn 2 of 1)A. Z onga, 2)A. caii—
ginoaa, 3)A. r aea, 4)A. chiorotica, 5)L. torre—
etl’28. Mean of data from October 1976 to October
1978.
150 —
100 —
50 —
400 t
/m2
12345
Thr
-ri - 1
1
150
100
B. SLURRY
t 200t
50 t
12345
CONTROL
50
400 t
FIGURE 1 .
12345
12345
12345
12345
329
-------
2
1
1
A. FYM
100 t 200 t
CONTROL
50 t
400 t
12345
12345 12345 12345 12345
B. SLURRY
100 t
1
1
50 t
CONTROL
200 t
400 t
r
Th
-rn
5
FIGURE 2 . Biomass of eartliworins, g/m 2 . Other data as in
Figure 1.
330
-------
No./m 2 SLURRY
150 —
100 —
r
IL
12345
r
Th
12345
CONTROL
I-
12345
g/m 2 SLURRY
B. BIOMASS
FIGURE 3 . Influence of farmyard manure and slurry. A. No.1
m 2 . B. Biomass g/m 2 . From data shown in Table 4.
Earthworm species as in Figure 1.
A. No .
FYM
50
TL
15
10
5
FYM
CONTROL
331
-------
TABLE 3. Total number and biomass gun 2 of earthworms at diff2rent le-
v ls of farmyard manure and slurry expressed as the meazi of
data from October 1976 to October 1978. Tables I and 2.
No./m 2 g/Tn 2
FYM SLURRY FYM SLURRY
CONTROL 126.5 126.5 20.0 20.0
50 t 183.3 199.1 23.2 23.2
100 t 218.4 236.7 30.9 27.2
200 t 225.2 231.2 40.0 20.7
400 t 218.9 184.8 26.5 21.5
TABLE 4 . The combined effect of different levels of farmyard manure
and slurry given as the mean of number and bioinass g/m 2
from October 1976 to Ottober 1978.
TREATMEMT SIGNIFICANCE
SLURRY FYM CONTR . S/c F/C S/F
A. longa g/m 2 3.80 8.90 7.24 +++ —
A. caliginoea 14.44 8.70 10.41 +4+ — +++
A. rosea ÷ A. chlorotica 3.38 3.88 4.04 + — ++
Lwnbricus terrestrie 1.68 5.42 2.70 + 4+ +++
Total 22.30 27.90 24.40 — + +++
A. longa No./m 2 11.50 42.62 18.68 +++ +4+ .4+4
A. caiiginosa 153.08 105.00 59.96 +++ +++ +++
A. rosea + A. chiorotica 43.36 50.92 43.82 — + 4+4
Lwnbricus terrestris 3.74 15.26 4.74 + +++ +++
Total 206.68 213.82 127.22 +4+ +++ —
Degrees of freedom (154) (154) (254)
was lower than control, but the number was highest in FY)!.
The total number of ear hwocms is equal (Table 4) in FYM and
slurry, and significantly higher than in control. The highest bio—
raass is seen in PYM. whersas bioinass i slurry was slightly lower
than in control. This small difference, however, was not significant.
In A. caliginoea the proportion of ad lts is 10% in both FYM
and slurry, but 26% in contcol (Andersen in pi p.). In A. Z.onga the
respective percentages are 10, 3 and 13. The number of adults is not
very different between the two types of manures and control, and an
increased reproduction appears to be the main effect. of the manure.
Slurry increases only the A. caligincea population, wbereas FYM in
general favours all species.
The reason why total number of adults does not incre.,se, cor-
responding to the itacreased reproductivity, probably lies in the fact
that the mechanical treatment levels off pop’ilation size each year.
:3:32
-------
Therefore the resulting biom’ ss in the two types of manuree is not
very much different from controls, although biomass in FYM (Table 4)
is significantly greater than biomass in slurry. The main reason for
this is the contribution by 19% from L. terrestr’Cs in Fm as cipposed
to only 7% in slurry, and the negative effect of slurry on the two
largest species A. 1.onga and L. terreatri8.
A more detailed picture of the influence of the two types of
manurer is seen when the influence of the different levels of manures
on population size is studied. In FYM A. Zorzga and A. caliginosa are
dominating with respect to nuinb r, and it is seen that the number of
A. ocziiginooc is increasing with increasing level of FYM (Figure 1).
With respect to biomass A. longa and A. caliginosa are equally impor-
tant, e d the ma cJmum values are reached (Figure 2) at 100 to 200
tons FYM/ha. Also tise biomass of 1. terreetrie is great at these le-
vels.
In slurry A. caUgi’iosa is the sole dominating species. T ae
maximum number and biomass are reached at 100 tons/ha (Figures 1 and
7). The maximum value for total number and biomass is ceen at 100 to
200 tons slurry’ha (Table 3).
Short term effects are seen in the spring of 1977 after appli-
cation in December 1976 of the different quantities of manure (Tables
1 and 2). For 50, 100 and 230 tor.s there are no significant differen-
ces in the number/ in 2 , but at 400 tons there is a decrease in the num-
ber of A. caUginoea with up to 50% in slurry. In October 1977 and in
October 1978 very high values are recorded in both FYM and slurry.
This is caused by an enormous hatching of new individuals.
The biomass seems contrary not to be affected in the same way
(Table 2), which indicates that a short term effect is mostly seen
in the juvenile individuals on application late in the year. These
are generally encountered in the more superficial layers of the soil
profile compared to adults, because of reduced burrowing capabilities.
Therefore juveniles will be more exposed to lhe direct influence of
the manures on the time of application iu December, where the adults
have moved deeper into the soil.
It is seen that a general increase in both number and biomats
has taken place from 1976 to 1978 (Tables 1 and 2). The low levels of
number and biomass seen in October 1976 were probably caused by se—
ve;:e sunmer drought in both 1975 and 1976. The influence of climatic
conditions are best seen in control plots and in plots receiving ins—
cure each year i.e. 50 and 100 tons/ha. In the spring of 1977, com-
pared to October 1976, there is a greater biomass (Table 1) in these
three treatments, whereas total number (Table 2) is little changed
or slightly lower. This is consistent with other studies (Rundgren,
1977). showing that in spring the number in general is lower than in
autumn in temperate regions. In OcPober there is a further increase
in biomasa at 50 and 100 tons/ha, whereas biomass in control is un-
changed. This is caused by the greater amount of available food in
FY 14 and slurry treated plots. In the spring and early suier of 1978
the activity of earthworms .,as low because of adverse climatic con-
ditions, but during July to October activity was very high (Andersen
in press). In control this caused a drop in biomass recorded in Octo—
3 33
-------
ber 1978 compared to October 1977. At 50 to 200 tons/ha biomass was
increased, although the number was lover. At 400 tons/ha there seems
to be a long term effect of this large amount of manure. In October
1978 there is a considerable increase jr number as well as in biotnass.
This is mai 1y caused by a very large hatching of new individuals of
A. caUginosa and likewise an increase in the number of adult indivi-
duals, especially in FYM.
The general impressior. is that FTh favours more balanced pro-
portions of the tndividual species than does slurry. The reason for
this must be that FYN satisfies the food requirements of a greater
number of species as compared to slurry, which also has a direct ne-
gative effect on deephurrowing species. The edaphic and biological
significance ot these findi’igs is that a greater number of deepbur—
rowing species as found by FYM treatment favours water infiltration
rates (Baeumer and Bakermans, 1973), gas exchange and deep rot pene-
tration. These soil properties are of great value f,r the crop dur-
ing both heavy rain and periods of drought.
QUESTIONS and COMMENTS
E.F. NEUHAUSER : Please differentiate between slurry
and farmyard manure.
. ANDERSEN : Slurry is a mixture of urine and faeces,
gericr lly encountered in intensive cattle and pig manage—
me: t. The slurry is stored in barrels in a liquid state
as cpposed to farmyard manure which is in a semi—solid state
also containing a certain amount of straw.
. HILL : Have you looked, or do you intend to look,
at the effects of composting manures or their effects on
e arthworins?
C. ANDERSEN : This has not been studied by us.
3311
-------
LITERATURE CITED
Andersen, C. (in press). Activity and vertical distribution of earth-
worms as influenced by climatic conditions in arable soil in Den-
mark. The Royal Veterinary and Agricultural University, Yearbook.
Andersen, C. (in press). Lead and Cadmium content in earthworms (Lum—
bricidae) from sewage Bludge amended arable soil. VII Internatio—
nal Colloquium on Soil Zoology, Syracuse.1979.
Baeumer, K. and W.A.P. Bakermans. 1973. In Advan. Agron. 25.
Barley, K.P. and A.C. Jennings. 1958. Earthworms and soil fertility.
III, the influence of earthworms on the availability of nitrogen.
J. Agr. Res. 10:364—370.
Currey, J.P. 1976. Some effects of animal manures in grassland. Pedo—
bic.l. 16(6:425—439).
Dexter, A.R. 1978. Tunneling in soil by earthworms. Soil Biol. Bio—
chem. 10(5:447—449).
L)unger, U. 1969. Fragen der NatUrfl.chen und Experiinentellen Besied—
lung Kulturfeindlicher Böden durch Lumbriciden. Pedobiol. 9:146—
151.
Edwards, C.A. 1975. Effecrs of direct drilling on the soil fauna.
Outlook Agric. 8:243—244.
Edwards, C.A. and .J.R. Lofty. 1976. The invertebrate fauna of the
Park Grass Plots. I. Soil fauna. Rothamsted Report for 1974,
part 2:133—154.
Gates, G.E. 1972. Burmese earthworms. An introduction to the syste—
matics and biology of tnegadrile oligochaetes with a special re-
ference to South East Asia. Trans. Amer. Phil. Soc. 62(7:1—326).
Craff, 0. and H. Kuhn. 1977. Inf_uence of earthworm activity in a
straw amended soil. Nutrient uptake und yield of ryegrass. Land—
wirtsch. Forsch. 30(1:86—93).
Leger, R.G. and G.J.F. Mile te. 1977. Properties of four Quebeck
soils after incubation with five species of earthworms. Can. 3.
Soil Sci. 57(2:165-171).
Nenmiing, 0. 1976. Animal manures for clover grass and pure grass.
1269. beretning fra .tatens Fors gsvirksomhed i Plantekultur:237—
257.
Rogaar, li i-nc J.A. Bcswinkel. 1978. Some soil morphological effects
of earthworm activity; field data a d X—ray radiography. Nether-
lands 3. Agric. Sci. 26(2:133—145).
Rundgren, S. 1977. Seasonality of emergence of eart1 vort.s in Southern
Sved’ n. Oikos 28:49—55.
Scbwer”tle, F. 1969. Untersuchungen zur Populationsdichte ,on Regen—
wil’meru bei herkömmlicher Bodenbearbeitung und bel “Direktsaat”.
Z.f. Pflanzenkrankh. Pflanzensch. 76 (11/12:635—641).
Seyers, J.K., A.N. Sharpel.y and D.R. Keeney. 1979. Cycling of nitro-
gen by surface casting earthworms in a pasture ecosystem. Soil
Biol. Biochem. 11(2:181—187).
Sharpley, A.N. and J.K. Seyers. 1977. Seasonal v ariation in casting
activity and the amount and release to solution of phosphorous
forms in earthworm casts. Soil Biol. Biochem. 9(4:227).
Stbp—Bowitz, C. 1969. A contribution to our knowledge of the systema—
tics and zoogeography of Norwegian earthworms (Annelida, Oligo—
chaata: Lumbricidae). Nytt Magasin for Zoologi 17(2:169—280).
Wilcke, D.E. 1962. Untersuchungen tiber die Einvirkung von Stalimist
und MineraldUngung auf den Besatz und die Leistung der Regenw ir—
mer in Ackerboden. In Monographie zur Angew. Er.t. Beihefte z.
Zeitschr. Angew. Ent. 18:121—163.
33.5
-------
EFFECTS OF HEAVY PIG SLURRY CONTAMINATION ON
EARTHWORMS IN GRASSLAND
J. P. Curry and D. C. F. Cotton
U ivers,ty Coilegi
Irelatul
IP’TRODUCT ION
Animal manures applied to grassland on various soil types as
semi—liquid slurry, have shown no significant Ill effects on earthworms
when spread at rates related to sward nutrient requirements and
transitory detrimental effects when these rates exceeded sward nutrient
requirements by an order of magnitude (Curry, 1976; Cotton and Curry,
1979a, b).
This paper reports on some effects of gross contamination,
arising from the disposal of large quantities of pig slurry over a period
of several years, on earthworm populations. Pig slurry can contain up to
700 ppm (dw) of copper resulting from the addition of 200 ppm copper as
sulphate salt to pig feed (McGrath et al. 1977). Accordingly, particu-
lar attention was given to the possibility of toxicity to earthworms
from this source.
EARTHWORM POPULATIONS
An abandoned quarry in an old pasture field at Ceibridge, Co.
Kildare, had been used for disposing of large quantities of pig .sluury
for 6 — 7 years until just over one year prior to our first earthworm
sampling. The quarry was located on a 25° s’ope and In wet weather the
slurry periodically overflowed, heavily contaminating the pasture down-
hill. The last major overflow prior to earthworm sampling occurred In
the Spring of 1977.
In April and November 1978 earthworms were sampled by the formalin
method at intervals along a gradient from the quarry lip to 76 in down-
hill. Soil and earthworm samples from each sampling station were
retained for copper analy 1s by atomic absorption spectrophotonietry.
Earthworms were held for 3 das to permit expulsion of soil from the gut
prior to analysis.
Earthworms were virtually absent from soil in the lnvnedtate
vicinity of the quarry In April (Figure 1) but populations reached a
density comparable with that in adjacent uncontaminated pasture at about
60 in downhill from the quarry. Blomass data exhibited almost identical
trends (Figure 2). Table 1 gives the species composition of the fauna
In April. In heavily contaminated soil adjacent to the quarry the com-
post worn, Elsenia foetida , was virtually the only species present.
And the surface, organic matter feeding species, Satchelhius maninalis
336
-------
oNov 78 oApril 78
Adjacent uncontaminated area
30 60
DISTANCE FROM QUARRY (m)
‘37
• oil ( pril 76)
2 Edge of contaminated area
Fig. 1. Density of earthworms.
Mean nos. at each
sampling station with
standard errors
Fig. 2. Mean Diomass of
earthworms with
standard errora
Fig. 3. Mean copper levels
with standard errors
0
0
120
80
40
c J
E
1
U
0 .
In
I.
U
E
a)
80
a
40
0
Is
120.
LI
1”
0
90
-------
TABLE 1. Earth ,.’orrn density (Hos m 2 ) at increasing distances
from the quarry in Apr11, 1978.
5s9
*
l an
37m
62m
Adjacent
uncontami tiated
area
Allolobophora chiorotica
(5ev.)
Aporrectodea callginosa
(Say.)
A. rosea (Say.)
. 1on a (LJde)
101 obophora/Aporrectodea
(ininatures)
Satcheillus manunalls (Say.)
Elsenla foetida (Say.) 2
Lumbricus terrestris 1.
1
4’
4
4
80
28 13
8
7
4
2
10
9
2
3
69
10
2
2
23
16
2
3
3C
14
1
2
63
3
2
12
L. festivus (Sav.J
L. castaneus (Say.)
L. rubellus Hoff.
Lumbri cus inmiatures
4
80
16
1
1
4
8
7
27
30
2
2
54
Total 2
228
14
51
191
185
*at edge of contaminated area
and Lumbricus spp. were present In Mgher proportions along the gradient
than in tree field away from the organic spill. This was particularly
true of one sample 5 m from the quarry at the edge of the spill where the
fauna appeared to have escaped decimation by the Spring 1977 overflow.
By November populatIon density and biomass had reached high eve1s,
particularly at the quarry edge where density exceeded 500 wonns/m and
bicinass exceeded 160g rn 2 (Figures 1 and 2. Table 2). At this time the
fauna In the vicinity of the quarry was dominated by surface dwelling
pigmented species, notably Lumbricus festivus , L. castaneus and E. foetida .
These species, and also S. maimnaliS and Den odrilus rubidji , decreased
noticeably in numoers with ii rea Tng distance from the quarry. By con-
trast, typical grassland soil species of the genera Allolobophora and
Aporrectodea were considerably more scarce in the vicinity 0f the quarry
than they were farthor down the slope, suggesting that these species are
much slower to recover from the slurry toxicity.
COPPFR TOXICITY
esults of copper analysis carried out in April 1978 conflnned
the presence of a gradient In the soil (Figure 3). Copper concentrations
338
-------
TABLE 2. Earthworm density I1os rn 2 ) at increasing distances
downhill from the quarry in Nov nber, 197E.
Qn
ii
15m
3 n
55n
iBm
Allolobophora chiorotica (Say.)
Aporrectodea caliginosa (Say.)
rosea (SaY.)
.1on9a(Sav.)
11oTobophora/Aporrectodea
38
2
1
16
22
3
1
16
29
17
2
38
74
24
3
3
54
130
23
4
61
82
29
11
4
132
ininatures
Satchellius maninalls (Say.)
Dendrodrflus rubidus (Say.)
DendrodrlTüs ininatures
Elseni a foetida (Say.)
V bricus terrestris L.
26
30
15
65
26
26
24
42
1
7
12
5
14
2
7
7
17
8
12
4
8
39
4
14
1. festlvus (Say.) -
t. castaneus (Say.)
t. rube11i iHoff.
Lumbricus Ininatures
61
82
19
155
32
42
26
155
50
14
62
34
17
10
17
94
38
15
8
119
4
18
Ii
82
Lumbricus eiseni Lev.
3
6
Elseniella tetraedra (Friend)
Octolasion cyaneum (Say.)
Octolasion lii*atures
1
5
‘
Total
514
422
291
327
430
437
In eartlwiorms in April paralleled this gradient, the highest levels
(82.5 ppm) recorded being in specimens of Lumbricus terrestris from
about 10 m e1ow the quarry lip. A less gradient in earth-
worm copper levels was recorded In Noveuber although a strong negative
correlation between copper levels and distance from the quarry was In
fact recorded Cr = -0.93).
There is evidence to suggest that levels of soil copper comparable
to those occurrir j adjacent to the quarry can be extr ne1y toxic to
earthworms (Nielscn, 1951; van Rhee, 1977). AccordIngly, further field
sampling and some laboratory tests were carried out to assess relation-
ships between pig slurry and possible copper toxicity to earthworms.
Table 3 gives data for two contrasting situations. Clearly. short-term
applications of pig slurry at high 1e’ e1s ha’c ’ little Influence on soil
or eerthworm copper levels. Long-term dumping at Ceibridge resulted In
a very significant elevation of soil copper and a much less pronounced
elevation In earthworm bodies. The copper content of the earthworm
faeces (460 ppm) reflected very closely that of the soil.
339
-------
TABLE 3. Levels of copper (ppm) In earthworms from
soils contaminated by pig slurry.
Contaminated
Site Soil
Earthworms
from Contain-
mated Soil
Earthworms
from IJncon-
taminated Soil
1.
Celbridge, Co. Kildare,
abandoned quarry where
large amounts of
slurry were dumped
1960-71.
483
53.6 10.5
16.3
2.
Johnstown Castle, Co.,
Wexford , sandy loam
grassland soil which
received 690 m 3 ha
20
18.5
17.5
slurry during 1976—77
Earthworms were cultured in two old pig slurry composts obtained
from disposal sites at (elbrldge and containing respectively 101 and
483 ppm copper. Worms of mixed species composition from local grassland
were used, six worms being added to each 1 kg glass culture Jar. Figure
4 indicates survival in the two culture series and Figure 5 shows how
copper levels in survivors varied with time. Survival trends were
fairly similar in both types of slurry until the third month when much
greater mortality was evident in the high-copper slurry. Thereafter,
the trends were fairly similar with approximately 30% survival until
the seventh month. Trends in earthworm -‘ pper levels remaining fairly
constant at 30 to 50 ppm in the “low copper” slurry whereas levels in-
creased quite dramatically in the “high copper” slurry, reaching 200
ppm after 5 months.
DISCUSSION
The study confirms that gross pig slurry pollution of grass 1 and
Is extremely toxic to earthworms in the short term. Test Introductions
Indicate that the slurry is no longer toxic to the coprophilous species
E. foetida after 4 wk but considerably longer is required for signifi-
cant natural recolonization to occur. It appears to take 12 to 18
mo for populations to recover to pre-contaminatlon levels and probably
considerably longer for many true soil-feeding grassland species.
The likely effects of high soil copper levels arising from pig
slurry on earthworm numbers are problematical. Mitchell et al. (1978)
-------
300
200
100
0
Months
Fig. 4. Survival of earthworms in slurry containing 101 ppm ( —.— )
and 483 ppm ( —o- ) copper.
Months
Fig. 5. Mean copper levels in earthworms in slurry containing lOlppm (—.-—)
and 483ppm (—0--—) copper.
6
4
2
U,
0
I-
S .-
0 )
I-
(0
•0
(0
4. ,
U,
-C
4 . ,
a. ’
S..
4- ,
U
I-
a)
U,
I.
C)
.
C
C
I0
U,
5-.
0
5-
I-
C)
V
5-
•0
0
(0
4- )
U ,
-C
4. )
.r-
0.
U-,
I—
C)
C)
S..
a)
0.
0.
0
1 2 3 4 5 6
31e1
-------
reported thriving populations of E. foct da in soil-sludge mixtures con-
taining up to 253 ppm Cu. most of which they considered to be largely
inmiobtle. On the other hand, present results suggest that toxic
copper doses can be acquired by earthworms from pig slurry. A diffi-
culty arises in determining how much of the copper present in slurry
is available to earthworms. Slurry copper is predominantly tightly
complexted in organometal form with minimal amounts (less than 3% In
the ptesent case) being acetic acid soluble. Copper levels recorded
in earthworm faeces suggest that most of this material passes through
the gut unabsorbed, but yet levels recorded from earthworm bodies can-
not be accounted for by the acetic acid soluble fraction alone. 11
appears likely that further fractions may be decomplexed and absorbed
during passage through the gut, thus leading to mortality or to the
kind of accumulation Illustrated in Figure 5. More Information is
needed on the availability of organic copper to earthworms before a full
assessment can be made of the environmental effects of heavy pig slurry
contamination.
ACKNOWLEDGMENT
We are indebted to colleagues in the Soil Science Department for
advice and assistance with the estimation of copper.
LITERATURE CITED
Cotton, D.CSF. and J.P. Curry. 1979a. The effects of cattle and pig
slurry fertilizers cm earthworms (Oligochaeta, Lumbrlcldae) in
grassland. Pedobiol. 19.
Cotton, D.C.F. and J.P. Curry. 1979b. The response of earthworm
populations (Oligochaeta, Lumbricidae) to high applications ‘f
pig slurry. Pedoblol. In press.
Curry, J.P. 1976. Some effects of animal manures on earthworms in
grassland. Pedobiol. 16:425-438.
Keeney, D.R. and L.M. Walsh. 1975. Heavy metal availability In sewage
sludge—amended soils. !n Proc. mt. Conf. on Heavy Metals In the
Environ., Toronto, Ontario, 27-31 Oct. 1975, Agrlc. Inst. of
Canada, Ottawa.
McGrath, D., G.A. Flaming and D.B.R. Poole. 1977. Hazards to pasture
and animal health arising from the land-spreading of copper-
containing pig manure. Symposium on Animal Manures, An Foras
Taluntais, Johnstown Castle. (Unpublished).
Mitchell, M.J., R. Hartenstein, B.L. Swift, E.F. Neuhauser, B.!. Abrams,
RJl. Mulligan, B.A. Brown, D. Craig and D. Kaplan. 1978. Effects
of different sewage sludges on some chamical and biological
characteristics of soil. J. Environ. Qual. 7:551—559.
yi.z
-------
Nielson, RI. 1951. Effects of soil minerals on earthworns. N.Z.J.
Agric. 83;433-435.
Rhee . J.A. van. 1977. Effects of soil pollution on earthwori s.
Pedoblol, 17:2C1—208.
QUESTIONS and COMMENTS
M.S. GHILAROV : Why is the copper content in pig slurry
so high?
J.P. CURRY : Because of the practice of adding 200 ppm
of copper as su1p ate salt as a growth promoting substance
in pig diets.
S.B. HILL : I feel thac we should be cautious to con-
clude that the repeated addition of non-biodegradable, p0-
tentially toxic materials, such as copper, to soils do not
pnse a problem. Surely the only outcome can be a jradual
increase in the concentrations of such materials (or their
dissipation into adjacent environments where they may also
have negative effects) and tije eventual reaching of thresh-
old levels at v1 ich negative effects are experienced. The
fact that copper is initially unavailable may not be permanent.
Critical thresholds may be reached, for example, following
a change in soil management practices. (Just as chlorinated
hydrocarbons stored in our own fat tissues are harmless until
we decide to lose weight:)
J.P. CURRY : I agree and indeed I am unhappy about the
assumption that seems to be frequently made that heavy metal:3
in organic wastes are largely unavailable and do not there-
fore constitute an environmental hazard.
14. HASSALL : Do you know in which tissues of the earth-
worm the copper is accumulated?
Do you know how efficiently the earthworms are at ex-
creting this copper load when returned to a copper free diet?
J.. .  S! : No, nor have I been able to find any in-
formation in the literature on this point.
No, in answer to your second question.
H. EXJSACF.ERS : Did you notice any avoidance of the con-
taininated soil by the earthworms?
.P. CURRY: No. We have observed that earthworms ex-
posed to heavy slurry contamination are killed very quickly
and we do not consider that they would be able to move out
c.f the affected area quickly enough to avoid the effects of
a major overflow.
-------
EARTHWORMS AS BIOLOGICAL MONITORS OF CHANGES IN
HEAVY METAL LEVELS IN AN AGRICULTURAL SOIL IN
BRITISH COLUMBIA
Alan Carter, Elizabeth A. Hayes and L. M. Laukulich
Unioers:iy of British Columbia
Canada
ABSTRACT
Individuals of Lumbricus rubellus and Allolobophora chiorotica were
sampled from an agricultural soil on Westham Island, British Columbia,
Canada. Earthwnrms, their faeces and soil were analyzed for cadmium,
copper, lead and zinc. Cadmium and Zn were concentrated by all species over
the soil levels while copper and lead were not. Mature adults of
L. rubellus had higher levels of Cd than had Immature adults.
In the laboratory, sewage sludge with high levels of the above
heavy metals was added at different rates to the soil. The effects of
the treatments on the concentrations of heavy metals in earthworm tissue
and faeces were examined. Of the metals, cadmium levels in the earth-
worms increased until soil levels exceeded 6 ppm.
INTRODUCTION
Various species of earthworms have been found to concentrate certain
heavy metals, both In soils which had low levels of metals and in soils
which were contaminated and so had high levels (see review In Fdwards and
Lofty. 1977). In recent studies, cadmium was concentrated by the compost
wona, Eisinia foetida Savigny and cadmium, nickel and zinc were accumulated
by individual. of this species when sewage sludge was amended with various
amounts of salts of these metals (Hartenstein et al., in press). In
Copenhagen, l enmark, Andersen (In press) found that several species of
earthworms concentrated cadmium, but not lead, over soil levels. In the
United States, a particular earthworm species studied by Helmke et al.
(1979) concentrated Cd, cobalt, mercury and Zn. Their field study on
the effects of sewage sludge application on heavy metal levels in earth-
worms showed that Cd, Zn and Cu levels in earthworm tissue increased as
sludge application rates Increased.
Earthworms I ave been shown to be Important ifl redistribution of
Cd, carbon and cesium in soils in the southeastern United States (Oak
Ridge National Laboratory, 1974). The Introduction of European species t
New Zealand pastures has greatly increased the amounts of molybdenum
available for plants (Edwards and Lofty, 1977). The Oak Ridge report,
referred to above, included data from radlotracer experiments. Such work
needs to be done in concert with Investigations of levels of stable
Isotopes of heavy metals in earthworms and their food. However, for a
3 4
-------
thorough evaluation of the role of earthworms in heavy metal redistribution
by their burrowing, feeding and excretory activities, data on possible
variation in soil according to depth and the corresponding levels in tissue
and faeces of earthworms in relation to age, species of worm and seasonal
activity are required. Ireland and associates studied variation within
earthworm species according to season and also variation between species.
Lead levels were highest in the winter months (Ireland and Wooton, 1976)
and Pb and Zn concentrations varied between the two species examined.
The objective of this study was to determine if earthworms could be
used to monitor levels of heavy metals in a particular soil. To investigate
this we compared the levels of cadmium, copper, lead and zinc in soil
collected from Westha Island, British Columbia and in the tissue and faeces
of different species of earthworm living in that soil. In the laboratory,
the effects of applications of sewa ie sludge, with high levels of the above
metals, on the concentrations in soil and earthworms were then investigated.
METHODS -
Random samples of earthworm populations in a clover field on Westham
Island, British Columbia were taken along line transects in September and
November 1978 and in April 1979. Worms were washed with cistilled water and
individually placed in plastic Petri dishes with moistened ashless filter
paper for six days and kept at 15 C. Faeces were collected daily. Earth-
worms and faeces were dried at 65 C for four days and then weighed on a
ml crobal ance.
The sample preparation method for earthworm tissue and faeces
depended on sample size. Earthworm samples of between 10 and 120 mg dry
weight and faecal samples of between 10 and 75 mg dry weight were acid
digested in small glass tubes while earthworms and faeces heavier than the
above weights were acid digested in glass beakers. The latter method was
also used for soil samples of approximately 250 mg dry weight.
The first method is a modification of that described by Kolrtyohann
et al. (1976). Oven—dried samples were weighed into glass vials (Kimax
70 x 20 m O.D.) and solubilized with concentrated HNO 3 and 30% H 2 0 2 using
a block digestor set at 150 C.
The method for larger samples was modified from Van Loon and
LichWa (1973). Samples were digested with concentrated HNO 3 in 100 ml
glass beakers heated on a hot plate. All glass and plastic containers
were washed in fiN HNO 3 . and water used for all dilutions and rinses was
distilled in glass and deionized.
Analysis of Zn, Cd, Pb and Cu was done using a Perkin-Elnier Model
3J6 atomic absorption spectrophotometer equipped with an HGA-2100 graphite
furnace and deuteriuni arc background compensation. Most samples contained
sufficient Zn (>0.5 ppm) for flame analysis. Cadmium. Cu and Pb analyses
were done using the HGA-2100. Twenty ui injections were made two or three
times from each sample. In all runs, NBS orchard leaves and bovine liver
“ .5
-------
and soil standards Were u:ed to check for accuracy. Also, an internal worm
standard was made up of earthworms wno gut . had been voided prior to
killing, drying and thorough grinding. Standards were prepared in O.16N
HNO 3 .
RESULTS
Cadmium and Zn were concentrated by all earthworms ever the soil
levels,and the low levels of these elements in the faeces (Table 1)
reflected their high assimilation by the earthworms. Mature adults of
Lumbricus rubellus had higher levels of cadmium than had inm’ tures
(Figure 1 and Table 1).
Copper and Pb levels in earthworm tissues were low in comparison
with soil levels.
Mature adults of L. rubellus were used in the sewage sludge
experiments. The effects of sludge applications on cadmium and copper
levels in the soil and in the tissue and faeces of this earthworm are
shown in Figure 2 and in Figures 3 and 4 respectively.
Cadmium concentrations in earthworm tissue Increased steadily as
soil levels increased to approximately 6 ppm after which concentrations
In the former appeared to level off. Concentrations in the faeces
initially increased but levelled off after soil levels exceeded 2.4 ppm.
In contrast, Cu concentrations in earthworm tissue and fa r .re not much
affected by sewage sludge applications. Variar’ces around t. -
in both these substrates were wide but concentrations were cot1si. -..
higher In the faeces (Figure 4).
DISCUSSION
Soils with lcw levels of metals
Data from other studies are conpared with t)se fra n this study in
Table 2. Where possible,we have indicated whether the earthworm san les
analyzed included mature adult3 er in nature adults or both. In all cases,
Cd was concentrated by earthwo: 1 is 3nd thf lev 1 ’ s in faeces were low.
Lowest levels of Cd were found i,i samples of mixed genera of various age
groups (see, for example, -- .;o data of Gish and Christensen, Table 2).
These low levels may have be ’, ‘ .ie t3 pooling of some earthworm species or
age groups 0 f low Cd levels t,ith other species or age groups of high levels.
In this regard, the low concentrations of Cd for ininature adults of
Lumbricus rubellus found in our study suggests that there may be variation
between different age groups of this species in other parts of its
geographical range and between age groups of other species also.
Low Cu levels occurred in both tissue and in faeces of earthworms
collected from soils vlth low levels. Lead levels in earthworms in our
-------
BLE I. LEVELS OF HEAVY METALS IN TISSUES AND FAECES OF EARTHWORMS COLLECTED
FROM WESTHAM ISLAND, BRITISH COLUMBIA
ppm DRY WEIGHT t SD
CADMIUM COPPER ZINC LEAD
TISSUE FAECES TISSUE FAECES TISSUE FAECES TISSUE FAECES
Lusthrlcus rubellus
Nature Adults 10 ± 3.0 (19) 0.3 ± 0.10 (15) 10 ± 3.0 (8) 30 t 2.7 (17) 260 ± 40 (13) 50 t 13 (15) 0.30 2 0.10 (5)
Ininature Adults 4 ± 1.0 (19) 0.2 t 0.03 (9) 13 ± 4.0 (5) 24 * 6.0 (10) 270 ± 30 (19) 35 ± 7 (9)
Allolobophora
chiorotlca 8 * 2.4 (13) 0.3 ± 0.10 (5) 8 ± 2.4 (9) 25 ± 4.9 (5) 21U ± 45 (14) 0.60 ± 0.50 (9)
Number of samples In parentheses
-------
151 x MATURES
• IPI1MATURES
10
I
CADMIUM
(ppm dry ut.) *
I
I
S
5
• • S
• I
• S. •
•
0 ______ _ p
0 40 60 120 160 200
BODY WEIGHT OF EARTHWORMS (mq dry wt.)
Figure 1. Cadmium levels in imature and mature adults of Lumbricus
rubellus
-------
RATE (g/kg)
Cu
(ppm dry wi.)
Figure 2. Effects of various appllcdtinn
heavy metal leve s in soil.
rates of sewage sludge on
2
Cd
8
Cd
(ppm dry wt.)
4
30
I0
0 (CONTROU 5 10 25 50 100
SLUDGE APPUCATION
0
-------
CADMIUM
IN
EARTHWORM
TISSUE
AND
FAECES
(ppm dry wt.)
5O
40’
30’
20
0
g (10)
f
zf
Figure 3. Effects of sewage sludge applications on cadmium levels in
tissue and faeces of mature adults of Lumbrjcus rubellus .
Rates of sludge application (g/kg air dried soil) in
parentheses.
I t SD
EARTHWORM FAECES
I t SD
(50: SEWAGE - g/kg)
E(25)
‘(100)
a
I
U - I
2 4
CADMIUM
6
I
8
- U • I
10 12
IN SOIL (ppm dry wt.)
-------
Figure 4. Effects of sewage sludge applications on copper levels In
tissue and faeces of mature adults of Lumt,ricus rubellus .
Rates of sludge app ication (g/kg air dried soil) in
parentheses.
100 EARTHWORM TISSUE. 1± SD
COPPER EARTHWORM FAECES T t SD (50: SEWAGE q/kg)
IN
80
EARTHWORM
TISSUE
(100)
AND 60’ (25)
FAECES 100)
(ppm dry wt.) 40
(0)1
I T
20’ 1 T I
I
V V • • I — • — — U V V - • V V •V
50 40 S0 70
COPPER IN SOIL (ppm dry wt.)
‘1
-------
study and In other studies were also low (Table 2). In all studies, Zn
was found to be concentrated by earthworms. Levels in faeces were
uniformly low.
Soils with high levels of metals
The very high levels of Pb In the acid tolerant Lumbricus rubellus
and Dendrobaena rubida from a mining area in Wales are strikin4j. This Is
the only case In which Pb is reported as having being concentrated by
earthworms over soil levels. The low levels of Pb in these species
collected by Ireland ar.d associates from the controt site were still higher
than those reported in this present study and elsewhere and reflect a
rather high Pb level (150 ppm) in the soil lIable 2).
Several studies hive focused on the effects of sewage sludge
application rates on heavy metal levels In soil and earthworms. Other
stude . have considered the effects of pollutants from automoblleswhile
that of Van Rh9e (1977) looked at the effect of pig slurry, high In Cu,
on the levels in soils and earthworms. These studies and our study on
sewage sludge applications will now be considered so as to evaluate the
use of earthworms as monitors of heavy metal levels In soils.
Gish and Christensen (1973) found that samples of mixed genera of
earthworms accumulated Cd, Pb and Zn over the levels in soil adjacent to
highways with heavy automobile traffic. Some of their data are included in
Table 2. Concentrations of Cd, Pb and Zn in both earthworm tissue and soil
decreased significantly with Increasing distance from the highways. Thus,
earthworms could be used to monitor levels of these metals in this soil.
In relation to Cu, Van Rhee (1977) found a significant correlation between
Cu levels in soils ar.d in earthworm tissue in pastures contaminated in pig
slurry. In this case, Cu levels in worms reflected increases in soil
levels.
Data from the sewage sludge application experiments are more
olfficult to evaluate. This is particularly so for field studies; those of
Helnike et al. (1979), Hartenstein et al. in press) and Andersen (in press).
In such studies, it is difficult to sample sufficient numbers of earthworms
for good statictical analysesand in long term studies possible variation In
heavy metal levels In earthworms according to age and season should be
considered.
In our laboratory study, cadmlim levels In mature adults of
Luinbricus rubelids increased steadily until the soil levels exceeded 6 ppm.
Moreover, the Cd levels in the faeces of these earthworms did not change
when soil levels were approximately 4 ppm and greater. These data suggest
that the feeding and excretory activities of the worms slowed down. This
may have occurred because of toxic effects of high Cd levels (and perhaps
those of other metuls such as Ni) at the higher sludge application rates.
Such effects would be more pronounced in studies carried out In laboratory
containers, as ours was. In the field, sludge—amended soil under the
Influence of natural weather conditions would likely undergo more extensive
physiochemical and blo’ gical changes. This would affect the availability
of metals co earthworms. De Vrles and Tiller (1978) showed that glasshouse
352
-------
TABLE II. LEVELS 0 HEAVY METALS IN EARTI!WORHS AND SOILS FROM VARIOUS STUDIES
pp OR? WEIGHT CWINEN IS REFERENCE
TA lON CR0 111181 COPPER LEAD ZINC
tuberculets
13.7 9.2 260 Ft-ca Coitrol Ha i fa it el (1919)
Feecec (N) 0.55 10.6 60 A as
Soil 0.5 100
A eporectodea
trepezoides
Ylssue N) 0.4 10.5 1 300 E.A. Ilenney
Faeces N) 0.3 32 ‘4 60 (unpublished)
A llebophora
chlorotice Present stud3r
Tissue (N • I) 7.5 7.5 0.60
Feeces(M -lI) 0.30
Lisbricus
ru bel lus
Tissue (11) 10 10 0.30 260
Faeces (N 0.30 30 - 50
Tissue (I 4 U - 210
Faeces (I 0.3 % ) 24 - 35
Soil 1.4 37 15 110
EisiMe betide
Ti 5bue 8-46 20— ISO I - 53 68-210 Harten;teln eta)
Sludge 12-27 aeo —610 160- 900 075-2100 (in press)
L. rubellus - 13 3590 740 Ncevy Pci- Ireland and
öendrobrens rubide - U 7590 310 luted RIchards (1917)
Soil - 1960 800 Ctystwyth Site end
. Rubellus
Tissue - 15 2S 650 Control Site Ireland end
!. Rubida WOOtOR (I97 )
•Tliiue - 15 j j 250
Soil - 2 ISO 110
-------
TABLE II. CONTINUED
ppm DRY WEIGHT COIIMEIITS REFERENCE
TA lON CA DM I I J I COPPER LEAD ZINC
A ll o lob op hora
Andersen (in press)
Tissue 5.1 4.6
Faeces 0.53 45 0
Soil I Sewage Sludge 0.65 28
Tissue 9.2 5 9
Faeces 160 105
Soil & Sewage Sludge 0.99 39
Luiebricus terrestris
Tissue 14 14 From Near Andersen (in press)
Major Street
Soil 0.65 14fl
Van Hook (1914)
Tissue 5.7 4.7 320 Mean of 6
Sites
Soil 0.37 27 43
Distance from
Major Highwejs
Mixed Genera
TEIIi1M e I) 12.6 2 O SGIfl Gish and
Soil 1.23 468 ;dm Christensen (1913)
Tissue (H • I) 8.8 113 4Df J 2Dm
Soil 0.72 136 1
Tissue (N + I) 0.3 Si 410)
Soil 0.72 11 64.1 4Dm
tissue (H • I) 6.9 44 3201
6Dm
Soil 0.68 48 szJ
Tissue (H + i) 7.1 53 243 180 in
Soil 0.72 53 6
Tissue (N • I) 3.0 12 2201
0.66 14 42J Control
Soil
41 . Saeiples From Van Rhee (1911)
Tissue Mean of 9
Soil 24 - Sites
N ano I refers to mature adults and ieieature adults, respectively.
-------
experiments, even with large pots, can give completely erroneous indications
of the probable uptake of heavy metals by vegetables In sludge-treated soils
under field condi’ions. Also, the si .dge and soil used in our experimets
were thoroughly mixed. In field experiments, sludge would not be so well
incor .orated with soil and there would certainly be more heterogeneity in
soil levels of heavy metals. Earthworms might then disperse from local
areas of high Cd levels or might selectively feed on soil of lower Cd
concentrations.
Our study and other studies indicate that earthworms of various
species can ba used to monitor levels of cadmium in soil and, under certain
conditions 1 copper levels in earthworms reflect soil concentrations. Further
work is required to be done on the uptake of cadmium by earthworms from soils
with high levels. Sucn investigations should also be carried out in mini—
field plots.
ACKNOWLEDGEMENTS
We thank L.M. Lavfrulich for critical comments and B. von Spindler
for technical assistance with the Graphite Furnace. L.E. Lowe provided
soil standards. The study was financed y the Natural, Applied and Health
Sciences Grants Coimilttee (The University of British Columbia), National
Sciences and Engineeriruy Research Council of Canada (67-6177) ar.
Agriculture Canada 65-0360) grants.
LITERATURE CITED
Andersen, C. in press. Lead and cadmium coi tent in earthworms (Lumbricidae)
from sewage sludge amended arable soil. Proceedings VII Soil
Zoology Colloquium, Syracuse, New York.
De Vries. M.P.C. and K.G. Tiller. 1978. Sewage sludge as a soil amend—
m nt with special reference to Cd, Cu, Mn, Ni, Pb and Zn -
comparison of results from experiments conducted inside and out-
side a glasshouse. Environ. Pollut. 16:231-240.
Edwards, C.A. and J.R. Lofty. 1977. Biology of earthworms. Chapman
and Hall, London, second edition. 333 p.
Gish, C.D. and R.E. Christensen. 1973. Cadmium, nickel, lead and zinc
in earthworms from roadside soil. Environ. Sd. Tech. 7:1060-1062.
Hartenstein, R., E.F. Neuhauser and J. Collier. in press. Accumulation
of heavy metals In the ea rthworm Elsinia foetfda . .J. Environ.
Qual.
Helmke, P.A., W.P. Robarge. R.L. Koroter, and P.1. Schomberg. 1979.
Effects of soil-applied sewage sludge on concentr . t1ons of
elements in earthworms. J. Environ. Qual. 8:322—327.
3.5.5
-------
Ireland, M.P. and CS. Richards. 1977. The occurrence of heavy metals
and glycogen in the earthworms Lumbricus rubellus and Dendrobaena
rubida from a heavy metal site. Histochc.mlstry 51:153-166.
Ireland, M.P. and R.J. Wooton. 1976. Vartations in the lead, zinc and
calcium content of Dendrobaena rubida (Oliriochaeta) in a base
mining area. Environ. Pollut. lO:20’—208.
Koirtyohann, S.R., 6. Wallace and E. Hinderberger. 1976. Multi-element
analysis of Drosophila for environmental monitoring purposes
using carbon furnace atomic absorption. ran. 3. Spectrosc.
21:61-64.
Oak Ridge Natioiial Laboratory. 1974. Enviror,mental monitoring of toxic
materials in ecosystems. p. 95-139 in Ecology and analyses of
trace contaminants. Progress Report .January 1973, eptenber 1973,
ORNL-NSF—EATC-6.
Van Hook, R.I. 1974. Cadmium, lead and zinc distributions between
earthworms and soils: potentials for biological accumulation.
Bull. Environ. Contam. Toxfcol. 12:509—511.
Van Loon, J.C. and 1. Llchwa. 1973. A study of the atomic absorption
determination of some important heavy metals in fertilizers and
domestic sewage plant sludges. Environ. Lett. 4:1-8.
Van Rhee, J.A. 1977. Effects of soil pollution On earthworms.
Pedobiologia 17:201-208.
QUESTIONS and COMMENTS
. GORNY : May you explain why the earthworms axe Living
in good condition and high density in such environments as
grasses near to roads, fields treated with slurry, where there
is a great deal of heavy vttetals?
. CARTER : Earthworms living near busy highways and in
other polluted environments may suffer sub—lethal effects of
heavy metal poisoning. In our study, the levelling off of Cd
levels in earthworm tissue without a concomitant increase in
faeca]. levels may have been due to the high Cd levels in the
soil having toxic effects. Thus, these high levels could have
slowed down the feeding and excretory activities of the worms.
P. BERTEET : Do you have any information concerning the
localization of the cadmium in the worm’s body? What are the
physiological iMplications of cadmium accumulation?
A. CARTER : Cadmium (unlike lead) has not been found to
be localtzed in earthworm tissue. Most of the work on the
physiological effects of Cd accumulation has been done with
556
-------
mammals. Cadmium may have marked effects on copper and, o
a lesser extent, on zinc metabolism. Antagonism of the former
metal by Cd could have a secondary effect on haemoglobin bio-
synthesis.
C.A. EDWARDS : Did you do any studies of excretion of
heavy metals from earthworms in clear soil?
A. CARTER : No.
3.57
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iNFLUENCE OF TRAMPLING OF A HORSE MANADE IN
CAMARGUE ON THE SOIL FAUNA AND THE FAUNA OF
CANOPY
Nicole Poinsot-Balaguer and L. Boigot
Cenirt £c.e.iI,f ique .fr Snint-jIr#nic
Fra,ice
INTRODUcTION
The trampling impact of a manade (a group of half-wild horses) was the
subject of this research. This herd was composed of seven mares from four
different breedings, yearlings and a stallion (during the period of reproduction).
The manade roamed over a 120 ha area in Camarque, which was dominated vegatvely
by Sallcornjctum frutlcosae . The authors while studying the feeding behavior
of these breeding horses oT Carmarque, observed that they graze mainly on the
salt and reed marshes and in the Saticornia fruticosa formations. Our research,
therefore, was concentrated on the latter habitat type In which two experimental
areas were established.
METHODS
Two squar quadrats (24 x 24 m) were delimited within the homogenous area
of the Salicornia fruticosa association (known also as Sansouire). Samples of the
pedofauna(olig chaetes and arthropods) and a canopy fauna were collected monthly
from the four smaller squares (each 4 m on a side) each within a grazed and a test
(control) quadrat. The fauna were represented by a few cosmopolitan sp cies.
RESULT S
Comparative Community Structures
When specific diversity, max1m 31 diversity and equitibiuity of collembolan
communities between the experimental sites were compared only a small difference
In equitability was noted, however, it was non-significant (Table 1). Likewise,
a comparison of these same animal global communit es using Spearman rank correlation
coefficients shows no significant difference in the communities. When the community
structure for two periods were considered, the first sampling period and the last,
we observed a change in equitability (Table 2).
Table 1: COMPARATIVE GLOBAL COMMUNITY STRUCTURE OF COLLEMBOLA AS
AFFECTED BY TRAMPLING OF A !IANADE
Con nunity Quantification
Grazed
Site
Test Site
Specific diversity
H
3.32 (Log Q — 2qi — log qi).
2.56
bits
2.49
bits
Maximal diversity
H
max
3.45
bits
3.45
bits
H
Equitabi1it
Wmax
x 100. .. .....
73.99
%
71.96
%
358
-------
Table 2: COMPARATIVE GLOBAL COMMUNITY STRUCTURE OF PEDOFAUNA (EXCEPT
COLLEMBOLA) AS AFFECTED BY TRAMPLING B? A MAMADE OVER TIME.
Community
Quantificati
Grazed
Site
Test
Site
First
Sampling
Last
Sampling
First
Sampling
Last
Sampling
Period
Period -
Period
Period
H max
3.45
2.50
3.45
2.80
Equitability
(%)
79.36
69.64
69.64
34.93
The decrease of equitability on the test site shows an increase of the heterogeneity
of partitioning of individuals belonging to a s1 gle or a few species; the contrary
occurb-ed In the grazed station.
Conc rning the pedofauna in general (except for the Collembola cited in
Table 1) the values of equitability show the following: 1) the faunal coripositlon
of grazed and non-grazed sansouire is not significantly different considered
annually, 2) the faunistic composition is not signiticant y different in the
first series of samples but differs significantly among the last samples. We can
then consider that by the end of a year there was a modification of pedofauna.
Concerning canopy fauna, composition and structure were not significantly
different.
Multivariate Analysis of Abundance
Multivariato analysis techniques wore applied to the numerical abu.idance
coefficients (Figure 1). At the microfaunal level (Collembola and Acarina),
factor 1 neatly differentiates between the test and the grazed area (61% of the
total inertia). The test area is positive, while the grazed area is negative.
Factor 2 (28% of total inertia) divided Collembola from the acarines. The
colleinbolan communities of the test area (Tclb) and those of the grazed site
(sclb) are positive, whereas the mite communities of the test area (Tacr) and
those of the grazed site (Sacr) were negative. Furthermore, factor 3 confirms
factor 2. It always opposes Tclb and Tacr, and Scib and Sacr, but with a
re ersai In relation to the first result. Factor 3 Is more specific to the
Collembola and opposes them more than it does the mites. This seems to Indicate
that Collembola have a different r,actlon than the one of the acarines to the
introduction of the manade. On the contrary, there Is little difference between
Tacr and Sacr, concerning this factor.
The same analyses were applied to the canopy communities and the results
conf rim those above. No noticable differences appear between communities of the
pedofauna of the test sansoulre and grazed sansouire that permits a measure that
can be related to the visable impact of the manade. On the other hand, canopy
fauna had a similar structure and their dynamics only differed slightly In each
blotope.
Finally, the pedofauna other than Collembola aid Acarina manifests here
again certain uniqueness; the distribution on factors 1 and 3 showed that in the
grazed sansouire was individually scattered away from the common nucleus of the
3.59
-------
species. ror example, two sets were very distinct, the first formed by oligocheates
and Imature thomasids. and the second formed by an unknown spider and carabid
larvae and the Coccidae. The scattertha of these two aggregates in the grazed
s n: iire was _aused by the frequentation of the manade.
Biomasses in this study were expressed uniformly as animal biomass/
vegetal bloniass unit/monthly sample (each sample corresponding to six sample
units). Variation in this bianass was negligible except fur a decrease in the
g1 azed sansouire during January and February and also in April and August.
DISCUSS ION
Concerning the fauna and mainly the microfauna, the few studies that have
been made regarding influence of trampling all point out a decrease of the number
of representatives. In our study, we can only note a range oi composition of
pedofauna other than microfauna. In the reaction of tnose mlcrofauna, particularly
of the Collembola responding to the introduction of the manade, those insects
were the first to react to the effects of trampling.
AzZ Ad
•1
Ildbt
__1
e
9
— _________________
S
A ll
FXGURE I — Multivariate analysis — Dis$ributipfl (in
bimodal) of oollembol.a and mites in test sansouire and in
grazed sansouire.
360
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SESSION V: INFLUENCE OF MINING SITE
MODIFICATION AND REHABILITATION ON
SOIL ORGANISMS
Moderator: Dennis Parkinson
University of Calgary
Alberta, Canada
361
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RESTORATION OF FUNGAL ACTIVITY IN TAILING SAND
(OIL SANDS)
D. Parkinson, S. Visser, R. M. Danielson and J. Zak
Unsvr dy of Calgary
Cai ,ada
INTRODUCTION
The Atbabasca Oil Sands Deposit (c. 88% of the known Oil Sands In
Alberta, Canada) contains more than 600 x 10’ barrels 3f bitumen re-
serves. Cociseqwnt ly thia area is subject to considerable natural
resource development, with two major extraction plants currently in
operation and several more In the planning phase.
In the two existing plants surface mining, involving etripping of
vegetation and layers of clay, sand, gravel and boulders (up to 150 feet
in thickness), is used to expose and remove .he I itumen bearing sand.
The exrractiou process involves the use of bet water, steam and caustic
soda, and produces, as well as the desired bitumen, large volumes of an
alkaline aqueous suspension cf clays atc. and large amounts of sand.
The aqueous suspension is stored In large tailings ponds which are
dyked using the spent sand. It can be readily appzecia ed that this
method of “waste disposal” creates severe problems for restoration of
the land, and, consequently, in 1975 a compr±ensive environmental re-
search program was Initiated to evaluate a range of aspects (air, land
and water plus social impacts) of this industrial operation.
Until recently the major efforts in reclamation of the tailing
sand centred round studies on plant species considered suitable f ,r
revegetation and on the effects of different types of surface amendment
on survival and subsequent success of the chosen plant species.
Since it is abundantly clea that soil organisms piay a vital role
in organic matter decomposition and nutrient cycling, in 1977 a research
progrnra began to study the effects of different surfece amendments on
the restoration of biologic 1 activity in hi h1y disturbed soils. This
present contribution presents data obtained In this program on the ini-
tial (1—2 year) effects of different surface amendments on the redevelup—
ment of biological activity In tai1in , sand from the Oil Sands.
EXPERIMENTAL PLAN
Large amounts of tailing sand were transported to Calgary and placed
in a soil tank (54 x 10 in) to a depth of 1 in. The tank was constructed
with Internal dividing walls to allow three replicates of each of four
different surface treatments. Pour test plant species were chosen for
growth in the tailing sand following application of the surface amendments.
362
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Details on the amendments used and the plant species chosen are given.
in Table 1.
TI 1 BLE 1. Summary of amendments applied and plant species grown on
tailing sand.
a. Plant species:
1. Pinua bwzlcsicma Lamb. (jack pine)
2. A1’otOataphyZOa uua—urai (L.) Spreng. (bearberry)
3. Agropyron trachycauiwn (Link) Malte (slender wheat)
4. Onob ’ychia cornicuiatua L. (sainfoin)
b. Amendments:
1 • No amendment (control.)
2. Fertilizer at level equivalent to 113.7 kg N, 113.7 kg
P 2 0 5 and 91.0 ‘ g lC O ha 1 1
3. Sewage 1udge at level equivalent to 46 metric tons ha
rototilled after application
4. Peat, applied to a uniform depth of 14 cm and rototilled
Planting of test plant species was accomplished linmed Lately follow-
ing am ndment application ia June 1977 Since then numerous soil bio-
logical parameters have been monitored on a regular basis in each amend-
ment regime. These parameters include fungal cosmunity structure and
standing crop, actinomycete and bacterial numbers, total microbial bin—
mass, decomposition rates of standard substrates, N 2 fixation (symbiotic)
and rates of mycorrb al development (ecto- and VA).
In the present contribution data on fungal development In tailing
sand as affected by surface amendaticn will be presented, this will
include basic data on mycorrhiza . development in. two of the test plant
species (i.e. jack pine and slender wheat).
G ERAL SOIL FUNGI
Qualitative studies on the fungi present In. the tailing sand fol-
lowing each type of atn ”duieut were made two weeks after ametdment appli-
cations in 1.977 (i.e. prior to any plant growth) and 15 montvts follow-
ing these applications i.e. in 1978 after two plant growing t aasons. At
each sampling time replicate soil samples were taken from the 0—5 cm
depth of each type of amended sand; however, at the second sampling time
soil samples were taken. only from plots on which slender wheat was
growing.
Isolation of fungi was accomplished using a soil washing method
(Bissett and Widden, 1972). Washed soil particles ware plated unto 2%
malt extract agar ntaining aureomycin and streptoinycin. The plates
363
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were Incubated at 13°C, and fungal colonies developing on the isolation
plates were sub—cultured and held for identification.
TABLE 2. Sii w ry of fungi most frequently isolated from each type of
air ended tailing sand (0-5 c m depth) in June 1977 and
September 1978. (Pl8ures represent 2 frequency of occurrence)
Fungi isolated Control Fertilizer Sewage Peat
1977 1978 l9 7 1978 1977 1978 1977 1978
Acrwi niwn
etrtctum C 0.8 0 0 0 25.0 0 0
Aura obasidi wit
boUeyi 0 6.7 0 4.2 0 25.0 0 15.0
Ch3’yeoaporiwn
p inoz’um 0 0.8 0 0.8 0 3.3 15.0 5.0
C1zi jeoapor wn
i’e,’ ’uooswn 0 0.8 0 0.8 0 3.3 5.8 8.3
CT.adoapor wn
oiadcepor oides 0 1.7 0 6,7 21.7 2.5 4.2
Cladoaperiw’n
ha,tbaiswn 5.8 3.3 0 1.7 0.8 0.8 2.5 3.3
Fucariwn app. 0 0 0 1.7 0.8 16.7 2.5 5.8
NortiereUa app. 0 1.7 0 0 0 4.2 7.5 5.0
Mucor
hierrezZie 0 0 0 0 3 36.7 0 0.8
O idi ode nth n
eohinuiatwz 0 0 0 0 0 0 10.0 0.8
PoniciUiw’n app. 0.8 1.7 0 0 0.8 0 11.7 4.2
Phiaiophora app. 0 0 • 8 0 10.8 0 0 10.0 2 • 5
Phoma app. 0 0 0 1.7 0 18.3 4.2 4.2
Ti hod
hasrab a 0 0 0 0 0 0 11.7 5.8
2 ichode2 ’n
harzianwn 0 0 0 0 0 0 5.0 3.3
2 chod
poZyaporwn 0 0 0 0 0 0 14.2 7.5
Tr hodemna
vii’ide 0 0 0 0 0 0.8 6.7 0.8
Sterile dark
forms 1.7 13.3 0.8 15.0 0 1.7 5.0 5.8
Yeasts 6.7 18.3 4.2 25.0 0.8 27.5 0.8 5.8
Table 2 — . izea the ieolatisn data obtained at the two sempling
times • From these data it can be seen that in 1977, shortly after a ’end--
went application, a small number of fting 1 taxa of low frequency of occur -
rence were isolated from all types of amended sand with the exception of
the peat amendment.
-------
Given the rates of amendment application, it is obvious that fungi
present in the amendments would form a potentially major ‘inoculum’
source to the tailing sand. With respect to the peat used as an amend-
ment, the most frequently encountered fungi were Chryeoaporiwn app.,
Morttei ’eiZa app., PeniciU iwn app., Sterile hyaline forms, Tri&iodeiraa
spp. and Yeasts. It can be seen (Table 2) that tiaeae fungi, with the
ezception of Sterile hyaline forms and Yeasts, formed the majority of
the fungal isolates from peat amended sand at the two week sampling time.
Such a phenomenon was not seen in the sewage amended plots. The
sewage sludge, prior to application, contained a significant fungal corn—
munity with the most frequently isolated taxa being Chr’yeoapor wn spp.,
Penioiiiizmz app., Sterile hyaline forms, and Yeasts. However the iso-
lation data from sewage amended sand at the two week phase yielded very
few isolates. This could be a result of the method of application of
the n”. ’idmeat, in which the sewage sludge (initially containing c. 85%
moisture) was spcead, allowed to dry on the surface of the sand, and
then rototilled into the upper layer of the sand.
Comparison of isolation data obtained in 1977 and 1978 indicates
that the diversity of fungi isolated after two growing seasons (i.e. In
1978) had Increased in the control sand and in the fertilizer and sewage
amended sand • The sewage amendment had the greatest effects In increa-
sing the diversity of fungal taxa. Presumably these effects were direct
(because of the input of organic and inorganic nutrients in the sewage)
and it.direct (because of the stimulatory influence of sewage on test
plant growth, and the subsequent enhanced Input of nutrients by the
plants).
In the peat amended sand the nimber of species isolated bad tot
changed in 1978 as compared with the 1977 data. The most frequently iso-
lated caxa also remained much the same (although In most cases appearing
with somewhat decreased frequency), however Auroobaaidiwn boZ.Zeyi was
isolated regularly for the first time In 1978.
Data on fungi Introduced to the sand via the amendments have been
mentioned eixlier, however other Inoculum input could come from both the
aix spora and from the seed (or other plant material) planted in the
sand • In the case of the present study air spora analysis indicated
that CZadoapori n cio4o8por1oid88 C. herbai’wn, Epicooczun pza’pureeaene
and white Yeasts werc the major species present. Studies of fungi pre-
sent on the seed coat of slender wheat showed Penicillium app., A icoc-
own pu cen’j 1 richo hecium roaeum, Alter’aaria alternata., and the
L’thriniwn state of Apioapora nvr tagnei to be the most frequently iso-
lated species. Considering these data in the light of data given In
Table 2 it must be concluded that fungi introduced into the sand via the
planted seed played little, if any, part In recolonization of the vari-
ously amended tailing sand.
Quantitative cata on amounts of fungal hyphae in each type of
amended tailIng sand were obtained from €eplicate samples of each type
of amended tailing sand usIng a modified Jones and Mollison (1948)
36.5
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method. Also, total micro .ial bioiuass assessments vere made using the
Anderson and Domach (1978) mbthod • Data obtained for samples taken in
1977 by the use of these methods are given in Table 3.
TABLE 3. Fungal hyphal lengths and total microbial biomass i.. 0—5 cm
sampl.es of each type of amended tailing wind taken in 1977.
Type of Total hyphal Length of hypbae Total microbial
amendment length with cell contents biomass 1
Cm g dwt ) (m g dwt’) (ag C.lOO g dwt )
Control 102.2 80.9
Fertilizer 29.9 15.3 1.6I
Sewage 73.4 52.5
Peat £234.5 246.3
(Values superscripted differently differ significantly
p 0.05)
The direct observation data on hyphal lengths indicated a higher
amount of fungal hyphae in the initial samples from the control Cnn-
amended) sand than might be expected given the poor nutrient and organic
status of that substratum. Another interesting feature of these data is
the high percentage of observed hyphae which contained cell contents.
From both fungal and total microbial biomass data it is clear that the
fertilizer amendation yielded a significant depression of microbial de-
velopment in the tailing sand in the period immediately following amend—
ation.
The quantitative data substantiate the qualitative data discussed
earlier in that, in the initial period following amendation, it was only
in peat amended sand that substantial f.ingal development occurred. In
all other amendations fungi were sparse both in terms of species di-
versity and in terms of amounts of inycelium.
MYCORREIZAL ASSOCIATIONS
Endomycorrhizal development was studied in the root systems of
slender wheat in the first growing season (1977). Root samples were
taken at ten weeks after emergence. At this sampling time three repli-
cate samples, each of fLve intact plants, were taken from each c.f the
four types of amended teLling sand. In the laboratory, the roots were
thoroughly tap—water washed on a 2 mm sieve to remove adhering soil.
Then the root systems were cut into 1 cm pieces and stained using the
procedure described by Phillips and Hayman (1970).
366
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a--. -- .—• -w
Mycorrhizal Infection of the roots was quantified using the line
intersect method (Olson, 1950). Pour types of observation were made:
length per plant with arbusculea unly, length per plant with arbuscules
and vesicles, length per plant with bypbae only, and, length per plant
uninfected. The data obtained are given in Table 4.
TA3LE 4. Effect of amnendat ion of tailing sand on endomycorrhizal
development of slende’ wheat after o .a growing season.
Root length (cm) Iplant
Percent
Amendment Total Infected Hyphae Arbuecules Vesicles Infection
Control 63 a 1 0 1
P2at 164 ab 37 30 5 2 23
Fertilizer 543 c 0 0 0 0 0
sewage 3231 0 0 0
(For total root length, values superscripted differently, differ
at p — 0.05)
The data show that endomycorrhizal Infection was highest in peat
amended sand, it was detected at only a very low level in control sand,
and was absent in plants grown in fertilizer and sewage amended sand.
The higher rate of endomycorrhizal infection in plants from the pent
amended sand is, presumably, the result of the presence of inoculum of
suitable mycorrhizal fungi in the peat app ied as a surface amendment.
The application of surf ac7 amendments containing substantial endomycor-
rhizal inoculmmi may be necessary for sustained (long term) plant devel-
opment in locations of severe soil disturbance. Even after 2 growing
seasons (detailed data not given here), endomycorrhizal infection was
not detccted in plants grown in sewage amended sand, whilst plants from
tinmnended (control) sand and fertilizer amended sand did ohow light
infection.
Factors such as soil structure, nutrient concentrations, organic
matter content and soil temperature may i .ay roles in effectively re-
stricting mycorrhizal development in slender wheat plants grovn in
control, fertilizer and sewage amended oand. The possibility that com-
ponents of the general root surface uiycoflora may be either inhibiting
development of rycorrhizal fungi, or may be competing effectively with
these fungi a the root surface under certain amendment regimes, caP t
be overlooked. Certainly the root surface mycof lore of sl der wheat
plants after 10 weeks growth in each type of amended sand showed con-
siderable differences; these are srnmi arized in Table 5.
367
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TA3LE 5. Most frequently isolated fungi from the root surface of
slender wheat plants grown In each type of amended tailing
sand.
a. Most frequently isolated taxa:
Control Fertilizer Peat
Aiternarta Epicoccwn Acremcnizan C zFIJ8oaporizun
E eariwn !ea ts CZadoapcriwn C’yUndrocarpon
Sterile brown ftichodsi,na
forms Csotrichwn Sterile dark
forms
b. Z root segments yielding no fungi:
Control Fertilizer Peat
24 44 23 29
Ectomycorrhizal development was studied in jack pine root systams
in the 1977 and 1978 growing seasons. Container grown jack pine seed-
lings were planted in each type of amended sand, and at the end of each
growing season replicate intact plants were sampled and the roots which
had grown out from the original planting ‘plug’ were examined under the
dissecting microscope and each short root was rated as infected or not.
Frequent, detailed, microscopic examinations using squash preparations
or sections were necessary to make accurate ratings. Data on Z mycor—
rhizal infection are given In Table 6.
TA LE 6. Effect of amerd&tiou of tailing sand on ectomycorrbizal
development in jack pine. (Figures Indicate Z short roots
showing mycorrhizae)
Amendment 1977 1978
Control 6.9 33.?
Fertilizer 4.6 245 a
Sewage 4.6 494 ab
Peat Z5.0 722 b
Values superscripted differently are significantly different
(p 0.05).
The 1977 data indicate that, with the exception of plants grown in
peat amended sand, the preaom.. e of nrcorrhizae was low at the end of the
368
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first growing season. It would appear that the tailing sand contained
very small, if any, mycorrhizal inoculum. Furthermore, it appears that
mycorrbiaal fungi which had developed in the containerized root ‘plug’
during greenhouse growth prior to planting out in the sand were unable
to infect roots which grew out from the ‘plug’.
In the plant samples taken at the end of the 1978 growing season
the highest level df ectcmycorrhizal. infection had, once again, occurred
in the peat amended sand. However substantial increases in infection
bad occurred in the other 3 types of amended sand. Ir.. the case of ecto—
mycorrhizal infection of jack pine sewage did not appear to have any
inhibitory off ects. Certainly different amendments appeared to affect
root growt .aid morphology. Thus, sewage amendment decreased the l x ii—
tiation of short roots, whilst, in the control sand, root weight per
unit root length was less than in other * ndments (presumably reflect—
lng the low nutrient levels In unamended sand).
Whilst the sewage amendment did not appear to inhibit ectomy cur—
rhizal development in jack pine, it is possible that other subtle
effects may attend the use of this amendment. Direct isolations of
symbionts from mycorrhizal roots of jack pine were made (both from in-
side and outside the planting ‘plug’). 2lzeiephora teri’eatria was the
domln.2nt isolate from plants in the control, fertilizer and sewage am-
ended sand, but was isolated with only 5% frequency from plants grown
in peat amended sand. Suiflus tomentosus was also i5olated in substan-
tial amounts from pl3nts grown in all, types of iiended sand except the
sewage amendment where it was completely absent (both on roots inside
and outside the planting ‘plug’). Once again it is difficult, at this
time, to explain this In terms of either ablot c or biotic factors.
The foregoing data on general soil fungi and on mycorrhizal fungi
indicate the differing and complex effects of each of the chosen surface
amendments on the development of fungi in tailing sand. Of these amend-
ments, sewage is probably the most interesting in that it allowed (over
the 15 month period described here) the development of a diverse myco—
flora yet had apparently complex effects on the development of mycor—
rhisal fungi. Other data, not nresented here, have indicated that an-
other effect of sewage aaen ’ -sent was to reduce s mbiotLc N 2 fixation in
sainfoin (as compared with the effects of other amenIIIvl its). On the
other hand, rates of cellulose decomposition in sewage amended plots
were, comparatively, very high (89% ry weight loss In 12 months as com-
pared with 0.6% in mimnendod sand, 13% in peat amended sand, and 32% lxi
ferti] izer amended sand).
In practical terms, final evaluatiut’ of the efficiency of surface
amendments in the rec’amation of disturbed will rest on their
effects in accelerating the establishment of a stabilized ecosystem.
While development of primary producers is the moat apparent criterion
for assessing such ecosystem establishment, it must not be forgotten
369
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that direct and indirect Interactions between primary producers and
decomposers do indeed play a major role in this process.
ACKNOWLEDGD(ENT
Fiaancial support for this project from the Research Secretariat,
Alberta Environment is gratefully acknowledged.
LITERATURE CITED
Anderson, 3 .P.E. and IC.H. Domsch. 1978. A physiological method for the
quantitative measurenent of microbial biomass in soils. Soil Sb]..
Biochem. 10:215—221.
Biasett, 3. and P. Widden. 1972. An automatic, multichamber soil
washing apparatus for removin.g fungal spores from soil. Can. 3.
Micro. 18:1399—3404.
Jones, P.C.T. and 3.E. Molliaon. 1948. A technique for the quantita-
tive estimation of soil micro—organisms. 3. gon. Microbiol.
2:54—69.
Olscn, F.C.W. 1950. Quantitative estimates of filamentous algae.
Trans. Am. Microsc. Soc. 69:272—279.
Phillips, J.M. and D.S. Bayman. 1970. Improved procedures for clearing
roots and staining parasitic and vesicular—arbuscular mycorrbtzal
fungi for rapid assessment of infection. Trans. Br. My:ol. Soc.
55:158-161.
370
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FUNGAL SPECIES iSOLATED FROM THE SENESCENT LEAVES
OF Neyraudi2 arundinacea GROWING ON AREAS DISTURBED BY
IRON-ORE MINING ACTIVITIES
M H. Wong and S. H. Kwan
Tl Chinese Unisers,tv of Hong Kong
h ong Kong
ABSTRACT
The preseut investigation is an attempt to study the fungal
population isolated from the senescent leaves of Neyraudia
arundinacea growing on the areas disturbed by the activities of
iron—ore mining as fungi pl y an itcportant role in the recycling
process in this man-made habitat.
Four locations were chosen for the study: the old iron—ore
dumps, the new dumps, the iron—ore tailings and an unaffected site.
Senescent leaves of N. arundinacea and the associated soil samples
were collected from the four sites for analysising the contents of
different metals (Ca, Mg, K, Na, Fe, Mn Zn, Cu and Pb). Fungi were
also isolated from the leaves using malt agar extract agar and
Czapel Dox agar.
The soil, and vegetation collected from the disturbed areas
contained a hIgher level of metals when compared with the unaffected
site. N. arundinacea growing on the affected areas had a smaller
number of fungal species and total number of colonies with exception
of those growing on the .,ld iron—ore dumps. They also supported a
different group of fungal flora when compared with those isolated
from the plants growing on the control site.
INTRODUCTION
The ei:fects of the iron—ore tailings deposited at the east
coa3t of Tolo Harbouc, an almost landlocked sea, have been reported.
The area is almost devoid of vegetation. The soil and the surround-
ing seawater contain a rather high level of various heavy metals,
e.g. Fe, Mn, Zn, Pb and Cu (Wong ct al., 1978a). Veget&tion
growing on the tailings was found to contain a rather high level of
these wetals (Wong and Tam, 1977; Kwan, 1979). Higher concentrations
of these metals were ..Uo revealed in other organisms inhabiting
the tailings, e.g. Paphia so. (clam) (Wong and Li, 1977) and
Scopimera intermedia (crab) (Wong et al., l978b).
37].
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There is an urgency to improve the delicate environment of
Tolo Harbour which is shallow and has only a narrow outlet. The
harbour has been constantly reduced ii size due to the constr.. .ction
of Plover Cove Reservoir by linking several islands, puinpicg out
the seawater and replacing it with fresh’ ater as well, as the recent
reclamation of Shatin New Town.
An ultimate solution for improving the tailings deposited on
the east coast of Tolo Harbour is to reclaim the area using &rass
species which are able to adapt to such a hazardous environment. A
large amount of rainwater would return to the atm iphere by evapor—
transpiration and the volumn of effluent water would be reduced
and hence the escape of pollutants to the sea, and the effects on
marine organisms ‘ould be mitigated.
Soil fungi have an important part in the building up and
maintenance of soil fertility. An early report has shown a
phenomena of fungal succession aecording to the different ages of
the tailing deposits (Wong et al., 1978b). The appearance of these
common soil fungi in the tailings indicates that the area is inhabit-
able and can be converted into a more fertile area.
A series of experiments has been commenced for improving the
contaminated area with the dual purposes of minimizing the pollution
problem of the surrounding areas as well as altering the unsightly
waste heaps.
This paper reported the funga]. species isolated from the
senescent leaves of N. arundinacca , one of the most dominant plant
species growing on the areas contaminated b7 the activities of
iron—ore mining. The metal contents of the vegetation and the
corresponding soil were also at alysed. A subsequent paper will
report on the decomposition rate. of the leaves and the release of
various ions during decomposition over a period of tweleve months.
DESCRIPTIONS OF THE STUDY SITES
The detailed descriptions of the surroundings of tht iron—ore
mine have been reported (Wong and Tam, 1977; Wong et al. l978a;
Kwan, 1979). Four .ampling sites were chosen for the present study.
Site 1 (Tailings) was located at the east coast of Tab Harbour,
2,6 Ian to the north west of the mine. It consisted of a sparse
vegetation cover (mainly N. arundinacea ) with the average bare
ground of a bout 85%..
Site 2 (New waSte rock dumps) was the largest terrace of the
southern waste rock dumps of the mine. N. arundinacea and
372
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other taller rasscs were abundant in this area with an average bare
ground of
Sire 3 (Old waste rock dumps) consisted of several small waste
rock dumps deposited from open-cast mining 5.5 km north west of the
mine. They were composed of mainly gravel zanging from 0.5-20 i in
diameter. N. arundinacea and some short grass species were found
growing abundantly with significnnt litter accumulation. Desmodium
sp. also had a htgh coverage.
Site 4 (Control area) was an uncontaminated area. 5 los away
from the main road leading to the mine site from the shore. It
consisted of a moderate plant cover (mainly N. arundinacea)as well
as decampcsing plant litter.
MATERIALS AND METhODS
1. Soil analysis
The surface soil samples of the fo x sampling sites wet”
collected. After being air—dried at 25—2°C, they were passei
through a 2 mesh sieve before the following analyses were
conducted:
Air—dried moisture (the weight difference before and after the
soil samples were dried at 105°C for four hours); texture
(Bouyoucos, 1951); pH (soil: water, 1:2.5 using a pH meter);
organic carbon (Walkley and Black, 1934S; water—soluble phosphorus
(Watanahe and Olsen, 1962); total nitrogen (semi-micro Kjeldahl
method; Bremner, 1960); total cation exchange capacity (Reese, l97i ,
individual excha geable cations (atomic absorption spectrophotometry
after the samples had been extracted by iN a tonium acetate) and
th total metal contents (atomic absorption spe:trophotometry after
the samples had been digested by mixed acid, HNO 3 :11C10 4 :H 2 S0 4 —10:4:1;
Allen et a]., 1974 .
2. Metal contents of senescent leaves of !. arundinacea
Senescent leaves of N. arundinace ’ were collected from the four
saLipling sites. The amount of various metals were analysed by means
of atomic absorption spectrophotometry after the samples had been
digested by mixed acid, HNO 3 :HC1O 4 :H 2 S0 4 5:0.5:1; Allen at al., 1974).
3. Fungal species isolated from the senescent leaves
The fungal flora was isolated from the senescent leaves of
N. arundinacea using malt extract agar and Czapek Dox agar after
the litter had been washed with 1% Teepol (7 changes) and then
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distilled water (8 changes). The number of colonies was estimated
and the fungal species identified.
RESULTS AND DISCUSSION
1. Soil analysis
The results of soil analysis are shown in Tables 1 and 2. Soil
samples from Site I (Tailings) were alkaline (pH 8.22), sandy
(92. ), licked total organic carbon (0.07%) and total nitrogen
(0.14%); but contained comparatively high contents of water—soluble
phosphorus (0.84 ppm), total cation exchange capacity (13.68 m.e./
100 soil) as well as total and exchangeable individual metal
ions particularly Mn, Fe, Zn, Pb and Cu.
TABLE 1 The edaphi 1 .. properties of the sampling sites (Each value
is a mean of three samples).
1
Tailings
2
New
dumps
3
Old
dumps
4
Control
Air—dried moisture %
1.3
3.8
3.0
4.7
pH
8.22
6.89
4.82
4.46
Texture: sand %
92.8
58.8
67.8
52.8
silt %
1.6
21.2
l .2
20.0
clay %
5.8
20.0
13.0
27.2
Total organic carbon %
0.07
0.28
0.18
0.96
Total nitrogen %
0.14
0.33
0.24
0.43
Water—soluble phosphorus
0.84
0.64
0.83
0.33
ppm
Total cation exchange
13.68
12.94
12.98
9.56
capacity m.e.f 100 g
Site 2 (New waste rock dumps) and Site 3 (Old waste rock
dumps) h’td comparable edaphic properties. However, Site 2 had a
higher pH value (6.89 compared with £ .82 at Site 3), less sandy
(59% compared with 68% at Site 3), and c,ntained higher levels of
total organic carbon (0.28% compared w .th 0.18%), and total nitrogen
(0.33% c’ynpared with 0.24%). However, the content of water—solu’,le
phosphorus was lower (0.64 ppm compared with 0.83 ppm). The
contents of total cat1 n exchange capacity were similar at both
sites (12.9 m.e.f 100 g 3011). These two sites also had comparable
metal contents, bc th in terms of total arid cxchan eab].e contents
although Site 2 contained higher levels of most metals except Mn
and Cu.
374
-------
TABLE 2 The metal contents of soil samples collected from+different
sites (Each value is a mean of five samp1e : mean-standard
error. a—exchangeable content, b=total content).
Site
I
Site
2
Site
3
Site
4
ppm Tailings
New
dumps
Old
dumps
Control
Na a 190.1 12.5 2.8 8.1
+ 3.9 + 0.1 + 0.3 + 0.4
b 598.6 708.4 342.3 — 208.4
± 64.5 + 71.7 ± 11.7 ± 28.2
K a 57.1 54.7 24.5 35.4
+ 1.0 + 9.4 + 0.8 + 0.5
b 1018.2 5514.3 g586.0 1678.6
± 42.7 ± 216.6 ±247.2 ± 198.8
Ca a 433.3 116.0 10.0 36,5
+ 4.0 + 45.3 + 1.2 + 1.9
b !405.4 — 727.7 — 25.7 — 42.2
±258.3 ± 181.6 ± 1.4 ± 5.2
Mg a 150.0 220.0 37.:S 58.7
+ 2.4 ÷ 67.1 + 0.8 + 0.7
b 7116.2 Th381.3 1741.7 — 74.7
±371.4 ± 158.2 ± 95.0 ± 6.2
Mn a 25.64 4.75 7.20 3.40
+ 0.9 + 0.9 + 0.4 1. 0.4
b 123.8 1216.4 1412.7 — 191.9
± 51.8 ± 231.8 ±132.8 ± 22.9
Fe a 6.67 3.50 1.40 0.40
+ 0.3 + G.4 + 0.3 + 0.2
b 12908.8 8180.3 17469.9 Th278.6
±1284.9 ±1584.6 ±1753.3 ± 426.3
Zn a 1O.1U 2.00 1.30 0.61)
+ 0.2 + 0.4 + 0.1 + 0.0
b 261.4 — 227.7 Th00.4 18.2
± 15.3 ± 12.1 ± 17.2 ± 2.9
Pb a 0.73 8.20 3.80 1.90
+ 0.6 + 2.0 + 0.7 + 0.4
b 116.5 — 93.9 103.9 — 73.6
± 2.6 ± 10.5 ± 27.2 ± “•
Cu a 3.33 1.05 1.05 0
b 12.6 48.3 115.0 1.81
± 0.3 ± 2.9 ± 10.4 ± 0.9
37.5
-------
Site 4 (Control site) was acidic with a pH of 4.46 which is
cotmaon on the surface of red—yellow podzolic soils (Fitzapotrick,
1974) as well as for the sOil in Hong Kong. It also contained
a higher portion of fine particles (sand:53%), high contents of
total organic carbon (0.96%), total n..trogen (0.43%), but lower
levels of cation exchange capacity (9.6 m.e./I00 g soti) and total
as well, as exchangeable individual netal contents, as expected.
Due to the magnesium limestone deposit of the iron ore (Davis,
1964), the contaminated areas were more alkaline and contained
higher levels of various metals dervied from the waste materials.
The higher content of water-soluble phosphorus originated fro the
parent materia 1 s of the iron-ore (Lai, 1959). The areas were
usually devoid of vegetation, lacked soil. profiles and contained
only little soil subsrrate . The present iron—ore tailings had
similar characteristics as thc’ 70 to 1. 0—year—old weathered
iron—ore spoil of West Virginia (Tryon and Maricus, 1953; Smith
et al., 1971).
2. Metal cc’ntents o senescent leaves of N. arundinacea .
The metal contents of senescent leaves of N. arundinacea used
for the isolation of fungi are listed in Table 3. However, it
must be noted that the root portions of the plants contained tiLe
highest contents of all heavy metals (Fe, Zn, Pb and Cu) except
Mn whereas the leaf portions con’ ained the highest levels of macro—
elements (Ca. Mg, Na ana K) (Kwan, 1979). It had been shown that
plants growing on waste materials concamiimted with high levels of
heavy metals tended to concentrate thesn metals in the root portions
especially the cell wall fraction (Eradshaw et al., 1965; Thrner,
1970). On the cc’ntrary, the high level of various macro—elaments
on the lea’ portions might be favourable for carrying out photo—
synthesis.
TABLE 3 The metal contents of the senesc nt 1eav s of N. arundinacea .
(Each value is a mean of 5 samples: mean—standard error).
ppm
1
Tailings
2
New dusms
3 4
Old dumps Control
Na
1161.9+327.2
154.3+ 56.2
127.0+ 20.1 1.14.6+ 32.1
K
1294.1183.3
961.0+ 80.9
493.9.i: 59.9 3471.2 641.2
Ca
3234.0693.U
5285.91 ’1211.3
2748.8 497.0 5264.0347.0
Mg
Mn
2880.4366.4
185.7 31.5
1781.4 312.2
20l.7 22.3
1178.2 411.8 855.9 36.3
90.5 14.4 76.8 11.4
Fe
869.6209.6
531.3 105.3
87.6 11.8 120.2 31.3
Zn
31.2 33.4
18.8 9.8
12.9 9.1 33.9 21.8
Pb
12.9 11.3
9.3 10.3
15.7 17.7 10.7 15.8
Cu
37.1 36.9
24.0 20.8
40.5 35.4 16.2 12.2
376
-------
However, the leaf portions also contained a rather high level of
various heavy metals especially Mn (Kwan, 1979 . It would be inte st—
ing to know if the contents of heavy metals had any effect on the
fungal flora growing on the senescent leaves of N. arundinacea , ne
of the most dominant higher plants growing on the contaminated sites.
According to Table 3, the leaves of N. ar ’. ndinacea collected
from Site 1 (Tailings) had the highest contents of Na, Mg, Fe whereas
those from Site 2 (New dumps) the highest M i ’ and Site 3 (Old duops)
the highest Cu. Those collected from the control site (Site 4) had
the highest ..cntents of K and Ca and comparatively low levels of ll
other metals. in general, the metal contents in the leaves reflected
the metal contents in the soil.
3. Pungal specis isolated from the senescent leaves.
The fungal species together with the number of colonies isolate .i
from the senescent leaves of N. arundinacea are listed in Table 4.
In general, the leaves collected from the contaminated areas had a
smaller number of fungal species and total number of colonies with
the exception of Old dumps Site 3). Furthermore. the results also
reveRled that the fungal species isolated from the leaves collected
from the contaminated areas were different from those collected
from the control site. There were thireteen fungal species (includ-
ing 1 sterile species) isolated from the contaminated areas which
could not be found in the control site. There were only six f .ngal
species (including 3 sterile species) isolated from the contro] site
which could not be found in the contaminated areas.
When comparing the three contaminated sites, the senescent
leaves of !• arundinacea collected from the tailings consisted of
the smallest number of fungal species as well as the total n r5ber
of colonies. Yus3riixn ap. was the most dominant fungal flora.
The results also indicated that both Site 2 and Site 3 had similar
fungal species, although the Old dumps (Site 3) had a higher total
number of colonies. Both sites were dominated by Fusarium sp. but
other fungal flora e.g. Phoma macrostoma, Pestaloptiopsis ap., etc.
also appeared frequently. The higher number of fungal. species and
total number of colonies of Site 3 might be due to the lower levels
of various metals especially Mn and Pe in the leaves of N. arundincea .
It has been reported that high concentrations of heavy metals
in plant litter would inhibit the C and N mtneralization, cellulose
and otarch deco ipoaition and enzyme activity of decomposers (Tyler,
1974; 1975; 1976; Liang and Tabatabai, 1977; 1978) and results in
smaller n Esber of microorganisms (Jordon and Lechevalier, 1965;
Williams et al., 1977). However, most of these studies were concerned
jith smelter and mine wastes which contained a very high level of
heavy metals, e.g. the inhibitory effects of Pb and Zn in the mine
waste and its vegetation was damonstrated by a greater accumulation
of litter and less soil humus (Williams et al., 1977). The metal
3?7
-------
TABLE 4 The fun a1 species isolated from the oe’iescent leaves of N. arundiacea .
Site
1
Site
2
Site
3
Site 4
Fungal species Tailings
New
Dumps
Old
Dumps
Control
Fusarium fusarloides (Frag.& Cif.)Booth 118 10 5 32
F. avenaceum (Fr.) Sacc. 1
F. Schwabe 8
F. eguiseti (Corda) Sacc. 1
Fusarium ap. 68 183 106 93
Phoma !g jn (Sacc.) Boeruma,Dorenbosch & van Kest 1 2 4
P. glomerat (Corda) Wo1J .env. & Ilochapf 1
P. macrostoina Mont. 9 2’) 33
Pestalotiopsia versicolor (Sp g.) Steyaert 1 2 17
P. palmarum (Cooke) Steyaert 1
Peataloptiopsis sp. 7 26
Trichoderma ap. 1 13
Acresonium sp.
Alternaria ap. L9
) laasariothea themedae Syd. 16
Curvularia lunata (Wakker) BoediJn 7
C. .! stidis (P. lienn) .J.A. Meyer 1
Sordaria humana (Fuckel) ‘1int 1 6
Nigrospora 3p. 1
Ulocladium atrum (Preuss) Sinmtons 1
Rhizopus atolonifer (Ehrenb. ex Fr.) Lind 1
Sterile ap. A 1
B 2
C 88
D 2
Total
number
of
species
8
9
12
11
Total
number
of
colonies
192
201
196
34.5
-------
contents of the soil and vegetation contaminated with the activities
of iron—ore mining in the present study were low when compared with
other reports, and a comparison could not be made as no atudy on
the isolation of fungal flora from vegetation grow ng on iron—ore
wastes could be traced.
The higlier number of funga]. species and the total number of
colonies isolated from the leaves collected from the Old dumps
(Site 3) might be due to the stimulation of fungal growth of the
slightly higher metal contents as similar phenomena has been
observed on the stimulation of root growth under a slight increase
of heavy metals (McNeilly nd Bradahaw, 1968).
There is also evidence that microbial populations of areas
contaminated by heavy metals develop an increased tolerance to
these metals (Hilton, 1967; Griff the et al., 1974; Williams et a]..,
1977). However, no conclusion could be drawn as to whether the
fungal flora isolated from the leaves from Site 1 (Tailing;) which
contained a rather high level of various heavy metals !:ere tolerant
populations. Further studies should be concentrated on the toxicity
of heavy metals on the fungi isolated from this area.
The leaves used for the isolation of fungal flora had been
washed thoroughly so as to prevent the aerial deposition f metals
on the leaf surface which wa.ld subsequently affect thc fungal
species isolated from the lea’ee. The lower number of fungal species
and total number of colonies obtained from the 1eave collected from
the two more contaminated areas: Site 1 (Tailings) and Site 2 (New
dumps) reflected that active growth of fungal hyphae penetrating the
leaves contaminated with a rather high content of heavy met ds was
partially inhibited.
ACKNOWLEDGEMENT
The authors would like to thank Dr. A. Johnston and his
associates of the Commonwealth. Mycological Institute for the
identification of fungal species.
LITE1 ATURE CITED
Allen, S.E., Grinishaw, H.M., Parkinson, 3.A. and Quarmby, C. 1974.
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plants. Pages 327—343 G.T. Goodman, R.W. Edwards and J.M.
Lambert. Ecology and the Industrial Society. Blackwell. Oxford.
379
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“ ‘•
Bremner, J.M. 1960. Determination of nitrogen in soil by the Kjeldahl
method. J. Agric. Sci. 55:1—23.
Davis. S.G. 1964. Mineraiogy of the Ma On Shan iron mine, New Terri-
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microbial rt.sietance to metal pollution. Pages 387—394 in M.J.
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Metallurgy.
Hesse, P.R. 19 1. A Textbook of Soil Chemical Analysis. John Mui ..ay.
Locdon.
Hilton, K.J. 1967. The Lower Swansea Valley Project. Longmans Green.
London.
Jordon, M.J. and Lechevalier, M.P. 1975. Effects of zinc smelter
emissions on forest soil microflora. Can. J. Microbiol. 21:
1855—1865.
Kwan, S.H. 1979. An Ecological Survey of Soil and Vegetation Contam-
inated by the Iron Ore Mining at Ma On Shan, Hong Kong. M.Phil.
Thesis. Chinean Univ. Hong Kong.
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nitrogen mineralization in soils. Environ. Pollut. 12:141—147.
Liang, C.N. and Tabatabai I’l.A. 1978. Effects of r.race elements on
nitrification of soils. 3. Environ. Qual. 7:291—293.
McNeilly, T. and Bradshaw, B. 1968. Evolutionary processes in
populations of copper tolerant grostis tenuis Sibth. Evo1:it on.
22:108—118.
Smith, R.M., Tyron, E.H. and Tynes, E.H. 1911. Soil development on
mine spoil. Bull. 604. West Virginia Univ. Agric. Expt. Stn.
West Virginia.
Tryon, E.H. and Markus, R. 1953. Development of vegetation on century—
old iron ore spoil banks. Bull. 3519. West Virgina Univ. Agric.
Expt. Stn. West Virginia.
Turner, R.G. 1970. Subcellular distribution of zinc and copper within
the roots of metal tolerant clones of Agrostis tenuis . New
Phytol. 69: 725—7 1.
Tyler, C. 1974. Heavy metal pollution and soil enzymatic activity.
P1. Soil. 41:303—311.
Tylet , G. 1975. HeaJy metal pollution and mineralization of nitrogen
in forest soils. Nature, Lond. 255:701—702.
Tyler, A. 1976. Heavy metal pollution, phosphatase activity and
mineralization of organic phosphorus in forest soils. Soil
Bid. Biochan. 8:327—332.
Walkley, A. and Black, l.A. 1934. An examination of the Degtjareff
method for determining soil organic matter and a proposed
modification of the chroinic acid titration method. Soil Sd.
37:29—38.
Watanable, P.S. and Olsen, SR. 19 2. Colorimetric detend.nation of
380
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p in water extracts of soil. Soil Sci. 93:183—188.
Williams, S.T., McNeilly, T. and Wellington, E.M.H. 1977. The
decomposition of vegetation growing on metal mine waste.
Soil Biol. Biochem. 9:271—275.
Wong, M.H. and Li, ?4.W. 1977. An ecologicsl survey of the heavy metal
contamination of the edible clam Paphia sp. on the iron—ore
tailings of Tolo Harbour, Hong Kong. HyIrobiol. 56:265—272.
Wong, M. . and Tam, T.Y. 1977. Soil and vegetation contamination by
the iron—ore tailinge. Environ. Pollut. 14:241—254.
Wong, M.H., Chan, X.C. and Choy, C.K. 1978a. The effect of the i on—
ore tailings on the coastal environmeni of Tolo Harbour, Hong
Kong. Environ. Res. 15:342—356.
Wong, M.H., Ho, S.K., Lai, K.W. and Li, M.W. 1978b. An ecological
survey of the inycoflora in the iron—ore tailings. 3. Environ.
Sci. Health. A13:33—64.
38i
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RESPONSE OF FIELD POPULATIONS OF TARDIGRADA TO
VARIOUS LEVELS OF CHRONIC LOW-LEVEL SULPHUR
DIOXIDE EXPOSURE
J. W. Leetham, T. J. McNary, J. L. Dodd and W. K. Laurenroth
Coáoraio Slal, Uiiiversily
USA
ABSTRACT
The soil populations of Tardigrada f a
northern 1n2xed-grass prairie were sasmied after
having been exposed to various chronic low levels
of sulfur dioxide. The populations of two differ-
ent sites showed substantial reduction, although
it was difficult to show the reductions were
significant, due to high variability of sample
counts. Substantial reduction in the frequency of
occurrence in the samples helped to substantiate
the popul3tion decreases. Three genera of
tardigrada have been identified from sample
material: Macrobiotus Shultze, Hexapodibius, and
Diphascon Plate.
INTRODUCTION
Along with the ever—increasing energy demands of the world,
there is an accompanying demanc for utilization of fossil fuels other
than petroleum. Foremost among the non-petroleum fossil fuels is
coal. The in-place use of large coal de’,osits in the North American
midwest for electrical power production is rapidly expanding and along
with this development is the accompanying problem of our pollutants
and the effects on the vast grassland ranges under which the coal
deposits occur. The impac of coal-fired power plant emissions on
native grasslands is currently the central subject of the U.S. Environ-
mental Protection Agency - supported Montana Coal Fired Power Plant
Project (CFPP) (Lewis et al. 1976). Attempts have been and are con-
tinuing to be made on evaluating the effects of air pollutants, espe-
cially SO 2 , on many of the component parts of the grassland system in
southeastern Hontana.
Although Vie biological effects of air pollutants, particularly
SO 2 , have received extensive attention, especially for plants, compar-
atively little attention has been directed to other segments of either
natural or agroecosystems. Detailed studies on the effect of SO 2 on
the soil and its flora and fauna are almost nonexistant. As part of
the FPP study, soil nematode populations were being censused after
having been exposed to various levels of chronic low-level SO 2 concen-
trations (detailed discussion will follow). Prom the same samples it
382
-------
was noticed that tardigrade populations appeared to be declining with
increased $02 concentrations. These findings precipitated this study.
Ti’rdigrades are small (<1.0 nmi) arthropod-liki animals generally
referred to as “water bears” because most known species are aquatic or
semiaquatic in habit. Very little is known about these animacules
even to the point that there is disagreement among the few scientists
working with them as to where they belong phylogenetically (R.ggin,
1962). Some people have given them separate phylum status while
others have included them in the arthropods. The functional or
trophic status of tardigrades is unknown, however, a few studies have
shown that fairly substantial populations do nccur in certain soil
systems (Franz, 1941, 1950; Ramazzotti, 1959). Population estimates
range as high as 300,000 m- 2 . Generally, the Tardigrades are over-
looked in soil faunal studies since most commonly used extraction
methods are inefficient in retrieviug them. Even though they ay have
a relatively minor role in soil ecosystem function when compared to
such things as neiiiatodes, their importance in ths study lies in the
fact that they may be very sensitive indicators of what the eff4’ cts of
air pollutants are on the soil ecosystem processes.
METHODS AND MATERIALS
Study area
The study area was located in southeastern Montana within the
Custer National Forest. The habitat type is classified as northern
mixed grass prairie with western wheatgrass ( Agropyron smithii Rydb.)
the dominant grass species. Two study sites were located on rolling
uplands with southwest slopes of less than 40 Soils of both sites
were derived from outwash of parent material from 2earby buttes and
ridges. Site I had a well developed grassland soil with a silty loam
texture, moderate permeability and water retention capacity; while
Site II had a silty clay loam soil with lover permeability and higher
water retention capacity.
The climate of the area is continental, semiarid, and extremely
variable. Approximately half of the average annual precipitatiou of
360 ma is received in April, Hay, and June. The average annual teraper-
ature is 7°C with an average 130-day frost-free growing season.
Grasses and forbs associated with the dominant western wheatgrass
include prairie Junegrass [ Koeleria cristata CL.) Pers.], Sandberg
bluegrass (Poa secunda Preal.), needle-and-thread grass ( Stipa comata
Trin & Rupr.), western yarrow ( Achillea millefolium L.), common
dandelion ( Taraxacum officinale Weber), and goatsbeard ( p g n
dubius Scop.).
Methods
Four plots (0.52 ha each) at Site I were exposed to controlled
levels of sulfur dioxide during the growing season for four years
(1975-1978) with four similar plots at Site II exposed for three years
383
-------
(1976-1978). Sulfur dioxide was distributed over the plots through a
network of perforated aluminum pipes located approximately 0.75 iii
above the soil surface (Lee and Lewis 1978). Concentrations within
the canopy of each plot were measured hourly with a Meloy Laboratory
sulfur analyzer (Model SA b0-2). Sulfur dioxide was applied to the
plots at a constant rate and logrithmic variations in SO 2 concentra-
tions resulted from variations in meteorological conditions, primarily
wind speed. Monthly median sulfur dioxide concentrations were ze .o
ft,r the control 1 52 pg • rn- 3 for the low, 105 pg rn- 3 for the medium,
and 183 pg • m- for the high concentration treatment. Each treatment
plot was divided into two equal replicates.
Each site was sampled once at midseason (July) in 1977 and
1978. Site I was sampled again in late 1978 (September). Samples
consisted of soil cores 5.0 cm thameter by 10.0 cm deep taken randomly
wi.thin the treated plots. Sampliig points were determined by a random
numbers table. Sample size was five per replicate (10 per treatment)
except in September 1978 when the sample size was doubled to 10 per
replicate. The tardigrades were extracted by a Baermann funnel process
which is a commonly used live or dynamic extracti3n technique. Speci-
inens were preserved in 70% ethynol and representatives were sent out
for identification.
RESULTS
Three genera of tardigrades have been identified to date from
the material oilected, although none have been identif it.- to species.
The identitied genera include Macrobiotus Schultze, Ilexapodibius , and
Diphascon Plate (=Hypsibius Ehrenberg). The Diphascon is probably
undescribed and further work with the other two genera is needed to
determine if they fit recognized species.
The mean counts for all sample dates show substantially reduced
populations in the high treatment plots and variously reduced popula-
tions in the intermediate treatments (Figures 1 and 2). As with most
field census data, high variability seriously hampered interpretation
of the results. A repeated measures analysis of variance was used to
test for significant treatment effects. The ANOVA was run on both the
raw and transformed data, the transformation being a log transforma-
tion by the formula:
Log (X+1)
The transformation was used because the variance tended to be larger
with the larger means plus the occurrence of a large number of zero
counts in the higher treatment plots.
The ANOVA results tend not to show as significant a treatment
effect as might be expected from initial evaluation of the data. For
Site I (JuLy dates in 1977 and 1978), a 3ignificant treatment effect
was_found in the raw data (P = .0545) but not in the transformed data
(P C .10). No significant treatment effect was found in either the
38
-------
a
0
x
E
C l)
w
z
SO 2 CONCENTRATION (pg• m 3 )
FIGURE 1. Mean counts of Tardigrades on two field sites in southeastern
Montana in 1977 and 1978 (a = Site I ard b = Site II).
fl 14 July 77
D8 July 78
3
b
2
0
Control 52 105 I 83
38.5
-------
SO 2 CONCENTRATION (pLg .m 3 )
FIGURE 2.
Nean counts of Tardigrades on Site I in Septenib r, 1978 in
southeastern flootana.
I0
0
x
‘4
E
w
m
z
8
Control
105 183
386
-------
raw or transformed data on Site I on September 16, 1978. The signifi-
cant treatment differences in the July dates were tween the control
and high treatment only. For Site II, a significant treatment effect
between the control and high treatment occurred for both the raw and
transformed data (P = .0313 and .0898 for raw and transformed, respec-
t vely).
The frequency of occurence of tardigrades in the samples was
calculated for all sample dates (Table 1). The results show a substan-
tial reduction in frequ ncy with increased SO 2 concentration. The
decrease was greater for Site I than for Site II, from 90% to 16.7%
for Site I as compared with 60% to 15% for Site II.
AB
LE 1
FREQUENCY OF 0
IN SAMPLES
CCURRENCE OF TARDIGRADES
.
1 reatments
Dates
Contiol
Low Medium
Site I
High
14
8
16
July
Ju1 ’
Sept.

77
78
78
80
100
90
-— 90
70 60
90 30
75 80
78.33 56.67
20
0
30
16:6;
Site II
14
8
July
July
77
78
60
60
20 30
30 20
20
10
60
25 25
15
Total
X
S.E.
78.0
8.00
57.0 44.0
13.56 11.22
16.00
5.10
CONCLUSIONS AND DISCUSSION
The occurrence of at least three spe:ies of tardigrades on the
sites ias added confusion to the interpretation of the census data
because only tota 1 . counts were made on each sample. The individuals
were not identified to species, therefore it is not known if the
reduced population sizes were the result of all species being affected
or just o ie or two. A qualitative analysis of the sample material
sent out for identification showed a majority of the specimens were
Macrobiotus .
387
-------
Although the substantially reduced tardigrade populations in
the treated plots were not easily shown to be stati t cally signifi-
cant, we are confident the reductions are real. The consistanii.ly
reduced frequency of occurrence in the samples helps to support this
conclusion. The high variability of counts among the samples from the
control and low treatment plots was undoubtedly the principal reason
for lack of good statistical confirmation. The hic h variability of
the data is not surprising since tardigrades, like nearly all organisms
probably have variously clumped distributions and the sample core size
(18.1 cm 2 surface area) was probably too sma .l to reduce or eliminate
the clumping problem.
At this writing, additional sampling of tl.9 treated plots is
being done in a continuing effort to get more concrete evidence of the
effects of SO 2 . A preliminary attempt to deti rmine the vertical
dist ribution of the tardigrades has shown they are essentially re-
stricted to the surface 1 to 2 cm of the soil profile. Based on this
knowledge, future sampling will focus on. increasing the surface area
of the soil core samples while reducing the depth so as to hopefully
reduce the variabilitj of the data.
Since the tardigrade population is appatently restricted to the
soil surface, they, as a whole, may be much more vulnerable to SO 2 and
other air pulittants than other soil faunal groups such as nematodes
and microarthropods since these occur at deeper levels of the soil
profile where any effects of SO 2 , etc., may be buffered out by the
soil. At this writing, further studies are planned to investigate our
hypothesis that for the soil SO 2 will have its major impact at or very
near the surface. Thin impact will ultimately be manifest in reduc’d
decomposition rates of litter material.
ACKNOWLEDGMENTS
We wish to thank thoLe people who gave assistance at various
times in this study including Ms. 1arilyn Canipion for statistical
analysis, Richard Nielson and Robin Cox for assistance in sample
procescing and counting, and Mr. R. 0. Schuster, University of
California at Davis for identification of reference material.
This research was supported by US/EPA Graut R805320-02-0.
LITERATURE CITED
Franz, H. 1941. Untersuchungen iZber die Bodenbiologie alpiner
Griindland und Ackerbdden. Forschungsdienst 11:355-368.
Franz, II. 1950. Etat de nos connaissances s r da microfaune du so].
Ecoiog’.e (Colloques mt. cent. natn. Rech. scient., Paris 1950),
81-92.
383
-------
Lee, J. J., and R. A. Lewis. 1978. Zonal air pollution system:
Design and performance. Pages 322-344. In: Preston, E. N., and
R. A. Lewis (Eds.). The Bioenvironinental Iwpact of a Coal-Fired
Power Plant. Third Interim Report. Colstrip, Montana.
EPA600/3-78-021. Corvallis, Oregon.
Levis, R. A., A. S. Lefohn, a u N. R. Glass. 1976. Introduction to
the Coistrip, ontana, coal-fired power plant project. Pages
1—12. In: Lewis, R. A., A. S. Lefohxi, and N. R. Glass (eds.).
The Bioenvironme tal Impact of a Coal-Fired Power Plaiit. Second
Interim Report. Coistrip, Montana. June, 1975. EPA—600/3-76-013.
Ramazzotti, G. 1959. Tardigradi in terreni prativi. Atti. Soc.
ital. Sci. nat. 98:199—210.
Riggin, G. T., Jr. 1962. Tardigrada of southwest Virginia: with the
addition of a description of a new marine species from Florida.
Va. Agric. Exp. Stn. Tech. Bull. 152. 145 9p.
QUESTIONS and COMMENTS
D. FRCXMAN : I wonder if variability in s .muner numbers
could be due to anhydrobiotics. Have you looked at or noticed
nhydxobiotic tardigrades in the top few cm?
J.W. LEETHAM ; Anhydrobiosis could possibly be responsible
for some of the variability, but of greater importance would
be the clumped distribution so cosmon to most soil organisms.
Anhydrobiosis could possibly be a factor in the differences
between suituner and fall population estimates.
B.S. AUSMUS : Why was the application made only during
the growing season? It seems soil biological effects might
be greatly affected by winter deposition?
J. . LEETHAM : Part of the reason for fumigation only
during the growing season is due to the mechanical difficulties
enâouritered in trying to run the system during the severe winter.
Also, the whole ecosystem functioning would be at its lowest
during the winter which would result in very low exposure to
functioning organisms. It is recognized that winter exposure
will be an integral part of the power plant functioning and
certain effects of the pollutants may result from accumulation
in snow cover. However, for our study we arbitrarily chose
to restrict our exposure times to the growing season only.
7. ADDISON : Since you do not fumigate your sites during
the winter, I was wondering whether by ignoring the possibility
of winter deposition of SO 2 in snow you may be missing a majoi
input of “acid rain”?
LEET M : (answered along with the response to the
questions by Berverly Ausmus).
MITCHELL : Do you know the actual cause of mortality?
389
-------
Are you monitoring the sulfur transformations in the soil?
LEETHAM : The specific cause of mortality are unknown,
but one suggestion we have put forth is that SO 2 can react
r.’ith water to form sulfuric acid and this may be happening,
at least periodically, at the soil surface and this possible
change in soil pU way be affecting the tardigrades.
We have not, £15 yet, monitored the sulfur as it enters
the soil, but plans are to pursue this as part of further
decomposition studies.
390
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THE EFFECT O AN INCREASED Ra CONTENT IN THE SOIL
ON SOIL ANIMALS
D. A. Krivolutsky
Academy of Science
USSR
The effect of baclcground radiation on soil inverte-
brates under natural conditio’is has neve: : been studied before.
OBJECTIVES AND METHODS
During two field seasons we studied the effect of an
increased radiation level caused by a natural radionuclide
radiunt—226 on soil animal complexes. The experimental plots
with an increased level of radiation of 50-4000,MRJhr were
small in area (1—2 ha). They were situated at a terrace
above a river valley with a meadow vegetation in the micidle
ta!ga subzone. A higher radiation background was caused by
the flooding of underground layer waters with an increased
Ra content. The content of_fl in the experimental plot soil
was 7.1 10 0 to 5.6 10 per gram of the annealed
sample. The soils were dern-podzolic.
Control plots were similar with respect to soil and
vegetation to the experimental, but had a normal natural
radiation background.
Hand sifting was used to study the soil population by
mesofauna at an area of 50 x 50 cm down to the level at ,hich
animals occu red (30 - 40 cm) and by microarthropods in
samples 1 dm in volume.
RESULTS AND DISCUSSION
The radiation levels at the plots under study varied
a good deal which evidently explains a great variance of
mesofauna populations from sample to sample.
Statistical treatment of material included reduction
391
-------
of the variants to normal distributior. by the formula
x = ig (x+1) • the data obtained being compared by the
Student index. Highly statistically significant differe ices
P< 0.01) were obtained for all long-developing groups
characterized by a relatively low motility, i.e. those which
are permanent residents of plots with an increased radiation
background. Such plots showed a much lower number of eart h—
worms comoared with controls, the same being true of dipteran
and click-beetle larvae. Sigrificantly lower numbers were
likewise recorded in other large invertebrates (Table 1).
Table 1: POPULATION OF MEADOW RIVER VALLEY SOILS WITH SOIL
MESOFAUNA IN CONTROL AND IN PLOTS WITH AN INCREASED
Ra CONTENT
Plot with increased
ANIMAL GROUP Control radiation level
INSECTA
Total
number
Mean 2 Total Mean
per in ;&umber per in 2
Diptera larvae
77
3.85
15
0.75
Elateridae larvae
77
3.85
13
0.65
Staphylinidae inunatures
215
10.75
164
820
Carabidae imntatu s
29
1.45
17
0.85
Total
398
19.9
209
10.45
LUNBRICIDAE
Eisenia n•rdenskjoldi
(Eisen.)
9
0.45
1
0.05
Dendrobaena octaedra
29
1.45
5
0.25
(Say.)
Octolaeium lacteum
(Oer ley)
3
0.15
0
0
Others
139
6.95
56
2.80
Total
180
9.00
62
3.10
92
-------
No statistically significant differences were found with
respect to the numbers of actively motile surface arthropods
(Staphilinidac. Carabidae, spiders end Phalangida).
The numbers of mature oribatids was 72± individuals
per dm 3 in the control against 39± 8 in the radium-polluted
plot 1 no faunistic differences being noted. No statistically
significe 1 nt differences were recorded as to the numbers of
other groups of soil mites and springtails. Thus, soil
dwellers proper, with lower motility and relatively long period
of individual development can serve as a convenient bioindi—
cators in studies of the natural radiation effect on zoocoe—
nosis.
Earthworms proved specifically sensitive to an increase
of radiation background. In fact, in mid-summer a plot wit.h
a radiation level of about lOO, .R/hr contained a 7-fold re-
duction of earthworms over the control, the experimental
earthworms also being smaller in size. Of particular interest
is the fact of a reproductive disturbance. The earthworm
population of the control contained a great number of young
individuals, these being nearly abcent in the polluted plot.
Evidently at polluted plots these young individuals are re-
tarded in growth and achievement of sex maturity compazec with
controls. In fact, in June when earthworms only start repro-
ducing, their control population was represented by only sexually—
mature individuals, and at experimental plots over half of the
population had failed to achieve sexual-maturity by that time.
The histological structure of the epithelium of integu-
ments and mid-gut (the tissues in direct contact with the Ra-
polluted soil) in animals from control and experimental plots
(with a radiation level of about 4000,ILR/hr) was investigated.
The subject of investigation was Dendrobaena octaedra (Say.)
and also Dendrodrilus rubidus (Say.). Both these species are
dwellers of the most superficial soil layers. The material
was fixed in the Bouin’s solution and prepared for histolog-
ical studies in a standard manner.
Dwellers of the superficial laysrs of soil proved to
have integuments consisting of one layer of heterogenous
epithelial cells and a cuticle consisting of a thin trans-
parent membrane. The epithelial cells include narrow cylin-
drical ones with a small nucleus and a compact plasm and
broader ones with glandular and inucousal cells filled up
39,
-------
with a mucous secretion (Semenova 1968). This mucous se-
cretion is excreted through cell pores, constantly moistening
by the worm body which protects it from drying up. There
are small cambial cells in the basal part of the epithelium.
Both earthworm species under study from the control
plots were characterized by a typical structure of the integu—
ntents (Figure l,A). The earthworms collected from the Ra—
polluted soil showed considerable chakges in the structure
of integument epithelium (shape and size of mucous cells).
The mucous cells of these earthworms are broader and larger
as compared with controls (Figure 1, B). The number of mucous
cells in the radiation-affected earthworms is much higher
than that in the control ones. There are fewer cambial cells
in these sections. The structure of the mid-gut epithelium
was also studied. The mid—gut epithelium was found to con-
sist of two of the following cell types: epithelial cells
which produce digestive enzymes and absorb digestion products,
and mucous cells that excrete mucus to moisten the food mass.
The amount of mucous and epithelial cells in the epithelial
thickness is nearly simi:iar (Semenova 1966). There are a
large number of regeneration nests and individual regenera— -
tion cells in the basal part of the epithelium. The typical
structure of the mid-gut described &?ove was found in both
species collected at control plots (Figure iB).
The earthworms collected at the experimental plot showed
changes in the structure of the mid-gut epitheliuut: epithelial
cells which produce enzymes were found in a much less number
as compared with mucous cells. The number of regeneration
nests and regeneration cells in the epithelial thickness is
Biso smaller compared with that in the control earthworms
(Figure 1 1 D).
Both species of experimental earthworms (radiation back-
ground about lOO—4000,u.R/hr) had a considerable increase of
mucous cell numbers in the epith2lium of the outer integuments
and mid—gut as well as an increased excretion of mucus which
is evidently a protective response to the action of O —
radiation.
Comparison of our data with those previously obtained
for land vertebrates dwelli ’tg at the sante plot (Maslov 1972.
Maslov and Maslov 1972) showed chat the general regularities
are similar: the greatest radiation effect is recorded in
sedative groups of long-time dwellers of plots with an in-
creased raeiation background in which disturbances in the
394
-------
Figure 1.
THE STRUCTURE OF THE INTEGUMENTS OF EARTHWORMS
(X 280). A-INTEGtJM.ENTS OF Dendrobaen , octaedi a
FROM CONTROL PLOTS; B - INTEGUMENTS OF Q. octaedra
FRCt4 PLOTS WITH HIGHER RI DIATION BACKGROUND; C -
EPITHELIUM OF MID-GUT OF Den rc4ri1ue rubidus from
CONTROL PLOTS; D - CROSS-SECTION OF MID-GUT OF
j). rubi4 FROM PLOT WITH INCREASED RADIATION
13ACKGROUND 9K. - EPITHELIAL CELLS, C K. -
MUCOUS CELLS, P - REGENERATION CELL,S
I
395
-------
eve1opment and functioning of che body surface and intestine
epithelium were noted. Along with that, the effect of an
increased radiation background for soil animals as manifest
not only at plots with high radiation levels (2C00-B000p.R/hr)
but also with a much lower level (100-200p.R/hr). This is
evidently explained by a closer contact of soil animals with
Ra-containing soil.
Earthworms are a specifically convenient subject for
studies of the effect of an increased radiation background
as these are not only irradiated from the outside but also
from the soil, they swallowed. All the rest of the land ani—
male under study so not swallow the soil and consume only
animal or vegetative food in which the radionuclide content
is considerably lower (by 1—2 orders) than in the soil.
REFEREN S CITED
Maslov, V.1. 1972. In: Radioekologicheskie issledovania v
prirodnykh biogeotsenozakh, M., “Nauka”, str. 9.
Maslov, V.1. and KI. Maslova. 1972. Ibid., str. 161.
Semenova, L.M. 1968. Zool. Zhurnal, t. 47, vyp. 2 1621.
Semenova, L.14. 1966. Ibid., t. 45, vyp 7, 986.
QUESTIONS and COMMENTS
DONS j: The data presented indicate a relatively
wLde range of aen itivity of soil animals exposed to radiation.
Are there also cases of increased populations?
4. KRIVOLUTSKY : No, we can see the decreased populations
only for all groups of soil animals.
96
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COLLEMBOLA OF REHABILITATED MINE SITES IN WESTERN
AUSTRALIA
1’enelope Greenslade and D. Majer
South A strti1,a,, Museum
S’ulh ,justrolia
‘lnslihde of Trchiiology
West A,stral,a
INTRODUCTION
Bauxite mining is an .mportant industry in Western Australia,
and takes place mainly in the ranges south east of Perth where
operations are currently being expanded. For the most part, a.’eaa
being mined oarrj native Eucalyptus forest which has never been
cleared cr grazed. The miiiing operation involves clear felling, then
burning and removal of top soil. Subsequently the ore is blasted and
heavy ma hinery used to remove it, leaving a ptt on average 2 metres
deep and at least a hectare in area. Efforts have been made to
reclaim the mined areas by landscaping, replacing top soil, ripping
the surface to enhance root penetration and revegetatirig by various
methods. Different rehabilitation regimes are being tested to
establish which is the mo st ‘successful’ in returning the mined area
closest to its original state. Con”entional botanical methods of
monitoring the dirrerent treatments are being supplemented by studies
of soil surface arthropods as they could p vide additional
information for’ assessing the different . nemes. Luff and i futaon
(1977) emphasise the benefits which origin : te from the soil fauna such
as litter breakdown, and improvement of soil aeration. They 3tress
that management of reclaimed land sho ald aim to encourage development
of’ the soil fauna. Here we describe the re—establisl’.ment of’
Collembolen populations in one set of rehabilitation trials and
compare treatment popu]ations with those ‘f undisturbed forest.
Results for ants have already been analysed (Majer in press).
SITES AND METPfODS
The experimental plots were situated in the Darling Ranges about
80 1 south of Perth at Del Park and Jarrahdale, where the predominate
vegetation is tall closed forest of Eucalyptus marginata (jarrah) with
sow’ ‘ ‘ alophylla and an uriderstory of Banksia grandis, Persoonia
. -. and Casuarina fraseriana . Three treatments were sampled:—
U, -- ‘ip .anted area where the only treatmert was replacement of top
soil and ripping; P, planted with seedlings of E. calophylla in June
1976 and spot fertilized, and S, treated as U but j ’e nted in July 1976
with a mixture of seeds and seedlings belonging to more th .n 20
species of Euca1yptu and Acacia and fertilised periodically. A
control plot, F, of undisturbed forest was chosen nearby. Plots U and
P were reclaimed with stcclcpiled topsi1 at the same time and were
adjacent to F; however the seeded plot was treated slightly
397
-------
differently with non-stockpiled topsoil, was reclaimed one month later
and lay some 20 1 north of the other plots, although on a similar
ao .1 and in similar vegetation. After two years both the U and P
plots still consisted mainly of bare ground with a plant cover area of
0% and 15% respectively. No additional plants had succeeded in
permanently colonising either plot although both were only about 200.m
from the nearest source area. By the same time a dense cover of
vegetation had developed on plot S and both planc area cover (73%) and
plant density (111%) were greater than that of the forest control C70%
and 2.6%). Some leaf litter was present on the ground surface on plot
S after two years but it appeared to be lying loosely on top of firm
textured soil; in contrast the forest soil was less compact and darker
with a higher content of organio matter and more extensive litter
layer.
Rainfall and temperature data for the area are given in figure
1. The climate is med. terranean with a hot, dry summer and cool, wet
winter. Sampling was carried out with a gr±d 15 x 15 a of 36 (6 x 6)
pitfall traps, 1.8 cm in diameter containing an alcohol/glycerol
mixture as described by Majer (1978). The traps were operated for one
week every month for the first year (June 1976 — July 1977) and
thereafter four times a year. All Collesbola trapped were counted but
they were on)y identified from a selection of 8 samples which covered
all seasons. Some disadvantages are implicit in using pitfall trap
sampling alone since catches are deper.dant on the activity as well as
the size of populations and influenced by density of surrounding
vegetation and litter; however they were considered adequate for this
survey for their convenience, speed and efficiency at collecting the
groups to be studied so long as results were analysed with care. Moat
species or Colleiabol . I.hat were collected were undescribed, but all
species were distinguished; numbered and voucher specimens are
deposited In the South Australian Museum, Adelaide, South Australia.
RESULTS
Abundance
Total numbers of Collembola trapped showed considerable
variation ‘,etween plots, and within plots between sampling occasions
(fig. 2). At least part of these differences are accounted for by
differing weather conditions on different sampling occasions. Overall
the treated plots, in particular plot S, show greater variation in
size of catch between sampling occasions than the forest control.
The following account refers only to the results from the eight
sampling times indicated on figure 2 and are s Imm rised in table 1.
Catches from plots U and P are strictly comparable because of the
physical similarity of their ground surraces. The uffect of the
denser ground vegetation and litter on plots S and F would be to
reduce antivity and hence catches so that high catches here reflect a
real increase in population density.
398
-------
FIGURE 1. Climatic data from Dwellingup near experimental plots.
A. Mean monthly maximum and minimum temperatures. B.
Mean monthly rainfall (histogram), and relative humidity.
30
U.
0
‘I
•1
E
E
30
A
F*S 7iun ku 9 ’ oct
1976
- I
Ju Au bct
1977 1978
I
Total Collembola trapped June 1976 — September 1978: A,
Forest control; B, Unpianted (U), Planted (F) and
Seeded plots (5). / — Samples from which Coflembola
were identified.
0
701
60
A
.‘ Ccflsn’boi dsnc. ssC
300
Fu
100
300
S.
p.
u0
100
1978
FIGURE 2.
1977
1978
399
-------
The total number of individuals trapped was highest on the
seeded plot (5), (figure 3°), with catches 50% greater than those in
forest. The planted and unpianted plots trapped few individuals.
Biomass was not estimated but since the majority of individuals on F
and particularly S were smaller than on U and P, biomass was more
evenly distributed between plots than is indicated by catches of
individuals.
Species Diversity
DiversIty measured by the total numbers of species identified is
highest in the forest control (F) (figure 3a) with the three treatment
plots carrying about a third as many species. On both the planted and
seeded plots (P and S) eighteen species were trapped. The differences
are more marked when species records i.e. the sum of species
occurrences are counted (figure 3b). Altogether 57 species were
recorded from the four plots (table 1).
Faunal affinities
The species composition c the four plots was compared using the
percentage similarity for each paIr of habitats:-
Number of shared species x 100
Total number of zpeoies in both habitats
TABLE 2. Percentage similarity
U—Unplanted, P—Planted, S-Seeded, F—Forest
U P S F
U 145 22 16
P 30 25
S 32
The planted (P), and unplanted (U), plots showed most similarity
to each other and the seeded plot CS) is slightly more similar to the
forest control (F) .han it is to the planted plot. As expected the
plot least similar to the forest control is that of the bare ground
(U).
Eguitabili y
From figure 3 it is clear that plot S must contain a small
number of species represented by a large number of individuals. In
order to investigate the diat.”ibution of individuals between species,
the species were grouped into octaves according to the number of
individuals by which they were represented:—
400
-------
A
300 B
1
Ii
U —
A
S S
6
0
Ji B
C
O SF C H
Octave
.1
K L N
Combined data from eight sampling occasions. A, Total
species recognised; B, Species records; C, Total
individuals. Plots: U, unpianted; P, planted; S,
seeded; F, forest.
Species grou ed into octaves (A—M) according to number
of individual.s by which they are represented. Lognormal
plot of species frequency distribution between octaves.
Plots: U, unpianted; P, planted; 3, seeded; F, forest.
I
0
5
U
&
C l ,
U,
U,
p
C
U P S F
FIGURE 3.
FIGURE 1;•
1+01
-------
TABLE 1. Number of Collembola species trapped on four
plots on 8 sampling occasions
Plots U—uplanted, P—planted, S—seeded, F—forest
&iinthur .dae U P S F
Sminthurides sp. 1 — 20O 6
Sminthurides sp. 2 59 8 J
Sminthurides ap. 3 — - —
1mm .Lndet. Sminthurides 3 18 — — —
Nr Sminthurinus sp. — 6 2 13 82
Slninthurinu.3 sp. 1 — — - 222
Sniinthurinus sp. 2 7 92 81 32
Parakatjanna sp. - — 2 5
Katianna sp. - 3 1 39
Terneritas sp. - — 1
Aneuempodja].js cinereus Worn. 1 — — 7
Rastriopes ap. - 1 5 16
Coryneohoria cassida Worn. — — 1
Corynephoria sp. — — 6
Dioyrtornidae — — 3
1mm. indet. Sminthuridae 3 87 81
Entornobryidae
Lepidocyrtoides ep. 1 — — 3 52
Lepidocyrtoldes sp. 2 — — —
Lepidocyrtoides sp. 3 — — — 1 81
Lepidooyrtoides australicus Schott — I — —
Lepidosira coerulea Schott — — — 162
Lepidobrya sp - — —
Lepidosira ep. — — — 330
1 repanorira sp. 1 — — — .1
Drepanosira ep. 2 - — — 22
Drepanura cinguelineata Worn. 1 2 61 13
Drepanura p. 2 — — II
Drepanura •3 - - — 1
a Entomobrya unostrigata Stach 82 98 — —
C Entomob ’a atrocincta Schott. 1 2 — —
Entornobrya ap. - 3 - 1
Pseudosir ella sp. 18 2 — 218
Acanthocyrtus sp. 73 80 513 113
1mm. indet. Entouobryidae 55 518 21 87
o2
-------
Table I (cont..)
Isotomidae
U P
S F
Folsomides exiguus Folsom
Folsomides sp.
‘ Proisotoma mthuta (Tulib.)
Proisotoma ripicola Linnaniemi
seris Wom.
Proisotoma sp.
* Cryptopygus thermophilus (Axel.)
C!Yptc pygUs antarcticus Willem.
* Folsainia caridida (Willem)
Acanthomurus ap.
Pro .satomurus sp.
Isotoma sp.
Isotoina sp. 2
Neanuridae
Xenyllodea ap. 1
Xeny].lodes sp. 2
ealandella ap. 1
Zealandella ap. 2
Zealandella sp. 3
Subelavontella ep. 1
Subclavontella sp. 2
Subclavontella sp. 3
Ni ’. Probrachystomella sp.
Australella ap. 1
Australella sp. 2
Pseudaohorutes ap.
1
7
- 32
— 22
— 14
— 33
7 31 14
3119
1
— 130
- +
- +
- ++
— +4
- ++
— ++÷ >ii 1•
- +4+
- +++
- +
2
— +++
2 +++
Total Species 12 18 18 149
t These species were individually counted in all samples except
that for June 1918 when the total was 1100 specimens for
all Neariuridae. + = < 10 individuals; 4+ = 31 — 100
individuals; +4- I > 101 individuals.
• Cosmopolitan species.
— 5000
415
2
1
1
3114
Oriychiuridae
* Tulibergia krausbaueri
group
—
—
I
—
Hypogastruridae
Triaoanthella sp.
1
—
3
155
1
1
1
403
-------
Octave A B C D K F 0 H I J K L H
No. of indjvjdual.s 1_2_Z4 8_l6_32_64_l28_256_512_l021_20 I8_4096_8 192
The data are plotted in figure 4. Plot F gives a truncated
normal distribution with a large number of relatively abundant
species. None of the treatment plots show a similar distrIbution
pattern since Individuals are inequitably distributed between species
with a larger proportion of rare species and some very abundant ones.
This is least obvious for plot U which baa the least diverse fauna.
Species Composition
Species collected are lisced in table 1 • & number of species
were 3n1.y found on he treatment plots and these all have cosmopolitan
distributions. Cosmopolitan species expressed as percentages of the
whole fauna on each plot were: ‘J, 17%; P, 17%; 5, 11%; F, 0.4%.
However 80% of individuals on the seeded plot wlere oosn’opolitan and
were ident Ified as Proisotoma minuta , a species common on compost
heaps and in other .iistur.bed sites In Australia where humidities are
hig’i, food is plentiful and predation p -essure is low, typical
habitats for the r selected species of Mcirthur and Wilsc,n (1961).
Proisotoma minuta is able to increase in numbers rapidly when abundant
food is present. Another cosmopolitan species, Entomobrya
unostrigata , was abundant on plots U and P. ThIs species is a
relaJ ively recent introductIon to Australia and is often found in hot
dry conditions on bare arable land nd in houses. Ent mobrya
atrocincta , although rarer on these i’Iots has the same recent history
and character stjcs in Australia.
On plot S, species associated with heath vegetaLjn such as
Rastriopes ep., Parakatianna sp. and Drepanura cinguelineata were
present in fairly high numbers. These species did not occur on plots
U and P and about half the number of individuals were trapped in the
forest compared with the seeded plot. &ninthurides app. were often
abundcnt on the treatment plots in winter where small pits formed
during ripping held puddles of water. The close similarity between
plots U and P indicate that the effect of s”edling trees on species
establishment was negligible. In fact only a single individual of a
species which lives mainly under bark or on trees Lepidoeyrtoidea
australicus , was trapped on plot P. Litter inhabiting Collenbola such
as Neanuridas, Triacanthella, Cryptopygus, Isotoma, Sininthurinu ,
Lepldoeyrtoides and Lepidosira species were present only in the
forest. Apart from those species discussed above the only species
able to colonise th mined areas and maintain their populations were
two native species: Aoanthomurus sp., a large isotc !nid, and
Acanthocyrtus sp. an entomobryid.
Seasonality
In spite of the variation between sampling occasions, figure 2
shows maximum catches in winter (May—August) and minimum in summer.
The low number for winter 1977 is an artefact due to loss through
-------
flooding of’ traps. In both 1977 and 1978, the seasonal population
increase began earlier in forest thar wine 1 areas and occurred
simultaneously with increasing relative humidity, which was a res’ lt
of falling temperatures in late March and early April. On the minec
plots the first population increase was in May and coincides with the
brc.aking rains of Autumn.
Bulked records of individuals trapped on the four plots, grouped
seasonally are ‘iven in figure 5. No Neanuridae, Nypogastruridae or
Isotomidae apart from Acanthomurus were trapped i.e. were active on
the soil surface, in summer (figure 5e). There are two groups of
Sminthuridae:- a) species mainly active in winter, and b) species
mainly active in summer. Both were present in low numbers in spring
and autumn. The Entomobryidae can also be classified into two
groups:— c) species active predominately in eummer, and d) aseasonal
species with a peak of activity in the humid conditions of autumn
before the winter fauna was abundant • Some species of Collembola were
still trapped on all plots even during extremely dry conditions in
summer when there is often no effective rain for ) 14 months and
temperatures are high.
Trends with time
Percent similarity of’ the faunas of’ treated plots and control
are compared in table 3 for the results of spring trapping in 1977 and
1978. There was no increase over the year even on plots S where gross
botanical changes had taken place.
TABLE 3. Percentage similarity of mined plots to
forest on two occasions a year apart.
U — Unpianted, P — Planted, S - Seeded, F - Forest
U P S
October 1977 F 21 18 23
September 1978 F 12 12 19
DISCUSSION
Reviews of other, mainly European work on the effects of mine
reclamation on soil animals are given by Luff and Hutson (1977) and by
Majer (In press). Three stages are involved in the development of a
fauna on a virgin landscape:- 1) immigration, 2) populatioE
establishment 3) population maintenance. The first stage, requires
species with dispersal ability. At least a third of’ the litter
inhabiting species which occurred in forest were also found on the
mined sites although frequently only single specimens were trapped.
Hance dispersal does not seem to be a major obstacle to faunal
development. For the second stage to be successful i.e. establishment
of a population, food and appropriate habitat and shelter must be
405
-------
E
Spur Su
D
i i
FIGURE 5. Seasonal ooourrence of s ,cies. Spr — Spring (September
— November); Su - Sunmier, (December - February); Au —
Autumn, (March — May); V — Winter, (June — August). A.
iinthuridae Katiannini, Sminthuridinae, Temeritas sp.
Total species 12. B. Sminthuridae Corynephor’ia ,p. 2
app • C. Entomobryida Drepariura app. Drepanosira ap.
Entomobr app. Total 3 app. D. Entoniobryidae
Acanthocyptus sp. Lepido ira app. L $docyrtoi ’s app.
Lepldobrya sp . Total 8 app. E. Isotoinidae anti
Neanuridae. ‘!‘otal 25 app.
A
10
5
0
A
100
100
0
(0
3
C
C
0
o6
-------
available. This was not the case on the unpianted (U) and planted (P)
plots and they did not support populations of coon litter species.
Although a litter layer was present on the seeded plot these litter
species also tailed to establish here. For the third stage, i.e.
maintenance of population, the population which has established must
be able to survive seasonal and short term varIation in the
environment. There was a relatively greater drop in number of species
active in summer on mined olots (U and P) (10% active) compared to
forest (F) (25$). This applied also on plot S with its dense shrub
vegetation. It seems that the high temperatures and low humidities in
leaf litter in summer do not permit many species to survive there.
Our results indicate that the Collembolan faunas of seeded,
planted and unpian ted plots were all markedly different from the
fore3t fa.zna after two years reclamatioi, even though the seeded plot,
because of the vegetation it rr, might be rated botanically
‘successful’. The major group t Collembola missing from all these
mined plots is the winter active species inhabiting litter. This
includes all the Neanuridae as well as some species of Isotomidae and
& inthuridae. In the forest, the autumn population increase in total
Collenbolan cat hes occurs more than a month before the increase on
the mined plots. It appears that an inactive population exists
throughout the sumsier in forest wbich becomes active again as relative
tn.midlties increase in early autumn. On the mined plots, no increase
catches occurs before the breaking rains. We suggest that on the
wined sites poor soil structure and low soil organic matter content
limit the availability of refuges from harsh summer conditions. Even
on plot S this seems to retard the development of a bal&riced
Coflemoolan fauna.
These results for Collembola are similar to those recorded for
ants (Majer in press), although the aiveraity of ants on plot S was
relatively higher compared to the other plots than it was for
Collembola. This probably results from the ability of many ant
species to exoavate their own refuges even in poorly structured soil.
From the point of view of the vegetation, recl nation of mined
areas by seeding appears to be most effective. However, development
of vegetation cover and litter layer is not all that is needed for
the recovery of the Colleinbolan fauna • Over the two year time scale
of these observations, some heath species of Collembola reinvaded the
seeded plot but none of the winter active litter inhabiting species
typical of forest became re—established. These are the species most
likely to contribute to decomposition and cycling of’ nutrients. We
have suggested that soil structure may limit their occurrence. Future
research could be directed towards examining this suggestion.
ACKNOWLEOGEMENTS
‘i . ’*s are due to Alcoa Ltd f r providing faoilties for research
and to B. Hutson and P.J.M. G:eenslade for critically reading the
manuscript.
£ 107
-------
This work was carried out while the senior author was in receipt
of a Australian B .ologioal Resources Grant, and field work was
supported by the Rural Credits Development Fund.
LITERLTURE CITED
Luff, M.L. and Hutson, B.R. (1977). Soil fauna populations.
B. Hackett. Land Reolamdtion Practice. I.P.C. Business Press
LtG., Guilaford.
NOA ,lthur, R.H. and Wilson, E.O. (1967). The theory of island
biogeography. Princeton University Press, Princeton, N.J.
Majer, J.D. (1978). An improved pitfall trap for sampling ants ‘tnd
other epi aeio invertebrates. J. Aust. Ent. Soc. 17, 261- .62.
Majer, J.D. (in press). Role of irwertebrates in bauxite mine
rehabilitation. Forests Depert ent Western Australian Builetin.
QUESTIONS and COMMENTS
LS. GHILAROVs Have you tried inocu1a ing the mined sites
with litter from the forest, to stimulate iievelo ant of the fauna?
. GRE!aIsL s I4ot yet, but that techniq ua would. be interesting
to try at some point in the research pro razma.
408
-------
EARTHWORMS ON FORESTED SPOIL BANKS
William E. Hamilton and J. P. Vimrnerstedt
Ohio Agricsdti re Re sarrh iid Dtvelopmrnl CrnIe,
USA
Pre enI Addr,ss
SIJNY CESF
US A
INTRODUCTION
Lands disturbed by surface mining are only slowly colonized by
the larger saprophytic invertebrates (tseumann, 1973). Without these
animals litter decomposition is alow (Edwards and Heath, 1963), and
thfrk litter mats acc m ulate on the soil surface. Earthworms ( Luinbri —
cus terrestris , L.) can be introduced on strlpmined spoil banks and
help to increase the rate of litter decomposition (Vierstedt and
Pinney, 1973; Hamilton. 19Th).
This is a report on the status and activity of an introduced
population of L. terrestria on forested mine spoils Lu southeastern Ohio.
One acre plantings of Alniia glutinosa and Robinia pseudoacacia were es-
tablished in 1962 on spoil material rich in limestone and near neutral
in reaction (Table 1). In Nay, 1967, 10 sexually mature L. terrestris
were released in the appro { ate center of each plantation.
Table 1. SITE DESCRIPTION OF TWO FORESTED SPOIL BANKS
Site
Soil
pH
mg NH 4 —Nf 100
g Soil

Depth
A—Horizon
(cm)
Basal Area
m 2 /Hectare
g Woody
Leaves
per m 2 21
5 herbace—
ous lea es
per m
Alnus
7.73
0.229 0.175
4. 2
13.8
(A].nus)
0.69
(other)
129 ±
23.97
16.16 ±
9.84
Robinie
8.22
0.258 0.207
5.25
11.9
(Robinia)
0.1
(Ot h r
89.2 ±
6.83
26.08 ±
2.73
and herbaceous leaf weights are fresh fallen leaves collected
during October and November.
Work supported by McIntir —Stenn 4 s funds.
-------
METHODS
In October, 1978 earthworms were sampled by chemical extraction
with dilute formalin solutions applied to 32 0.25 m 2 plots (Raw, 1959).
Each sample plot was twice extracted on consecutive days. Prior to ex-
traction surface litter of each plot was carefully collected, oven—
dried (at 80° C for 24 hours), and weighed.
Within 1 m of each extracted plot a second 0.25 2 plt was also
cleared and the litter oven—dried and weighed.
Weekly collections of the fallen litter were made through October
and November from plots which had been treated with formalin. Fallen
litter on cleared unextracted plots was not disturbed. In March, 1979
both extracted and unextracted plots were cleared, and litter was oven—
dried and weighed. Weight of leaf litter collected from plots devoid
of worms represented 100Z of litter fall for each plot pair. Weight of
leaf litter collected from unextracted plots represented weight of leaves
not acted on by worms. Initial clearing of plot pairs showed that the
weights of leaf litter on each member of the pair were not significantly
different.
Decomposition studies were conducted using a series of 1 gallon,
glass, screw—top jars into which a uniform quantity of spoil (1.2 kg),
leaves (3.85 g), and water (1/3 bar moisture, 26.7% HOE) were added. In
some jars two active L. terrestris adults (combined weights from 7.5 to
9.1 g) were added. Leaf species were varied ( . oaa and A.psendo-
acacia) , and, in some jars, spoil and leaves were autoclaved (at 2400 C
for 2 hours). The autoclaving procedure was expected to reduce microb—
lel numbers and open micro—niches, but not to completely sterilize the
system. Table 2 indicates the 8 treatments.
Carbon dioxide evolution from l: .tter and spoil was measured at
24 hour intervals. Titrations of an a -a1ine C02 absorbent (0.8 N
NaOH) with 0.8 N NC following saturation with BaC12 determined 1flgCO .C
evolved. Large jars and daily aerations insured the maintenance of
aerobic conditions within the containers.
After 3 weeks of incubation at 160 C in the dark, spoil material
was removed from the jars and 100 g sub—samples were treated iith selec-
tive inhibitors (cycloheximide, 150 mg; atreptomycin sulfate, 150 ing)
and a carbon—eu rgy source (glucose, 200 mg) in order to determine the
bacteria to fungi ratio of each (Anderson and Domech l978a, 1978b).
Amendments to subsamples were added dry and thoroughly mixed iato spoil
by hand. Samples were then incubated at 22° C, in the dark, for 8 hours
in clean, 1. gallon, glass, screwtop ja:s with a beaker of alkaline CO 2
absorbent (0.2 N NeON). The alkali was titrated against 0.5 N 11C1 after
E.aturation with BaC1 2 .
410
-------
Table 2. RESULTS OF LIrraK DECOMPOSITION STUDY: CO 2 EVOLUTION FRflM
A STANDARD SPOIL-LITTER SYSTEM. 1 MEASURED BY STATIC C02
AI3SORPTION SYSTEM OVER 21 DAYS.
Treatment Cumulative
mg
% Weight Loss
Weight Gain
Relative
C02-C
per
.lar
of Litter
by Ilorms
Fungi on
Litter 4
A. gtuUnosa 60.78 54.7 21.8 0
leaves, earth- i (1.66) ± (1.61) ± (2.23)
worms 2
A. glutixtosa 48.39 19.3 4-L-f
leaves ± (2.18) ± (3.26)
A. zosa 49.56 38.0 10.0 .4-f
leaves auto— ±(3.71) ± (3.71 ± (2.55)
claved, 3 earth-
worms
A. glutirtosa 28.86 11.2 II • I
leaves, auto— ±(0.45) ± (1.03)
claved
L pseudoacacia 5j..67 41.6 4.8 0
leaflets, earth— ±(1.42) ± (5.59) (2.38)
worms
. pseudoacacia 40.89 8.1 0
leaflets i(1.1Q) ± (0.80)
1. pseudoacacia 46.32 9.1 3.8 0
leaflets, auto— ±(1.89) ± (4.47) ± (3.75)
claved, earth-
worms
R. psendoacacia 27.45 5.2
leaflets, auto— ±(1.37) ± (0.58)
claved
11.2 kg spoil, 3.85 g leaf t Lssue; spoil brought to J13 bar
moisture (26.fl RON); in 1 gallon, glass, screw—top jars incubated at
16° C in the dark.
275 to 9.1 g combined weight, 2 adult L. terrestris per jar.
3 ”Autoclaved”: both the 1.2 kg spoil and the 3.85 g leaf tissue
were autoclaved at 2400 C for 2 hours.
4 Measured as relative surf a e area of leaves with fungal growth.
5
Numbers in parenthesis indicate standard error.
‘I 11
-------
RESULTS AND DISCUSSION
Sampling within each plantation and in immediately surrounding
areas in Octobe 1979 showed that after 12 years the introduced L.
terrestris had successfully multiplied and had dispersed throughout
their respective woodlots. The worms had x’ t, however, colonized the
surrounding, non—wooded areas. Also no c idence of invasion of L.
terrestris from outside the study area wa. observed.
Under A. 3 no8a, L. terrestris reached a significantly greater
biomass per ci 7 (164.26 vs 60.00 g fresh vt/rn 2 ), and buried leaf litter
to a greater degree over a six month period (91.7 vs 43.0%) than
under Robinia psuedoacacia (Table 3). This preference for A. glutinosa
leaves compared to R. pseudoacacta leaflets was also reflected in the
incubation experirneucs where unautoclaved A. glutinosa treatmenta with
earthworms produced significantly greater amounts of CGZ over a 3 week
period than comparable treatments with R. 2 doacacia leaflets (Tables
3, 4). Worms feeding on A. leaves also showed signifIcantly
greater weight gains than worms which fed on It. pseudoacacia leaflets
(Table 3). A. glutinosa leaves are a highly pief erred leaf by k.
terrestri8 , (Satchell and Lowe, 1967) and have a high food caloric
value (Bocock, 1964). R. pseudoacacia leaflets, however, contain phy—
totoxic compounds and cardiac gluc sideg (Eardin, 1962), substances
which may make leaf tissue lees palatable to worms.
Table 3. EARTHWORM ( .1ERRESTRLs ) 1’OPULATIONS ON TWO FORESTED SPOIL
BANKS AND TEE PERCFNT OF WOODY LEAP LITTER REMOVED OVER A
SIX MONTH PERIOD, OCTOBER 1978 — MARCH 1979
Site
U Adult Worms
per
g Adult Worms
per a 2
:1ean Wt.
Adult Worms
X Leaf
Litter 1
Removed
A.
glutinosa
56.5**
164. 26**
3.03*
91.7*
R.
psaudoacacia
27.52**
60.O0**
2.12*
43 Ø*
**sjg to p <.001
*sig to p .: ..0l
Detertnined by paired plots, one of which had worms while in the
other worms were removed with formalin.
Reynolds (1972) noticed low earthworm numbers under R. pseudo-
acacia stands in Indiana. He felt that the worm populations were in-
hibited bc.cause rapid microbial decomposition of R. pseudoacacl a
-------
leaflets was moving leaf carbon directly into htmzus carbon, thus decreds—
ing the amount of food available to leaf—feeding worms. Observations,
however, in this paper showed that over a 21 day incubation period, A.
glutinosa leaves (which in the field supported a high density of worms)
decomposed more rapidly than R. pseudoacacia leaflets (Table 2). Pres-
ence of chemicals antagonistic to the worms in the B.. pseudoacacia leaf-
lets seems a more logical explanation for the low earthworm numbers.
There was greater observed fungal growth on A. glutinosa leaves
(Table 2), and a tendency for higher soil fungal percentages (Table 4)
in treatments with A-. z . osa litter. Possibly, this reflects the Lack
of inhibitory substances in A. glutiziosa Leaf tissue.
Table 4. BACTERIA, FUNGI RATIO (B/F) AND RELATIVE MICROBIAL ACTIVITY IN
SPOIL MATERIAL rr a 4 WEEKS OP INCUBATION WITH VARIOUS TREAT-
MENTS
Treatment
B/F 2
Re
Nb
lative
Activity 3
Spoil, A. glutinosa leaves, earthworms
40/60
15.39
Spoil, A. j osa leaves
70/30
6.28
Autoc.1.aved 1 spoil, autoclaved A..
leaves, earthworms
45/55
16.79
Autoclsved spoil, autoclaved A- glutinosa
leaves
30/70
12.59
Spoil, R. p 1doacactd leaflets, earthworms
Spoil, R. u.1oacacia leaflets
tiutuclaved spoil, R. pseudoacacia leaflets,
earthworms
40/60
40/60
60/40
12.59
7.68
18.19
Autoclaved spoil, R. pseudoacacia leaflets
90/If)
10.48
1 ”Autoclaved”, both the spoil material
claved at 240° C for 2 hours.
and the leaves were auto—
2 Bacteria/furzgi zatio of relative activities as measured during
8 hour incubation after specific inhibition. Rounded to nearest 5%.
3 Relative 8 hour pro 1uction of CO 2 C after the addition of 200
mg glucose to 100 g of soil.
-------
Dit. erences in C0 2 .C evolved per jar between autoclaved samples
with worms and autoclaved samples without worms (21 mg C02.C for A.
. j osa, and 19 mg C0 2 .C for R. pseudoacacia ) are greater than
differences between unautoclaved samples with worms and unautociavecf
samp1e without worms (12 mg C02.C for A. osa, and 10 mg C0 2 .C
for R. pseudoacacla ) (Table 5, Fig. 1). This difference either rep-
resents colonization of autoclaved systems with intestinal micro-
organisms from the earthworms, or accelerated growth, ac a consequence
of actiona of worms, of those microbes which survived auto claving pro-
cedures.
Table 5. ANALYSIS OF VARIANCE OF C3 2 PRODUCTION FROM LITTER ON SPOIL
MATERIAl. AFTER VARIOUS TA ENTS
Source of Variation Degrees of
Freedom
Sum of
Squares
Mean
Square
F
SI gulf—
icance
Leaf species 1
1
264.87
264.87
17.4
0.005
Worms 2
1
2405.45
2405.45
158.05
0.005
Autoclaving 3
1
1489.74
1489.74
97.89
0.005
Species of leaf x
autoclaving
1
78.38
78.38
5.15
0.05
Species of leaf x worms
1
3.85
3.85
<1
————
Autoclaving x wornis
1
182.88
182.82
12.01
0.005
Species of leaf x
autoclaving x worms
3.
1.37
1 37
<1
——-—
Error
Total
3].
471.79
15.2190
38
—
4898.33
‘Either A. glutinosa or R• pseudoacacia .
2 Either w rms (L. terrestris ) were present or not.
3 tlAutoclaviagu = both the leaves and the spoil were autoclaved.
at 240° C for 2 hours.
The greatest soil microbial activity, measured as C02.C evolved
over 8 hours after adding 200 nig glucose to 100 g spoil, was observed
in autoclaved treatments with worms. The least soil microbial activity
was observed in unautocla,ed treatments without wor is. Possibly, the
414
-------
60
____ _____ F Li ___
Alnus Rcbinla —W -f-A —A
(sig. 0.005) (sig. 0.005) (slg. 0.005)
-A_ -A_ U
Alnus Robinia —A +A
(sig. 0.05) (s g. 0.005)
Figure 1: RESULTS OF ANALYSIS OF VARIANCE I N DECOMPOSITION STUDY
Abbreviations: W (worms)., A (autoclaving)
-------
former represents an opened microbial system being colonized y rapidly
metabolizing, opportunistic organisms (either from worms’ intestines or
as a consequence of actions of worms), while the latter represents a
more slowly metabolizing, equilibrium population of microorganisms. A
more exact determination and quantification of both soil microbial popu-
lations and intestinal tnic:oflora of worms is needed ti determine
whether or not active “seeding” of microbes b vorus is occurring in
these systems.
LITERATIJRE CITED
Anderson, .7. P. E. and K. H. Domach. l978a. Mineralization of bacteria
and fungi in chloroform—fumigated soils. Soil Biol. Biochem. 10:
207—213.
Anderson, .7. P. E. and K. H. Domach. 1978b. A physiological method for
the quau itative measurement of microbial biomass in soils. Soil
Biol. Bloehem. 10: 215—221,
Bocock, K. L. 19E’. Changes in the amounts of dry matter, nitrogen,
carbon aid energy in decomposing woodland leaf litter in re].a—
tion to the activit.eg of the soa.l fauna. 3. Ecol. 52: 273—84.
Edwards, C. A. and C. W. Heath. 1963. The role of soil animals in the
breakdown of leaf meteial, p. 76-83. In .7. Doekson and 3. van
der Drift, Soil Organisms. North Hollar.d, Amsterdam.
Hamilton, W. E. 1979. Earthworms on forested spoil ba 1 iks. Master’s
Thesis, The Ohio State University. 70 p.
Rardin, 3. W. 1961. Poi on, .i’i 1ants of North Carolina. North Carolina
State Bulletin #44. Raleigh, North Carolina.
Neumann, U. 1973. Succession of soil fauna in afforested spoil banks
of t: e brown—coal mining district of Cologne, p. 335—348. In
R. 3. Hutnik and C. Davis, Ecology and reclamation of devastated
lands. Vol. 1. Gordon and Breach, New York.
Re;, F. 1962. Studies of earthworm populations in orchards. 1. Leaf
burial in apple orchards. Ann. Appi. Biol. 50: 389—404.
Reynolds, 3. V. 1972. The relationship of earthworms ( O jgochaeta:
Acsnthodriljdae and Lumbricidae ) distribution and biomass in six
heterogeneous woodlot sites in Tippecanoe County, In:liana. .7.
Tenn. Acad. Sd. 47(2): 63—67.
Satcheli, 3. E. and D. G. Lowe. 1967. Selection of leaf litter by
Lumbricus terxestris , p. 102—119. In 0. Graff and 3. E.
Satchell, Progress in soil biology. North Holland, Amsterdam.
Vi” rstedt, 3. P. and 3. H. Pinney. 1973. Impact of earthworm intro-
duction on litter burial and nutrient distribution in Ohio strip—
mine spoil banks. Soil Sd. Soc. Am. Proc. 37(3): 388—3 l.
416
-------
QUESTIONS and COMMENTS
. RICHTER : Can nutritional content of Alder i.e.,
calories and/or chemical composition account for the differences
in preference between . nos and . seudoacacia rather
than phenolic compounds?
Are you aware of any chemical. changes with respect to
phenolics and senescence in . øseudoacacia i.e. are secondary
substances reabsorbed, broken down etc. prior to leaf abcision?
W. HAMILTON: Alnus leaves are known to be high in calories
and sugars and are highly preferred by . terrestris . Whether
the difference in preference by . terrestris for Alnus and
Robinia is due to a high preference for Aln s on a rejection
of Robinia could not be answered absolutely in this experiment.
I am not aware that that occurs. It is my understanding
that there are, indeed. phenolic compounds in the freshly
fallen Robinia leaflets.
AT BELL : Do you think the greater stimulation of
microbial activity obtained in your autoclaved leaves could
have been due to nutrien mobilization by the autoclaving?
Perhaps this could be clarified in an experiment using irradiated
litter.
WE. HAMIi!DON : The autoclaving is a very severe physical
manipulation. and I am sure that it did have an impact on the
physical and chemical properties of the leaves. Perhaps an
alternative method of “sterilization” could be employed.
. FAIZY : Will you please g .ve some reasons for
the strikingly large variation (from
-------
SESSION VI: EFFECTS OF SILVICULTURAL
PRACTICES ON SOIL ORGANISMS
Moderator: Veikko Huhta
Universily of Jyvaskyla
Jyvaskyla, Finland
-------
THE EFFECTS OF HARVESTING PRACTICES ON ORIBATID
MITES AND MINERAL CYCLING IN A SITKA SPRUCE FOREST
SOIL
Alison P. Frater
Westfg,la Col!i’ge
Unii.’s ,, of [ omEn,,
England
INTRODUCTION
In Britain, coninercial rorestry is concentrated in the wet,
infertile uplands of Scotland and North Wales. Large-scale
a forestation of th3se areas, previously used for grazing or arable land,
is relatively recent. The fir t planting began in the 1920’s. although
the major surge of planting occurreo in thB 1953’s. These primary
plantations arc presently being harvested and the seccnd rotation
established. Work in progress by the Forestry Cormiission, the
t1 caulay institute for Soil Research, Institute of Terrestrial Ecology
ar 1 d various university departments may provide some . , .ndication as to
the effects of various felling practices on both the physical nd
biological propertiec of these phosphorus-deficient and, for most of
the year, anaerobic forest soils.
Recently, whole tree harvesting (removal 0 f most uf the tree
including normal forest residues) has been suggested for the future
in order to maximize yield. Such a practice will result In consider-
able r utrient ren oval from the site (In branches, needles, boles, for
example) as well as initiating a changea pattern of soil damage The
absence of ‘iop a d top’ will expose the soil surface to considerable
weathering and possible erosion.
Within the Forestry Commission’s objectives of determining
both short-and lang-term effects of harvesting practices on the
establIshment, long-term success and management of the sezond rotation.
this paper is designed to outline certain microenvironmental changes
brought about as a result of two contrasting felling practices,
standard clear-felling and whole tree harvesting. Concomitant changes
in species composition and diversity of the oribatid mite component of
the soil fauna are being monitored, and some preliminary results arc
presented. The possible functional significance of such changes on suon
long-term processes as mineral cycling are discussed.
SITE DESCPIPTION; MATERIAL3 AND METHODS
The study site is si uated in Beddgelert forest in the Snowdonia
National Park, North Wales (S.H. 5659, altitude 3OO-38 n). The soil
type is a peaty gley wIth dispersed iron pan, the surface peat i iyer
being approximately 25-30 cm thi’k. The pH of tnis layer varies
between 2.8 and 3.8 and decreases with depth. 8 fore felling, the crop
was Sitica spruce, planted at 1.4 m square spa irig with a maximum annual
increment oF 12 m2.ha-1.yrl. The crop was plqnted in 1930 and was clear-
felled by sky lining in June 1978.
1. 120
-------
Two experimental plots 1 Ban x 80, within the harvested area.
were marked and staked iith an intervening buffer zone of 1O-15m. One
plot was left untreated with none of the felling debris removed this
plot is termed CF. It. has very litt]e, or no, ground vegetation but
a cover, iarying between 50cm and Im deep 1 of felling debris, branches,
twigs and needles. The ather plot was cleat-ed of ell felling debris
except large discarded trunks. This plot .s intended to simulate a
complete or ‘whole tree’ harvesting pract:.ce, and is termed wTH.
Finally, a control plot IC). 8Dm x 8Dm. was establIshed in an adjacent
forest stand. The soil and tree conditions almost exactly reproduce
those of the two experimental plots prior to felling.
Sampling and measurements
Samples are taken at three to four month intervals beginning i.t
June 1978. A regular sampling program has been disrupted by bad
weather but results have been obtained for June 1978, November 1978,
January 1979, (larch 1979 a;sd July 1979. On each sampling occasion,
14 cores (18.3 cm 2 x 5.5 cm ), seven from the combined litter and
fermentation layer and seven from the humus layer, are taken along a
transect line in each site. Orihatid mites are extracted from the
samples using Kempson bowl extractors. Additional samples of the humus
layer are taken for measurement of p 1 -I. moisture content, organic content
and bulk oensity from each site on each sampling occasion. These para-
meters outline the effectije environment of the soil system. t hey
describe the amount of living space and indicate the availability of
food. Changes in pH mel be direutly attributable tc changes in carbon
dioxide levels and thus may provide an indicator of community metabolism.
A 12 hour temperature profile is recorded in the s’irf ce litter,
sub-surface litter and humus at each site and on each sampling occasion.
Atomic absorption spectroscopy
Calcium analysis of two mite speci9s has been undertaken using
A.A.S. Preliminary results are presented.
RLSULTS
Temperature
Figure 1 shows the variations in litter temperature over a 12 hour
period at each of the three sites during March 1379 sampling. These
curves are typical of those obtained on other sampling occasions. Clearly
there are distinct differences between the control plot and the two
experimental plots which appear directly attributable to harvesting
practice. Removal of both canopy and felling debris in WTII produces
wide fluctuations in temperature. Increases of up to 15°C were
recorded within one hour in the litter layer of thi 4 plot, compared
with a maximum variation of only I or 2°C in the control plot. These
fluctuations are dampened to a certain extent by the presence of a
surface cover of felling debris in the CF plot, although variations of
up to 9.5 0 C within one hour were recorded here.
4 2 1
-------
ri ur 1 • v ri tion in j].Lt 5I
during March 1979 in
(C = control, CF =
harvested).
oc
j
Mc ,isture content
temperature over a .ii nour perioc
each of the three sampling sites
clear-felled; WTh = whole tree
Data on moisture content, expressed as % of fresh
given in Table 1.
weight, are
TABLE 1. Moisture co.itent (U of samples from h layer in each of the
three sampling sites. Values are means of eight subsamples.
Sampling Sampling sites
occasion
C
CF
WTH
June 1978
84.6
84.3
21.7
November 1978
62.5
52.6
32.0
January 1979
62.5
80.4
56.0
March 1979
66.4
75.6
61.2
July 19/9
71.0
75.0
62.3
These values indicate considerable drying out in W T H, particularly
s an immediate effect after the felling period. Felling debris in CF
and the presence of a closed canopy in the control obviously afford
considerable protection and reduce evapotranspiration, although tie
variable nature of the CF values may, in part, indicate the patc’ y
debris cover in parts of this site. The moisture content in WTH
increases over the last three sampling times and this is directly
attributed to the development of herbaceous vegetation in this Plot,
consolidating the ground surface and preventing excess water loss from
the site.
,,is ms 131$
WTH
C
Tim.
k22
-------
PH
Data on pH of the humus layer at each site are given in Table 2.
TABLE 2. pH values of san.ples from humus layers in Bach site, measured
in O.O IM CaCl 2 at 1:20 W/V suspension (means of four subsamples .
Sampling Sampling sites
occasion
C CF WTH
June 1978 3.65 3.65 4.05
November 1978 3.50 3.58 4.45
January 1979 3.20 3.00 3.70
March 1979 3.40 3.05 3.65
July 1979 3.60 3.30 3.90
It may be noted that WTH sustains a higher pH value than the other
two sites throughout the period, although the difference is certainly
being reduced in the last two sampling occasions. This initial increase
in pH in WTH nay be the result of an initial loss of organic material
from the sr’il (see belowi. It is interestFig to note in passing that
Sundman, Huhta and Niemela (1978) recordez a rise in bacterial numbers
irnnediately after harvesting in a spruce forest, and this may have
been a response to a soil pH increase sLch as has bee!1 found here. The
tendency of p11 values in WTH to come closer to those of the control on
later sampling occasions may indicate a reversion to a steadj state
after an initial change ±n the activity of the soil system.
Loss on ignition
Data for loss of weight on ignition of the humus layers from each
of the sites indicate a decline of up to 30% in WTH compared with the
control and CF plots irmiediately after felling. This is possibly due
to erosion of organic layers as well as the renoval of organic input
in WTH. This ib further reflected in bulk density measurements of the
organic layer of the three sites. Dragging effects of the WTH simula-
tion appear to have loosened the soil, increased the bulk density and
therefore the living space, whilst reducing thE organic content, and
theref ore food availability.
Species composition and diversity
Table 3 shows the total numbers of oribatid.s, total numbers of
species and the equitability components for each site on the first
three sampling occasions. Data for the later samplings have not
yet been analysed.
423
-------
TAF’LE 3. Total numbers of individuals (NJ. species (5) and equitability
components (e) of oribatid mites in each of the sampling sites
on three samplit ig occasions (14 cores per site).
June 1978 November 1978 January 1979
C CF WIN C CF WTH C CF WIN
N 476 632 226 337 531 316 1051 633 512
S 15 19 13 16 16 18 19 17 14
e 0.66 0.39 0.69 0.84 D.44 0.65 0.55 0.73 0.89
It is interesting to note that there are considerably fewer
individuals ir vJTH than in thc control a,,d CF plots on all three sampling
occasions, but particularly in June 1978. The number of species is
also lowest in WTH at this time, although the number of species does not
alter significantly between plots or between sampling occasions. On
the other hand, appreciably higher numbers of indivit luals are recorded
from CF. compared with thR control on the first two sampling occasions,
altnough this contrast dons not occur on the third sampling occasion.
An examination of equitability compcnents for the first two
sampling ocrasions may provide an interesting interpretation of these
results. In WTH equitability is relatively high in June 1975. hardly
departing at all from that ;‘rnwn by the control. In November 1978 .
equitability remains at t’ie same level as in the previous June in WTH
but has increased in the control. However, in CF the equitability is
considerably lower than either the control or WTH on both sampling
occasIons, indicating that a change in species composition has
occurred in this site.
The two harvesting practices, clear-felling and whole tree
harvesting have quite distinct and inmediate impacts on the soil
environment. The initial effects of whole tree harvesting are physical.
or mechanical, and as far as the oribatid fauna is concerned thare
appears to have been an indiqcriminate reduction of individuals.
irrespective of species. This effect can be attributed directly to
the removal of surf ace organic materiad. and considerable mechanical
disturbance in the site. Further evidence for this is provided y
the canplete absence of Platynothrus peltifer (C.L.K.) from WTH in
. lune 1978 and by a l ower nber of individuals of many other litter-
dwelling oribatid species. In addition. Maliaconothrus punctatus 1 v.d .
rL9rivuen) which was present initially in the control and CF plots becomes
considerabl , reduced in WIN. This species prefers wet biotopes, and
its low numbers in WIN nay be a reaction to the urier conditions
prevailing here. Such changes in species composition would not
necessarily change the equitability value, since this statistic gives
a measure of the apportioning of individual among available species,
rather than the absolute numbers of species and individuals.
424
-------
By contrast, changes occurring in Cr are characterised by
population increases in certain opportunisitic or explc tive species.
P. peltifer, Oppia quadricarinata (Mich.), Suctohelbella vera (Mcritz)
and Opria obsoleta (Paoli) in)une 1078 . and Phthiracarus affinis
(Hull) in November 1978 are present in considerably higher numbers in
CF compared with the control. The immediate effect of clear—felling
is to increase th u oraanic input, in the form of ‘lop and top’ into
the sail. This j.s a b±ological effect, sharply in contrast with the
physical effects produced in WTH. This increased organic input may
favour a selectIve group of litter—dwelling scecies, particularly those
which feed on naedles, such as P. affinis . The shifting balance of
populations in favour of such species could account for the low
equitability levels observed in CF on the first two sampling occasions.
The data for January 1079 ace more difficult to tnterpret. There
are some indications that the initial shock to the soil system. occasioned
by the harvesting practices may now be becoming attenuated. Numbers of
individuals tncrease in all sites, although this may be due to an
intrinsic seasonal cycle. As already mentioned, there are no significant
differences between the numbers of species present, compared with the
two previous sampling occasions, but the equitability values heve
changed quite considerably from those obtained in November 1978. The
vaJue for the control is now approxinating that obtained in June 1978
and, prrhaps, this is indicative of a seasonal cycle. Equitability in
CF has now risen well beyond its esrlier valLues and, sgain is
approaching that of the control, possibly ir.& ating that some mcasure
of environ mental stability is being achieved. In WTH. equitability
rises to a surprisingly high level in January 1979. There is no obvious
explanation for this increase, although it should be noted that the
character of this site has changed considerably frcm its uriginal
condition with the welopment of a herbaceous ground layer. Such a
transition from forest to a more open g:assland type is likely to
produce a reduction in the numbers of oribatid species and, iieybe
also, a more equitable ‘edistribution of individuals among the
remaining species. Data from suLisequent s mp1ing should clarify this
situation.
Calcium analysis
The identification of shifts in species dominance and diversity
is not merely of academic interest in nutrient-deficient sites, such
as the one studied here. Oribatid mites vary in their roles as
potential reservoirs of available mineral elements. The calcium contents
of two species have been analysed by atomic absorption spectroscopy,
and the results obtained illustrate this point adequately.
The two species in question are Phthiracarus affinis and
Platynothrus peltifer . and the mean values for calcium content, in ppm.
are given below:
! . affinis P. peltifer
x = 1489.6 x - 112.8
42,5
-------
It is evident that P. affinis consistently shows a higher
calcium content than r. peltifer by a factor of 14 or 15. Both have
itlatively low values, as would be expected in such highly acid soils.
This analytical approach will be extended to other species occurring
in the sites in due course.
CONCLUSIONS
1. Felling practices, particularly whole tree harvesting, have
immediate, short-term effects on temperature, moisture and p 11
regimes in forest soils.
2. These effects are reflected in changes in species composition
and diversity of oribatid mites.
3. Short-term physical, or mechanical, effects are particularly evident
after whole tree harvesting where a reduction of individuals has
occurred without a change in species composition or diversity. A
different effect is evident in the clear-felled plot where a
restricted number of opportunistic species may have benefited from
the increased organic iaput.
4. Long-term effects are only just becoming apparent and these seem
to involve a recovery from the harvesting perturbation in the
clear-felled site. Changes in species’ abundance in the whole
tree harvest site may be associated with the development of a
ground layer of herbaceous vegetation.
5. Species of oribatid mites differ in their ability to concentrate
such elements as calcium. This fact is being used to interpret
the significance of changes in abundance end diversity of the
oribatid fauna in the context of mineral cycling in the harvested
plots.
LITERATURE CITED
Sundmar., V., Huhta, V. and t Jiemela, S. 197B Biological changn in
northern spruce forest after clear cutting. Soil Biol. Biochem.,
10: 393-397
-------
ASSESSMENT OF TOXIC EFFECTS OF THE HERBICIDE 2,4, 5-T
ON THE SOIL FAUNA BY LABORATORY TESTS
H. Eijsackers
Ressirch Ii,shtut, for Nature Mruage,nenl
The N ,Ih ,rla d
Intrnduct ion
During the past decades it has become clear that the envirunmental risk
of new synthetic chemicals has to be assessed before introducing these
chemi al into the environment. This holds especially for pesticides,
since these ar developed to kill animals or plants. And although these
pesticides are meant to be selective, numerous examples of environmental
side effects show that this is tiot always true.For this reason suitable
risk assessment methods should be developed. To find out the risks
involved in the application of new pesticides field plots can be sampled
regularly before and after a treatment. Alterflatively in the laboratory
a number of selected species can be tested for their sensitivity for
pesticides. Laboratory research has the advantages of speed, low cost,
relative simplicity and controlled environmental conditions. However,
becat se of this simplicity numerous relationships between the species
under study and other members of the soil fauna have to be neglected.
Moreover, laboratory conditions have to be selected and fixed contrarily
to the locally and temporarily fluctuating conditions in the field.
In this study it is tried to meet these discrepancies. Therefore,
ways have been analyzed in which soil fauna species get into contact
with the herbicide 2,4,5—T. 2,4,5—T has been widely used in forestry.
In The Netherlands it has been applied in forests and nature reserves
to control black cherry ( Prunus serotina Ehrh.). In recent years there
is a growing concern about the toxicity of this compound for non—target
organisms, but little information is available on the fauna exposed to
the herbicide. Because a large part of the herbicide reaches the ground
either directly during spraying or indirectly after leaf—fall of sprayed
Prunus shrubs, possibh ffects on the soil fauna are of special concern.
Therefore in the laboratory experiments about effects of 2,4,5—T by
direct contact have been done with 14 suil fauna species to evaluate
their [ relative sensitivity. With three of these species, reprnsenting
different functional soil fauna groups, further experiments have been
27
-------
carried out concerning th way the mobility and food corsumption of
the animals are influenced by the herbicide. Furthermore, the effect of
changing and constant environmental conditions (temperature and
moisture) on the herbicide’s impact has been studied.
Materials and methods
For the experiments animals were collected freshly from the litter of
a forest next to the Institute with tnt’ aid of Tuligrens funnels and
pitfalls or by hand sozting. They were stored in the’ laboratory on a
moist soil substrat.e in the daik at 15°C for a maximum period of three
weeks. The animals were fed regularly.
The experiments about the effects of direct contact with the herbicides
were cart ied out in glass dishes (0 9 cm) or refrigerator boxes (20 x 20 c
with a substrate of moist sifted sand (1 mm mesh.). Substrate and animals
were spray’d with a spraying apparatus adapted from Ten Houten and
Kraak (1949).
Food consump’ion experiments were carried out in small glass • r plastic
dishes (0 respectively 5 and 2 cm). The different food items re
sprayed with the herbicide or soaked in it. in a partial vacuum. The
amount of food consumed was measured as food weight loss or pellet
prosuction. The amounts of herbicide in the soil substrate and the
different food items were analyzed by gas chromatography. All experiments
were carried out in climate rooms at 15°C and 907. RH. For full details
about the set up of the different experiments and the chemical analysis
the reader is referred to Eijsackers (1978 a, b, c and d).
Results
I. Possible ways of uptake and effects of 2,4,5—T on mortality.
The effects of 2,4,5—T on the longevity of 2 isopod species, I millipede,
4 cotlembole and 7 carabid species after spraying 0.3, 1.25 and 5%
aqueous solutions of 2 ,4,5—T on the animals and the soil substrate are
summarized in table 1. Spraying of a 5% solution causes with all the
species a decrecsed longevity, which varied from 5% up to a 20 feld
decrease. This variability exists both within and between the different
soil fauna groups. The more sensitive species also show a distinct
decrease after treatment with a 1.25% and even with an 0.32 solution
of 2,4,5—T. The species selected for further experimentation do show
a more or less medium sensitivity. The selected species were the isopod
Philosciamusc ’or m Scopoli representing th? primary decomposers;
the collembole Onychiurus guadriocellatus Gisin representing the
secondary decomposers and the carabid Notiophilus biguttatus Latr.
as a predator. The different ways these species can contact 2,4,5—T,
-------
1;tti It’ 1 L. .tig v it y relal i Vp Lu la ,trt ’aL.!d spec itnert of I sopod, mi 1 ii- r” th.,
coI1t mb ,.Le and raL d t*fi..er treatment with djffti nt
dO 5t ’ of , ,l4,5—T. - -_____________
ConceritraLion of 2,li,5 —T
Species 0.3% 1,25% 5%
I SOPODS
Phtloecia muscox’im
Oniscus asellus —
MILLIPEDES
Glower is warginata
o OLLEMBOLE S
Onychiurus guedriocellatus 0
Tomocerus flavesceris
Tomocerus minor
Orchesella cincta .
C ARABI DS
Abax ater 0
Abax parallelis + +
Nebria brevicollie 0 -
Pterostichua oblongoDunctatus +
Asaphidion flavipee + +
Leistus rufomarginatus
Notiophi].us bigut batus
no or hardly any difference in longe .ity with control
—1+ decreaee/iri rease of longevity of 5—90%
—_ decrease of longevity wiLh a factor 2—20 e.g. from 4 to 20, reap. 2d.)
429
-------
are shown in Fig. 1. The 2,4,5—T solution drifting zway during sprayirg
and dripping of the leaves afterwards has an irregular distribution or,
the forest floor (Table 2). Because of this irregular distribution
and the distribution of the soil fauna and its mobility, it is not only
necessary to establish the effects under continuous exposure with a
completely treated substrate, but also on a partly treated substrate.
In this situation it is important whether the animals are able to
distinguish treaLed from untreated areas of the substrate.
2. Impact of the mobility jf the animal on the effect ruf the herbicide.
To study the behaviour of the animals, individual specimens were observed
directly during 10 minutes after enterir.g a box with a pattly treated
substrate. When entering and making a first choice between the treated
and untreated part of the substrate (Fig. 2) neither th isopod nor the
carabid showed an avoidant:e of the treated part. The isopod even
preferred th substrate sprayed with a low dose of 2,4,5—T compared
to the control experiment in which extra water was sprayed as a
treatment. However, the sprin?tail clearly avoided the part treated
with the herbicide. Comparing the distribution of the residence times
in the treated and untreated parts of control, low dose and high dose
experiments (Fig. 3), there was made again no significant distinction
by isopod and carabid whereas the collemboic showed a distinct iepeltent
reaction, consequently they were able to avoid or withdraw from a
treated area. To evaluate this avoidance over a longer period, experiments
were also done during which the animals were observed once a day during
a 30—day period. From figure 4 it becomes clear that the carabid still
did not show any avoidance, but the isop l and the collembole avoded
the treated area. Notwithstanding this avo dance, the isopod and
collenibole have an increased mortality on the * ubstcate partly treated
with a 1.25% solution of 2,4,5—T. This increased mortalit; also holds
for the carabid. Compa ing the mortality of co. tinuously exposed animals
and animals with a temporary exposure on a partly treated substrate
(Table 3) it is cleaT that. the possibility to avoid or to withdraw from
treated areas of a soil substrate d , inishcs the mortality of isopod,
collembole and carabid.
3. The effect of the herbicide via food consumption
Saprophagous soil fauna plays an important role in litter break—down.
4 .30
-------
•L tLi1t 2. Di LributiuH of 2,1 1 , ,—T (0.001 m]/dm2*) on thu
Furt t tloc r.
type i,t ;prayt’r
wlLuunt
app]ied
utidi r ;hrubs
between shrubs
hand
12
J /ha
)(b—1? )
2( 1— )
motor
8
1/ha
4( -i)
‘
2.5(1—f )
* 0.001 ml/dm 1 liter/ha.
Tab).e 3. Perc .nt.age m’rt.aJ ity of isopod, co]lembole and
carabid after 1C i ays on a coinpleteiy or partly
treat t•d c.j] substrate with 1 .25% , 6 —T.
L.iiUSCLLI mw . rwn
connpIi-t ’ 1y

coni ro1
PU
:‘o
2,le,5—T
90
60
0uy hi urt . uuadriu .:] 1at.u!
l. QIflhi) .. l t: ly
Ly
0
1
‘ill
17
‘ .jLjOJ)IIj lus bLgL1ttnLu
..npI t. y
p .iiy
8
0
100
30
-------
Figure 1: Possible ways of c ’ntact of’ soil fauna 2pecies with a herbicide
after 5vrayirg.
432
-------
(
EXPERIMENT WITh WATER (CONTROL)
number c i iecpods m treated part
H il ft I
ol Isogods a, LI*reated part
1 raaler cA epringtalls
i:L Ji1J I
I i u y r ii I— T
I 2 3 4 S S 7 S S lb 2030
EXPERIMENT WITH i.25% 2,4,5—T
IIII M I
!
234
0 kvmg
dead
animals
Figure 2: Distribution of’ first choice of lit specinens entering a soil
substrate partly (right, half) sprayed with wa.er (control) or
with a low or high do3c of 2,h,5—T ester.
-------
Figure 3: Distribution of rfsi(]ence time in percentages of 10 spocimens
during 15 jr ut. s on a soil substrate partly (right hal.f) treated
with water (control) or with a low or high dose of 2,h,5—T ester.
first choice
EEJ __ __
* L*J Li J L
Figure : Distribution in p rc.ntages of living and dead (hatched) specimens
of isopods, ccllemboles and carabids on soil substrates partly
treated with water (control) or with a 1.25 solution of 2, 1 4,5—T
ester.
bw does dose
p iod of s y control 0.003 mi bT O )25 mi&1m
cwa d j j Eli E
-------
Because of its low assimilation efficiency large amounts of titter
have to be ingested. In this way considerable amounts of 2,4,5—T are
ingested too. Predators like the corabid nay irgest considerable
amot:nts of 2,4,5—T due to bio—accumulation. The persistence of 2,4,5—T
in cherry leaves and litter contained respectively 200—400 and 100 ppm
2,4,5—T. The various ways that soil fauna can ingest 2,4,5—T are:
consei tion of sprayed cherry leaves, contaminated litter items,
and contan-inated prey. The necrophagious behaviour of the springtails
may result in consumption of died, cantaminated relatives. Ingestion
of 2,4,5—T may result in a changed rate of consumption and an ir.creased
mortality as well.
The effects of different treated food items on consumption rate and
longevity of collembole, isopod and carabid are summarized in Table 4.
When a number ot’ litter components (birch litter, larch needles and
green algae Pleurococcus) are offered tc. the springtail, the effects
are quite different. With the algae the springtail shows a marked
decrease of consumption, whereas mortality increases. The effects on
mortality with birch litter and larch needles are smaller, with larch
needles there is also a decreased consumption rate. The isopod also
consumes less treated than untreated birch litter and shows an increased
mortality. In contrast with the findings above, breakdown of cherry
litter collected freshly every week is not hampering at all. Primary
breakdown by the isopod as well as secondary breakdown of the litter
fragments in the isopod pellets by groath of fungal hyphae and graz .ng
of springtails, is better with treated than untreated cherry litter.
Isopods show a significantly dec’eased mortality whereas the mortality
of the collen-boles is somewhat increased • Observations and some minor
experiments about the effects of necrophagy with the springtail did not
reveal that the ingestion of herbicide by consuming springtails killed
oy the herbicide does affect the colleniboles adversely. Predation by
the carabid of contaminated springtails causes a considerably increased
mortality however. This has been obs-ar ed with prey that wjs still
mobile after being sprayed with a 0.32 solution of 2,4,5—T and with
prey killed by 2,4,5—T. Mobile prey is strongly preferred to immobile
prey, but when only the latter is present it is eaten eagerly.
k35
-------
t Pablc7 . Effects of tr at.m.ist u i I ’.. l uith 2, )s, —T on consumption
r. . ai i uinrt a] i y -.V irq. ii , o 1] • mbc. I c and carat. id,
e;l .r ’ ;”:i as er •i .& •1 ’ i Xi ’ ras (+) or decrease (_
i’.’ I a’ i i. • 1(3 Un t rtat ‘ I 1’. ) ..)d
consumer
fc.od type
c: ’ . zn .tic ’. rat- mortality
cc11emt’ l
hirc I i tcr
—
1 tr L r eed1c
—
—
algae
—‘ ‘: ‘
+Lrr
iso cd pel1et
+1i,
+
isop d
of cherry ! ‘‘ r
birch litter
—7 ’
+1
car ’tI. j.i
cherry 1itt . r
j ’r f j1 I.lLj I
+ 7
+73%
q . 1 b I 5 l ’ri .nt .tgt . asirta lily •f e ,l ).‘z ,,tio] .- ‘ ‘.i .1 carabi d
t1.’r 1(1 dayn wh ir 1 :Irayed wtlu C). % ‘,14,’,_ ’j’
.ir u.s:; .rz ye ’d w i hi c r w i t huu ridui I I i un of’
U) il. ?’’ 7) $ . j l ’u i i i
Wi ‘.h,uI. V... d riJdi t.j •.ia
— - -
wj $1,
l ’ uud
add.i tion
‘ ‘ .u ,i ’ .r u,i
. •,ll , ‘,_ J ’
u;iihr .l
,5—T
t. ’l I .-; ,iIu.ult.
I )
I j
1
; ‘) ,
eti”,I,ii
‘(
“ ,
u5
-
Figure 5: .‘, 1 4,5—T content (ppm) during a
cherry leaves and’ litter after
2,b,5—T ester
6 months r ’riod of timi ’ nf lle.ck
sprayii a O.7 solution of
I— -
bOO
2,4.5-1 content (ppm)
200’
l50 ’
b c ’
So’
Black cherry leaves
litter under shrubs
0 ‘ ‘ I -- I
200
l 50
I00
50
0 T 0
bsween shrubs
I I I I
1 2 3 4
Months
-------
The influence of feeding uncontaminated food upon the specimen’s
sensitivity was tested by comparing experiments in which after
spraying unsprayed food t ies added to the experiments described in 2.
From Table 5 it is clear t.hat with additior. of uncontaminated food the
mortality of collemboles and cay;iids is reduced. This reduction is
not caused by a lower mortality due to the absence of starvation,
as in the control experiments in which no food was added, the mortality
was very limited. Furthermore, tt experiment with collemboles was designed
in which in the centre of a moist soil substrate treated or untreated
food was added. With untreated food the springtai ls strongly preferred
the food area. After treatment of the food with 1.25% 2,4,5—T about
50% of the springtaiIs avoided the ood area initially, but on the
third day the numbers of springtails in the food area were about equal
to the numbers i -i the control experimentt.
4. Impact of varying en ironmertal conditions
The laboratory experiments described in the preccding sections were
conducted at a fixed temperature ( 1 5°C ), which is the mean litter
temperature in our fnrc’cts during and after the period of spraying
operations. The relative humidity was kept at 90% and the soil moisture
content was about 222. However, under natural conditions these
variables fluctuate locally and temporarily. Therefore, the effects
of variable moisture and temperature levels were investigated in
further detail.
In our direct obser vation experiments with a partly treated substrate
(par. 2) the field moisture fluctuations were imitated by treating
half of the moist substrate with a 2,4,5—T solution or with extra water.
In the control experiment all three experimental species had a slight
preference for the sprayed (wetter) part of the substrate (cf. Fig. 3).
When the suobtrate is sprayed partly with the same amount of an aqueous
solution of 2,4,5—T the preference is opposite; the repellent action
of 2,45—T decreases the preference for s moist substrate. An experiment
as also designed in which springtails were exposed to a dish with a
moist centre sprayed with 2,4,5—T, surrounded by a dry sand substrate.
During the experimental period of 17 cays all the collemboles stayed on
the dry substrate and about 25% of then died due to desiccation.
Soil temperature has a distinct diurnal rhythm. Therefore, an
p .
experiment was carried out in which collemboles were treated with
1.25% of 2,4,5—T and then placed in climate rooms with constant temperaturt
of 15 and 25°C, or with a temperature fluctuating between 15 0 C (night)
and 25°C (day). After 10 days the mottality percentage with a fluctuating
temperature was about the same as with constat.tly 25 °C; respectively
60 and 65%. 437
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However, at 15°C the mortality percentage was 45%. So obviously
in this experiment the limited periods of maximum temperature
determined the effect of the herbicide, whereas the mear. temperature
gives an underestimation of the possible effect of the herbicide.
Concluding remarks
One of the main problems in evaluating penticides effects in laboratory
experiments is the discrepancy between laboratory conditions and the
situation in the field. On the forest floor the—e is a patchy
disttibution of thc herbicide. Th!.s might enable soil animals to avoid
or withdraw from thc treated areas. However, the places ihere 2,4,5—T
drips on the forest flocir very likely will be tied with the places
where normally rain is dripping on the ground. The moisture content
viii be high at those places. These moisture patch provide optimal
conditions for isopod and collembole, in respect to food and su vival
(Den Boer 1961; Verhoef 1978). Therefore, the presence of 2,4,5—T will
be tied with the presence of food and moisture. Despite the repellent
action of 2,4,5—T, over a longer period the chances of getting into
contact with 2,4,5—T will therefore be high. Moreover, from these
results it can be concluded that the classical. LD 50 tests with a
continuous exposure to the pesticide give an overestimation of the
herbicide’s effect. Nevertheless, in an experimental set—up which
simulates the natural conditions to a greater extent, the herbicide
is still toxic for isopod, collembole and carabid at equal amounts which
occur in the forest floor.
It can be concluded from the experimencs with contaminated and
uncontaminated food that consumpticsn of Litter and prey contaminated
with 2,4,5-T during and ins ediately after spraying may cause harmful
effects on representative species of the soil fauna and consequently
it is expected that fragmentation processes performed by these soil
fauna species will become hampered. Treated cherry leaves which come
available for consumption after leaf—fall do no cause harmful effects.
Fragmentation of this litter is enhanced by spraying as well. The
consumption of uncontaminated food however, might decrease the herbicide
impact by direct contact, although mostly the chance of direct contact
will be tied with the presence of contaminated food. Although it would
be interesting to study these phenomena over a longer period of time,
it is questionable whether this will be possible in laboratory experiments.
because over a longer period there may occur significant aberrations
in food consumption as Van der Drift (1975) found with the millipede
Gl. meris marginata .
-------
Besides food, the temperature and moisture fluctations in the forest
litter may influence the amount of effect.
From our results and observations it is concluded that vari le or
varying environmental conditions do not diminish the toxic effects of
the herbicide. Fluctuating temperatures may reinforce the herbicide’s
effects, whereas the repellent action of the herbicide may retain soil.
animals on a dry area of the soil substrate and so increase the chance
of fatal desiccation. A temperature increase will promote the
mobility of the animals, and so the chances 10 get into contact with
2,4,5—T. Moreover a higher temp rature will, increase the animal’s
metabolism resulting into r .i ,ed ingestion of 2,4,5—T, but also an
increased bTeakdown.
Without being able to asesq fully the effects of all these processes,
it is clear that the irtegular distribution of animals, food, TmoisLure
and pesticide on the forest floor as well as temperature fluctuations
have to be incorporated in risk assessment procedu es. However, in
deve.oping laboratory tests for risk assessment of De3ticides and other
contaminants with respect to the soil fauna, it is questionable to what
extent it is worthwhile to complicate experiments iii order
to approach natural conditions as much as possible. Moreover, it is
questionable wtether it is of interest to predict exactly the amount of
effect of the herbicide under mean constant conditions or to assess
roughly the possible toxic effects under extreme conditions. From the
experiments described above it has been made reasonable that in the
testing prograzz s these extreme conditions have to get more attention.
This has to be accompanied by a thorough analysis of the niche parameters
of the soil fauna sp cies under study in order to get laboratory experiments
which are suitable for assessment of toxic effects of pesticides on the
soil Fauna.
Acknowledgements
Thanks are due to Drs. D. Barel, P. Botterweg and P. Doe]jnan for
their con ment on the mar’.iscript. Mrs. E. de Ruiter-Djjkman carrir:d
out the 2,Ii,5—T analyses, Mr. G. Hei .jmans was of great help with
the exper ments. The figures vtre prepared by H. Jacobs, M. ‘Hombouts
and. R. van Beek, the manuscript was typed by H. de Gast and b. Sop1 nit.
14.39
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heferoncen
hoer P.. ] . den ( 1{)61 ) The coi g “tj s F: jfjeatic f ar’ i v y i . . r’
i i i I 1 r wr ’otjI c’us,’ Porcci..Lic. sca: t r jntr. lsnj ...‘ia. Ar’ h. • .
• li i, Rig — sO
rir’ J. van ‘tar (l’i(5): T ue :t;r1 ’ . t.r . iif’ ti’ ni ilip. 1 ‘ .ir r’:-
rnrg uath ( “ill n ) for oaV—Li’ I r .fer. m;’ ..-.i ic ’’ :a’irj rig. c i : - .
f it part H ruergy flow.
In J. Vanek cd.: F’rogresc ; ;..H . ‘ 1 gy. lrje. ‘I ]‘. .
— . 1 r 7 J %. 1 7 : —
Yijsa.’Pr’rr; Ii. ( Iui 1 ): CiJ’ • ‘rr ’ r .1 i i ‘ri •
repro.ttction, foo.l consumption, arid mnui .ir.g c’f tL€ ‘pringlail
‘ inychiurus quadriocellatus Gisin (coli’-jnu’ola). Z. arig. Ent. ti’. 1l.1 — t”).
Eijsackers H. (197 %): Side effects •f the v.ri.ividr. 2,h,5—T aff.’rtiig
the carat’id Notiophilus biguttatus Fal’r., a prcdatc.r nf spriii,;taiir.
Z. ang. Ent. 86, 113—128.
Eijsackers H. (tn i8c): Sid° effects nf thr ti rt’iide c’,h,5—T affiartirig
mcciiity and mortaiity of th° springtai] Onyctiturur guairiccc llat”r
Gisin (Cciilenboln). Z. ng. Ent. 86, 3li9— 72.
Eijsa:kers I i. (1978d): fide effects of thø herbicide 2, 1 ,S-T aff e t. ing th e-
i zopod : , it’ IC I ct rJj: ’ ’ruxri V• opoI i . Z. — . • . 8j, _
!louten J.G. ten ar.d M• Xrafl (1’) IM): A t’ertieal spraying a rara’uc fey
th” lai .orat ry e eiuatior 9 of’ at] tyrr.n c i ’ liquid pcist ecn ’r ,1 q
A • - ;. p: —..
Terst N .‘r . 1 .. ( piT h): flrg:i’iat i i’.q O1 :, —ii 1 . p11 P4 li •
p 1t. Env I rnr,m r’ t tj l Qun lii y it ‘ y • Ni; :‘i r. r t V t’ . wn” 1T . . • —
Verhcrf H. (1978): An ecriogica] study on water relations jr C&Iirmbnlo,
Thesis Fre t!rivnrsty of Amst rdam. Il l
‘SO
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EFFECTS OF DRAINAGE UPON THE SPIDER FAUNA
(ARANEAE) OF THE GROUND LAYER ON MIRES
Seppo Koponen
Uniptrqgy of Ti ,rku
Finland
INTRODUCT ION
The proportion of peatlands, mires, has been high in
northern Europe, but intensive human activity has changed
the situation. In Fin]and, for example, about half of the
peatland area has now been ditched, mainly for forestry but
also for agriculture and peat industry. The mires, once typi-
cal and common habitats, are n’ wadays one of the ecosystems
undergoing greatest changes in northern Europe.
In the present paper, the effect of drainage upon
spiders on Sphagnum mires is discussed, and comments are
of fared on the usability of the spider fauna data for moni-
toring the situation of mire habitats.
STUDY AREAS, MATERIAL, AND METHODS
Bog Karevanrahka is situated near Turku, southwestern
Finland, and bog Vissmosse near Hörby, southernmost Sweden.
The study habitats at Karevanrahka were three natural sites
with Sphagnum (an Alnus swamp, a Phraqmites fen, a Calluna
peat bog) and a peat harvesting area. This man—made site
consisted of dry peat isthmuses without Sphagnum . The har-
vesting area was a Calluna peat bog before human activity.
There were 10 pitfall traps in each site at Karevanrahka
from April to September. At Vissmosse, the study included a
natural Eriophorum-Ca11una- phagnum bog and a dried part of
the bog, now a Calluna-Cladonia site (without Sphagnun ).
There were 20 t From May to October. The material con-
sisted of 1207 identifiable spider specimens from Karevan-
rahka and 2146 from Vissinosse.
RESULTS AND DISCUSSION
At Karevanrahka, the number of species and individuals
was highest in the Phraqinites fen, but no clear difference
was found between sites. The lo iest Shannon index was observ-
ed in the mafl—made site, but differences in diversity were also
4 l
-------
small (Table 1). At Vissmosse, the species and individual num-
bers were higher in the dried site. This was probably due to
the fact that both hygrophilous (r a1 rnire species) and xero-
philous spiders occurred in the material. The diversity of
spider fauna in the dried part of the bog was smaller than in
the natural part (Table 2).
TABLE 1. Structure of spider fauna at Karevanrahka
Alnus Phraqmites Callun Harvesting area
Species number 38 48 36 37
md. number 226 355 338 388
Shannon index 2.76 2.98 2.85 2.57
TABLE 2. Structure cf spider fauna at Vissrnusse
natural bog site dried bog site
Species number 5)4 62
md .. number 728 1418
Shannon index 3.11 2.80
The proportion of small soil ( Sphagnum ) dwelling spiders
was decreasing after the drainage: e.g., 48% of individuals in
th natural site were linyphids as against 21% in the dried site
at Vissmosse. Xerophilous lycosids and gnapho ids became more
dominant in the human—influenced sites: Xerolycosa nemoralis
(Westring) 36% o individuals at Karevanrahka, and Pardosa nigri-
ceps (Thorell) 23% ar.d Cnaphosa leporina CL. Koch) 15% at Viss—
mosse. The diversity of spider faunas has sometimes been used as
an indicator of the situation of habitats (Uetz, 1975). In the
present material, t o clear difference was found in diversity
between natural and man—made sites. However, the man—made sites
were rather old (10 to 15 years), and their fauna may thus have
reached a stable situation. As the epigeic fauna (pitfall trap
material) changes rapidly after environmental changes (Huhta,
1971), the diversity may be more useful indicator immediately
after the habitat has changed.
There were typical abundant species in each site. At Kare—
vanrahka these included Pirata hygr phi1us Thorell, Bathyphantes
parvulus (Westring), and Wideria melanocephala (0. P.-Cambridge)
in the Alnus swamp; Pirata insularis Ernerton and Maro ] p .dus
Casemir in the Fhraq,nites fen; Pardosa hyperborea (Thorell) and
Scotlna palliardi (L. Koch) in the Calluna neat bog; and Xero-
lycosa nemoralis and Pardosa lugubris (Walckenaer) in the har-
vesting area. At Viesmosse, typical species in the natural stte
included Pirata uliginosus (Thorell), LepthyDhantes ericaeus
(Blackwall), and L. cristatus (Merige), and in the dried bog site
Gnaphosa lepor..na and Neioneta affinis (Kulczynski).
-------
Certain dominant species could perhaps be used for moni-
toring the situation of mire habitats (Koponer, 1979). Such
indicator species of a site could be Pirata hygrophiius, P. in-
sularis, Pardosa hyDerborea and Xerolycosa nemoralis at Karevan—
rahka, and Pirata uliginosus and Gnaphosa leporina at Vissmosse
(Tables 3—4).
TABLE 3. Rank order of certain abundant species at Karevanrahka
rank in
Alnus Phragmites Calluna Harvesting area
Pirata hygrophilus 1 - -
Bat yphantes parvu].us 2 45 31 13
Wideria melanocepha].a 9 - —
Maro lepidus 21 5
Pirata insularis - 6
rardosa hyperborea 8 1 26
Scotina palliardj 28 7 —
Xerolycosa nemoralis 1
Pardosa lugubrjs 18 2
TABLE 4. Rank order of certain abundant species at Vissmosse
rank in
natur 1 }. I t’ dried bog site
Pirata uliginosus - 10
Lepthypiiintes ericaeus 40
L. cristatus 7
Gnaphosa l porina 2
Meloneta affinis 8
LITERA’T’UR CITED
Huhtr . V. 1971. Succession in spider communities of the forest
fl ”r after 1 ar—cutting and prescribed burning. — Ann. Zool.
Feri i i 3, 453—542.
I • c’i, S. 1979. Differences of spider fauna in natural and man—
habitats in a raised bog. - National Swedish Environment
i rotection Board, Rep. PM 1151, 104—108.
Uetz, G. W. 1975. Temporal and spatial variation in species diver-
sity of wandering spiders in deciduous forest litter. — Envir.
Ent. 4, 719—724.
1443
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STUDIES ON REQUIREMENTS AND POSSIBILITIES OF ZOO-
AMELIORATION OF AFFORES 1 ED ARABLE LAND
Andrzej Szujecki, Stanislaw Mazur. Jan Szyszko. Stanislaw Perlinski and Henryk Tracz
Warsaw Ag,Icuthiral University
Poland
Results of the first stage of our investigations.
presented at the Sixth International Soil Zoology Colloquium
in Uppeala (Szujecki 1977), defined the requirements of
forest soil macrofaunal reestablished on afforested arable
land. The search for the right d3rections of soil fauna
reestablishment on aforested arable land was preceded by
studies of biological characteristics of afforested arable
soils; in comparison with forest soils. afforested arable
land, it was found, inhibited the development and the func-
tioning c.E the reestablished forest ecosystems. These bio-
indicative features included the following:
1. Concentration of macrofauna and its activity in surface
soi] layers
2. High mobility of epigeic fauna
3. Occurrence of xerothermophile forms
4. Too small proportion of saprophages in soil fauna, as
compared with phytophages arid predators
5. Low average biomass of the specimens and low level of
biomass of total macro.Eauna
6. High average b:cmass of specimens in pcpulations of
epigeic species (this is characteristic of poor habitats
and pioneering succession stages)
7. High proportion of the spring type Carabidae species of
short life cycle and high maintenance cost
8. Changes in sexual index of Carabidae population charac—
ter stic of poor habitats..
The enumerated characteritic features of inacrofauna are
reEponsible for the limitation of the circulation of elements
(especially organic carbon and nitrogen) into the litter
layer, for the acceleration of circulation, and for signif-
icant losses of energy connectec with higher maintenance cost
of soil macrofAuna r- afforested land. Analyses of soils,
especially analysis of fractionated humus parts confirmeU
these findings, thus substantiating the thesis of different
circulations of elements on afforested arab].e and on forest land.
-------
The purpose of zooamelioratiort measures would be to
reestablish the forest soil fauna. Such re—establishment
uould control the circulation of biogenes, it would effect
penetration of the circulation into the deeper layers of
soil and reduction of faunal maintenance cost, int’ nsifj-
cation of humifying processes, and acceleration of succes—
processes. Sapro hages were assigned the major role
in zooamelioration procedures. They essentially affect
I’umus formation and improvement of physical properties of
50i1 and are deficient in young cultures and stanc ’; on
afforested arable soils. It did not seem rationaL to intro-
duce t e organisms of higher trophic levels of zoocenoses
into the existing systems. These animals wc ,uld have in-
sured the transfer of matter in ecosystems of afforested
land without providing a nutritional basis. It was, there-
fore, assumed justified to accept, as a pri; ciple of zoo—
amelioration me.agures, some preliminary phytoamelioration
treatment, e.g. introduction of Washington Lupine, wild-
blackberry, spruce undergrowth, or introduction of some
organic bulk of slow decomposition rate, such as fragmented
pine bark or sawdust. These measures were designed to
facilitate the introduction of some species of saprophage
animals into afforested arable land, e.g. Nopoiulus fuscus
Am. Stein, Diplopoda, or to ensure protection of local
saprophaqes.
A possibility of r’ ducing the impact of predators on
soil saprophages was al .. examined; this was assumed to be
achieved through a change of the compounds of exploiting or
competitive character that occur in various layers of forest
floor, both litter and mine.r. l soil. Artificial colonization
of Formica predator species was to serve the purpose. In
order to accumulate more lcnowledge on the possibilities of
controlling the changes occurring in soil macrofauna concen-
trations, the effect of various kinds of soil preparation
to afforestat ..on was studied. By distributing tl e designed
phytoameltoration procedures wtthin growth J nes of forest
stands on afforeste arable land diversd effects were obtained
which changed the present—day systems in communities of soil
mactofauna.
Arable soil may be prepared for af fore station by em-
ploying various kinds of cultivation. Among the various
ways of ploughing, e.g. striped, shallow total, and deep
total, the latter produces the greatest changes in macrofauna.
The negative effect of deep ploughing upon reestablis lmtent
procesze.; of communities of forest macrofauna manifests itself
-------
through preference fcr xerothexinophile, eurytope. and hemi—
zoophage forms, through an increase of the degree of synan—
throphization in this habitat, and it also leads to retarda-
tion of the succession process. Thus, striped loughing
seems to be most recommendable.
The introduction, at the same time, of bark, and
c specially of pine sawdust ca ises a reduction of macrofauna
occurrence already after two years; it is only Chilopoda
and Lumbricidae that sho z increased density which is the
highest in areas fertilized with bark in the amount 270 m 3 /ha.
The use of a mixture of lAO in 3 bark and 90 in 3 sawdust per
1 ha reduces the density of macrofauna to 60%. compared with
the control plot. The application of sawdust at only 180 in 3 /ha
reduces macrofauna to 35%. A quantitatively significant de-
crease occurs among phytophagea, as their density in relation
to growth inhibition of weeds is five times lower than that
on non-fertilized plots.
Both surface phytophages and eudaphic Selatosomus larvae
(characteristic of fallow and first successional stages of
afforested land) suffer this 1imit tion. Also Carabidae
undergo limitation. whereas the population of Staphylinidae
is significant. On areas fertilized only with bark the
density of saprophagic Diptera larvae undergoes reduction.
Thus phytophage which depend upon an optimal nutritional
basis, and mobile species of zoophages respond most readily
to the treatment of bark and bark with sawdust. The intro-
duced organic matter exerts influence on ] ocal saprophages
in a variety of ways, but it certainly allows the introduction
of species not occurring in young afforested areas, e.g.
Nopoiulus fuscus - a species characteristic of the yourLgest
pine stands in Poland. As a saprophage and a niicophags it
has a fairly wide trophic spectr .mt whose component is also
pine bark ifl various degrees of decomposition. Discharged
excrements of this creature (in young forests, on average
16 • 6 kg/ha dry iaatter annually) contain organic matter and
are deposited in various parts of soil profile, thus enriching
the soil with easily decomposable compounds. In addition,
they become a place of vital activity of microorganisms.
A limitation of the degree of nechanical cultivation of
soil and the introduction of fragmented pine bark with an
addition of sawdust creates a possibility that inhibits
mineralization processes characteristic of afforested arable
land. This procedure seems to be advantageous, since nutri—
44e6
-------
tional requirements of young pine forests is not high at this
stage. Conditions are created for the development of sapro-
phagic fauna favourable for humification processes typical of
forest soils. D velopinent of this fauna is favoured, for
example, by preceding the treatment described above witn a
crop of Washington Lupine on arable s3ils designed for af for-
estation. The introduction of wild blackberry into afforested
pine stands (which should be done, optimal].y, between 10-40
years of age of a forest stand) increases the density and bio—
mass of macrofauna, especially of facultative saprophages
and soil zoophages, and limits mobility of the latter. Nore-
over, this kind of treatment raises the level of macrofauna
in deeper layers of soil (depth 10-20 cm) which supposedly
may cause the deeper distribution of organic carbon and nitro-
gen in soil profile, as well as circulation of these elements
between litter and mineral soil.
The introduction of deciduous undergrowth creates great
possibilities of influencing soil of pure pine forest stands.
However, this kind of treatment is practically impossible when
the population of fallow-deer is high. Hence, in some affor-
ested lands of North—West Poland, pine is introduced together
with common spruce which produces forest stands with rich under-
growth. In 45—year old forest stands spruce undergrowth exerted
a limitiflg influence on the whole macrofauna and showed pre-
ference for species characteristic of earlier succession stages
of macrofauna. The spruce undergrowth is not reconanended as
the one favouring restitution processes of forest fauna.
The last procedure of zooamelioration possible in all
age groups of afforested arabie land is an artificial intro-
duction of ! rmica ants. The influence of ants upon other
soil fauna depends on the ants species and the species of prey
animals. First of all, it was observed that increase of
inacrofauna density depends on distance of its occurrence from
ants nests. The litter—soil macrofauna is the most limited
by Formica polvctena , and to a smaller degree by ! mica rufa .
Impact of . pratensis is more differentiated 8patially arid
thus more difficult to define. It is mainly directed to small
phytophages and to small litter zoophages, whereas . polyctena
mainly limits saprophages and F. rufa a different food group
the zoophages. The dominant species of macrofauna are the
most strongly limited. Furthermore, it was observed that sinai]
ants ( Tetramorium, Myrmica ) are more numerous in the neighbour-
hood of ant—nests of Formica species in the soil layer, where-
as on the surface of the forest floor mobility of these insects
4 e7
-------
increas with the distance from For . ij a t—nests.
Results of investigations on justification of using
the larger ants to control trophic levels in communities of
soil macrofauna do not indicate that representatives of
Formica species would influence an increase of population
density of big saprophages in litter or mineral soil by
limiting the population of epigeic predators such as Carabidae.
Within the area of the ants’ influence their impact on macro—
fauna is of a total character. Soil saprophages are also
subject to their influence: at adult stage they become victims
of species of Formica genus. It may be assumed that in the
presence of ants there occu a change of one group of non-
specialized predators into another. In addition to what has
been said above, the range of ants, even those artificially
co]onized, is too small in relation to the area of a forest
stand to expect that their presence would radically change
biological activity in the Ap accumulation horizon.
However, the knowledge of structure and function of
forest biocenoses is too scanty to state that the discussed
studies of trophic and competition interrelationship of soil
and epigeic macrofaunia have exhausted all the possibilities
of ants use for zooamelioration purposes. On account of
specific differentiation of Formica species, the distribution
of various taxa of macrofauna seems to indicate that the
presence of this group of insects favourably affects multi-
plication of directions of dry matter transfer in poorly
differentiated habitats such as newly afforested lands. The
complexity of the natter circulation may, in turn, exert a
stabilizing influence on the functioning of these ecological
systems.
It can 1.e concluded that, although the processes of
macrofauna communities restablishment and shaping of spatial
and time structures of its numerous functional groups are
long—term processes, there seem to exist high possibilities
of their controlling and accelerating adequate technical
procedures, including zooan elioration ones. The purpose of
such activity would be to create conditions for correct
circulation of biogenes in the environment of afforested
arable land throughout the whole life cycle of new forest.
An additional aspect of the phyto- and zooamelioration
measures discussed cibove are the enrichment and activation
of microorganisms, including the species antagonism to root
polypores and creating the conditions for the occurrence of
ruimerous valuable compounds of forest entomocenosis connected
-------
with wild blackberry. The production of ecological systems
similar to those in forest sites would mark a significant
progress on the way to reestablishment of natural habitats
on afforested arable land; this would not, however solve
the ecological problems which accompany total clearing of
pine stands.
LITERATURE CITED
Szujecki, A.7., J. Szyszko, S. Mazur and S. Perlinski. 1977.
Changes in the structure of macrofauna communities on
afforested arable land. Pages 580-584 j U.Lohm and
T Persson. Soil Organisms as Components o Ecosystems.
EcoL. Bull. (Stockholm) vol. 25.
4 9
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EFFECTS OF FIRE ON SOIL FAUNA IN NORTH AMERICA
‘Louis J. Metz and “Daniel L. Dindal
U.5 Fonw 5.’rt’.cc
“SUNY CESF
USA
INTRODUCTION
In forest soils the vast majority of the invertebrates live in
the surface organic layers, or forest floor. This floor, consisting
primarily of leafy material from the trees, is divided into three
layers. From the surface down these are: the L (litter) layer -
recently fallen material still Intact; the (fennentation) layer -
broken and partially decomposed material; and the II (humus) layer -
material so far decomposed that its origin is not evident. Of these
layers, the L, which is loose in structure and thus usually quite
dry, affords t he most inhospitable envirov nent In the floor for in-
vertebrates and few are found there. The lower layers, toward the
mineral soil, are more covpact and moist, and many animals are found
in these F and H layers, e3peclally the latter which lies directly
above the mineral soil. In the mineral soil the density of animals de-
creases with depth from the surface. The vertical distribution o’
mites and collembolans can be Illustrated from data collected in a
loblolly pine ( Pinus taeda L.) forest in the Southeastern united
States (tletz and FarrIer , 1973). The percentages of these animals In
the 1, F, and H organic layers and the 0—1, 1—2, and 2-3 cm of mineral
soil were 2, 34, 48, 9, 4, and 3, respectIvely.
The forest floor is involved In all forest fires and In fact
practically all fires begin In this part of the forest. There are
two general types of forest fires. WI1J fires are caused by man, un-
intentionally or maliciously, and by lightnIng. Prescribed fires are
those set by man to achieve a cettain purpose — create a seedbed for
a nev generation of trees, kill young trees of certain species which
are not wanted In the forest, or to reduce the fuel so that if a wild
fire occurs there will be less blonass In the forest to burn and thus
damage will be kept to a minimum. Since prescribed fires are care-
fully controlled by man they are often called controlled fires. The
control consists of having fire lanes around the area to be burned,
burning when the wind and humidity are just right, and when the
moisture conter t of the floor Is such that only part of It will burn.
Since fire is relatively economical procedure for achieving certain
desired objectives in the forest It Is being used more and more In
the USA. Of course, if standards for aIr and water quality cannot be
met, its use may decrease in the future.
Any fire In the forest Is going to kill some soil Invertebrates.
The extent of damage is related directly to the amount of heat gener-
11.50
-------
ated. In addition to killing animals directly and indirectly, fire
changes the coninunity structure. A fire severe enough to consw ie
most of the forest floor can produce a food shortage for carnivorous
as well as phytophagous animals.
Wlldflres often occur when the forest floor is dry. Under
these conditions the floor is completely reduced to ashes and all thc
Invertebrates in the floor, except those that fly away, ar killed.
Since much heat is generated under such conditions, many of the
animals in the surface layers of the mineral soil are also killed.
A well executed fire consumes only the surface layer of
needles and leaves; that is, the L and part of the F layer. Since
most 1.,vertebrates inhabit deeper, wetter layers, rel3tively few are
killed.
Effects of fire on the forest ecosystem have been studied for
many years, but most effort has been concerned with the vegetation,
primarily trees. Although work on fire and the soil fauna has been in
progress for some tIme, there is still a paucity of research results.
REVIEW OF SPECIFIC RESEARCH
Some work has been done with various insects that spend but a
part of their life cycle in th forest floor or mineral soil.
Fires in Australia 1 both prescribed and wild, reduce the popu-
lations of stick insects (piasmatlds) to a very low level if the forest
floor is completely consumed. Both nymphal and adult stages are
affected, and the burning has a long tenn depressing effect on popula-
tions (Campbell, 1961). Beetle populations In an area of shrub steppe
vegetation In southeastern Washington that had been burned by a wild-
fire were examined and compared with the populations of an unburned
area. Of the four species studied, all were found In both areas, but
the populations of two species were significantly reduced by burning
(Rickard, 1970).
The effect of buring 0.4 ha (1—acre) plots on the invertebrate
component of grassland in Ohio was brief, and populations were back to
normal in 3 months. Sampling was done by the vacuum method, and so few
soil fauna species were involveci (Bulan and Barrett, 1971). In a study
of this type, small plots and the mobility of the Insects sampled could
have masked the effects of the burning. Beetle populations in Florida
pine forests that had been burned annually were compared to those in
grass that had not been burned for 10 or more years. Of the total
number of carabids trapped, 85 percent were taken in the unburned plots
(Harris and Whltcomb, 1974). In New Jersey, the distribution of the
periodical cicadas ( gicicada spp.) was studied in 1902 and in 1970.
In the 1970 study, the insects had disappeared from many of the loca-
tions where they were found earlier. Disappearance was attributed to
destrjctjon of forests, forest fires, and urbanization (Schmitt, 1974).
kji
-------
— — - — ----. — I C -
Prescr’bed fire can be used as a sanitation measure In the forest
(Miller 1978). The red pine cone beetle ( Conaphthorus resinosue
Hopkins) destroys the cones of red pine ( Pinus resinosa Al t.) and
greatly reduces seed production. The adults of the beetles spend the
winter months in the forest floor and burning during this period
greatly reduced or eliminated the damage caused by the Insect. In
Michigan the maple leaf cutter ( Paraclmnemsla acerifoliella (Fitch))
reduces the leaf area of sugar maple ( Acer saccharum Marsh) and thus
causes a decr ce in flow of the sap used in maple syrup production.
Preccrlbed fire kills the pupae while they are In the forest floor.
Pupal mortal ity was nearly 90 percent and was higher than hemlcal con-
trol percentage obtained by other workers using Carbaryl (Simons et
al. 1977).
For what might be called the ‘true soil fauna”, that is, those
animals which spend nearly all 0 f their lives In the organic or miner-
al soil layers, practically all studies show the animals are decreased
In nunber by fire. These findings are world wide as evidenced by work
In many countries outside the USA.
In Austria, mites, the most comnon soil organisms collected,
were less abundant In burned areas (Jahn and Schlmltschek, 1950). In
the coniferous forest of northern Sweder more mites were found in un-
burned than burned forest floor, but the .uthor ascribed the difference
to normal variation In their population (Forsslund, 1951).
In Finland, clearcutting forests that had a thick raw humus
layer and thea burning the areas a year later greatly reduced the popu-
lation of oribatid mites. Five years after the burn the oribatids
still showed no sign of recovery (tCarpplnen, 1975; Huhta et al., 1967,
1969). After wildflres swept through Pinus radiata plantations in
Australia, the soil fauna were exam1neT sltes that had been lightly
and severely burned. The populations In the severely burned areas
were lower than In lightly burned areas (French and
Kelrle, 1969). In Canada, the density of soil fauna was found to be
decreased in both the forest floor and surface 5 In. of mineral soil
2 years after a slash burn (Viug and Borc’en, 1973). “Fuel re-
duction fires” of even low intensity irr Australian dry forests caused
substantial mortality of soil fauna in both the forest floor and
surface soil. Or these sites it was estimated that It would take from
2 to 6 years for the fauna populations to return to a prefire level
(Leonard, 1977).
A prescribed fire In western Australia (Sornmnlssza, 1969) elm-
mated all organisms from the forest floor and 85 percent In the upper
5 cm of mineral soil. Two o’ three years after the fire the Insect
fauna recovered fully, but mites, especially oribatlis, requIred 4 or
5 years for populations to return to normal. The influence of pre-
scribed burning on soil fauna under two species of Euca]yp ti was
studied In Australia (Springett, 1976). The unburned plots h d 6 times
the number of animals per unit area, and 1 .5 tImes the number 3?
species, when compared to the burned plots. Only large animals such
as spiders, pill bugs, and millipedes, which could be identified with—
L .52
-------
- -—- - — - - -.-—- -- - -— - - -- - --
out magnification were tabulated. The author also states that a de-
crease in the number of species and population density was still
evident at the end of the prescribed burning rotation, presumably
5 to 7 years, but presents no data on the subject. In burned and
unburned Australian eucalypt forests, ant fauna were intensively
studied (Majer, 1978) Animals were collected in pitfall traps.
Even though mc ’e ants were collected on the unburned than on the
burned plots Majer found that both areas were “characterized by a
high ant species richness and moderate ant equitability”.
Earliest work 4 n the USA on effects of fire on soil fauna was
done in the longleaf pine ( Pinus palustris Mill.) region of the
South (Ileyward and Tlssot, 1936). Stands that had been protected
from fire for at least ‘0 years were compared with stands on similar
soils that hac’ been burned frequently. In this study, the larger
animals were sorted by hand and the smaller ones were extracted
with funnels. Although no statistical tests were made it was ob-
vious, from the large differences found, that fire depletes the
fauna.
An indirect estimate was made of the larger fauna by count-
ing holes at least 1.27 cm (1/2 in.) in diameter on numerous spots
on each study. This was done clearing away all organic material
and exposing the mineral soil. In general about 10 tImes as many
holes were noted on the nonburned plots as on the burned ones, and
these holes were attributed to beetles and small mammals. Iloles
smaller than 1/2 in. were Ignored because many were disturbed when
the organic layers were removed and it was felt the count would be
inaccurate. Five times as many animals ranging in size from mites
to millipedes were found in the organic layer on the nonburned plots
and 11 times as many in the surface 5.08 cm (2 in.) of mineral soil
as on the burned plots. Of the animals counted, about 85 percent
were mites or collembolans.
From 1937 throuah 1941, a stand of loblolly pine in North
Carolina was burned each year, and an adjacent stand of trees, not
burned, was used as a control (Pearse, 1943). Area samples coi,eri ng
3.25 sq. m. (36 sq. ft) were taken, and the material was sorted by
hand and identified with no magr.if lcatlon. The control plot con-
tained about 3 times as many animals as the burned one. In both
plots, ants made up over half of the animals collected.
Prairie fires in Illinois reduced the popu1at1on of both soil
fauna and surface Insects (Rice. 1932). As In some other studies,
ants were often found in greater numbers on burned than on unburned
areas.
About a year after a major fire swept through the Pine Barrens
of New Jersey, burned and nonburned sites were sampled for soil fauna
(Buffington, 1967). AnImals were separated from the substrate in
liquid and no magnification was used - hence mites, collembolans and
similar sized animals were not counted. Bufflngton found that both num-
bers of taxa and numbers of Individuals were s Igni fi cantly less in the burned
453
-------
over rec. Our further evaluation of his data shovs that fire usually
caused reduct1 ns In the Indices of coi nunity structures of macro-
arthropods of the Pine Barrens (Table I).
TABLE 1. DetaIl of coninuni
from the New Jers
burned sites (Cal
1967)
ty structure* of m€ croarthropods
ey Pine Barren, burned and un-
culated from data of Buffington
H’ rm
Species Species Species
Diversity Richness Eçuita-
(loge) (loge) bility
Total macroarth opods
Unburned
Burned
2.3730 6.1865 .6309
2.0464 4.4428 .6209
Ants
Unburned
Burned
2.0429 1.9352 .7741
1.8593 2.5813 .6702
Spiders
Unburned
Burned
2.0885 2.8237 .9509
.6932 1 .4427 1 .0000
*HI (after Shannc’ and Weaver, 1963). rma (after Margalef. 1958).
J’ (after Pielou, 1969)
Species diversity, richness and equitability (with one exception) were
all lower In burned areas. Most of the change in diversity was caused
by reduction of the richness component; equitability, as the other
component of diversity, was affected very little by fire. Ants appeared
to be least severely affected, wIth 2 species, Formica fusca 1 . and
Leptothorax r ande1 Emery, appearing wore abundant in the burned
than In the u burned areas. About 95 percent of the organisms
collected were ai’ts.
The coninunity structure of soil microarthropods (e.g.. mites and
collembolans) from the New Jersey Pine Barrens also reflected the
effects of fire frequency of the sites they inhabit (DIndal, 1979). Six
vegetative sites with various histories of burning were sampled and three
Indicles of the coninunity structure of mlcroarthrcpods were determined
(Figure 1). Group diversity was highest In the pitch pine lowlands and
1e54
-------
A
L0W UATURAL. (MODEJUIZE6uWIrI,
FIRE I 1.1I&%I M0Vc. AT
FRE UENCV SUBSTRATE- SOIL CROWJ1 120-40
, IPg a 5 ,p 4Y 5&oo
FIgure 1 • Indicies of coninunity structure of soil microarthropods of
the New Jersey Pine- Barrens: A) Group (order—suborder) Diversity.
B Group Richness, C) Group Equitability
the hardwood swamps which have the lowest frequency of ground-soil sub-
strate fire (Figure lA). Also In agreement with earlier findings of
Metz and Dindal (1975), diversIty was least In sites burned annually.
Considering Figure lB and C. group richness, in general, appeared to
be the most Important component deterining the relative diversity
levels. WI !h the exception of annual burn sites, group equitability
I
,I3
I-I
2
I-
0
.9
B,
-7
3
I I
-9
R I
0
2
%1%
RI
2
fl
C
S
b
1 f55
-------
remained a rather constant diversity component, changing very little
from site to site.
That the effect of fire is often transitory on soil fauna
populations is evident from work In northern Idaho (Fellin and Kennedy,
1972). They sampled prescribed burns 1, 2, and 3 years old and found
that 2 yr and 3 yr old burns had 2.3 and 7.7 times, respectively, as
many animals as the 1 yr old burns. Most of the animals recovered
were Coleoptera.
The Influence of prescribed burning on nmnatode populations was
studied In the pine forests of Louisiana (Harrison and Murad, 1972).
One plot had been burned annually sinc 1915 and the control had rot
been burned since 1912. It was found that the total nmnatode popula-
tions differed significantly between the plots. The unburned one
yielded significantly greater numbers of larvae and total populations
in 17 of the 24 inos they sampled. No significant difference between
plots was noted for adults.
Mesofauna were scudled in loblolly pine 1i he Southeastern
Coastal Plain of the United States on unburned, annually bur’ied, and
periodically burned plots (Metz and Farrier, 1973). The latter are
burned every 4 or S yrs which is the general practice for prescribed
burning In the South. The v,umber of animals recovered from the un-
burned and periodic burned areas did not differ significantly but they
both had significantly more animals than did the annually burned areas.
Since the periodic plots were sampled about 4 yrs after belng burned
this period indicates the time it takes for them to recover. Of the
animals collected in the above study 83 percent were mites and 11 per-
cent were colleubolans. Since taxonx y work on cnllenbolans is further
along than mite taxonomy it was decided O further analyze the results
of the above for the collembolans at the species level (Metz and Dindal.
1975; Dlndal and Metz, 1978). We found chat burning, both annual and
periodic, increases the species diversity of the collembolans in the
F-H, the (i-i, and 1-2 cm layers. We also found that the general
Lepidocyrtus and Tullbergla are represented on all sites and are gen-
erally associatediiith each other or with burned site conditions.
Perhaps the differences In species that are found in these two genera
‘re indicative of similar niches being filled under slightly different
nil crohabitat conditions.
Not only are Individual Collanbolan species sensitive or tolerant
to the action of fire, but also interspecific assocIations exhibit like
sensitivities and tolerances. Comparing responses 1’om the control to
the most stressed site, there are reductions in th’! frequency of nega-
tive interspecific associations ranging from 36 percent to 0. Although
the numerical complexity and number of associations are reduced by
periodic burning some semblance of order within the conmu nity Is re-
tained. However, major reductions, as seen on annual burn sites.
could have dramatic effects on negativo feedback loops and coninunity
stability. Therefore, it appears that fire can cause shifts for and
against certain species and associations of Collenibola, thus modly-
Ing their total coninunity structures (Dindal and Metz, 1977).
456
-------
Apparently, moderate use of fire, such as prescribed burning
every 4 or 5 yrs, does nct pennanently damage the soil fauna. The
great recuperative powers of these animals seen to overcome such
temporary setbacks.
LITERATURE CITED
Bornemissza, G.F. 1969. The reinvasion of burnt woodland areas by
Insects and mites. Proc. Ecol. Soc. Aust. 4:138.
Buffington, J.D. 1967. Soil arthropod populations of the New Jersey
pine barrens as affected by fire. Entomol. Soc. Am.
60: 530-535.
Bulan, C.A. and G.W. Barrett. 1971. The effects of two acute
stresses on the arthropod component of an experimental grass-
land ecosystem. Ecology 52: 597-605.
Campbell, K.G. 1961. The effects of forest fires on three species of
stick Insects (Phasinatidae: Phasmatodea). Lint,. Soc. N.S.W.
Proc. 86:112-121.
Dindal, D.L. 1979. Soil arthropod microconinunities of the Pine
Barrens. Pages 527-539 in R.T.T. Forman (ed.). Pine Barrens-
Ecosystems and Landscapes. AcademIc Press, NY.
Dindal, D.I.. and L.J. t4etz. 1977. CommunIty structure of Collembola
affected by fire frequency. Pages 88-95 in W.J. Mattson (ed.).
The role of arthropods in forest ecosystems.
Fellin, D.G. and P.C. Kennedy. 1972. Abundance of artnropods in-
habiting duff and soil after prescribed burning on forest
clearcuts in northern Idaho. USDA For. Serv. Res. Note fliT—
162, 8 p., Intenntn. For. Range Exp. Stn.
ForssIund, K.H. 1951. Oin hyggesbrannlngens inverkan pa markfaunan.
Entomolog. Meddelfiser 26:144—147.
French, J.R. and R.M. KeIrle. 1969. StudIes in fire-damaged radiata
pine plantations. Aust. For. 33:175-180.
Harris, D.L. and W.II. Whltcont. 1974. Effects of fire on pop iati ns
of certain species of ground beetles (Coleoptera: Car bidae).
Fla. Entomol. 57:97-103.
Harrison, R.E. and J.L. Nurad. 1972. Effects of annual prescribed
burning on nenatode popu1at ons from a Louisiana pine forest.
J. Nematol. 4:225-226.
Heyward, F. and A.N. Tissot. 1936. Some ch inges In the sot! fauna
associated with forest fires in the longleaf pine region.
Ecology 17:659-666.
45?
-------
Huhta, V., E. Karpplnen, M. Nunninen and A.. Valpas. 1967. Effect of
%flvlcultural practices upon arthropod, annelid and nematode
populations in coniferous forest soil. Annu. Zool. Fenn.
4:87-145.
Huhta, V., N Nunninen and A. Yalpas. 1969. Further notes on the
effect of silvicultural practices upon the fauna 0 f coniferous
forest soil. Annu. Zool. Fenn. 6:327-334.
Jahn, E. and G. Schlinitschek. 1950. Bodenkundllche und bodenzoologlsche
Untersuchungen uber ?uswfrkungen von Waldbranden Im Hochgeblrge.
Osterreichische Vlerteljahresschrift fur Forstwesen.
91:214-224; 92:36-44.
Karpplnen, E. 1957. DIe Oribatiden—Fauna elniger Sch’ag-und
Brandflachen. Entcmol. Fenn. 23:181—203.
Leonard, B. 1977. The effects of forest fires on the ecolo’jy of leaf
litter organisms. Victorian Nat. 94:119-122.
Najer, 3D. 1978. Preliminary survey of the epigaeic Invertebrate
fauna with particular reference to ants, In areas of different
land use ac Dwelhlngup. Western Australia. Forest Ecology and
Management, p. 321-334. Elsevler Pubi. Co.
Margalef, ft. 1958. InformatIon theory in ecology. Gen. Syst.
3:36—71.
Netz, L.J. and D.L. Dlndal. 1975. Collembola populations and pre-
scribed burning. Environ. Entomol. 4:583-587.
Metz, L.J. and M.H. Farrler. 1973. Prescribed burning and popi’latlons
of soil mesofauna. Environ. Entomol. 2:433-440.
Miller, WE. 1978. Use of broadcast burning to control red pine cone
beetle In seed prodiction areas. Environ. Entoniol. 7:698-702.
Pearse, A.S. 1943. EfFects of burning over nd ra¼ing off litter on
certain soil animals In the Duke Forest. Am. Midi. Nat.
29(2) :406—424.
Plelou, EC. 1969. An Introduction to Mathematical Ecology. Wiley-
Interscience, NY. 286 pp.
Rice, L.A. 1932. The effect of fire on the prairie animal coninunitles.
Ecology 13:392-401.
Rickard, N.H. 1970. Ground dwelling beetles in burned and unburned
vegetation. J. Range Manage. 23:293-294.
Sclmuitt, J.B. 1974. The dF 3 trlbutton of brood ten of the periodical
cicadas In New Jersey in 1970. J. New York Entomol. Soc.
82:189—201.
1458
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Shannon. C.E. and W. Weaver. 1963. The Mathematical Theory of
Communication. Jniv. Illinois Press, Urbana, Ill. 117 pp.
Simmons, G.A., 3. Mahar, M.K. Kennedy and 3. Ball. 1977. Prelimln-
a-y test of prescribed burning for control of maple leaf
cutter (Lepidoptera: Incurvarildae). The Gr. Lakes Entomol.
10:209-210.
Springett. J.A. 1976. The effect of prescribed burning on the soil
f3una End Ofl litter deco npos1t1on In Western Australia forests.
Aust. J. Ecol. 1:77-82.
Viug, M.. and J.H. Borden. 1973. Soil acarl and collembola populations
.affecteo by logging and slash burning Iii a coastal British
.lwnb1a coniferous forest. Environ. Entomol. 2:1016-1023.
459
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EXPERIMENTAL STUDY OF THE DIRECT EFFECT OF LITTE1
BURNING ON SOIL MICROARTHROPODS IN A DECIDUOUS
TEMPERATE FOREST
Guy Vannier
Mtisum Natinnal dH,s o,r, Nagiir,II,
Frnnce
We have used an improved dry funnel extractor to
carryout an experimental study of the direct effect of
litter burning on soil microarthropods which are made up
of mites and springtails. The material Is the same one as
compared to the automatic extractor used in the dynamic
study of microarthropod behaviour towards soil water
evaporation (VANNIER, 1970). The principle of the model
resides in measurement of water loss, using a recordit g
• balance, conducted with rectangular slabs of soil covered
with original intact litter layer and placed into a sieve.
and in periodic collection of animals by an automatic
fraction collector (Fig. 1).
Two kinds of analysis were undertaken at the same
time
1 - Temperature distribution at three evels in
the soil sample (litter, soil surface, and 2—5 cm deep),
and mass transfer evolution made up of water evaporation
by natural convection and loss of matter due to combustion.
2 — Analysis of the animal fall out in successive
collecting vessels at two hours intervals.
Twin soil samples (20 x 10 x 2.6 cm) were taker from
Oak forest, one tobe used as control, tne other for litter
burning experiment. Air conditions around the samples
were maintained at 20°C and 70% R.H. Extraction took
13.5 days.
Ignition occured after four hours of extraction.
The heat of the burning litter rose the temperature about
480°C no longer than about ten seconds, but at the
soil surface and at 2.5 ciii deep there was a very little
rise in temperatire for a st rt while, respectively from
16°C to 45°C, and from 15°C to 20°C. It followed that
animals were not a great deal disturbed in the burned
sample.
Epigeous forms like Sminthuridae and Entomobrjidae
Collembolans have shown a little increase in their activity,
60
-------
Figure 1. - Schematic diag ’am of material for analysing
the direct effect of litter burning on soil
microarthropods.
(1. - Beam scales recording continuously the weight
of soil sample ; 2. — Oak litter ; 3. - Sieve containing
a rectangular slab of soil (20 x 10 x 2.5 cm) ove ed
with original intact litter layer (mesh 2 mm) ; 4. - Probes
measuring temperature distribution litter, soil surface
anl 2.5 cm deep ; 5. - Recorder ; 6. - Funnel wich steep
sides ; 7. - Automatic fraction collector recovering
microarthropods fall out at two hours intervals ; 8. -
Timer.)
461.
-------
but endogeous forms like Isotomidae. Poduronorpha Collembo-
lans and Oribatid mites were less affected by the prescribed
burning. Thirty minutes after ignition, 15% of Smlnthuridae
left the soil sample, and 10% of Entomobryidae , compared
to only 1.5% of Mesostigmata , 1.1% 3f Oribatel and 0.9% of
Isotomidae .
Two hours later after ignition, the motor activity
of all soil animals, expressed in terms of probability for
an individual leaving the sample, rapidly diminished to
attain low values in each group, as long as the moisture
was available within the soil. When soil moisture content
decreased beyond 24% (pF 4.2 permanent wilting point) for
Collembolans and 16% (pF 5) for Oribatid mites, motor
activity increased abruptly until fall-out was completed
after 300 hours when extraction ended (see concept of
water accessibility for soil microarthropods in VANNIERI
1970).
However no significant differences existed between
two soil samples, one used as control, the other subjected
to litter burning, in terms of the number of individuals
in each zoological group (table 1). Due to heterogenous
distribt tion of an*mals within soil, there were more
individuals in the treated sample than in the control,
except foe- Mesostigmata and Sminthuridae , as it is shown
in the following table
SOIL
MICROARTHRL ’P0DS
COUNT IN
CONTROL SAI’IPLE
COUNT IN
BURNED SAMPLE
ORIBATEI
1,061
1,2f
tIESOST 1GMATA
85
706
NEELIPLEONA
9
13
SM NTHURIDAE
66
45
POCUROMORPHA
12
24
ISOTOMIDAE
309
315
ENTQM OBRYIDAE
Total
213
268
2,524
2,625
-------
When considering population structure of a litter-
dwelling species as Sminthurinus signatus (Collembola,
Sminthuridae), it was possible to show the actual damage
caused by the litter fire. The first-instar juveniles that
hatched from eggs and sexually mature females were drasti-
cally affected, whereas the litter-fire halved their
numbers. Reversely the number of other instars (2d and 3
instar juveniles, sub-adult males and females, nature males)
did not differ significantly.
For further informations on related subjects, see
VANr4IER, G. (1970). - Reactions des microarthropodes du
sol aux variations de l’ëtat hydrique d sol. Techniques
relatives a l’extraction des arthropodes du sol. Editions
du CNRS , Paris, sêrie PBI-RCP 40, 320 pages. and VANNIER .
G. (1978). - Etude expérimentale de l’effet immédiat du feu
de litière sur les microarthropodes d’un sol forestier.
Bull. Mus. natn. lUst. nat. , Paris, 3 séric, N° 519,
sept-oct., 42 : 51-63.
463
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SESSION VII: HUMAN IMPACT ON TROPICAL
SOIL ECOLOGY
Moderator: G. K. Veeresh
University of Agricultural Sciences
Hebbal Bangalore. India
ie6
-------
EFFECT OF THE ANNUAL BURNINGS ON TESTACEA OF TWO
KINDS OF SAVANNAH IN IVORY COAST
Marie-Madeleine Co teaux
Mi ,f.un Ni Iional Il-I i sbn , NabNreIlr
Frnn€e
The Tropical Ecology Station at Lamto (Ivory Coa!t
has been the center of integrated studies on all the loc l
ecosystem types. The analytical approach has been an
energetic evaluation of primary production and animal
consumption (LAMOTTE, 1977) within the framework f the
I.8.p.
The effect of the fire on the Th amoebian fauna
‘tas been analysed in other countries : Metropolitan France
and French r,uiana (COUTEAIJX, 1976a, 1977 and 1979 ; BETS
and al. , 1979) in case of accidental, punctual burnings
in the time and followed by more or less long spell durir.r’
what the biotop tries to find again its stability.
The characteristics of the burnt savannas of Lamt’
consists in the fact that the turning is voluntary provoked
each years, at the end of January, that is in the midst
the dry season and that the populations have only one year
of respite before the next perturbation.
A quantitive study of Testacea of two savanna
ecosystems at Lamto was made on samples taken in April 1974.
I - DESCRIPTION OF THC BIOTOPS
Two sampling plots were lccated in a savanna, called
“Savane du Rocher” which has few trees (Boracsus aethiopurn)
and lies on tropical ferruginous soil. The microbiological
activity of these soils is low (POCHON and BACVAROV, 1973 ;
RAMBELLI and al. , 1973).
The sampling areas are located on : a transect exten-
ding from table—land savanna to the forest. The herbaceous
covering of the upland savanna is dominated by Hyparrhenia
chrysar irea, H. diplandra and Androj ogon schirensis . The
transect continues through a second savanna type do in the
slope with Loudetia simplex on a hydromorphic soil with
pseudogley. Here the hydrous system is particularly evident
since, in the dry season, a single heavy shower is sufficient
to inundate It. In the rainy season the water-table is on
the ground surface. The transect ends with a al1ery-forest
which extends along the mar got.
466
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The annual burning gives a characteristic appearence
to th savanna. The herbous covering consists of well defined
crass tussocls of which, after fire, only burnt stalks remain.
Between the tussocks there is bare earth where, at the
beginning of the rainy season, the surface of the soil is
eroded on the table-land and on the slope. When the sampling
carrleo out, three months after the fire, the tussocks of
Hyparrhenia and Loudetia were green but the roots were a
flttle bared and burnt trails were still very evident.
II - TECHNIQUE
In each st tion, ten core samples were taken with
a borer of 660 mmd. At the distributional scale of the
Protozoa such an area of soil surface is liable to contain
several communities. In the s3vanna, one half of the
samples were bored in the tussocks and tI e other in the
bare soil. The cores were divided into two horizontal
layers 1,5 cm thick. In the tussocks, the level upperlayer
a consisted of the surface litter and stem bases and the
Tevel b was bored in the root mat.
The animal population density of the surface layer
can L’e estimated by the technique of suspensicn-dilution
of a fixed stained sample ( COUTEAUX. 1975 ).
The biomasse can be calculated with respect to the
volume of the liv ng cells (COUTEAUX, 1976b, 1978 .
Diversity was calculated using Margalef’ Index.
III — RESULTS
A — Total density of the populations
The two principle characteristics of this
protozoan fauna is their low numerical abundance as well
as the number of species in the commLinity. Mean populatior
densities were : 2,46 living individuals per mm 2 representing
17 species in the savanna at Hyparrhenia ; 2,38 per mm 2
and 18 species in the savanna at Loudetia .
B — Influence of the depth (Table I)
a b a+b
Savanna at
Kyparrheni
Bare soil
0,92
0,79
1,71
Tussocks
1,52
170
—
3,22
Savanna at
Loudetia
Bare soil
0,58
0,33
0,91
Tussocks
1,66
2,19
3,85
TABLE I : Numerical abundance per nm 2
Le67
-------
There is no evidence of differences between the two
levels of the Soil cores. Indeed, in the savanna at
Hyparrhenie , 1,22 individuals er mm 2 has been found,
on the surface and 1,25 per mm in the depth ; in the
savanna at Loudetia 1,12 per mm’ on the surface and 1,26
per mm 2 in the depth. The paucity of the substratum in
organic matter explains this uniformity of the vertical
distribution.
C - Influcence of the roots (Table I)
The influence of the roots is more evident. The
density in the tussocks reaches 3,22 living individuals per
mm 2 in the savanna at Hyparrhenia and 3.88 per mm 2 in the
savanna at Loudetia whereas, on bare soil, it r3aches
1, 1 per 1m 2 in the savanna at Hyparrhenia and 0,91 per
nm in the savanna at Loudetia . Th6 roots constitute,
indisputably, a more significant biotop for the Testacea.
Several factors may contribute to the biological activity
of this region
1) the higher content of nutrient elements
2) the protection from fire
3) these rnicvohabitats are not affected by
erosion
4) the microclimates are favourable and protec-
ted agRinst dessication.
The bare soil is colonized by the populations which
live in tussocks but this colonization is arrested perio-
dically by the successive perturbations of fire o erosion.
This explains the low likelihood that the populations
reach equilibrium densities and the fact that c nly a few
pionneer species occupying these habitats. Unc er these
conditiuiis a fine interactive community will not be esta-
bi ished.
D — The empty tests
The proportions of the living and empty tests
is of interest since it indicates, to some extent, the
speed of the population turnover. In che blotopes where
the degradation is fast, the proportion of en’ ty tests
is low. In the savanna t Hyp3rrher.ia, it is very high
and a little lower in the savanna irLoudetia. The high
values are correlated with the ecfect of the fire because
the l vlng individuals are killad arid it does not damage
the majority of the empty tests. Therefore the production
of empty tests by the action of fire Is more important
than in a normal bio .ope without for all that, implicating
the speed of their eliminetion.
68
-------
The source of the empty tests is as often as not
local, any tests come from next microbiotopes carryed away
by the wind or the run-off.
E - Biomass (Table II)
a b a+b
Savanna at
Hyparrhenia
Bare soil
0,14
0, 4
0,18
Tussocks
0,11
0,08
0,19
Savanna at
Loudetia
Bare soil
0,05
0,02
0,07
Tussocks
0,33
0,66
0,99
TABLE II Blomass (kg per ha)
The total bi niiass reaches 0,183 kg per ha In the
savanna at Hyparrhenia and 0,532 kg per ha in the savanna
at Loudetia . These values are low in comparison with
the other animals. In the savanna at Hyparrhenia , there
is almost no difference between the tussocks and the
bare soil whereas, in the savanna at Loudetia , the biomass
in the tussocks reaches almost 1 kg per ha even though,
between the tussocks, there are negligible protozoan
population densities.
F — Diversity (Table III)
b Bare soilTussocks total
Savanna at
Hyparrheni a
2,10
1,31
1,12
2,30
2,50
Savanna at
Loudeti
2,48
1,64
1,51
1,82
2,98
TABLE III : Diversity (Margalef’s index)
The diversity, calculated with the Margalef’s
Index Is low in the both savannas. It is, in general,
higher en the surface and in the tussocks and, on all
the populations, in the savanna at Loudetia than in the
savanna at Hyparrhenia .
69
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IV - DISCUSSION AND CONCLUSIONS
In the both savannas, ressemblances exist at the
level of the structural characteristics of the communities
the number of species, individuals, biomass and diversity.
In all the parameters the tussocks are higher than th!
bare soil. It seems that the structural characteristics of
the savanna protozoan species assemblage are principally
determined by the low nutrient status of the soils and
their morphological instability.
It is known that exposed biotopes are not favourable
for the Testacea (COUTEAUX, 1976c) because they offer little
protection and are liable to intense evaporation from the
superficial layers where the Testacea are living. It might
be expected that the hydrous system would be accountable for
this effect as studies on the water—table in the forest of
Sénart (France) have shown (COUTEAUX, 1976d). But this
extreme low local abundance must be attributed to another
factor. Indeed it has been shown, in France and in French
r,uiana (COUTEAUX, 1976a, 1977 and 1979 ; BETSCH and al,
1979) that the fire entirely destroys the Thecamoebian
fauna in the first centimetres of the soil because the
soil Protozoa are not capable of rapid migration to refuge
nicrohabitats. In this case, the roots of the herbous
tussocks can be considered as refuge zones from which the
bare spaces are colonized.
This phenomenon is slow however that a stable species
association is never established at low population densities.
It is, therefore, coiicluded that the energetic participation
of the Testacea to the ecosystem of burnt savanna is very
low and localised in the roots of grass tussocks.
LITERATURE CITED
BETSCH, J.M., KILBERTUS, (L, PROTH, J., BETSCH-PINOT, M.C.,
COUTEAUX, M.M., VANNIER, S. and VERDIER, B., 1979. -
Effets de la deforestation a grande êchelle de la
forêt tropicale sur la microfaune et la microflore.
Collogue International de Zoologle du Sol , Syracuse
(U.S.A.).
COUTEAUX, M.M., 1975. - Estimation quantitative des Théca-
moebiens ëdaphiques ar rapport a la surface du sol.
C.R. Acad. Sc. , Paris, 281 : 739-741.
COUTEAIJx, M.M., 1976a. - Modifications de la faune thécamoe-
blenne sous l’effet d’un Incendie de forêt en region
submëditerranéenne. C.R. Acad. Sc. Paris , 282
92 5-928.
COUTEAUX, P1.M.. 1976b. - Etude quantitative des Thécamoeblens
d’une savanne a Flyparrhenia a Lamto (COte d’Ivoire)
Prostitolojjca, 1976, 12 : 563—570.
470
-------
COUTEAUX, M.M., 1976c. - Le peuplement thécamoebien du sol
et la nature ae l’eau disponible. Bull. [ col. ,
7 : 197-206.
COUTEAUX, M.P1. , 1976d. - Dynamisme de 1 ‘équilibre des
Thécamoebiens dans quelques sols climaciques.
P4ém. MUS. Hist. Nat . N.S., serie A, Zoologie,
96 : 183 p.
COUTEAUX, M.M., 1977. - Reconstitution d’une nouvelle corn-
munauté thécamoebienne dans la litiêre d’une forét
incendiêe en region subméditerranêenne. Bull. Ecol. ,
(Stockholm) 25 : 102-1C 8.
COUTEAUX, I1.M., 1978. - Etude quantitative des Thécarnoebiens
êdaphiques aans une savanne a Loudetia A Lanto
(COte d’Ivcire), Rev. Ecol. Biol. Sol , 15 : 401—412.
COUTEAUX. M.M., 1979. — L’effet de la deforestation sur le
peuplernent thécanoebien en C uyane francaise : étude
prClirinaire. Rev. Ecol. Biol. Sol , 16, sous rresse.
POCHON, J. and BACVAROV, I., 1973. - Donnêes préliminaires
sur l’activité microbiologique des sols de la
savane de Lamto (Côte d’Ivoire). Rev. Ecol. Biol. Sol ,
10 : 35-43.
RAMBELLI, A., PUPPI, G., BARTOLI, A. and ALBONETTI, S.G.,
1973. - Deuxiêi’ie contr tbution la connaissance de la
microflore fongique dans les sols de Lamte en
COte d’Ivoire. Rev. E..ol. Biol. Sol , 10 : 12-23.
-------
EFFETS A COURT TERME DE LA DEFORESTATION A
GRANDE ECHELLE DE LA FORET DENSE HUMIDE. EN
GUYANE FRANCAISE SUR LA MICROFAUNE ET LA
MICROFLORE DU SOL
‘J. M. Betscb, G. Kilbertus, ‘J. Proth, ‘M. C. Betsch-I’inot, ‘M. M. CoGteaux,
G. \‘annier and B. Verdier
•.Wi. Fu n National dHis?ojr, Naturvile
“IIn ’,, itf dv Nancii I
Fra ‘ice
INTRODUCTION
Devant l’ampleur du programe initialement prévu (600.000 ha en
15 aris) de deforestation a des fins papetléres de la forêt guyanaise,
la D.G.R.$.T. (Delagation Générale a la Recherche Scientifique et
Technique — Gestion des ressources natureUes renouvelables) a incite
4 organismes de recherches fondamentales et appliquées (C.T.F.T.,
I.N.R.A., Museum, O.R.S.T.O.M.) a effectuer une étude pluridisciplinaire
des consequences êcologiques de l’exploltation et de la transformation
de la f rèt tropicale humide de Guyane. Cette action comporte dew
aspects principaux
- L’êtude du recru naturel sur tine parcelle expérimertale
(dite “Arbocel”) de 25 ha coiipée a blanc en 1976 dans 3 des conditions
identiques celles ‘fe l’exploitation papetlère (18Or /ha environ, soit
40% oe la biomasse végêtale restent sur place ; G1’IRAUD, 1979) ; c’est
cet aspect qui sera développe id
- L’étude de l9nstallation d’écos ,3,stèmes simplifies
(páturage, arboriculture fruitière, reboisements monospCcifiques, ...)
sur 8 bassins versants assoclés A 2 bassins témoins (B.V.A a a, de
1,5 ha en moyenne) ; ces maniplalations de 1 ‘écosystènse forestier
débuté en 1978, apres deux annêes d’etalonnage sous conditions
natut’el les.
La station experimentale de Guyane ce sltu2 dans la Zone êqiia-
toriale (5°30’ ‘at. N ; 530 long. W) ; la pluviosite moyenne est
estimée A 4.000 tin, avec une saison relativement séche d’aoOt a
novembre, la temperature moyenne étant de 28°C.
Dans la parcelle Arbocel, la couverture pédologique, sur schistes
Bonidoro, (HUMBEL, 1978) est constituCe en grande partie de Dlate ux
dont les sols sont a horizon humifêre trés peu épais et a cheminement
de l’eau superficiel et lateral et de quelques bas-fonds hydromcrphes.
Le pH est compris géneralement entre 4,3 et 5. La forêt dense humide
avolsfnante a une production de litière annuelle de l’ordre de 8,5 T/ht
(PluG, sous presse).
METHODES
Dans la parcelle Arbocel de 25 ha (Fig. 1), eux transects
472
-------
- ‘1 —• —
stationnels ont Ctê retenus, l’uri, T sur sols dra nês,
l’autre. 12 en bas fond hydromorphe ; les prêlèvements ont
lieu 50 rn a lintérieur de la forét (térnoin ; - 50), a
() m de la litière a l’ir.térieur de la parcelle (+ 50) et
vers son centre (+ 300 sur T 1 ; + 200 sur 12). Le feu ayant
ravage des 1976 une partie de l’abatis, cette situation
(trés courante en Guyane) a fait lobjet d’une étude
comparative en particulier en Ti + 50 NB (non brülê) et
+ 50 B (brülé). De mème, ii a paru utile d’étendre la
prospection aux cheinins de halage du bois par les engins
iécani ues (240 rn/ha), mais le niveau “zero” du sol n’est
pas comparable a celui des autres biotopes, ëtant oruié
l’arrachement mécanique au cours du dêbardage et l’êrosion
consécuti ye.
Les prélëvements pour la microfaune, la niatiëre
organique, la retention hydrique et les mesures d’actlvité
respiratoi e ont lieu aux niveaux suivants : litlére
(êventuellement), H 1 (0-1 cm), H 2 (-1-3,5 cm), H 3 (-3,5—6 cm),
H 4 (-6-8,5 cm).
Les résultats ne pouvant tous Ctre présentés, nous
nous sommes souient limités aux comparaisons des 4 situations
les plus representatives de la parcelle, sur le transect
n° 1 (sol drainé)
- 1 : forêt—témoin ; T - 50
- 2 : abatis non brOlé T 1 + 50 NB
— 3 : abatis assez fortement brUlé ; T + 50 B
- 4 chemin de halage ; CH.
Dans les abatis non brOlés, la couverture vegetale
composée d’espêces pionnières a pousse trés rapide, essen-
tiellement Cecropia et Goupla , atteint 4 m de hauteur deux
ans apres la coupe. Sur les abatis assez fortement brülês
Pt les chemins d i ’ halage, la vegéta ’’ n était alors
inexistante. Les ‘ ewpératures enregistrées dans le sol
(exemple a — 1 m Fig. 1) sont nettement plus élevêes
dans les bioto cs c tcouverts que dans l’abatis avec recru
naturel.
RESULTATS
1 - Matière organigue
La méthode de dosage du carbone selon Anne n’étant
bien appropriêe que pour des sols dont le taux ne dépasse
pas 3%, nous avons adopté la méthode d’attaque par H 2 0
a chaud, donnant le taux de rnatiëre organique totale par
di fêrence de pesée du sol sec. Cette analyse est complétéc
par une separation par flottation des él ments figures
incomplétement biodégrades surnaqea’its et de la matière
ii73
-------
rig. 1 - A. - Situation de la parcelle expèrimenta’e en
Guyane Françalse. B. - Dispositif experimental
pour 1’êtude de la deforestation et des manipu-
lations de l’êcosystenie. C. - Parcelle expérl-
m 3ntale et situation des stations de prëIëvements
sur les transects. D. - Coupe schématique du
transect 1. E. - Coupe schématique du transect 2.
F. - Coupe schematique du sol montrant les diffé-
rents horizons étudies et leur profondeur. G. —
Courbe de temperature a -1 cm dans le sol dans les
abatis brOlé et non brOlé a T + 50.
4
-------
Ftm
/
‘iLl
‘4 ’
UkU11tI
—N S .55
F
•1 5 5
7,
Ti - - -.-
1T2+*NI
,ai lW
D
G
A
N’.
.5.
WI
1..
.5.
I I •
, — a
B
)
I — .
E
T1.iSbrOS 11,NnonbrO$
475
-------
•1
I .1 •$ 4
•batii non brülö
(2)
riTh
•ba* s brüIá
‘3)
I -I .$ -I .U
cP minds hilags
(4)
I .l .$ .a .g is
Fig. 2 - Courbes comparat1ve entre les 4 situations prin-
cipaies du taux de matière organique (blanc
matlère organique liëe aux substances minérales,
gris : matlêre organique figuree), de i’humiditê
actuelle (en grise) située par rapport a pF 0,
pF 2,5 et pF 4,2 et de l’activité respiratoire
cans chacun des horizons ëtudiês.
I
a
NA VSIDI Nriaii
,Dlr,
ETpI
SI.,., ’
AersYsri aispsairarni
N
Phfh
-------
—- .-.-———.T
organique ltêe aux substances minérales, en particulier aux
argues.
De ces analyses, on peut tirer les conclusions sui-
vantes (Fig. 2 et 3)
- les taux de m tiêre organique sont três élevës
pulsqu’lls varient entre 33% et 9% dans les horizons supe-
rleurs et atteignent encore 7% dens les horizons -6-8,5 cm.
- le taux de matiëre organique total décroit
de la forêt a l’abatjs non brOlé, puis a l’abatis brOlê.
Mais cette diminution porte surtout sur les deux premiers
horizons (0 a -3,5 cm) et affecte principalement la matiëre
organique surnageante. Les taux de matière organique flee
aux substances minérales varient peu d’un sol a l’autre,
quel que soit le traitement subi, deux ans aprês la
déforestat ion.
- les taux de matiêre organique du chemin de
halage peuvent surprendre mais il faut tenir compte du
stock existant, des apports lors du debardage et par le
ruissellement. Par contre, le taux de surnageant est trés
faible en l’absence de végêtation.
- on constate un enrichissement des sols sous
couvert entre mars 1917 et avril 1978, surtout en matiêre
organique surnageante qui peut provenir de la chute de
litiëre des espêces yecolonisatrices dans les abatis non
brOlés, mais aussi d’un phénomène salsonnier puisqu’il
apparait aussi en forét (les prélêvements ne sont pas
exactement superposes dans le cyc e annuel).
II - Retention hydrigue
Les humidités actuelles des sols relevées au moment
dss prelevements pour la inicrofaune, la microflore et
1 ‘activité respiratoire ont êté comparées aux humiditês cie
ces mémes sols soumis sous pres e a membrane a pF 0, pH 2,5
et pF 4,2.
La figure 1 Illustre les comportements hydriques
daris les 4 situations—types en sols dralnés
- la forét-témoin et l ’abatis non brCilé présen-
tent une décroissance de l’humidité actuelle de leur sol
avec la profondeur, ce phénoméne êtant evidemment trés
accentué dans Ia forêt clim_cique. Les courbes d’humiditê
aux trois valeurs référence de pF suivent la même tendance.
- l’abatis brOlé volt l’humidité actuelle de son
sol croitre avec la profondeur et ceci quel que soit le
moment de la dernIère precipitation (10 mInutes ou 2 jours).
Ii est remarquable que les courbes d’humidité aux trois
valeurs référence de pF ne suivent pas cette tendance ;
dans les deux horizons superficlels, l’humldité correspond
a des pF supérleurs a 2,5 et méme proche de 4,2 en surface.
-------
—
Fig. 3 - Courbes comparatives de 1’évolution du taux de
matiêre organique et de l’activltë respiratoire
des sols entre mars 1977 et avrll 1978, en forêt
témoin et dans un abatis.
-------
- le chemin de halage présente une humidité
croissant avec la profondeur, mais gui est id en accord
avec les courbes aux trois valeurs référence de pF.
III - Ilicrofaune du sol
1 - Thecamoebiens
L’ëchantillonnage a porte en 1977 sur l’abatis
T 1 + 300 B (5) et les abatis non brUlés T 1 + 300 NB
sans litiêre (8) et avec Iitiëre (9), et en 1978 sur les
stations 1, 2 et 3 (voir figure 1).
Quatorze especes ou variétës ont ete trouvêes sous
forme d’individus vivants dans les stations indiquees
Centropyxis a2•(l). Cyclopyxis kahfl (2), Eu lypha laevis
(1), Euglypha rotunda var. minor (ou E. capsiosa ou E.
h alina ) (1), yalosphenia subflava (50 pm ; 9). H. subflava
(100 pm ; 9), W. subflava (135 pm 2), Nebela militaris (9),
Phryganella acropodla (1,5, 8, 9), P. acropodia var penardi
( 1,9), Trinema complanatum (9), T. enchelys (9), 1. grande
(1,9), 1. lineare (9).
L’estiniation de 1 densité sur 2 cm de profondeur
vane entre 1,14 et 21,49 individus vivants au mm 2 , Ia
biomasse de 012 a 1,71 kg/ha.
L’abatis non brOlé 00, de plus, la litiêre est en
place est le biotope Ie plus riche tant pour le nombre
d’espêces que pour le nombre d’individus. Sur la base
des données pr 1iminaires dont nous disposons actuellement,
II n’y a pas de difference significative entre ce type
d’ab3tis et la forét—témoin. La couverture de litiêre et,
pour 1978, la recolonisation par les Cecropia conférent
& ce biotope un caraçtère abnité qui s’apparente a un
milieu forestier (COUTEAUX, 1979).
Par c’ntre, en abatis brülé, les niveaux de surface
sont dCpourvus de Thécamoebiens. Cet effet néfaste du feu,
déjà observe en France et en Côte d’Ivoire (COOTEAUX, div.
pubi.), intervient par l’élévation de la temperature, la
modification chimique du milieu, l’érosion des couches
superficlelles qui sont les seules a abriter des Théca—
moebjens et la modification de la dispunibilité hydrique.
Ii existe environ 3 fois plus de theques vides que
d’individus vivants. Cettc proportion, faible par rapport
a ce qui a été trouv en forét tempérée humide ou en savane
tro icale (COtITEAUX, div. Pubi.), peut témoigner d’un
turn-over plus rapide.
Le79
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2 - lAicroarthropodes du sol
Les résultats quantitatifs globaux concernent une
période sensiblement identique au cours des années 1977 et
1978 (en pleine saison des pluies) 00 les populations sont
a leur effectif et leur diversité maxima. Les autres
r rê1èvements, en aoUt ou novembre, ne montrent pas de
modification spectaculaire de ces deux données (environ
60% des effectifs maxima).
- Effectifs globaux
La figure 4,A donne le niveau des populations de
microarthropodes du sol dans les 4 horIzons êtudiës et
éventuellement, dans la litière, 20 niois aprês la coupe
a blanc de la forêt. Les deux types de forêt-tëmoin, et,
dans une mesure a peine moindre, l’abatis non brOlé sur
sol hydromorphe, renferment des populations nombreuses a
presque tous les niveaux du profil (8 remarquer que les
chlffres ne donnent pas une bonne idee de la biomasse dans
la litiëre oO la taille des individus est nettement plus
forte que dans le sol). Tous les autres sols ayant subi un
traitement prêsentent des populations peu nombreuses ;
l’abatis fortement brOlé n° 3 est même totalement dépourvu
de faune dans son horizon supérleur.
L’évolution des effectifs de l’abatis non brOlé n° 2
entre mars 1977 (litlére au sol provenant des arbres
abattus) et avrjl 1978 (Iitiêre de Cecropia et Goupia ,
du recru naturel) montre une stabilitê numérique des
populations dans la litlére mais une chute trés marquee
des effectjfs dans le sol (Fig. 4, B). De méme, l’abatis
brOlé n° 5 volt sa population se réduire deux ans après
la co zpe 8 blanc.
A cette diminution trés forte des •:ffectifs s’ajoute
une diversité trés réduite des groupes zoologiques représen-
tés dans les zones manipulees.
- Rapport Acariens/Collemboles
Ce rapport, generalement utilisé pour un sol total
(cf. en particulier MALDAGUE, 1961), est en réalité trés
variable selon les horizons du sol. La figure 4, C montre
que Ce rapport présente une courbe ascendante assez voisine
dans les deux types de forët—temoin, mais aussi dans l’abatis
non brOlé sur sol drainé, et, avec une amplitude blen
noindre, dans l’abatis non brOlé sur sol hydroniorphe ; les
deux abatis non brOlés, qui constituent la modification la
moms accusée de l’écosystëme, suivent donc assez blen les
caractéristiques des sols des formations climaciques. bus
les autres sol nanipules présentent des courbes non
interprétables actuellement.
‘e80
-------
- Analyse globale des Collenibcles
Devant l’impossibilitê de déterrriner au niveau speci-
fique un nombre suffisant d’especes de Collemboles (par
manque de travaux systématiques exhaustifs), nous avons
appliqué le crit re différentiel d’ODUM aux 5 grands groupes:
Neêlipleones, Symphyplêones, Poduromorphes, Isotomides et
Entornobryens. Les relations entre les stations comparées
deux a deux sont mises en evidence, de mênie gue leur êvolu-
tion relative entre mars 1977 et avril 1978. L’analyse ri’a
été effectuêe que pour la litière et les deux premiers ho-
rizons (Fig. 4, D, E et F) ; en-dessous. la faiblesse des
effectifs ne permet pas d’obtenir de rêsultat representatif.
Les deux types de forêt-têmoin sont êvidemment hien
lies, surtout dans la lltiêre ; dans le sol, le c ractCre
assez hydromurpl e de la station 6 se répercute ,ur les
valeurs du lien ; le léger rapprochement dans le tenips semble
dü a Ia phénologie du cl5mat un pei différente en 1978.
En ce qui concerne les zones modifiées . ii faut remar-
quer imniédiatenient l’isolement total de l’abatis fortement
brülé (3 ; sauf a partir de H 2 , mais avec e oignenient) et
du chemin de halage (4) ; l’abatis non brOlè sur sol drainé
(2) conserve dans l’ensemble de bons liens avec son témoin
(1), mais sen éloigne a tous les ni eaux. L’abatis brOTh
n° 5 présente de bons ou assez bons liens avec l’abatis non
brOlé n° 2 dont ii se rapproche même en surface aprës
I’eloignenient initial dO au traitenient subl ; mais ses
liens compares avec l’abatis non brOTh (2) et l’abatis
fortement brOlë (3) montrent qu’il existe nioins de diffé-
rence entre le non brülé et le faiblement brOlé qu’entre
ce dernier et le fortement brOTh. Quant a l’abatis
non brUlê sur sol assez hydromorphe (7), il s’êcarte de
son tënioin (6) pour la litière, mais s’en rapproche pour
les horizouus du sol, avec un lien moyen a bon.
- Données qualitatives sur les Collemboles
Symphypléones.
Ce groupe essentiellement épigé est intéressant par
les renseignements qu’il peut donner sur les caractéristiques
du biotope, qu’il soit forestier primaire, secondaire ou
découvert. La litière de la forét—temoin sur sol draIné (1)
renferme les genres typiquesde forét comme Temeritas,
Collophora, Pararrhopa’ites , Neosminthurus et Sphyrotheca
auxqueis s’ajoutent, a 1’etatWisperse,Tis Dlcyrtomidae .
En 1977, la litière de l’abatis non brOTh (2) re renfermait
que des Dicyrtomidae gui s’ nt caractéristiques des forêts
secondaires en eone intertropicale ; en 1978, une partie
ducontingent de Symphypléones de forèt primaire était
deja present dans la litiëre du recru naturel de ce même
abatis : Sphk rotheca et Pararrhopalites qul s’étaient ad-
joints aux Dicyrtomfdae.
8i
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Fig. 4 - A. - Evolution du nombre total de microarthropodes
du sal en fonction de la profondeur dans les dif-
férentes stations. B. - Evolution du nombre total
de microarthropodes entre 1977 et 1978 dans les
stations 2 et S. C. - Evolution du rapport Acariens/
Collemboles en fonction de la profoncleur dans les
différentes stations. D, E et F. - Schema des
relations entre les stations et de leur evolution
base sur le crltére différentiel d’ODUM appliqué
aux Collemboles (D, litière ; E, horizon H 1 ;
F, horizon H 2 ).
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IV - Microflore du scil
L’élimination partielle ou totale des microorganismes
peut être considerée comnie un facteur de Ia mesure de
l’activitê biologique, mais la suppression des gerines, con-
trairement a celle de la faune, entraine des phênomènes
irréversibles. La microflore saprophytique du sol, au même
titre que la photosynthese et les êléments géochImiques, est
en effet indispensable au niaintien de la vie sur ter e, car
son activité métabolique permet le recyclage des êlêments
organiques élaborees par les plantes. Mêine si les effets de
la deforestation ne sont pas drastiques, l’éclipse d’une
flore specifique, la cellulolytique par exemple, enipêchera
temporairemert le déroulement dun cycle vital, en retardant
la degradation microbienne dun composant majeur des cellules
vêgëtales le polysaccharide en l’occurence. La fragilité
des sols tropicaux ètant bien connue. le blocage ou Ie fref-
naqe d’un processus biologique de ce type peut avoir des
consequences trés néfastes en contrecarrant les futurs
essais de reboisement.
1 - Donnees quantitatives et qualitatives.
Deux ans aprés la deforestation, la microflore totale
ne vane que tr s peu au cours de la saison des pluies
(KILBERTUS, 1979). Mis a part une station en pente qui
présente un appauvrissement en germes par rappgrt aux sols
Forestiers correspondants (1,5 contre 3,4 x 10° germes/g de
sol), dans toutes Ies autres stations, les chiffres sont
compnis entre 3,2 et 4,8 x 106 microorganismes par gramme
de sol. Etant donné l’imperfection des techniques de flume-
ration, ces differences ne peuvent être considérées comme
étant significatives.
Durant la saison séche, les differences sont plus
Importantes : selon les stations,les moyennes vont de
i. a 28,2 x 106 bactérjes par gramme de sol. Seule la station
brOlée (3) et celle du taiweg (7) renferment des quantités
de microorganismes comparables a celles des milieux boisés
(respectivement 10,8 et 28,2 pour 12.9 - 9,2 - et 18,6 x 106
cellules par gramme de sol dans lec stations boisëes). Ces
deux parcelles présentent une écologie particullére : la
premiere (3) est trés riche en flêments ininéraux resultant
de la calcination des arbres, la seconde (7) situee dans
un taiweg, reste constammerit humide (KILBERTUS et PROTH,
1978). Ces particularites permettent e partie d’expliquer
leur composition microbiologiqie.
Du point de vue qualitatif, l’êlimlnatlon de la forét
se traduit par une raréfaction ou une dispanition de cer-
tames espéces caractéristiques des biotopes boisés
48
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- dans les stations de plateau, les Micro-
coccus disparaissent ou diminuent sensiblement en noiiibre
dans les parcelles dêboisêes. Par contre, les diffêrentes
espëces appartenant au genre Arthrobacter résistent trës
bien. Les memes remarques s’appliquent aux stations de
pente.
- dans les stations de taiweg, Bacillus
licheniformis toujours present dans les sols forestiers,
n’appara t plus dans les zones déforestées. Ii est
intéressant de noter que dans ces dernières, certains germes
caracteristiques des parties moms humides ( Arthrobacter
et Bacillus bv evis ) sont isolés au cours de la saisôñ sèche.
Ces modifications qualitatives semblent caractériser
un stade transitoire- la durëe de l’ëlimination des arbres
étant insuffisante pour provoquer la disparition totale
de certains microorganismes ielluriques.
Signalons enfin que la composition qualitative de
la inycoflore ne semble être guëre affectêe (KILBERTUS, 1979).
2 - Apports de la microscopie electronique
La microscopie électronique apporte des données
complementaires
- elle confirnie que les sols dépourvus de
strate arborêe, même ceux des chemins de charriage, conti-
nuent a renfermer des bactéries vivantes, géneralement
protêgées par les argues.
- Les colonies de procaryotes, lorsqu’elles
sont visibles, se présentent souvent sous forme damas de
celiules englobêes dans un mucilage a la surface duquel
s’adsorbent des 7euiuiets d’argile (Fig. 5, 1). Le
polysaccharide et les phyllosilicates jouent un role
important et leur presence explique la survie des germes
au cours de periodes defavorables (KILBERTIJ’S et coil., 1977).
- ces colonies bactériennes sont abondantes
dans les sols forestlers au cours de la saison seche, mais
elles sont remplacées par des formes isoiêes durant la
période humide. La station Soisëe de taiweg renferme
d’aiIleurs essentiellement des procaryotes isolés, ce qul
sembie confiner l’infiuence des saisons.
Par contre, dans les parcelles sans arbre, c’est au
cours de la saison humide qu’apparaissent les associations
de bactéries, la saison sêche êtant caractérisée par des
formes a i’etat de vie latente,rêtractêes A l’intërieur
du mucilage.
- chaque station renferme des germes a
ultrastructure particuliëre, comme celui reprCsenté dans
la figure 5,4.
l 85
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Fig. 5 - Microflore du sol ; clichés au microscope é1ectro
nique a transmission. Les ëchelles sont données
en im. Les coupes or,t éte contrastées selon la
technique de Reynolds (R) ou de Thiéry (1).
- 1, colonie bacterienne dans un sol forestier (1).
- 2 et 3, germes isolés rencontrés 4ans les sta-
tions déboisêes (R). — 4, germe particulier ren-
contré dans une station déboisée en pente CR).
86
-------
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87
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— enfin, les stations 3 et 7 se distinguent
des autres sols par des quantités plus importantes de ma-
tière organique imparfaitement décomposée.
Nous pouvons donc conclure que la période d’êtude
nous semble trop courte pour provoquer de differences
tranchêes entre les stations boisées ou non. Mais on assiste
néanmoins a la diminution ou a la disparition c e certains
orocaryotes aux dépens d’espèces mieux adaptées aux nou-
velles coiditlons de vie. Ces rêsultats sont dOs a la
persistance de certaines sources trophiques : les élëments
minéraux resultant de la calcination des arbres dans la
station brOtêe, la presence de nombreux troncs morts dans
les parcelles non brOlees. D’autres facteurs sont également
A prendre en compte, car le chemin de d bardement (4)
totalement dépourvu de végétation nest pas biologiquement
Inactif. Les microorganismes possêdent en effet des niêca-
nismes de protection (endospores, chiamydospores, protection
par les argues, ...) qul leur permettent de resister du-
rant les périodes défavorables (KILBERT S et coll, 1978,
1979).
V - Activité respiratoire des sols
Les sols séchés, tamisés A 2 mm, sont remouillés
a pF 3 ; us sont maintenus 7 jours a la temperature
d’incubatjon retenue (29°C en général ; 45°C pour certains
sols d couv rts, compte tenu des êlêvations de temperature
qui y ont éte relevées). La mesure de la respiration est
rëalisée a pression constante sur 5 g de so (poids sec).
Le CO 2 étant absorbé par la potasse. la depression dans
la chambre respiratoire correspond a la consommation
d’oxygene potentielle que l’on mesure par déplacement d’un
index dans un tube capillaire.
En sols drainés, la consommation d’oxygene (Fig. 2)
décroit de maniëre sensible de Ia forêt-têmoin (1) A
l’abatis non brOlé (2), et dans des proportions trés fortes
dans l’abatis brOlé (3) et le chemin de halage (4). L’ëvolu-
tion de l’activité respiratoire entre 1977 et 1978 est
lllustrée par deux exemples : la forCt-témoiri (1) ne volt
de modification que dans son horizon supérleur tandis
que l’abatis non brOlé (7) enreglstre une chute remarquable
de son activité respiratoire.
DISCUSSION - CCNCLIJSION
Ii est difficile de degager un strategie commune
488
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pour l’ensemble des fonctions d’un biotope donné. Ln effet
tes microorganismes telluriques peuvent être presents dans
un ol fortement modifië par leurs formes de résistance
ce dont les microarthropocies du sol sont generalement
incapables ; de méme, l’activité de la mlcroflore peut être
importante alors que les microarthropodes peuvent alors
être relativement peu nombreux.
Pour nous en tenir aux quatre situations principales
sur sol drainé consécutives au déboisement, les grandes
lignes dégagées par nos observ 1 .tions sont les sui rantes
- le sol de la forêt climacique présente
une forte teneur en matière organique, une forte capacité
de retention hydrique, des populations de mlcroarthropodes
nombreuses et diversifiées, des populations importantes
de microorganismes principalement sous forme de colonies,
un niveau élevé d’activit respiratoire.
- dans l’abatis non brOlé, les principales
modifications concernent le niveau assez faible des popu-
lations de microarthropodes, une capaciU de retention
hydrique plus réduite et un niveau assez faible d’activitê
respiratoire ; certaines données qualitatives chez les
Collemboles permettent de dire que l’eloignement dans le
temps de cette station par rapport au témoin peut connaitre
apres deux ou trois ans un renversement tie tendance.
- Les deux situations dramatiques repré-
sentêes par une action importante du feu et celle des engins
mécanisés de halage des bois volent pratiquement tot s les
doinaines d’activité se degrader dans de trés fortes propor-
tions. Les niveaux relativement élevés d’activitë micro—
blenne sont a mettre de maniêre pratiquement certaine en
rapport avec le stock de source trophique encore disponible
ou amen e par ta calcination des bois. Mais, les données
qual itatives montrent que ces deux types de biotopes sont
en equilibre instable et risquent, par une prolongation
de la suppression de couvert végétal, de devenir irréversi-
blement inpropres a Ia régénération de la végét tion.
REME’ CIEMENTS
Nous remercicins trés vivement Mrs. Francis DEVAUX,
Yann MIKHALEVITCH et Frédéric SEVOZ pour leur précieuse
aide technique et l’exploitation des donnêes.
LITTERATURE CITEE
COOTEAUX, M.-M., 1979. - L’effet de la deforestation sur
le peuplement thécamoebien en Guyane Française
489
-------
étude préliminaire. Rev. EcoL Biol. Sol (sous presse).
GIJIRAIJD, A., 1979. - Etat d’avancement des travaux du C.T.
F.T. Document ronéotypE DGRST, 2 : 21-26.
HUMBEL, F.X., 1978. - Caracterisation par des mesures
physiques, hydriques et d’enracinement, de sols
de Guyane Française a dynamique de Peau superfi-
cielle. Document ronêotypë ORSTOM : 171.
KILBERTUS, G. et PROTH. J., 1.78. - Differences micro-
blologiques et ultrastructurales entre trois sols
de la Guyane Française. Influence du couve”t fores-
tier. C.R. 103° Congr. Nat. Sociêtês Savantes
331-345 (litterature citée).
KILBERTIJS, G., 1979. - Microbiologie du sol en Guyane
Française. Document UniversitC Nancy I : 1-53.
MALDAGUE, N.E., 1961. — Relatior’s entre le couvert vëgetal
et la microfaune. Leur importance dans la conservation
biologique des sols tropicaux. Pubi. I.N.E.A.C.,
90 : 1-122.
P’JIG, H. - Production de litiêre en forêt guyanaise
(sous presse).
QUESTIONS and COMMENTS
. KOEHLER : Can you say anything about the reestablish-
ment of trophic structures (Carnivores, phytophagea and
detritophagous organisms) on the cleared plot?
TSCH : Actually, only general aspects and
certain particular data concerning the relations between
different habitats have been analysed. Moreover, data of
natural regrowih are available for only the first two years;
these data are not yet sufficient Lo allow us to describ’
the 3tages of reestablishment of trophic structures. -
490
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RELATIONSHIPS OF SOME ISOTOMIDAE (COJ.LEMBOLA)
WITH HABITAT AND OTHER SOIL FAUNA
Pen.Iope Greenslade and P. J. M. Greenslade
•Sou:h Australian Miis,um
• CSIRO
South Ausjrahg,
INTRODUCTiON
One might expect competitive interactions to play a significant
part in population processes of microarthropoda and other
invertebrates inhabiting the soil since they live in diverse
communities in a sheltered environment. This applies especially in
the humid tropics where ground layer invertebrate faunas are very rich
and the climate is equable and favourable (Bullock, 1967). One would
also expect competition to be diffuse (Terborgh, 1971; MacArthur,
1972), with any one species liable to interact with a patchwork of
others at varying densities and in varying combinations. Competitive
interaction of this sort has been described by Kaczmarelc (1975a, ) in
Polish pine forests. The distributions and densitias of ‘Oligovalent’
coileinbolan species (i.e. specialised in respect to habitat), depended
to a large extent on moisture. The pattern of density of ‘Polyvalent’
species, with less specialised habitat requirements, varied inversely
with t.he density of the more specialised ones. Kaozmarek concluded
that the latter had a limiting effect on the unspecialised species.
Their distributions could not be accounted for in terms of any one
oligovalent species and so diffuse competition is indicated. Here we
continue a re-examination of data on the soil fauna of the Solomon
Islands in the light of recent ideas in ecology and report similar
results. A previous paper dealt with the ants (Hymenoptera
Formjcjdae) of the same area (Greenslade and Greenslade, 1977).
AREAS STUDIED
Three sites were sampled on the north coast of Guadalcanal,
Solomon Islands, in the southwest Pacific. They were situated amongst
grasslands, coconut plantations and lowland tropical rain forest in an
area with a moderately seasonal tropical climate.
Shifting cultivation sequence
A subsistence garden and adjacent forest provided three plots
representing ear].y stages typical of shifting cultivation:
(a) Forest that had not been recently disturbed and had a well
developed litter layer.
(b) Bare ground immediately after clearing Fcrest. Treec had
been felled and the trunks laid in a grid; other vegetation bad been
heaped up and burnt.
9l
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(c) A Garden of’ ca 0.3ha of sweet potato, ( Ipomoea batatas
Lam.), six months old which had been planted without general
cultivation of the soil. The foliage gave a light ground cover and
there was a thin litter layer.
Coconut plantation transect
A line or 18 square contiguous quadrats, eac i 0.37m 2 , was laid
out across a vegetatior discontinuity in a coconut plantation (Figure
3). Zone I consisted or grasses, 15cm deep in Zone Ia, reaching im
near the base of a paim in Zone lb. 2one II carried a sparse growth
of Staehytarpheta sp. (Verbenaceae).
Plantation ground cover trial
Another coconut plantation was clean cultivated two years prior
to sampling and divided into three blocks of’ 4ha, each of which was
subdivided between three treatments.
(a) Co er Crop, .‘ueraria , up to its deep with a litter layer.
(b) Short Grass, reoolonising grasses mown to maintain a award
lOom deep.
(c) Long Grass, mown less frequently and reaching a height of
its.
METHODS
Sampling
In the Solomon Islands the soil fauna is concentrated close to
the surface (Greenslade and Greenslade, 1 68) and large, shallow
samples were used, 2.5 or 5cm deep, 275cm 2 in area. Large area
reduces variability caused by highly aggregated distributions and low
average density of many individual species. Apart from mites and some
immature Collembo].a all the extracted fauna was sorted to speoi s,
although, coiflbined with the large size of the samples, this limiI ed
the number of samples that could be handled. 3amples were taken at
random as follows:
Shifting Cultivation Sequence: Forest Bare Ground Garden
Litter Depth 7 — 14
0—2.5cm 7 5 14
Soil 5—7.5cm 14 14 14
10—12.5cm 8 14 8
Plantation Transect : three samples per quadrat, 5cm deep.
Plantation Ground Cover Trial : litter samples (Cover Crop only),
soil samples from 0 to 2.5cm and from 2.5 to 5cm at four points per
plot.
Extraction
Samples were extracted in simple plastic funnels. Preliminary
trials tested the effects of retaining samples within cylindrical
92
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FOREST BARE
GROUND
GARDEN
—
.
FOREST BARE
GROUND
p cari F E Hemiptera
— Collembota
lsotomidae
Hymenoptera
t
Coleoptera
Diptera F
L (larvae)
Lepidoptera
{ (larvae)
—
Araneida
[ Opiliones
Isopoda
O 5I
FIGURE 1. Shtttin g Cultivation Sequence, mean numbers per sample
(2 75cm 2 ).
GARDEN
F
— Symphyla
U
—
0 10
Litter
0-25cm
L 5-75cm }Soil
0 10
10-125cm
Diplopoda
-------
FOREST BARE GARL N FOREST BARE GARDEN
GR
r Tyr rUcMhO 5 __ __ C o4eid e
r [ dev islum o
r L (b) Diplurn
L_
,..Utter
F 0-1.1cm 1
(a) Pseudoseorplones cm 3a0
O-I1 m J
FIGURE 2. Shifting Cultivation Sequence, mean numbers per sample
(275cm 2 ) of (a) pseudosoorpions, (b) Diplura. Five
sp . s of pseudoscorpion were recorded in the Forest
samples, those in the Figure and one example each of’ a
Smezingoohernes and an Alocobisium species. In the
order, T. beieri Beier, M. nana Beier, I. pugh ,
Morilcawa, these three species form a sequence of’
decreasing pigmc ntation and reduction in oce].li as their
distributions extend further into the mineral soil.
Similarly, in the Diplura, the Campodeidae have long,
fragile appendages and in the Solomon Islands are
generally found near the soil surface and in litter
(Manton 1972). The more robust Japygidae, with shorter
appendages are more trequent in mineral soil.
k94
-------
FIGURE 3. Coconut Plantation Transect, mean numbers per sample
(275cm 2 ), per quadrat. The distribution and numbers
per sample of the ant, Monoi orium talpa are shown below
‘Acarl’.
ZONE
a
Short Grass
I I ZONE ii
lb I
t r s Sparse Weed
I Cover
I Acari
I!I(, Iiiii l
200
I
i II
I
ZONET ZONEfl
a
Short Grass I l.ong S rs Weed
IGrou’ Covr
I ptera(klrvaE
L L
I Lepidoptera
Hemiptera I izopteridae
IIIIIi IIl II_ -
M.ta lpa
1 OC
No
per 5
Sample
qA_O v 1
I Total Collembola
Isotcmidae
ol Cyphoderint
I
I L1 IjLIJIIIL
Ld
I Other
I_JL1I 1 iPoduroidec
I
I
Nos.
per
Sample
Other Ertomobryidac
nhII.III I I Ij_ . J.
5
r
Lgd4; Tiii.’;
Isymphyla
ILllI ILil
IJçLo o th
d 1 Pauropoda
LL
i !
5
n
‘iO
1(
•
I
ParoneUidae
—
•
1 ‘Neelidae
.
Smkithuridae
iEIL1 [ ELAI
Hymenoptera
p Formicidae
I

5
200
5
n
III
I lAraneida
I .! i Iii i i i. i I
n
Quodrat
Xigochaeta
Quadrat
r
I
-------
Forest levels of density and diversity were not regained. A few
species of Cryptostigmatid mites were disproportionately abundant in
samples from the Garcen. The Coleoptera, Diptera and Hemiptera
contain many species of varied function, usually with winged adults,
and appropriately adapted species entered the cleared areas as the
habitat became suitable. But, in the Coleoptera for example, the
entry of a few upen habitat Carabidae did not compensate for the loss
of the many staphylinoid species occurring in Forest.
Coconut plantation transect
This area had not been cultivated and shows some effects of
vegetation oove independently of other factors. The fauna under Tall
Grass in Zone Ia had some forest—like features : maxima in neelid and
neanurid Collembola and the presence of a schizopterid (Heniiptera) and
the pseudoscorpion, Tyrannochthonlus belerl (Figure 3). There was
evidence of interactions with a veil established aLit fauna. In Zone I
the numbers of mites in samples .(log n + 1) were negatively correlated
with numbers of a cryptic myrmicine ant, Monomorium t.alpa &lery, with
a dense nesting population in Zone Ia (Figure 3) Cr = 0.51 1,
pC0 .001). This ant also occurred in the Ground Cover Trial where it
was widely distributed and here mites were obtained in about equal
numbers from Long and Short Grass (Tatle 1). The numbers of
oyphoderine Coilembola, inhabitants of ant and termite nests, were
positively correlated with total ants from samples over the whole
Transect (r = 0.611, pc0.0Oi). Two faunal elements that were present
in the Garden reappeared under the sparse vegetation of Zone II of the
Transect. They were groups with soil surface or above ground
mobility, at least as adults (spiders, Opiliones, Diptera,
Lepidoptera), and soil inhabitants able to escape from the surface
climate (Japygidae, Symphyla) (Figure 3).
Plantation ground cover trial
Most groups were :,btained in the greatest numbers from samples
from the Cover Crop (Table 1, Figure 14). Forest-like elements of the
fauna of the Cover Crop were Pselaphidae and, as in the Long Grass of
the Transect, Neanuridae and Tyrannochthonius beieri . En the Short
Grass the lack of protection from insolation seems to have caused
downward movement by the fauna. Depression of vertical distributions
here as compared with the Long Grass is seen in 10 out of the 11$
groups in Figure 14. The proportions of total individuals extracted
from soil and coming from the lower soil samples were: Cover Crop,
214%; Long Grass, 27%; Short Grass, 33%.
Distribution of isotomid species
Four common isotomid species on each site formed a
isorphosequenoe of increasing adaptation to life in mineral soil • This
involves differences between species in development of the ocelli,
pigmentation, length of appendages (Christ .ansen, 19614), and shape of
abdomen: fusiforzn with tip horizontal in surface and litter species,
1196
-------
TABLE 1. Compo.Iitjon of soil and litter faunas; mean
numbers of individuals per sample (275 cm 2 ); +, taxon present,
mean of less than one per sample.
C, 00nut
Shifting Plantation Plantation Ground
Site Cultivation Sequenci 1 Transect Cover Trial
Bare Cover Long Short
Treatment Forest Garden Zone I Zone II
Ground Crop Grass Grasa
Vegetation structure, lb
rank mass and cover 1 9 6 5 2 8 3 2 7
Litter layer present CL) L 1. L
Depth of soil
sampling 0—12.5cm 0— Scm
Loan 778 363 755 300 11414 756 715 708
ollembola, Isotomidae 511 22 7 11 3.2 57 70 73
Other Collembola 110 39 97 76 28 377 196 22
Hymenoptera, Formicidae 53 5.7 22 127 11 192 185 187
Other Hymenoptera + - - - - 1.0 . —
Coleoptera 2 14 11.1 15 1.3 + 10 9.0 9.0
Diptera (larvae onlp) 25 3.11 8.6 1.7 + 1.1 + +
Lepidoptera (Larvae only) 15 12 27 2.1 1. 4 16.5 + +
Hesiptera 15 1.2 2.9 3.2 + 23 20 25
Thysanoptera — — - + — - 3.0 6.2
Orthoptera 4 — - - + — —
Blattodea 1.0 + - + — —
Isoptera — - — — - —
Dermaptera — - - — — - — 1.0
Diplura 7.0 11 16 + 1.2 I4. • 1.8
?rotura 3.1 2.6 3.5 • . .8 11.2 14.2
Symphyla 19 20 20 26 17 146 26 30
Olilopoda 3.5 — 3.1 2.3 + 7.0 1.2 1.0
Diplopoda 211 2.8 2.0 ... • 36 30 29
Pauropoda 7.0 + 5.2 1.7 20 18 143
Pseudoscorpicoes 7.1 16 11 1.8 . + — —
Araneida 14.6 1.3 4.6 1.6 1.0 3.2 1.0 +
Opiliones + - 1.7 - - -
PaLp1gra i 3.8 1.14 + — — 1.0 1.0 1.2
Uropygi - - • - - - - —
Schlzomida - - - 4 - - - -
Isopoda 8.14 1.5 + • • + ..
Olig icbaeta • I + 16 7.5 1.6 + —
Mo lluaca 1.0 — — + — 1.14 + •
Totals 1160 510 1030 577 219 1560 1280 12140
I .. .
97
-------
COVER CROP LONG GRASS SHORT GRASS COVER CROP LONG GRASS SHORT GRASS
_____ Acari Protura
CollemboLa Isotomidae Symphyta ________
0 50 ______
Hymenoptera Formicidcie Chilopoda
L.? ° ‘ “ ‘•‘ 2. r
___Coleoptera 6TS Diplopoda
Lepidoptera (larvae) Pauropooa
I_
P Hemiptaro _______ _______ Other
Arochnida
Diptura F (so poda 025
r Litter
.O—25crn
L2-5—5cmJ 5 I
FIGURE 2 L Plantation Ground Cover Trial, Dean numbers per sample
(fl5 2 )
-------
Forest levels of density arid diversity were not regained. A few
species of Cryptostigm tid mites were disproportionately abundant i’
samples from the Garden. The Coleoptera, Diptera and Ilerniptera
contain many species of varied function, usually with winged adults,
and appropriately adapted species entered the cleared areas as the
habitat became suitable. But, in the Coleoptera for example, the
entry of’ a few open habitat Carabidae did not compensate for the loss
of the many staphylinoid species ocuurring in Forest.
Coconut plantation transect
This area had not been cu].tivated and shows some effects of
vegetatian cover independently of other factors. The fauna unde” Tall
Grass in Zone Ia had some forest-like reatures : maxima in neelid and
neanurid Collembola and the presence of a schizopterid (Hemiptera) and
the pseudoscorpion, Tyrannoohthonius beieri (Figure 3). There was
evidence of interactions with a well established ant fauna. In Zone I
the numbers of mites in samples (log n + 1) were negatively correlated
with numbers of a cryptic myrmicine ant, Monomorium talpa nery, with
a dense nesting population in Zone Ia (Figure 3) (r = —0.5 1,
pcO.UO1). This ant also occurred in the Ground Cover Trial where ±t
was widely distributed and here mites were obtained in about equal
numbers from Long and Short Grass (Table 1). The numbers of
cyphouer’ine Collembola, inhabitants of ant and termite nests, were
positively correlated with total ants from samples over the whole
Transect Cr = 0.614, picO.O01). Two faunal elements that were present
in the Garden reappeared under the sparse vegetation of Zone II of’ the
Transect. They were groups with soil surface or above ground
mobility, at least as adults (spiders, Opi].iones, Diptera,
Lepi optera), and soil inhabitaflts able to escape from the surface
climate (Japygidae, Symphyla) (Figure 3).
Plantation ground cover trial
Most groups wer obtained in the greatest numbers from samples
from the Cover Crop (Table 1, Figu ’e 14). Forest—like elements of the
fauna of the Cover Crop were Pselaphidae and, as in the Long Grass of
the Transect, Neariuridae and Tyrannoohthonius beieri . In the Short
Grass the lack of protection from insolation seems to have caused
downward rnovement by the fauna. Depression of vertical distributions
here as compared with the Long Gra s is seen in 10 out of the 114
groupn in Figure 11. The proportions of total individuals extracted
from soil anc coming from tl’e lower soil samples were: Cover Crop,
211%; Lone Grass, 21%; Short Grass, 33%.
D3.atribution of isotomid SpCCiêS
Four comson isotomid species on each site formed a
morphosequence of increasing adaptation to lifc. in mineral soil. This
involves differences between species in development of the ocelli,
pigmentation, length of appendages (Christiansen, 19611), nd shape or
abdomen: fusitorm with tip horizontal in surface and litter species,
99
-------
cylindrical with the tip reflexed in soil inhabitants. The species
can be scored 0 to 2 for each these characters and the sum used as a
measure of adaptation to mineral soil : Cryptopygusthermoohjlus
(Axelson), 1; Isotomiena minor(sc iärrer),1s; Folsomidea exiguus Folsc ,m,
7; Isotomodes trisetosus Dents, replaced in the plantation transect by
I. productus (Axelson), both 8. The distributions of theso species in
Figure 5 show typical vertical patterns in the Forest and Cover Crop
(Figure 5a, a) with C. thennophilus mainly in litter while Isotomodes
penetrates mineral soil to a greater extent.
In the Shifting cultivation sequence (Figure 5a), clearing
Forest greatly reduced the number of the two species most dependent on
a litter layer (compare pseudosoorpions and Diplura, Figure 2). In
the single stratum of samples from the Plantation Transect (Figure 5b)
the order of increasing penetration of Zone II was the same as the
order of penetration of soil in Forest (Figure 5a), a consequence of
the surface climate affecting upper profile more than lower profile
species (compare Japygidae and Symphyla, Figure 3).
In the Plantation Ground Cover Trial the greatest ni.imbers of
Isotomidae came from samples from grasses, the reverse of the
treatment distribution of most of the rest of the fauna (Table 1). In
the Short Gra s, where the rest of the rest of the fauna moved away
from he poorly protected soil surface, most Isotomidae came from the
upper samples (Figure 5c). As the fauna as a whole returned towards
the surface in the Long Grass, most Isotomidae came from the lower
samples. This suggests that diffuse interaction with other fauna is
an adverse factor operating against Isotomidae at the level of the
lower sample in the Short Grass, almost eliminating Isotomodes , and at
the level of the upper sample in the Long Grass, releasing
Isotomodes . It is not possible to be more specific as to the nature
of the interaction since all the taxa likely to be important as
competitors or predators of isotomlds had similar vertical
distributions (Figure l4)
Composition of isotomid associations
The contributions of each of the four species to total
Isotomidae in eaoh treatment are compared in Figure 6. Most tropical
forest soils little organic matter (Lee 1969; Burnham 1975). They are
not a favourable environment for soil—inhabiting Collembola and in the
Forest (Figure 6a) Isotomodes was poorly represented. By analogy with
the Plantation Ground Cover Trial, the two litter species were
adversely affected by interaction with the rich fauna of the litter
layer. The long grass of the undisturbed Transect had the most
forest—like plantation fauna and its isotomid association resembled
that of Forest (Figure 6b), although lower diversity near the surface
seems to have allowed an increase in the representation of C.
thermophilus The immediate effect of clearing Forest on upper profile
Isotomidae is shown again in Figure 6o. They may have been barred
from the Garden (Figure 6d) by the other two species and the rapid
entry of paronellids. The similar combinations of species is Zone II
500
-------
FOREST
CrypIopy j
thermophElus
IsotolTido
niwior
Folsomides
Isotomodes
trisitosus F
Cryptopygus
therrnoph is
is’ tomidlo
mi or
r Litter
______ I- O-25cm .,
L 25-5cm J
FIGURE 5. Isotocnidae (Collembola), mean numbers per sample (a)
Shifting Cultivation Sequence; (b) Coconut Plantation
Transect; ( ) Plantation Ground Cover Trial.
BARE GARDEN
GROUND
Zot* I Zonsfi
a
Short Long’ Sparse Wood
IGra Covw
I Ii I.i
I
10
5
0
5
o J
It
(b)
0
Litter
O-25cm
(°) 5-lScm 15011
IO I 2 .ScmJ
Isotomi&la

•LI bLIA
I ‘Felsomiass
I S iQII4
JL 4U 1a
r pI L 1 .J:L
QUADRAT
COVER
CROP
LONG
GRASS
SHORT
GRASS
E’ fl d,$
lsutomods
trisitosus L j
(c)
li
501
-------
Scale
6 50
Ground (di Garden
.
L
If) Transect
Short Grass ifa)
FIGURE 6.
I
v v.
fl ransed
Weed Cover(fl)
I
.
Ground Cover Trial
Short Grass
Isotomiclae (Collembola): t ta].
each of four species expressed
isotoinid individuals (see text
(ii Cover Crop
numbers of individuals of
as percentages of botal
for explanation).
Forest

KEY
ryptppyg
therrnophla
Isotomuella
minor
Folsqmudes
species
(hi Ground Cover Trial
Long 3rass
502
-------
of the transect (Figure 6e) but with only the uppermost species
lacking, can be related to the climate of the soil surface. Under
short grass in Zone I of the Transect (Figure 6f) the ant Monomorium
appears to have suppressed lower profile Isotomi ae as well as
mites. The isotomid associations of grasses in the Plentation Ground
Cover Trial (Figure 6g,h) were accounted for in the previous section.
The effects of cultivation account for differences in the
Isotomidae of the two long grass areas (Figure 6bh). In Zone lb of
the Transect the fauna wes concentrated in a mat of grass litter and
roots near the surface. In the Ground Cover Trial, cultivation
destroyed this mat and incorporated it into the mineral soil to a
deptn of ca 5cm, thereby impro rtng the habitat for lower horizon
Iaotomidae • The balance of species in the Cover Crop (Figure 6i) can
be seen an transitional or intermediate between the association in
Figure 6h and those in Figures 6a,b.
DISC’JSSION
The responses of the soil fauna to disturbance such as
cultivation or clearing forest emphasize the importance of the gross
morphology of different taica. This determines species’ mode of
locomotion on which depends the ability to survive the disturbance by
escaping into the soil and the capacity for recolonising by
migration. A distwbed fauna’s recovery may be slow, limited by rates
of recolonization; the ant communities of’ these si’.es take several
years to adjust after disturbance, even though the local ant fauna
contains many widely distributed, vague species (Greenslade and
Greenslade 1977). Any discrepancy between potential and actual
biomasa or density of’ the soil fauna leaves a gap of unused or
inefficiently used resources into which opportunist species such as
these Isotomidae are likely to expand. Rere their occurrence has been
explained in terms of two processes, neither of which are sufficient
alone: first, there is the action of the same factors that determine
the suitability of habitat for other members of the fauna: climate,
structure, food supply, effects of ants. Secondly there is diffuse
interaction with other soil animals. Whenever the rest of the fauna
is poorly developed those isotomid species’ different but overlapping
habitat requirements allow one or more of them to exploit an
opportunity at any level in the upper part of the soil profile.
Opportunist behaviour and diffuse interaction are to be suspected
whenever a taxon shows ecological rtlease in that its distribution
runs counter to the main patterns seen in the rest of the fauna (e.g.
Diplura, especially Japygidae, Syinphyla, Figures 1-EU.
Dirruse competition Ms been notea also amongst the ants of
these sites (Greenslade and Greenslade 1977). If this, or more
broadly, diffuse interaction, is frequent in communities of soil
animals, quantitati e studies of single species in isolation may be
misleading. Relationships with a variety of other species could be
overlooked. But there are difficulties of sampling, extraction and
503
-------
identification when many species are considered simultaneously. Vlijm
Vander kraan and Van Wingerden (197i) recommended quantitative :3tudies
of ‘Key—species’, the most abundant apecies at each trophic level
whose direct fUnctional relationships form a community’s ‘Skeleton’
(Elton 1966). They also refer to Elton’s ‘Girder system’ of indirect
relationships involving rarer spec ee. ‘Damping down fluctuation arid
slowing down deviation from the norm.’ The process of diffuse
competition and the activities of opportunists such as these
Isotomidae are part of the girder system. Diffuse competition appears
to be one of Elton’s (1966)’ Strong ecological .forces against
monopoly’ (Greenslade and Greens].ade, in press).
Anderson arid Healey (1972) proposed that fugitive species of
Colleinbola might coexist with superior competitors by moving between
temporarily unexploited patches of their habitat, behaviour similar to
that described here for opportunist Isotomidae, and by Kaczmarek
(1975a,b). To use a single terminology, both opportunist and fugitive
species are r—strategists In MacArthur ard Wilson’s (1967) r — K
spectrum (Southwood 1977). The oollembolaL family Isotomidae contains
.nany species that occur in species—poor communities in disturbed and
tempora”y habitats, on the sea—shore, i i deserts, on mountains and in
polar regions (e.g. Greenslade and Greenbiade, 1973). These
environments represent the area in Southwood’s (1977, Figures 10,13)
‘Habitat te•ipiet’ of r— and Adversity—selection (Greenslade and
Greerislade, in press). The species of Cryptop !., Isotomiella,
Folsomides and Isotomodea that we discuss here ere clearly
—strategists apart from the evidence of the present observations.
They have efficient dispersal mechanisms and are widely distributed,
all being cosmopolitan except f or Folsomides which is found
throughout Australia, the Pacific and tropical Asia. They are
prominent in temporary habitats and may reach hig i densities there.
We see I ere how r—strategists such as these isotoiaids can also play a
part in species-rich, stable, favourable environments.. They have the
potential to bUffdr the effects of temporal change in the supply of
resources caused by variations in weather or densities of key—species
within ‘norii’al’ ranges of variation. The popuLations that expand most
rapidly if the availability of a reaour’-e increases are those of
r ’—seleoted species and they are most uaoeptible to the effects of
intensified competition as the supply contracts.
ACICNDWLEDG 4ENTS
This work was carried out while the senior author was in receipt
of a research grant from the Royal Society of London.
LITERATURE CITED
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variations in major components of th gut contents of some
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Bullock, J.A. 1967. The Arthropods of some tropical soils and leaf
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methods for terrestrial arthropods, pages 150—185 in Phillipson,
J. (Ed.) ‘Methods of study In quantitative soil ecology.’
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Greenalade, P.J.M., and Greerislade, Penelope. 1968. Soil and litter
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Greenslade, P.J.M., and Greenslade, Penelope. 1977. Sose effects of
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Kaozmarek, H. 1975b. Influence of humidity and specific interactions
on collembolan populations in pine forest, pages 333-339 j J.
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Lasebikan, B.D., Belfield, W., and Gibson W.H.B. 1978. Comparison of’
relative efficiency of methods for the extraction of soil
arthropods. Rev. Eec .. Blo].. Sal. 15 : 39—65.
Lee, K.E. 1969. Some soils of the British Solomon Islands
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MacArthur, R.H. 1972. ‘Geograph eal ecology, patterns in the
distribution of species.’ Harper and Row, New York.
MacArthur, R.H. and Wilson, E.0. 1967. ‘The theory of island
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Jersey.
Manton, S.M. 1972. The evolut1oz of arthropodan locomotory mechanisms.
Part 10. Locomotory habits, morphology and evolution of’ the
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Southwood, T.R.E. 1977. Habitat, the templet for ecological
atrate&. ? J. Anim. Ecel. 46 : 337—365.
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506
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FEEDING BEHAVIOR AND FUNCTIONAL ECOLOGY OF
TERMITES OF A TROPICAL SAL FOREST
Udai Raj Singh
Md,ht Collegr of Sn,nce
India
INTRODUCTION
Ecological systems must be systematically anallzed for revealing
structure and function of the components in order to have a better under-
standing ansi intelligent manipulation of the ecosystem. Ecology ef termites
has hardly passed the stage of recording facts. The observed facts need
a synthesis with a view to test the concepts of ecology. On the basis of
nonographic studies of all the termite species regarding distribution,
biotope niche, diversity and abundance, certain theories may be developed
to determine the role of termites In the ecosystems. It is Important to
determine their function of decomposition of cellulose, as It may effect
the soil. Their role in the regenoratlon of vegetation may be more important
tnan the damage they might cause to agriculture and forestry.
Macfadyen (1963, 1964) constructed a balance sheet for total annual
flow of energy through a temperate Eleadow supporting domestic cattle. Of
the total energy captured by plant via photosynthesis, less than 1/7 is
respired by the plants, 2/7 is consumed by herbivoures and 4/7 are exploited
by “decomposer industry” after the plants have died. There are no comparable
figures for tropical grasslands where termites are often very abundant and
where they influence the flow of energy at both the herbivore and decomposer
level. In such areas the relative respiration of herbivore and decomposers,
and thus the fate of plant tissue (primary production) may be strongly
influenced by the relative abundance of .erbivorous and saprophagous termites.
The most obvious component of a tunctionol niche is nutrition. The
food taken from the environment is experimentally defined. Vegetative
material contains protein, lipids, nitrogenous bases, and other organic
compounds, minerals and water, besides various carbohydrates. The latter
constitute 18.7 % by weight of a fresh praire grass (Bouillon 1970).
Within the same habitat different species of termites may have a choice
of plant species or their special tissues. Beyond the spatial and
ecological diversity and decomposition agents which prepare and are a
component of diet of many termites. They are present In Its general
environment, In its nests, and in its digestive tract when different
groups of decomposition agents succeed and replace one another. The
gradual action of many successive decomposers facilitates to complete
the mineralization of plant material.
OBJECTIVES
The goals of this study about two numerically dominant species of
termites, Odontotormes obesus Rambur and Odontotermes redemanni Wasn’ann
of a Sal forest at Varanasi, India and to provide quantitatlveIaseline
data for compartment modelling in the Indian MAB context to help better
understand ecosystem.
507
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Field Activities of Termites Studied
The annual cycle of population, swarming, Foraging and construction
activities on Odontoteriues obesus and 0. redomanni based on the field
observations is presented in Figure 1.
METHODOLOGY
Rearing and Maintenance of Termite Population in Laboratory
An incubator was used as an environmental chamber for laboratory
rearing. Temperature and humidity within the incubator was controlled at
the mound level in complete darkness. The food preference was tested by
feeding inside incubator.
Caloric Estimation
The calorie estimation of all the ecological materials was do;ie by
Parr Plain Oxygen Bomb Calorimeter (Parr Instrir.ient Company Manual 1968).
Respiration Studies in Laboratory
Respiration measurements were made on individuals of each c s e in
a Warburg respirameter. The bottom of the respiration chamber had an area
of approximately 15 cm 2 , whiCh is large enough to permit considerable
movement of tcv’ml te (WTegert 1970).
RESULT AND DISCUSSION
Feeding Habits and Food Preferences
The workers are the only members of the colony which can feed them-
selves, whereas the other castes are fed by theii on the r urgitated and
partially digested food. Unlike the finding of Arora and Gilotra (1959),
no cannibalism was abserved during this study, in either of the species.
The queen was noted to secrete a fatty substance through the pores of her
abdomen and the workers were seen licking the sides of her abdomen. Arora
and Gilotra (1959) have also reported this behavior. Rajagopal and Veeresh
(1976) have studied the food storing habits of Odontotermes wallonensis
and have reported that they store copped food material from grasses,
graminaceous seeds and bark pieces of 1 to 2 nun size in separate cavities
which are modified chambers in the middle of the termite mound. But
during this study, 0. obesus and 0. redernanni both were noted on the semi-
decomposed (1nfecte by fungus) n Tst pieces of non-leaf litter and leaf
letter of Shorea robusta . When the litter pieces are kept with the
fungus garden (freshJ the Individuals are noted to prefer the leafy one.
None of the test species was observed feeding on the heart wood. Among
the leaf litter 0. obesus was found to prefer the softer part first, while
0. redeinanni took the vein part first. Some blotting paper pieces were
iTso tested for food but none of the species prefered them. Results of
of food preference tests are given in Table 1.
508
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Figure 1.
A COMI4ON GRAPHIC REPRESENTATION OF ANNUAL CYCLE OF POPULATION.
S ARMING, FORAGING AND CONSTkUCTION ACTIVITIES IN Odon termeS
obesuS Rambur and 0. redem!fli!i.. Wasmaflfl (Based on fTëld obierva-
ti oi iY .
509
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V
Table 1: FOOD PREFERENCES OF ODONTOTERMES OBESUS AND 0. REDEMANNI
FOOD
DEGREE OF
CONSUMPTION
Q.. obesus
redemanni
Heart wood of sal
Not consumed
Not consumed
Fresh bark (living)
Not consumed
Not consumed
Dry moist dead bark
Consumed
Consumed
Veins of leaf litter
Less consumed
More consumed
(moist)
Softer part of leaf
Heavily cor sumed
Heavily consumed
litter (moist)
Fungal infected leaf
Se erely consumed
Severely consumed
and non-leaf moist
litter
Fungus conth
More severely
consumed
More severely
consumed
Cow dung (not fresh)
Heavily consumed
Heavily consumed
According t Kushwaha (1964) 0. obesus eats the seedlings of different
plants like Mang ifera indica and Citrus while Chatterjee (1970) reported that
Eucalyptus is perhaps the worst sufferer of 0. obesus feed. Agarwal (1970)
has observed the species feeding on sugarcane also.
Energetl cs
Energy Is the driving force of the system. A part of energy exposed
to decomposer system, (input to decomposer cycle) Is utVlized by the termite
population. The major proportion of this utilized energy is spent on the
maintenance of population that can be referred to as maintenance cost.
This is measured by respiratory energy loss. The remaining part of the
utilized energy has two channels. A part of it goes through tne first
channel, the deconposer system through faecal matter. The rest of the
energy is stored in second channel in form of tissue growth. Some of the
energy also goes into the decomposer system through death and decay of
Individuals.
Energy Intake by Termites
Laboratory coloiiies of 0. obesus consumed more litter than 8% of
their body weight/day, whereas in 0. redemanni this value reaches about
10%. Both the species can consume more than 9% of their oven dry body welght/
day (Tables 2A, B). In terms of calorIes, 0. obesus consumed 352.2 cai/]
termite/day and 0. redemann 404.34 cal/g termite/day (Table 2A). Of the
amount eaten, 51T(181.6 cal/g termite/day) in 0. obesus and 41% (165.6
cal/g termite/day) in 0. redemanni are assimilated. Seifert (1962) found
that in feeding experiments. kalotermes flavicollis , with a mean weight of
510
-------
Table 2A CALORIC INGESTION, ASSIMILATION AND EGESTION
BY TERMITES (CAL/G TERMITE/DAY)
OF LiTTER
ASS 1111 LATION
EFFICIENCY 1%)
about 7/mg/animal. att 0.16 - 0.18 mg of pine sap and heart-wood per day, i.e.,
2-3% of fresh body weight. More than 60% of the amount eaten was completely
assimilated (0.098 - 0.11 mg/termite/day or 13.0 to 15.7 mg/g termite/day).
Tue rates of food consumption of Nasutitermes exitiosus, measured by Lee
and Wood (1971), are less than half that measured by Slefert (1962) in
K. 9aivollis . In both the cases, cultures were maintained at 26°C, but the
ffifferent termite species used may have affected the results. The food
material tested was different, and the culture methods u%ed by Siefert
differed in many respects from that of Lee and Wood (1971). The assimilation
rates measured In my present study are nearer to those of Lee and Wood
(1971) wiio reported it to be 54%. But It is lower than that of K. flavicoills
as recorded by Seifert (1962)
T, e mean energy intak e by total termite population In the study area
is more than 34 cal/mZ/day which comprises about 19 ca of energy consumed
oy 0. redemannl and 16 cal by 0. obesus populations /m 2 /da (Table 3).
Egested energy was calculated by subtracting the percentage of assimilation
(51% 0. obesus and 41% 0. redemenni ) from Ingested energy values. Because
of the higher assimilation efficiency of 0. obesus than that of 0. redemanrij
the calculated ege ted energy of redemanni (1IT1 cal/m’/day) T more
than that of 0. obesus (7.85 cal/i /day). In contrast, 0. redemanni (Z.7 cal/
m 2 /day) could aslimilate less energy than that by 0. obcsus (8.13 cal/me/day).
SPECIES
coNsuMPTION
(C)
ASSIMILATION
(A)
EGESTION
(C-A)
Odontotermes obesus
356.20
404.34
181.56
165.65
174.6
238.7
0. rederianni
Table 2B FOOD (DRY ‘..EAF & NON-LEAF LITTER) CONSUMPTION,
AND ASSIMILATION BY TERMITE (MG/G TERMITE/DAY)
EGESTION
SPECI ES
CONSUMPTION
EGESTION ASSIMILATION
O.obesus
87.3
42.8
44.5
51
ii.
redemanni
99.1
58.1
40.6
41
5U
-------
T$ b . 3- I tak sge.Uon ai sisiatlation of ei.zgy by tsz,gtsi in Yaranasi forast (on1/m /da!)
- toterns obeaU 2. xeder mjt Total on a sa bars
I ?T?
za k; e iin atT — — rursr.
tLOII.
1925
Janusgy 12.7549 6.3531
6.4013
14.5982
0.6170
6.0213
27.4533
14.9291
12.5028
Pebnisq 9.5888 4.7002
Mardi 8.5654 4.1985
4.8725
4.3524
3.7.0124
11.4804
.O.0432
6.7833.
6.9696
4.7072
26.6013
.0462
14.7435
9.5117
14.9157
9.0536
Apr11 6.7787 3.3220
3.4445
0.V927
5.3132
3.6872
13.7714
8.b352
7. 1317
May 9.6051 4.7082
4.8807
11.3470
6.7o42
4.7042
4.6325
Z.9521
11.4124
Juns 21.6821 10.6280
11.0176
24.0720
14.5844
9.0701
45.7541
25.2124
20.8J77
July 36.4845 17.0837
18.5393
33.5022
22.7487
15.7868
74. 867
43.6324
34.3261
Auçjugt 26.3689 13.3991
Scptei .r 25.6291 12.5627
27.8012
13.0232
1..4240
31.3370
11.4260
18.5 .b2
11.3991
12.8489
54.1701
56.i .291
29.8591
31.0779
24.7982
25.0721
October 11.8148 5.7913
6.o 36
13.3495
7.8874
S.4’36
25.1643
13.6787
11.4772
övsmbsr 11.8076 5.7878
5.9999
14.4377
8.5303
5.9198
26.2453
14.3181
11.4772
Os smbet 10.9838 5.3849
5.5823
13.4897
7.9703
5.5311
24.4 153
13.3552
13.5526
N s a n 13.0055 7.8434
0.1330
13.7734
11.0931
7.6998
34.7780
18.9470
15.8320
-------
Respiratory Energy Loss
The valuLs of oxygen consumption measured by Warburg’s apparatus
in laboratory are converted to caloric equivale ts and used to calculate
the respiratory energy loss of the termite population both on per mound
and per mater square basis (Table 4). This conve sion Is made on the
assumption that the combustion of 1 litre of 02 (siP) produces 4.7 K cal
biomass (Brody, 1945 and Lee & Wood, 1971). It is evident from Table 4
that the individual energy consumption of workers (0.201 cal/day) and
nymphs ( 0.073 cal/day) of 0. redemanni is more than that of 0. ooesus
(0.196 cal,’day worker and O 5 al/day nymphs). The erverseTs the
case wltn imago (1.21 cal/animal/day 0. obesus and 0.884 cal/animal/
day 0. redeman j ) and soldier (0. obesus 0.22 calianimal/day and 0.
redemanni 0.165 cal/animal/day). In a tatal co ’puted respiratory energy
loss of 14.315 cal/m 2 /day, 3. r demanni (7.365 cal/m 2 /day) loses slightly
more than 0. obesus (6.95 c T/nt/day) does.
Oxygen consumption values from this study in relation to body weight
agree with the values given by Wiegert (1965) and Smalley (1960) for
several species of grasshoppers and Wiegert (1970) for termite ( Nasutitermes
costalis). Golley and Gentry (1964) found the oxygen consumption of ants
of genus Pogomyrmex to be on order of 8—10 times greater than that of
grasshoppers studfed by Wiegert or Smalley. Thur it can be admitted that
the termites are rather sedentary animals compared to most ants; yet they
did not exhibit a moderate amount of activity in the respirometers I.e..
they are more active In nature. Furthermore, this low rate of oxygen
consumption cannot be due entirely to lowered activity levels be:ause seden-
tary mez.dow spittlebug nymphs as reported by Wiegert (1964) had normal
rate of oxygen consumption.
Respiratory CO 2 release of an entire population in nature was measured
directly by alkali absorption method. These values were converted at STP
and their caloric equivalent has been computed. Assuming a value of 6.0
cal/mi C02 with non-protein R.Q. of 0.80, the data are tabulated In Table 5.
It is evident from this table that the respiratory energy loss per in 2 from
0. obesus (15.24 cal/day) population Is higher than that of 0. redemanni
t12.97 cal/day). The ratio of respiration estimated by thc traditional
Warburg laboratory method (14.315 cal/m 2 /da ’) to population resplratloi
measured by alkali absorption method (29.18 cailm’/day) Is 0.496. The
data of respiratory energy loss measured under field conditions are more
than double as obtained by Warburg method presumably because it also
includes the resolratlon of termitophilas, bacteria and fungi. The animals
do not remain as active in the Warburg apparatus as in the field. Secondly,
the respiratory energy loss by eggs has not been Included in the laboratory
method which also adds to the lowering of the total respiratory energy
loss by traditional Warburg apparatus method. Odum al. (1962) and
Wiegert (1965) have also found the laboratory method toIi underestimating.
Wiegert (1970) has also reporte notable difference of respiratory act1 Ity
as measured 4 n field and laboratory. It m y be noted that he used infra—red
gas analyser instead 0 f alkali absorption for estimating CO 2 output. The
real value o respiratory energy loss of population lies somewhere between
14.315 cal/m’/day and 29.180 cal/m 2 /day.
513
-------
Table 4 - RESPIRATORY ENERGY LOS.. OF TERMITES (0. obesus and 0. redeniarini ) i! LABORATORY CONDITIONS
AT NAUGARH FOREST - VARANASI (CALCLJLMTD ON BASIS TH T THE COM USTION OF 1 LITRE OF 02
PRODUCES 4.7 K CAL BIOfIASS - LEE AND WOOD, 1971)
CATEGORY - Odontotermes obesus 0. redemanni Total (O.obesus and 0. redemanni )
Per Per Per Per Per
Individual Moupdl/ nr 2 /day Individual Mound un -Z/day I. dividual Mound m 2 /day
Day Day Day Day Day Day
WORKER 0.196 10670.60 5.2S .201 15000.0 5.9 .397 25S20.5 11.315
SOLDIER 0.220 645.04 0.33 .165 632.3 0.3 .385 1277.3 0.576
NYMPH 0.055 574.37 0.29 .073 1135.2 0.5 .128 1709.4 0.740
II4AGO 1.210 1867.03 0.94 .89 1871.4 0.7 2.84 3738.5 1.684
Total 13756.68 6.S50 -— 18639.1 7.4 32395.8 14.315
All valve ’s are in calories
-------
Energy flow
The food energy metabolized by an animal Is ultimately utilized
in tne performance of several basic organismic functions. As a result,
the total energy budget car be partitioned between the requirements of
basal metabolism (respiratory energy loss at rest) activity expenditure
and production of biomass. Presumably a small fraction of respiratory
energy is lost due to calorigenic effect (increase In heat production
following food consumption when the animal is in a thermo-neutral environ-
ment).
Thus the total energy requirement of an animal population can be
represented by the equation:
1R+P+E
where,
I = ‘.ngestion of total energy intake
R Energy loss at heat
P = Ilet increase in energy content
Energy content of food material egested or eliminated from
the body
The flow component is therefore sum of R + P.
The total annual secondar.X production of 412.5 cal/n 2 /yr (210.95 call
m 2 /yr, 0. obesus and 202.3 cal/me/yr 0. redemanni) is about 7.32% (3.74%
0. obesus and 3.59% 0. redemanni)of the total energy flow (Table 5),
through termite population in the area. But the production of 0. obesus
and 0. redemanni are equivalent to about 7.68% and 7.99%, respectively,
of the annu l energy flow through the population of respective species.
The compartmental flow of energy through termite population at
Varanasi forest is shown in Figure 2.
Maldague (1964), Wiegert (1970) and Hebrant (1970) have estimated
populations and energy flow of termites In tropical rain forests and
savanna in Central America and West Africa. These results have been
compared with those of the present stu iy (Table 6). Wlegert’s estimates
show that termites utilize 0.26% of total available energy which differ
little from my data. While accordinc’ to Maldague’s population estimates,
the termite would utilize about 2.53 of the available food energy.
Although the population /m 2 in Puerto Rico (120/rn 2 ) is more than one and
a flaif times higher than that of Varanasi forest (74/rn 2 ), the total energy
flow of both the studies are more or less similar. In the present study
both the test species have nearly equal share of total energy flow/m 2 /yr.
The total energy flow estimated by Hebrant (1970) was about three times
(14 K cal/ni 2 /yr) more than that reported herein (5.637 K cal/m 2 /yr). Thus
the mound building termites in the Varanasi forest, with a total energy
flow of about 6 K cal/m 2 /year seem to represent only small fraction of
the total input of energy into the detritus decomposers food chains.
515
-------
TsbJ.s °2 iwolutlos - - respiratory sn.z y loss from termite population at study ..tt• infield
c nditLons (energy loan baa been cal ilatsd en described by Wiegext. 1970 — 6 cal/mI C0 2 )
CO 1 evolutlcn/eeun6 Respiratory energy lees oil/day
I ntb ___ Q _ flfl -
1975
January 4354 5053 26124 30318 13.192 U .97 5 25.167
V.bz aary 4201 5256 25206 31526 12.729 1.2.456 25.18$
IIag h 4106 4205 24636 25230 12.441 9.965 22.406
April 3505 4073 21030 24450 10.620 9.6 532 20.302
May 451$ 4384 27090 26304 13.600 10.416 24.096
Jim. 5753 6105 34518 36630 17.431 14. 468 31.899
July 6503 8254 40818 49524 20.613 19.561 40.174
August 1 00 5053 42024 48318 21.222 19.005 40.307
SSpt..b.r 6751 9154 40506 54924 20.455 21.694 42.149
O tober 4655 4955 27930 27930 14.304 11.45 4 25.758
Novuis er 4302 5603 35812 33618 13.035 13.350 26.314
Dscembeg 4405 5501 26430 33006 13.347 13.370 26.384
_ a a a — — — a a — — a — a a — — — — — — a — — — — — _ — _ _ — —
Avsz qs 50w. $ 5883.2 30177 3S399 15.240 12.970 35.150
-------
Figure 2. FLOW OF ENERGY THROUGH TERMITE POPULATION IN VARANASI FOREST
P - Primary Producer compartment
S - Secondary Producer compartment
D - Decomposer compartment
All valu!s are in K. calories; Values on arrows are rates of
flow (/m Ida)
NPP - Approximate net primary productiXity /m 2 /yr
NAD - Net imput to decomposer cycle /m’/yr per mwtwr square/yr.
Sd - standing crop of termite /m’
TU - termite utilization / /yr
TP - termite production /md/yr
R - Respiratory energy loss /m 2 /yr
E - Egested energy line/yr
p
51?
-------
Table 6 - ENERGY CON UMPTI0N BY TERMITES IN TROPICAL. FOREST AND SAVANNA
VEGETATION
I.E R M I I E S
.
‘
—
Species
NO 2

!
BIOMASS
K cal/
g/rn 2 in 2 /yr
Total
Energy
Flow
K call
rn 2 /yr
Productive
o K call
m’/yr
Total
Available
Energy
K cal/rn 2 !
year
%
Energy
Utilized
by Thrmite
References
Rain Various
forest Species - 11.0 133.9* 5290 2.53 Malda9ue
(Yanganti, (1964)
Congo)
Rain Nasuti-
forest tormes
(El Verde, costalls 120 0.075 0.599 5.86 0.474 2255 0.26 Wiegert
Puerto (1970)
Rico)
Savanna Cubite —
(Congo) ermes
exlguus - 1.15 14.00 0.90 Hebrant
(1970)
Deciduous Odonto-
forest termes
dominated obesus 36 0.045 0.259 2.747 0.2109 2489 0.1104 Present
by Sa Study
Varanas, 0. red-
India emaii iT 38 0.046 0.270 2.891 0.2023 2489 0.1161
0. obesus
—+ 74 0.092 0.529 5.637 0.4125 2489 0.2265
0. red-
ia T
* Calculated energy utilization tlna1 of Hebrant (1970) for Cubitermes exiguus —
-------
ACKNOWLEDGMENT
Invaluable guidance and encouragement of Prof. R. Misra, Banaras
Hindu University, Varanasi India is gratefully acknowledged.
REFERENCES CITED
Agarwal, R. A. 1970. Problem of termites of sugarcane in India. Meeting
Termitologist of India, Flew Delhi, 1—12.
Arora, G. L. and S. K. ‘3ilotra. 1959. The biology of Odontoternies obesus
(Rambur) (Isoptera) Res. Bull. (N.S.) Punjab Univ. 10(111, IV):
247—255.
Bouillon, A. 1970. Termites of the Ethiopidn Region. Biology of termites.
Pages 153—280 in K. Krishna and F. M. Weesner (eds). Vol. II,
Academic Press, N.Y. and London.
Chatterjee, P.N. 1970. The role of termites in Indian forestry.. Meeting
TErmitologist, New Delhi.
Golley, F. B. and J. B. Gentry. 1964. Bloenergetlcs 0 f Southern Harvester
Ant, Pogomyrmex badisus . Ecology 45: 217—225.
Ilebrant, F. 1970. Etude de flux energetique chex deux expecs du genre
savanes tropicales de la region ethiopeinne. D. Sc. Memoir,
Universite Catolque de Louvain lab d’ Ecol anim. 227 pp.
Kushwana, K. S. 1964. A note on infestation of termites (Insecta: Isoptera)
around (Jdaipur (Rajasthan) (India) Univ. Udapur Res. Stud. 2
(Spi. No.), 105—107.
Lee, K. E. and T. S. Wood. 1971. Termites and Soil. Academic Press. London
and New York, 1—251.
Macfadyen, A. 1963. The contribution of the microfaur.a to total soil
metabolism. Pages 3-16 in J. Doel:sen and J. Vander Drift (eds).
Soil Organisms. North H Tland, Amsterdam.
Macfadyen, A. 1964. Energy flow in ecosystems and its exploitation by
grazing. Pages 3-20 in 0. J. Crisp (ad). Grazing in Terrestrial
and Marine Environments. Blackwell, Oxford.
Maldague, N. 1964, Importance des populations de termites dans le sols
equaturiaux. Trans. 8th mt. Congr. Soil, Sc Bucharest 3:
743-751.
Oduin. E. P., C..E. Cornell and 1. B. Davendort. 1962. Population energy
flow of three primary consumer components of old field ecosystems.
Ecology 13: 89-96.
519
-------
Parr Instrument Company, 1968. Oxygen bomb calorimetry and combustion method.
Manual No. 130.
Rajagopal, D. and G. K. Verresh. 1976. Food storing habits of the mound
building termite, Odontotermeswallanensis (Wasmann). Proc. All
India Symp. Soil. Biol. Ecol. ( Abst.), p. 29 .
Seifert, K. 1962. Die chemische Veranderung der Boizzeliwond Komponenten
unter dem Einf uuss tierischer und pflanzlicher schadlinge. 4.
Mitteilung: Die Verdauung con Kiefern—und Rothbuchenholz durch die
Termite Kalotermes flavicollis Fabr. Holzforschung 16: 161-168.
Smalley, A. E. 1960. Energy flow of salt-marsh grasshopper popu’ation.
Ecology 41: 672-677.
Wiegert, R. G. 1964. Populatien energetics of Meadow spittlebugs
( Philaenus ! pumerll.Ls 1.) as affected migration and habitat.
Ecology Monog 34: 217-24]
Wiegert, R. G. 1965. Energy iynamics cf grasshopper population In old
alfalfa ecosystem. Oikos 16: 161-176.
Wiegert, R. G. 1970. Enirgetics of nest building termite, Nasutitermes
costalis (Holmgren), in a Puerto Rican forest. Pages 57-64 in
H. 1. Odum (ed). Study of irradiation ecology at EL verde, Puerto
Rico Div. Tech. Inf., USAEC, Oak Ridge.
F
520
-------
SESSION VIII: BASIC SOIL ECOLOGY:
NUTRIENT CYCLING, MICROORGANISM-
FAUNAL RELATIONSHIPS, FEEDING AND
REPRODUCTIVE STRATEGIES
Moderator: Stuart B. Hill
Macdonald College of McGill University
Ste. Anne a’e Bellevue, Quebec, Canada
-------
THE FATE OF CATIONS IN BEECH AND SPRUCE LITTERS
INCUBATED in situ
G. Parmentier, P. Buldgen and J. Remade
Unirercii it Li?ge
Belgium
1wrR xL’rIoN
The aim of the research is to assess the lipact of Spruce
forests upon the environimmt and specially upon the nutrient bidget
ccepare. with the caduceous forests.
FOr this [ irpose, it was decided, in a first step, to study
from a dynamic point of view the leaching rate of cations from
litter falls in a Bee th forest and a Spruce forest. These forests
are located in the “Hautes Ardennes” district, in Belgium, (Alti-
tude 555 neters) on acid bcown soils.
M CS AND MATERIAlS
The cation evolution was recxrded or 27 ucnths in Beech
leaves and Spruce needles in order to know the long term behaviour
of decosposing litters Beec leaves and Spruce needles ware sanpied
in Autunr 1976, air-dried foL 3 éeks to a constant weight after
the nethed of Lousier and Parkinson (1976). Subeanpies ware oven-
dried at 850 C with a view to determining the co ecticn for dry
weight.
Ten grams litter were put in a (1 x 2) inn mash net rectan—
gu].ar plastic bag (20 an x 20 an x 5 cm in size). So, ten grams
litter covered ‘ico cm 2 sthich was similar to the annual litterf all
(Lousier and Parkinson, 1976). The (1 x 2) mu nesh net was chosen
to rrdniinize leaf drop-out and to avoid water umcbilization in the
bag.
Sixty bags were made up respectively tor Beech leaves and
for Spruce needles. The bags were placed on the soil surface.
At each sanpling tine (Ca every nonth), 3 to 5 bags were
taken at random and analyzed for K, Na, Ca, Mg, Fe and Pb by atomic
spectronetry. Besides, a faster netl d was a ].ied in order to assess
the release of netal ions. It was similar to the Nilsson nethod
(Nilsson, 1972). On the basis of the deconposition degree ani5 nvr—
phologica]. features, the Beech leaves ware divided into four dif-
ferent classes ar4 the Spruce Iiee il es into three different classes.
By this way, each class contains leaves or needles decxxiiposed to a
defined degree. After drying, 100 leaves or needles from each class
were mted and weighted separately in order to obtain the sean
weight. Therefore, it was possible to evaluate the nean ancunt of
522
-------
el nts per leaf or per needle.
Besides, leaf falls e recorded in the Beech and Spruce
forests in order to kncw the catk n p001 per surface unit : they
averaged 2908-2836 and 1650 Kg/ha respectively in Beech forest and
Spruce forest.
RESULIS
First, e have evaluated the total input of nutrients by
litterfal]. in both forests by knowing the litterfall anowits and
the cation concentration. We have compared our results with the
data of similar wench forests (Table 1).
TABLE 1. Inpu .. of cations by litter fail (Kg/Ha) in Beech (B) and
Spruce (S) forests.
K Mg Fe Ca
B S B S B S B S
PaL1 entier (1976), Belginat 5.4 2.9 1.4 0.6 0.85 0.78 20 8.5
Ausseriac et al (1969), France 5.6 2.4 1 0.7 0.4 0.4 14.5 11
It will be seen that the anowits of cations in the French
and Belgian forests are similar and that the inputs are always lower
in Spruce forests than in Beech forests. Now, let us examine the
cations evolution during the Beech leaves deco1Tç osition in plastic
nets • The units expressing the cation content v re very inçortant.
Indeed, owing to the decomposition, the ight of leaves decreased
irore or less rapidly. This f ct caused an obvious weight difference
spec filly between the three years old leaves and the just fallen
leaves. This loss of organic matteL conduced to a relative increase
in elenent concentration (Ren ar 1e and Vanderhoven, 1973). But this
relative increase is eliininatedby calculating the cation content as
ng/leaf (or needle) and g/m 2 . We have adopted these units. The
results are sunrnarized in Table 2. In this t- h1e, all the cation
contents are related to the sane initial basis, index in December,
in order to conpare the evolution of the different cation anc .mts vs
tine easily.
523
-------
TABLE 2. Weight and cation contents in Beech leaves. De embe :
index 100.
Leaf weight
K
Na
Ca
Fe
Pb
1976
December
100
100
100
100
100
100
100
1977
January
82
41
55
76
60
113
164
Fe uary
81
30
42
75
71
136
127
May
78
37
41
63
54
168
—
June
77
34
34
56
56
179
176
Augustus
72
39
24
56
54
179
87
September
70
30
21
48
57
233
115
1979
March
66
35
39
41
52
413
279
Septethber
65
23
38
38
27
413
—
October
64
28
24
32
42
388
411
November
64
28
56
33
2(
458
—
1979
March
60
17
—
3
32
501
386
It appears that the riost iaportant leaching process occurs
just after the beginning of the e q eriinent i.e. after the litter-
fall and during the greatest loss of the litter weight. So, 59 %
PotassIum are leached during the first nonth, it neans that 3 • 2 Kg
K/ba are supplied to the bottan I rizons. F\irther losses are then
very low. The one—year-old leaves still contain 1.6 Kg K/ha, then
after bo years’ incubation, 78 % are released only.
Similar trends are obeerved for Sodium, Calc uir and Magne-
s turn contents. H ver, the decrease of Calcium and Magnesium
contents is slower than for Potassium and Sodium and closer to the
weight loss of litter.
On the contrary, Iron and Lead tend to accunuilate during
litter deociiçosition. The Iron and Le I contents are respectively
four tises and seven tii es as high as the initial contents.
Therefore, by considering the cation losses vs lit c.er decom-
position, it is possible to identify three t jpes of ion evolution :
- The first group is mainly represented by Potassium and Sodium evo-
lution, the ions disappear such faster and sore rapidly than the
decrease of organic matter; this is obvious In the first nonths of
incubation.
- In the second group, the release of the nutrients Calcium and
Magnesium is slower. The release of Calcium is rather similar to the
organic matter decrease.
- Finally, Iron and Lead belong to the third gr ip, In which the
contents increase with deoceçosition
As to the Spruce needles deccmçosition and cation contents,
the evolution of needle weights was difficult to assess as owing
to their thin shape, sose needles escap?d out the plastic net making
evaluation of weight decrease and ion content a difficult task.
-------
However, by considering the ion co icentrations the sane
groups of evolution can be recognized as in beech litters (Tab.e 3).
TABLE 3. Cation concentrations in incui ated litters, B : Beech
leaves, S : Spruce need.les (Dec T1ber : 100)
K
Na
Ca
Mg
Fe
Pb
B
S
B
S
B
S
B
S
B S
B
S
1976 L c •
100
100
100
100
100
100
100
100
100 100
100
100
1977 . an.
50
39
67
73
93
90
73
75
138 94
200
122
Feb.
37
30
52
68
93
83
88
68
168 102
157
146
May
48
35
52
59
81
63
69
75
215 132
—
171
Jun.
44
35
44
64
73
57
73
73
232 132
229
185
Aug.
54
31
33
64
78
51
75
60
249 153
121
263
Sep.
43
31
30
68
69
58
81
55
333 140
164
293
1978 Mar.
53
30
59
77
62
71
78
63
626 202
414
341
Sep.
35
32
59
64
57
—
41
60
626334
—
488
Oct.
43
34
37
68
50
53
65
73
606449
642
463
Nov.
44
30
88
77
51
42
41
78
716 426
—
—
1979 Mar.
29
27
—
—
59
53
53
55
835 474
644 463
Concerning 1 tassiuin, it can be assuned that 2 Kg K/ha are
lost during the first ncnth of incubation, which is lower than in
beech litter.
Besides, the ion evolutions were evaluated by the Nilsson
net1 Kd.Beech leaves litters and Spruce needles litters were sampled
fran the soil surface and divided respectively into four and three
fractions in relation to their degree of decomposition (Table 4).
TABLE 4. Cc tion content in Beech leaves and Spruce needles.
a) Beech leaves classes (class 1 : Index 100).
Class
Weight K
Na
Ca
Mg
Fe
Pb
1
100 100
100
100
100
100
100
2
88 22
27
75
68
90
—
3
57 7
18
48
46
70
83
4
37 9
12
32
30
100
116
b) Spruce needles
classes
(class
1
: Index
1(0)
Class
Weight K
Na
Ca
Mg
Fe
Pb
1
100 100
100
100
100
100
100
2
105 28
14
90
52
100
115
3
71 20
9
31
33
120
149
525
-------
Again three groups can be distinguished in Beech litters as
well as in Spruce Litters.
- The group characterized by Sodium and Potassium, in which the
nutrient relea’e is faster than the leaf weight loss. Fbr example,
whereas the decrease of litter weight equals 43 %, the release of
Sodium reaches 92 %.
- The group characterized by Ca and Mg. In these cases, the release
of the nutrient is well cxrretatr.d with the decrease of leaf weight
mainly in the case of Beech litter
- Finally, the acctnailation of Iron and Lead.
plan, in further observations, to divide the lea s and
needles in a greater nuniber of fractions in order to obtain nore
accurate data about the ion evolution. Nilsson (1972), I niayer-
de Snet (1974) arid Migno].et (1977) also noted Lead accunuilation in
litters. Nilsson assuned that this accumulation resulted from a
positive sorption process oDnflected with the leaching fran the tree
canopies and aerosol or n taI ions deposits, Lead being stored in
leaf canopy through root aksorption as expected by Cenayer-de Snet
(1974). Besides, ar upc zards flux of cation cannot be excluded. The
Lead storage may delay the litter decc.ii osition. The sane processes
can be implicated in the Iron accuinilation (Gosz et al., 1973, Lou&..er
and Parkinson, 1 97&). This Iron accunulation could influence the
Nitrogen cycle. Indeed, it could lead to an iimo Llization of nitvate
ions by adsorption on anion exchange sites provided by iron oxidcts
(Vitousek et 1., 1979). Finally, it mist be noted that the relc.ase
of catioris from litters Is cai licated by the fact that the inputs of
rations due to rain. and through fall can be very important and nnich
higher than the cation contents of leaves and needles. For example,
31 Kg K/ha.year are supplied by canopy leaching under Beech forest
i.e • six tines the leaves fall input; under Spruce forest, 17 Kg K/ha
year are contained in canopy leaching, whieh equals also six tines
the Potassium inpit by needles fall.
C(UCLTJSICNS
F an these preliminary data, it can be concluded
- The inputs of the nutrients K, Na, Ca, Mg are higher under Beech
forests than under Spruce forests. This is true for litter J all and
canopy leaching.
- These nutrients are released from the litters mainly at the begin-
ning of the decomposition.
- The fate of nutrient in leaves and needles litter can be characte-
rized by three types of evolution,
- a leaching rate greater than the decomposition rate
- a leaching rate i ore or less correlated with deccstçosition
526
-------
- an accumulation of ion during deco tçosition.
- The supp.y of nutrients by rain and canopy leaching is nore important
than the release by litter.
LITERATURE xri u
Anseenac G., 1969. Production de Utière dana divers peuplesents
forestiers de l’Est de la France. Cecol. Plant., 4, 225—236
Aussenac G., Bonneau M. and I.e Taon F., 1972. Restitution des élé-
n nts rninëraux au sol par 1’ intermëdiaire de la litière ec
des précipitations dens quatre peuplez €nts forestiers de
VEst de la France. Gacol. Piant., 7, 1—21.
BuldgEn F. and Remade J., 1979. Influ ’nce of Enviroriiierital Factors
upon the leaching of i ons in undisturbed microcnsns of
Beech and Spruce litters (to be published).
Berrthard—Reversat F., 1972. Deccqiçosition de la liti re de feuilles
en forêt ombrophile de basse 05th d’ Ivoire. Oecol. Plant.,
7, 279—300.
Denayer-De Sn t S., 1974. Cycle biologique annuel et distrilxition
de planb dana tin pessi re (Picetum) et une hêtraie (Fags-
turn) ëtablies sur m ae roche-im re. Bull. Soc. roy. Bot.
Belgique, 107, 115—125.
Duvigrieaud P. and Denayer-De Snet S., 1969. Litiëre totale annuelle
et restitution des polyéléteii bicgenes. Bull. Soc. roy.
Bot. Belgique, 102, 359—354.
Gloaguen J.C • and Touffet J., 1974. Production de litiëre et apport
an sol d’ élënents minéraux dens une hêtraie atlantique.
Oecol. Plant., 9, 11—28.
Gloaguen J.C • and Touffet 3., 1976 • Production de litière et a ipo 1
an sol d’ êl nents minéraux dens quelques peuplatEnts rési-
neux de Bretagne. Ann. Sci. forest., 33, 87—107.
Gosz J.R., Likens G.E.. and Bormar n F.H., 1973. Nutrient release
fran decammosing leaf and branch litter in the Hu ard
Brook Forest, New Hampshire. Ecol. ncgr., 43, 173—191.
Ledel P., 1975. Le ra çort retcmibée annuelle/litière totale an aol
dana quelgues peuplenents forestiers de Belgique. Bull.
Soc. roy. Bot. Belgique, 108, 261—272.
Len .e G. and Bichaut N., 1973. Pecherches sur les éoosyst ies des
reserves biologiqjies de la Fbrêt de Fontairiebleau. II.
Décxmposition de la liti re de feuilles des arbres et
liheration des biOél LtS. Oecol. Plant., 8, 153—173.
527
-------
Lousier J.D. and Parkinson D., 1976. Litter de...’csçosition in a cool
temperate deciduous forest. Can. 3. Bot., 54, 419-436.
Lousier J.D. and Parkinson D., 1978. Chemical ele entdynamiçs in a
decc r osing leaf litter. Can 3. Bot., 56, 2795—2812.
Mignclet, 1977. Deux n thodes de caractérisation de la vitesse
d’hurnjdffjcation dens les sols forestiers • In : Lohrn U.
and I rsson T. (eds) Soil Organisn as Ccznponents of Eco-
systems, Ecol. Bull. 25, 561—564.
Nilsson I., 1972 ccLmu1atixn of netals in spruce needles and
needle litter. Olkos, 23, 132—1345.
REnacle 3. and Vanderboven C.,. 1973, Evo .uttc of carbon and nitro-
gen contents n incubated litters. P1. Soil. 39, 201-203.
Van Lear D.H • and Goebel N.B., 1976 • T af fall ami forest floor
characteristics in ID1 oly Pine Plantacions in the South
Carolina. Soil. Sci. Soc. m. 7., 40, 116—119.
Vitousek P.H., Gosz .3.R., Grier C.C., Melillo J.M., Reiners W.A.
and Todd R.L., 1979. Nitrate losses frosi disturbed eco-
syst as. Science 204, 469—474.
These researches are supported In part by contract
AW781081 5 to University of Liege (Belgium).
QUESTIONS and COMMENTS
M.S. GflILABOV : Were there animals inside net bags?
Was the increase of lead and iron in percents to dry weight
oi in absolute values?
. REMACLE: The leaves and the needles are air—dried
before being arranged in the net bags. Therefore it can be
assumed that animals can be killed. The increase of lead
and iro 9 are expressed in absolute values (mg/leaf or needle
or mg/rn )
528
-------
ANNUAL CARBON, NITROGEN, AND CALCIUM TRENDS IN
LITTER AND SURFACE SOIL OF A MIXED HARDWOOD
STAND
Mark F. Tardiff and Daniel L. Dindal
SUNY CESF
USA
INTRODUCTION
A large body of literature has been generated, in recent years,
on nutrient cycling in forest ecosystems (Gosz et aL, 1973; MacLean
and Wein, 1978; Lousier ano Parkinson, 1978; Pomeroy, 1970). Most of
this lnfonnau.iuvi Is concerned with litter decomposition and primary
productivity. While chis is important information, one area often
neglected Is the nutrient relationships between the litter layer and
the soil.
The nutrient dynamics of forest litter Is often monitored using
litter bags. This is an ingenious method of analyzing the deconiposi-
tion of a known quantity of litter, but the technique does have its
drawbacks. First, there is the problmn of mesh size. With small mesh
sizes, invertebrates are excluded, and with large mesh sizes fragments
of the litter are often lost. The other serious problem associated
with litter bags is that usually the moisture regime or the litter In
the bags Is hIgher than the surrounding litter. Finally, the mirgatlon
of the litter bags down through the litter layers Is often at a differ-
ent rate than unconfiried litter.
The purpose of this research was 1) to analyze the carbon. ni tro-
gen. and calcium trends in unconfined mixed hardwood litter concurrent
with weight loss for one year. 2) to determine the elemental trends of
the surface soil and relate their nutrient fluxes with litter trends
from the same sites, and 3) to suggest differences between earlier
litter bag-nutrient studies with those of unconfined litter. Correla
tion and partial correlation techniques were used to investigate the
varioLs trends.
METHODS
RESEARCH SITE
A 50 x 50 in area was staked out and subdt i44ed Into 10 x 10 m
quadrats in a mixed hardwood site. Samples were collected in the first
week of every other month for one year, starting In February 1977. The
February samples were collected from under about 70 an of snow, and the
following December samples were collected from under about 10 cm of snow.
Five 10 x 10 in plots were selected for each sampling period.
From each plot, two litter samples (730 cm 2 each) and two soil samples
529
-------
(5 cm diameter x 10 cm deep) were collected. No distinctions of F, 1,
and II layers were possible because virtually all leaf litter dis-
appeared from the soil surface by fall.
LITTER SAMPLE ANALYSIS
The litter was handsorted for macro-invertebrates, then oven
dryed at 60°C for 72 hours and ground In a Wiley mill to pass a No. 20
mesh (840 ,u) screen. Carbon was determined by a modification of the
calorimetric technique presented by DeBolt (1974). Kjeldahl digestion
procedures and an aninonlum specific Ion probe method, as described by
Breainer and Tabatabaf (1972) and Nelson and Soniners (1972) were used
for 1trogen. Calcium determinations were made with a calcium Ion
probe after dry ashing, as described by Allen et al. (1968). Litter
weight was determined to two decimal places. All litter analyses were
run in duplicate.
SOIL SAMPLE ANALYSIS
The soil samples were air dryed and sieved to pass a 4 nm mesh
screen. Carbon and nitrogen levels were determined with the above
technique. Exchangeable calcium determinations were made with a specific
ion trobe after extraction with soldum acetate (Woolsen et al., 1979).
Determinations of pH were made with a Fisher calomel electrode. All
soil analyses were run in quadruplicate.
RESULTS AND DISCUSSION
LITTER SAMPLE WEIGHT (Figure 1)
The first point of interest in the litter sample weight graph Is
the low average sample weight in Decamber relative to the previous
February. Litter fall commenced both years around the second week of
October. In the fall previous to sampling, cold weath* r and accumulated
snow reduced the rate of ramoval of fresh litter by invertebrates. The
following fall was unseasonably warm. Consequently, the Invertebrate
populations were more active, and a substantial amount of the fresh
litter was decomposed and coimninuted before snow accumulation.
The weight loss In litter bag studies often follows a negative
exponential curve. Justification for this relationship was developed
primarily by Olson (1963). Using litter bags Mlnderman (1968) found
that a good negative exponential curve fit could only be obtained with
a hoinogenous litter source. When several types of litter are mixed,
the negative exponential equation is no longer valid. We regressed our
data from this study using both a negative exponential model, and a
linear model. There was no difference between the r square values.
This suggests that our systen with 11 tree species and using leaf as
well as woody bi anch litter In our samples has too many litter com-
ponents with different decomposition rates to fit a negative exponential
model. Therefore, we conclude that the reduction of weight through time,
In our systen is best represented with a linear model.
53°
-------
CNARACTEPJ TPC o/’MI%W HAP P WOOD c g rr UrrEL
Gur.&y 3.. A *YE7TE XPE I M ENIAL STATIOP.J • SOIL E C QLOG LA.BoRArORy. QNON DA&A CO.,r•IY
FlGUs E 2
U -- - 1
APR. JUN. AU6 OCt DEC.
4
H
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0’
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U
0’
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-J
301
—w
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0 •
4’
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I
FE
-------
The increase in litter sample weight in August may be explained
in one of two ways. This could be due to heterogeneity In the litter
layer of the hardwood stand or there may have been an input of fresh
litter in the system.
LIflER NUTRIENT DYNAMICS
Percent Carbon in Litter
In litter bag studies, the percent carbon in the litter Is
usually a constant (Wood, 1974; Bocock, 1963). This is not the case
with unconfined litter (Figure 2). We believe that the increase in
the percent carbon occur as a result of the selective removal of the
more palatable litter, namely leaves, by invertebrates. This more
palatable material would be characterized by a high nutrient content
and a low percent carbon. Virtually all of the leaf litter had been
removed by October of the sample year. The 47% carbon level reflects
the branch litter.
The crease in the percent carbon in August coincides with the
increase in sample weight previously noted. This indicates a litter
input of low percent carbon material, such as flower parts, rather than
sample heterogeneity. The relatively high percent carbon levels in
October and De-ember reflect the high rate of invertebrate activity of
that particular fall; the fresh litter with a low carbon content and
high nutrient content was selectively removed. Therefore the percent
carbon values appear high in December.
Percent Nitrogen In Litter (Figure 3)
There are three sources of nitrogen input to the litter layer,
other than litter fall. These are nitrogen fixation, insect frass,
and rain fall (MacLean and Wein, 1978; Lousier and Parkinson, 1978).
The nitrogen levels In the litter ac any given time reflect the inter-
action of input and removal. Prior to June, the rate of input exceeds
the rate of removal. With the increase of Invertebrate activity In the
sunnier, the rate of removal exceeds the rate of input. There Is a
large confidence interval around the average percent nitrogen level
for February. This is evidence that the subnivian coninunity is a
mosaic of biologically active and Inactive sites (Tardiff and Dindal,
1980). SItes with high inlc’oblal and invertebrate activity have higher
nitrogen levels than areas with little or no activity.
These results are inconsistent with litter bag studies. With
confined litter, the percent nitrogen continuously increases from var-
ious Inputs (Anderson, 1973; Cragg et al., 1977; Gosz et al., 1973).
The decline In the percent nitrogen In unconfined litter is due to the
selective removal of nitrogen rich material by Invertebrates. This
activity is restricted by litter bags.
Litter C/N Ratio
The relationships of percent carbon to percent nitrogen (Figure
532
-------
4) is relatively constant during the first four sample periods. This
is evident also when comparing individual curves of percent carbon
(Figure 2) and pei cent in nitrogen (Figure 3) with the C/N ratio
curve. The drop in April is probably due to an increase in nitrogen
from fixation coupled with a slow rate of removal by the low density
spring Invertebrate populations.
litter bag studies using leaf litter only, usually show a de-
crease In C/N ratio as nitrogen is accumulated (Anderson, 1973; Cragg
et al.. 1977; Gosz et al., 1973; Wood, 1974). LikewIse, in our study
as the various components of leaf litter become enriched with nitro-
gen, and the C/N ratIos of the leaves decrease, the invertebrate
populations remove these components. However, since the net result
is a proponderance of woody branch litter, the C/N ratio may appear
to be constant or to Increase temporarily. An example is the
October C/N ratio which reflects the higher C/N ratio due mainly to
branch litter.
Percent Calcium In Litter
Calcium in the litter may be thought of as originating from two
different sources. First, calcium Is a structural component of
plant cells (Burges, 1956). Second, according to Chandler (1939), cal-
cium Is not retracted from leaves prior to litter fall. Therefore,
there Is a pooling of calcium in the leaves through the growing season
which is reflected in the litter. These two phenomena explain the
trend seen in Figure 5.
The Initial high levels of calcium In February reflect the Un-
retracted calcium pooled In the leaves prior to leaf crop. The large
confidence Interval about this point probably reflects the extent to
which different tree species accumulate calcium in there leaves. The
decline In percent calcium concentration covaries significantly with
sample weight loss of the unconfined litter. This is consistent with
litter bag studies (Burges, 1956; MacLean and Wein. 1978) and indicates
that calcium Is 1nnob1liz d as a structural component in the litter
until It is physically broken down.
LITTER NUTRIENT CORRELATION ANALYSIS (Table 1)
The variables available for litter ccrre lation analysis are car-
bon, nitrogen, calcium, and litter sample weight. Both simple and
partIai correlations were calculated. The partial correlation reflects
the relationship between the two variables of Interest with the effects
of othe other two variables removed. Simpson et al. (1960), Poole
- 533
-------
P/6CIRE 5
‘/M %ED I4MVWOOD og qr UrTER ,
SUNY LAFAYETTE EXPERIMENTAL STATION SOIL EcoLoGy LAE0RAToRy.0 1401.JDAGA C. .frJY
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50
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44
2
F 3.
-------
TABLE 1. LITTER NUTRIEN1 CORRELATIONS
Correlation
Simple Correlation
Partial Correlation
—.654
-.712
Sample WT:C
C:Ca
.178
.275
Sample WT:Ca
C:N
.142
.294
.296
.315
Correlations are significant at .250 (o .O5)
(1974). Snedecor and Cochran (196F) completely discuss this technique
which has the advantage of showing the relationship between two vari-
ables after the effects of other dependent variables have been renoved.
Litter Sarn le Weight related to Percent Carbon
Both the simple and partial correlations relating litter weight
to percent carbon are negative and significant (Table 1). ThIs correla-
tion reflects the different decomposition rates of the constituents of
the litter. The litter with a lower percent carbon concentration
(mainly leaves) is decomposed and conininuted at a faster rate than the
litter with a higher percent carbon concentration (branch litter).
Consequently, as the sample weight decreases, the percent carbon in the
remaining litter Increases.
Percent Carbcn relaxed to Percent Calcium
The simple correlation of percents carbon to calcium Is not
significant; however, the partIal correlation shows a significant re-
lationship between these two variables when the effects of percent nitro-
gen and sample weight are removed (Table 1) Such a correlation is ex-
pected since it indic ates t-at carbon and calcium are related as
structural components in plant material.
Litter Sample..Welght related to Percent Calcium
With these variables the partial correlation procedure indicates
the relationship between sample weight loss and the loss of the calcium
component which Is accumulated In the leaves during growth. The co—
variation of calcium with carbon is not reflected in this partial cor-
relation because the variation due to the carbon concentration has been
statistically removed.
Percent Carbon related to Percent Nitrogen
The correlations represent a constant relationship between these
535
-------
two variables (Table 1). Correlations are mostly supported by the
first four sample periods (Figure 4). Also, as noted before, this
Is not the case with litter bag data.
SOIL NUTRTENT TRENDS
It is inmiediately apparent from Figures 6-8 that carbon,
nitrogen, and calcium are much less variable in the surface soil of
the site than in the litter layer. Less variation is expected be-
cause: 1) these data were collected on only the top 10 cm of soil,
and It is expected that much of the input from the litter as mi-
grated via leaching and faunal activity to the lower soil hc’rizons;
and 2) the relative stability of these nutrient levels probably re-
flects a dynamic equilibrium between cation exchange capacity and
plant root u takc.
The large confidence Interval around the February nItrogen
mean Is probably due to the same mosaic effect noted for litter ni-
trogen. In sections of the surface soil where the microf lore renain
active throughout the winter, nitrogen is pooled. In areas where
mjcroflora were inactive, nitrogen was lost or was not mineralized.
SOIL NUTRIENT CORRECTION ANALYSIS (Table 2)
Percent Carbon related to Percent Calcium
As stated in the methods section, the calcium dor considera-
tion here is only the exchangeable component. These significant
positive correlations reflect the probable interaction of calcium as a
cation and the C.E.C. of humic material.
TABLE 2. SOIL NUTRIENT CORRELATIONS
Correlation
Simple Correlation
.530
Partial Correlation
.390
C:Ca
N:Ca
.872
.786
Ca:pl!
.632
.441
Correlations are significant at .250 ( O = .05)
Percent Nitrogen ...l ated to Percent Calcium
Lutz and Chandler (1946) reported that calcium in soils stimu-
lates microfloral and faunal activity. This interaction Is represented
by the relatively high, positive correlations between percent nitrogen
and percent calcium. As microftoral and faunal populations increase due
to an increase In calcium, more nitrogen Is inniobilized.
536
-------
7,
cHAnAcmrn TIc4 O/’MI%EDI4ARDWOOD ORE T £‘OIL
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FEB. APE. JUN. AUG. OCt DEC.
-------
Percent Calcium related to PH
Three processes may potentially interact to produce these posi-
tive relationships (Table 2, Figures 8-9). First, calcium raise5
soil pH (Lutz and Chandler, 1946). Second, under anaerobic conditions,
such as moisture saturation, microflora produce acidic metabolites
which reduce the pH of the soil and result In leaching of catlons such
as calcium (Gray and Williams, 1971). Third, a soil pH change from
6.0 to 7.0 increases the solublIfty of calcium carbonate from 30% to
60% (Emerson and Green, 1938).
LITTER-SOIL NUTRIENT FLUX (Table 3)
Simple and partial correlations for 1ftter:soll carbon, nitro-
gen, and calcium are not significant. The reason is that the litter
and soil samples were collected at the same time, and these litter
nutrient levels are not reflected Instantanlously in the soil. The data
were rearranged so that the soil nutrient information was compared with
TABLE 3. LITTER TO SOIL CORRELATIONS
Correlation
Without Shift
With Shift
.361
C:C
.254
Ca:Ca
.095
.255
N:N
e118
.008
Correlations are significant at .250 ( .05)
the nutrient information for the litter sampled the preceding period.
This rearrangement showed nutrient løvels In February litter to be
correlated with those pf April soil, nutrient levels In April litter to
be correlated with those of June soil, and so forth. This shift pro-
duced better correletions representing the carbon and calcium fluxes.
The nitrogen relationship did not Improve because nitrogen moves through
the syste at a much faster rate than two months. The actual lag time
for these nutrients could be determined with samples collected over
shorter intervals.
CONCLUSIONS
NUTRIENT TRENDS
1. Data show that weight loss In unconfined litter, in a mixed hard-
wood forest system, Is linear.
538
-------
2. Percent carbon in the total hardwood forest litter increases
through the year. This Is because litter of lower carbo ’ con-
tent (leaf material) is decomposed at a faster rate than that
with a higher carbon content (woody branch material).
3. CalcIum loss I. positively correlated with weight loss In the
litter since calcium Is a structural component of plant tissue.
4. Surface soil nutrient fluxes are of a much lower magnitude than
litter nutrient fluxes.
CORRELATION ANALYST S
1. Litter sample weight Is inversely correlated with percent of
carbon.
2. The percent carbon related to percent calcium correlation Indi-
cates that calcium is a structural component of litter.
3. LItter sample weight related to percent calcium reflects the
loss of unretracted calcium accumulated prior to leaf drop.
4. Percent carbon related to percent nitrogen correlation indi-
cates a relatively constant C:N ratio for most of the year.
5. The soil percent calcium related to pH correlation may be inter-
preted as a biological (Microbial metabolite and physical
(solubility) relationship.
6. Percent soil ritrogen related to percent soil cclclum reflects
an 1 ncrease tn microbial activity with an increase In calcium,
and therefore an increase In immobilized nitrogen.
ACKPIOWL EDGMENTS
This research was supported in part by funds from the Mc lntire-
Stennis Cooperative Forestry Research Program, USDA (SUNY RF No. 210—
L0076).
LITERATURE CITED
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nut ( Castanea sativa Mill.) and Beech ( Fagjis sylvatica L.) leaf
litter in two deciduous woodland soils. I. Breakdown, leaching,
nd decomposition. II. Changes In C, H, N, and polyphenol con-
tent. Oecologla l2(3):25l—2 9.
Allen, RD., J. Hobley and R. Carrierc. 1968.. Comparison of a liquid
ion exchange electrode and the AOAC method for determining
calcium in animal feeding stuffs. JAOAC 51(6): 1177.
5 39
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Bocock, (.1. 1963. Changes in the rnount of nitrogen In decomposing
leaf litter in sessile Oak ( Quercus petraea) . J. Ecol.
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Brejmner, J.M. and M.A. Tabatabai. 1972. Use of an ammonia electrode
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Burges, A. 1956. The release of cations during the decomposition of
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Chandler, RJ. 1939. The calcium content of the foliage of forest
trecs. Cornell Univ. Agr. Exp. Sta., men. 228:4-14.
Cragg, J.B., A. Carter, C. Leischner, E.B. Peterson and G.N. Sykes.
1977. Lltterfall and chemical cycling in an sspen ( Populus
trenuloides ) woodland ecosystem in the Canadian Rockies.
Pedobjol. l7(6):428-443,
De Bolt, D.C. 1974. A high sample volume procedure for the c3lorl-
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Emerson, R. and L. Green. 1938. Effect 0 f pH on Chiorella photo-
synthesis. Plant Physlol. 13:157—158.
Gosz, J.R., G.E. Likens and F.H. Borman. l9 . ‘. -““ -1 ase from
decomposing leaf and branch litter In th uu... ?1rest,
N.H. Ecol. t4onogr. 43(2):173-19l.
Gray, T.R.G. and S.T. WillIams. 1971. SoIl Micro-organisms. Longman
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Lousier, J.D. and D. Parkinson. 1978. Chemical element dynamics In
decomposing leaf tter. Can. J. Bot. 56:2795-2812.
Lutz, H J. and R.F. Cnand !r. 1946. Forest Soils. John Wiley. New
York, N.Y.
MacLean, D.A. an RN. Weri. iS78. Weight loss and nutrient changes
In : ec’ or ng litter and forest floor materIal In the New
w . f re t star!ds. Can. J. Sot. 56:2730-2749.
Mindennan, G. 1968. Addition, decomposition and accumulation of organic
matter in forests. J. Ecciogy 56:355-362.
Nelson, D.W. and L.E. Soniners. 1972. A simple digestion procedure for
estimation of total nitrogen In soils and sediments. J.
Environ. Qual. l(4):423—425.
Olson, J.S. 1963. Energy storage and the balance of producers and de—
composers In ecological systems. Ecology 44:322-332.
-------
Poineroy, L.R. 1970. The strategy of mineral cycling. Ann. Rev. Ecol.
Syst. 1:171-190.
Poole, R.W. 1974. An Introduction to Quantitative Ecology. McGraw-
Hill, Inc., N.Y. 532 p.
Simpson, G.G., A. Roe and R.C. Lewonton. 1960. Quantitative Zoology.
Harcourt Brace an 1 World, Inc., New York, N.Y. 440p.
Snedecor, G.W. and W.G. Cochran. 1967. Statistical Methods. Iowa
Univ. Press., Ames, Iowa. 593p.
Tardiff, M.F. and D.L. DIndal. 1980. A method for pitfall trapping
active subnlvlan invertebrates. Georgia Entomol. Soc. 15(1) 41—46
Wood, T.G. 1974. Field investlgatio’is on the decomposition of leaves
of Eucalyptus delegatensis in relation to env ronmenta1 factors.
Pedoblol. 14:343-371.
Woolsen, E.A., J.H. Axley and P.C. Kearney. 1970. SoIl calcium deter-
mination using a calcium specific ion electrode. Soil Sd.
109(5) :279.
-------
KINETICS OF N-K INTERACTION AS RELATED TO STEM
ROT INFECTION AND WATER HOLDING CAPACITY OF LEAF
TISSUES OF TOMATO PLANTS
S. E-D. A. F...izy
Unwrrsity of Tanh
Egypt
Abstract :
Stem-rot infection followed by lodging and death of tomato
plants occurred following abundant N fertilization. K
fertili,ation was found to red x,e the intensity ot infection.
The relationship between infection and N/K ratio in soil
extract and whole plant tissues and moisture loss from excised
leaves were outlined. K exerted a mixed type inhibition on
the net influx of N H 4 .
Introduction
Abundant N fertilization was found to decrease the disease
resistance of plants to soil born pathogens, as a result of
ri ndering cell wall material more thinner as well as reducing
the incrustation of call walls with silicon and also increasing
the concentration of the soluble amino acids and other pala-
table compounds (von Uexkull,1976 , Ismunadji, 1976 and Mitchell,
et al. 1976). The form of N seems to have an effect on fungus
infectior, abundant NH 4 —N nutrition was found to increase the
infection (Barker, et al. 1967). Potassium, on the oth r hand,
was found to increase the resistance of plants to fungus
infection (Maynard, et al. 1968, Mengel, 1976, and Faizy, 1977).
The objectives of this study were to investigate the
susceptability of tomato plants to stem rot infection by,
naturally occurring, soil born pathogens as affected by dif-
ferent N and K fertilizers as well as its relationship to
water loss from excised leaves and NH 4 —R interaction.
Materials and Methods :
Tomato plants (Lycopersicum esculentum) were germinated in the
field and transplanted (3’) days old) to pots containing saline
soil (pH — 8.5) from Kafr El Sheikh. The plants were fertilized
with a split application each of 1O.g of a mixture of ammor 1 ium
nitrate, superphosphate and potassium sulfate fertilizers.
The mixing was made up in the following ratios (of N P 2 0 5 K 2 0):
(a)1 1— 21—. 31—, 51—v
(b) — 1 2, 1.2 1 2, 2.4 1 2, 3.6 1 2, 4.8 1 2, 5,9 1 2:
Cc) — 1 4, 1.2 1 4, 2.4 1 4, 3.6 1 4, 4.8 1 4, 5.9 1 4:
Cd) 5 1 —‘ 5 1 2.1, 5 1 4, 5 1 64, 5 1 8,6, 1 10.7:
-------
The first fertilizer application was made at 20 days after trans-
planting and the second one 30 days later. Five days after the
first fertili?er application sylnptomo of stern rot infection
(lodging followed by death) were apparent The number of dead
plants were calculated and % infection was obtained.
Two harvests were -taken, the first was taken prior to addition
of fertilizer and the second one 50 days later and at the same
time soil samples were taken. Plant and soil analysis were
carried out as outlined elsewhere (Faizy, 1978) and the net
influx was estimated by the method of Brester and Tinker (1972).
The water loss was estimated by rapidly weighing leaves after
exc sion and % loss in weight was calculated (g/g/min) after
10 minutes at noon.
Results and Discussions
Unlike in other studies (Faizy, l979 made up on soil of the
same area, NH was the dominant form of N and no NO 3 was detected
in the satura€ion soil extract.
The % of infected plants were hyperbolically increased with
increasing the equivalent NIL/K ratio in soil extract (fig. 1).
Consequently the infection was similarly related to the
equivalent N/K ratio in whole plant tissues (fig. 2). The
resistance to stern rot infection was therefore increased by
nigh K nutrition (Maynard, et al. 1968 and Mengel, 1976). One
of the reasons for the induction of this resistar e might be
that K increased the synthesis of cell wall materials on the
expense of soluble amino acids and thus cells would maintain
a mechanical resistar e against fungus invasion (Mengel. 1976)
as well as low palatability.
An increase in water loss from excised leaves was observed with
increasing the N/K ratio in plants (fig. 3). Similarly,
transpiration rate was reduced in sugar beet with increasing
K nutrition (Mengel and Forester, 1973). It was interesting
to n e that the % of infected plants were hyperbolically related
to the water loss (fig. 4). The high water loss might be due
to low protein content of cells (Stutt and Todd, 1969, Gusave,
1965) or high permeability of cell membranes (Mengel, 1976).
The influx of NHA was estimated in the absence of K (average
endogeneous K coircentration = 0.39 ± 0.10 me/lOOg at ) and
in the presence of K fertilizers (average K concentrafl6fc =
0.73+ 0.09 me/bOg at .95 in saturation soil extract). The
response curves were sigmoidal (Faizy, 1978 and 1979 indicating
the presence of at least two active sites per carrier enzyme.
Using the Woolf—Augustinsson-Hofstee plot of the Hill equation
3
-------
ob, C, G=a,c d
C
0
I )
Sc,
4C ’
4
NH 4 / (
fig. 1 St -rot infection (%) as affected by the equivalent
NH /I( ratio in saturated soil extract with different
tr atiT flts.
fig. 2 Stem—rot infection (%) as affected by the equivalent
N/K ratio in & o1e plant tissues with different treat-
ment s.
0
‘3
‘3
c4C
o=I: , .=c 1
I I & I a
2
6
B
S
S
‘0
0 •
..--_-o- ._.C ioNadded
4
12
-------
%
1’2
U)
(A
.2 ‘8
0 )
.1.,
0
0
. . I a
4.
& 12
N/K
fig. 3 The percentage of moisture loss from excised leaves
against the equivalent N/K ratio in ole plant tissues.
C
.2
‘a,
‘4C
C
I—
0
0
a a — - a _ a_ — A —
.4 1’ %
moisture loss
fig. 4 Stein—rot infection (%) as related to
from excised leaves.
moisture loss
0
0
0
0
0
0
0
54 5
-------
I
fig. 5
fig. 5 Woolf—Augustinsson-Bofstee plot 1 showing a mixed type
inhibition of the NH influx ) by high concentration
of K (Ck) in saturation soil Jtract. At 1o p, C the
maximal theoretical NH influx (F ) was 32.5 afld the
affinity or substrate c ncentrati o at half maximal
response (K ) was 1.16. At high C, the F was inhibited
by a factor 5 of 0.85 to 27.5 nd the was
inhibited by a factor e( = 1.35
32•5
27•5
>1
‘V
r 0
1:
039
VCN
-------
(Segel. 1975). Potassium was found to exert a mixed type
in ibiti n on the maximal theoretical net NH 4 influx (3.25 x
10 B/cm /day) by a factor f3 0.65, and on the intrinsic
dissociation constant by a factor of = 1.35 (fig. 5)
It was therefore concluded that plants can be made more disease
resistance with K fertilizers either directly through its
physiological effects on cell constituents ‘r indirectly by
inhibiting the NH influx. This conclusion might be of special
importance to the Egyptian agriculture, especially after the
construction of the Aswan Dam (1964) and the resultant decrease
in K—replenishment of the soil.
References :
1. Barker, A. V., D. N. M iynard, W.H. Lachman (1967)
Soil Sci. 103:319—327
2. Brewster. J.L. and I.B.H. Tinker (1972)
Soil Ferts. 35:355—359
3. Faizy, S. E—D.A. (1977)
P1. Physiol., suppi. 59:13
4. Faizy, S. E—D. A. (1978)
Proc. tnt. Arid Land Conf. on Plant resources, Texas
Tech Univ. (in print)
5. Faizy, S. B—fl. A. (1979)
Agron. Abst. pp.170
6. Faizy, S. E—D. A. (1979)
Proc. 14th colloq. mt. Potash Inst., Sevilla, Spain
(in print)
7. Gusave, N.A. (1965)
Proc. Symp. “Water stress in plants”, Prague pp.117
8. Esmunadji. M. (1976)
Potash Rev. Subj. 23. 49th suite 6/7 pp.4
9. Maynard, D.N., A.V. Barker and W.H. Lachman (1968)
Am. Soc. Hort. Sci. 92:537—542
10. Mengel, K. C1976)
Potash Rev. Subj. 23. 49th suite 6/7 pp.17-19
11. Mengel, K. and H. Forester (1973)
Z. Pflernhr. Bodenk, 134, 2 148—156
]2. Mitchell. G.A., F.T. Bingham, C.K. Labanauskas and D.M.
Yermanos (1976)
Soil Sci. Soc. Am. T. 40:64—68
13. segel, I.H. (1975)
“Enzyme Kinetics”. John Wiley p.214
14. Stutte C.A. and G.W. Todd (1969)
Crop Sci. 9:510—512
15. von Uexkull HR. (1976)
Fertilizing for high yield rice, mt. Potash Inst.
Bern/Switzerland, Bulletin 3
547
-------
SULPHUR TRANSFORMATIONS IN OXYGEN-LIMITED
SYSTEMS: SOILS, SEDIMENTS AND SLUDGES
• S. G. 1-lornor, J. i-I. Waugh and M. J. Mitchell
SUW t CESF
USA
Pr,s,,iI a4dress: Virginia Polytechnic In stitute
USA
Sulfur is a major element essential to all life on earth.
It is constantly being converted, transformed and transported between
major organic and inorganic pools in both natural and anthropcgeni.c
systems. Both biochemical and geochemical pathways are involved
in the cycling of sulfur between these pools in the biosphere, atinos—
phere, hydrosphere and pedosphere. In addition to ics importance as
a major biogeochemical element, atmospheric inDut of oxidized inorganic
sulfur compounds derived from the combustion of fossil fuels has
resulted in a major international research eff ’ct aimed et elucidating
mechanisms and pathways cf sulfur cycling.
Microorganisms play a major role in determining both the magnitude
3nd rates of sulfur fluxes Due to the diversity of metabolic pathways
crerating in natural microbial communities of diments and soils,
in situ inicrobiota are able to transform sulfur through all five
of its oxidation states and to fcrm a variety of inorganic and or-
ganic sulfur species. Biogenic evolution of sulfur compo .rnds is
the least well—known component of the global sulfur cycle; however,
it appears that the majority of liogenic sulfur is evolved in the
forms of hydrogen sulfide (H 2 S) or dimethyl sulfide ((CH3) 2 S)
(Hill, 1973; Moss, 1978).
Environmental conditions required for biogenic sulfide pro-
duction are aet in oxygen—limited, organic—rich systems such as
intertidal ir.arine sands, bogs, marshes, swamps, and their man—made
analogs such ac sewage sludge. Oxygen—limited systems are character-
ized by 1) a high moisture coiitent , 2) a rapid microbial turnover
of labile organic matter, 3) an adequate supply of organic or inor-
ganic terminal electron acceptors, which may replace oxygen in microbial
resp .ration, and 4) a dynamic redox gradient. The fourth
characteristic is a consequence of the first three and is delineated
by a zone of oxygen depletinn.
The lower limit of this zone constitutes the redox discontinuity
layer, where oxidizing processes become displaced by reducing pro-
cesses (Fenchel and Riedi, 1970). By virtue of the dynamic interplay
between net oxidation and reduction of nutrients by the natural
microbial community, this zone represents the area of maximal
bacterial activity and organic matter transformations (Kepkay et al.
1979). Below this zone, reduced products of anaerobic community
metabolism accumulate; these products are toxic to most plants az’d
548
-------
a-imals ar.d to many m.. roorganisms. Oxygen depletion is due to the
combination of low oxygen solubility in water, slow passive diffusion
of oxygen into water-filled pores and rapid biological and chemical
oxygen consumption. Systems which are inrcrmittantly flooded, such
as rice paddies and salt marches, are characterized by a vertical
movement of the redox gradient. During periods of exposure and
drainage, aerobic metabolism similar to that in aerobic soils
proceeds, while during periods of submergence, anaerobic metabolism
prevails (Ponnamperuma, 1972).
Bacterial Coimnuni y Metabolism in Oxygen—Limited Systems .
Since the majority cf metabolism in oxygen—limited systems is
heterotrophic and anaerobic, bacteria are the primary agents in
decomposition, although faunal constituents may serve an important role
in altering bacterial activity (Abrams and Mitchell, this volume).
The natural bacterial conmiunity in such systems can be divided into
three functional groups, based on their respiratory metabolism:
1) facult tive anaerobes, 2) obligate anaerobes and 3) fermentors.
Respiratory reduction of a terminal electron acceptor such as
oxygen or sulfate is directly coupled to the oxidation of a reduced
carbon compound such as glucose; this coupling of oxidation—reduction
react nLLs is required for biological transformation of energy into
adenosine triphosphate (Al?) from adenosine diphosphate (ADP) and
yields carbon dioxide and reduced electron acceptors (e.g., H 2 0,
H 2 S). Aerobic respiration, in which molecular oxygen ( 2 ) is
reduced to H 2 0, yields the maximum quantity of energy (in the form
of ATE, per mole or organic reducing agent. Thus the facultatively
anaerobic bacteria, which are widely distributed in 0 2 -limited systems,
utilize 02 as a terminal electron acceptor as long as a sufficient
quantity is present. The lower limit of 02 concentration which is
required for aerobic respirat5on has been determined to be 3 x lO- 6 N
in several types of soils (Greenwnod, 1961). When 02 is pre t In
lower quantities, facult2tive aneerobes switch to anaerobic respiration,
utilizing nitrate s a terminal electron acceptor (Gambrell and
Patri k, 1970).
The switch to anr*erobic respiration has a profound impact on
the chemical and physical environment, resulting in reduction of the
ucrounding substrate. The relative oxidizing and reducing potential
of natural systems is Indexed by the redox potential or Eh, a measure
of the electron—escaping tendency of a reversible redox system (Zobell
1946). In aqueous systems, the oxidation states of hydrogen, carbon,
nitrogen, oxygen, sulfur and several metals are affected by Eh. 02
becomes undetectable at an Eh of +350 isV. Below +330 isV, nitrate
reduction may be initiated but this process is generally not marked
above an Eh of +220 mV (Patrick and Delaune, 1977).
When nitrate becomes depleted, the metallic cations,oxidized
manganese (Mn(IV)) and ferric iron (Pc(III)), re generally reduced in
that order as electron—rich fermentation products accumulate.
Fermentation differs from respiration in that the total energy—yielding
5 9
-------
redox reaction is intracellular and tne electron acceptor is organic.
Thus a reduced carbon compound suc 1 as glucose Is catabolized to
fermentation end—products such as ethaTiol, succinate, propionate and
lactate (Doelle, 1969). Mn (IV) is reduced to Mn (II) at an Eh of
about +250 my, while Fe (III) is reduced to ferrous iron (Fe (II))
at about +125 mV. These metallic cations play a major role in poising
Eh in natural systems ar.d in determining the solubility of sulfur
compounds.
In the sequential reduction of natural systems, the next major
biological electron acceptor is sulfate. Sulfate reduction is carried
out by a specialized group of obligate anaerobic bacteria, Desulfovibrio ,
DesulfomonasandDesulfomaculum, which reduce suliate to sulfide in
the Eh range of +115 to —450 isV, although an Eh of —95 mV and a pH
greater than 5.0 ts required for initiation of the process (Cappen—
berg, 1974; Zinder and Brock, 1978). The sulfate reducers generally
carry out incomplete carbon metabolism, yielding acetate as well as
CO 2 from substrates such as the fermentation produccs lactate,
succinate, malate and ethanol. Dissimilatory reduction of sulfate
to sulfide is a major mechanism governing sulfur metabolism in 02—
limited systems.
When most of the sulfate in mud or sludge has been utilized,
and the Eh has dropped to less than —250 mV, C02 itself may serve as
an electron acceptor and be reduced to methane (CU 4 ). Therefore,
methanogenic bacteria are restricted to extremely reduced environments,
utilizing low molecular weight organic acids. especially acetate,
plus CO 2 and molecular hydrogen (H 2 ) to form CH 4 (Cappenberg, 1974).
Reduction of CO 2 releases the smallest amount of energy per mole of
re’!ucing equivalent due to the high enthalpy of CR4.
Not all of these sequential redox reactions may occur in a
single 0 2 —limited system. For instance, soils and sediments which
we permanently flooded may not exhibit denitrification since nitrate
may not be present. However, all these reactions may be expected
to occur in alternately flooded and drained systems or in reduced
soils or sediments which are in contact with 2 at the surface. All
microbial metabolism follows similar pathways up to the point of
pyruvace; beyond this point, the divergence of heterotrophic metabolism
results in a variety of metabolic prDducts (Wolin, 1974). During
sequential oxidation of organic compounds, sulfur components are
also nietabolized and evolved in a manner dependent on availability
and on oxidatio i state, as discussed in the next section.
Distribution of Sulfur Compounds in Soils, Sediments and Sludges .
Total sulfur content and major pools in three different systems
are presented in Table 1. The soil data is based on studies of 37
surface agricultural soils in Iowa. The majority of sulfur in these
soils occurs in organic form, primarily as ester sulfates, which
include choline sulfate, phenolic sulfates and sulfated po].ysaccharides.
The carbon—bonded component (C—S) consists primarily of the amino acids
.550
-------
methionine and cy3teine (Tabatabal and Bremner, 1972). The percentage
of ester — SO 4 increasel with depth in soils while the C—S fraction
decrea3ed.
TABLE 1. MaJor Sulfur Pools in Soils Lake Sediments and Sludge
Agricultural’ Lake Sediment 2 Sewage Sludge 3
Soil Oxidized Reduced Oxtdized Reduced
Total SuL ur 0.03 0.16 0.13 1.10 1.22
(% g 1 dry wt)
Sulfur Pools:
(% of Total Sulfur)
1—5 42 0 li 7
S-SO 3 ‘ SO 3 ND ND ND 13 30
FeS, S 2 , HS ND 25 59 0 14
FeS 2 , S 0 ND 0 21 ND ND
Total Inorganic S 1—5 67 80 24 51
Ester—SO 4 31—63 ND ND 37 5
c—S 3—20 ND ND 3 45
Total Organic S 95-99 33 20 76 49
‘Tabataba and i3remner, 1972.
2 Recalculated fron Nriagu and Coke—, 1976.
3 waugh and Mitchell, in prep.
ND = no data
Although sulfur speciation in submerged soils has not been studied
to the same extent, we can predict that at a pH near neutrality organic
sulfur and sulfate would be disslinilated to 11 2 S, thiols and volatile
organic sulfur and that H 7 S would react with metallic cations to forri
insoluble suif ides (Ponnaiipervma, ‘.972; Connell and Patri , 1968). ThIs
type of speciation has been found ir. reduced secliwents of Lake Ontcrio,
where the surface sedimenzs are oxidized and sedimern.’ deeper than
six cr are reduced (Nriagu and Coker, 1976). The redox discontinuity
layer occurred at 4 to 6 cm and this zone contained the highest
concentration of total sulfur, over 65% of which was black, .4mor—
phous iron sulfide (YeS). Above this zone (0 to 2 c i i), 25% of the
551
-------
total sulfur was in the form of FeS and below this zone (8 to 10 cm),
59% was present as FeS. In addition to ?eS, pyrite (FeS 2 ) and
elemental S (S°) were present in reduced sediments. Unlike soils,
less t1 an half of the total sulfur can be accounted for as organic sulfur
in lake sediments, due to the stability of inorganic oxidized and
reduced sulfur.
Sulfur specia.tion in aerobically digested sewage sludge has
been studied in our laboratory and results concur with those of
Sotmners et al. (1977). Tb,. total sulfur content of sludge is one to
two orders of magnitude greater than that in soils and sediments and
spectation reflects the high initial quantity of organic sulfur. As
would be predicted, oxidized sludge retains a large fraction of organic
component, which is evenly divided between two major orgaric pools
while the reduced sludge contains a low percentage of ester—SO 4 but a
high percentage of thiosulfate (S—S03) and sulfite (So 3 ). Although
thes two latter compounds are not found as intermediates in sulfate
reduction, they may be stable intermethates resulting from polythionate
reduction (Chambers and Trudinger, 1975; Docile, 1969). The fraction
of FeS in reduced sludge mayinitially appear to be too low ‘zhcn com-
pared to reduced sediments, but the absolute concentration is f r in
excess of that c ccurring in sediiuer t , and is limited by the avail-
ability of ferric iron relative to sulfide. The excess of sulfide
ions is demonstrated in the evolution of H 2 S in sludge, as discussed
in the next section.
Sulfur Trangfnrmatjong in Oxygen—Limited Systems .
Microbial sulfur transformations can be either assimilatory or
dissimilatory. Bacteria are able co assimilate sulfur from a wide var-
iety of inorganic and organic compounds for synthesis of the essential
S—containing amino e ids methionine and cysteine (Alexander, 1.977).
Under 02—limited co ditiops, the primary S source is reduced organic
S , derived from protein hydrolyses. In soils with low S content,
such as agriculatural soils, sulfate immobilization in an organic form
is the primary transformation. Since the major form of S in oxidized
soils, ester—SO 4 , is not available to plants, fertilizers are routinely
used (Tabatabai and Bremner, 1972).
0 2 —limited systems rich in organic material generelly are not S—
limited, since most of the organic material is derived from S—rich
plant bion’ass. Freshwater macrophytes contain 0.8 to 1.0% S on a dry
weight basis whi.e phytoplankton contain 0.65% (Nriagu, 1968);
bacteria generally contain 0.1 to 1.0% S (Alexander, 1977). The
majority of S transformations in 02—limited systems result in pro-
duction of volatile inorganic or organic su1fides see Figure 1.
Sulf ides may be released a 1125, or bound as metallic suif ides, de-
pending on the availability of cations n pe i, 1972). Pyrite
formation occurs in reduced ssdimer.ts when ferric sulf ides are under—
saturates and soluble sulf ides are present (Howarth, 1979).
552
-------
FIGURE 1. Major microbial sulfur transformations in oxygen—limited
systems.
N
(CH 3 ) 2 S (CH 3 ) 2 S 2
553
-------
In saltmarsh sediments, where sulfate levels are very high
(approximately 28 mM), sulfate reduction is not controlled by sulfate
supply but by temperature, H 2 availability and nutrients, ospecially
lactate (Nedwell and Abram, 1979; Rees, 1973). In freshwater marshes
and submerged soils, where the sulfate concentration is below the
level necessary to saturate enzyme activation sites, sulfate re-
duction is limited primarily by sulfate concentration. Diffusion
rates of R 2 S from flooded soils, sediments and sludges depend not
only super.aturation of metallic cations, but also on diffusion and
mass flow (Kleiber and Blackburn, 1978). Respiration rates of
very reduced systems, such as sewage sludge, are controlled in part
by outward diffusion of reduced products which are toxic if
concentrated (McDonnell and Hall, 1969).
Evolved H 2 S may be biologically or chemically oxidized. These
oxidized compounds may combine with atmospheric water and be returned
to the earl’h’s surface in the form of acid precipitation (Likens
and Bormann, 1974). Alternatively, suif ides may be biologically
oxidized ‘o sulfates and elemental sulfur by the chemoaututrophic
bacteria Thiobacillus or by the photosynthetic bacteria Chlorobium
and Chromatium (Doelle, 1969). Elemental sulfur may then be further
oxidized to sulfite, tfiiosulfate and sulfate by other members of
Thiobacillus or serve as an electron acceptor, as can sulfite and
thiosulfate.
H 2 S can also be released in di imilatory metabolism of organic
sulfur compounds, as can the volatile organic sulfides methane thiol
(CH 3 SH), dizrethyl sulfide ((CH 3 ) 2 S, dimethyi. disulfide ((CR 3 )2S 2 ),
carbon disulfide (CS 2 ) and carbonyl sulfide (COS), as noted in Table 2.
(CH 3 ) 2 S 2 is formed as an oxidation product of CH 3 SH (Segal and Starkey,
1969). Organic sulfide evolution in o ddized soils occurs generally
when the organic content is greater than 5% on a dry weight basis
(Banwart and Bremnez, 1976a). However, when oxidized soils are water-
logged, even those with low organic Content evolve suif ides, primarily
in the forms of CH 3 SH and (CR 3 ) 2 S. Thus organic sulfide evoli.tion
is noc restricted to reduced systems but lb. enhanced by 0 2 —limltation.
TABLE 2. Volatile Sulfur Compounds Released from Soils, Sludge—Amended
Soil and Sludge
Organic
Sample Type Matter (%) Treatment
Belinda 1 Silt Loam 2.17 A None
W CR 3 SCH 3
Sharpsburg 1 Silty Clay Loam 3.91 A None
V CR 3 SCH 3 , CR 3 SSCH 3
591w
-------
TABLE 2. (Continued) Volatile Sulfur Compounds Released From Soils,
Sludge—Miended Soil and Sludge
Organic
Sample Type i4atter (7.) Treatment
Hayden 1 Sandy Loam 5.78 A CR 3 SCH 3
W CH 3 SCH 3
Okoboji 1 Silty Clay Loam 12.1 A None
‘•1 W CH 3 SCH 3
Soil + Sludge A CH 3 SCH 3 . CR 3 SSCH 3
W CH 3 SH, CH3SCH3,
CH 3 SSCH 3
Sandy Soil + Sludge 2 A C}I 3 SSCH3, CS 2
V CHiSH, CH3SCH 3 ,
CILSSCB 3 , COS, CS 2
Sludge 3 60 A H 2 S, CH 3 SII, CH 3 SCH 3
V HIS, CH3SH, CH 3 SCH3,
CH 3 SSCR 3
‘Banw3rc and Bremner, 1976a.
2 Benwart and Bremner, L976b.
3 Hornor, in prep.
A Aerobic
V = Water—logged
Sludge—amended soils evolve a variety of orgauic suif ides under
both aerobic and water—logged conditions. Sludge alone evolves these
compounds as veil as H 2 S under similar Incubation conditions. The little
that is known about the mechanisms and organisms responsible for evolution
of these compounds in soils and sludges is derived from pure culture
work and from sulfur—amended soils and sludges (Bremner and Steele, 1978).
The prJ’nary organic sulfur source for H 2 S formation is cysteine, while
the majority of the organic gulf ides are derived from methionine (Francis
et al., 1975). Several bacterial isolates including Clostridium,
PseudolnorLas and Achromobacter have been found to dissimilate methionine
to vo atile suif ides (Segal and Starkey, 1969; Alexander, 1974).
Additionai].y actinomycetes, yeasts and higher fungi have bc en shown to
evolve these compounds (Kadota and Ishida, 1972).
555
-------
CH 3 SH has received more attention than other volatile suif idea
due to its powerful and offensive odor and phytotoxic propeities;
this gas, as well as H 2 S, may accumulate in soils of rice paddies and
cause rice root damage (Alexander, 1974; Joshi and Hc.llis, 1977).
The sulfur—oxidizing bacterium eggiatoa , occurring naturalLy in rice
paddies, is able to detoxify these sulf ides. H 2 S is also toxic to
nematodes (Rodrlguez—Kabana et a].., 1965) and developing fish eggs and
fry (Smtth and Oseid, 1972).
Burrowing by invertebrates exerts a profound influence on nutrier.c
cycling and decomposition in heterotrophic systems. Invertebrates may
stimulate microbial activity and decomposition by a number of mechanisms
including coimninution, re noval of senescent colonies, enrichment by
nitrogenous excretions, elimination of antibiotic metabolites, enhance-
ment of oxygen penetration, and addition of mineral nutrients. These
effects occur in soils (Syers et al., 1979; Kitchell et al., 1979),
sediments (Fenchel and Harrison, 1976) and sludges (Mitchell et a]..,
1977; Abrams and Mitchell, this volume). In 0 2 —limited systens,
burrowing . .ttvities, or bioturbation of sediments and soils, may
markedly increase substrate oxidation, alteri.ig edox gradienta that
control many mineralization processes and redistribute nutrients
across system strata (Kitchell et al.., 1979; Withers, 19 8).
The major mechanisms by which fauna may influence sulfur bio—
geochemis try are thr’-ugh either a direct effect on the microflora or
through physical anJ chemical alteration of the surrounding envir3n—
ment,. Aitnough there is little data on the specific roles which
animals play in modifying uulfur compounds, there is evidence that
a sediment—dwel1inp polychaete worm stimulated rates of microbial
sulfate reduction and increased solubility of metallic cations (Aller
and Yingst, 1978). In contrast, Hornor and Mitchell (in review) have
shcvn that earthworm feeding may decrease rates of sulfide evolutio ..
in sludge. Also, interstitial metazoans are able to actively
scavenge sulfide ions in sediment pore water, detoxify the sulfide
and release it back into the surrounding environment (Powell et a]..,
1979).
The most striking difference between aerobic and anaerobic
decomposition is the nature of the metabolic products released. In
a normal, well—drained soil, the priin ry products of microbial
decomposition are carbon diox 4 .de, nitrate, sulfate and refractory
humus—like material. In submerged or waterlogged soils, sediments
and sludge, carbon dioxide, methane, ammonia, hydrogen sulfide, and
volatile organic sulfides such as methane thiol, dimethyl sulfide
and dimethyl df sulfide plus refractory peat—like organic material
predominate. Due to absorption of H 2 S in systems with low total sulfur
content and high metallic catiolk concentrations, such as soils and
oxidized sediments, H 2 S is produced but not evolved.
5.56
-------
In aerated soils, sediments and sludges, the major microbial
S transformations are 1) oxtdation of elemental sulfur, sulfide and
organic sulfur to sulfate and 2) assimilatory reduction of sulfate
into biomass. In 0 2 —limited systems, the major transformations are
1) dissimilatory sulfate reduction to sulfide and 2) dissimilation of
S—containing amino acids methionine and cysteine (derived from protein
hydrolysis) to H 2 S, thiol.s and volatile organic suif ides. A diverse,
ubiquitous microflora capable of transforming S through all of its
oxidation states is present in 0 2 —limited systems. Microbial com—
wunity S transformations are controlled by several environmental
parameters, including Eh, pH, the availability of labile organic
compounds serving as electron donors and the availability of
inorganic electron acceptors.
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560
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ON THE INCIDENCE AND DISTRJBUTION OF PARASITES OF
SOIL FAUNA OF MIXED CONIFEROUS FORESTS, MIXED LEAF
FORESTS, AND PURE BEECH FORESTS OF LOWER SAXONY,
WEST GERMANY
Kurtesh Purrini
Unkeysily 4 Goellingen
W ,s Ctrmany
INTRODUCTION
It Is well known that the soil fauna are Important in the formation
of the earthss soils. Soil fauna, their population densities and character-
istics have been studied by different authors in the recent years. But
practically no data exist concerning their pathology and parasitic diseases.
This study Is the first major contribution on Incidence and distribution
of parasites belonging to different groups of the microorganisms found In
natural populations of soil fauna from a spruce forest of Lower Saxony,
West German.y.
MATERIAL AND METHODS
The forest organic soil samples used in examinations of the soil
fauna were collected during !978 and 1979 in 2 different localities in mixed
coniferous forests (pine, Scoth pine, and larch as primary trees), mixed
deciduous forests (beech, elm and oak as primary trees), aad pure beech
forests, mainly in Lower Saxony, West Germany.
Samples containing 8478 specimens were extracted via modified Tuligren
extractors. Larvae, pupae 1 and adults were firstseparated and then studied
individually under light microscope. Adults were dissected and their organs
as well as eggs were isolated before being studied intensively. . ey were
smeared dry on slides, fixed with methanol or Bouin’s fluid and stained with
Glemsa-Romanovslcy or Heidenhatn’s iron haematoxylln solutions. Usually tne
contents of the body of an Infected animal were sufficient enought for the
preparation of one smear. For staining nuclei of the spores f pathogens,
a small 5pot of stained smear was treated with a droplet of the 1% HCL, and
the droplet was heated for 3bout a minute over a flame until a bubble appeared.
The smear then was washed with cold water and stained again with Giemsa
solution for 1—2 mm. The developmental stages of parasites and their sizes
were evaludted In smears of freshly dissected material as mellas fixed—
stalneo preparations using an ocular micrometer.
Only the heavily infected parts of the host could be fixed In situ
and the organs prepared In the usual way for embedding into eDon-araldite for
stud, with electron microscope. The tissues of infected anli;als were fixed
at 4 C for 2 hrs. in 2% glutaraldehyde and postflxea in 2% osmium tetroxlde,
each being dissolved in 0.1 M cacodylate buffer (pH 7.4). Tissues of infected
animals were then bulk stained for 14 hrs. in 3% aqueous uranyl acetate
followed by routine dehydration (60 to 100% Ethanol), and embedded In epon-
-------
araldite. Thin sections ( 400 _ 500 g) were cut with LKB ultramicrotome (Ultratome
III) and stained in uranyl acetate and lead citrate. Micro-photographs were
taken with a Philips 301 Electron Microscope.
RESULTS
Major parasitic and pathoganic components of th, e 8478 specimens of soil
fauna judged by their abundance, frequency and biotopes are shown in Table 1.
and 2. Three groups of decomposers: oligochaete, acarines, and collembolans
were intensively studied as organisms in which the high numbers Present in
the samples and their Intensity of transformation of organic materials in
forest soils pla)s an important role in nature. The highest infection level
for these groups occurred in mixed leaf forests (Table 1). The lowest
percentage of infections was in mixed coniferous forests. The pure beech forests
lie In between. These data show tPat there is a considerable difference
betweu deciduous and coniferous forcsts. These differences may be due to
the $fferences in the occurence of variety of fauna and higher density
of their population within broad-leaf forests compared to coniferous forests
Table 1. TUE SURVEY AND INCIDENCE OF PARASITES OF SOIL FAUNA
OF LOWER SAXONY, W. GERMANY, 1978 — 1979.
lost
Animals
No.
TOTAL:
Ex. % Inf.
Pure
beech
forests
BTIOTOPES:
M lxed
deciduous
forests
Mixed
coniferous
forests
ANNELI DA
Oligochaeta
480
54
16
32
6
ARANE IDA
Acarina
2600
42
11
23
8
MYRIOAPODA
110
-
INSECTA
Apterygota
2100
7
2
4
1
Orthoptera
52
6
1
5
-
Rhynchota
64
7
3
4
-
Coleoptera
560
22
6
14
2
Hymenoptera
52
12
3
5
4
Diptera
340
16
5
8
3
Lepidoptera
120
28
7
15
6
562
-------
Results obtained from the studies of parasites occurring in all group
of animals show that the population densities of soil fauna of spruce forest
SullS of Lower Sexony were found to be infected by nematodes. and four groups
of microorganisms: viruses, bacteria, fungi, and protozoa (Table 2).
Table 2. THE PERCENT OCCU. ENCE OF DIFFERENT GROUP OF PARASITES
FOUND IN THE SOIL FAUNA OF LOWER SAXONY, W. GERMANY
1978 — 1979.
Total:
Types of Pa
rasites:
Protozoa
%
j f
ø •’
-
ANNELIDA
Oligochaeta
54
— —
- T5
2 34
ARPIP EI DA
Acarina
42
1 —
2 6
- 33
MYRIOAPODA
-
- -
- -
INSECTA
Apterygota
7
— -
- 4
- 3
Orthoptera
6
- —
- 6
- -
Rhynchota
7
- -
- 7
- -
Coleoptera
22
2 -
- 17
- 3
ilynienoptera
12
3 —
- 9
- -
Dlptera
16
- —
- 10
2 4
LepldopterQ
28
2 3
1 22
- -
The highest level of Infection n three group of decoinposers was caused by
protozoans and fungi. Nematodes and bacteria were found rarely as parasites
of deconiposers. For other grour.s of Insects the most Infectiorts were caused
by Fungi, Protozoa, and the N 2odes
Many important genera were found to be pathogenic in Arthropoda and
they were distributed within the 21 localitIes examined. (Table 3) In
Acarina (Tab1’ 3), generally the genus Gregarlna showed tl e highest level
of Infection tn all localities. There was a little difference between the
563
-------
Table 3. THE PERCENT DISTRIBUTION OF IMPORTANT GENERA OF FUNGI AND SPOROZOA (PROTOZOA) OF ORIBATEI (ACARINA)
— AND COLLEMBOLA INVESTIGATED IN DIFFERENT LOCALITIES OF LOWER SAXONY, W. GERMANY, 1978 - .1979.
kOCALITIES
C
C)
C) C
•1 .
3 C. I. U
0 .D U U @1 W I ..
4.’ U i— N •i- .Q (U
I. C . I— . : C
i : U U U •r- Y)
J C. U) UJ
(U
s .
U I .-
4 . ’ 1.
0
.,- C
C) i— 4.’ U in
N U U in C)
I— •C in S
‘U (U 0 ‘U U
U) =
U
4.’
I. U
(U
C C) U S..
U I C . U
C) U I U +1
S.. in U 4.’
U 0 I—

MIXED CONIFEROUS FORESTS
PARASiTE GENERA
FOUND IN
CRIBATE I
(ACAR1NA)
PURE BEECH FORESTS
C C
U C U
C) U In
U I C .0
•1 C U I
I— i W I D ,—
a, . > C UI
5.. 0 0 0 C
I- U) m J
MIXED DECIDUOUS FORESTS
- --
-
S°O tOZOA
11 EI cosporl di urn
3
2
3
Gregarina
t4osema
8
-—
31
2
1—-
7
— — --
6-——-
33
5
31
4
36
6
2—-
30
3
16
5
28
2
18
2
10
7
30
20
3--
31
2
26
2
39
2
14
5
Plelstophora
6
1
2
5
3---—
3--
2
2
2-—
Thelohania
—
2
1
——
1
!b0sP0 ’ *
12
17
——
14
12
16
—-
1].
——
18
20
10
19
18
15
--
16
19
PARASITIC GENERA
-
FOUND IN COLLEMBOLA
FUNGI
Entomophtora
3
—-
2
2
2
3
--
-—
SPOROZOI%
Gregarina
-
3
6-—
Adelina?
3
Noserna
5
5
2
--
- -
Thelohanla
3
2
-—
2
--
-—
Auraspora !j.nOv.
Encephalitozoon
2

2
1

--
--
IPP organisms like Haplosporida
-------
mixed leaf forests (18%), and mixed coniferous forests (16%). The highest
level of infection by different species of Haplosporidia (?) was again
confined to mixed leaf forests (14.5%) and the lowest in mixed coniferous
forests (8%), For different genera of Microsporidia including Nosema sp ’.,
Thelohania spp., and Auraspora gen. nov . the highest level of Infection was
found in pure beech forests (1.8%), followed by the mixed deciduous forests
(1.4%), and mixed coniferous forests (1%). The Helicosporidium p rasiticum
Keilin, was found only in three localities. In the localities of Fartow and
Adelebsen the infections were totally absent. The percentage of infections
by pathogenic genera in Collembola was generally low, witi. very few found in
any of the localities investigated. In comparison, Sporozoa (Protozoa)
infected several groups of decomposers Including tne Oligochaeta and species
of moss-mites and Collembola (Table 4).
DISCUSSION
The results presented in this paper are of a preliminary nature and
more work is called for, although efforts have been made to identify the
parasites, particularly their family, genera, and In s iie cases the species
of Fungi, and Sporozoa.
Our work raises certain Important questions which need irnedi ate
attention as very little work has been published (Meier 1956, Stammer 1961)
on the pathology and diseases of soil fauna. However, we have only established
microsporidian Infections in two species of moss—mites Rh sotri ti a ardua C. L.
Koch (Earn. Euphtiracarldae) and Hermania gibbs C. L.Koch (Fam.1lermaniidae)
(Purrini and Baumler 1977, ‘978), but have also recorded a large number of new
species of different groups of microorganisms (Purrini I 76, 1979; Purrini and
Weiser 1979; Purrini, Bukva and Baumler 1979). The present study presents
some data on all groups of decomposers found in natural populations of soil
fauna in forest soils.
Nematodes, Viruses, Bacteria, Fungi, and Protozoa, were found in all
of the materials investigated. Most of the infections was found in the cells
of the fat bodies, body cavity, and also from muscles, ovaries, eggs, male
gonads, and intestingal epithelium of hosts (Figures 1—45). In all, 14
different parasites were found in oligochaeta, of which 11 specIes belong
to the Family Monocystldae (Eugregarinida, Sporozoa, Figures 1_6). One
parasite was close to the genus Hel I cosporl dl urn (He1icoeporida Protozoa)
(Figures 7.8), and two belong to the genus Nosema(Microspor . Sporozoa)
(Figures 8,9,lt)). Of those, He 1 icosporidlum para iticum , 7 s ’:’ es of Family
Monocystidae, and two of Nosema spp. are new for the Oligochaet ’.
Some of the Important pathogens of moss-mites are presen ed in Figures
11-19 and 4A,45. There were 9 species uf Microsporida , of which 6 belong
to the genus Nosema (Figure 18), two are Pelistophora species (Figure 19),
and a Thelohania species was found. Eight species belonging to Sporozoa
(Protozoa) were from genus Gregarina (Eugregarinida. Sporozoa, Figure 17);
one was a memberof Class Ciliata (Protozoa, Figure 16), and the remaining
two wete H. parasiticum (Figures l2:,13) and Nematodes (Figure 11).
-------
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i¼.. ‘.
2• J - . of .- vil1osn ii. hod.,• cr vit. , Y5L x.
3. C]i oc1 etoc j 3L,r. , our ; c.; t i . bc.d. c ivix.i, 00 x.
I’-. Stc. , t o trctthczoit i i pairs, bod.) cevit•,
1,00
5a. Oligochaetocystissr.o. , free trophozoit in pairs; 5b. free
tror.hczoit of At o1oq,,stis sfl. , 300 c.
c. onoc:jstiss , , the n .ature sporccy&ts in fat body, 3000 x.
6 . emvoc s s p., the mature c orc’cysts in fat body 3000 x.
2. Hel-lcosporidjura parasiticurn , free mature spores, 3000 x.
8. 1 osema s .,and . parasitic . 1 mixed infection• mature
— I
scores of both p rasites 1!i fat body, 1200 x.
. osems . , mature spores in fat body, 1200 x.
1G. .o ema . , mature spores in fac body, 3000 x.
I
2OOn u (Fig.2)
I -
1.00 m 1 u (Ag. 1,3, 5)
I I
45mju (Fig2,9)
50m 1 u (Fig. 6 1 6a,7jO)
-------
.
5
7
567
-------
Figs. 11—19: ORIBATEI / igs. 1,17: fresh condition; 12,19: phaco;
13,14,15, and 16: Heidenhains iron haematoxy—
un stain; 18: Giemsa stain/
11. Nematode of Eupht aoaruae:pp. , body cavity, 300 x.
12,13. Helico poridium arasjtjcum of pht yraoarug sp . , 12.
mature spores, intestine, 1200 x.; 13. vegetative stages
and mature spores, intestine, 3000 x.
14,15. ! 1osporidia ? of Darnaeus c1avi es ; 1 i.. different vege-
tative stages in Nephrocyts, and cells of fat body in
Casoum, 3000 x; 15. Mature spores, 3000 x.
16. Ciliata , cilia in body cavity Cf Etiphtyracarus spp. , 3000 x.
17. Gregarjn . pp . of Steganacarus apDlicatus , two mature
gamonts, intestine, 1200 x.
18. No ema app . of Demasus_onuatus, mature spores in fat body,
3000 x.
19. P1e sto spp . in Microtitia minima , nephrocyts lull
with vegetative stages and young spores of parasites, 1200 x.
- s
450 m (Fig. 11)
45 m u (Fig. 13j4,15 1 16j9)
50m 1 u (Fig. 12.171
568
-------
569
-------
Pigs. 20—28: CCLL 1 1 30LA /Pi s. nd 3: fresh condition; 21,24,
and 2 : rh co; 2E ,27, a!ld 28: Uie. sa t 1n/
20. -tomo 1tor s . of’ oceru isvesc r. , conidia M
sjo res i.:. bod cavity, 750 x.
2’ ,22,27. A jsç ? of I e uramuseori , ir f3t bodj; 21.
pre ture cysts, 1200 x; 22. preuiature cyst, 00O x; ? .
mqtiire c , st with porocysts, 3 0C x.
24,2 . I osena s p . of Leoidocyrtus c anet s , 1n ’ture sc e in
fat body, 12CC x.
26. eha i pp . of i vescer s , di feren vegetative eta-
ge 3rld mature spores in fat bode, 30CC X.
27. e13h ri spp . of LeT dccdrtus 1 gnor , sporotiasts with
rL ture spores in fat body, 4000 x.
28. Aura ora en.nov . of L. lignoruxn , iaa uure spores in gonads,
3000 x.
100 m 1 u (Fig. 2O 21,24,25J
5Om j (Ag. 22,23 .2528)
50mju (Fig. 27)
570
-------
—
I
1, ‘
*
-------
Figs. 29—38: DIPTERA / Figs. 29,30,31 and 33: Heidenhains iron hae—
matoxylin stain; 32,35: fresh condition; 34,39:
phaco; 36,37, and 38: Giemsa stain!
29,30. Helicosporidiu.m parasiticum of Ctenosciara hy61ipen js ,
Different vegetatl:e stages and r’ ature spores in fat
and intestinale epitheliu , 3000 x.
31. H. parasitjci.w of Ctenosciara app. , differer t vegetative
stages and mature spores in fat body, and intestina].e epi—
thelium, 3000 x.
32,33,34,35. Ascocjy2tis spp . of Megaselia subnitida , di±Tereut
vegetative stages and spores (oocysts) in ovaries,and eggs.
32. L(ature gametocyst with les& then 300 oocysts; a. free mature
oocysts, 750 x.
33. Mature gametocyst inside of one hosts—egg; a. cyst, b. egg—
vltellus, 300 x.
34. Free mature oocysts; a. ga iont, 1200 x.
35. Free mature oocysts, 3000 x.
36. osema app , of 1atosc arus socialis , mature spores in
fat body, 3000 x.
37. Nose s pp . of Epidaipus atomarius , mature spores in fat
bcdy, 3000 x.
38. Hepatozoon spp . ? of 0orn teras . , schizonts ? in fat
body, 3000 x.
Fig. 39: COLEOPTERA / Fig. 39: phaco/
39. Actinon y idia ? in fat body of one larvae of Coleoptera app .
1200 x.
1O0rn u (fig. 29,3O,3t35.36 37.39)
200 mju (Fi9. 32)
200mju (Flg.30)
100 rngu (Fig 34 )
-------
4
-------
Electron microscopy :
Figs. 4O— 3: Aux aspora gen. nov . of Lepidoqyrtus lignorwu , the
atuze spores, Fig. 40: 22000 x, Fig.41: 30000 x.
Pig. 42: 60000 x, Fig. 43: 38000 x.
574
-------
.40
4 .
.1
.4’
575
-------
Figs. 44,4 : Haplosporidium pp . ? of Damaeusclavipes , the sporo—
gonia]. stadies of parasite,
Fig. I4: 37000 x., Fig. £ .5; 380C0 x.
-------
... i
4 %
:
L 1’ ’
U ’)
-------
Table 4. THE I?c 0RTA 1T GENERA OF SPOROZOA (PROTOZOA) OF S(’TL DECOPIPOSERS FOUIW !N FOREST OF 1O ER SAXOIY.
W. GERMANY, 1978 — 197 ?.
Parasite
Host
TO
;b.Ex.
TAL
Inf.%
EUGREGAR
lion.
INfl)A
reg.
COCC
Ad
lOlA
?
Nos.
4ICRO
P1.
SPflR
Th.
10K
hi.
HA”LOSPORIDA?
a i.
-
O1igochaeta
480
36
30
—
—
4
-
-
—
-
CRT8P .CI:
Steganacarusrnagnu
59
20
-
10
-
-
-
-
-
-
1C
S. a ul1catus
242
59
-
21
-
2
-
-
-
—
36
S. striculus
161
61
—
:9
—
2
-
—
-
-
3;
Rnysotrltla duplicata
311
65
-
31
—
—
15
-
—
—
Mjcrot,-jtja minima
98
27
.
5
6
“
12
Nots;rus silvestris
14)
—
—
-
-
—
—
-
29
Piaty1o rLI peltlfer
Der eus clavlpes
89
412
26
76
-
6
26
—
2
3
-
-
-
-
-
-
-
18
47
. onustus
299
57
-
25
-
2
-
-
-
-
Ccp’ieus dentatus
Cara o es coriaceus
83
91
45
50
-
—
25
21
—
—
—
2
5
2
-
-
-
-
-
-
15
25
£upeo s h irtus
Eur tes g1o j1us
Euphthjraaaridae spp.
82
112
162
19
29
34
—
—
-
10 —
]0 —
9 -
2
—
-
-
-
—
—
4
-
-
-
-
—
-
7
19
COLLE ’.3OLA:
—_____
Tor.cc2rus flavescens
263
8
—
2
-
—
-
3
2
-
-
Le’rdccyrtus 11g oru’n
140
7
-
3
-
2
-
1
-
2
-
1. c:n.ceu
63
6
—
3
—
3
-
Ci cliiur s quadriocolIatus
412
11
—
-
-
11
—
-
-
-
-
J. spacta iHs
23
2
—
•
—
2
—
-
-
-
-
Ni nura n uscorum
‘ 7
6
-
-
6
—
-
-
-
Folcor.:ia qtiadrioculata
41
2
-
-
-
2
-
No. Ex. Number examined
Inf. = infected
Mon. = lonocystis spp .
Greg. recarina s p .
Ad. Adehna spp . ?
Nos. = t%osenia j .
P ora .
Tn. = T”e I
A.... = nov .
Hapl. = i )oor dium j p.
-------
ihe investigations of parasitic agents In moss-mites have been recorded
photographically by us for the first time (Figures 14, 15, 44, 45) a group of
microorganisms never s . en befobe (Table 5). The Infection was localized in
nephrocytes and cells of caecum. However, the morphology and life cycle of
this new group of parasites do not suggest a clean systematic status, an” w:
have yet to ascertaim whether these microorganisms belon ’ to Protozoa or
Lower Fungi. We consider that these may be close to Sporozoa and the organisms like
HaplosDorida . Detailed light and 1ectron microscopic studies of life
cycle and their importance as pathogen of moss-mites are under way. It
is hoped that this will help us in deciding more precisely their systematic
position. This group of parasites, H. parasiticum , 8 members of Gregarina
spp. and 9 species of Microsporida of Ortbatel are new.
Of the spring—tails, 9 different microsporidian (Figures 24—28),
one occldian ( Adelina spp. ?, Figures 21-23), and one Entomqphtorans spp.
(Entomophtoraceae, Fungi) parasites were found during our Investigation. Cf
microsporidian parasites, three were belonging to the genus Thelohania, 4 to
genus Nosenia , while one was close to the definition of the genus Enco ha1itozoon
(or Perezia of the recent revision or French authori)and one belongs to a
genus Auraspora p. nov. (Figures 23, 4—, 41, 42, 43) which Is not yet included
in th system of cro porld . All the discovered species of parasites in
Collembola are also new.
It is evident that s3i1 fauna other than those reported then were also
infected by different parasites. Intensive studies have been carried on the
parasites of dipterans and coleopterans. Of 340 specimens of dipterans
inspected, L’ie infections rate ‘ as 16% (1C% Fungi, 2% RI’iizopoda, and 4% Sporozoa).
The most Important pirasites were as follows: Helicosporidium parasiticuii
found in Ctenosciara h ,yallpennls Meigen (Fam. Sciaridae, Figures 2q.31);
Sporozoa of the genus Ascocystis (Lecudinidae, Eugregarinida) n Megaselia
subnitide Lu,ndbeck (Fam. Phoridae, Figures 33-35), and two Nosema spp. (Micro-
sporidia) in Platosciara socialis Winnertz and Epidapus atomarius Degeer (Fan.
Sciaridae, Figures 36, 37), and perhaps the genus Hepatozoon ? (Sporozoa Coccida
Figure 38). The questionable genus Hepatozoon C?) was found in one dipteran of
Corynoptera spp. (Fam. Sciaridae). In Coleptera the infection rc te was 22%
(2% Nematodes, 17% Fungi, and 3% Sporozoa) in samples of 560 specimens examined.
The most interesting parasites of Coleptera were the group of Sporozoa:
Actinomyxidla (?) found in one host larvae (Figure 39). This group of parasites
found in Coleoptera is very inusual for insects as hosts. The infection levels
of Orthoptera, Rhychota, Hymenoptera, and Lepidoptera are presented in Table
1 and 2. No infections was recorded in the t4yriaopoda.
CONCLUSIONS
Studies on the parasites of soil fauna in mixed coniferous forests,
mixed leaf forests, and pure beech forests of Lower Saxony, W. Germany reveal
that:
1. Of all soil fauna (8478 specimens) examined, the highest level of
infection was found in the animals of mixed deciduous forests verage level
12%), followed by pure beech forests (6%), and mixed coniferous forests (3%).
579
-------
2. The population densities of soil decomposer fauna in the forests
surveyed iere regulated by the Nem itoda, and four groups of microorganisms,
namely; Viruses. Bacteria, Fungi, and Protozoa.
3. Of total percentage of infection of decomposers, the highest level
was shown by Oligochaeta (54%), Acarina (42%), and Apterygota (7%).
4. Of parasites, the nost Important group of pathogenic agents were
Sporozoa (Protozoa) and Fungi.
5. Sporozoa (Protozoa) infecting the decomposers were studied and
identified to the family, genus or species level. This revealed a larqe
number of new species belonging to: Microsporida , Coccida , Gregarinida
and possibly Actinomyxidia, and Haplosporida
6. These studies also revealed one unknowfl group of microorganisms
which infected 15 species of moss-mites (Oribatel, Acarina). Detailed studies
of their life cycle are under way.
7. The establishment of Helicosporidium parasiticum Keilin, in
different species of phtiracarus spp. Euphtiracaridae) and in Ctenosclara
hyalipennis (Sciaridae, Diptera) represent also a very important feature
for the pathology of these Arthropoda.
ACKNOWLEDGMENTS
I am indebted to the following collegues who gave taxonoinic assistance
with the so 1 organisms and parasites: Prof. Dr. J. Weiser (Microsporida ),
Dr. Rene Ormieres (Gregarinida), Dr. Stanislaw Balazy (Fungi), Dr. V. Bukva
(Acarina), Dr. Bohuslau Mocek (Diptera), Dr. P Lastovka (Diptera) and Dr.
H. W. Dunger (Collembola). Also, my appreciation Is extended to Prof. Dr. F.
Mayer dfld Mss. V. Mofacker for their invaluable help with the e 1 ectron
microscope techniques.
LITERATURE CITED
Bulla, A. 1. and C. Th. Cheng. 1977. Comparative Pathology. Volume I-I l,
Phenun. Press, Ne,i York and London.
Grasse, P. P. 1952-53. Protozoaires. Traite de Zoologie, Volume I, Masson
et Ci , Paris.
Grell, K. 6. 1973. Prctozoology. Springer, Berlin-Heidelberg-New York.
Hall, R. p. 1971. Protozoology. Prentice-Hall Inc., New York.
Krieg. A. 1973. Arthropoden,iren. Georg Thleme, Stuttgart.
Kudo, IL IL 1971. Protozoology. (6th Ed.) Thomas, Publ. Co., Springfield,
Illinois.
Meter, M. 1956. Die Monocystidenfauna der O1igochaeten von Erlangen und
Umgebung. Arch. f. Protisetenkde, Bd. 101 (4): 337-400.
580
-------
Muller—Kogler E. 1965. Pllzkrakheiten bei Insekten. P. Parry, Berlin und
Hamburg.
Poinar, 0. G. and M. G. Thomas. 1978. Diagnostic manual for Identification
of Insect Pathogens. Plenum Press, New York and London.
PLsrrin1, K. and W. Baumler. 1976. Nosema ptyctiinae n. s _ p . eine neue Micro-
sporidie aus Rh sotrltia ardua C. L. Koch (Farn. Phtiracaridae,
Ptyctima Ac T aJ. Anz. Scr’.adel igskde., Pflanzenscutz, Un ,eltschu1tz.
49: 169—171
Purrini, K. and W. Baumler. 1977. 1osema herinaniae n. s elne neue
Mikrosporidie aus Hermania gibba C. L. Koch (Fam. Hermani’idae,
Oribatel, Acarina) in Fichter.boden. Zool. Anz. 199 (1/2): 107—112
Purrini, 0., V. Bukva and W. Baumler. 1979. Sporozoen in Hornmilben (Oribatei,
Acarinaj au Waldboden Suddeutschlands nebst Bescheibung von Gregarina
postneri n. sp und G. fuscocetis n. sp . (Gregarinida, Sporozoa,
Protozoa). Pedobiologia (in p ss) .
Purrini D. 1979. On a new parasite of Ascocystis spp. Grasse 1953
(Lecudinidae, Eugregarinida, Sporozoa) of Megaselia subnitida Lundbeck
(Phoridae, Brachyct ra, Diptera). Arch, f. Protistenkdè. (in press).
Purrini, K. 1979. A Newly Discovered Group of Parasites of Moss-mites
(ORIBATEI, ACARIHA) in Spruce Forest Soils. (in manuscript) .
SLhwenke, W., W. Baumler and H. Koschel. 1970. liber die Verteilung, Biologie
und Okologie von Enchytreiden, Lumbriciden, Oribatiden und Collembolen
im Boden schadlingsdisponlerter und nlcht disponterter Nadeiwalder.
Anz. f. Schadllngskde. Pflanzerschurtz. 3: 33—41.
£ieign, M. A. 1973. The Biology of Protozoa, Arnol, London.
Stammer, J. H. 1962. Protozoen und Wurmer als Parasiten in Insekten. Deutsche
Entomol. Zeitschr. V (9): 441-460.
Steinnaus, E. A. 1949. Principles of Insect Pathology. McGraw—Hill Book Co.
Inc., New York, Toronto, and London.
Steinhaus, E. A. (Ed.). 1963. Insect Pathology, and Advanced Treatise.
Volume t-II. Academic Press, New York.
Weiser, J. 1961. Die Mikrosporidlen als Parasiten der Insekten. P. Parey
Hamburg und Berfln.
Weiser, J. 1966. Nemoci hmyzu. Academia, 2 rague.
Wei er, J. 1977. An atlas of Insect Diseases. Academia, Prague.
Weiser, J. and K. Purrini. 1979. Seven new microsporidlan parasites of spring-
tails (Collembola) In West Germany, Zeitschr. f. Parasitenkde. (in
press).
Westphal, A. 1974. Protozoa. Blackie, Glasgow, and London.
-------
QUESTIONS and COMMENTS
CA. EDWARDS : Did you investigate the pathogens of
ne!natodes?
K. PURRINI : No, we didn’t.
E. WALDORF : Wuuld you speculate on the differences in
incidence between Colleinbola and Acari?
K PURRINIe Yes, there are big differences. The acarines
are not very resistant against the diseases. In L ,wer Sexony
(West Germany) the level of infections in acarines was 62%7
in Collembola only 7%.
. EASTMAN : Will you or your Institute colleagues be
looking at virus infections in roil arthropods?
K. PURRINI : Yes, we will be looking at virus infections.
I’ve just found two viral diseazies, one in N. muscorum
(Collep bola), nd cine in the larvae of Cantharus ep. (Fain.
Cantharidae, Coleoptera).
62
-------
INTERACTIONS BETWEEN NEMATODES AND BACTERIA IN
HETEROTROPHIC SYSTEMS WITH EMPHASIS ON SEWAGE
SLUP E AND SLUDGE AMENDED SOILS
Bonnie I. Abrams and Myron 1. Mitchell
SUN? CESF
LISA
The high densities of free—living nentatodes in a wide variety of
ecosystems has long prompted interest in their functional role. Since
bacteria appea to be responsible for only a minor fraction of nutrient
regeneration in marine systems (Johannes, 1968), faunal grazing has
been considered to be a major decomposition pathway. Therefore, by
virtue of their high density and ele’,ated metabolic rate, nematodes
have beer. considered important with regard to nutrient cycling and
energy flux by workers on marine benthos (Johannes, 1965; Tietjen, 1967;
Tietjen et al,, 1970; Gerlach, 1971).
In contrast, terrestrial eco1og sts have stressed the dominance
of bacteria and fungi as well as the subservience of the ¶nicrofauna and
mesofauna in decomposition processes. Therefore, investigations of the
ecological importance of terrestr:Ial nematodes have largely overiooked
their possible role in decomposition and have instead concentrated on
their population dynamics and their contribution to total community bio—
mass and respiration. However, previous workers have demonstrated that
invertebrates play a role far more significant than their biomass or
population metabolism would indicate by their stimulation of microbial
populations and hence alteration of decomposition rates of various
organic substrates (Hinsheiwood, 1951; MacFadyen, 1961, 1963; Vcath,
Edwards and Arnold, J964; Johannes, 1965; Stout, 1973, 1974; FeTichel
and Harrison, 1976; Mitchell, 1978, 1979). Our previous work has demon-
trated that bacterial feeding nematodes, specifically Pelodera punctata
(Cobb), s&.iraulate bacterial population growth and activity and thus have
an accelerating effect upon 8evage sludge decompcsition (Mitchell,
Hornor and Abrams, 1980; Abrams and Mitchell, in rev.).
The purpose of this paper is to present and compare our findings
with those from other investigations so that a more complete understand-
ing of the role of nematode—bacterial interactions in beterotrophic
s stems may be ascertained. Specific emphasis will also be placed • n
the investigations of Anderson and Coleman (1977), AndEtson et al.
(1978) and Coleman et al. (1978). since these latter studies are the
only ones presently available which a ccmparable to our work.
Nematode population metabolism and biomass in various habitats
Nematode abundance, bicinass and respiration data, which were
obtained from various sources, are presented in Table 1. Several
investigators have estimated the contribution of nematodes to total soil
metabolism. It is evident that in those habitats dominated by plant
583
-------
TABLE 1. NEMAXODE DENSITY, BIOMASS AND POPULATION METABOLISM IN VARIOUS HABITATS.
labitat
Nematode
Densities
(individuals
1r 2 )
Neinatode
Biomass
(g m .- 2 )
Population
Metabolism
(ul O nr 2
H— I .
Temperature
(°C)
Dominant
Feeding
Group
z
Contribution
to Total
Faunal
Metabolism
iluthority
(oorland
Soil
3.06x1 0 6
0.75
4.9x10 2
16 ! Plant
Feeders
.6
Banage, 1963
Grassland
i._________
i.iOxlO 7
10.5
l.lxiO 3
16
Plant
Feeders
16
Nielsen, 1949
MacFadyen, 1963
IBeech
orest
i.09x10 6
0.28
24xl0 2
16
Plant
Feeders
5
YeateB, 1972
Phillipson et al.,
1977
Subarctic
Tundra
3.56v10 6
2.64
8 0x10 3
——
Bacteria,
Feeders
75
Kuzmin, 1976
4arine
(Salt
Marsh)
2.10x10 6
18.4
l.8x10 5
20
Microbia
Feeders
33
Wieser 6 Kanwisher,
1961
Sewage
Sludge
1.40x10 7
2.80
5.OxlO 4
22
Bacteria:
Feeders
61
Mitchell et al.,
1978
Abrsms & Mitchell,
in rev., Unpub-
lished data
-------
(niacrophyte) feeding umnatodes, they contribute a relatively small
proportion of the total soil metabolism. Examples of such eyst ns
include bog or moorland soils where the acidity precludes high densi-
ties of bacteria and thus plant and fungal feediag rematodea dominate
(Banage, 1963).
The abundance of herbaceous material in grasslanü also tends to
favor plant feeding neinstodes. However, Twinu (1974) noted that popu-
lation densities of hacterial feeding nematodes varies considerably in
grasslands and they sometimes compose up to 50% of the total neinatode
fauna. This variation has been attributed 1 in part, to the spatial
arrangement of vegetation. Ren e, selection of certain samples in
accordance with vegetation location may bias density estimates toward
plant feeding nematodes and overlook the contribution of bacterial
feeders Which wculd be found in more open areas (Twiun, 1974).
In deciduous forests, such as the beech mull studied by Yeates
(1972) and Phillipsnn et al. (1977), the wide variety of food resources
allows nematodes to be distributed throughout various trophic groups.
In addition, the favorabla soil conditions in such habitats permit a
wide variety of organisms, including bacteriophagous inacrofauna to
fiourigh. Therefore, the relative contribution of nematodes to total
soil inetaboliem may be less.
It is in more severe environments that the importance of nema—
todes becomes most evident. In spite of the relatively low pH of 5 in
the subarctic tundra site Which was studied by Kunmin (1976), bacteria
were far more abundant than fungi (Cheruov et al., 1975). Hence,
bacterial feeding neuzatodes were dominant over plant and fungal feeders.
Kuzmin (1976) also noted that although nematodes comprised only 30% of
the biomass in some sites, they wore responsible for up to 75% of the
total faunal metabolism.
In both marine sediments and sewage sludge the ability of nema—
todes to survive anoxic conditions permits them to be active in habitats
where other fauna are excluded. Oxygen depletion may occur in estuarine
environme its, where microbial activity is cons derab1e as well as in
profunda). sediments (Weiser and Kanwiaher, 1961). As an adaptation to
these low oxygen tensions, some marine species, such as Enoplus brevia
(Bastian) possess oxyhaexnoglobin to regulate oxygen supply to various
tisaues as well as store oxygen when it is present in low concentra-
tions (Atkinson, 1975). Similarly, P. punctata , the dom 4 ” nt species
in an activated sludge, is also able to survive anoxic conditions and
be active under low (p02 7000 dyne oxygen tensions (Abrame and
Mitchell, 1978). This is especially critical in the early stages of
sludge decomposition, when anaerobic processes may predominate and
o ,gen depletion occurs G Ltchel1, Hornor and Abrams, in rev.).
The importance of neinatode-bacterial interactions on substrate
metaboLism
A field study of sewage sludge in drying beds revealed high
densities of P. a and other bacterial feeding rhabditid neinatodea
565
-------
when decomposition, as indexed by oxygen consumption end methand evolu-
tion was proceeding rapidly (Mitchell et al., in rev.’. Similarly,
in a study of the effects of sludge addition to a silt loani topsoil,
nematode densities increased, then decreased with time in correspondence
with organic matter catabolism (Mitchell et al., 1978). Studies of
nematode—bacterial interactions in glass bead microcosms have demon-
strated that bacterial activity, which was raf1e ted in oxygen consump-
tion and carbon dioxide evolution is sigrificantly increased in the
presence of neinatode grazing (Anderson a&&d Coleman, 1977; Mitchell et
a].., 1980). In addition, bacterial population densities were also
aignificantly (p ‘0.05) increased by nematodea (Mitchell et al., 1980).
Studies in sterilized sludge microcosms yielded similar results. The
feeding activities of rhabditid nematodes (P. punctata ) stimulated
microbial ( Pseudoinonas fluorescens ) metabolism as was reflected in
significantly (p ‘0.01) increased oxygen consumption and bacterial
densities (Abrams and Mitcholl, in rev.). In addition, nematode move-
ment also helped to distribute Ps. fluorescens within the sludge.
Organic matter losses were found to be twice as great over 35 days in
microcosins c’rntaining nematodes and bacteria than in those containing
bacteria alone (Abrams and Mitchell, in rev.).
While this effect is of major importance in substrates uith a
h1 h organic matter content, it stay not be as pronounced [ n mineral
soils where food resources are more limiting. En microcosms containing
sterilized mineral soil, Anderson et a].. (1978) noted that bacterial
densities were slightly higher after 17 days of nematode feeding but
after 24 days were significantly (p ‘ 0.05) reduced. However, the
metabolic activity of the mineral soil microcosms was only a fraction
of that observed in the sludge inicrocosms, Even ai ter substantial
(600 ppm) gluco2e amendments, bacterial densities did not exceed 10
individuals g 1 dry weight in the mineral soil throughout the 24 day
study Anderson et al., 1978). In contrast, bacterial densities
(inoculated at the same order of magnitude) in the sludge microcosms
were as high as 101]. individuals g” after 5 days. Assuming a
respiratory quotient (R.q.) of 1.00 for carbohydrate catabolism, the
data of Coleman at al. (1978) for mineral soil can be compared with
the sludge respiration data (Figure 1). Carbon dioxide evolution in
the sludge mictocosms over 14 days was more than 600 times greater than
that of the mineral soil microcosms. Although the organic matter con-
tent of the mineral soil, with glucose additions was no more than one
sixth of that in sludge, losses over 35 days would only amount to
0.00347% of the organic matter as opposed to 6.89% in the sludge micro—
coams for the same time period. In the absence of nematodes, organic
matter losses would be .00015% and 3.51 for the mineral soil and
sludge inicrocosms, respectively.
The data support the ypotnesis that nematodes have an accelera-
ting effect upon decomposition, and that this effect is of greater
significance in substrates high in organic matter. In such substrates,
food resources may not be as limiting and, hence reproduction of
bacteria may be rapid and continuous. Predation by nematodes keeps
bacter a1 populations actively growing and distributed throughout the
586
-------
FIGURE 1. Comparison of sewage sludge (Abrams and Mitchell, in x ev.)
and mineral soil (Coleman et al, 1978) catabolism in the
presence and absence of bacterial feeding nematodes.
0
C.,
•1
WAGE SLUDGE
a
I
I
F
I
I
II
F
F
I
F
— — I
--4
MINERAL SOIL
I
I
I
a —
— S — — - —
a—,
— NEM1.T00C5 &u*CI R,a
BACTCIIA *tOei(
I 2 3 4 5 B 7 B 9 tO II I? 13 14
DAYS
587
-------
material. In substrates where organic matter is less abundant, pre—
dat on by nematodes acceleratEs the natural decline of microbial
populations which accompanies the depletion of the food resources,
Direc:jons for future research
More direct observations of the feeding habits of soil nematodes
are needed. Previous studies have been based largely on gut content
analyses or buccal cavity shape. Gut content analyses may be somewhat
inaccurate since often, only hard, indigestible i’mns are recognizable
(McIntyre, 1969; Tietjen, 1969; Tietjen and Lee, .977) , In addition,
bacteria and other small organisms may be taken in with larger food
it ns, causing discrepancy as to the predatory nature of some species
Buccal cavity shape may be misleadin ç a well, since different types of
buceal cavities may be correlated with other physiological functions,
such as oxygen uptake (Wieser and icanwisher, 1961). In addition,
atomal shape may be indicative of the size classes of food items, not
necessarily the biological origin of those items,
The effects of bacterial feeding nmnatodea on soil processes
such as carbon flux and mineralization should be explored further. In
addir ion, the relationships among nematodes and other soil organisms
should be investigated. Emphasis on microfloral—faunal interactions,
rather than c3mpartlaentalization of specific taxa would enhance our
understanding of decompositicqi processes within heterotrophic systems.
REFERENCES
Abrams, B.!. and M.J. Mitchell, 1978. Role of oxygen tn affecting
survival and activity of Pelodera punctata (Rhabditidae) from
sewage sludge. ematologica 24: 456—462.
Abrams, 3.1. and M.J. Mitchell. In rev. Role of nmnatode—bacterial
interactions in heterotrophic syecems with emphasis on sewage
sludge decomposition. Oikos.
Anderson, R.V. and il.C. Coleman. 1977. The use of glass microbeads in
ecological experiments with bacteriophagic itmnatodes • 3.
Nematol. 9: 319—322,
Anderson, R.V., E.T. Elliot, J.P. McClellan, D.C. Co].eman, C.V. Cole
and LW. Hunt. 1978. Trophic interactions in soils as they
affect energy and nutrient dynamics. III. Biotic interactions
of bacteria, amoebae, and nematodes. Microb. Ecol. 4: 361—371,
Atkinsot, H.J. 1975. The functional significance of hasmoglobin in
a marine .iematode, p1us brevis (Bastian) • J. Exp. Biol.
59: 267—274.
588
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Banage, WJ. 1963. The ecological importance of free—living soil
neznatodes with special reference to t ose of moorlaxid soil.
3. Anla. Ecol. 32: 133—140.
Cheritov, Y.3., E.V. Dorogostaiskaya, T.V. Geraslmeuko, t.V. Ignatenko
N.y. Matveyeva, O.M. Parinkina, T.G. Polozova, E.N. Romanova,
V.P. Schawurin, LV. Smirnova, IV. Stepanova, BA. Tomilin,
A.A. Vinokurov and 0.V. Zalenaky. 1975. Tareya, USSR. Pages
159—181 in T. Rosswall and 0.W. Real (eds.). Structure and
function of tundra ecosystems. Ecol. Bull. (Stockholm) 20.
Coleman, D.C., R.V. Anderson, C.V. Cole, E.T. Elliot, L. Woods and
M.K. Campion. 1978. Trophic interactions in soils as they
affect energy and nutrient dynamics. IV. Flows of metabolic
and biomass carbon. Microb. Ecol. 4: 373—380.
Fenchel, T. and P. Harrison. 1976. The significance of bacterial
grazing and mineral cycling for the decomposition of particulate
detritus. Pages 285—299 in 3.14. Anderson and A. Macfadyen
(eds.). The Role of Terrestrial and Aquatic Organisms in
Decomposition Processes. Blackwell Sci. Pubi • Oxford.
Gerlach, S,A. 1971. On the importance of marine microfauna for
benthos cosmunit ies. Oecologia 6: 176—190.
Heath, G.W., C.A. Edwards and M .1C . Arnold. 1964, Some methods for
assessing the activity of soil animals in the breakdown of
leaves. Pedobiologia 4: 80—87.
Hinsheiwood, C. 1951. Decline and death of bacterial populations.
Natur2 167: 666—669.
Johannes, R.E. 1965. Influence of marine protozoa on nutrient regenera-
tion. Lianol. Oceanogr. 10: 434—442.
Johannes, ILE. 1968. Nutrient r generation in lakes and oceans.
Pages 203—213 in M.R. Droop and E.J. Ferguson Wood Cede.). Ad-
vances in Microbiology of the Sea • Academic Press, London.
Ruzmin, L.L. 1976. Free—living nematodes in the tundra of western
Taimyr. Olkos 27: 501-505.
MacFadyeu, A. 1961. Metabolism of soil invertebrates in relation to
soil fertility. Ann. Appl. Biol. 4: 215—z .8.
MacFadyan, A. 1963. The contributions of the microf auna to soil meta-
bolism. Pages 1—17 in 3 Doekeen and 3. van der Drift (eds.).
Soil organisms. Proceedings of the colloquium on soil fauna,
soil microflora and their relation&’ips. North Holland Publish-
ing Co., Amsterdam.
589
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Mcintyre, A.D. 1964. Meiobenthos of sublittoral muds. J. Mar.
Biol. A58. U.K. 44: 665—674.
Mitchell, M.J • 1978. Role of invertebrates and microorganigma in
sludge decomposition. Pages 35-50 in R. Rartenstein (ed.).
Conference proceedings on utilization of soil organisms in
sludge management. SUNY, CESY, Syracuse, New York.
Mitchell, MS. 1979. Functional relationships of macroinvertebrates
in heterotrophic systems with emphasis on sewage sludge
decomposition. Ecology, :Tn pze.ss.
Mitchell, NJ., R. Hartenstein, B.L. Swift, EF. Neuhauser, B.l. Abrams,
R.M. Mulligan, B.A. Brown, D. Craig and 1), Kaplan. 1978.
Effects oi diffetent sewage sludges on some chemical and biologi-
cal characte jstjca of soil. 3. Environ. Qua3.. 7: 551—559,
Mitchell, M.J.., S.C. Rornor and LI. Abrains. 1980. Utilization of
microcosms in studying decomposition processes in sewage sludge.
In press, in J.P. Ceis Jr. (ed.). Microcosms in ecological
research.
Mitchell, N.J. S.C. Kornor and B.I. Abrams. In rev. Carbon flux
rates in heterotrophic sewage sludge drying beds as affected by
earthworm feeding. J. Environ. Qual.
Phillipson, 3., R. Abel, S. Steel and SSR..TI Woodel].. 1977. Nematode
numbers, biomass and respiratory metabolism in a beech woodland.
Wytham Woods, Oxford. Oeco].ogia 27: 141—155.
Stout, S.D. 1973. The reL tionship beLT.een protozoan populations and
biological activity in soili3. Amer. Zool. 13: 193—201.
Stout, S.D. 1974. Protozoa. Pages 385—420 in CR, Dickinson and G.J.F.
Pugh (eds.). Biology of Plant Litter Decomposition. Academic
Press, London.
Tietjen, 13.3. 1967. Obaer7ations on the ecology of the marine nematoce
filicaudata , Ailgen, 1929. Trans. Amer. Microac, Soc.
86: 304—306.
Tietjen , JR. 1969. The ecology of shallow water meiofauna in two New
England estuaries. Oecologia 2: 251—291.
Tiet3 n, 3.11., 3.3. Lee, S. Ruliman, A. Creengart and 3. Trompeter.
1970. Guotobiotic culture and physiological ecology of the marine
nematode Rhabditia marina , Bastian. Limnol. Oceanogr. 15(4):
535—543.
590
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Tietjen, 3.11. and 3.3. Lee. 1977. Feeding behavior of marine nsmatodes.
Pages 21—35 in B.C. Coull (ed.). Ecology of Marine Benthos.
Univ. South Carolina Press, Columbia.
Twinu, D.C. 1974, Neinatodes, Pages 421—465 in C.il. Dickinson and G,J.
F. Pugh (eds.). Biology of Plant Litter Decomposition.
Acadcic Press, London.
Wieser, W. and 3. Kanwisher. 1961. Ecological and physiological
studie.s on marine neinatodes from a small salt marsh near Woods
Hole, Massachusetts. Limnol. Oceanogr. 6: 262—270.
Yeates, G .11. 1972. Nematoda of a Danish beech forest • Oikos 23:
178-189.
QUESTIONS and COMMENTS
D. COLEMAN : Did you determine the fraction of the total
organic carbon which was soluble?
If this was high (perhaps ½ of your total of 60% organic
matter) that would account for your very high microbial activity.
B.I. ABRAMS : This sludge contains a high percentage of
labile carbon compounds and hence its decomposition rate is
extremely rapid. More information on the chemical composition
and decomposition rate of this sludge has been presented in
Mitchell et al. (1978). which is referenced in our paper.
S. HILL : Do you consider that r ematode movement is im-
portant, in addition to feeding. n their promotion of bacterial
activity?
B.I. f BR MS : Their movement through the sub3.trate does
create additional surface area and micropore space and also
distributes bacteria within th substrate. However, where this
effect is active and of a mechanical nature in the case of
larger invertebrates, it is paseive in the case of nematodes
since they move in an aqueous film.
591
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/
USE OF M1CROARTHROPODS (MiTES AND SPRINGTAILS) AS
VALUABLE INDICATORS OF SOIL METABOLIC ACTIVITY
Guy Van. ier
Centre National de In Rrchrrchr Sc,rntifq,ie
Franc.
ABSTRACT
It is well krown that most of the metabolic, activity
in soil is due to microbial activity. Accordingly, overall
soil respirometry or mIcrobial counts are often used as an
indicator of soil metaholism. Because conflicting ‘-esults
are often obtained, so l fauna is not yet considered as a
reliable indicator for this puroose. In this paper we have
tried to determine whether soil fauna c n be used as a
valuable indicator of soil metabolic activity.
Soil cores frori t so forest soil types (a rendzine
or caicareous soil, pH8.5, and a pocizol or loamy sandy
soil, pH 3.7) were desiccated or sterilised by heat (30°C,
60°C. 105°C, 200°C) then replaced in the field, to allow
invasion by Microarthropods and Microorganisms from
surrounding soil. Respirornetric activity was measured weekly
in treated and undisturbed soil core samples during a one
month incubation period. At both sampling sites, qualitative
and quantitative variations f bacteria and fungi were
carried out, and invasion by Mites and Collembola were
checked weekly. Soil respiration rates and microbial counts
were much higher in calcareous soil cores than in those of
loamy sandy soil. Colonization by Collembola was signifi-
cantly more intense than by Oribatid Mites in alkaline soil
cores, but in acid soil an opposite pattern was observed.
These preliminary results indicate that it may be possible
to characterize soil biological activity by Microarthropods
invasion, related to relatively fast microbial growth,
enhanced by previous esiccatlon of soil cores.
RESUME
Tous l s spéclalistes du sol s’accordent a declarer
oue l’activité mêtabolique d’un sol est principa1ement
dOe au développement de la microflore tellurique. En
consGquence, les mesures respiropiêtriques du sol et les
ënumêrations de germes constituent d’excellents indicateurs
de l’activite mêtabollçue totale du sol. Parce que de
59Z
-------
nombreux résultats contradictoires ont êté souvent obtenus
la faune su sol ne peut être encore considërée commo un
indicateur sür du nétabolisme du sol. Dans cet article, nous
proposons une méthodologie nouvelle permettajit a’utiliser
les mlcroarthropodes du sol comme estimateurs de Uactivité
mêtabolique au sol.
Des êchantillons de terre provendnt de deux types
de sol (rendzine pH = 8,5 et podzol pH = 3,7) ont êté
dess chës ou stêrilisës a la chaleur (30°C, 60°C, 105°C et
200°C). puis réintrodults a leur emplacement dans le terrain
de manière a permettre le libre retour des Microarthropodes
et des Microorganismes. Des mesures d’activitê respiratoire
ont êtê effectuêes chaque semaine pendant ur mois sur les
ëchantillons traitês et têmoins, ainsi que des estimations
qualitatives et quantitatives des germes bacteriens et
fongiques. Simultanetnent et respectant la même përiodicite,
le retour des Acariens et des Collemboles d Pu être contr lé.
Les consommations d’oxygêne et les ênumêrations de
germes ont êtê plus élevêes dans le sol calcaire que dans
le sol limoneux. De même, la colonisation par les Collem-
boles a ete beaucoup plus intense que celle des Acariens
dans le sol alcalin. alors que le processus est inverse
dans le sol acide. L’ensemble de ces rêsultats démontre
qu’il est possible de caractériser l’activitê biologique
d’un sol par le taux de colonisation des Microarthropodes
provoqué par une relance de l’actlvlté microbiologique
dans des echantillons de sol prealablement dessêchês, puis
réintroduits in situ .
INTRODUCI ION
Most of the metabolic activity in soil is due to
microbial activity and soil biologists generally admit that
animal metabolism accounts for only 10 per cent of the
total soil metabolism (MACFADYEN 1968). CROSSLEY (1977)
reports that some recent studies have estimated that soil
fauna contributes less than 1% to the annual average CO 2
production from forest soils. Acccrdingly some authors
have attributed indirect requlation, through microfloral-
faunal interactions, as playing a major role for soil
arthropods. It is a common finding that in animal sampling
some soil samples contain low counts of all species while
others may contain many abundant species although soil
respiration values remain very uniform. Because conflicting
results are often obtained, soil fauna is not yet considered
as a reliable indicator of soil metabolism. Under these
conditions, nost studies of soil metabolism mainly concern
microbial activity and have used evolution of CO 2 production
593
-------
over time as an indicator of overall respirometry activity
(COLEMAN, 1973).
To remove any uncertainty about the use of soil fauna
as an objective tool for estimating soil metabolic activity,
we have attempted a new approach based on the re olonisation
by microarthropocJs in heat desiccated soil samples, main-
tained in the laboratory, then replaced in the field.Little
is known about how quickly and by what route treated soil
becomes recolonjsed. The recolonisation of sterilised soil
by soil arthropods was previously studied by BUAHIN (1965)
who showed that soil sterilised by chemicals was recolonised
by all arthropods more Slowly than soil sterilised by heat.
This paper reports results which are partly drawn
from a previous work on relationships between soil fauna
and soil microflora (KILBERTUS, VANNIER. VERDIER, 1976).
METHOD!
Two types ov forest soil were used for comparison.
At Brunoy, South of Paris, an alkaline soil or brown
calcareous soil in Hornbeam wood (pH 7.5-8.5 ; C/N 10-12),
and an acid soil or sandy loam soil in Oak forest (pH 3.7-4.4;
C/N 23-30).
In each forest site within a five square meters area
and at the same time in spring 1975 (12th May - 9th June),
were cored 96 soil samples (5cm deep, 20 cm 2 area), brought
into the laboratory, desiccated at different tenperatures
(30°C. 60°C, 105°C. 200°C), then replaced in the field to
allow invasion by tnicroarthropods and microorganisms from
surrounding soil. All these treated soil samples were free
of any arthropods and those heated at h gh tempr’ratures
(105°C, 200°C) were totally sterilised.
After one week of incubation in the field, six soil
samples of each treatment, plus six of undisturbed, soil
were removed weekly during one month, and used for respi-
rometry measurements in an incubator, counts of microbial
germs on gelose culture, and microarthropods extrdctions
by a dry funnel system.
In addition, soil moisture was controlled in each
site at the same time. After only one week of natural
incubation, all treated soil samples restablished their
optimal moisture content compared with the surrounding
soil.
59
-------
Figure 1. - Weekly respirometry activity in heat desiccated
soil samples then replaced In the field, and in
control s.
, ; ai M l I
IM
ALKALINE SOIL
, 5Ic
ACID SOIL
I
-------
RESPIROMETRY ACTIVITY
Each soil sample used for respirometry activity was
placed in a small chamber or incubator from which a small
volume of gas was removed arter two hours Incubation, then
analysed with a Scholander 0.5 cc. gas analyser, as des-
cribed in VERDIER (1975). Respirometry activity is best
charactarized by the oxygen consumption rather than by the
CO 2 production, in the case of alkaline soil because of
the combination of CO 2 with carbonates (VERDIER, 1975).
In figure 1, respirometry activity is expressed as
a ratio between 02 consumption ir. treated soil samples and
02 consumption in undisturbed soil samples or controls. The
level of respirometry activity in controls indicates the
line of reference (+1) to be compared to the levels of
respirc”ietry activity in treated soil samples.
In alkaline soil, soil samples initially heated at
high temperatures (60°C. 105°C, 200°C) showed a peak of
activity after two weeks and a second increase two weeks
later. Conversely a low response was recorded in the case
of soil dried at 30°C.
In aci’i soil samples, results were quite different
respirometry activity in soil heated at high temperatures
(105°C and 200°C) did not attain the level of natural soil
activity. In the cases of soil treated at 30°C and 60°C,
aFter a short increase during the first week, the respiro-
r etry activity dropped under control levels.
tIICROBIAL COUNTS
Microbial counts have been made on agar-agar culture
using the method described by REISINGER and KILBERTUS
(1975).
Desiccation always promotes growth of a limited
species of germs, but in large quantities, at the expense
0 f total microflora. Table 1 shows the same phenomenon in
all treated soil samples of alkaline soil except for the
treatment at 30°C. Drying by heat followed by natural
rehydration caused the development of an overwhelming
number of microorganisms where Actinomycetes dominated
for instance 597,000 germs per gramme o dry soil in
treate’I soil samples at 105°C versus 3,668 germs per
gramme of dry soil In control soil samples. A restricted
number of fungi species were found, only five at 30°C, six
at 60°C none at 105°C and 200°C whIle normally twenty-two
specI- s occur in untreated soil.
596
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Table I. - WEEKLY COUNTS OF GERMS (x 10 ) PER GRAMME OF
DRY SOIL IN HEAT DESICCA1ED SOIL SAMPLES THEN
RE PLACED IN THE FIELD, AND IN CONTROLS.
ALKALINE SOIL
WEEKS

‘REATMENT
FIRST
SECOND
THIRD
F3URTH
at 30°C
35,320
25,700
21.200
52,500
at 60°C
74,430
255,000
339,000
223 O0O
at 105°C
130.960
453,000
597,000
264,000
at 200°C
81,150
148,000
72,200
106,000
CONTROLS
19,090
19,700
3,668
13,800
ACID SOIL
WEEKS
FIRST
SECOND
THIRD
FOURTH
REATMENTS
at 30°C
78,75
12,550
14,400
3,2 O
at 60°C
45,840
40,800
9.000
25,400
at 105°C
8,302
20,400
42,600
29,100
at 200°C
32,800
40,800
85,000
92,800
CONTROLS
t__
5,415
15,900
2,990
—
3.400
-
.59?
-------
In acid soil, microorganisms are less abundant than
In alkaline soil and differ by the lack of Actinomycetes
which are replaced by Bacillus and Arthrobacter . Counts
concerning acid soil samples are no very high (Table 1)
reflecting a lower microbial activity than in treated
alkaline soil samples. These results corroborate those
recorded previously in soil respirometry study (Fig. 1).
ASSESSMENT OF MICROARTHRO!’ODS
Invasion by mites ( Oribatei, ilesostigmata ) and
springtails (Isotomldae an ntomobryidae) was compared in
each type of ói1 at the same temperature treatments
(Fig. 2 and 3). P.elative frequencies were expressed as a
ratio between the number of Individuals extracted from
treated soil samples and the number of in.. ividuals extracted
from undisturbed soil samples (controls), so that the
reference line (+1) represents the animals identified In
the control soil samples.
In alkaline soil, at 30°C, Isotomidae and Entomo-
bryidae rapidly invaded the treate .oil samples as compared
to those found in untreated soil samples (controls). Oribatid
mites, on the contrary, did not reinvade on these treated
soil sa nples.
The same pattern was evident at other temperature
treatments (Fig. 2 and 3). Recolonlsatior. by Collenibola
was always more intense than by Oribatid mites ; for
instance at 105°C and on fourth week of incubation,
Isotomidae were eight times as abundant in control soil
samples and Entomobryidae were 5.5 times more abundant,
while a half of the Oribatid populations were collected
in the same treated soil samples. At 200°C, the numbers
of Isotomidee and Entomobryidae greatly diminished in
treated soil samples but still exceeded those in undisturbed
soil san .: es.
In acid sclil at any temperature treatment an opposite
pattern was recorded. Oribatid mites were commonly collected
and their numbers always exceeded the populations in
undisturbed soil, while the Collembola populations in the
same treated soil samples were lower than in controls. At
30°C, 60°C, 105°C and 200°C temperature treatments, Oribatid
mites were respectivnly 4.2. 2.3, 6.2 and 2.2 tImes as
abundant as in controls after three weeks of incubation.
A crossed experimental paradigm was performed in
December 1975 in the same sites where desiccated acid soil
sariples at 105°C were placed in alkaline soil area, and
desiccated alkaline soil samples were Introduced in acid
598
-------
Figure 2. - Recolonisation of heat desiccated soil samples
(30°C and 60°C) by mites and springtails as compared
to controls in two types of forest soil.
I
I I
I
I
ALKAUNE JIL ACID SOIL
Figure 3. - Recolonjsatjon of heat desiccated soil samples
(105°C and 200°C) by mites and springtails as
compared to controls in two types of forest soil.
ALKALI’, E IL
ACID SOIL
rwcJ
i ci
1200c1
I
-------
Figure 4. - Crossed experimental model showing the specifity
of recolonisatlon pattern in heat desiccated soil
samples.
cEc.qED D S L &* PL6
JRED IN A FO 1 ALX 1JNE IL
U • cRIBAm
O IQ D MXIJJNE SOIL SJIPLE
ED IN A FO D SOIL
U—0 M ocn6s*7A
U.----. tsom z
6oo
-------
soil area. Figure 4 summarizes the results
- in alkaline soil area, treated acid soil samples retained
the typical pattern of an acid soil, with a low rate of
recolonisation by Collenbola, with however an absence of
Oribatid mites.
- in acid soil area, treated alkaline soil samples maintained
the specific pattern of an alkaline soil with a high increase
of Collembola ( Isotomidae and Entomobryidae) , and much less
Oribatid mites than in controls.
All these results tend to confirm the specificity
of the process of recolonisation by microarthropods towards
the overall activity in a forest soil.
CONCLUSION
These preliminary findings indicate that it may be
possible to distinguish soils with a high metabolic activity
from soils with low metabolic activity, using a process of
recolonisation by soil animals into desiccated soil samples.
It Is not necessary to establish a statistical analysis
to demonstrate that the colonisation by microarthropods
is influenced by a fast microbial growth enhanced by
previous desiccation of soil samples.
This method may be useful since little work is
involved, and only limited knowledge of soil biology is
required. The procedure is simple and merely involves
collection of soil samples from the field, desiccation in
an oven at 60°C or 105°C over 48 or 24 hours, replacement
of the samples in the field, then after one week, the
extraction of soil fauna from experimental and controlled
soil samples. In case of loose ground, small cylindrical
baskets made of wire gauze sieve (mesh 2 mm) were used,
filled with heat desiccated soil, then introduced in field.
This procedure makes easier the removal of treated samples.
In addition, desiccated soil samples incubating in
natural soil provides a substrate to which a great number
of soil animals are attracted only one week later. For
instance, we have collected 96 Lepidocyrtus lanuginosus
(Collembl Entomobryidae ) in one treated soil sample
(100 cc. volume) as compared to 9 in untreated soil sample
of the same size, 27 PseudosinelIa elba ( Entomobryidae )
versus 6, and 8 Orchesella villosa ( Entomobryldae ) versus
none in respective samples.
Similar results were obtained from a previous field
experimental method consisting of putting into a forest
rendzine soil some 100 cc. desiccated soil samples of three
601
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grain sizes (1 - between 10 and 4 mm ; 2 - between 4 and
1 mm ; 3 - ( 1 mm) without fauna, and to check the rate of
settlement an each sieved fraction at regular interval
(VANNIER, 1975). The return of soil animals from surrounding
area was achieved for all zoological groups after 21 days.
Collembola as Poduromorpha, and particularly Neelipleona
and Entomobryomorptia reached a higher density in the coarse
and middle fractions than ones in the natural undisturbed
soil
LITERATURE CITED
BIJAHIN, G.K.A. 1965. The problems of soil recolonisation by
microarthropods. Ph. D. Thesis, University of London.
COLEMAN, D.C. 1973. Soil carbon balance in a successional
grassland. Olkos, 24 : 361—366.
CROSSLEY, D.A. Jr. 1977. The roles of terrestrial sapro-
phagous arthropods in forest soils : current status
of concepts. In The role of arthropods in forest
ecosystems , e T W.J. MMTS0W Sprtnger Verlag,
Berlin : 49-56.
KILBERTUS, G., VANNIER, G., VERDIER, B. 1976. Etude in situ
de la recolonisation par la microfaune et la iiiTcro- -
flore des échantillons de sol forestier ayant subi
un traltement thermique. Bull. Mus. Nat. Hist. Nat. ,
Paris, 419, 33 : 113—142.
MACFADYEN, A. 1968. The animal habitat of soil bacteria.
In Ecology of soil bacteria , ed. T.R.G. GRAY and
D. PARKINSON, Liverpool UF . : 66-76.
REISINGER, 0., KILBERTUS. G. 1975. Documents T.D. de
microbiologie. Université de Nancy I.
VANNIER, G. 1975. Etude in situ du retour des microarthro-
podes sur des fra ions de sol de granulométrie
différente. Bull. Ecol. , 6, 2.: 87-98.
VERDIER, B. 1975. Etude de ]‘atmosphere du sal. Elements
de comparaison et signification êcologique de
l’atmosphère d’un sd brun calcaire et d’un sol
lessive podzolique. Rev. Ecol. Biol. Sol , 22,
3 : 591-626.
QUESTIONS and COMMENTS
H. PETERSEN : Can your observation that oribatids are
more important as immigrants into the acid treated soil cores
than Colleinbola be explained by the low pH or by compounds
evolved during heat treatments which are repellent towards
Collernbola? I noticed that the collenibolan numbers in the
alkaline soil cores culminated in the second week whereas
602
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oribatid numbers in acid soil cores culminated in the third
weei . Could the dominanc’ of Collembola in the alkaline cores
therefore be explained by their greater mobility, followed
by competitive exclusion of the oribati ?
G. VNNXER : We noed further precise inforiration about
selective recolonization upon heat desiccated soil samples.
We can advance a lot of reasons to explain that certain animals
are attracted and others excluded. In addition to your suggestions.
I think that the enhancement of microflora growth is the most
important factor of attraction. I mean, when a microarthropod
invades a treated soil sample, it deposits some droppings from
which a developm;ent of germs starts, precisely the germ strains
it eats.
To answer your second question, I think mobility differences
between mites and springtails are not too much involved in
my experiment because the small size area of the treated soil
samples. I collected samples each with an area of 20 cm 2 .
H. KOEHLER : What role does the dispersal power play for
the rehabilitation of the sterile soil?
Does the change in soil parameter... (water content, texture,
porosity) favor some specific colonizer groups?
G. VANNIER : 0u experimental study did not last enough
time (four weeks) to answer you about the role of dispersal
power on the rehabilitation of the sterile soil. pirst we must
look at the rehabilitation of germ balance which sways the
microarthropods colonization. I’ll keep in mind your interesting
suggestion.
I don’t think such pararneters are involved because I am
convinc d that the colonization by microarthropods is mainly
influenced by a fast microbial growth. enhanced by previous
desiccation of soil samples.
6o
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TFJF ROLE OF INVERTEBRATES IN THE FUNGAL
COLONIZATION OF LEAF LITTER
David A. Pherson
N&,rtl,wg.stern University
USA
INTRODUCTION
Various roles have been given to the arthropods which inhabit the
forest litter coomiunity. While many of these roles are speculative due to
difficulties in experimental methods and/or observations (Crossley, 1977),
they have included fragmentation of the litter (Edwards and Reath, 1963)
thereby enhancing sL.rface area for mic:obial attack, substrate modification
by fecal production (Nicholson et al., 1966; Webb, 1977), and dispersal of
microbial spores either on the body surface (Jacot, 1930; Poole, 1959;
Mignoler, 1971) or by passage through the gut in a viable state (Behan, 1978;
Mignolet, 1971; Witkamp, 1960). In fact, many microarthropod species (mites,
collembola) are known to actively feed on bacteria and fungi (the maJor
decomposecs in forest ecosystams), the latter being known to accumulate
nutrients in their tissues to concentrations much greater than the surrounding
habitat (Cromack et al, 1975; Stark, 1972). Thus the role of art.hropods in
nutrient cycling has been suggested (Crossley, 1976; Crossley and Witkaino,
1964). Therefore an important role of microarthropods is their catalytic
interrelationship with microorganisms (Drift, van der, 1970; Ghilarov. 1963;
Mignolet, 1972; i!itchell and Parkinson, 1976).
The purpose of this study was to investigate and quantify the role which
litter arthropods play in the dispersal and fungal colo3ization of beech
( Fagus grandifolia ) leaf litter in a beech-maple climax community in extreme
southwest Michigan at Warren Woods, Berrien County, Michigan, U.S.A.
METHODS AND MATERIALS
Two aspects of arthropod-inicrofungal interactions were studied. The
first consisted of placing individuals of v:irious arthropod orders singly
onto agar media for a period of 24 to 48 hours at which time the individual
was removed and saved for identification. tr. som cases fungal growth had
covered the animal prior to removal so that identification was restricted to
the level of order. All pertinent information concerning the date, and
litter layer, the species identification as well as the fungal isolates
obtained were recorded. A total of 459 litter organismr including 29 Aceri
49 Collembola, and 45 Diplopods were studied.
Originally an array of agar media was used for the invertebrates including
potato dextrose agar, Czapek-Dx agar, i’nd cellulose agar. Eventually soil
-------
extract agar was used exclusively as it was a non-selective media vhtch isolated
all, the fungi. it also produced slower growth and increased sporulation due
to its nutrient-poor composition. The resultant fungal colonies were sub-
sequently isolated onto malt extract andlor Czapek-Dox agar slants for identi-
fication.
The second experiment involved the use of fine and medium nylon mesh
litterbags of two sizes (5 and 500 microns respectively) which conta ,ned
sterilized (via propylene oxide gas for a /2-h3ur period) and unsterilized
beech leaf discs each in separate litterbags. Each litterbag (10 cm 2 ) contained
10-2.3 cm diameter leaf discs. These litterbags were placed intc the forest
leaf litter at the interface of the L-F horizons. After two weeks in the
field the litterbags were aseptically retr ’ned to the laboratory whereby the
leaf discs were plated individually either on soil extract agar or in damp
chambers. The study consis’ed of two 8easonal periods (Spring and Fall)
corresponding to the pievioualy determined popul& tion peaks of the micro-
arthropods. Each season contained three sampling dates (May, June, and July)
and (October, early December, and late December). For the spring season,
ten sites were utilized within a date, each site containing four litterbags
representing fine and medium mesh each with a sterile and unsterile set of
discs. Thus a sampling date yielded tOO discs per litterbag treatment. Fifty
of these discs were olated onto soil extract egar for isolation of fungi
actively growing on t e discs as well any spores present. The remaining
fifty ere plated by damp chamber method whereoy fungal growth was obtained
from the leaf tisnue only. The Fall season experimental design was similar
with the following modificstions. Only five sites were used per eamplin
date. Each site c3ntained a set of litterbag treatments as in the Spring.
In addition, a chlordane solution application was . pplied to a second set
which was placed at the same sampling site. The chiordane treatment was
devised as an additional method for excluding arthropods while not affecting
the fungal populations (Browu, 1978).
All leaf discs were examined under a binocular microscope with fungal
isolations, identifications and frequency of occurrences (presence or absence)
recorded for each litterbag treatment. All data was compiled for computer
analysis. Since the frequency of appearance of a particular fungi approximated
the b nom , .ial distribution, an arcsine transformation of the percentages of
leaf discs coloni.. ed per sampling unit produced homoscedasticity enabling
analysis of variance to be performed.
RESULTS
Arthropods on agar plates
Four fungal genera commonly found on leaf litter ( Penicillium, Cladosporium,
Trichoderma , and Mortierella) , were determined to be the most frequent isolates
obtained froa the litter invertebrates placed upon the agar media (Appendix A).
A total of nine genera and twenty species were isolated (Pherson, 1979). The
genus Penicillium was the most frequent isolate occurring on 567 of the indivi-
duals plated. This genus, however, contains over several hundred species of
which more than twenty were identified from this study. The other three
genera included single species of Cladosporium, Trichoderma , and Mortierella .
O5
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If this data is c impared with the only similar study (Christen, 1975)
a high diversity of fungal genera may be considered as potentially transported
by these arthropod vectors although only the genera Penicillium, Cladosporium ,
and to a lesser extent Trichoderina and Mortierella were frequently carried.
Lu addition, the number of genera isolated from an individual was, in many
cases a function of size (Appendix B). Oligochaeta, Diplopoda, Coleoptera,
and A -aneLda generally had a greater furigal generic diversity although much
“ariation existed within an order (e.g. Acari, Collembola).
Litterbag experimants
The preliminary results of Pherson (1978) were confirmed with this
investigatton as the expanded litterbag experiments, utilizing a total of
2400 leaf discs, revealed reduced frequencies of colc nization for three of
the four arthropod-carried genera when the leaf discs were enclosed in the
fine mesh. Analysis of variance (Appendix C) indicated that colonization
frequency was both attributable to samplins DATE and TR ATMEN effects.
MEDIA influence, when present, showed the species favored soil extract agar.
A more detailed analysis of variance of the treatment effects (mesh, steriliza-
tion) revealed that sterilization was usually significant. While this may
be explained by the fact that the fungi colonizing these sterilized discs
were unable to reach the frequencies of those discs not sterilized during the
two week interval, it was not ascertained whether the propylene oxide had
produced a time-lag for colonization. More importantly, there was also a
significant mesh effect for Cladosporium, Trichoderma , and Penicillium , as
follows: Cladosporium significantly colonized sterilized discs found within
iiedium mesh more frequently than those within fine mesh during the Spring
season. In the Fall, colonization was once again favored on medium mesh
discs although statistical significance was lacking. Trichoderma was found
to exhibit a similar pattern. Penicilliuin was deter nined to be significantly
more frequent on sterilized discs in medium mesh litterbags than in fine
mesh for both the Spring and Fall season. A significant chlordane effect
was also observed for both Cladosporium and Trichoderma as it was found to
reduce their presence.
DISCUSSION
It has been shown that a particular subset of the leaf litter micro-
fungal community is carried disproportionately by leaf litter invertebrates.
These fungi are considered by Swift (1976) to be resource non-specific or
“generalists”. They consist of four morphologLca .ly diverse fungal gene .a;
a very abundant “dry-spored”, air-borne primary colonizer ( Cladospo:ium) ;
an abundant “dry-spored”, “soil fungus” ( Pciculium) ; a wet-spored soil
fungus CFrichoderma) ; and a soil fungus (which produces endogenous sr res
enclused within a sporangium Qt,rtiezcLla) . All of these are known to be
associated with deciduous leaf litter fungus succession (Hogg and Hudson,
1966; Hudson, 1968, 1971; Jensen, 1974; S ito, 1956).
It may be questioned why these particular fungi, among all those involved
in the leaf litter decomposition process were carried by the leaf litter
invertebrates. Among the possibilities include their prolific spore-producing
606
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capacity. Cladosporiuni is the most commor. air-borne fungi becoming so
abundant that it is one of the major causes of “hay-fever” allergies.
It is also one of the first surface colonizers of deciduous tree buds and
leaves in the Spring. The other three fungi are generally categorized as
“soil fungi”. As such they are frequently noted as appearing on leaf litter
from six months onward after leaf fall. However, Penicillium and Trichoderma
are also known to be common indoor air-contaminants. The prolificity of all
these fungi is reflected in their numerical abundance through soil dilution
plate counts (Jensen, 1963).
Another possibility is that there exists specialized dispersal mechanisms
and/or adaptive morphological features. A close examination of the onidia
(exogenous spores) of Cladosporium, Penicillium , and Trichodexma and the
sporangiospores (endogenous sporcs) of Mortierella reveal highly disparate
morphologies. Cladosporium conidia are large and barrel-shaped; Penicillium
conidia are minute and round to elliptical, Trichoderina conidia are aLnilar
in size to Penicillium but are wet due to a mucilaginous substance; while
Mortierella spores are small and enclosed within a saclike sporangium which
“dissnives” upon contact with another surface.
Even the nzyinatic capacities of these fungi are variable. It ‘& generally
state that the primary colonizers (e.g. C.adosporium ) can produce a wide array
of enzymes (Pugh, 1974), first attacking the easily decomposable sugars on
the leaf surface and later when the leaf becomes senescent, penetrating the
cuticle and attacking the cell walls. Meanwhile the most persistent fungal
flora, those found in the soil, generally have this potent1 l as well as f or
antibiotic production ( Penicilliuin and Trichoderma) . Indeed Penicilliuin,
Cladosporiuin , and Trichoderma are able to decompose cellulose. Interestingly
Pentcillium, Trichoderma , and Nortierella are capable of decc.mposing chitin
(Hudson, 1972). This prompts speculation that invertebrates carry fungi
which may actually attack their o ti integument. Studies of insect fungal
parasites (Madelin, 1968) however show that only Penicilliurn may be parasitic
even though it probably occurs through integuinental wounds. Nevertheless,
my studies have demonstrated that those individuals which died while on agar
media yielded Penicillium and Mortierella growing from their bodies. Alternatively,
this chitin-decomposing capacity ‘tay enable these species to attack the cell
walls of other fungi..
Litterbag experimi nte have been used previously to demonstrate the role
of invertebrates in leaf litter breakdown (Edwards atid Heath, 1963) and foc
assessment of inicroarthropoci populations (Crossley and Hoglund, 1962). This
investigation used litterbags to determine whether invertebrate-carried fungi
would be reduced in colonization frequency on leaf material if the invertebrates
were prevented from entering. The results tend to support this premise for
three of these fungi ( Penicilliin!i, Cladosporium. Trichoderina) .
Several alternative explanations, however, do exist which must first be
examined. These include spore size, hyphal growth activity, litterbag micro-
environments, and water dispersal. These are explained as followe: spore size -
only Cladosporium can be excluded from entering the fine mesh due to its large
spores. Both Trichoderma and Penicillium are small enough to enter and have
done so in laboratory expe iinents; hyphal activity - if differential
growth rates occur for a particular genera, colonization may be affecteU.
607
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This seemed unlikely as all fungi possessed rapid growth rates for colonization
over a two- ek period. (D. Wicklow, pers. comm.). Also hyphae/myceiia were
small enough to easily pass C rough the fine mesh; lit:terbag microenvjronments -
while evidence $ s available to suggest a modification influence (Anderson, 1973),
if strongly present, this would have been demonstrated in major frequency
differencec between mesh sizes containing unsterilized disca. This effect
was infrequently observed; water dispersal - while water may be important in
fungus dispersal (Bandoni and Koske, 1fl4), especially for wet-spored species,
this was not observed for Trichoderma even though it could nass into the
fine mesh bags.
Circumstantial evidence therefore suggests that frequency reduction in
fine mesh litterbags nay be due to the in ibility of mtcroarthropoda to enter.
If true, in what ways may inicroarthropods influence the colonization of leaf
Litter inicrofungi, its successional pattern, and its u .timate effect on
decomposition and nutrient release? While most stuciies show that inicroarthropod
species (mites, colleinbola) are primarily generalist feeders (Anderson, 1975;
Anderson and iea1ey, 1972; Luxton, 1972), feeding preference studies (Christen,
1975; Hartenstein, 1962; Luxton, 1972; Mitchell and Parkinson, 1976) have
shown that Cladosporium and Trichoderma are among the most preferred. This
provides speculation that a poastble mutualistic interaction analogous to
pollination and seed dispersal systems may be operating whereby the animal
while feeding upon a colony becomes encrusted with additional spores which
are then carried about. Additionally, some of the spores or hyphae may psss
through the gut in a viable state (Behcn, 1978; Christen, 1975; Nignolet,
1971; Poole, 1959; Witkamp, 1960). This mutualistic effect may provide
additional stability (May, 1973) to the leaf litter community structure.
Fungal successional patterns may be indirectly influenced by this
arthropod dispersal. Swift (1976) states that one of the potential actions
of primary f mgal colonizers may be to metabolize modifier compounds (polyphenols,
tannins) in leaf litter thereby increasing its palatability to soiL animals.
These animals, in turn may be of potential significance in the spore dispersal
of the later colonizers. The results from this study provides supportive
evidence.
Finally, it is suggested that man-made disturbances upon leaf litter
arthropod populations (e.g. pesticides) may potentially alter the leaf litter
community structure, not only by reduction in litter fragmentation but by
modifying fungal succession through loss of dispersal vectors.
CONCLUSIONS
It is apparent that a particular generic subset ( Penicillium, Cladosporium,
Trichoderma , and Mortierel1 ) of the leaf titter mic.rofungal community is carried
by various arthropod orders in beech ( jagus folia) leaf litter. Of those
arthropod-carried fungi, three a’cnicillium, Cl8dosporiuzn, Trichodernia ) exhibit
significantly reduced colonization frequencies when sterilized leaf discs are
en?losed in fine (five micron) nylon mesh litterbags which exclude the micro-
urthropods. While various alternative hypotheses are shown to be only
partially plausible, circumstantial evidence does suggest an artbropod-dispersal
phenomenon.
608
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It ii speculated that potential 3ffects of man-made disturbances
(e.g. pesticides) on forest lc .f lLtter may affect nicroarthropod populations
which in turn may alter fungal colonization, decomposition and nutrient
cycling processes.
ACKNOWLEDGEI’thNTS
I wish to thank the Department of Natural Resources, the State of
Michigan for permission to work in Warren Woods State Park. L also wish
to thank my wife, Janette, for her assistance in the preparation of this
manuscript.
609
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APPENDIX A. Number and frequency (in parentheses) of selected fungal genera
isolated from a variety of live litter organisms from Warren Woods, Michigan, U.S.A.
Order N Penici!lium Cladosporium Trichoderina Nortierella
Acari 292 149 (.51) 31 (.10) 14 (.05) 20 (.07)
Collenibola 49 37 (.76) 4 (.08) 8 (.16) 1 (.02)
Psocoptera 6 3 (.50) 1 (.14) —
Pseudoscorpionida 4 4 (1.0) 1 (.25) - -
Diplopoda 45 20 (.44) 2 (.04) 5 (.11) 6 (.13)
Chilopoda 4 4 (1.0) -
Isopoda 5 5 (1.0) -
Coleoptera 14 11 (.78) 3 (.21)
a ’. (Staphy linidae,
Carabidae)
Diptera larvae 4 2 (.50) 1 (.25) 2 (.50)
(Unidentified) -
Araneida 25 15 (.50) 10 (.33) 3 (.10)
(Linyphidae)
O ligochaeta 11 6 (.55) 2 (.18) 5 (.45) 1 (.09)
TOTALS 459 256 52 35 33
FREQUENCY .56 .11 .08 .07
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APPENDIX B. Fungal genera diversity associated with
beech leaf-litter invertebrates
X no. fungal
Species N ( genera) per animal
Acari:
Galumn%a ithacensis 76 .46 ± .74
Phthic&tracarus setosuzn 51 .25 ± .48
Hypochthonius rufulus 8 .25 ± .46
Scheloribates sp. 17 .53 ± .80
Unidentified (Oribatid) 38 1.10 ± .34
Veigaia nernorensis 9 .67 ± .50
Colleebola:
Entoinobryoides purpurascens 4 1.25 ± .96
Isotoma albella l. 2.21 ± 1.37
Pxisea claviseta 14 .50 ± .65
Ptenothrix ma -’norata 6 1.17 ± .55
Diplopod :
Unidentified sp. 31 1.29 ± 1.07
Araneida
Linyphiidae 10 1.30 ± .82
Oligochaeta :
Lumbricidae 9 2.0 ± 1.41
Coleoptera :
Staphy linidae 7 1.43 ± .98
6u
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APPENDIX C. ANALYSIS OP VARIANCE FOR LIt1 ERRAC EXPERIMENTS
ALTERNARIA CLADOSPORIUM EPICOCCUM TRICHODERMA MUCORALES PENICILLIUM
SPRING
Date **
Treatment ** *** :_ A
Media * ***
Interaction *** *
Treatment:
Mesh **
Sterilization ** *** * 4 -
Interaction ** **
FALL
Date *** * *** *** **
Treatment *** *fr* * *
Media *** ** *** **
Interaction ** * *** *k* *
Treatment:
Mesh **
Sterilization ***
Chiordane *** ** *
Interaction ** ** **
Significance Level .05 = * .01 = ** .001 =
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and G. J. F. Pugh (eds)., Biology o Plant Litter Decomposition,
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Saito, T. 1956. M robia1 decomposition of beech lLtter. Ecol. Rev. 14:141-147.
Stark, N. 1972. Nutrient cycling pathways and litter fungi. Bioscience 22:
355—360.
Swift, M. J. 1976. Species diversity and the structure of microbial cotenunities
in terrestrial habitats. Pages 185-222 in J. N. Anderson and A. MacFadyen
(eds.), The Role of Terrestrial and Aquatic Organis,us in Decomposition
Processes. Blackwell Scientific Publicattons, Oxford.
Webb, D. P. 1977. Regulation of deciduous forest litter decomposition by
soil arthropod feces. Pages 57-69 mW. J. Mattson (ed.) The Role
of Arthropods in Forest Ecosystems. Springer-Verlag, New York.
Witkamp, H. 1960. Seasonal fluctuations of the fungus flora in mull and mor
of an oak forest. Meded. Inst. Biol. Ondern. Nat. 46:1-52.
QUESTIONS and COMMENTS
S.B. HILL : I was interested in your conunent regarding
chitin decomposition by fungi. I once worked with an insectiv-
orous bat guano medium.which consisted largely of chitin. It
supported one species of fungus, Penicilliuijj lanthinelliun arid
one species of oribatid mite, Rostro-etes foveolathus comprised
80% of the mesoarthropod population arid it appeared to be
feeding primarily on the Penicillium . I had previously con-
cluded that the low pH (4.00) and the antibiotic activity of
the Penicilliuin was responsible for the absence or low population
density of other species of microarthropods. Now I wonder if
they may have been directly attacked by this Penicilliuzn . I
would be interested in your conunents on this.
Q4. P RS0N : I feel that your conclusions are justified.
Little is known 1 the enzymatic capacities of in6ividual species
of the genus Penicilli n to confiaently state that cuticular
attack is responsible for the absence of other microarthropod
species. Rather it appears that Rostrozetes foveolat is
particularly adapted to feeding on that Penicillium species
without suffering from any antibiotic effects.
615
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a
EVOLUTIONARY ASPECTh OF MYCOPHAGY IN Ariolinw.x
coluinbianus AND OTHER SLUGS
Klaus 0. Richter
Urnvers,Iy of Wash:ngloi, and
jul 91 Graham a,ig Co.
USA
INTRO )UCTION
Large size, mobility, and terrestrial habits frequently preclude
slugs from biological investigat ons of decomposition, nutrient cyci.ng,
and other aspects of soil zoology. Only through recent studies of con-
sumption, assimilation, and excrement production (Pallant, 1969, 1970,
1974; Newell, 1967, 1971; Jensen, 1975; Jenntngs and Barkham, 1976;
Richter, 1979) has slug importa. ice in b mas , energy, and nutrient
transfers within soils been clarified. Clearly, these studies show that
slug consumption of fresh, sen escent, and dead vegetation directly
influences plant decomposition and soil humification.
An indirect arid perhaps more significant way by which slugs in-
fluence decomposition and other a . ects of community ecology may result
from slug feeding on fungi (mycophagy) and the concomitant dispersal of
sport s. Fungi are primary agents of decomposition, serious saprophytes,
and form essential mycorrhizal associates with plants; thus their dis-
persal by slugs may significantly influence more involved aspects of
community dynamics.
Slugs feed on a variety of plant and animal matter (Runham and
Hunter, 1970), including fungi in the con ferou, forest of western
Washington, where both slugs (specifically, Ariolimax columbianus Gould)
and fungi are especially numerous. There are no published accounts of
mycophagy in Ariollinax and only few literature accounts of slug feeding
on fungi in North America (Bullet, 1909, 1922; Gregg, 1944; Ingran,
1949; Hand and Ingram, 1950). Accounts of slug mycophagy in Europe are
moz numerous and indicate that most slugs are inycophagous and eat a
wide variety of fungi. Generally, authors itemize fungi ingested by
slugs (Taylor. 1907; Benecke, 1918; Elliott, 1922; Kittel, 1956), although
in Fr mming’s (1940. 1954, 1962) publications consumption was quantified.
The purpose of the present study is to document myco 3 ihagy in
Ariolimax an ” analyze its relationship to fungal taxonomy, listribution,
phenology, and nutritional value. Results will be interpreted within an
evolutionary context in which fungal density, availability of alternate
foods, caloric and chemical composition, and other factors important in
determining herbivore diets (Schooner, 1971; Pulliam, 1974, 1975) will
be investigated. Potential reproductive benefits accruing to fungi from
slug mycophagy will also be considered.
616
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SPECIES DESCRIPTION AND STUDY AREA
Ariolimax columbianus is the dominant and largest indigenous slug
throughout the wet coniferous forests of western North America, often
£ttaining a length of 15 cm and a weight of 20 grams. Seasonal activity
extends from April through October when temperatures are between 7°C and
25°C (Richter, 1376). Maximum densities of slugs within the study area
were estimated at 2500 per hectare, with a total consumption of 62 kg/ha/yr
(Richter, 1979).
Field observations were conducted in a second growth Pseudotsuga
menziesii heterophylla zone, Franklin and Dyrness, 1973) forest
located 55 kin east of Seattle, Washington. The dominant trees include P.
menziesii, A].nus rubra, Aeer circinatum , and Prunus Common
shrub and herb species are Pteridium aguilinum, Gcultheria shallon,
Berberis nervcsa, Polystichum munitum , and Linnaea borealis. Abundant
epigeous fungi include members of the families Russulaceae (e.g., Russula
einetica and Lactarius auraxa.iacus) , Boletaceae (e.g., Suillus lakel and
Boletus zeller!.) , Trieholomataceae (e.g., Laccaria amet y tina and L.
laccata) , and Cantharellaceae (e.g., Cantharellus cibar s) .
METHODC
Slug feeding was observed along transects sur;’eyed at least twice
t.eekly during the study period. Noted during each feeding observation
were length of feediug bout, host age, host part eaten, and the relativc
density of host and its surrounding vegetacion. Feeding preference for
eaten fungi and plants was calculated using Ivlev’s (1961) selectivity
coefficient CE) in which preference is calculated as the relation between
the food item In the diet and the habitat according to
—
E—
where
rj = pexcentage of itc’m in the diet
Pj percentage of item in the habitat
Inorganic nutrient analysis for lichens and senescent leaves, unless
otherwise referenced, follows the methods outlined by Piper ( 944) and
Jackson (1958).
Separate 1aborat. ry experiments were conducted to clarify differ-
ent aspects of mycophagy. In the first group of experiments, a slug
starved for 24 ho rs and one mature aporocarp were placed in several
different 1—liter plastic cups. For 30 minutes slugs were continually
observed through cl ’ar lids under subdued light. Observations were
recorded for this 30-minute period and again 24 hours later to assess
diel feeding.
61?
-------
To d erinine selectivity, an array of 17 species of fungi were
distributed In a circle within a 50— x 50— x 200—cm wooden box whose
base was covered with 2 cm of moist soil. Within the sporocarp -ing,
five slugs were placed o that each animal faced in different directi 1 .rn.
Each slug was subsequently observed and the data recorded on fungi and
part eaten, as descrIbed in the cup experiment.
Phenological preferences were specifically tested in a s t of
experiments in which starved slugs were of fercd immature and mature
sporocarpa of several species. One starved slug was placed in each
eontain€r with either a young or mature sporocarp. After 24 houts
observations were again made on fur gi and part eaten.
RESULTS
Feeding Behavior
In the field, Ariolimax was frequently observed to orient, crawl
towards, and feed extensively on epi geous fungi. They crawled directly
towards Russula emetica and Lac’aria laccata which had been picked and
placed up to 2 m away. In laboratory feeding trials, slugs were observed
to iinmediatcly orient and move towards edible species 0.5 m away. Obser-
vations and documentation that slugs exhibit a highly developed sense of
suieJi (KIttel, 1956; Bunham and Hunter, 1970) and that many mature fungi
give off strong odors (Maser, Trappe, and Nu ,sbaum, 1978; Miller, 1978),
support my observations that Ariolimax ]ocatt c edible species by olfaction.
Importance of Mycophagy
Mycoplu&gy accounted for 11% and 5 of 1973 and 1974 f ding
observations (Richter, 1976) and was limited to a few epigeous basidiomy-
cetes such as R. emetica , R. pologonia , R. placata, Lactarius obnybylus ,
and Boletus adler!. Common but uneaten fungi included Amanita silvi ola,
Coltricia perenis , Cantharelluscibarius, Lyophyllum uiulticep3 , and the
ascomycete l1elvella lacunosa . Feeding on ft. emetica accounted for more
than 50% of total feeding observations, with the balance being distributed
among other ussulaceae, Tricholomataceae, and Boletaceae. Mycophagy, as
expected, primarily occurred in October when sporocarps were abundant.
During this month, fungi accounted for 39% and 13% of the 1973 and 1974
diets, respe’ tively. Lower dietary importance of fungj in 1974 reflects
temperatures above and precipitation below the 10—year norm, which
reduced sporocarp production and extended availability of vegetation.
The Shannon—Weaver diversity index was applied to observed slug
diets. H’ was calculated from the equation
S
— I pilogpi
1=1
618
-------
and corrected for the bias of the estimate (Poole, 1974), and indicated
that slug feeding is responsive to sporocarp production and vegetation
phenology. A 0.98 October 1973 value quantifies and supports the observa-
tion that slugs feed on few food sources, of which fungi were the major
component. A significantly higher 1974 value of 1.54 suggests that diet
was incre diverse than in 1973 and indicated that sporocarps and plants
exhibited equal numerical importance.
Field Preferences for Fungi and Hymenium
Inspection of Table 1 showu that, of six cate&ories of food items
eaten, fungi and the lichen Parmelia were the most preferred (index
+0.9). However, feecing bouts on fungi was significantly longc r than on
Parinelia sp. and alternative items (Extended Median Test, P < 0.5;
Conever, 1971). Mean feeding bouts on sporocarps averaged 47 and 48 min-
utes during 1973 and 1974, whereas on Pteriiium aquilinum , the second
most popular item, f eding was significantly Lower, at 27 and 32 minutes,
respectively (P c 0.01). Although P. aguilinum , senescent leaves, and
other foods were eaten more frequently than fungi in 1974, and Parmelia
sp. exhibited an identical preference index as fungi in both years, only
slugs feeding on fungi exhibited higher composite values of frequency,
preference, and length of feeding bouts.
TABLE 1. Importance of and preference for fungi, lichen, and other
items in the October diet of Ariohmax (— = value undetermined)
Number of
% of Total
Preference
Feeding Time
Observations
Observations
Index
(minutes)
Dietary Component 1973 1974
1972 1914
1913 1974
1973 19Y
Fungi
(e.g., Russula ometica) 14 10 39 13 40.9 40.9 47 48
Lichen
(e.g.,Parmeliasp.) 4 12 11 16 +0.9 40.9 36 14
Senescent deciduaus leaves
(e.g.,AInosrubi ) 5 16 14 21 40.9 0.0 28 36
Senescent forest herbs
i.e., Pteridium açuilinum) 12 23 33 30 40.4 40.4 27 32
Others
(e.g., Trillium o aWm) — 8 — 11 40.8 -— 12
Fruit
(i.e., Caufrhe,ia ,J,allon) 1 7 3 9 -0.8 -0.4 15 19
619
-------
In addition to Ariolimax’s preference for fungi over other foods,
slugs preferred certain fungal parts over others. Combined two—year
feeding data reveal that, of 24 feeding observations, 63% were restricted
to mature sporocarps and of these 85% to the hymenium. The stipe was
preferred in all four m ’n ture specimens eaters and only accounted for
15% of feeding on mature fungi, while the pileus was not observed to be
eaten during any feeding bout. Clearly, the hyn enium is preferred c ,er
the stipe or pileus in mature fungi a’td the stipe over other parts in
imm ture sporocarps (Chi square — 11.2, P < 0.01, df 2).
Laboratory Preferences
Many fungi, including A. silvicola , C. cibtrius , and H. lacunosa ,
which were common but not observed to be eaten in the field, were eaten
during laboratory preference tests. This may be expected as the short
48—minute field feeding bout increases the possibility that less preferred
fungi may have gone unrecorded. Additionally, starved laboratory slugs,
when offered limited choice, are more inclined to feed on low preference
species. Only three species, Coprinus atramentarious, Lactarius auran—
tiacus , and one unidentified Cortinariaceae, were avoided both in field
anca laboratory. In total, 18 of 21 (86%) tested species were eaten
without any immediately apparent ill effects. These data suggest that
many more fungi may contribute to autumaal food requirements than are
suggested from field observations alone.
Taxcnomic trends in slug feeding preferences are apparent for
those families represented by the several species of fungi eater during
testing (Thbles 2 and 3). Generally palatable to Ariolimax ai e the
Boletaceae (represented by one genus, three species), Russulaceae (repre-
sented by two genera, five species), and lricholomataceae (represerii ed
by five genera, six species). C. atramc’nt zrious (Coprinaceae), Corttnai ius
sp. (Cortinariaceae), and L. aurantiaeus (Russulaceae) were not eaten.
Russula sp. and Lactarius flu 3 s were the two species most readily
eaten, followed by P. emetica , L. multiceps , and Boletus sp. Although R.
emetica is not always the most preferred as determined by laboratory
tests, it remains the most important to Ariolimax because of its density
and ubiquitous distribution.
In the cup experiment, in which Ariolimax was given no alterna-
tive to the test species, 13 of 17 (76%) fungi were eaten (Table 2).
Only five (29%) species were fed upon during the first 30 minutes of
testing; the remaining speciec were eaten within 24 hours. Results of
the smorgasbord test, in which slugs chose from among 17 simultaneously
available species, were similar to the cup teat. However, two species,
L. laccata and Col. ybia sp., were not eaten, and one species, Boletus
mirabilis , was eaten in the smorgasbord but not in the cup test (Table 3).
Feedii g ’ ,n nine (53%) species, five of which were also promptly eaten in
the cup experiment, commenced within the first half hour. However, since
five slugs were tested in each replication of Lhc smrrgasbord test, a
greater probability of observing some prompt feeding would be expccted.
620
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TABLE 2. Results of cup palatability tests on 17 species of fungi including replications, start
of feeding, minutes of feeding, and fungal part ingested (U = undetermined, N = no feeding
observed, H = hymenium, P pileus, S = stipe, 1 feeding initiated within 15 minutes,
2 feeding initiated between 15 e’ d 30 minutes, 3 = feeding initiated after 30 minutes)
Number of
Replications
In Which
Feeding
Feeding
Time In
Sporocarp
Part
Fungi Replications
Species Eaten
Interval
Minutes
Ingested
Ascornycetes
Helvellaceae
He! ye/la lacunosa 1 1 2 30 S
Basidiomycetes
Amanitaceae
Amanita si/vicola 2 1 1 40 H
Boletacaae
Boleu,s mirabilis 1 0 N N N
Bolews zelleri 1 1 3 U H
Suillus !akei 2 2 1, 1 45, 40 H
Cantharellaceae
canthare/lus cibarius 2 2 1 • 2 25. 30 P, H
Copiinaceae
Copi-inus atramentarious 1 0 N N N
Cortinariacea
Cortinarius sp. 1 0 N N N
Russulaceae
Lactarius aurantiacus 1 0 N N N
Lactariussanguifluus 2 2 3,3 U, U H, H
Russula cascadensis 1 1 3 U H
Russula ernst /ca 2 2 1 • 3 45, U H, H
Ruzu!asp. 2 2 3,3 U, U H, H
Tricholomataceae
Ccllybiasp. 1 1 3 U H
Leccarie amethyst/na 2 2 2,3 35, U H
Laccaria Mcc ta 2 1 3, N U, N H
Lyopliy !Ium mu/f/caps 1 1 3 U H, S
621
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TABLE 3. Results of smorgasbord palatability tests on 17 spccies of fungi incluiiing replications.
start of feeding, minutes of feeding, and fungal part ingested (U = undetermined, N no feeding
observed, H = hymenium, P = pileus, S = stipe, 1 = feeding initiated within 15 minutes, 2
feeding initiated between 15 and 30 minutes, 3 feeding initiated after 30 minutes)
Number of
Replications
in Which
Feeding
Feeding
Time In
Sporocarp
Part
Fungi RepUcations
Species Eaton
Interval
Minutes
Ingested
Ascomycetes
Helve’laceae
He/ye/la lecunosa 2 1 3 40 S
Basidiomycates
Amanitaceae
Amanitasilvicola 5 3 1,1,3 15, 30, U H, HS, H
Boleteceae
Boletus mirabilis 3 2 3, 1 U, 10 H, H
Boletus zelleil 2 2 3, 2 U, 30 H, H
Suiiluslakei 2 2 3,2 U,25 H,H
Cantharellaceae
Canthare/fus cibarius 5 2 1, 1 15, 15 H, H
Coprinaceae
Coprinus atrementarious 3 0 N N N
Cortinariacea
Cortinarius sp. 3 0 N N N
Russulaceae
Lacterius auranriacus 2 0 N N N
Lactarius sanguifluus 5 3 3,2, 1 lJ, U, 40 H, II, H
Ru ula :accadensis 3 1 2 25 H
Ruwila ernetica 5 3 2,3,3 30, U, U HP, H, H
Ruwilasp. 5 5 3.3,3,3,3 U,U,U,U,U H,H,H.H,H
Tricholomataceaa
Collybiasp. 3 0 N N N
Laccaria amethysti,a 5 2 2, 1 25, 15 H, H
Laccaria laccata 5 0 N N N
Lyophyflum multiceps 2 2 3, 2 U, 20 H, S
622
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Although the same fungi were generally eaten in both experiments,
feeding bouts fat single slugs in cups were longer on five of six eaten
species. This difference may be accounted for by .he fact that slugs had
only one type of ‘ungi from which to choose and no secondary stimuli
from other fungi species. The pileus and stipe are occasionally eaten;
however, 90% of mycophagy occurred on gills in both the cup and smorgas-
bord experiments (Tables 2 and 3), thus indicating a preference f or the
hyinenium and confirming field observations.
Table 4, depicting the laboratory results of Ariolimax’s feeding
on young and mature fungi, indicates that, of the four species eaten,
a preference was exhibited for mature sporocarps (Chi square 17.71,
P < 0.001, df 1). In two of the four species, Mycena haeaatopus and
Naeinatoloma fa iciculare maturu sporocarpa were almost exclusively eaten.
In the other two species, R. emetica and Amaiiita m’iscaria , both young
and mature sp imens were eaten; however, a greatev proportion of mature,
rather than immature, sporocarps were consumed.
TABLE 4. Results of Arioshnax fecding on young and mature
fungi (A = species avoided regardless of age, P probable
difference attrihutable to age)
Young S
Fungi Yes
porocarp
No
s Eaten
E
Mature S
Yes
porocarp
No
a Eaten
General Result
Ascomycetes
Hellvellaceaa
lic/vdlla Facunosa 0 5 5 0 5 5 A
Basidiomycetes
Amanitaceae
Arnanita miiscaria 4 3 7 5 1 6 P
Cantharellaceae
anthareIIus cibarius 0 5 5 0 5 5 A
Russulaceaa
Russula emetica 3 7 10 10 0 10 P
Strophariaceae
Naemato!oma f,,scicu!are 1 6 7 4 3 7 P
Tricholomataceae
Marasmius creades 0 3 3 0 5 5 A
Mycenahaen,otopus 0 4 4 6 1 1 P
623
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DISCUSSION
Ariolimax Columbi3nus , like other slugs, feeds heav±ly on fungi.
Taylor (1907) indicated that Anon subfuscus Drap. ( fuscus Mull.) showed
a preference for fungi and Elliott (1922) found that L1ina c maximus , L.
cinereoniger Wolf ( maximus L.), and ArLon ater L. fed on most of 60
species of fungi tested, although ArLon circumscniptus Johnst, Limax
arbortim Bouch ( 1atus Mull.), and Milax sowerbyi Fer. showed low
feeding preference for many of the same species. In extensive studies
Fromming (1954) determined that both Anon ittermedius Norm, and Limax
teneU.us Nilss. ate all of 24 tested species, although A. intermedius
never ate the quantities observed eaten by L. tenellus .
Certain factors may explain the widespread use of fungi by slugs.
According to optimum foraging theory, slugs should respond to changing
food density and quality by selecting those f tems that maximize growth
and reproduction (Schoener, 1971). Mditionally, theory postulates that
nutritious food sources should favor specialization, whereas poorer
sources should lead to generalization with respect to diet (Morse, 1971;
Schoener, 1971). Recent refinements to herbivore feeding theory have
also encompassed aspects of plant phenology (Feeny, 1970; McKay, 1976)
and coevolutionary strategies between hosts and animals in that plant
defensive chemistry determines the breadth of herbivore diets (Rhoades
and CatEs, 1976; Rhoades, in press).
Food enstty
During October, when epigeous Basidiomycete are most abundant
(Littke, 1978), Anlolimax preferer.cially feeds on fungi to the exclusion
of other available and commonly eaten foods. Fungi availability certainly
accounts for their numerical importance in the diet; however abundance
alone cannot account for the extensive mycophagy observed in Aniolimax
and other slugs. Nutritional characteristics, including physical and
chemical defenses and caloric and elemental composition, are also ex-
pected to be important. In autuma nutrition is especially signifIcant to
Aniolimax and other long—lived slugs which must store reserves prior to
winter brumation.
Food Quality
Physical Defenses . Fungi may possess morphological special za—
tions that are effective against slugs. Field and laboratory observations
on Aniolimax and other slugs (Fr ing, 1954, 1962) indIcate that both
the pileus and stipe may be better protected from grazers than the
spore—bearing hyinenium. For example, hyphae of thc highly preferred
hymenium az. sparse and thin-walled when compared to the less preferred
stipe and pileus, in which hyph ,e are densely intertwined and compara-
t 4 voly thick—walled (Pil t and Us k, 1958). Additionally, chitin is the
major cell wall material of both Ascomycetes and Basidiomycetes and is
found in sIgnificantly higher concentrations in the stipe than pileus
(Fr ing, 1962). Although slugs have the capacity for hydrolyzing
chitin (Runham and Hunter, 1970), the energy required for extracting
nutrients may be prohibitive.
624
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Ryphae may further be categorized as forming shaggy fibrils or
scalt s on the pileus and stipe and spines or teeth on the hynienium, as
observed in Hydnaceae. These characteristics could additionally function
as physical deterrents to invertebrate mycophagists. Because species
with these unique adapatations were not represented among those fungi
.ested, it is unknown to what extent these specializations influenr.e
palatability or the role structural characteristics play in defense,
reproduction, and other functions.
Chemical Defenses . Buller (1909) suggested that toxins protect
fungi from slugs. This contention is directly supported by my unpublished
observations, in which several L. maximus died from feeding on iimn ture
Amanitamuscaria, and those of Taylor (1907) and Elliott (1922), in
which slugs succumbed after devouring other species. ConsIdering all the
chemicals isolated from fungi (Cochrane, 195 i; Shibata, Natori, and
Udagava, 1964), one nay certainly expect to find species toxic to slugs.
Alkaloids which are known to deter herbivory and result in poor growth
and reproduction in several invertebrates (tevin, 1976a, 1976k) are
prevalent in fungi (Tyler and Stuntz, 1962, 1963) and could similarly
affect slugs. Differential susceptibility of slug species and indiv!duals
within a species to fungi may alsn be expected (Crawford—Sidebotham,
1971).
Nutritional Aspects . Fungi rank high in both caloric and chemical
content when contrastea to a1 ernative dietary components. Caloric
values of 4.1 to 5.2 kcal gm dry weight in fungi are higher than
values found in senescent forest herbs, and comparable to values calcu-
lated for senescing leaves of deciduous trees (Table 5). Since fruits
generally have higher caloric values, fruits of Gaultheria shallon
probably would exhibit caloric values between 5 and 6, similar to that
of Vaccinium deliciosum .
During autumn chemical content of many plants is at its lowest
(Lugg and Weller, 1948; Fraenkel, 1953) beause leaf senescence is
accompanied ‘y a sharp reduction in N (Edel’man, 1963; Richter, 1979)
and frequently other nutrients including P, K, Ca, Mg, etc. (Richter,
1979). Fungi therefore become iicreasingly valuable to slugs for their
high concentrations of these elements (Cochrane, 1958) and for the
organic compounds they contain (Singer, 1961). For example, fungi exhibit
significantly higher percentages of protein than senescent leaves of
Pteridium aguilinum, Trillium sp. Dicertra sp., and the lichen Parmelia .
Similarly, carbohydrate content in fungi is substantially higher than in
available P. aguilinum and probably also highcr than that found in
Parmelia and the senescent leaves of both herbs and trees (Table 6).
Some fungi are considered excellent sources of nicotinic acid, riboflavin,
niacin, and pantothenic acid, and a fair source of vitamins B, C, E, and
K (Singer, 1961), which may additionally be valuable ir. supplying slugs
with certain trace compounds unavailable from other sources.
That slugs particularly relish the hymenium is demcnstrated in
this and numerous other studies (Buller, 1909; Benecke, 1918; Fr&iming,
1954, 1962). It is interesting to note that the hymenium exhibits a 13%
to 20% higher caloric value than the pileus or stipe (Smith, 1965), and
625
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TABLE 5. Caloric composition of fungi, senescent vegetation, and fruit, of
which the same or similar species are eaten by Ariolimax and other slugs
Dietary C mponent Kilocalories/Gram’ Dry Weight Reference
Fungi
Ru uIa decolorair,
Hymenium 4.8 Smith, 965
Pileus 4.0 Smith, 1965
Stipa 4.2 SmIth, 1965
Suillus tomentosu:
Hymenium 5.2 Smith, 1965
Pileus 4.2 Smith, 1965
Stipe 4.1 Smith, 1965
Senescent Forest HerLs
T&llum recurvatum 3.9 Kieckhefer, 1962
Dkon’ra canadensis 4.0 Kieckhefer, 1962
Senescent Deciduous Leaves
Alnus rubra 4.6 — 5.8 Jensen. V., 1974
Acer rubrum 4.4 Jensen, V., 1914
Fruit
Vaccinium deliciosum 5.3 Smith, 1970
6 26
-------
TABLE 6. Chemical composition of fungi, lichen, and senescent vegetation,
of which the same or similar species are eaten by Ariolimax and other slugs
value undetermined. ‘protein N x 6.25)
Percent 0
ry Weight
Carbo-
Dietary Component Protein Fat
hydrate Ash Reference
Fungi
Boletusod ,ilis 32—35 5 58-59 6—8 Singer, 1961
Lactan , ,sdeliciosus 27 7 28 6 Singer, 1961
Tricholormafavovirens 15—18 —- 71-78 7—11 Singer, 1961
Agaricus sp.
Pileus 62 3 — 7 Singer, 1961
Stipe 48 1 -— 7 Singer, 1961
Lichen
Parrnelia sp. 5’ — —— --- Richter, 1979
Senescent Forest Herbs
Pteridiwnaquilinium 91 22 14 1)MoonandPal,1942
2) Shearer, 1945
3) Williams and Foley, 1976
Trillium reculvatuin 12 — — Kieckhefer, 1962
Dicentra canadensis 9 — — — Kieckhefer, 1962
Senescent Deciduous Leaves
A/au: rugo 111 . — 8_142 1) Kaushik and Hynes (1971)
in Willoughby, 1974
(angiosperm lifter)
2) Jensen, V., 1974
627
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that the hymeniuin, including the pileus, has a 33% higher protein content
than the stipe (Singer, 1961). Because the value of food lies in its
digestability as well as its nutritional content, it is significant to
note that, of six leaves of plants and the fungi Arniillaria ( Armillariellaj
mellea fed to A. ater , both highest consumption and assimilation rate
occurred when this slug ate Armillariella (Jennings and Barkham, 1976).
Ilycophagy and Reproductive Success of Fungi
As early as 1889, Stahl observed massive quantities of germinating
spores of Morchefla esculenta in the faces of Anon empiricorum . However,
Voglino (1895) first suggested that slugs are important agents of spore
germination and dissemination in epigeous fungi. Specifically, Voglino
observed improved germination in snores of numerous species of fungi
which had first passed through a slug’s digestive tract. For some species,
he observed that spores required slug digestive fluid as a prerequisite
to germination.
Buller (1909, 1922) disclaimed a symbiotic relation betwecn slugs
and fungi, contending that slugs are troublesome ectoparasites affording
no advantage to fungi. However, Buller must now be rcevaluated in context
of current fungi ecology. For example, it has long been known that fungi
must depend on readily available organic substances for growth and
reproduction, but it has only recently become established that the
essential ectomycorrhizal associations that many fungi must form in
order to take up required nutrients occur withii a few select hosts
(Trappe, 1962). In addition, information based cii induced germination in
spores of ectomycorrhizal fungi within slug digestive enzymes (Bowen and
Theodorous, 1974, in Fogel and Trappe, 1978) suggests that slugs may be
significant in ensuring the success of these essential associations.
Furthermore, the dispersal of fungi among their mycorrhizai
associates may be aided by slug feeding behavior. Ariolimax , for example,
exhibits host fidelity (i.e., feeds on relatively few core species),
thus facLlitating the dispersal of spores between different individuals
of the same species. Slugs thus offer a directional component to spore
dispersal that would be unattainable from wind or water dissemination.
Although most spores are likely to be excreted within a few days follow-
ing feeding, Ilasaii azad Vago (1966) found that spores in slugs were
regularly excreted and viable within feces for eight days, a sufficient
time Zor slugs to find conspecifics of the original fungal host or other
suitable mycorrhizal associates, depending on fungi specificity.
Slug feces possess the necessary biological and physical traits
of a good germinating substrate. Slug feces provide nutrition for devel-
oping mycelia (Wagner, 1896; Neger, 1908; Hasan and Vago, 1966). Both
chiamydospores and hyphae exhibit narrow tolerances of humidity, tempera-
ture, and pH (Lamb and Richards, 1974), which to some extent is favorable
in slug feculae. Thus slug feccq provide a readily avail&ble and favor-
able innoculum which is important for oidia and basidiospore germination
and has been shown to be essential to chiamydospore and hyphae survival.
628
-------
Slug preferences for the hymenium of certain ftngi, the mixing
within crop and intestine of spores and hyphae from conspecifics, host
fidelity, and the nonrandom distribution of innoculated feces greatly
facilitate recombination and outbreeding. These actions are especially
important to ‘the great majority of higher fungi... characterized by
obligatory crossmating, and, in all cases, self—sterility is imposed by
an Incompatibility mechanism” (Raper, i966, p. 39). Slug feeding and
dispersal characteristics are highly beneficial to fungi characterized
b) an vn!ven distribution of mating types. For example, mycophagy on
heterothalic species increases the probability that two spores of
different sex germinate near each other so that a monosporic mycelia can
copulate to form a fertile mycelium of binuclear cells. Evolution of the
dikaryon, parasexualicy, and mating types have made pcssible the success
of fungi as a group. It is through uffective spore and mycelial dispersal,
in which slugs play a significant role, that successful germination,
penetration, and host colonization occur.
In st ry, Arlolimax perferentially feeds on fungi which, in
general, provide a food resource that is abundant, nutritioun, and more
readily assimilated than other available food. Additionally, Ariolimax
and other slugs select the hymenium whose tissues exhibit the least
mechanical barriers to feeding while simultaneously possessing the
highest nutritional content c l all fungi structures. Benefits to fungi
of slug mycophagy probably include induced and/or improved germination
of spores through digestive processes and a benigi fecal innoculum,
directional dispersal of prop gules, and increased opportunity for
genetic recombination and outbreeding.
Comparison of Snorocarps and Vascular Plant Fruits
The most interesting aspect of this study was the observation of
a striking par il1e1 between the development of aporocarpa In fungi and
the ripening of fruit in higher plants, and mycophagy In slugs and
frugivory in birds and m mi’ ls. The dispersal of sporer by air is the
prime function attributed to the sporocarps of epigeous fungi (Ingold,
1953). My stud’, however, suggests that animal dispersal may be equally
important. Sporocarpa are essentially morphologically and physioLogica].1.y
analogous to vascular plant fruits in that sporocarps protect developing
spores (i.e., unicellular seeds) from drying out, defend against premature
predation by molluscs (and probably also arthropods and ‘nn’n’ils), and
attract animal dispersers to mature forms by producing attractants and
inactivating defensive mechanisms.
In addition, phenological changes (including exposure and availa-
bility of the highly nutritiouia spore—bearing hymen.Lum; a rise in palata-
bility, most likely attributable to a change in toxicity; and exudation
of secretions and production of strong odors that frequently characterize
fungi growth and development) suggest that sporocarp evolution represents
an adaptation to antmal as well, as air dispersal. Similar morphological
and physiological characteristics in hypogeous fungi, wnich exhibit no
mechanisms for di8charging spores above ground, have been considered
traits that encourage mycophagy and facilitate dispersal. (Ingles, 1947;
Fogel and Trappe, 1978; Maser, Trappe, and Nuasbaum, 1978).
629
-------
In conclusion, it must be noted that the ccmparison of fungi
sporocarps with iascular plant fruits are currently speculative since
they depend on limited data, especially with respect to fungal metabolites.
Nevertheless, this p p r does provide inforviation and support that can
be more extensively analyzed to detect the mutually beneficial aspeets
of mycophagy and funga]. reproduction d dispersal.
ACKNOWLEDG tENTS
I would like to thank Chris Karan for help in collecting and
identifying certain fungi and John Dragavon for editing an early draft.
Drs. Jim Trappe and David Rhoades kindly reviewed the martiscript aud made
valuable suggestions. Last, but not least, X am grateful to Mary Lou
McDonald for editing and preparing several drafts and the final manuscript.
The work was supported in part by NSF Grant No. DEB—74-20744 AOA to the
Coniferous Forest Biome Ecosystem Analysis Study. This is Contribution
No. 354 from the Coniferous Forest Biome.
APPENDIX A
INDEX TO VASCULAR PL 4TS
Family - Cc us, Species, Authority
Ac era ceae Acer circinatum Pursh
Berberidaceae Berberis nervosa Pursh
Betulaceae A]nus rubra Borg.
Alnus rugosa (Du Roi) Spreng
Caprifoliaceae Linnaea borealis L.
Ericaceae Caultherja shajj.on Pursh
Vaccinium deliciosum Piper
Fumariaceae Dicentra canadensia (Goldie) Val .
Liliaceae Trillium recurvatum Beck
Pinaceae ! eudotsuaa met!ziegii Mirbel) Franco
Tcuga heterophylla (Raf.) Sarg.
Polypodiacs ’ae Priystichum munitum (Kaulf.) Presi
Pter diujn aguilinum (1.) Kuhn.
Rosaceae Prunus (Dougi.) Waip.
630
-------
APPENDIX B
INDEX TO FUNGI
Family Genus, Species, Authority
As comy tes
Relvellaceae Helvella lacunosa 2r.
Morchella esculenta Pers. ex St. Adams
Basidiomycetes
Amanitaceae Amanita silvicola Kauff.
Amanita muscaria (Fr.) S.F. Gray
Boletacene Boletus mirabilis Murr.
Boletus zelleri Murr.
Suillus lakei (Murr.) Smith and Thiers
Car1tharellaceae Cantharellus cibarius Fr.
Coprinaceae Coprinus atramentarious (Bull. ex Fr.) Fries
Cortinariacea Cortinarius sp.
Russulaceae Lactarius aurantiacus (Fr.) S.F. Gray
Lactarius sanguiLluus (Paulet ex.) Fr.
Russula cascaden is Shaffer
Russula emetica (Fr.) Pers.
Russula sp.
P.ussula obscuratus
ussula pol.ogonia Niolle
Russula placata Burl.
Tricholomataceae Armillariella inellea (Vahiex Pr.)
Collybia sp.
Laccaria amethystina (Bolt. ex Hooker) Murr.
Laccaria laccata (Sop. e.x Fr.) Berk. and Br.
Lyophyllum niulticeps Peck
Marasmius oreades (Bolt. ex Fr.) Fr.
Mycena haemotopus (Fr.) Quel.
Strophariaceae Naematoloma fasciculare (Huds. ex Fr.) Karat
Gastromyce tea Phallus impi dicus Pers.
631
-------
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Elliott, W.T. 1922. Some obRervations on the mycophagous propensities of
slugs. Trans. Br. Mycol. Soc. 62(1):183—191.
Feeny, P.P. 1970. Seasonal changes in oak leaf tannins and nutrients as
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51: 565—581.
Fogel, K., and J.M. Trappe. 1978. Fungus consumption (mycophagy) by
small animals. Northwest Sci. 52(1):l—31.
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Washington. P14W Range and Experiment Station, USDA Forest Service
Gen. Tech. Rep. PWN-8. 417 pp.
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den Blatter — und Locherpilze: . Ang. Bot. 2 .:157—167.
Fr niming, E. 1954. Biologie der mitteleuropaschen Landgastropoden.
Duncker and Humbolt, Berlin. 404 pp.
Fr&nming, E. 1962. Des Verhalten wiserer Schnecken zu der Pflauzen ihrer
Umgebung. Duncker und Humblot, Beclin 348 Pp.
Fraenkel, G. 1953. The nutritional value of green plants for insects.
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Entomologj, Amsterdam, 1951.
Gregg, V.0. 1944. Notes on land slugs of Los Ar.geles and Orange County
California. Nautilus 57:109-115.
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Hasan, S., and C. Vago. 1966. Transmission of Alternarj brassicola by
slugs. Plant Disease Reporter 50:764—767.
Ingles, C.G. 1947. Maals of California. Stanford University Press,
Stanford. 258 pp.
Ingold, C.T. 193. Dispersal in Fungi. Clarendon Press, (bxford. 197 pp.
Ingram, W.M. 1949. Natural history observations on Philomycus carolini—
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Ivlev, V.S. 1961. Experimental Feeding Ecology of Fishee. Yale University
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Jackson, M.L. 1958. Soil Chemi. al Malysis. Prentice—Hall, Englewood
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Levin, D.A. 1976a. Alkaloid—bearing plants: An ecogeographic perspective.
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Lugg, J.W., and R.A. Weller. 1948. Protein in senescent leaves of Tn—
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Maser, C., J.M. TrappL, and R.A. Nussbaum. 1978. Funga1—s nall in ”mnl
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McKey, D. 1974. Adaptive patterns in alkaloid physiology. Amer. Nat.
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6%
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THE USE OF COTTON STRIPS IN A MiCROCOSM STUDY OF
THE ENERGY COST OF A PREDATOR-PREY RELATIONS} IP
J. A. Springett
Ministry &if AgricsiI1ur and F,shrnes
New Zealnnd
INTRODUCTION
It has been stated (Macfadyen, 1963) that a major role of the
soil fauna is to increase the rate of litter decomposition in the
soil by stimulating microbial activity. Standen quoted In Heal et
al. (19Th) states that decomposition Is i.35 times higher when
enchytraeid v rms are present. The loss in tensile strength of cotton
cloth burled In the field (Latter and Howson, 1977) has been used to
compare relative rates of decomposition (Heal et al., 1975). Springett
(1979) showed that under field conditions a reduction in the species
diversity of soil mlcroarthropods is correlated with a reduced rate of
decomposition as 1ndIcat d by loss in tensile strength of cotton strips.
This same technique has been extended for use in laboratory microcosms
where the effects of changing the species composition of the micro-
arthropod fauna can be measured under controlled conditions.
METHODS
Microcosm chambers were made from soil extract agar plants
sprinkled with a thin layer of fine soil (Sprlngett, 1964). The soil
was not *rllized and had been treated only by thorough mixing and the
renoval of those organisms which could be seen under 40x stereo-
magnificetion. Each microcosm possessed a compimnent of microbial life
and it was assumed that the fungi, yeasts, bacteria and protozcla were
evenly distributed throughout the 60 replicates of the experimental
treatments. Al I the microcosms were kept at constant 20°C in a saturated
atmosphere during the experiment.
The experimental treatments were:
1. microcoms containing breeding populations of
the collembolan Folsoinia candida Willen
2. microcoms containing breeding populations of
F. candida and a predator, an unidentified
mesostigmatid mite (Neoparasltidae).
3. microcosms without added .nicroarthropods.
637
-------
F. candida is a generalized detritus feeder whose ut contents in
the m1crocosmsj u31ly consist of: recognizable plant and fungal
debris, amorphous dark material and small mineral particles. The
adult mesostigmatid mite feeds on all life stages of f. candida In the
mlcrocosms and the juvenile mite on the eggs and the newly hatched
collembo es.
The relative rates of energy flow In each experimental treatment
were estimated by measuring the loss In tensile strength of small strips
of cotton cloth, such loss being related to the degree to which t1 e
cellulose had undergone decomposition during the 41 da of the experi-
ment. This method estimates the comparative average rates of energy
flow over a period of time covering the full life cycle of the orgar.lsms.
The animals were introduced into the microcosms, and after the first
coll .bolan eggs had hatched the resulting juveniles were allowed to grow
to breeding size (44 da) before the Initial cotton strips were replaced
by new cnes and the experiment started. Throughout the experiment the
microcosms contained between 100 and 150 Individual of f.. candida (ex-
cluding eggs) and an average predator population of 4 indIviduals.
Three cotton strips of a standard size (10 wasp threads by 50
weft threads) ;vere placed on the surface of the agar in each microcosm.
After 41 da tgie cotton strips were removed and stored at 50% humidIty
and 20°C for 24 hr before the tensile strength was measured. Measurement
of the tensile strength of subsamples of the cloth at the beginning of
the experiment and on the strips from the microcosms were made u5ing an
Instron Tensile Testing Instrument with a strain rate Of 5 cm/mm, a
chart speed of 10 cni/niin and a full chart load of 10 kg.. The results
are expressed ac mean kilogram load per cotton strip and as percentage
loss In strength (Table 1).
TABLE 1. THE TENSILE STRENGTH AND PERCENTAGE LOSS IN STRENGTH
OF COTTON STRIPS IN SOIL MICROCOSMS
Mean Initial strength of cotton cloth = 1.47 kgms
strip (S.E. • 02)
per
Treatment of microcosm
mean strength
(kgm/strlp)
% loss In
strength
n60
1.
2
3.
Folsomia caridida only
F. candTda plus
R microarthropoda
0.40 S.E.=0.05
0.27 S.E.=O.03
0.55 S.E. O.07
73
81
63
638
-------
Fi 9 ure f: ? D4TO PREY ELATEP TO TIME’
AWt MU ROCC*M.
‘pa
0
c i
c)
‘4 .
U i
2
150
Ii ,
lob
75
25
TiMe 3 I &Y ’
OLLEM&OLAN E&&6
200
I75
150
I2
100
15
Co/f niô./a w/q (‘i’)
o__o
.0
•
2,
0
1 ’TAL OL.L2MBe’LA
0
8
4
2
0
V I. APid g
\
-b—— *-.
+ 8 sZ U. P Z4 2832 3 40444€ 2 % 0 44 S 72 7 8o 4
1 1 I I I I I I I
6 ,9
-------
RESULTS
Figure 1 shows the mean nt.unber of eggs and total f. candida per
microcosm and the mean number of adult and juvenile mites per micro-
cosm and Table 1 the decomposition of the cotton strips In the micro-
cosm.
The results In Table 1 and Figure 1 show that with no signifi-
cant difference in average standing crop of animals, the use of the
cellulose energy source was accelerated by 8% when the system contained
predators as well as prey. The grazing action of the collembola on the
microbial population also increased the decomposition rate of the cotton
cloth (10%). but these sets of microcosms cannot be directly compared
because the collembolan population represents an addition to the stand-
ing crop bloniass of the mlcrocosnt.
CONCLUS IONS
This work provides direct evidence that Increasing the diversity
within the same physical limits Increases the flow of energy through a
system. When a trophic level is added to a system then the trophic
level below it is called upon to provide an additional energy supply
without Itself having access to more resources. To do this it increases
its own rate of energy flow implying that the faster energy flows
through a trophic level the more frequently system excesses (Wiens,
1973) became available to the next trophic level.
Under controlled conditions In the laboratory changes in the de-
composition rate of cotton strips were correlated with changes in the
soil faunal populations. This suggests that it may be valid to corre-
late changes in the decomposition rate of cellulose in the field ex-
periments with animal activity and in particular with species diversity.
LITERATURE CITED
Heal, 0.W., H.E. Jones and J.B. Whittaker. 1975. Moor House U.K. in
Structure and Function 0 f Tundra Ecosystems. Pages 295-320 in
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Latter, P.M. and G. Howson. 1977. The use of cotton strips to indicate
cellulose decomposition In the field. Pedobtologia B.
17:154—155.
Hacfadyen. A. 1963. The contribution of the microfauna to the tOtal
soil metabolism. Pages 3-17 In Doeksen, J. and J. van der
Drift (eds.). SOIl Organlsms)lorth Holland Publ. Co.
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15:175—177.
640
-------
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Wiens, JA. 1973. Pattern and process In grassland bird convnunities.
Ecol. Monogr. 43(2):237—270.
QUESTIONS and COMMENTS
A. MACFADYEN : Please will you elaborate on the nature
of the food of Folsomia ? The implication therefore is that
collembolan grazing enhances microbial metabolisrL.
J. . SPRINGETT : Folsomia is a generalized feeder in
these cultures; t ne gut usually contains amorphous material,
ngal hyphac and spores and small mineral particLes. There
were never any cotton fibers inside any of the animals we
examined.
} . EIJSACKERS : Do you have any explanation for the
stimulatory effect on cotton strip decomposition by Collembola
after adding predators?
J..A. SPRINGETP : The collembola in the cultures with
predators appeared to be much more active; at any one time
more individuals were runnir g across the agar or were actively
feeding. This increased mobility may have required sore energy.
As the mites were reyi g on the collembolan population without
decreasing significantly the standing crop of Collembola,
presumably the production of Collembola must have been stimulated.
As the cotton strip represents the energy source to the micro-
cosm an increased energy demand should result in increased
decomposition of the cotton strip.
. SNIDER : Is it possib]e that the size distribution
varied in the Colleinbola populations due to the selection of
certain sizes by the predator? Did you analyse the size dis-
tribution at the end of the experiment?
LA. SPRINGETT : We did check on the size distribution
as we had the impression that there were more large colleu boles
in the cultures without predators. There was no significant
difference in the body lengths of the populations. The larger
specimens in the predator—free cultures were a very dense white
which may have indicated a difference .n biomass or develop-
ment of fat bodies, however this was not measured.
A. MA FADYEN : Are you suggesting that the microbial
activity on the cotton strips is increased or are the Collembola
feeding directly on the cotton fabric?
J.A. SPRINGETT : Yes, I . m suggesting that feeding by
6’i1
-------
Collembola stimulates microbial activity by removing non-
active colonies, by exposing new areas of cellulose for
cr lonization and by distributinq spores across the cotton
strip. The Collembola does not appear to feed directly on
the cotton fab’ ic.
642
-------
A NEW TECHNIQUE FOR THE ANALYSIS OF THE DIGESTIVE
TRACT CONTENT IN CARABID BEETLES
G. Benest and ‘Z Massoud
Uniuers,Ir Paris 7
Fra,, ,
Musriim Nal,o,gal d I-Ijstopre Nahirelir
rrance
RESUME
Jn des problémes majeurs de lEcologie du Sol est la
determination de la place que chaque espèce occupe a
l’interieur du réseau trophique. Ce problëme se résoud par
la connaissance du régime alimentaire des espèces de
chaque niveau trophique.
Notre étude porte sur les Carabiques carnassiers
inféodês a lecosystéme forestier.
Les méthodes utilisêes jusqu ‘a present pour
determiner le régime alimentaire exact des Carabiques sont
parfois fastidieuses, et souvent peu précises. Seule
l’étude du contenu des jabots d’animaux récoltés dans la
nature peut donner l’image exacte du régime alimentaire.
flaiheureusement, pour les carnassiers, l’identification
des debris dans le tube digestif est fort difficile. La
méthode que nous proposons est basee sur la reconnaissance
de ces debris au Microscope Electronique a Balayage. La
covnparaisln du tégument et des fragments de pI’anëres
trouvés dans les jabots avec ceux d’animaux captures dans
le biotope originel des Carabiques permet la determination
precise des proies. La precision de cette méthode peut
aller jusqu’a la determination au niveau spécifique.
Ground beetles are well known predaceous Coleoptera.
In fact most of them mostly eat animal prey; and numerous
carabids are uniquely carnivorous. However, this is not
true for all of them: they also often accept feeding on
plant tissues, sometimes partially, sometimes totally.
LINDROTH observed as soon as 1949 entirely phytophagous
carabid beetles. Thus, these beetles can potentially
constitute crop pests.
Thus, there was a dilemna concerning the actual
role these animals play in an ecosysteni. Are they to be
considered as deleterious pests Or are they to be
61 3
-------
considered as effective predators and then eventually
utilised in oiological pest control? In fact, the answer
to both questions is yes, depending on the species
considered. The question thus remainlnq is to determine
‘he exa t place eaci species occupies in tie trophic
network, i.e. the diet of each species.
According to the literature, forest ground beetles
are mainly carnivorous, while phytophagous Carabids are
found in open land. This probably explains why the
bulk of the studies on Carabids diet is concerned with
field carahids. The use we can make of the animals
firstly depends cn the width of the prey spectrum. In fact,
a predator tihich s a speclalistis so dependent upon its
prey that it can hardly regulate the prey populatio’ . On
the contrary, a generalized predator, when able to switch
from one prey to another would more effectively limit
increases in population.
Most of the species 3ctually investigated show a
broad spectrum of prey. For example, SKURAVY studied the
crop content of 12 field species. She found that
Pterostichus, Harpalus, A onurn and Calathus preyed upon
at least 18 different families of Arth-opods: Arachnida,
Formico dea, Aphido Tdea, Curculionidae... Pterostichus
cupreus chose its preys among 14 of tiese different
families, while karpalus aeneus preye upon only 4. Thus,
P. cupreus has the widest spectrum of prey among the
Cirabidae SKURAVY studied. KABACfl’.-WASYLIK observed that
P. cupreus also ate eggs and dead animals. From t iese
results, P. cupreus is at the same time a scavenger, a
primary consumer, a secondary and a tertiary consumer:
a true case of generalisation. Opposite to this example
are oligophagous species of Carabidae: they exist, but
are very few in number compared to generalized species.
They have not formely been described among the forest
dwelling species.
In her work, SKURAVY did not determine the prey
from crop content more precisely than the family level;
this is true also for nearly all authors, and is due to
the method used: the technioue consists of dissecting
the digestive tract, displaying its content on micro-
slides and observing with a photonic microscope. Thus
the identification of prey is done from prey fragment.
It is thus possible only when the pieces are parts of
appendages, heads, etc, or recognizable organs. In such
a situation, it is practically impossible to recognize
at more than merely the family level.
Some authors succeeded in determining some prey
species of certain Carabids. ERNSTING demonstrated
-------
Notiophilus biguttatus preyed upon the Collembolan
Orcheselia cincta and Tomocerus minor . However these were
laLoratory experiments: ERNST NG gave previously identified
Collembola to N. biguttatus . Such observations do not
prove that thei Collembola are natural prey; they only
demonstrate the possibility. Therefore analyses of the
contents of the digestive tract are necessary on animals
captured in their habitat.
The extraction of the contents of the digestive
tract must be done from the anterior part of the tract.
Further posterior the meal will be digested and pieces
will be unrecognizable. In the case of Carabid beetles.
this means the extraction must be done when the meal is
between the mouth and the proventriculus, 1. e. in
oesophagous and crop. In fact, one can find there the most
recognizable fragments.
When dissecting, one will notice that the crops are
either full of solid items, or full of liquid items, or
sometimes empty, depending on the species dissected. Thus,
solid items are never observed for example in the Carabus
group, the crop of which, if full, only contains liquid.
This is due to its type of food uptake: extraintestinal
digestion. Up to now only one process of digestion has
been described in ground-beetles. According to this process.
three types of Carabidae are distinguishable: those with
totally intraintestinal digestion, those with exclusively
extraintestinal digestion, and those with intraintestinal
and extraintestinal digestion.
It is thus very clear that visual analyses of crop
content are hampered by extraintestinal digestion, although
it is the most generally used method. In spite of these
difficulties, the visual method for analysing crop contents
must be maintained for t least twn reasons:
1) It is te only available method providing
statistical oata;
2) the crop cortains the only available information
for the identificetion of natural prey.
In fact every prey fragment in the crop is a piece
of dietary information. However, i 1 ntill recencly, these
very small fragments could not be precisely utilized,
unless they were recognizable organs. That 15 why we have
devised a new method for the identification of natural
prey from the very small prey fragments contaiiied in the
crop. This method consists of the observation of these
fragments with a Scanning Electron Microscope.
In a full crop, numerous fragments of unidentifiable
organs are observable, which lack a particular shape, size
-------
or feature recognizable as belonging to a given prey
species. These fragments can only be identified as belon-
ging to c re or more Arthropods. At a greater magnification
the epicuticular relief is observable: setae, spines,
pores, . .. the exact shape of which is not actually
observable with another technic than S.E.M. Fig.1
show some spines which differ in size, shape and density.
The question remains to c -re1ate each type of spine to
one species of Arthropod. Is this “micromorphology”
species characteristic? It certainly is if we refer for
example to the colors of some Insects cuticule: these
specific colorings are due either to pigments or to
peculiar epicuticular microscuiptures. To prove this point
of view, we observed two species of the same genus:
Lithobius calc ratus and Lithobius forficatus . Table 1
gives a list of per inent features, I.e. those features
from which It is po3sible to distinguish L . calcaratus
from L. forficatus and vice-versa. — -
The body and appendages of th these Lithobius
are covered with a kind of scale on nearly all the surface.
1. calcaratus has rippled pseudoscales while L. forficatus
ills dotted pseudoscales. These microscuiptures are also
found on the bases of the sensilla trichodea. The
posterior hedge of the pseudoscales generally bears some
little spines: the length of which Is variab1e. The
longest spines are observed on the pseudc,scales of
L. forficatus .
TI’e surface of the setae of every sensilla,
whatever its length is, are very much alike in the two
species: they all are grooved and the grooves may twist
round the setae. It is thus remarkable how shiilar the
sensilla are all over the body and in both species, the
only difference being their bases. In fact, the tetae
bases vary a lot in shape both when comparing two setae
bases of one individual and when comparing the setae
bases of the two species. All the setae bases are
protuberant except one type which is flat: this type is
only f• und in L. forficatus . The setae bases are crescent
shaped well mai1 ed in 1. calcaratus , while more discreet
in L. forficatus ; in till latter species some bases have
the c ape of a semi—circumference and son:e others are
nearly rouno. In both species the setae bases bear
generally two big spines and often more or less numerous
little ones. Their shape, number and position vary from
a species to the other: fIg. 2; are the diagram of
the most frequently observed setae bases. In both species
the sensilla trichodea are generaly accompanied by one
or two secretory gland the pore of which are seen at
each side of their base. At last, similar sensilla
placodea are observed in both species.
646
-------
UTHOSIUS FORFICATUS
C
c e
Q
C
LrTHOSIUS CALCARAILS
1 )
FIGURE 2 “ - rations of -the form of selae bases
647
-------
FIGURE 3 L1thobIu forficatus
1 : sensj Ha trichodea;
2 : general vi€w of pseudoscales;
3 : pit on pseudoscales;
4 : sensilla placodea;
5—13 : setae bases of sensilid trir.hodea.
648
-------
-------
riGURE 4 : Lithobius calcaratus
1 sensilla trichodea;
2 : general view of pseudo scales;
3 ripple on pseu- scale3;
4 : sensilla placodea ;
5—10 : setae bases of sensilla trichodea.
650
-------
651
-------
To summarize this comparison, it appears clearly
some similarities in both Lithobius : sensilla placodea,
setae, pseudoscales; those similarities correspond to the
fact both forficatus and calcaratus belong to the genus
Lithobius . However there exist some differences, the
structure of the pseudoscales and the structure of the
setae bases. Those differences, observable only with a
S.E.M., are enough to distinguish one species from the
other, even from very small pieces.( Fig. 3 and Fig. 4)
to conclude we shall just ask one question: why
has this micromorphology never been used up to now by
systematicians? The reason was probably there was no
interesting aim. Which new information would this
micromorphology afford? None if we only are soil zoologist.
But if we are soil ecologist, we have n w an attractive
aim: the analysis of crop content of naturally captured
predators.
REFERENCES
The only review on nutrition of Carabids is that of
LU. THIELE: Carabid beetles in their environments,
Zool. Ecol. 10, pp. 369 (1977).
AC}CNOWLEDGMENTS
We would like to thank Mrs. Munoz and Mrs. Vannier
and Mtss Munsch for typing and preparing the figures.
TABLE 1 . Caracteristic features of specit. r f Lithobius
UTHO i CALCARAT Umoetus FORACATuS
I — ‘ cs
s
I
,t
p it
.
5s Hb ( —
5l ih4... lb...
v _v.
(,fpp
Oor2tontlp.
O r2u,
I. P°’
rr
pit
Oor2tIv.m_v .,
isis d tt
O 2gIa .b,
. .
;-_-
,‘s
I . .
652
-------
THE GEOPHAGOUS EARTHWORMS COMMUNITY IN THE
LAMTO SAVANNA (IVORY COAST): NICHE PARTITIONING
AND UTILIZATION OF SOIL NUTRITIVE RESOURCES
‘Patrick Lavelle, “Boubacar Sow and “Roger Schaefer
Erok Normale SupFr,eurr SInIiou dEoThgii Tropsn,le de Larnio • Uun’ers,t de Parts XI
France Ic’orv Coact Fra n
The few descriptions of earthworm communities available from
tropicril. grasslands clearly show dominance of the g ophagous species.
This has particularly been verified in the tropical pastures of Lagu—
na Verde (Vera Cruz, riexico) (LAVELLE, MAURY and SERRANO, 1979), in the
north Guinean savannas of Foro-Foro (Bouak , Ivory Coast) (LAVELLE, un-
published) and in the south Guinean ones of Lamto (Toumodi, Ivory Coast)
(LAVELLE,, 1978) ( Table 1). In the first locality, almost the entire
community is cc’mmose 1 of geophagous ear hwotms. In thi.. . Lan.t.o avannas,
the herbaceous facies are also stocked with a great majority of gee —
phagous (97%) whereas the shrub facies (89.27k) and the savanna which
has been unburned for 12 years (69.7 ) which has a thick shrub cover,
have morc diversified communities. At the Fore—Fore station, 230 km
iiorth of Lamto, the savanna is rather thickly covered with shrubs and
77.8 to 88.I of the earthworm biomass is made of geophagous mdlvi —
duals. On the contrary, temperate gras5londs stocked whith Lumbricidac
have few geophagous worms : 13. 1% or the total biomass in e French pas-
ture (BOUCHE, 1975).
TABLE 1. Tropb .ic structure oZ some earthworm ccmm’:nities in
tropical and temperate grasslands (in Z of total biomass).
Locality
Vegetation type
Geopha—
geous
Detriti--
vorou
Aut rs
Laguna Verde
(Vera Cr z,
liexico)
Secondary pasture
100
c
LAVELLE, MAURY
and SERRANO,
1979
Foro Foro
(Bouaké,
Ivory Coast)
-
North I
guinean I
savannas
Parenox
savanna
.
Lophz.ra
savanna
88.1
77.8
11.9
22.2
LAYELLE,
unpublished
Lamto
(Thumodi,
Ivory Coast)
South
guiaea
savannas
grass
savanna
shrub
savanna
unburned
savanna
(12 years)
97.0
89.2
69.7
3.0
10.8
30.3
LAVELLE, 1978
Cit e aux
(Dijon,
France)
Permanent pasture
13.1
86.1
BOUCIth, 1975
65
-------
This dominance of geophagous populations seems to be a general
characteristic of tropical grasslands. It is, therefore, important to
know their community structure and how they feed on the soil, in order
to understand theix general function. Four years of field observations
in the Lamto savanna and laboratory experiments focus on this question.
NICHE PARTITIONING IN THE EARTHWORM
COMMUNITIES OF TilE LAMTO SAVANNAS
The earthworm communities of Larato savannas are made up of eight
principal species ; six are Megascolecidae : Dichogaster agilis, D.
terrae—nigrae; Mil1. so;iia anomala, 14 lointoiana, i. ghanenoie and Agae—
tr ’odiZua opisth. gynus ; the two others are Eudrilidae Chuniodrilus
z eZae and Stuhirnannia porifera.
Their eccil,gical n cher can be defined with sx principal va-
riables. Three of them describe the spatiotemporal niche : vertical dis-
tribution of populations in the soil, horizontal distrib ition in the mo-
saic drawn up by the different vegetal fades (herbaceous or shrub savan—
nas, burnt or unburnt patches) and the seasonal cycle of abundance (Fig.1).
The three otheT variables represent the trophic dimensioi. of the niches :
species size, demogr;Apriic profile, and energetic value of ingested food
(Table 2).
TABLE 2. Trc phic niche of the different species of earthworms
in the Lainto savannas.
Species
Maximal
weight
(5)
Vood
Energetic
value of food
in Kcal/g
Demo—
graphic
index
0. agilia
M. laintoiana
M. anornala
v. terrae—nigr’ae
Eudrilidae
14. ghanensis
A. c’pisthogynus
0.60
32.0
6.0
28.0
0.25
16.0
4.0
litter
litter
soil (0—10cm)
soil. (10—30 cm)
soil (0-30 cm)
soil (10—40 cm)
soil (20—40 cm)
+ Eudrilidae ?
4,000
4,000
90
50
150
40
?
200
17
50
4.5
200
2.9
4.9
The index (D 10 c ) combines different elements of the de-
mographic profiles : adult fecundity (F), duration of the growth period
until maximum weight (C), and life expectancy of young hatchling (E)
(LAVELLE, 1979).
Spatiotemporal niche overlap has been estini ted with the Ojk
index of PIANKA (1974) along each of these previously wdntioned three
axes (Table 3).
Seasonal cycles have high overlap ratios (0.72 to 0.95 with a
mean value of 0.90). Thus, niche separation is mainly realized through
the colonization of different savanna fades (Ojk = 0.13 to 0.96 ;
6 5l+
-------
FtGURE !. M iri ‘:onstituants of the Lamto’s earthworms spatiotempor 1 niches.
G — grass suvanna, S — shrub savanna, US — unburned.
Ou$h
(c i i i)
I-
a.
.noma
a
Vsrlicsl distiibuftoa
%0
a. i:icts,
so
o S
a. I
as I
S
F-
r’ 1 , 5cm
Hov somtal dlstribullsii
6 $ US %annsi&’
Ssaasnai cFIs
60.
*
PIAIJ
Reproduced
50 .
Is.
20 .
i:2$cm
S
MNS. .J*
isasa.is
is cm
655
-------
03k 0.7(1) and the occupation o the diverse layers of the. soil
(03k. = 0.06 to 0.93 ; 03k = 0.47).
TAbLE 3. Spatiotemporal niche overlap (Ojk index) hi the earth—
worms communities o Lamto savannas (D.a. : Dichogaster agil s ; M 1.
l.filioonia lcrjntoiana ; M.a. : Millcor a cmomala ; D.t. : D. terxae—
ai )r’a . ; Eu. : E riUdae ; C.z. (Yliuniodritzw z elae ; S.p. Stuhi—
mannia porifera ; A.o. : Agaatrodrilus opiethogynus ; M. g. 14. gha-
nencis).
A. Vertical distribution
N.l. 0.93
L1.a. 0.91 0.96
D.t. 0.1] 0.44 0.49
Eu. 0.38 0.48 0.62 0.57
A.o. 0.08 0.10 0.2 0.33 0.91
M.g. 0.02 0.05 Ci.24 0.29 0.77
D.a. La. D.t. A.o.
- B. Horizontal distribution
M.l. 0.95
Ma. 0.73 0.89
D.t. 0.13 0.55 0.74
C.z. 0.94 0.53 0.79 0.75
S.p. 0.54 0.95 0.82 0.47 0.41
A.o. 0.76 0.56 0.97 0.71 0.72 0.92
M.g. 0.64 0.37 0.89 0.55 0.53 0.95 0.96
D.a. M.l. }1.a. D.t. C.z. S.p. A.o.
C. Seasonal cycle
M.l. 0.80
M.a. 0.94 0.91
D.t. (3.84 0.92 0.95
Eu. 0.93 0.87 0.93 0.94
Ac. 0.82 0.91 0.92 0.99 0.95
M.g. 0.80 0.89 0.91 0.94 0.87
D.a. M.l. N.a. D.t. Eu. A.o.
A matrix of results has been established after multiplication of
the calculated values as th threc variables seem to be independent
(PIANKA, op. cit.) (Table 4).
6 6
-------
TABLE L Total spatiotemporal niche overlap.
M.l. 0.71
La. 0.62 0.65
D.t. 0.01 0.21 0.34
C.z. 0.33 0.40 0.46 0.40
S.p. 0.19 0.11 0.47 0.25 0.41
A.o. 0)4 0.05 0.24 0.23 0.62 C.79
M.g. 0.01 0.02 0.18 0.15 0.36 0.64
D.a. N.l. La. D.t. - C.z. S.p. A..o.
Tiough the total spatiotemporal niche overlap (Ojk 0.01 to
0.80 ; Ojk = 0.35) is low among most of the species, a good ecological
separation is evidently indicated. Two groups of species however appear
ratht’r close in this spatiotemporal space (Fig. 1). D. agiZis, M. 1-am —
toiana and )‘ . anomala inhabit the upper layers and ?refer burnt or un—
burnt shrub savannas. On the other hand, A. opt.sthogynua., N. ghanensis
and the E drilidae (C.z elae and S. porifera) re deep soil dwellers,
characteristic of the open savannas.
Nevertheless, the exariination of trophic niches shows that those
species whose spatiotemporal niches are similar are in fact distinctive
in that they exploit their resource in different manners. The distribu-
tion of species in the trophic space has been figured using orthogonal
axes —as it is easier to represent— despite the fact chat the variables
are certainly more or less linked (LAVELLE, 1979)(Fig. 2).
Detritivorous sçeciee are clearly separated from the others be —
cause of the high caloric value of the litter that they ingest. D. agilia
is small with a high demographic index. M. lwntoiana is large and its po-
pulations turn over is not so high. Among the geophagous species, mall
one are distinctive in that they feed on relatively rich soil and have
a high demographic index (the two Eudrilidae : C. zielae and S. poz’ifcra);
there are also two large species with a low demographic index and poor
food (V. terrac—nigra.: and N. ghanenuie) and an ntermediate one, M. a.no—
mala. A. opiethogynua, whose exact diet is not known, has not been figured
here. Some recent indications could show that this species is partly car-
nivorous and feeds on Eudr5lidae.
After combining the two niche spaces, the separation is clearly
the consequence of rather high specialization. This pe:mits the five main
geophagous species to exploit well—separated compartments of the ecosystEm.
Vertical distribution makes great differences M. anomala exploits the up-
per layers of the soil, unlike N. ghanenais and V. terrae—nigrae which
are deep dwelling species. It is difficult to study individu .. ly the ver —
tical distribution of the two species of Eudrilidae as the young cannot be
distinguished. Nevertheless, some indications show that C. zielae is more
limited to upper scrata, as is N. anorr ala whereas S.porifera could be a
deep dwelling worm.
65?
-------
FICU E 2. Representation of Lamto’s earthworms trophic niches. Wx maximum
weight of the species ; D : domographic index (F : adult fecundity. ( Pntal
length in months of growth period until maxii wm weight, E : life expectancy
of young a birth in months) Q: energetic value of the ingested food in
kcal/g dry weight).
W* ( O
D.t.n.
10.
1,
M i
D.a.
I
D:10 3 -
6j8
-------
Pl(WRE 3. Representation of Lc mto’s earthworms spatioteuLporal niche overlap
coefficients (Pianka’s 03k) in the space of the three principal axes.
659
Horizontal distribution
-------
M. anorn2la and the eudrilid C. zielae differ in size, and,
therefore, they exploit the environment in different manners ; the
first one, a quite large species, demonstrates no preference for the
organic content of the soil, while the second, thanks to its small
size, ingests only soil enriched in organic matter. Indeed Eudri—
lidac can more easily feed on low organic matter concentrations (de-
composed rootlets and surface organic film), and they do not ingest
the large sandy particles. The composition of casts of these two ta—
xa demonstrates this difference and confirm the r.enezncy of M. anoma—
la to be generalists while Eudrilid e appear more specialized, using
the soil in a “coarse grained manutv” (Table 5).
TABLE 5. Granulometric composition and main characteristics of
organic matter in casts of M. anomala and Eudrilidae and control soil
in a herbaceous savanna.
Contrul soil
(0—40 .a)
Eudrilidse
Clay < 2 j
Fine silt 2—20 i
Coarse silt 20—50 .i
Fine sand 50—200 .i
3.3—3.7
5.7—6.5
7.5—8.5
25.5—29.0
5.0
7.3
12.0
40.0
5.2
8.6
11.5
27.0
Coarse sand 200—2,000 1
c 0/00
N C l
C/N
Organic matter
50.5—56.5
1.9—8.2
0.17—0.57
10.8—15.3
0.6—1.4
32.0
10.1
0.76
13.3
1.7
- 46.5
5.8
0.57
10.2
1.0
The two large geophagous species M. ghanen ia and D. terrae—
n4,v’ae have close trophic niches ; the separation is made by a dif-
ferent vertical distribution ar4 the colonization of different patches
of savanna : N. ghanenszc prefers the sandy soils of herbaceous savan—
nas whereas D. terrae—nigrae is more likely to be found in the more c Ia—
yey and better drained soilu of the burnt shrub fades.
The structure of these communities raises two questions that we
have tried to answer.
1. I .. the vertical distribt.tion of these species a consequence
cf the present competitive situation or of real adaptation, including for
the deep dwelling geophagous whose food seems very poor ?
2. How do these earthworms utilize the organic matter contained
in the soil ?
660
re
Mfllsoni a
anomaia
-------
RELATIONS OF SOIL DEPTH WITh INGESTION
AND GROWTH RATES OF GEOPHAGOUS EARTHWORMS
In order to answer the first question, we have fed individuals
of the three main spRcies CM. cozornala young and adults, young 14. gha—
nenai.a and D. terrae—nigrae) with soil taken from the different soil
layers of a shrub savanna. Five layers have been distinguished, whose
main characteristics appear in Table 6.
TABLE 6. Main characteristics of organic matter in the different.
strata of the shrub savanna soil used fox earthworm cultures.
Depth. (cm) 0—1 2—5 5—10 10—25 30—40
I

o

Organic carbon
Total nigrogen faa
C/N ra.io
Total organic matt tr 0/00
11.8
0.58
20.40
20.4
9.8
0.50
19.
16.8
8.3
0.40
20.8
14.3
7.0
0.30
23.3
12.0
4.1
0.30
13.6
7.0
00 1 .J

o
c °f
N
C/N
0.29
26.7
7.4
3.6
0.22
36.7
5.6
6.6
0.24
42.2
4.6
9.3
0.10
41.6
3.6
11.7
0.15
29.6
3.8
7.9
ue
•.-i.u
.1
,j
Toyal fulyic acids Un C 0/)
Total humic acids (in C 0/)
2.53
0.61
1.91
0.74
.1.57
0.74
1.54
0.43
1.36
0.16
AF/All 4.18 2.58 2.12 3.69 8.25
Total btunic matter 3.14 2.65 2.31 2.02 1.53
Ilustification coefficient 26.5 27.] 27.8 29.0 37.5
Soils characteristics
Most of the data shows a vertical gradient of the otganic matter
characteristics in the soil. The highest values of total organic matter
content as well as total introgen, light organic fraction or total humic
acids are observed in the 0—1 cm layer, decreasing more or less regularly
towards depth. Total fulvic acid follow the same pattern whereas humic
acids are more concent d in the 2—10 stratum. C/N ‘atios of total orga-
nic matter show erracic va.iati ns, but as far elS the light organic frac —
tion is concerned, C/N incr .ases regularly with depth. Tb AF/AW ratio
shows rather different variations with minimum values between 2 and 10 cm.
Methods
The s.•il ingestion by earthworms has been measured by a method
already utilized in several works (LAVELLE, DOUHALEL and SOW, 1974
LAVELLE, 1975) and subsequent weight variations were observed. All con-
ditions we’e alike in the different cultures except for the soil origin.
As many earthworms as possible have been put in cultures in order to ha-
ve significant results. As a matter of fact, the growth of these earth—
worms does not follow a regular pattern. In the normal course of the ani—
IT al’s life, very intense growth periods occur followed by rest periods
661
-------
characterized by a no growth or even a littic decrease of the weight
due to a decrease of soil inges:ion L.AVELLE, 1978). According to these
observations, the total duration of cultures (140 to 700 worms x days in
each different series) should give significant means in most of the ca —
ses despite the fact it has not been possible to establish any statisti—
cal proof.
Results
Table 7 illustrated by figure 4 gives tim main results, the detail
of hich will be given in a rurther publication (SOW, to be published).
TABL.E 7. Mean daily weight ya Lations (&W /day) and relatiye
soil. ingestion (C(l in g dry soil 5nge.sted/g fre.sK weight/day) of
three geophageous species fed with soils from different layers.
Species
I
Tot l, du-
ration of
cultures
(worm x
weeks)
Soil
layer
(cm)
W fd
C(W
M4 /d
Young
M. anornala
I
100
100
100
100
100
0—1
2—5
5—IC
10—25
30—40
2.79
2.32
3.26
1.65
0.34
17.3
18.0
17.3
15.1
6.1
0.161
0.129
0.189
0.110
0.055
dult
M. anomala
30
20
20
20
20
0—1
2—5
5—10
10—25
30—40
—0.31
1.17
0.11
—1.24
—0.86
5.66
6.81
6.07
5.53
3.95
—0.055
0.172
0.018
—0.224
—0.218
Young
M. ghanensi8
64
66
32
64
81
0—1
2—5
5—10
10—25
30—40
0.09
0.22
0.22
0.45
0.23
5.03
5.62
4.21
5.98
6.67
0.018
0.039
0.052
0.075
0.034
Young
D. terrae—nigrae
74
67
76
49
65
0—1
2—5
5—10
10—25
30—40
—0.01
0.16
—0.17
0.38
0.02
4.16
5.62
5.34
7.17
6.35
—0.0024
0.028
—0.032
0.053
0.003
This demonstrates important Jariations in relative soil ingestion
(dry weight of daily ingested soil divided by the earthworm ‘a fresh weight)
as well as in the animal weight changes as a function of soil depth.
— Young N. anomala have the highest relative soil ingestion
(C/ 17 to 18 g dry soul 8 fresh weight/day) in the upper strata (0 to
662
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FIGURE 4. Mean relative soil ingestion (C/W in g dry soilIg fresh weightfday)
and daily weight variations (%/day) of three species of geophageous earthworms
fed with soil taken from diE fercnt depths in a shrub savanna.
relative daily msan
consumption weight
AW%/d
012.5
..— .- ... — — —
young
N. ano.Tla Ia
‘.4
C l
S. 2
a.
4. 1
adults
M.anosnala
0.1 2.5 5.10
—
I
— — — — —
—
10.23
2
stratum
young
O.t.Tra-nlgrae 8.
6L
4.
2.
young
N.ghanensia
OAO
1 •• • ’
0,20
/
.
(cm)
10.2$ 3o 4o
663
-------
ID cm) but it decreases in the deeper layers, first slightly (15.1 in
the 30—25 cr layer)then m irkedl (6.1 in the 30—40 cm soil).. Weight
‘ariations are always positive ; they are elevated in the first three
layers (2.3 to 3.3%/day), and the maximum is oL’served in the 5 to 10 cm
stratum. In the deeper soils, poorer in organic matter, growth diznini —
sties greatly but is never reduced to zero.
Within the same experimental conditionq, ddult M. ancnnala have
a clear preference for the 2 to 5 cm horizon as this is the only one
that allows then a significant increase in weight ( WZ/dav = 1.17).
En the 5—10 cm soil their growth is very slow (0.I1 day) and in the
other ones, they lose weight (—0.31% in the 0—1 cm stratum, —1.24% and
—0.86% respectively in the 10—25 and 30—40 strata). Soil ingestion fol-
lows similar variations , though it is somewhat decreased. It is maxi —
mal in the 2—5 cm soil (6.8) and diminishes regularly towards deeper
horizons (6.1, 5.5 and 4.0 in the successive strata from 5 to 40 cm) as
well as in superfical ones (5.7 in the 0—1 cm soil).
These results confirm the narrowing of fcologic3l tolerances of
adults with respect to environmental factors such ‘r. temperature and
soil moisture (LAVELLE, OOUHALEI and sow, 1974 ; L bELLE, 1975).
Cultures of young N. ghanenoi8 give very different results.
Weight variations are positive in all of the soils, but they are maxi-
mum with the 10—25 cm earth (0.45%/day) while they decrease gradually
in the more superficial (0 22 to 0.09%/day) ones. Soil from the 30 —
40 co stratum still permits an increase of weight, but it is less si —
gnificant (0.23%/day). Relative soil ingestion does not vary much, al—
L 1ough it seems to increase regularly with depth.
Young D. terrc e—nigrae show rather simila - patterns. interes—
.ingly, it is the 10—25 cm stratum that . nsures the fastest and moat
regular growth. It is erratic, in the upper strata, and mortality is
elevated. We often observe first a period of fast growth, followed by
an equally rapid decrease that leads to death. Those soils richer in
o:ganic matter allow a quick but temporary growth as if some deficien-
cy disease could appear. On the contrary, in the 10—25 stratum, growth
is slow, but regular, and the mortality rate is low. Soil from the 30—
40 stratum just allows earthworms to maintain their weight, ant the
mortality rate is rath elevated. Relative soil ingestion shows varia--
tions similar to M. ghanensCa as it increases slowly when given soils
from deeper strata.
Conclusions
Weight variatiou of worms of the three studied species are de-
pendent on the soil they ingest. The optimum depth is 2 to 5 cm for
adult U. anomala, 5 to 10 for the immature and 10 to 25 for young M. gha—
nensia and D. ter’rae—nigrae.It can be concluded that these two last ape —
cies are truly adaptated to the ingestion of soil from the dcep strata
that they use to colonize, while M. anomala has a better growth in the up-
per strata where it is more likely to be found. Therefore, the vertical
distribution of the populations does not seem to be a consequence of a
present competition for spare and food, but rather the result of particu-
lar adaptations.
66
-------
Relative soil inge’ition appears to be regulated according to the
soil depth ; it decreases with depth as far as it concecnes 14. a,wmala
and increases for thi two other species. The mechanisms of this apparent
regulation do not seem to be sinipJe.
On the other hand, growth rate and growth efficiency (of which
the ratio t W7.Iday gives an idea), are never proportional to the orgavüc
C/W
matter content of the soil that decreases regularly with depth. It £‘
thcrcfore to be expected that it is the quality of organic matter and/or
the microbial activity of the soil that determines its digestibility by
earthworms. Experiments have been designed to test these two last hypo-
theses with young M.anornaia.
VARIATTONS OF SOiL TNCESTION AND GROWTH RATES OF lP 1ATURE
M. AP/OM.IL.4 BRED IN SOIL ENRICHED WITH DIFFERENT VECETAL COMPOSTS
Global data from Table 6 are too coarse to explain the results
described in the previous paragraph. However, this organic matter seems
to be much too diluted to allow more precise chemical analysis. In order
to overcome this difficulty, we have added to a control soil (from
the stratum 10—25 cm of a shrub savanna) diverse vegetal compost
which is easier to analyze.
Methods
— Compost was made ot pulverised roots or leaves of the graminea
Loudatia sinrplex decomposed in aerobic or anaerobic conditions during 0,
2, 5 or 10 weeks. Fifteen series of cultures were undertaken : one control
was whithout compost and fourteen were enriched with 1% of each of the pre-
pared po’ ders. Each series was composed of two cultures of five young
M. anonp2la. The experiment lasted 10 weeks so that the total lenght of each
series was 700 worms x days.
Results
In all of the series, the growth rate was higher than in the con-
trol. The grass aerobic composts gave the best results, but the other se-
ries give similar figures with smaller amplitudes (Table 8).
t WZ/day
Mean growth efficiency (E = — ) is 107 tn tne control,
C/W
5O in the aerobic root, 155 in the anaerobic root, 236 in the anaerobic
leaf and 355 in the aerobic leaf compc,sts.
One percent of leaf wder added to control soil permits the dou-
bling of mean daily growth rate that raises from 1.93Z to 4. 14Z (Fig. 5).
The best growth is observed with the two weeks earobic cOmpO3t (LA 2 ) 4.26Z.
Then it decreases with more decomposed substrata 3.86Z with LA 5 and 2.31R
with LA 1 . The soil ingestion urve is exactly opposite. Ingestion is maxi-
mum in £tie control soil (C/us. IBg dry soil/g fresh weight), decreasing with
leaf powder L (10.7), aud is minimum with compost LA 2 (7.7). It increases
wit.h LA 5 (12.2) and LA 10 (12.4), remaining, however, inferior to control
value.
665
-------
____________ — —
EC,L
1W
600
500
400 15
300
200 10.
100
0 5
C-
i 0 L 2 A
a
L5A
growth
rate
âw9Sfd
mean relative
soil ingestion
ejw
( E= AW%/clay io )
LiSA
FIGURE 5. Mean growth rates, relative ingestion and growth efficiency of
young M. wiomaZa fed with soil from the 10—25 cm laynr of a shrub savanna (C)
enriched with different pulverized grassleaf aerobic composts (La : grassleaf,
L A 2 : two weeks aerobic. compost, LA 5 five weeks...).
204
3
2
growth
efficiency
666
-------
TABLE 8. Global, results of young M. anornaZ .a cultures in control
soil (T) enricbe4 with. different vegeta]. composts (1.. leaf, R roots;
A : aerobic, N : anaerobic ; 2, 5, 10: time of decoiiiposition).
ttW fday : mean daily growth rate ; CfW : mean relative soil ingestion ;
E = 0 ’ &WZ/day growth efficiency rate.
c/W _____ _____
Serie
AW %/d
C/W
E
T
:.93
18.0
101
Leaf
Aerobic
LD
4.14
10.7
368
2
L.A 5
LAiO
4.2b
3.86
2.31
7.6
12.2
12.4
564
316
186
Anaerobic
LN 2
LN5
Lt 10
3.60
3.39
1.99
10.5
15.0
13.7
338
226
145
RooL .
Aerobic
R 0
2.33
13.0
210
RA 2
kA
PJt 10
3.06
2.73
1.45
14.4
20.2
14.4
213
135
101
Anaerobic
RN 2
RN 5
RN 10
2.75
2.77
2.03
15.5
le.ó
14.6
178
149
139
We have tried to find a relationship lietween the composition of the
added powders and the culture data. With this purpose, the energetic value
of the different glucidic fractions (hydrosoluble fractions extracted be —
fore and after lipid extraction and hemicellulosis) have been evaluated by
measuring their reducing power. The separation of these different consti —
tuenv has been made accordi tg to methods described by JARBICE (1961), and
the reduction potential measured by the HAGEDORN and JENSEN micrometliod.
Lipid content has also been measured.
The progressive humification of grassleaf powder is followed by a
clear decrease of the energetic value of hydrosoluble fractions and lipids,
whereas hemicellulosis increases (Table 9). All things considered, the ad-
dition of 17. of these powders do not even double, in the best case, the
global nutritive value of the ingested soil. On the other hand, the varia—
The growth efficiency rate (E) is minimal in the control (E 107),
reaching 261 with L 0 , and culminating with LA (457). It then diminishes
in mire humified composts : 316 with LA 5 and 86 with
Consequently, the growth of young H. anomaia is not proportional
to the organic matter content of the ingested soil, but it seems to be clo-
sely dependent on its composition. On the other hand, the quantity of inges-
ted soil shows great variations : when the medium is highly nutritive, it
can decrease, reaching less than 50% of control value.
667
-------
tions observed show a rcgular decrease of the soluble energetic fraction
while the less digestible hemicellulosis increases.
TABLE 9. Energetic values of the different glucidic fractions
(in mg equivalent glucose per g) and lipid content (in mg/g) of the grass—
leaf aerobic comoosts and control soil.
Hydros luble Ltp d iLydrosoluble Heinicellulosis
fraction I fraction 2
T
0.35
0.05
e
2.1
L 0
24.7
6.3
2.9
13.3
LA 2
LA 5
LAID
9.0
7.4
6.9
4.6
3.6
3.4
2.3
1.4
1.0
14.0
15.0
16.1
These results dc not explain the variations of growth rate and
esp:cially of growth efficiency that culminate in the cultures enriched
with compost LA 2 (two weeks of aerobic decomposition).
This means that more precise analyses should be perform- d in or-
der to identify the exact composi ion of the energetic fraction we mea —
sured. An cther hypothesis could be that these relations are ixpla ed
by earthworm—microorganise interrelations, as it is usually mentioned
that humivorous animals cculd feed on microorganisms. In order to test
this hypothesis, we have performed some experiments.
PRELIMINARY STUDY OF MICR00RGANI5M—EARTHW0R 1 INTERRELATIONS
First, we have tried to ascertain if a relation could be esta —
bushed between microbial. activity of the ingested soil and earthworm
growth. If demonstrated, it could indicate that the earthworm feeds on
microorganims or utilizes the product of their metabolism.
Thus we have measured re piration of soils during one week (that
is the interval between two changes of the soil in culture). The method
used is a macrorespirometric one (Stokiasa) ; CO 2 is extracted by depres-
sion and titrated by a system of Barium hydroxyde—oxalic acid (RASRID and
SCHAEFER , 1978). The analyzed substratum is pulverized while dry, then
moistened and homogenized by repeated stirring, so that the measured res-
piration is accurate and repeatable. Figure 6 A illustrates the experimen-
tal data.
Respiration rate is lowest in the control soil, highest in the soil
enriched with 1% undecomposed grassleaf, an’i ic decreases progressively with
the gradual humification of grassleaf powder. It remains, however, superior
to the c r trol value. The microbial activity seems to bn highly stimulated
by a substratum rich in easily assimilated energetic elements (the
grassleaf), and it decreases prog’ essively when the grassloaf ge more huizi—
fied ant the soluble fraction less important.
668
-------
30—
mg
C (CD 2 )
I lOOg
dry soil 40
FICURE 6. ¶.eekly respiratinn of control soil (C) enriched uith I Z of the
different grassleaf aerobic composts (A) and saae experiment (B) after repla-
cing control soil by casts of young M. cowma2c (T) fed with the control soil.
669
30-
20-
A
B
- I
— I
-------
The same experiment has been done after having replaced the
control soil, by the casts of young IlL anoma7 a fed on this soil. The
casts respire much more than the control as the microbial activity
3.5 almost doubled (16 to 29 mg. C (C0 2 )/IOC g dry soil). It is ii-
keJy that mucus produced by earthworms has a stimulating effect ;
the u chanical action produced by earthworms is also responsible for
this stimulation as it induces movement of substrata and a niodifi —
cation of microorganism associations. In return, addition of , rass—
leaf and composts powders co the casts gives respiration patterns
inferior to the previous ones. With grassleaf (Le) the decrease is
lo c (55 to 47 mg. C (C0 2 )/IO0 g dry soil). It is, however, most im —
po cant with two—weeks—old leaf compost (LA 2 ) (35 to 15) which gives
the lowest respiration rete, and more humLfied compostsLA 5 (29 to
16) and LA 10 (28 to 26), whose respiration is still inferior to the
cast.
It seems, therefore, that an explenation to the 14. anomala
growth variations ouli be d ri ed from these results. The earthworm
could produce in its casts a substance that inhibits the aetivity of
mi.croorganisms in lightly humif led substrata. This inhibition would
not be apparant with added grassleaf powder. Its soluble energetic
fraction is important enough to avoid competition between microorga-
nisms and the earthworm. The inhibitory effect could be maximum with
the two weeks compost and diminishes with more humif led substrata.
It would reverse in control soil because the organic matter is highly
humified. Such results can be expected if we suppose that earthvormc
do not feed on soil microorganisms but rather can in certain condi —
tions be in competition with them for the exploitation of the most
digestible energetic substrata. When given a riche food (Lu), the in-
hibition i.s low because there is no competition. With a more humifi d
substratum less rich in soluble energetic substances (LA 2 ), competition
becomes maximal. The effect is reversed when the humification process
is more advanced ; competition turns to symbiosis as earthworms try
to utilize energetic substances produced by microorganisms from more
complex substrata (hemicellulosis, cellulosis) that they cannot alone
digest. In the control soil poor in hydrosoluble elements, the micro-
bial activity is then clearly favoured.
CONCLUSIONS
These preliminary results indicate that geophagous earthworm
nutrition from soil organic matter depends on m ey complex factors. It is
clear that abundance of organic matter and, above all, its composition play
an important role ; nevertheless it is perhaps more understanding the in —
teractions of each species with the soil microflora that will explain the
particular adaptation which make possible Lhe wide functional diversity of
the geophagous community.
AC NOWLEDG1 HENTS
We are greatly indebted to Roger VUATTOUX Director of the Lainto
Ecological Research Station for his help in the resolution of many material
problems and to Spyros NOLFETAS and Donald SCHIJERT f or the revision of the
text.
670
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LUERATURE CITED
BOUCHE, M.B., 3975. Fonctions des Lombriciens. III. Premieres estima-
tions quantitatives des stations françaises du FBI. 1° Colloque de la
Soci cé d’Ecologie, mai 1973. Rev. Ecol. Biol. Sol, 12 (3), 25—44.
JARRIGE, R., 1961. Analyse des constituants glucidiques des plantes
fourragéres. I. Fractionneinc’it des con.sLituants de la membrane par les
hy 1 icolyses icides. Ann. Bio. anim. Bior”. Biophys., 1 (2), 163—212.
LAVELLE, P., 1975. Consomma&ion annuel].e de tarre par une population
naturelle de Vers de terre (Millaonia anomizia Otnode3, Acanthodr,2idae)
d.rns Ia savane de Lamto (C6te d’Ivoire). Rev. Ec ,l. Biol. Sol, 12 (1)
I 1—24.
LAVELLE, P., 1978. Les Vets de terre de la savane de Lamto (C6te d’I—
virc) pe 1 .plcments, opulaticns ct fonctions dans l’écosyst ne.
These Doctorat, Paris VI. Publ. Labo. Zool. K.N.S., 12, 301 p.
LAVELLE, P., 1979. Relations entre types éc’alogiques et profils d&uo—
graphiques ch2z les Vers de terre de la savane do Lamto (C6te d’Ivoire).
Rev. Ecol. Biol. Sol, 16 (1), 85—101.
LAVELLE, P., DOUHALEI, N. and SOW, B., 1974. Influence de l’humiditë du
sol sur la consonunation et la croissance de MiUson a anorirala (Oligo—
ches—Acwitlzodrilidae) dans la savane de Lamto (C8te d’ Ivoire). Ann.
Univ. Abidjan, B, 7 (1), 305—314.
LAVELLE, P., MAURYJ N.E. and SERRANO, V., 1979. Estudio cuantitativo de
la fauna del suelto en Ia region de Laguna Verde (Vera Cruz, Mexico).
Epoca de iluvias. Inst. Ecol. Pubi., 6, at press.
PLANKA, E.R., 1974. Niche overlap and diffuse competition. Prpc. Nati.
Acad. Sci. USA, 71 (5), 2141—2145.
RASRID, G.H.. and SCHAEFER, R.. 1978. Observations sur l’interdêpandance,
dans sa vari6té saisonniCre, en re l’économie des ressources énergêti—
ques et les activit s inicrobiennes dans une chatna topographique de
sols. 103° Congr. national des Sociët€s savantes, Nancy, 1978. sciences
(IV), 243—256.
QUESTIONS and COMMENTS
C. ANDERSEN : Was there any difference in soil consump-
tion between the investigated species?
Was there any difference tn the gut anatomy of the super-
ficial living species contrary to the deep living species?
P. LAVELLE : These differences are discus3ed in the text.
The gross anatomy as studied for systematic purposes
did not show differences in the shape and sise of typhiosoles.
It was although demonstrated that the deep dwelling species
are relatively longer than “surface” dwelling and have a
longer gut (LAVELLE, 1973. Peupleinents et production des
vera de terre dana lea savanes de Lainto (Cote d’Ivoire]
Ann. Univ. Abidjan, E, VI [ 2] : 79—98.
671
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HILL : I think that successional changes in micro-
flora should be taken into account before concluding that
earthworms are not deriving nutrients direccly or indirecti;
from decomposer microorganisms. Your results could simply
mean that the “initial” and “late” stage microflora in the
succession are less attractive to earthworms than those in
the “mid” stage.
P. LAVELLE : These earthworms eat the soil as it is, so
it is impossible for them to select certain microorganisms
for their feeding. We also think that the microorganisms
that d”elop in the early stages of decomposition feed mostly
on simple and very digestible substrates. So the products
of their metabolism are expected to be more complex and thus
less digestible for the worm.
G. BENGTSSON : You evidently have difficulties proving
any positive correlation between growth rate of the animals
and the concentration of less digestible organic compounds
in the soils. Why did you make these analyses in preference
for analyses on more digestible compounds such as amino acids.
simple carbohydrates and fatty acids and on the enzymatic
activity, which should represent part of the microbial activity.
P. LAVELLE I have in fact measured these digestible
compounds as I think that simple carbohydrates. amino and
fatty acids are contained in the two hydrosoluble fractions
we extracted. As far as microbial activity is concerned we
preferred, ir this preliminary study, making total respiration
measures that are easier to realize.
. KNAPPER : Die aufgeworfenen Fragen sind sehr sinnvoll.
Wir beatatigen die Angaben und können behaupten, dass in
unserer Arbeit in Rio Grande do Sul einige Arten der Gattung
Pheretima zur Oberfläche koim en wenn ihre “nicho” mit Stroli
bedecht sind.
672
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DEVELOPMENT AND FECUNDiTY OF THE MANURE WORM,
Eisenia foetida (Annelida: Lumbricidae), UNDER LABORATORY
CONDITIONS
A. D. Tomlin and J. J. Miller
.1gr.n Iture Ciutada
Londo,,. Caitada
INTRODUCTION
The lay and technical literature are replete with co;.flicting claims
on the growt . rates and fecundity of the manure worm, Eisenia foetida
(Savigny, 182b) and even its identity (Fosgate and Babb,1972). In
addition, suspected fraudu.&ent claims were ani continue to b made by
dishonest hOTin breeders seeking co entice more people into the manure
worm hreeding business. We undertook this research project to provide
some clear answers as to what the growth rates and fecundity of the
mai 1 ure worm are under a variety of temperature and worm density conditions.
METHODS AND MATERIALS
Several hundred specimens of the manure worm were obtained from an
Ontario grower, verified by key (Reynolds, 1977) as E. foetida ; and
used as a continuously reared laboratory culture.
Experiments were carried out on worms confinod to plastic petri
dishes (15 cm dia. X 2 cm deep with a 15 cm dia. while filter paper on the
bottom) containing approximately 130 ml of moist (82% water by weight)
manure (leached dairy cattle manure:maple sawdust, 3:1 or leached horse
manure) pH of both approx. 6.8, ueighing about 100 gin; the manure was re-
placed weekly. Tenperature dependent experiments were performed in con-
trolled environment cabinets with ±lC° preci.sion. Oishes “are checked
daily to remove cocoons which were placed singly in 4 dram 1ear plati’
snap cap vials which contained a moist filter paper disc. When the young
worms hatched from the cocoons, the date was marked on the vial label
and their subsequent growth and development noted.
RESULTS
The length of one life cycle varied from a mean of 51.5 clays at
25°C to more than 166 days at 13°C, from freshly deposited cocoon
through clitellate worm and deposition of the next generation of cocoons
673
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(Table 1).
TABLE 1: Maturation periods for Eisenia fuetida at various temperatures
on dairy cattle manure.
Elapsed
time (days)
for maturity
periods
Temp.°C
To
Hatch
To Incipient
Clitellum
To Complete
Clitellum
To Cocoon
Production
No. W:rms
Stud cd
13
45.2
107.5
116.9
none by 166
22
16
31.2
68.8
77.3
98.6
25
19
26.7
58.7
62.2
70.3
24
22
19.8
46.0
53.5
55.5
11
25
18.9
45.1
48.1
51.5
16
The number of yotng worms hatching from viable or fertile cocoons
incubated at 25°C varied from 1 to 11 (one event) with a mean of 3.35±0.28
of 310 cocoons studied. The percentage hatch of cocoons obtained on
horse manure at 25°C varied from 50.9 to 90 with a mean of 80.7 (Table 21
TABLE 2: Percentage hatch of Eisenia foetida cocoons in horse manure at
25 C.
Dish
No.
No. of cocoons
Mean No. Worms/Cocoon
% Hatch
1
39
2.80
89.7
2
53
3.81
83.0
3
53
2.75
50.9
4
22
3.14
86.4
5
38
3.55
89.5
6
33
4.24
87.9
7
32
1.45
50.0
8
40
4.70
90.0
Total
310
Grand mean 80.7
Increasing temperature reduces both the percentage hatch of cocoons
from 57.3% and 60.8% at 13°C and 16°C to 41.2% at 25°C, and the number
of young worms produced per cocoon (Table 3).
As the density of mature clitellate worms per unit volume cf manure
increases the number of cocoons/parent/wk, the hatching fraction, and the
number of young worms/cocoon declines. If these 3 numbers are multiplied
674
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TABLE 3. Effect of temperature on the no. of worms produced per cocoon
and the percentage hatch of Eisenia foetida cocoons (Dairy
Cattle Manure)
Temp. °C Mean No.
Young worms/
cocoon
Mean No.
Young Worins/
Vi ible Coccon
Total No.
Cocoons
No. Viable
Cocoons
%
Hatch
13
16
19
22
25
1.71
1.94
1.80
1.01
0.65
297 a
323 a
2.90
3 b
1.58
82
78
73
80
80
47
48
39
38
33
57.3
60.3
53.0
47.5
41.2
a, b - Numbers followed by the same letter are not significantly
different from one another. Numbers followed by different
letters are significantly different from each other (NO.05)
Duncan’s New Multiple Range Test.
together for each density level (Table 4), we obtain a “productivity”
figure expressed as No. of young wo inilparent worin/wk which varies from
5.45 at the lowest parent density to 1.19 at the highest.
TABLE 4. Effect of parent crowding (density) on young worm production
at 25°C on dairy cattle manure (200 mi/dish) over 14 weeks.
No. Parent
Worms/Dish
No. Cocoons
Produced!
Parent/wk
Hatching
Fraction
No. Young
Worms!
Cocoon
No. Young Worms!
Parent!
wk*
2
2.0
.79
3.45
5.45
4
...
.73
2 47
2.Jb
6
0.8
.77
2.56
1.58
8
1.2
.42
2.36
1.19
* Product of Columns 2, 3 and 4.
Population density also had an effect on weight over the 14 week
duration of the experiment. At densities above 2 worms per dish,
reductions of between 11.1 and 15.6% occurred (Table 5).
67j
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TABLE 5. Effect of population density on weight of Eisenia foetida
at 25°C over 14 weeks (2 replicates for each density).
No. worins/
Dish
Mean
at
Wt (gm)
start
Mean ivt
at 14
(gm)
wks.
Wt.
2
O.4
0.44
0
4
0.45
0.38
-15.6
6
0.45
0.40
-11.1
8
0.45
0.38
-15.6
DISCUSSION
The rate of development is, as expected, pc.sitively correlated
with temperature. Obviously growing worms unsheltered 1 in cold weather
climates will result in dramatically reduced production during the
winter months. Low temperatures also suppress either mating behaviour
o reduce cocoon production; since the clitellate condition is reached
at 116.9 days at 13°C, but no cocoons are produced for at least 50
days following.
It is also interesting to note that at 25°C a life cycle can be
completed in 51.5 days as opposed to the 60-90 days suggested by Gaddie
and Douglas (1975).
The varied hatchability of the cocoons is similar to that found
by Watanabe 3nd Tsukamoto (1976). The maximum number of worms they
found from one cocoon was seven; herein we report a maximLu.; of ii. Also,
in results similar to theim we noted a range in the mean nu nber of
worms produced per cocoon from 3.35 in the autumn to 1.58 in the winter.
This is a long way from the mean of seven proposed by Gaddie and Douglas
(1975).
From Table 3 it appears that increasi;ig incubation temperatures
are negatively correlated to the number of young worms produced per
cocoon. There are perhaps a number of possible causes of this result,
but there is the possibility that at higher temperatures respiration
rates within the cocoon might only be maintained with difficulty and, if
there are several worms developing, this could result in cocoon mortality
which is reflected in the lower percentage hatch at higher temperatures.
The parent worm density had an unexpected result on the number of
worms produced per cocoon. Somehow the reduced density of mature worms
results in a larger mean number of worms/cocoon being produced, a higher
676
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hatchability percentage (fertility rate), and a larger number of cocoons/
parent being produced. Presumably this allows for a more rapid population
expansion to ultilize the larger food resource (manure) available at the
lower parent worm densities. A similar effect has been observed with
the waterf lea, Daphnia pulex , where fecundity was reduced at higher
densities (Frank, Boll, and Kelly, 1957).
The average number of cocoons/parent/wk varied from 2.0 to 0.8 over
14 weeks during the winter. Graff (1978) averaged from 5.0 to 3.5 on
14 day tests during spring and summer. We don’t feel there is a conflict
in the results here because we observed many cases where worms produced
5 or more cocoons/week, but this rate would only be maintained for 2 or
3 weeks. Naturally over longer periods this average would decline which
has considerable implications for some of the more outrageous claims of
growers where high cocoon production rates are assumed to be naint .iined
over lorg periods.
We have received several reports from commercial worm growers
corcerning sudden reductions in size (weight) of worms. This was
usually attributed to reduced food and/or moisture supply. Since fresh
manure was supplied weekly to our cultures, we do not feel that this is
necessarily the reason. There is, however, some correlation between
worm density and weight loss.
CONCLUSIONS
The lumbricid worm, E. foetida, can complete a life cycle in as
few as 51.5 days. Maturation is strongly correlated with temperature
in the range 13°C to 25°C. The maximum number of worms found in a
single cocoon was 11, but the mean lay between 2 and 3. Parent worm
density is negatively correlated to cocoon production, cocoon fertility
and th number of young worms produced from a cocoon.
LITERATURE CITED
Fosgate, Q. T. and M. R. Babb. 1972. Biodegradation of animal waste by
Lumbricus terrestris. J. Dairy Sci. 55: 870-872.
Frank7P. W., C . Boll, and R. W. Kelly. 1957. Vital statistics of
laboratory cultures of D phnia pulex De Geer as related to density.
Physiol. Zool. 3O 287—305.
Gaddie, R. E. and D. 5. Douglas. 1975. Earthworms for Ecology and
Profit, Vol. 1. Bookworm Publishing Co., Ontario, California.
677
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Graff, 0. 1978. Physiologische Rassen bei Eisenia foetida (Savigny,
l826) OIigochaeta, Lumbricidae)? Em E itrag zur Frage der
Domestikation dieser Art. (Physiological races in Eisenia
foetida(Savigny, 1826)(Oligochaeta, Laimbricidae)? A contribution
to the question of domestication in this species. Rev. &ol. Biol.
Sol. 15: 251-2(3.
Reynolds, .J. I V. 1977. The Earthworms (Lumbricidae and Sparganophilidae)
of Ontario. Life Sciences Misc. Public., R.O.M., Toronto.
Watanabe H. and J. Tsukamoto. 976. Seasonal change in size class and
stage structure of lumbricid Eisenia foetida population in a field
compost and its practical application as the decomposer of organic
waste matter. Rev. Ecol. Biol. Sol. 13: 141-146.
ACKNOWLEDGMENTS
The authors acknowledge the technical assistance of Ms. P. Vander
Deen, and thank Mr. J. L. Lewis of Jimaur Bio-Organic Cultures Ltd.
for supplying the worm culture. Contribution No. 764, Research Ilthtitute ,
Agriculture Canada, London.
QUESTIONS and COMMENTS
J.E. SATCHELL : Can you suggest t e mechanism causing
the weight losses at higher population density?
A.D. 0MLIN : No. We are fairly certain, however, that
the weight losn was not due to reduced food substrates since
they were replenished weekly.
A.J. REINE KE : Did you consider the possibility that
diurnal, fluctuation in temperature with a mean of say, 200 C
co’ald lead to quite different results than a constant temper-
ature of 20°C as far as time until hatching goes?
AD. TOMLIN : Yes, but we were interested mainly in
finding the minimum time for development from deposition of
cocoon to sexual maturity. Introducing another parameter
would have complicated the experiments even further.
D. LIVINGSTONE : Were the manures leached of urine?
AD. ‘ IVMLIN : Yes and the average pH was 6.8.
678
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SEASONAL VARIATIONS OF SEX-RATIO IN FOREST
GROUND-BEETLES NATURAL POPULATION
eGilles Benest and J. P. Cancela da Fonseca
Uuipersii, Puns t’I!
‘Ecole 1’lon,nafr 5u.pe’ zeure
France
Because of its importance for reproduction, the sex-
ratio of a population is one of the factors effectively
influencing the dynamic of a population. This ratio varies
with the species and population age (DAJOZ, 1971); in Carabid
beetles, it is generally thought to have value one (PENNEY,
1967), but seems to vary with the habitat (MOSAKOWSKI, 1970).
V.d. DRIFT (1951) observed its variations also with the
seasons; a problem about which thereare a very few studies.
It is difficult to know the sex-ratio of a natural
population of Carabidae because the traps are not identic-
ally effective for both sexes : in fact, GRUM (1962) shows
that the females locomotion, more important at the period
of laying the eggs, alter the male/female ratio of the capt-
ures. This work studies the seasonal variat .ons of the sex-
ratio according to the activity cycle of Carabidae.
METHOD & MATERIAL
C
Animals have been trapped from february 1972 to
january 1974 included. The traps are pitfalls of BOIJCHE
type (1972); the captured animals ae killed and fixed
with a NaC1 saturated solution. A wire-netting stops
the leaves from falling in the trap. The 13 pitfall traps
are visited each month; captured animals are taken out
and kept in alcohol 700.
Study place the “Tillaie” biological reserve is
an area of 33.74 ha, situated in the N.E. fourth of the
“Forët de Fontainebleau”. The 700 m2 urder study are a part
of an Aspero Fagion established cn a mull-moder: the org-
anic matter content is 4-5%, the percentage base saturation
30%; pH is 4.5 (B’)UCHON et al. 1976).
All insects were dissected for measuring and weighing
the gonads.
RESULTS, DISCUSSION
At “La Tillaie”, 12 species of Carabid-beetles be..
longing to four families were captured : Carabidae, Nebriidae,
Trechidae, Pterostichidae . Captures were homogenous between
the two years according to the number of captures and to
their specific distribution. Thus, we summarized data from
both years : we shall then analyse the sex-ratio of both
years together.
679
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Moreover, we shall be inte sted here only on some
Pterostichidae . There were six species of this hmiiy
in the traps : Ar2utor oblongo unctatus, Abax ater, Abax
p. ..ralle1lus, Abax oval s, Svnuchus nivalis, Calathus piceus .
The former four, three of which belong to the same gen us,
constitue 87.89% of all the captures. Here, we shall not
take in account S. nivalis captured once during 24 months
and C. picew 1 , as we captured two males and 32 females of
this species.
We showed (BENEST and CANCELAda FONSECA, 1979) tnat
the activity perioc of these animals were
A. oblogonpunctatus
A. ater
A paralleflus
A ovalis
march-july, with a maximum in june;
april-october, with a maximum .n july;
march-september,with maxima in april
and june;
april-august with a maximum in may.
Thus we shall observe the evolution of the sex-
ratio (d’/t) during these periods. The activity periods we
observed at “La Tiliaie” correspond to the dates of reprod-
uction of these species : spring for A.obloi gqpunctatus and
autumn for A ater for example.
Generally, observations provide a sex-ratio of value
one (PENNEY, l.c.). While in the four populations we studied,
this ratio is more often different from one (fig.1). However,
Wa draw attention on the following facts : 1) sex-ratio
vari’ s according to the months; 2) on the dates of maximum
activity, the sex-ratio is nearly one for A. ater, A. ovalis
and A. oblongoi unctatu , and 3.5 for A. paraUellu .
AT,o
I
I
AN OV$ INDICATE ACTiVITY NAXIIaJN CF EACH SPCO
FIGURE 1 z Variations of sax—ratio according to rnsasons.
p
-J
—
— &ib)iigopwicP& aa
A. psrufl.IIus
I
4
1
14 A P4 I j
680
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Thus, it clearly appears that for the 3 first species
the number of maiPs j5 equal to the number of females at the
time of mating and laying eggs; this has already been obs-
erved by v.d.bRIFT (ic.) .
However, this is not true for A.paraiiellus , the
behavior of which is different from that of the other
three species : in fact, this species shows a great excess
of males on the two dates of maximum activity. This partial-
lar behavior deserves attention for it clearly distinguishes
A. parallellus from he two other Abax.
Thus, it is clear that, for these four species, the
share of each sex to the active population varies with time :
this phenomena is related to the different activity of each
sex according to the season. This hypothese , although disp-
uted by some author (SflSZKO,1976) is fully corroborated
for A. ater, A. ovalis and A. oblongopunctatus . However,
it does not fit A. pa alie4 . the behavior of which is
particular the females of species are the only ones,
arong the known C abidae , to be able to lay two batches
of eggs in one year (LOSER, 1970).
For a better explanation of the3e phenomena, we must
study the gonadal state of the captured animals. By the
males, the most important variations are observed on the
ac’essory glands (CORNIC, 1970). Though JONES (1979) found
it difficult to study them on newly captured animals; this
is due, in part, to the technic : pitfalistrap active animals
from a locomr’tory point of view as well as from a sexual
point of view. Thus we could not observe any significative
variations considering either the diameter or the dry weight
of the glands. While by the females, it is easy to count
2nd weight the eggs contained in the abdomen. Therefore,
the fcllowing results concern only the females.
The relation between the locomotory activity period
and the reproduction period appears clearly in the four
species from the fact that
1) as soon as the first captures of the year, some
female carry eggs, but those of A. ovalis ;
2) eggs are only produced during the period of imp-
ortant activity (BENEST-CANCELA da FONSECA,l.c.)
3) variations of the proportion of egg-carrying fem-
ales follow quite closely the locomotory activity
variations lznown from the captures.
-------
IGURC 2 Va iationa of egg production
Abax ater;
$ Abax ovalie;
Abax parallellus;
$ Argutor oblongopunctatua;
( ) u Ratio (%) s egg—carrying femalae / all
captured females;
Total number of eggs;
s Average number of eggs per females in the populatthn;
z Average weight of eggs per females in the population;
$ Variation of the eax—ratie;
$ Date if maximum weight of one single egg;
$ Date •f maximum number of egga carried by one female.
682
-------
2:
p
I
1!
I
I
I
EPJ
It
-------
On the contrary, the production of eggs is not at a
maximum when the activity is maximum i. e. when the sex-
ratio (d’/?) is of value one. We measured egg-production with
four criteria (fig.2)
- the number of eggs per female in the population;
- the maximum number of eggs carried b ’ one female:
- the egg weight per female in the population;
- the maximum weight of a single egg.
These four criteria provide very homogenous data for
the three Abax : by the three species, they are maximum
at the time when each population contains the most egg-
carrying females. This is not true for A. oblongopunctatus ;
however, we must recall that for this species only one female
was caught in april and in july, and it carried eggs this
constitues a bias in the data.
By A. ater , the time of the maximum egg production
is cne month earlier than the time of maximum activity; for
ovalis, maximum egg production is two mont1 later than
ma .imum activity; for A. parallellus , every maxima happen
together in april, but with one month inbetween during
summer. There %ain appears A. parallellus originality.
CONCLUS ION
Thus, thei app ar no relation between egg-production
and sex—ratio. In fact, the relation is closer between the
period of reproduction and the period of locomotory act-
ivity. Reproduction processes consist, among others, oF
mating and laying eggs : these two processes imply female
locomotion first for mating, second for choosing the
suitable laying place.
684
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LITE1WIURE CITED
BENEST G., CANCELA da FONSECA J.P., 1979, Etude d’un peu-
plement de Carabiques forestiers (Hêtraie de La Tillaie,
Forêt de Fontainebleau), Pedobiologia, in pub.
BOUCHE M.B., 1972, Lombriciens de Prance : Ecologie et Sys-
téinatique, Ann. Zool. Ecol. Anim. H.S. INRA, Paris, p.671
BOUCHON et al., Cartes et notice des sols, du peup]e-
ment forestier et des groupements végétaux de is reserve
biologique dc La Tillaie en for6t de Fontainebleau. PBI-RCP
N°165,CNRS, ORSAY
CORNIC J.F., 1970, Etude préliminaire des Carabidae d’un
verger de pommiers de la Region Parisienne. Th.3° cycle,
PARIS.
DAJOZ R., 1971, PARIS DUNOD; Précis d’écologie, pp.454
VAN DER DRIFT J., 1951, Analysis of the animal community
in a beech forest floor, Tidj.v. Ent., 94 : 1-168
GRUM L., 1962, Horizontal distribution of Larvae and im-
agines of some species of Carabidae, Ekol. Pol. A 10:73-84
JONES M.G., 1979, The abundance and reproductive act-
ivity of common Carabidae in winter wheat crop, Ecol.
Entomol., 4 : 31—43
LOSER C.H.., (1970), Brutfflrsorge und Brutpflege bei
Laufkäfern der Gattung Abax Verh. Deut. Zool. Ges.
Würzburg, 1969 : 322—326
MOSSAKOWSKI D.Z., 197P,, Okologische Untersuchungen an
epigalschen Coleoptera atlantischer Moor -und Heidistandorte,
Wiss. Zool., 181 : 233—316
PENNEY M. M., 1967, Studies on the ecology of Feronia
oblongopunctata (Coleoptera Carabidae), Trans. Soc. Brit..
Ent., 17 : 129—139
SZYSZKO 3., 1976, Male to female ratio in Pterostichus
oblongopunctatus (Coleoptera Carabidae) as one characteristic
of a population, Pedobiologia, 16 : 51-57
QUESTIONS and COMMENTS
A. CARTER : Data from pitfall trapping cannot be used
alone to determine the actual sex ratio or proportion of
teneral to older adults in carabid populations. What comments
do you have on this?
G. BENEST : Pitfalls are known to trap only active animals,
685
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males or females,teneral or older; in fact, this technique
does not give a good estimation of the total population. I
only say that the contribution to the active part of the
population is different for t.ne males and the females according
to the season.
J.A. ADDISON : Do the micromorphological characteristics
that you used to discriminate between the two Lithobius species
remain constant for all stages in the life cycles of these
two species?
G. BENEST : Probably Lithobius sp. do not change micro-
morphological features according to developmental stages.
But that is not true of all animals. Great differe nces
exist between larvae and imaginals in Coleoptera for example.
SZUJECKI : Sex ratio in the Carabidae population is
not stable, it varies in time and space in relation to the
change in environment and in the population. We observed
however that sex ratio in the population of Pterostichus
oblongopunctatus is rather stable (on the average) in this
same site conditions (higher in pure pine stands and lower
in rich bzoadleaf forest). It also changes during the devel-
opment process in the stands (in various age classes of stands).
This may be followed by various degrees of competition between
species in the Carabidae community in various site conditions.
H. PETERSEN : Do you have evidence whether the sex-ratio
is determined from the egg stage, or is it a consequence of
differential mortality between males and females?
Did your experiments with marked animals show different
life times for adult males and females?
. BENEST : Actually there cannot be any answer to the
question because pitfalls are concerned only with imagines.
Moreover, research on reproduction in Carabia beetles has only
begun and very little is known about egg production in natural
conditions.
There seem to be no great differertce: between male and
female life times.
. LAVELLE : How many species is it necessary to study
to be able to determine the whole Carabid diet?
G. BENEST : Oligophagous Carabids are rare. Skuravy has
demonstrated that some Pterostichidae could eat up to 18
different families of prey. Among these Pterostichidae,
Harpalus aeneus eat 14 of these families; moreover it is able
to eat eggs and dead animals.
That is the difficulty of this type of work. Carabidae
have a very broad spectrum of prey.
686
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INTRODUCTIONS EN SURPOPULATION ET MIGRATIONS
DE LOMBRICIENS MARQU S
‘Denis Mazaud and **Marcel B. Bouch
INA Par:s .Grignon 16
Frana
INRA Stalion de fauna du sal
France
INTRODUCTION
L’etud ecologique fonctionnelle des lotnbxiciens doit, pour l’es-
sentiel, se faire in situ , les données de laboratoire n’offrant présente-
ment aucune garantie, notainment en raison du fait que l’ n ne peut que
rarement les recouper par des informations acquises en conditions natu—
relies -
A l’exception de l’étude de certains phénomênes se produis nt A
la surface du sol, nous sonsnes obliges géndrale nent de faire des obs rva-
tions destructurant le sol. Ces observations, par prê].èvenents cu Lectu—
re directe dans le gol. nous oblige donc au choix d’emplacements diffd-.
rents a chaque fois. Les inforlnationb sent acq-iises & un instant ; leur
repetition permet de constater une serie d’images successives se rappor—
tant & des emplacements diffCrents sur des animaux diE fdrents de sorte
qu leur interpretation en terme dynamique set pratiquement impossible
dans la plupart des cas (voir cependant Lavelle, 1971, pour des donnees
demographiques). Toutefois, le marquage des animaux permet de retrouver
lee niêmes cohortes d’individus, voire leb mëmes individus, et ainsi de
suivre des variations d’états diachroniques en fonction du temps).
DistinguOnS immédiatement les marquages individuels des marquages
isotopiques. L’usage d’isotope permet de suivre A i’intdrieur d’un orga-
nisme, ou en gdndral d’un système, le devenir de cet isotope et ses asso-
ciitions avec des molecules, des tissue, des individus, voire des chain s
trophiques.
Le marquage individuel vise A reconnaitre un individu, ou une co].-
].ection d ‘individus ( une cohorte), parmi un ensemble plus vaste. De
três noinbreuses techniques sent thdcriquemerit applica.b].es pour reconnai—
tre c s enimaux marques mais en pratique seules quelques—unes peuvent
At e - acement mises en oeuvre. Dans certaines circonstances, les iso-
.ttent la reconnaissance d’individus male jeneralement cette
possibflité es très iimitde car lee isotopes peu ou faiblement radio—ac-
tiEs ne se “voient” pas et ndcessitent des moyens d’analyse lourds et
destructeurs (broyat des tissue) ; quant aux isotopes fortement radio—ac-
tiEs, lie sont interdits dane la nature. NOUS nous sommes donc tournds
-iers le marquage individuel directemerit visible (Mazaud, 1979) et non
isotopique. Deux approches ont tentdes : la cautérisation individuel-
le de soies et le marquage colord.
La cautdrisation des soles, d’usage délicat, a des consequences
687
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peu standardisables. Elle pourrait conv%nir en certains cas au tnarquage
de quelques individus mais ne per net pas de travailler sur des cohortes
iinportantes. Af in de suivre au terrain le devenir dc cohorLes d’indivi-
dus, 1.es techni.ques de coloration ont été éprouvées et étendues. Conune
Ia cautérisation, cette te *rt ue est originale a l’e cc eption de l’usage
du vert menthe E (vME) propose antérieurement par I .. Me ihardt (1976).
Pour apprécier les difficultés pratiques de mine en oet ‘re de cette nou—
velle méthode, divers l&c.hers de lombriciens, . r. surnombre, ont Cté ef-
fectuäs sur tin sol non perturbé préalablement. Puis len lombriciens, mar—
quds ou non, ont été recaptu 4s au lieu de làchage et autour de ce lieu,
ce qui a pe: znis d’acquérir des informations relatives a la migration et
& l’effet do surpopulation.
MATERtEL ET METHODE
Marquage des animaux
La technique résulte de multiples ess.is préalables et de contra—
len de l’état physiologique d 1 s animaux qui n’ont p s perinis de mettre
en evidence des troubles profonds chez les lombricier.s colorés au labora—
toire (Mazaud, 1979). La méthode standard utilisée au terrain comporte
le dtapes suivantes
— capture des animaux A la méth de au formol, & proximité du fu-
tur lieu de relAcher,
— rinçage.
— pesée,
— determination en espèces et stades, voire de poids des animaux
choisis,
— coloration,
— relácher dans l’aire d’accueil,
— après un délai variable, recapture dans l’aire et A proximitd,
des colords et non colons.
La Loloz tion des aniniaux s’effectue par ].avage (quelques dizaines
de secondes), égouttage—séchage sur gnillage plastique (environ 5 minu-
tes), coloration (de 2 sin 30 & 3 inn) par trenipage dens une solution cob—
rante, égouttage (quelques secondes) et séchage (3 A 10 sin selon la tail—
le et les espéces). Vingt et un colorants “histologiques’ ou “alimentai—
res ” ant dté testes ; deux colorants histologiques (rouges) ont dnnné
des résultats encourageants Cia safranine et la phioxine) quoique leur
toxicité variAt avec l’origine des produits. Deux colorants alitnentairer
le vert menthe E CE 102 + E 132) et la coccine (5 124) rouge ant donnd
satisfaction ils furent utilisds au terrain. Deux dispositifs expéri-
mentaux ant dtd mis en place au terrain, chacun dans une bocalité diffé—
rente (Grignon et Citeaux).
Len essais effectués a Grignon (départenient des Yvelines) ont été
faits en prairie permanente A sal alluvial liniono-sableux. Len animaux
furent captures “au formol”, colorés en vent (VME) ou rouge (surtout sa—
franine et cocaine) pour caractériser dane chaque espéce ‘Nicodrilus giar—
d i giardi (Ribaucourt, 1901) ; Lumbricus terrestrjs L. 1758 em. Sims,
1956 ; .4llolobophora icterica iateriaa (Savigny, 1826)) des classes de
688
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CONCLUDING REMARKS
All of the evidence presented in this paper strongly suggests
that the soil rr.tcroarthropods of a juniper site in the Mojave aesert
exhibit characteristics of an ‘r’ selected system. The ecological
significance of distInguishing between ‘r’ and ‘K’ selected syatems
is that, in the former, emphasis is pleced on productivity, whereas
efficiency is t,e hallmark of the latter. ‘r’ selected systems have
a high rate of turn-over of biological naterials and, looked at in
terms of the decomposition process occurring in the soil, this means
a high rate of nutrient release and a rapid depletion of these
nutrients through leaching. This is reflected in the low organic.
content of hot desest soils .ind may explain why, in the profile under
juniper at the Joshua Tree site, discrete fermentation and humus
layers are absent.
LITERATURE CITED
Edney, E.P., Franco. P.J. and McBrayer. J.F. 1976 Abundance and
distribution of soil microarthropods in Rock Va’ley, Navada.
US/IBP Desert B±ome Research Memoranda 76-24 Logan: Utah State
University. l4pp.
Johnson, ‘ .A. and Whitford, W.G. 1975 Foraging ecology and relative
importance of subterranean termites in Chihuahuan desert cosystems.
Environmental Entomol. 4: 66-7C
Lloyd, N. and Ghelardi, R.J. 1964 A table for calculating tho
‘equitability’ component of species diversity. J. Anim. Ecol.
33: 217-225
MacArthar, R.H. 195? On the relative abundance of bird species.
Proc. Nat. Acad. Sci., Wash. 43: 293-295
Nay-heir, I. 1973 Desert ecosystems: environment and producers.
Ann. Rev. Ecol. Syst. 4: 25-51
Pianka, E.R. 1970 On r- and K-selection. Amer. Nat. 104: 592-597
Santos , P.F., DePree, E. and Whitford, W.G. 1978 Spatial distribution
of of litter and mioroarthropods in a Chihuahuan desert ecosystem.
J. Arid Environ. 1: 41-48
Schumacher, A. and Whitford, W.G. 1976 Soatial and temporal variation
in Chihuahuan desert ant faunas. Southwest, Nat. 21: 1-8
Waliwork. J.A. 1970 Ecology o Soil Animals. Maidenhead: McGraw-hill
283 pp.
Wallwork, J.A. 1972a Distribution patterns and pooulation dynamics
of the micro-artfropods of a d sert soil in southern California.
.1. Anim. Ecol. 41: 291-310
Wallwork, J.A. 1972b Mites and other microarthropods from the Joshua
Tree National Monument, California. J. Zool. London 168: 91-105
Whitford. W.G. 1976 Foraging behaviour of Chihuahuan desert harvester
ants. Amer. hlidl. Nat. 95: 455-458
Wood 1 T.G. 1971 The distribution and abundancs of Folsomides
desercicola Wood (Collembola: Isotomidae) and other microarthropods
in arid and semiarid soils in southern Australia . with a note on
nematode popuL.tions. Pedobiol. i i: 446-468
767
-------
the total number of species present on a site. The observed distri-
bution of inoividuals among speciee is compared with the ‘broken
stick’ model of MacArthur (1957) which apportions individuals among
species about as equitably as Is possible in nature. The extent to
which an observed distribution departs from MacArthur’s model will
be measured by the extent to which the equitability ratio falls below
unity. According cc Lloyd and Shelardi (1964), equitability is
sensitive to the stability of physical conditions, and ‘r’ selected
systems have relatively low equitability ratios.
Estimates of the various parameters requirad for the calculation
of equitability in the Josnua Tree site are presented in Table 2.
Thase estSmates are based on data from 20 specIes of m 4 tos and
Co12.qmbola and, thus, are direotlj comparable witn estimates provided
by Lloyd and Shelardi (1964) for soil microarthropods in a temperate
beech forest.
TA5L’ 2. A omparison of d ersity parameters fror , temperate forest
and hot desert (Mojav f).
Tor,iperato Hot
forest desert
s 44 20
H 5.46
max
H .16 2.66
s’ 26 9
e 0.59 0.45
where:
s • the observed number of species
= the maximum diversity obtainable if all species were
equally abundant
H = the observed species diversity (Shannon-Wiener)
= the theoretical number of equally abundant species which
would be renuired to give the observed species diversity.
e = the measure of equ2tability; the ratio s’/s
It is evident that uquitability is lower in the hot desert
Mojave site than in the temperate beech forest. In other words
tnere is ar appreciable departure from the Mac Arthur model.
766
-------
Population densities
Low densities i cr microarthropods in desert 3011! ware first
reported by Wood (1971) (Australia) and Wallworl. (1972a) (North
America). More recent studies in North American deserts are very
much of the same order of magni;ude as these earlier estimates, as
shown in Table 1. For purposes of ccmparison, Table I also Includes
a ra.;ge of microarthropod densities reported by variout. workers from
a variety of cool, moisr temperate, lowland grasslands. Clearly
densities of desert microarthropods are lower, in general, by a factor
if ten, than their counterparts In other parts of the temperate region.
TABLE 1. Densities of microarthropods in different desert soils
compared with cool moist temperate grasslands.
Locality Avi’. nos. Authority
(xlO ,m )
Desert grassland, 2 - 3 Wood (1971)
Australia
Juniper soii, 1.6 Wallwork (1972a)
Mojave
Mojave litter, 1 - 13 Edney, Franca and
various Mc6rayer (1976]
Chihuahuan 0 146-3 1 Santos, DePree and
litter, vaeious • Whitford (1976)
Cool temperate 32-298 Waliwork (197fl)
grasslands
These low population densities in deserts are 3nother indication
of an ‘r’ selected system. Not enough data are available to determine
whether or not populations within a particular site show erratic density
changes; a long-term sampling program is required for this puroose.
However, Santos et al. (1978) have shown that there is a high correlation
between microarthropod densities and the amount of surface littee
present. The distribution of surface litter in the Chihuahuan sites
studied by these workers is very much influenced by surface run—off
af water during heavy rains. Hence, it could be argued that micro-
arthropod densities may be influenced, perhaps indirectly, by physical
factors whIch are stochastic in character. If densitIes respond in a
similar stochastic manner, it c’uld be expected that changes will be
unpredictable in their timing and magnitude. The hypothebis that
microarthropods respond to physical parameters in the desert environment
receives some support from a consideration of equitability ratios.
Equitabs) ity
The concept of ‘equitability’ (Lloyd and Chelardi, 1964) relates
the way in sshich the total number of individuass are distributed among
76g
-------
28
24
20
E
C
12
< 8 prey

4 - ,/
•\ predator
......... .‘.... .••
I 1 1
Oct Nov Dec Jan Feb Mar Apr May Jun
FIGURE 3. Population curvas for a pr8dator/prey bysten in Juniper
soil. Upper curve is obtained by poo1 ng counts fDr
Joshuella strtata and Ilaplochthonius variabilisj lower
CUrVe is for Spinibde]] .a oronini .
76k
-------
again, is a characteristic nf an ‘r’ strategy.
The main microartnrnpod predator i . this system appears to be
the prostignatid mite Spinibdella cronini (Baker and Balcock) and it
has been shown to prey on juvenIles of bath of the oribatids mentioned
above. Here, it displays real opportunism, as the curves n rigure 3
illustrate. The prey curve, in this FIgure. is a composite derived
by pooling the monthly population estimates of 3. striata and
H. variabilis , and its birnoda)ity reflects the dit’Ferent contributions
made by these two species to total micro3rthropod numbers at different
times of the year. The lowar carve in tt.e Figure shows monthly
variations in the numbers of S. cronini and, again, this curve is
bimodal. The two peaks coincide witlflwu periods of recruitment
(Wallwcrk, 19?2a), and it is obvious that one of these corresponds
to that of one of the prey species (the January peak for 3. striata) .
and the other, anc larger, peak to the April/May recruitment of
H. variaoilis . This is no classical orsdatnr/orey ccrve for there is
no lag phase iii the build-up and decline of populations of prey and
precator. The predator has been able to gear Its life cycle to
correspond exactly with the prey cycles. This implies that the
predator population is not food-limited and, hence, will not be
competing with any other predators on the site for food. It can be
concluded that S. cronini is an opportunict living in a non-competitive
situation - a s eefita an’r’ stra’ sgist.
Reproductive strategies
It will be clear., from what has been said above, that the three
species of m.te which constitute an impurtant numerical part of the
nicroarthropod fauna in Joshua Tree have periods of recruitment which
are largely restricted to one or two months of the year. At other
times of the year, the .opulations are composed almost entirely of the
adult stage. This irrinediately suggests that post- smbryonic development
to adulthood is rapid. It was previously noted (Wallwork, 1972a) that,
in contrast to the adults which were recovered mainsy from the mineral
soil at depths of 8—14 cm , juveniles of all three of these mite
species occurred mainly in the surFace litter layer. Juveniles
apparently migrated upwards from the mineral soil into the littei
after hatching, and this dispersal activity would bring theae imbtures
into regions of higher temperatures which would accelerate post-
embryonic development. Rapid development times are characteristic of
‘r’ strategists, and another of the criteria net out at the beginning
of this paper is partly satisfied. To satisfy this criterion completely,
daca are required on reproductive rates and longevity. These are not
availaule, but in the case of lc’ngevity. an inference can he made. As
noted above, for most of the year populations of 3. striata, H. variabilis
and S. cronini consist virtually of adults. There is not the mixture
of age classes in the popalations which would characterise species
with overlapping generations. It may be concluded, then, that
generations do not overlap and are, therefore, short-lived - another ‘r’
strategem. Indeed, in the case of Haploc.hthonius variabilis , the
available data suggest a completa separation of generations since,
after a peak in adult numbers in November, the species is hardly
encountered again in samples until the start of its recruitment period
in the following April.
763
-------
increase in the litter in the December to February period and, after
a decline in March, produce a second peak in April and ray. These
populatior. peaks coincide with periods of recruitment 1 as will become
apparent snortly.
f e.tnfall evtrts are discontinuous and stochastic in I’iot de5erts,
their timing and n agnitude have a large random component. Hence,
desert soil microarthropods O W ba said to live in 1 and respond to,
an unpredictable er vironment, thus satisfying the first criterion for
an ‘r’ selected system.
Faunal succession
A total of 33 nicroarthropod species was recorded from the
Joshua Tree sits, mainly oribatid and prostigmatid mites and Collembola.
In the context of ‘r’ and K’ strategies, it is naces ary to establish
.ietht r or not this constitutes a ‘pioneer’ fauna. This requires a
knowladge Cf faunal succEssion which cannot be obtatned from a nine
month sampling program and, in the absence of emr’.irical data, it is
necessary to seok theoretical explanationa. Two categories of
avidence are relevant here. Firstly, the suil at the Joshua rree site
consIsts of a surface layer of juniper needles lying directly on a
quart?itic mineral layer - with no intervening humus or fermentation
layers. This is, essentially, an embryonic stage in soil formation and,
intuitively, it could ne expected that its fauna would be a pioneer
one. Secondly, oribat d and prostigmatid mites ano Collenibola are
often early colonisers of developing soIls, particularly those of a
mineral character, in many parts of the world, and it is perhaps no
surprise that, collectively, these groups contribute nearly two-thirds
of the n Icroarthropod species recorded from the site.
Opportunism
It has been shown (Wallwork, 19?2a) that the December peak in
the population cirve depicted in Figure 1 is largo]y cause -i by the
influx of an astigmatid mite, Glycyphagus sp., into the mineral soil
(see also Figure 2). This mite is phoretic as a hypopus on insects,
and this mode of life is, essentially, an opoortunistic one. Its
ability to flourish in an environment which places a premium on
opportunism indicates that it is an ‘r’ strategist.
rhe most abundant oribatid mite on this site, Joshuella striata
Wallw., ts also an opportunist. Its life cycle is geared to the
December rainfall, such that a new generation of individuals appears
at this time and in the following months of January and Febr uary
CWallwork. 19?2a). Opportunistically, J. striatc takes advantage of
the wettest mcnths of the year to produce juv€.nile stages which will
be exposed to the least environmental stress. The second most
abundant oribatid at this site, Haplochthonius variabilis %‘.allw., does
not respond with such inniedia..y to December moisture; it :ecruits
mainly in the months of April and May. In this sense, H. variabilis
appears to be less opportunistic than . st i iata oat it must be
pointed out that there is still an appreciable amount of moisture
present in the litter Zwhere these juveniles are exclusively found;
during April and May. Moreover, the temporal separation of recruitment
periods for J. striata and H. variab±lis may be Interpreted as a device
to eliminate competition between these two saprovore species. This,
$2
-------
FIGURE 1. Monthly variation in microarthropod numbers in a juniper
soil: litter end mineral sc’il counts combined (each
value is a mean of 8 cores).
Max.
rainfall (S.E.t 12%)
30
20-
C
I
a
• 10-
o N D i F M A M
Month
FIGURE 2. Monthly variation in microarthiopoa numbers in juniper
litter and mineral soil.
I
Lift.,
n
1 I I I I I I I I
‘14
I
I
44
11IHU
Millif Ii SS1
o we I P M A
M.stb
M I
761
-------
S. Usually occur in low densities which change erratically.
6. Equitability, or ‘evenness’ component of species diversity is low.
‘ K’ selected
1. Live in stable envirorunents.
2. Are late colonisers.
3. Are specialists living in competitive situations.
4. Are lo.g-lived; I,ave low reproductive rates and long development
times.
5. Have stable populations at or near carrying capacity.
5. Equitability comonent is high.
STUDY SITE
Sampling was conducted over a nine-month period in the Joshua
Tree National Mon.ament, Riverside Count , California from October 1966
until June 1967, at a site where juniper bushes provided enough
protection from wind and water to allow a permanent litter layer to
develop. A detailed description of this site, together with ecological
data on its soil microarthropod fauna hays been published previously
(WallworK, 1872a) and need not be repeatud here.
ANALYSIS AND ARGUMENT
What follows is a re-examination of the Joshua Tree data within
the broader cuncepsual framework af survival strategies. This can be
carried out tey applying, in turn, each of the six criteria listeo
above.
Stability and predictability
It has been argued (see Ncy-Meir, 1973) that the ‘level-
controlling-flows’ paradigm 1 whith adequately describes each compart-
ment in a cool, moist temperate ecosystem model is less appropriate
to hot deserts than the ‘pulRe ard reserve’ paradigm. Essentially 1
the difference between these two modules is that the former describes
continuous processes and variables, the latter discrete events.
According to the ‘pulse and reserve’ paradigm, an environmental
variable trIggers off a pulse of biological activity, of growth and
reproduction. Much of the production occurring during this time is
lost due to mortality, but some is chsnnelled into a reserve - sbeds
in the case of plants, eggs or aestivating stagns in the case of
animals. This reserve is, essentially, a nc-growth compartment from
which the next pulse of activity originates.
The driving environmental variable in hot deserts is rainfall,
and pulses of biological activity are closely linked to rainfall
events. Figure 1 clearly indicates that this is true for the micro-
arthropods in the Joshua Tree site. Here, there is an ininediate
biological response to a December rainfall manifested by a virtual
doubling of population sizes. This moisture input will have its
most obvious effect on the environment of the soil sur t ace, in this
case the lItter layer. Figure 2 shows that densities of microarthropods
760
-------
DESERT SOIL M1CROARTHROFODS AN ‘r’-SELECTED SYSTEM
John A Waliwork
Wes lfield College
Union sity of Lor.don
E ngla nd
INTROOUCTION
Hot desert soils and their inhabitants represent relatively
simple ecological systems. Microarthropods feature prominently in
such systems, and they have been the subject of incre4sing attention
by biologists during the last decade or so (Word, 197;; Wallwork,
1972a, 1972b; Edney, Franca and Mc6rayer. 1976 , Johnson and Whitford,
1975, Schumacher and Whitford, 1976, Whitforc t 1976). As a result
of these studies, much information is accumulating or the species
composition, population densities, spatial distribution, and the
role of soil animals in decomposition in hot deserts. With this
information cones an increasing awareness of the strategies which
permit microarthropods to survive in the inhospitable environment
of the hot desert soil. This paper presents a preliminary analysis
of data from one desert site, and a synthesis which suggests that
a strategy survival does exist, which conforms to that elucidated
in current ecological theory.
ECOLOGICAL STRATEGIES
Two basic, and contrasting, life styles are recognised: ‘r’
end ‘K’ strategies (Pianka, 1970). These two categories are not
absolute in that a particular species population may not fit neatly
into one or other of t,ie two: it may display attr±butes ef both.
Again, a particular taxononic group, such as oribatid mites or
Collembola, may exhibit ‘r’ selection under one set of environmental
conditions and ‘K’ selection under a different set. Again.
generalisations about an ecological system must be made with caution
since it is conceivable, for exanple. that a pr datcr may be an ‘r’
strategist while its prey may be ‘K’ strategists.
Despite these reservations, the broad concept of ‘r’ and ‘K’
life styles can be applied in the present analysis and before develop-
ing this further, it is pertinent to recall the contrasting features
of these two strategies.
‘ r’ selected
1. Live in unstable/unpredictable environments.
2. Are early colonisers.
3. Are opportunists living in non—competitive situations
4. Are short—lived; have high reproductive rates and short development
times.
759
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to occur. We have some current research on this topic in
the British Antarctic Survey.
P1. R SSALL : With respect to those species which showed
clear differences in population density between the two years
studied could you please tell us what is the average life span
of these species and could you opeculate on the reasons for
the observed differences in density?
Do the species with glycerol .n the body fluids show
seaso ial differences in glycerol content? If so, do you
know which stimuli trigger ofE the physiological response of
glycerol production?
W. BLOCK : We have no information on the life span of
these species. The between year differences (mainly a re-
duction in the second year) could have been due to a high
winter mortality. Subsequent sampling suggests that the
decline observed was not permanent.
We have sou e preliminary data which show seasonal
fluctuations in glycerol levels in the mite Alaskozetes
anarcticus . Low temperature, lowered RH levels both stimulate
glycerol production in this species.
L. BENNETT : Is the cold adaptation of Anarctic mites
aided by the sugar trehalose?
W. BLOCK : Trehalose has been found in both Collembola
and mites from the Antarctic, but there is no quantitative
information available. In general, juveniles of the crypt.o—
stigmatid mite Alaskozetes antarcticus appear to employ sugars
as well as a variety of polyhydric alcohols in their cola
tolerance physiology, whereas the adults rely almost entirely
on glycerol.
7.58
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Jennings, P.G. 1976b. Tardigrada from the Antarctic Peninsula
and Scotia Ridge Region. BuJ 1. Br. Antarct. Sury. No. 44,
77-9,.
Maslen, N.R. In press. Additions to the neaiatode fauna of the
Antarctic Region with keys to taxa. Bull. Br. Antaxct.
Sury. No. 51.
Smith, H.G. 1978. The distribution and ecology of terrestrial
Protozoa of sub—Antarctic and maritime Antarctic Islands.
Br. Antarctic Surv. Sci. Rep. No. 95, 1-1’) .
S mo , L. 1978. Notes on the cold-hardirnas of prostigmate mites
from Vestfjella, Dronning Maud Land. !iozw. J. Entomol. 25,
51-55.
Tilbyook, P.J. 1977. Energy flow through a population of the
collenbolan Cry itopygus antarcticus . Pages 935-946 in
G.A. Liano (Adaptations within Antarctic ecosystensT Gulf
Publishing Co., Houston, Txas.
Vallwoaic, J.A. 1973. Zoogeography of some terrestrial micro-
Arthropoda in Antarctica. Biol. Rev. 48, 233-259.
Walton, D.W.H. 1977. Radiation and soil tenperatures 1972-74:
Signy Island terrestrial reference sites. Br. Antarct. Surv.
data No. 1.
Wirth, W.V. & Gressitt, J.L. 1967. Diptera : Chironomidae iidges).
Pages 197-203 in J.L. Greasitt (Entomology of Antarctica),
American Geophysical Union, WashinUton, D.C. (Antarctic
Research Series, Vol. to).
Wise, K.A.J. 1967. Collembola (Springtails). Pages 123-148
J.L. Gressitt (Entomology of Antarctica), American Geophysical
Union, Washington, D.C. (Antarctic Research Series, Vol. io).
Young, S.R. 1979a. Respiratory metabolism cf Alaskozetes
antarcticua . 3. Insect Physiol. 25, 361-369.
Young, S.R. 1979 . Effect of tesperature change on the metabolic
rate of an Antarctic mite. 3. Comp. Physiol. B.
Young, S.R. & Block, V. In prep. E erimental studies c i the cold
tolerance of an Antarctic mite.
QUESTIONS and COMMENTS
K. RXCBTER : Why do mites freeze more readily with a
full gut content?
In extended constantly cool but not freezing weather
the low gut content animal is favored. Can these aniutale
survive with this limited food supply? If so, how? Wouldn ‘t
they have to extensively feed to build up reserves prior to
bruntation to survive the cold period?
. BIO i Gut contents contain ice nucleation agents.
especially small particles • and water which promote freezing
of individual mites in the supercooled state.
No, the low gut content animil is only favoured during
subzero temperatures. The Antarctic species studied to date
are able to overwinter without much food being ingested, but
reserves are prob’bly built up during sununer to allow this
757
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a
polar soil faunas have developed and colonized habitats, and
suggest the possible dispersal mechanisms employed by soil
invertebrates.
ACKNOWL&GE) NTS
I thank the British Antarctic Survey for support and
research facilities, and Drs. D.G. Goddard and S.R. Young for
allowing me to quote from their unpublished wozic.
LI IERkflJPE CuED
Block, W. 1977. Oxygen consumption of the terrestrial mite
Alaskozetes antarcticu& (Acari : Cryptostigmata). 3. exp.
Biol. 68, 69—87.
Block, W. 1979. Oxygen consumption of the Antarctic springtail
Parisotoma octooculata (Wilism) (IsotouzidLie). Rev. Ecol.
Biol. Sol. 16, 227— 33.
Block, V. & Tilbrook, P.3. 1975. Respiration studie. on the
Antarctic colimabolan Cryptopygus antarcticua . Oikos 26,
15—25.
Blocks V. & Young, S.R. 1978. Metabolic adaptations of Antarctic
texTestlial miczo-arthxopoda. Coeq. Biochmiz. Physiol. 61k,
363-368.
Block, V., Young, S.R., Conrad2.-Larsen E.-M. & Sjóiane, L. 1978. Cold
tolerance of two Antarctic terrestrial artbropods. Experientia
34, 1166—1167.
Goddard, D.G. 1977a. The Signy Island terrestrial reference sitos:
VI • Oxygen uptake of Gamaaell racovitzai (Trauessart) (Acari :
Mesostigmata). Bull. Br. Antarct. Surv. No. 45, 1-11.
Goddard, D.G. 1977b. The Signy Island terrestrial reference sites:
VIII. Oxygen uptake of some Antarctic pvostigmatid mites
(Acari : Prostigmata). Bull. Br. Antarct. Surv. No. 45, 101-115.
Goddard, D.G. 1979. The Signy Island terrestrial reference sites:
XI. Population studies on the Acari. Bull. Br. Antarct. Sur i.
No. 48, 71-92.
Gressitt, 3 .L. 1967. Introduction. Pages 1-33 in .T.L. Gressitt
(Entomology o Antarctica), American Geophysical Umon,
Washington, D.C. (Antarctic Research Series, Vol. 10).
Moidgate, M.V. 19(.4. Terrestrial ecology in the maritime Antarctic.
Pages 181-194 in H. Carrick, MW. Hoidgate & 3. r vost
Biologie antarctique), Hermann, Paris.
I{oldgate, M.W. 1977. Terrestrial ecosystems in the Antarctic.
Phil. Trans. H. Soc. Lond. B. 279, 5-23.
Janetschek, H. 1967. Artbropod cology of South Victoria Land. Pages
205-293 in J.L. Gressitt (Entomology of Antarctica), American
GeopbyE&ical Unin, WasI gton, D.C. (Antarctic Research Series,
Vol. to).
Jennings, P.8. t976a. The Tardigrada of Signy Island, south Orluiey
Isla ids, with a note on the Rotifera. Bull. Br Antarct
Sarv. No. 44, 1-25.
756
-------
field and culture. Data for this species supports the hypothesis
of cold adaptation by metabolic rate elevation (Block & Young, 1978),
in that its metabolic rate is higher than that 3f comparable
temperate species measured at the same temperature. This enables the
Antarctic mite to remain active at environmental temperatures that
would inmw ilize those temperate forms. Such an adaptation is
clearly of paramount use for this species, and similar metabolic
phenomena may exist in other Antarctic species.
Overwintering survival
The limits of cold tolerance of several Antarctic mites have
been examined (Block et al., 1978; S imne, 1978), but a detail’ d
investigation of the physiological and biochemical mechanisms
involved has only been undertaken on a single species, . ântarcticus
from Signy Island. Freezing is fatal in both juvenile and adult
stages, and survival in the field takes place by means of the
avoidance of freezing by supercooling (the inaintainancE of their body
fluids as liquids below their freezing point). Food materials in the
guts of individual mites has been shown to contain efficient ice
nuc]eators and detract from supercooling ability (Young & Block, in
prep.). Therefore animals with empty guts survive better under
freezing field conditions. Glycerol aids aupercooling in adult
A. antarcticus , and this is supplemented y other polyhydric alcohols
and sugars in the juveniles. Cold tolerance, as measured by glycerol
concentrations and supercooling points, was increased to -30° C by
exposure to low temperatures (0° to —10° C), and low relative
humidity (4 O to 60%), both of which can be related to its field
habitat.
In Antarctic springtails, which are also freezing susceptible,
similar limits of cold tolerance have been found (Block, et al. 1 1978),
but sugars rather than glycerol appecr to be the main factor for
improving their supercooling ability.
CONCLUSIONS
The species considered in this short review are seen to be
well adapted to their harsh maritime t.ntarctic environment, both in
terms of their biology, ecology and certain of their physiological
characteristics. The study of such Antarctic invertebrates is
concerned essentially with the problems of miaptat ion, and the
several facets oc the adaptational strategy which are adopted by both
the individual and the population. I4uch of what is iciown about the
ecology of such fonna suggest that they are ultimately controlled
by environmental influences rather than L+erspecific competition.
Until more information is available on the details of species
biology, especially their trophic relationships, it is both
difficult and dangerous to go further.
However, the physiological adaptations prompt various questions
such a are these mechanisms novel and evolved in response to the
polar environment, or are they merely extensions of pro-existing ones?
Future work should be comparative, not only within the Antarctic
Region, but also with aimilar forms from along climatic gradients
such as cool temperate - sub-Antarctic - maritime Antarctic - Antarctic
continental fi-.Lnge. Such studies would indicate the ways in which
7.55
-------
FMAMJJASONDJ
1973
FIGIJRS 5. Mean snow depth of SIRS 1 & 2 during 1972-74. Dotted
line repreeents approximate ice thickness.
SIRS 1
U
I
‘U
a
0
(1)
60
50
40
30
20
10
0
80
70
60
50
40
30
20
10
0
SIRS 2
J F MAMJ J ASONDJ
1972
-------
TABlE
FOOD M&IERIAL UTILIZED BY SPECIES OF ACARI AND COLLEMBOLA
IN THE FIELD AND IN LABORATORY CULTU1 8 AT SIGN! ISLAND
Type of food naterial
Species Colleinbola Acari Algae Fungal Lichens Organic
NESOSTIGMTA hyphae debris
Gamaaellua racovitzai + +
CRYPTOSTIG MATh
Alaskozetes antarcticus + + + +
Halozetes belgicae + + + +
ASTIGMAI’A
Neohyadesia signyi +
PROSTIGMATA
rnodes ininutus + +
Ereyne-tes macguariensis + +
Stereotydeus villosius +
Nanorchestes antarcticus +
Tydeus tilbrooki + + +
ISOTONIDAE
Cryptopygus antarcticue + + + +
-------
For C. antar ticus , ilbrook (1977) recorded a stable size
class structure xoi the Signy Island population with few seasonal
changes.
Few details of the feeding ecology of Antarctic soil
arthropods exist. Observations at Signy Island sugUest that algae
and fungi are favoured by the majority of the Acari especially the
prostiç matidz (Table 5) • Current work on C. antaroticus is to
determine qualitative food preferences and measure ingestion and
assimilation rates at field temperatures, whilst that on the
predator, . racovitzai , is investigating its interaction with various
prey organisms.
Microclimate
S2asonal fluxes in solar radiation, au temperature and soil
temperature at five points in the vertical profile of the SIRS moss
peat have been given by Walton (1977). Temperature is a major
determinant of arthropod activity, which on Signy Island is limited
to C. five months of the year (November to March) • The microclimate
of the surface layer of the sites is characterized by short periods
of high insolation with temperatures of up to +25° C being recorded
in some situations 1 which are often associated with raptd temperature
changes (1° C mm is caisson) . Much longer periods of fairly
constant low temperatures occur especially after a snow cover has
been established (Figure 5). Snow depths vary between sites and
between years, and up to I m may occur on bryophyte communities in the
maritime Antarctic. At melt, greenhouse conditions may prevail
locally, which encourage plant growth and invertebrate activity wader
the ice layer.
Of major importance for such communities are the frequent
freeze-thaw cycles, which are a feature of both spring and autuami
conditions. Substrate water content changes markedly with season
particularly in peat sites. Annual water contents in respect o’ ’ core
dry weight were 609-666% (SIPS 1), and i480 -i8 2% (SIPS 2) for
1972 and 1973 respectively.
PHYSIOLOGY
The maritime Antarctic environment presents certain
physiological problems to poi.kilotherms inh .biting it. Low temperatures
may depress respiration rates, activity, feeding and growth, whilst
wide thermal fluctuations may result in large variations 3.n metabolic
rates. Extreme winter tmi eratures may cause tissue freezing.
Respiratory metabolism
A considerable body of data now exists on the respiratory
levelE of many Antarctic arthropods. For Collembola, Block &
Tilbrc.ok (1975) a’rn Block (1979) detail results far C. antarcticus
and Parisotoma octoo ulata (Wiliest) • In the Acari, Goddard (1977a,
1977b) gave information on G. zacovitzai and the Prostigmata
respectively, whilst Biuck T19 J and Young (1979a, 1979b) reported
on the respiratory metabolism of the oribatid A. antarcticus in
752
-------
TABLE 4
POPU lATION Pi SPIRATION OF LIPS 1 ACARI AND COLLZMBOLk ( ml. 02 m 2 y )
Year
Species 1972 1973
Ereynetes i cuu.irien is 82.17
Eupcides mirn u ‘ 3.87 29.91 ,
Nanorcheste aiitarcticuz 81.40 70.72
Gnmasellus racuvitza 12.49 4.52
Total Ac arj 219.93 129.18
Total Co11eniI, 1a
Cryptopyqu ntarcticus 893.35 685.84
7.5].
-------
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iUI li. Mfe stage con oajtion of four species of Acari on SIRS I
during 1972 -74.
750
-------
70
60
50
40
30
20
10
0
10
8
6
4
2
0
10
8
6
4
2
0
50
40
30
20
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FIGURE 3.
Live weight bioinass changes in populations of four mite
species on SIRS 1 during 1972—74.
Gamasellus racovftzai
Eupodes mm Ut us
I
Ere ynetes macquariensis
Nanorchestes antercticus
J EMAM J JASONDJ FMAMJ JASOPJDJFM
1972 1973 1974
e9
-------
Population biomass
Total acarine biomass varied from 23.0 tc 38.2 mg 1..ve
for the two year study. Of this G. racovitzai contributed 44 and
57% respectively, the remainder being made up of the three prostigmate
species. Following the decline in population density, the live
weight mite biomass decreased by c. I 0% from 1972 tG 1973 (Figure 3).
For C. anj e.rcticus, ltve weight biomass varied from
to 1,124.8 ing in during 1972, with an annual mean of 793.4 ing in
which was 26 times greater than the Acari.
On an individual live weight basis the species ranged in the
following order: E. minutus and E. macquariensis (0.3 - 2.0 &g),
N. antarcticus (0.2 - 8.5 p.g), Stereotydeus villosus (Troueasart)
37.1 pg), G. racovitzai (4.4 - 115.5 pg).
Population respiration
Calculations of annual species population respiration have
been made by a computer progranmie using data for monthly population
density, life stage composition, live weight bicinass, mean daily
field temperatures and the relation of inctabolic rate (weight
specific oxygen uptake) to temperature for each species of arthropod
on SIRS 1.. Daily population respiration values were calculated and
sunmied for annual estimates (Table 4) . Differences in respiratory
activity occur between species and years, the former governed
principally by the metabolism - temperature curve and the latter
by population density levels. Between year changes are ezhibited
by the total Acerj. data, the 1972 estimate being 1.7 times higher
than the 1973 level. The total oxygen consumed by the Acari was
almost all used by the Proatigmata. The Collmnbola (entirely C.
antarcticus ) contributed 8C-84% of the total soil arthropod
respiration for both years.
Life cycles and feedtn
I : oxination on life stage composition (Figure li) ha.’ been
obtained by Goddard (1979) and other w rkera for mites and by
Tilbrook (1977) for springtails in th. maritime Antarctir. In the
Acari, several species have been observed to lay batches of c gs in
spring and early summer, whilst others oviposit throughoi t the
st er period. Larvae arc abundant only in simmer, whil t large
numbers of mymphs of all stages are found at all seasons. The
duration of the nyniphal stages is variable, even within a sj ecies,
which results in a mixed stage nyipphal component of the popui.at ion.
From such a nymphal pool, varying numbers Of individuals mature to
adult influenced primarily by environmental conditions. Nymphs have
been found to be more cold tolerarLt than adults in the oz-ibatid
Alaskozetea antarcticus (Michael) by Young & Block (in prep.), and so
n7mphal mortality may be low. I terms of time, 12 to i8 we cs front
egg to adult have been observed for Tyieus tilbrooki (Strandtmnarmn) at
laboratory temperatures (Goddard, 19791. Under field conditions it
may take at least one year for . antar’-ticus to reach s ia.g. matu.iity
with a further 9 to 12 months of adult life. Life cycles are
therefore variable in duration dependent upon site and microclimate.
7k8
-------
TABLE 3
ANNUAL MEAN POPULATION 1 N5ITIES FOR FOUR CONNON SPECIES OF ACARI
AND COLLEMBOLA FOUND IN TI SIRS I SAMP lES
-2
Nunibera of uidi.y duals n
Year Nanorchestea Ereynetes Eupodes Gamaseflua Total Total
antarcticus macciuariensis minutus racovitzai Acari Collembota
1972 3,376 2,752 3,877 10,469 60,410
1973 1,278 1,086 3,144 469 5,977 36,182
1972
and 2,327 1,919 3, O 8,223 48,296
1973
* Entirely yptopy ua antarctiais
-------
TABLE 2
SPECIES OF ACARI AND COLLENBOIA RECORDED FOR
TWO 1’l)SS SI JES AT SIGNY ISLAND, MARITINE ANTARCTIC
ACARI
Crypbostiginata 2 species Alaskozetes ant ctic (Michael)
Halozetos belgicae (Michael)
Mesostig ata I specie Gainasellus racovitzai (TrouLasart)
Prostigmata 6 species Nanorchestes ant arcticus (Strandtmann)
odea minutus (Str ndtmann)
Halotydeus si!niensls (Strandtinann)
Ereynetes inacquariensis (Fain)
Stereotydeus villosus (Troucasart)
Tydeus tilbrooki (Strandtinann)
Astigmata I species Neocalvolia q ctica (Hughes & Tilbrook)
COL1ENBOIA
3 species Cryptc pygus antarcticus WilIem
Frisea grisea (Schaffer)
Parisotonia octooculatn (Willein)
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FIGURE 2.
Vertical distribution of Acari in 2 * cm deep cores on
SIRS 1 (two winter and two sunmier 3ample 1) together
with water content as percentage of core dry weight.
4’
r
r
-------
FIGURE 1. Seaagnal I iu tuaticsis in mean population donsity
( 1O md m ) on SIRS I durinQ 1972-74. Monthly
mean vai es (*SE14) are plotted frog Goddard, 1979.
I 72
-------
This review will consider aspects of the ecology and
physiology of micro-arthropods Living in these coumnmities, which
highlight their adaptations to the environn ent of the maritime
Antarctic. These include features of their populations, life cycles,
respiratory metabolism and cold tolerance.
ECOLOGY
Species composition
Consideration of the arU ropod species list (Tabl 2) for the
two moss sites at Signy Island shows a typical structure with the
majority of the fauna comprised of prostigmatid mites, three
collembolans, two crypto tiginatids and a single mesostigmatid
predator. In general, a species poor and much simplified arthropod
connmmity than that found in temperate habitats.
Population densitj
The moat numerous species present on the SIRS (Table 3) is the
ubiquitous ?prir gtail Cryptopygus antarcticus Willem, which over a
two year study 2 period maintained a mean population of 8,296
individuals m , six times as many as all the Acari. The Acari
averaged c. 8,223 individuals m for the same period. Between year
differences occurred in two species of Prostigmata, NanJcheates
antarcticus (Strandtmann) and Ereynetes macquariensis Fain), which
showed over 50% decline in numbers during the second year. Eupodes
minutus (Strandtmann) and Gamasellus racovitzai (Trouessart)
maintained fairly constant numbers for 1972 and 1973.
Seasonal changes in mite population density were recorded
(Figure 1, from Goddard, 1979) which followed a pattern of low
numbers in winter with high sui er numbers. 6. racovitzai was the
only species which had similar yearly cycles of abundance, which
may be related to its predatory role in the community. Few seasonally
related changes occurred in the collmnbolan population of this
site (Tilbrook, .977).
In terms of vertical distribution, most Aca.ri and Collembola
were found in the uppermost layer of the moss peat profile, except
during winter when a reversal of the proportion of the total mite
population in the 0-3 an and -6 cm layers occurred. . antarcticus
was consistently (80-90% of its population) in the 0-3 cm stratum
throughout the year, whilst E. macquariensis was found mainly at
cm. Deeper core samples collected on four occasions (Figure 2)
revealed that Acari did not penetrate beyond 18 cm in the profile,
and confinned that E. macquariensis was a deeper dwelling form than
the othez species present. Little information exists on the
horizontal distribution of the micro-arthropoda on these sites, but
they appear to be highly aggregated especially during spring and
the early part of the austral st er.
3
-------
TABiJE 1
SOIL INVERI BRATES OF MARITIME ANTARCTIC HABITATS
N. of species recorded Distribution Reference
Protozoa 12& Ubiquitous rnth, 1978
Rotifera Number unknown but Adirieta, Mainly in wet moss Jennings, 1976 a
other Bdelloidea, and communities
Nonogononta recorded
Tardigrada 11 Wet moss communities Jenr irgs, 1976 b
Nematoda 40 Ubiquitous Maslen, in press
Enthytraeidae 2 ? Organic detritus in Block, unpublished
South Shetland I lands
Colleabola 8 Ubiquitous Wiee, 1967; Wallwoxic, 1973
Diptera 2 South Shetland Tjlands, Wirth & Gresaitt, 1967
Antarctic Peninsula
Acari 40 Ubiquitous Gressitt, 1967; Waliwotlc, 1973
Mesoatigmata 9
Cryptoatigmata 16
Astiginata 5
Pro gmata 10
-------
ASPECTS OF THE ECOLOGY OF ANTARCTIC SOIL FAUNA
William Block
BriIi h Antarctic Survey
England
INTRODUCTION
The Antarctic Region can be divided into ecological zones
(Holdgate, 196 ) including the sub-Antarctic, the maritime and
continental zones. This paper is concemed with the maritime
Antarctic zone south of 600 latitude. The majority of land habitats
seasonally free of snow and ice occur here and hence its importance
to the soil fauna. It is also an area in which nuich of the
Antarctic soil biological work has been undertaken. The maritime
Antarctic zone south of 600 latitude includes the South Or4aiey and
South Shetland Islands, together with Adelaide Island find the west
coast of the Antarctic (Graham Land) Peninsula and its offshore
islands.
Apart from the microbial groups (fungi, yeasts and bacteria)
in maritime Antarctic soils, there are eight invertebrate groups
represented ranging from Protozoa to higher 4 isects (Diptera).
Table I presents the numbers of species found to date for these
groups. Due to their wide distribution tZuoughout the maritime
Antarctic and the increasing body of information about then, this
paper will concentrate on the arthropods in general and on the mites
(Acari) and springtails (Colleinbolq.) in particular. Such soil
inicro-arthropods penetrate further south than most other invertebrates,
and exhibit ecological features and adaptations to the environment,
which may be considered typical of the Antarctic soil fauna generally.
The soil fauna is the dominant terrestrial component, there being no
permanent land dwelling vertebrates and above ground invertebrates
are generally absent. There is considerable variation of terrestrial
habitats within the maritime Antarctic, and Holdgate (1977) has
discussed this in detail. Briefly, invertebrate soil communities
axe fouud in a range of habitats from exposed felifield types
(similar to the chalikosystem of Janetachek, 1967) to the closed moss
dominated (bryosystem) in addition to relatively wi a1 1 areas
covered by flowering plants (the grasø DeschAmpsia antarctica Desv.
and the cushion plant Colobanthus crassifolius (D’Urv.) Hook.f.
) zch of the iraformation reviewed here has been collected from
bryophyte coimmmities on Sigziy Island in the South Orimey Islands,
where a.rthropoda occur in relatively large numbRrs and the fauna is
comparatively diverse. Two sites have been investigated in detail:
SIRS (Signy Island Reference Site) 1 and SIRS 2. The former is a
fairly dry moss turf composed of Polytrichuin alpestre Hoppe and
Ch...orisodontium acipityliwu (Hook.f. et Wils.) Broth., whilst the
latter is a reittively wet moss carpet composed of Callier on
sarinentosum (Vahlenb.) Kindb., Calliergidium austro-stramineum
TC. ell.) Bartr. and Drepanocladus uncinatus (Hedw.) Warrast.
-------
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Ecosystems. Springe -Ver1ag, New York.
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djurforiner. Medd. Statens SkoqsfOrsOksanst, 34: 341—364.
Gilyarov, M.S. and N.G. Bregatova (Eds.). 1977. A key to
soil—inhabiting mites. Mesostiginata. Nauka, Leningrad:
718 pp.
Hammer, M. 1952. Investigations on the microfauna of northern
Canada. Part 1. Oribatidae. Acta Arct. 4: 1—108.
Hammer, M. 1955. Alaskan Oribatids. Acta Arct. 7: 1—36.
Hill, S.B. 1969. The Ecology of Bat Guano in Tamana Cave,
Trinidad, W.I. Unpublished Ph.D. Thesis, Univ. West
Indies, Trinidad: 310 pp.
Hinsheiwood, C. 1951, Decline and death of bacterial
populations. Nature (Lond.), 157: 666.
Hudig, J. 1949. Nitrogen production and utilization. Nieuwe
Veldbode, 16: 77-90.
Hultén, E. 1968. Flora of Alaska. Stanford University Press.
xi and 1008 pp.
Hurd, P. 1958. Analysis of Soil Invertebrate Samples from
Barrow Alaska. Final Report Project ONR—173 and ONR—193.
Arctic Institute of North America: 24 pp.
Ives, J.D. 1974. Biological refugia and the nunatuk hypothesis.
Pages 605-636 in Ives, J.D. and R.G. Barry (Eds.), Arctic
and Alpine EnviFonments. Metheun, London.
Janetschek, H. 1949. Tierische Successionen auf hochalpinem
Neuland. Schlern—Scnr. 67: 1—215.
Janetschek, H. 1958. Uber die Tierische Wiederbeniedlung im
HornkeesVorfeld (Zillertaler Alpen). Schlern—Schr. 188:
209—246.
7,7
-------
Atyeo, W.T. 1960. A revision of the mite family Bdellidae
in North and Central America (Acarina, Prostiginata).
Univ. Kane. Sci. Bull. 8: 345—499.
Banks, N. 1919. The Acarina collected by the Canadian Arctic
Expedition 1913—1918. Rep. Can. Arctid Exped. 1913—1918.
3: Hart. H:ll—13.
b han, V.M. 1978. Distribution, Diversity and Feeding Habits
of North American Arctic Soil Acari. Unpublished Ph.D.
Thesis. McGill Univ. 428 pp.
: han, V.M., S.B. Hill and D.K.McE. Kevan. 1978. Effects of
nitrogen fertilizer, as urea, on Acarina and other
arthropods in Quebec Black Spruce ( Picea mariana Mill.)
humus. PedobiologLa, 18: 249—263.
Blake, W. Jr. 1970. Studies of glacial history tn Arctic
Canada. 1. Pumice, radiocarbon dates and differential
post—glacial uplift in the eastern Queen Elizabeth Islands.
Can. J. Earth Sci. 7: 634—664.
Bohnsack, K.K. 1968. The distribution and abundance of the
tundra arthropods in the vicinity of Pt. Barrow, Alaska.
Final Report to Arctic Institute of North America.
Subcontracts, ONR-308, NR-32l. Wa thington, D.C. 111 pp.
Brassard, G.R. 1971. The mosses of Northern El.i.asmere Island,
Arctic Canada. 1. Ecology and Phytogeography, with an
Analysis for the Queen Elizabeth Islands. Bryologist,
74: 233—281.
Crossley, D.A. and M. Witkamp. 1S64. Forest soil mites and
mineral cycling. Acarologia, 6: 139—146.
Danks, H.V. and 7.R. Byers. 1972. Insects and Arachnids of
Bathurst Island, Canadian Arctic Archipelago. Can. Entomol.
104: 81—88.
Douco, G.K. 1973. The population dynamics and community
analysis of the Acarina of the Arctic coastal tundra.
Unpublished M.Sc. Thesis, Univ. Georgia. Athens. 69 pp.
Douce, G.K. 1976. Biomass of soil mites (Acari) in Arctic
coastal tundra. Oikos, 27: 324—330.
Douce, G.K. and D.A. Crossley Jr. 1977. Acarina abundance and
community structure of the Arctic coastal tundra.
Pedobiologia, 17: 32—42.
Downes, J.A. 1965. Adaptations of insects in the Arctic. Ann.
Rev. Entomol. 10: 257—274.
736
-------
data, a more gradual decrease in diversity from low to high
arctic is evident (Table 5). This suggests that some of the
four-fold decrease in diversity is a result of difficulties
in dispersal from mainland to island sites.
While there is a ten—fold decrease in oribatid and
mesostigmatid diversity between subarctic and polar desert,
there is only a four—fold decrease in Prostiginata. On the
basis of what is presently known of Prostigmata survival
capacity, tolerance of low relative humidity, st orter life-
span and greater egg-layirg capacity than that of Oribatet,
they can be considered r—strategists a’2d can probably invade
more arid environments than Oribatei (Atyeo, ‘.960; Jeppsor
Reiier and Baker, 1975; Douce and Crossley, 1977).
If the dimension of geological time is included in the
gradient from subarctic to polar desert, there is the added
factor of decreasing years since glacial retreat. Polar
desert sites can, therefore, be considered as youthful seral
stages in the tundra biome (McAlpine, 1964; Dunbar, 1968).
In such areas, successful species tend to have the biologicaa.
characteristics of Prostigmata (Margalef, 1975). In the
Antarctic, Pros tigniata are ulso the dominant acarine group and
are represented by the same families as in arctic polar
desert: Nanorchestidas, Eupodidae and Rhagidiidae (Janctechek,
1967).
The ratio of population density of Acari to Collembola
decreases in general along the latitudinal gradient from
subarctic to polar desert. In the Alps, Janetschek (1949,
1958) demonstrated that in the first stage of recolonization
after the glacial tongue has withdrawn, Collembola are
predominant. He observed that as the habitat matured and its
soil and vegetation developed, Collembola decreased in density
relative to mites. Collembola are also numerically dominant
in all habitats in the antarctic (Janetschek, 1967, 1970).
This overall predominance in cold desert localities is probably
related to their short life-span and high intrinsic rate of
increase (Douce and Crossley, 1977).
LITERATURE CITED
Alexandrova, V.D. 1970. The vegetation of the tundra zones
in the U.S.S.R. and data about its productivity. Pages
93-114 in Fuller, W.A. and P.C. Kevan (Eds.), Productivity
and Conservation in Nc’rthern Circumpolar Lands. IUCN
Pubi. 16, Morges, Switzerland: mt. Union Conserv. Nat.
735
-------
T&BLE 5. Changes in density and diversity of arctic soil Acari with latitude from subarctic to polar
desert.
Acari
Zone
C
Zone B
Zone A
Polar Desert
High
Arctic
Subarctic
Low Arctic
Number of Species
163 (9.6)1
84 (3.7)
78 (9.8)
140 (8.2)
87 (3.8)
63 (7.9)
With
Point Barrow
Without ,
Point Barrow
17 (1)
23 (1.)
8 (1)
Oribatei
Prostigmata
1 ’lesostigmaca
48 (2.8)
54 (2.3)
26 (3.3)
36 (2.1)
40 (1.7)
19 (2.4)
Total Acari
325 (6.8)
1.1:1
2.1:1.
1.9:1
290 (6.0)
1.4:1
2.2:1
1.6:1
128 (2.7)
2.1:1
1.8 l
0.9:1
95 (2.0)
2.1:1
1.9:1
0.9:1
48 (1)
2.9:1
2.1:1
0.7:1
Ratios
Prostigmata:Hesoscigmata
Uribatei:Hesostigmata
•OribaLe!i: ’rostigmata
Diversity expressed as a ratio of polar desert diversity.
2 liigh arctic sites that are all Insular.
3 Iligh arctic areas including the mainland site, Point Barrow, Alaska.
-------
TAIL! 4. St..sry of ch. . . in ablotic and blo tic factors vith latitude Ire. subarctic to polar 4sosrt.
F*çtors
Zoos C
ZOO I
ctjc High Arctic
Zen. A
Po t Dssart
AbioUc 1
Subarctic
Low Ar
Nat Rodiation
Aosual Precipitation
positive
100 os
— — — — —
—
— — nr ati n s
10 co
Annual T°C
positive
P [
— — —
—
— — —16°C
1
Stotic —
250-500
100—200
0—100
Nat production Fi . 2 /yr.
Net production
($rouin season)
Abov.:Below roosd biasass
Nooses
2
Li sns
of
Woody plants
5
1:4.55
1:7.2 [
44 *
1$
• 16
1:4.83
31
60 —
2
34
65
0
vs$.t.tion
Hsrbacoous
4
22
4
liocic - Aniosi
Oribats i
163
140
3 — -
‘
— 17 10*
No. of Prosti ata
84
8’
“ 40 —
23 37*
Species Woao.tigzata
78
63
19
— $ 10*
Total
325
290
95—
4$
Acari:Co lbosbole
Oribat.i:Prow t ijn.ta
p.r tins
poaitivs
fls tiv.
o stive
•
Gso loica l
Tt _
TIm. sinc, last Jacia.
Wbb.r (1974).
733
-------
7 ’)
TXcU Oa. 0Oa1$O$ of thi North Iricm .retic on tk• riGuft 6 b. gonulon of 16. North srIcon .rcn*c on thi
hosts of thu Poll Acstt. boils of its vs sts1to* (AluiPodrova 167S)
rIGIJU I e. bombs of thu North husnicis arctIc on 16.
hosi. of fbort cq iYouo l 71).
-------
Inconsistencies between the two zonations are:
a) Inclusion of the northern half of Ellesmere Island in
Zone 1 (Figure 6b). Based on both the acazine fauna
and vegeta’ion analysis (Brassard, 1971), this area should
be included in Zone 2.
1,) Somerset Island is included in Zone A (Figure 6 a) - Samples
from this site were, however, from a restricted coastal
area. Further study of this site may alter the present
data on acarine diversity.
C) The lower limit of Zone 3 (Alexandrova, 1970) and Zone 4
(Young, 1971) is treeline. No such definite boundary is
evident in zonations based on the mite fauna (Figure 6 a).
Although, in the present study, species are found in
subarctic and not in arctic localities, there is generally
a closer similarity between arctic and subarctic sites in
the same geographical location than between arctic sites
in general. Treeline, therefore, apparently has little
affect on soil mites, except the inacrophytophagous Phthiraca—
roidea, which are common in coniferous litter and rare in
the arctic.
All of the Acari in Zone A have a ciraumpolar distribution
similar to the plant species (Young, 1971).
They tend to be species of common occurrence in a wide variety
of habitats throughout arctic regions. In Zones B and C the
percentage of circumpolar species decreases rapidly.
GENERAL DISCUSSION AND CONCLUSIONS
The survey of changes in diversity and density of arctic
soil Acari, recorded in this study, with changes in latitude,
is summarized in Table 4. In subarctic localities, as in most
temperate areas, Oribatei are the dominant component of the
soil Acari. Oribatid dominance continues into low arctic sites,
but, as the environment becomes increa& ing1y harsh, there is a
rapid drop in oribatid diversity and Prostigmata take over as
the dominant group. The overall decrease in mite diversity by
a factor of seven from subarctic to polar desert is correlated
with L icreasing severity of abiotic factors and decreasing
annual primary productivity.
The four-fold decrease in both oribatid and niesostigmatid
diversity from low to high arctic is more marked than the
decrease from either sukarctic to low arctic or high arctic
to polar desert. In the present study high arctic sites are all
insular, as Point Barrow, a high arctic site (Douce and Crossley,
1977) was not considered separately from northern coastal arctic.
If species that occur at Point Barrow are included in the high wctic
731
-------
Tabls 3. S4russ.&o Iad.x of •1ot1arit for 31 sItog is tk North Asoricin arctic sad iv arcttc sad ,iotth.ra ewmotkd, US$1.
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-------
FIGURE 5
Hierarchical classification of 37 sites in the
North American arctic and subarctic and northern
Chukotka, U.S.S.R., based on SØrensen’s index of
similarity.
O/ Similarity Sites
0 10 2Q 30 40 50 60 70 80 90 1 )
‘ 29.0
Nunivak Island
Pribilof Islind.
Aleutian Island.
Soutliw. .tori
Coa.tai area
Lhaun Bay
Chugath Ntns. and
£ naL Peninsula
Neilinicy Park
Brook. Range — N. Foothill.
Brooku Range — S. Foothill.
Brook. Range
Fairbanks Region
Nort leae blcrn
Coa.tai Area
Noz tbelrn Coastal Plain
A tk asuk
5 5Sf in 7.land
MacMenu. Delta - .ubarctic
riecxeijuje Delta
.nioaula
Yukon Terratory
lorth.rn Qi. b.c
Keewatil i
Nerechel laland
Victoria I.iand
Banke I.lAnd
Devon lalend
Bathur.t leland
Melville Island
Ell e..er . Islau.I
Igloolik lalanu
Lilef RSqne. Island
labrador - .ubarctic
Sou .rSSt I da h O
Marth Rent l.land
Ward Runt l.Iand
Sey ur I.land
sing Chriatian I.land
AMel Moib.rq Zatand
3
I
‘I
I
S
I
-
Zone
Zone
C
Zone
B
Zone
A
729
-------
FIGURE 4 • Ratio between the number of individual mLtes and
Collembola at 17 sites in the North American
arctic a d subarctic and northern C) uJcotka,
U.S.S.R.
Ratio
Acari to
Collembola
desert sites
High arctic and polar I i— Low arctic and subarctic
Sites
I
it’ll
U,
a
C l ) Z o 5 Cl) Z U _ z
1 Abbreviations as in Table 1.
-------
to Collembola ratios are available for 16 sites (Figure 4).
Although results are not statistically significant, the ratio
tends to be Lowest in mid to high arctic and polar desert
localities. Bathurst, Devon, Igloolik and North Kent Islands,
for example, have a ratio of less than or approximately one.
Previous studies from arctic localities support these results
(Douce, 1973; Watson et al., 1966).
Community Analysis Between Sites
SØrensen’s quotient of similarity (SØrensen, 1948) was
used to determine affinities between arctic and subarctic sites
on the basis of the mite fauna of each site. Species lists from
36 sites were analysed, 34 from the present study and data
from Ellef Rignes Island (McAlpine, 1965) and Melville Island
(Lindquist, in lit., 1977). Where species other than those
recorded in the present study are known to occur at a
particular site, they were included in this analysis. Indices
of similarity for the 36 sites are given (Table 3), sites
having a high similarity being adjacent.
A hierarchical classification using data from Sørensen’s
quotient of similarity (Table 3) was developed based on the
formula of MountfGrd (1962) (Figure 5 ). This shows that
western Canadian arctic sites are most similar to laskan sites,
which is expected based on the Pleistocene history of the
western arctic (Hultén, 1968). These combined groups are more
similar to the Soviet arctic than they are to islands in the
arctic archipelago. The one exception is Baf fin Island, which
has a particularly rich acarine fauna.
Islands of the extreme northwestern arctic, although
showing low affinity to each other, do form a group separate
from other arctic sites. Similarly, the Aleutian, Pribilof and
Nunivak Islands form a loosely knit group, separate from other
arctic and subarctic localities (Figure 5 ).
Groups delimited ii Figure 5 can be used to divide the
North American arctic into zones (Figure 6 a). This zonation,
based on the acarine fauna, can be compared with that of
Alexandrova (1970) and Young (1971). Alexandrova divided the
arctic into: Zone 1 — polar desert; Zone 2 high arctic;
Zone 3 - low arctic (Figure 6 b), based on the floris tic
composition. Young divided the arctic into four floristic
zones defined on the basis of the northerly distribution of
certain vascular plants (Figure 6 C).
As mites are directly or indirectly related to the
vegetation in an area, there should be some similarity between
zonations based on similarity of acarine species and those based
on vegetation patterns. Zones 1 and 4 of Young (1971)
correspond to Zone A and C of the present study and Zone 2
and 3 approximate Zone B. Zonat-ions in the present study,
however, most closely approximate those of Alexandrova (1970).
727
-------
FIGURE 3.
Ratio of
number of
Species of
Oribatei to
Prostigmatá
Ratio between riurber of species of Oribatei and
Prostigmata for sites in the North American arctic
and subarctic and northern Cbukotka, U.S.S.R.
6 i— Low arctic and subarctic
1
Abbreviations as in Table 1.
High arctic
—
<>zz
-------
Qribatei
Prost igr ata
Mesoetigmata
FIGURE 2. Total number of acarine species and the number of
species of Oribatei, Proetiginata and Mesostigmata
at 35 sites in the North American arctic and sub-
arctic, and northern Chukotka U.S.S.R.L
Abbreviations as in Table 1.
a
CmKp
KPM) FR
Number
Of
Spec ee
50
40
30
20
I0
0 Total number of species/site
1
-------
C. guadridentata var. arctica on Victoria Island
ts the only record of this genus in the arctic islands, which
suggests that the family is not tell adapted to high arctic
and polar desert environments.
Quantitative Results between Sites 1
Total number of acarine species and number of species of
Oribatei, Prostiginata and Mesostigmata at each of the 34 sites
is superimposed on a map of northern North 1 inerica (Figure 2).
There is a decrease in number of species with increasing latitude.
Causes incThde, the shorter post—glacial period, increasing
climatic harshness and decreasing food reseurces for the mites,
associated with reduced vegetation. Exceptions to this are
Baff in Island and Ellesmere Island.
The climate of the southern part of Baffin Island is milder
than that of other islands in the arctic archipelago. Subarctic
conditions exist in the extreme south of the island, although
parts of the north are still glaciated. Baff in Island is also
situated in proximity to Greenland.
Ellesinere Island may have partially been an ice—free
refugium during the last glaciation (Blake, 1970). Brassard
(1971) found 151 species of moss in northern Ellesmere Island,
50 per cent of which are rare.
Ratio of Oribatei to Prostigmata
Douce (1973) working at ioint Barrow was the first to
demonstrate the importance of Prostigmata at a high arctic site.
In the present study, the majority of high arctic and polar
desert localities, such as Bathurst Island, King Christian
Island, Seymour Island, Somerset Island, northern Ellesinere
Island, Devon Island and Igloolik Island show greater diversity
of Prostigmata than of other acarine groups (Figure 3).
Axe]. Heiberg Island and North Kent Island are exceptions
possibly because of the small number of samples taken at these
sites. In mid to low arctic and subarctic habitats Oribatei
are more diverse than Prostigmata (Figure 3).
Ratio of Acari to Collembola
The ratio of numbers of individual mites to Colleinbola in
soil faunal studies is generally positive (Forsslund, 1945;
Murphy, 1953; Behan et al., 1978). Zn the present study, mite
1 These results are based on raw data because of variability in
a) sampling methods, size of samples, sampling personnel and
time between sample collection and extraction; b) types of
habitats sampled at each site. As a result only minimal
statistical analysis could be carried out.
72J
-------
The oribatid fauna of both the Canadian and Alaskan
arctic more closely resembles that of the Soviet arctic than
that of Scandanavia or northern Greenland (Table 2). At the
present time, data concerning Mesostiginata and Prostigmata
are inadequate to make similar comparisons.
The western arctic, comprising the Alaskan arctic and
arctic regions of the Yukon Territory and MacK anzie Delta,
supports a more diverse mite fauna (331 species) than the
eastern arctic (199 species)- This may be
explained by: a) the northerly extension and island pattern
of the eastern arctic that have presented difficulties to
post-glacial invasion by Acari; b) treeline sweeps far to the
north in the west, e.g., in the MacKenzie Delta it reaches
69 0 50’N. In the eastern arctic treeline is found as far south
as 60°N and the arctic archipelago is treeless; c) there is
strong biological and geological evidence for the presence of
ice—free areas in north and central Alaska during the two
most recent glaciations, the Illinoian and Wisconsin (Ives,
1974; Matthews, 1975).
Diversity of arctic acarine genera and species between sites
Certain genera are strongly represented in the arctic in
comparison with other genera, more so than could be expected
if the arctic fauna is solely a reduced southern fauna, as
hypothesized by Downes (1965) for insects. Eleven species of
Arctoseius , 12 species of Epidamaeus ,
and 5 species of Trichoribates , occur in the arctic.
This suggests that these genera were particularly capable of
adapting to post—glacial conditions.
The family Arctacaridae was first described from Point
Barrow, Alaska (Evans, 1955). As two other species have been
described from the eas torn Soviet Union (Gilyarov and Bregatova,
1977) this family may have an east Asian or Beringian origin.
in this study its distribution is restricted to the western
arctic and subarctic, other than a single record from Keewatin
District. Absence of this family from the arctic
islands is probably a result of distributional rather than
environmental difficulties, as its abundance at Point Barrow
suggests that it is able to survive in the high arctic.
lugoribates gracilis , previously unrecorded from northern
Canada, has been recorded from almost all sites, particularly
those with high arctic or polar desert environments.
The genera Ceratoppia, Metrioppia and Pyroppia (Family
Metrioppiidae) are well represented £ the western arctic,
particularly in Alaska. The latter two genera have
no representatives in the eastern arctic. The occurrence of
723
-------
TABLE 2.
Similarities between arctic Acari from Nearctic and Palaearctic Regions.
% Canadian Species Recorded In:
Acarine
Groups
Oribatei
Mesostigmata
- Prostigmata
Alaska
69.0%
35.0%
49.0%
Northern and Western Greenland
30.0%
(39
spp.)
—
—
Scandanavia
35.6%
(46
spp.)
—
-
Soviet Union arctic
39.0%
(50
spp..)
—
—
% Alaskan Species Recorded In:
Northern and Western Greenland
27.5%
(41
spp.)
-
—
Scandanavia
33.0%
(49
spp.)
—
•
Soviet Union arctic
42.0%
(63
spp.)
—
—
-------
METHODS
Samples for this study exe collected by many arctic
researchers and this precluded any overall sample uniformity.
Most samples were less than 10cm x 10cm and in any particular
habitat a uniform sample size and sampling method were used.
Samples were usually cut with a knife and removed from the
ground with a spade, or, less frequently, the ground was sampled
with a 5.5 cm diameter corer. In many habitats, for example,
screes, talus slopes and high arctic localities, where the
active layer is less than 2cm in depth, a handful of this layer
was removed. Thus, samples were not directly comparable because
of variability in collecting personnel, sampling methods and
habitats. Samples were placed in plastic bags immediately after
collection and were extracted either immediately, or one to SiX
weeks later, after storage at a cool temperature.
Extraction was carried out in a modified (Hill, 1969;
Behan, Hill and Kevan, 1978) Ksmpson, Lloyd and Ghelardi (1963)
apparatus. Each sample was divided into 2.5cm deep subsamples
where necessary.
RESULTS AND DISCUSSION
Qualitative Results
Three hundred and ninety—three species of Acari from 87
families were recorded from the 833 samples from the North
American arctic and subarctic. These include 181
species of Oribatei from 78 genera, 10]. species of Mesostigmata
from 40 genera and ill species of Prostigmata from 45 genera.
Of the species recorded 52 were found only in subarctic
localities and 95 only in arctic areas. Three
species recorded at Chaun Bay. U.S.S.R. (MacLean et al., 1978)
were not recorded from the North American arctic - E phis sp.,
Haemogamasus dauricus and Raplozetes vindobaenensis .
SLnil.arity between Acari of Alaska and Canada is greatest
among the Oribatei (Table 2). This is probably because the
oribatjd fauna of the North American arctic is comparatively
well known, only 46 undescribed species being recorded, whereas
69 specitn are undescribed in each of the Mesostigmata and
Prostigmata. Previous studies in the North I merican arctic
have recorded 219 species. This study has increased this
number t 404 species.
72].
-------
0
SITES SAMPLED IN THE
NORTH AMERICAN ARCTIC
AND SUBARCTIC AND
NORTHERN CHUKOTKA
FIGURE 1..
-------
Table 1. Sampling sites in the North American arctic and
subarctic and northern Chukotka, U.S.S.R.
NO. OF
SOIL
REGIONS SITES AND ABBREVIATIONS SAMPLES
Western High
Arctic *1_i Batharst Island (Ba].) 32
1-2 Somerset Island (SomI) 12
1-3 Seymour Island (Sel) 2
1—4 King Christian Island (KCI) 22
Eastern High *2_i Ellesmere Island (El) 38
Arctic *2_2 Devon Island (DI) 14
2-3 North Kent I3land (NKI) 2
2-4 Ward Hunt Island (WHI) 2
2-5 Axel Heibarg Island (AHI)
Western Low 3-i Banks Island (BI) 12
Arctic Islands 3-2 Victoria Island (VI) 16
MacKenzie *4_]. Yukon Territory (?T) 1].
District *4-2 MacKenzie Delta - subarctic (MDsa) 10
*4—3 MacKenzie Delta (MD) 14
4-4 Tuktoyaktuk Peninsula (Tuk) 14
4-5 Herschel Isj .and (HI) 6
Keewatin 5-1 Kee ’atin District (Ne) 12
District
Baff in Island *6_i Baf fin Island (BfnI) 107
Region 6-2 Igloolik Island (IgI) 49
Labrador and 7-1 Northern Quebec (NQ) 16
Northern Quebec 7—2 Labrador — subarctic (Lsa) 7
Alaska *8—1 Northern coastal plain (Ncp) 64
8-2 Brooks Range — northern
foothills (BRnf) 73
*3.. 3 Brooks Range (BR) 36
8—4 Brooks Range — southern
foothills (BRsf) 21
* 8-5 Fairbanks reaion — subarctic (FR) 44
*9—6 Northwestern coastal area (NWc) 42
8—7 Southwestern coastal area (SWC) 15
8—8 Atkasuk (Atk) 46
8-9 i( nti Peninsula and Chugach
untains ( nKp) 18
8-10 McKinley Par1 (McKP) 35
8-Il Ai.eutian Islands (Al) 29
8—12 Pribjiof Is1an1 (P1) 3
tl—13 Nunivak island (NI) 7
—l Chaun B y (CB) ii
* 3 te from 1 ari. have been previous].y ccl]ecte .
719
-------
that Coliembola play a more significant role relative to mites
in tundra than in other ecosystems (Douce and Crossley, 1977).
Mites predominate in organic substrates, whereas mineral soils
support higher densities of Collembola (Watson et a].., 1966).
In coastal tundra, ar ,und Point Barrow, density and diversity
of Prostigmata is greater than that of other acarine groups
(Douce and Crossley, 1977). This contrasts with most temperate
regions where Oribatei qenerally predominate in nndisturbed
soils (Waliwork, 1916).
In the past 12 years interest in arctic and subarctic
ecosystems has greatly increased with the exploitation of oil,
gas and mineral reserves in these regions. Yet data concerning
acarine species diversity are scant. In view of the importance
of soil mites it was relevant to determine, in greater detail.
their distribution and diversity in the North American arctic
and subarcUc and changes in their distribution and diversity
along a latitudinal gradient from subarctic to polar desert.
Site Descriptions
From 1970 to 1976, 833 soil samples were collected from 34
major sites in the North American arctic and subarctic (Table I,
Figure 1). Of these, 698 were from arctic and 135 from subarctic
areas. The Canadian samples were assigned to seven geographical
regions following the terminology of the Canadian Committee for
the Terrestrial Conservation Section of the International
Biological Program (Nettleship and Smith, 1975). Sites in Alaska
were, for simplicity, placed in one geographical region. Eleven
soil samples were co] .lccted from Chaun Bay, northern Chukotka,
U.S.S.R. in 1975. Data trom these samples, discussed by MacLean,
Behan and Fjellberg (1978), are compared with results from the
North Unerican arctic in the present study.
A brief description of the location, ecology and climate of
each site, with a list of species collected is given in Behan
(1978). Previous data on acarine diversity were available for
only nine of the 34 sites sampled; Bathurst Island (Danks and
Byers, 1972); Ellesmere Island (Oliver, 1963; Lindquist in lit.,
1977); Devon Island (Ryan, 1972, 1973, 1974); Yukon Territory
and MacKenzie DeltE’, subarctic (Hammer, 1952); Alaska, northern
coastal plain (Hammer, 1955; Hurd, 1958; St.randtmann, 1967;
Bohnsack, 1968; MacLeai, 1971; Douce, 1973, 1976); Brooks Range
and Fairbanks Region (Har ’uer, 1955) and Northwest coastal area
(Watson et al., 1966).
-------
DISTRIBUTION AND DIVERSITY OF NORTH AMERICAN
ARCTIC SOIL ACARI
Valerie M. Behan and Stuart B. Hill
Macdonald College of McGill University
Canadia
IN’rRODUCTION
In the arctic, as in all ecosystems, various environinent ].
factors are interrelated, changes in one causing changes in
others. Rate of nutrient turnover and subsequent rate of
primary productivity are dependent primarily on microorganism
activity. This, in turn, is limited by food, space, dispersal,
cropping, biost3sis and senescence (Hinsheiwood, 1951). These
effects are, however, counteracted by the activities of soil
animals, such as mites. Mites not only serve as catalysts for
microorganism activity (Edwards and Heath, 1963; Crossley and
Witkamp, 1964; Macfadyen, 1968) but also constitute an important
mineral reservoir (Hudig, 1949; Webb, 1977).
Yet prior to }lanune.r’s (1952) monograph on the Oribatei of
northern Canada, the mite fauna of the North 1 xnerican arctic was
virtually unknown, except for reports of 16 species from the
Queen Elizabeth Islands (MacLachen, 1879; Banks, 1919).
Subsequently, Acari were collected from Lake Hazen, Ellesmere
- Island (Oliver, 1963; Lindquist in lit., 1977); Ellef Rignes
Island (MeAlpine, 1964, 1965); Baf fin Islt id and Iruvik (Swales,
1966); Bathurst Island (Danks and Byers, i972) Devon Island
(Ryan, 1972, 1973, 1974) and Melville Island (T4ndquist in lit.,
1977). Literature on these studies stresses the low species
civersit” the arctic.
Soil acarine studies in the Alaskan arctic were initiated by
Hammer’s (1955) major study on tne Oribatei of Point Barrow and
subarctic forests. Subsequently, mites of the coastal tundra
around Point Barrow were intensively studied by Hurd (1D58),
Strandtznann (1967), Bohnsack (1968), MacLean (1971, 197!), Douce
(1973, 197g.) and Douce and Crossley (1977). Soil mites of Cape
Thompson were also studied following a proposal by the U.S.
Atomic Energy Commission to build a deep-water port there
(Watson, Davis and Hanson, 196C).
These studies revealed differences between acarine faunas
of arctic and temperate soils. Life—forms in the arctic are
associated with soil surface, litter and moss cover, deep forms
and arboreal species being absent (Douce, 1973). It appears
717
-------
pendLa 4. DiutrlRuUon of no11 o1an specie, on Devon Island, Cornvallis luland and king Chriatien I sL ud, 8. 1 1.1., in relation to
individual plant species.
2 total no. individuala at seth .icro.ite
DEV00 ISLAND CORNVALLIS ISLAND KING CHRISTIAN ISLAND
Beach Ridge Traneition Zone
a a a
2 2 a Z
___________________ fr II i iI i 1 I
Bppoaaatrura tuliberni (Schif far)
R pogestrura op. nova
Miurida aranari . (Nicolet)
! Iicanurida pynaea lOrner
! li’! R ip.
Otychyiuru. groenlandicu . CTullberg)
Tuliberit. ainolex 7 Clam
Stachancr..a op.
701500111 tuetularie Meaner
P. (TuIlberg)
!. bleetnea Gieth
!. duodectanetnea Meaner
! e1on ta NacCillivrsy
Itotone violeeea TuUberg
I. paluerria ( 11011cr)
I. ekoani I’jellberg
. group
1. oP.
Vsrtaaoo ap. nv brevica Carpontsr
Bet brya corear ta Folso.
Meaalothoraz athiani (Willie)
Total no. Individueli
in 10 .a.plee
87.1 81.9 19.1 13.5 17.5 12.7 46.5 81.3 20.9
9.2 11.4 9.1
- 0.4
0.6
0.3 5.7
0.3 1.3 1.9 0.2 0.6 0.1 0.4
2.1 3.8
5.3 1.1 18.2 5.5
2.3 7.3 71.3 80.4 53.8 60.1 51.2 10.3 58.4 58.3 ‘1.5 70.1
0.2 0.8
4.2 5.2 6.0
0.3
0.7 1.7 9.8
0.1
0.3 2.6 7.4
2.4 2.6 2.7
0.3 2.4 3.0
2.9 0.7 0.2
0.2 1.3
0.? 0.3 1.6
3.9 32.4 17.1 16.9
0.5 0.7 1.9 0.2
400 432 1,424 796 634 1,337 909
310 281 253 368 33
-------
Strickland, A.H. 1947. The soil fauna of two contrasted plots of
land in Trinidad, B.W.I. J. Anim. Ecol. 16:1-10.
Svoboda, J. 1977. Eco1og ’ and primary pi oductivity of rained beach
communitics, Truelove L wland. pp. 185—216. In L.C. Bliss
Cod.), Truelove Lowland, Devon Island, Canada: High Arctic
Ecosystem. Univ. of A]ta. Press.
Walker, S.D. and T.W. Peters. 1977. Soils of the Truelove Lowland
and Plateau. pp. 31—62. In L.C. Bliss (ed.) Truelove Lowland,
Devon Island, Canada: High Arctic Ecosystem. Univ. of Alta.
Press.
Winner, C. 1959. Schaden an Zuckerrliben durch Onychiurus campatus
Cia. Nachr. Deut. Pflanzenschutzdienstes, Berlin 11:67—69.
ACKNOWLEDGEMENTS
I would like to express my gratitude to the Arctic Institute
of North America for use of their field camp on Devon Island, Sun
Oti Ltd., for the use of their camp on K.C.I., and the Polar
Continental Shelf Project (Can. Dept. Energy, Mines and Resources)
for logistic support. During this study I was supported by an NRC
Scholarship and Killam Scholarship (1974) and an NRC Postdoctoral
Scholarship (1975—1977). Addir 4 onal fLnancial support was provided
by grants made to D. Parkinsoi, (NRC A—2257) and I.C. Bliss (ALUR)
and NRCC—IBP funding to the De’on Island Project. Taxonoinic
expertise was provided by W.R. Richards and J. Rusek, K. Chris’lansen
and A. ??jellberg. Thanks are also due to P. Nosko and his assistants
for collecting soil samples in 1978 and to P. Addison and N. Diamond
for advice and criticiss in the preparation of this manuscript.
-------
Gauch, H.G., S.D. Lanyon and R.H. Whittaker. 1971. Bray—Cur:is
Ordination. 12 pp. mimeo.
Gauch, H.G., and R.H. Whittaker. 1972. Comparison of ordination
techniques. Ecology 53:868—875.
Haimner, M. 1953. Colleuaboles and Oribatids from the Thule District
(Northwest Greenland) and Ellesinere Island (Canada). Medd. om
Gr$nland 136:4—16.
Hammer, M. 1954. Colleaboles and Oribatids from Peary Land (Northern
Greenland). Mindd. on Gr Snland 127:4—28.
Knight, C.8. 1961. The Tomocerinae in old field stands of North
Carolina. Ecology 42:140—149.
MacPadyon, A. 1954. The invertebrate fnuna of Jan Mayen Island (East
Greenland). J. Anim. Ecol. 23:2b2—297.
MacFadyen, A. 1962. Soil arthropod sampling. Adv. Ecol. Ras. 1:1—34.
Martynova, E.F. 1969. New species of the Family Isotomidae
(Collenibola) from the Asian part of the U.S.S.R. Zool. Journal
48:1342—1348. (Ii Russian).
i4cMillan, J.H. 1976. Laboratory observations on the food preference
of Onychiurus areatus (Tulib.). Gisin (Collembola,
Onychiuridae. Rev. Ecol. Biol. Sol. 13(2):353—364.
MUller, G. 1959. Untersuchungen Uber des Nahrungswahlvermöger
elniger im Ackerboden hailfig vorkommender Collembolen und
milbon. Zool. Jahrb. Abt. Systemet. Okol. Geograph. Tiere
87:231—256.
Muller, C.H. and C.H. thou. 1972. Phytotoxins: an ecological
phase of phytochemistry. pp. 201—216 In J. Earbox-ie (ed.),
Phytocheinical Ecology, Academic Press, London.
Pallisa, A. 1967. Uber die Wirk g versehiedener Pflanzenstoffe auf
Bodentiere. pp. 89—92 In 0. Graff and J.E. Satchell (eds.).
Progress in Soil Zoology, Vieweg, Braunsehweig.
Savil.e, D.B.O. 1960. Limitations of the competitive exclusion
principle. Science 132:1761.
Seniczak, S. and V. Plichta. 1978. Structural dependence of moss
mite population (Acari, Oribatei) on patchiness of vegetation
in moss—lichen—tundra at the north coast of Horrisund, West
Spirsbergen. Pedobiologia 14:145—152.
S ren..en, T. 1948. A method of establishing groups of equal ampli—
tiide in plant sociology based on simi].rrity of species
co1l cted and its application to analyses of the vegetation
on Danish coons. Vid. Seisk. Mol. Skr. 5:1—34.
Stebaeva, S.K. 1963. Ecological distribution of Collembola in the
forests and steppes of the Southern Tuva. Pedobiologia
3:73—85. (In Russian, with German summary.)
7 11i
-------
CONCLUSIONS
Collombola were more abundant in soil samples with. vascular
plant cover than in bare soil. Although Collembola ‘ c e sometimes
more abundant under certain plant species than others, the species
of plant was apparently not as important as its growth form.
In general, species of Collanbola could sot be linked with a
particular species of vascular plant. The collembolan faunas under
different plant species within a single plant cnmmunity were very
similar, and differed considerably from the faunas of the some plant
species in a differe.at plant cesmiunity on the same island. Differ-
ences in the composition of the coU.enbolan fauna of different isl.and
were greater than intra—i iland Chabitat) differences.
It was concluded that zoogeogxaphic and iaicroclimatic conside-
rations were more important than the species composition of the
inacrof].ora in determint g the distribution of Collembola in the High
Arctic.
- ITERATURE CITED
Addison, 3 .A. and D. Parkinson. 1978. Influence of collembcilan
feeding activities on soil metabolism at a high arctic site.
Oikos 30:529—538.
Addison, P.A. 1977. Autecological tudies of Lusula confusa : a
plant’s response to the high arctic environment o King
Christian Island, N.W.T. Ph.D. Thesis, University of Alberta.
Blackith, R.E. 1974. The ecology of Collembol in Irish blanket
bogs. Proc. Roy. Irish Acad. 74:203—226.
Bliss, L.C., G.M. Courtin, D.L. Pattie, .R. Riewe, D.W.A. Whitfield
and P. Widden. 1973. Arctic Tundra Ecosystems. Ann. Rev.
Ecol. System. 4:359—399.
Christiansen, K. 1964. Bionomics of Colleinbola. Ann. Rev. Ent.
9:147—178.
Qirry, 3.P. 1976. The arthropod communities of some common grasses
and weeds of pasture. Proc. Roy. Irish Acad. 76:661—665.
Cruickehank, J.G. 1971. Soils and terrain units i iround Resolute,
Cornwa].lis Island. Arctic 24:195—209.
Dunger, V. 1962. MethoJen cur vergleichenden Auswertung von
Futterungeversuchungen in der B denbio1ogie. Abhandl. Ber.
Naturkundemuseums 37:143—162.
Fjellberg, A. 1975. Redescriptioas of some little known Collembola
from Scandinavia (Ins3cta: Colleinbola). Ent. Scand. 6:81—88.
713
-------
herbivorous species appeared to discriminate between host plant
species, it was not possible to differentiate between samples on the
basis of detritivorous species.
In this study differences between the numbers of Collenibola
under dii:ferent species of plants were demonstrated. Stebaeva (1963)
suggested one possible way in which different plant species might
affect collembolan abundance. She reported that Collembola were more
numerous and were found at lower depths under plants with deeply
penetrating root systems than under shallow—rooted plants. This how-
ever cannot account for differences observed in the present study
since the root systems of all species penetrated at least 7.5 cm,
but 75—90Z of the Collembola were extracted from the top 2.5 cm of
soil with,<5% occ arring below 5 cm.
The most likely explanation for the fact that Collembola were
more abundant under certain plants than others is that their abundance
was related to the growth form of the plant. At the Beach Ridge Site
on Devon Island, S. oppositifolia had short internodes and formed
compact cusions that would trap snow in winter, and withi.n which
organic niatter would accumulate. The water holding capacity and hence
humidity could be expected to be higher here than in the surrounding
area (Svoboda 1971). At this site D. integrifolia plants formed a
loosely structured sat, of which most of the surface was dead. It is
likely that Colleinbola would prefer the compact cusion plant growth
form of S. oppositifolia to the growth form exhibited by I).
folia . At the Devon Island Transition Zone, S. oppositifolia had
long internodes and its growth form resembled that of a prostrate
shrub (Svoboda 197:). This latter growth form was also exhibited by
S. oppositifolia on the sites sampled on Cornwallis and King Christian
Island. This growth form would not be as attractive to the Collembola
as a densecushion plant. S. caespitosa always exhibited a compact
cushion plant growth form, perhaps explaining why this species always
contained high numbers of Collembola. Collembola were also abundant
under L. confusa , which formed a dense mat rather than a cushion
plant. This plant species was only found in less exposed parts of
the sites; areas with good snow cover in winter (Addison, 1977).
These areas would be expected to contain htgh numbers of Co1J .embola
regardless of the species composition of the vascular plant cover.
The lack of host—specificity in arctic CoUembola is not
surprising. Environmental conditions are so harsh, and nutrient and
energy inputs are so low, that from an evolutionary point of view, an
organism cannot afford to become too specialized. It must be able
to tolerate a wide range of environmental conditions and utilize
different food sources and microhabitats for survival. As Savile
(1960) pointed out, in anvironinante where abiotic factors are of such
over—riding importance, biotic interactions between species may often
be of little consequence. It is suggested that if host—specificity
amongst Collembola does in fact occur, it is more likely to be found
in more temperate areas than in the impoverished soils of the Arctic.
7 12
-------
DISCUSSiON
The results of this study (Table 1) indicate c learly that in
impoverished soils Co].lembola are indeed closely tied to the immed-
iate vicinity of a plant species as suggested by Blaca ith (1974).
Similar results were obtained by Seniczak and Plichta (1978), who
compared the numbers of oribatid mites in soils with a cover of lichen,
moss, and S. oppositifolia and found the mites were fliOSt abundant
under S. oppositifolia .
Attempts to link colleinbc,lan communities or individual collem—
bolan species with individual plant species failed. tu comparing the
collembolan faunas of different islands, zoogeographical considerations
must obviously be taken into account. The absence of a species on a
particular island can be attributed to one of two factors; that the
species near reached the area, or that having reached the area it was
unable to maintain itself in sufficiently high numbers to be taken
in the samples. Whatever the reason, many species of Collembola
simply did not occur on some of the islands, so that their absence
under a particular plant species at such . site is not strictly
comparable to an absence under a plant at a site at which it was
present. In general the species composition of the Devon Island fauna
resembled those of Northern Greenland (H mner, 1954) and Ellesmere
Island (Hammer, 1953). and was quite distinct from the collembolan
fauna of King Christian Island • Cornwallis Island contained elements
from both the eastern arctic (Devon Island) fauna azid that of the
western arctic Cling Christian Island).
This study also failed to detect specific plant—collembole
associations within a single island. The collembolan faunas of
S. oppositifolia and D. integrifolia at the Devon Island Beach Ridge
Site were very similar to one another, and very different from the
fauna of the same plant species in a different plant coMmunity a mere
10 m away. It was expected that if species of Colleinbola were
attracted by some characteristic of a particular plant species, such
as root exudates, the rhizoskhere flora, or characteristics of the
organic matter, then these Collembola would be found in close prox-
imity to the same plant, regardless of the plant community. It
should be r m mbered however, that the various characteristics of
specific plants mentioned above might themselves be altered by
characteristics of the different sites and so differ in their ability
to influence Colleniboja.
The conclusion that Collembola were associated with a particu—
lar plant community rather than a particular plant species differs
from that of B]ackith (1974). The results of the present study are
in agreement with those of Curry (1975) who found that although
711
-------
TABLE 2. Mean number of Collenibola per sample (23.75 2) Means not underscored by the same line
differ at the 0.05 level using a Student Newman Keuls Multiple Range Test.
Site Mean no. Coll nbola/sample
Devon Island-
Beach Ridge Plant D. int rifolia S. oppositifolia
28.1 51.0
Transition Zone Plant D. g foli S. oppositifolia S. caespitosa L. confusa
7 15.3 25.5 36.8 40.0
Cornwallis Island Plant S. oppositifolia D. g o1ia S. caespitosa
x 20.6 41.1 88.9
King Christian Island+ Plant S. oppositifolia L. confusa S. caeanitoaa
61.1 84.9 121.0
+ log 10 Cx + 0.5) transformation of original data used. Derived means shown.
-------
FIGURE 2. Bray—Curtis Ordination of InicLosites (plant—site
combinations), based on Percentage S1 ilarity.
• S. oppositifol3a , AS. caesp osa , UD. integrifolia 1
•.! confusa .
0
U
0
0
a
C
0
C,
0
KCI
Cl
Relative Perceni Difference
709
-------
FICTJRZ 1. Bray—C-.irtis Ordination of microsites (piant—site
combinations), based on Coefficient of Conuminity.
•S. oppositifolia,AS . caespitosa,•D. j rifo1ia,
•L. cortfusa .
oo
C.)
C
0
0
I .-
0
C
0
C)
0
BR
2
Oo
20 40 60
Relative Percent Difference
708
-------
n. e — —— — —
Effect of individual p1ai t species on colleinbolan communities
The collembolan faunas of the twelve microsites (plant—site
combinations) were compared using the Cornell version of the Bray—
Curtis Ordinetion technique (Computer Programs CEP4Ø and CEPSØ
(Gauch, Lanyon and Wnittaker, 1971)). These programs use two indices
of similsrity: coefficient of community (Sorenson. 1948) and percen-
tage similarity (Gauch and Whittaker, 1972). The former inaex uses
qualitative (presence and absence) data only while the latter incor—
porates both qudlitative and quantitative information. The results
of these analyses are shown in Figures 1 and 2. Regardless of which
similarity index as used in the ordinatic.a, the microsites
clustered out In groups accerding to site (or plant community).
These was absolutely no tendency for the microsites to cluster
according to plant snecies.
The modified version of the Bray—Curtis Ordination Technique
was also uaed to express the degree of s mi1arity between the colleni—
bolan faunas of different plant species at the same site. In all
cases there was considerable overlap in the ordination of the
individual samples, and groups of points represent±ng the faunas of
individual plant species could not be identified.
Effect e individual plant species on abundance of Collembola
Although in general the species composition of the Collembola
taken under different plant species at the same site was similar,
evidence of within site selection of certain plant species over
others can be seen by considering the abundance of Colleinbola under
the different plant species (Table 2). Differences in the abundance
of Col].enibola under different plant species are especially evident
in the polar semi—desert sites (<20% vascular plant cover). The
speiies of plant containing the highest numbers of Collenibola varied
according to site, so no one species could be identifiea as providing
the most favourable habitat for Collembola.
Effect individual plant species on distribution of collembolan
species
The distribution of collembolan species in relation to indivi—
uual plant species is shown in Appendix A. One species ( Fo].somia
regularis ) occurred under all plant species at all sites, but no
species of collenibole could be linked with a particular species of
plant regardless of its siLe. Several species were found only at one
site or one island (e.g. Tullbergia simplex — DBR; Lols nt elongat3 —
CI ). Although Vertagopus sp. nr brevicauda was cofl.ected only from
under S. ca’ spitoaa on Coinwalils Island in 1975, this species occurred
under both S. oppositifolia and L. confusa as well as S. caespitosa
on lUng Christian Island. Tn fact it was also found in samples of
S. oppositifolia from an unidentified plant community near Resolute
Bay, Cornw& lie Island in 1978. These samples also contained
specimens of Willemia op., a spccies that as absent from all samples
of S. 2puositifolia taken in 1975.
707
-------
METhODS
Ten replicate cores (23.75 cm 2 x 7.5 cm deep) were taken from
each plant species at each site in which it occurred. In addition,
ten cores of soil from non-vegetated areas approximately 15 cm from
S. oppositifolia plants were taken from the Devon Island Beach Ridge
Site, and a similar series of samples was taken on ICing Christian
Island, approxImately 75 cm fromL. con! usa .
Each core was divided into three 7.5 cm sections, and the
Collembola were extracted In a high gradient extractor modified from
MacFadyen (1962).
All the Devon Island samples with the exception of those frcim
S. caespitosa and L. confusa were collected in August 1974, and were
extracted on site. Samples from Cornwallis and King Christian Island
were taken in August 1975, and were shipped south to Edmonton, Alta.
before the CoUembola were extracted. The Devon Island S. caespitosa
and L. confusa samples were obtained 1n August 1978 and were also
extracted in Edmonton.
RESULTS
Effect of vascular plant cover on abundance of Collanbola
A comparison of the nu’nbers c f Collembola obtained frm soil
samples with and without vascular plant cover (Table 1) shows that in
both the Devon Island Beach Ridge and the Ki’ g Christian Island Site,
Collembola were much more abundant in samples containing a vascular
plant than in samples of bare soil.
TABLE 1. Influence of vascular plant cover on abundance of
Col.leabola. Means based on 10 samples.
Site Vascular Plant M an no. Collembola/
sampi.’. (95% conf...ience
l Imits)
Devon Island— 51 (36.1—65.9)
Beach P 4ge Bare soil l’.5 (4.9—18.0)
King Christian 3 ij confusa 75.8 (52.2—99.4)
!sland+ Bare soil 4.6 (0.0—10.1)
-‘- statistical comparison of : sample types from XCI
no strictly valid since variances—are unequal.
706
-------
Under these conditions it was easy to obtain “pure” samples from the
differmnt plant species since each 1ndiv dual plant (including its
Tact systam) was distinctly separate from any other vascular plant.
The Collembola associated with the folluwing four species of vascular
plant were studied: Saxifrag opp eitffolia L., Saxifraga caespitos
L., Dryas integ ifolia N. Vahl and Luzula confusa Linci eb. Samples
were collected from three different islands in the Northwest Terri-
tories in Canada; Devon Island, Cornwallls Island and King Christian
Island. Two diffe 1 ent plant conIml!nitles were sampled on 1)evon Island,
giving a total. of four sites in au.
SITE DESCRIPTIONS
Devon Island — Beach Rid (DBR)
A cushiun plant/lichen comm nity was associated with this site.
Vascular plant cover was <20%, lichens covered approximately 60% of
the area, and 20% was entirely bare (Svoboda, 3. )77). The soil at
thin site wa a Regusolic Static Cryosol. (Walker and Peters, 1977).
Devon Island — Transition Zone (PrZ)
k cushion plant/moss community was associated with this site.
Vascular plants coveted nearly 60% of the area, with lichens and moss
making the total plant cover up to 100%. The soil was classified as
a Brunisol.ic F tat1c Cryosol (Walker and Peters, 1977).
Cnrnwalli.s Island (CI)
SampleE were taken from a cushion plant and lichen covered
area approximately 1.5 Ion NNW of the north end of the runway at
Resolute Bay. Vascular plant cover was <10%, and the soil was
described by Cruickshank (1971) as a “shallow polar desert soil.”
King Christian Island ( XCI)
A lichen-moss—rush community was characteristic of the site.
Vasc ular plants covered only 8.7% of the area, and 33.2% of the soil
was unvegetated. The soil was a Regosolic Static Cryosol (Addison,
1977).
Using the nomenclature of Bliss et al. (1973), the sites on
King Christian Island, Cornwallis Island, and the Beach Ridge site
on Devon Island would all be classified as polar—seni-.desert areas
(2—20% vascular plant cover), whereas the Devon Island Transition
Zone Site would be classified as a tundra site (>20% vascular plant
cover).
705
-------
INFLUENCE OF INDIVIDUAL PLANT SPECIES ON THE
DISTRIBUTION OF ARCTIC COLLEMBOLA
J. A. Addison
Unit’ers., of Caigny
Canada
INTRODUCT ION
The macroflora is generally considered to effect collmnbotan
populations indirectly, by modifying the microclimate, soil structure
or microbial populations (e.g. Strickland, 1947; MacFadyen, 1954;
Knight, 1961). Christiansen (1964) pointed out that the importance
of the macroflora as a factor influencing collenbolan distribution is
reflected in the fact that there is generally at east a moderate
degree of correspondence between plant and collenbolan associations.
Direct effects of the macrof lore on collenbolan populations
have also been postulated. NL’ller (1959) demonstrated that the living
plant root systems of indi’9idual p].aut ap c4es iif].uenced the dis—
trioution of Collesibola in a wetland soil, and although he was unable
to determine the cause, he was able to show that the plant root system
must be alive to emert thiE effect. Many Collembola show distinct
feeding preferences, and will selectively feed 3U certain species of
leavea (Dunger, 1962) plant roots (Winner, l 59) or fungi (McMillan,
1976; Addi3on ax!d Parkinson, 1978). Biologically active substances
sccreted br,’ plants have also been shown to influence different collen—
bolan species. (Palissa, 1967; MUller and rhou, 1972).
In spite of the overwhelming evidene for both direct and in-
direct effects of the macroflora on colimabolan distribution, there
is little evidence for the restriction of individua 1 collembolan
species to the tmaediate vicinity of any one plant species (Chris—
tiau en, 1964.) More recently Blackith (1974) suggested that in
poorer soils (“tundra—type s’ils”), where energy and nutrient input
are limited, Collenbola may be more closely tied to the immediate
vicinity of a plant thati in soils such as arable or woodland soils
which contain sufficient decomposing material to allow them to live
aiiay from the plant root and stem system. Based on his own work in
an Irish blanket bog, and evidence from the non—English literature,
he also suggested that Collentola choose plant root systems on a host—
suecific basis.
The purpose of this study was to investigate the relationship
between individual vascular plant species and their associated
collembolan faunas. The study was carried out in the high arctic
region of Canada, in areas with generally sparse vegetation cover.
704
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SESSION IX: BASIC SOIL ECOLOGY:
SOIL ECOLOGY OF THE ARCTIC AND DESERTS,
STRUCTURE AND FUNCTION OF SOIL
ORGANISM COMMUNITIES
Moderator: M. B. Bouch
Station de Recherchec sur Ia Faune du So!
Dijon. France
703
-------
Ces nouvell.es techniques peuvent dtxe utilisées pour les etudes de
taux de !ziortalité, d’accroissement de bii. masse, de migrations êt de fai—
sabilitd de la biostimulatiOfl des so].s par l’introduction de lombriciens.
SUMMARY
Overpopulated introductions and migrations of labelled earthworms.
In the aim to improve new techniques to label earthworms, research
on those techniques was made and led to the coloration of animals in red
and green by stainning. Such labelled earthworms were introduced in field
in addition to the original communities. Migrations and weight evolutions
of both labelled and unlabelled earthworms were followed during months.
among a lot of observations some main facts were noticed
1) overpopulation increases disapearence (mortality or migration)
in field,
2) this overpopuiaticn harms all the community without respect of
the introduced species or ecological, group (interspecifiG com-
petition),
3) migration of settled earthwor 1 us is very limited in space (be-
low 50 cm) for must earthworms while some pioneers migrate far
away (few meters),
4) width of both migration types depends of ecological groups.
These techniques would be used to study mortality rates, biomas
increments, migration and feasability of soil impro nnent by earthworm
introduct.i.ons.
REFERENCES BIBLIOGR PHIQUES
BOUcHE, M.B., 1972 - Lombriciens de Prance. Ecologle et systématique. Ed.
I.N.R.A., Ann. zool. — écol. anim., numCro special, 72—2, 1—671.
LAVELLE, P., 1971 — Recherches sur la ddmogra ,hie d’un ver de terre d’A-
frique ; Milisonia anomala Omadeo (Oligoch tes, Acanthodrilidae).
Bull. soc. écol., 2, 4, 302—312.
MAZAUD, D., 1979 - Evaluation de méthodes de marquage permettant. le répé-
rage des lom r ..ciens au te rain ; pzemieres applications. These doc—
teur—ingénieur, sciences agronomiques, I.N.A. Pari —Grignon, Paris,
1—178 + Annexes 1—80.
MEINHABDT, U., 1976 - Dauerhafte Markierung von Regenw rmen durch ihre
Lebendf&rbung. Nach. Deuts. Pflanzenschutzd,, 28, 6, 84-86.
701
-------
fin, lee NicodrilUs anéciqueS présentent dans leur ensemble un taux meil—
leur ( 19 %) que La moyenne générale.
CONCLUSION
La isdthode .le marquage—YeCaPtUre pratiqude a titre d’essais & Gri—
gnon et Clteaux a été d’un emploi difficile surtout en raison de aléas
cliinatiques et des difficultés techniques d’ échantij.lonnage. La marquage
par coloration s’est montré satisfaisant ; ii a dté réus,i ave quatre
colorants dont trois ont servi an terrain. Ii a dtd possible d’observer
des migrations : ceilca—ci sont très faibles chez lee endogés, au T2axi—
mum de l’or’ r de 1 ci/mois pour lee anéciques et de 2 an/niois chez lee
épigds.
A Grignon, lee L. terrestriS ont migre plus que IJicodrilus giardi
et Allolobophora icterica. A Citeaux, lee L. castancus out migré rapide-
ment par rapport aux icodri1us anéciques tandis que lee Allolobophora
furent apparemment trés stables la vitesse de migration épigds > ané-
ciques > endogds est conforme aux nioeuxs de ces categories ecologiques.
En raison du caractére sédentaire des animaux, l’état de surpopu-
lation a entrainé des effete cur les autochtones et alloc-htones. Ceux—ci
migrant sur quelques ddcimétres, fuyant La zone de surpopulation initia-
le a la manière d’une vague concentrique (Grignon) et une difference de
8 % art affectif (C teaux) entraine un taux de recapture plus faible dens
la parcelle A forte surpopulation (24 %). Cette surpopulation. due A des
endogds et dpigds, affecte égalernent lee recaptures des andciques. La ré—
duction de la suxpopulatton se fait A la fois par elimination d’autc chto-
nes et d’i llochtones. Ce n’est pas an niveau de chaque espéce on mieux
de chaque catégoxie dcologique que 1 ‘équilibre aprAs une surpopulation
allochtone colorée se fait aprAs le l&cher mais au niveau de l’enccsble
du peuplement : ceci illustre la competition interspécifique entree lois—
briciens cohabitants.
RESUME
Dane le but de maitriser les divers aspects du marquage par colo-
ration (en rouge ou vert) des lombric ens, une dtuUe technique a dté con—
duite. Lee loebriciens marques ont dtd ajoutes a des peuplements naturels
et lea evolutions spatiales et poridérales furent suivies pendant plusieurs
isois. Parmi la multitude des infozmatioris acquises, quelques traits domi—
nants peuvent être ddgagds
1) la surpopulat3.on accrott La disparition (mortalité ou disigra-
tion) au terrain,
2) cet effet affecte tout le peuplement indépendament de 1 ‘espAce
on du groupe ecologique introduit (comp4tition interspdcifique),
3) spree installatIon, lee lombriciens migrent generalement pen
(moms de 50 cm) tandie que certaine pionniers franchissent
qusiques metres,
4) l’aptitude aux deux t:’pes de migration vane avec lee catégo-
ries écologiques.
700
-------
FIGURE 8 :
Citeaux. Pourcentage de recapture par rapport au nonthre d’animaux
1&chés (méthode formo]. quantitative). 0: tous Nicodrilus anéci-
ques. •: tous animaux. Zone Zt traits pleins. Za : tirets.
U
40
.
a
F!I JRE 9
.
S.
OOc brC • Jaiivler FIvrler • • Avril
Nit
FIGURE 9 : C! teaux. Nombre de ver marques recaptures par la méthode forniol
quantitative. 0: tous Nicodrilus anéciques. •: tous animaux.
Zone Zt : traits pleins. Zone Za : tirets.
FTfWRE S
“0
20
a
S
‘S
5%
5 %
S 5
‘S
‘S
5’
a
DICe bTe • Janvler • FSvrler
Avril
Nil
Ju In
.
S
S
5%
S
a
699
-------
de au formol s’est avérée d’une efficacité stable pour les vers autochto—
nes et nous adinettrons pour Les co].orés qt e pendant cette période favora-
ble lee résultats ‘ont pas été biaisés par la méthode de prélAvement.
Nous présentons fig. 8 le pourcentage par rapport au lAcher initial de
recaptures des anim ux marqu s dans l.a zone ayant reçu uniquement les
andciques (Za) et celle ayant recu andciques et autres vers marques CZt)
(86 % des recaptures sont celles d’andciques). Le test de Wilcoxon—Mann—
Witney nous permet de znontrer que l.a difference de recapture entre les
deux series est significative (A 5 %) en admettant une evolution lineaL-
re avec le temps.
TABLEAU 6
Vitosse Cv) minimale de déplaceinent de pionniers. D : durde c e ,é)our
sur le terrain. d : distance minimale parcourue (du milieu du carrd B au
carrd de recapture). + valeur obtenue dans le cas oü on adinet que la
migration n’a débuté que debut fdvrier en raison du froid hivernal.
D moisde d v
en jours recapture en rn en n/nois
L. ca at azieus
48
Janvier
3
2
Ni codril us
175
Mai
3
0,5
91
Eevrier
1,5
1,5
I.e peup .ement recapture baisse de façon sicjnificative avec I.e temps
(fig. 9) pour le peuplemcnt total (regression liné ire significative au
seui]. 0,05). L’effectif des animaux recaptures est A oeu pres le mdnie
dans les deux aires d’accueil et le noinbre d’animaux qui réussissent &
se maintenir semble donc dépendre des paramétres éco]ogiques de l’aire
d’accue l. assez hamogénes entre lee deux zones. Pour Lee Nicodrilus seuls
l’dvolution des zones Za et zt est bien distincte ; l.a zone la plus gu i-
peuplee présente moms de recapture.
Ainsi, c’est le niveau global des allochtones qui se stabilise
mais non celui des espdces ou categories dcolog ques allochtones, ce qui
indiquerait une certaine competition interspecifique des Lombriciens co-
habitants. cela rejoint les travaux de l’un d’entre nous (Bouchd, 1972)
sux La faune Zrançaise mettant en oeuvre le coefficient d’exoécie permet-
tant de mesurer une “égalitd de compdtition entre ez pèces différerttes
cohabitantes dans un méme lieu. Sans avoir Ia mAme function, lee lambri-
ciens cohabitant, appartenant & diverses catdgories coat partiellement
inter-compétiteurs. Sur l’ensemble de l’experience de Citeaux, L I. a dtd
possible d’établjr is pourcentage de lombriciens recaptures par rapport
auic lAchds (peuplenient total 17 %) lee endogds .4llolobophora report—
dent sal A l.a indthode au formo]. ( 6 % de recapture) ; lee L. castaneus
ties mobiles ‘quittent” rapidement l’aire de recapture en raison de Leur
mobilité et de leur vie brAve (aouch4, 1977) ( 18 % de recapture) ; en—
698
-------
recaptures au cours de l’étude, par carte
FIGUF 6
Noinbre total d’ ndividus
de prélêvernent.
lethod. foi
0
QT
pr61lv ents qvantitatif% IQT) it
qvallt.tIrS (CL)
Nithode foruol .b&cbe
NIECIQUES
o
E1 DOG S
FIGURE 7 : Emigration A Citeaux. Noabre d’individus recaptures par zone de
pr 1èvement externe (chaque zone est symbolisCe par une bande hori-
zontale). 0: Nicodrilus anCciques adultes. S : Nicodri.Zus anCci—
ques juveniles. : L. castaneus. Lorsque I.e nombre n’est pas in—
diquC, ii n’y a pas de capture. L ligne de lAcher la plus exter-
ne dans l’aire d’accueil.
Distance ens
fI M( 7
a
x
I’
- -
/
.
/
,,
a
2
2
3
a
C C
/
I
/ S
0*5 Li
-
S
•

7 33 7 2
oa.o. oa. . S S
£xtlrliur di lure d’accwll —
AI D’AcCtUL
juin L
FIGUE 6
F2. A I C
£ FIN
A IC D L
£2
£1
01
a
C l
3,5
3,0
2,5
z,0
1,5
1.0
0.5
-n
0(cabre • Jumier , FIvrIer , rs AvrI l
697
-------
Lácher unique sur une aire : Citeaux
Les résultats des aniinaux recaptures dans les carrés de prélève—
inents sont donnés au tableau 5.
TABLEAU 5
Citeaux. Nombre d’anii aux marques recaptures dans ].es carrés d s parcel—
les de preléveinent. TOT : total des recaptures. TOT° recaptures esti—
mées on tenant compte de la bande rnédiane de l’aire d’accueil non éc.than—
tillonnée (voir fig. 2).
A
B
C
D
E
TOT
TOT°
W. aod’r A.Lu. Ad.
MLaod /iJ.Lu6 J.
bus UcsdiJ1u.a
Tous AUo tobopho’t
L. ca6.taneu4
17
72
89
8
10
24
48
72
0
5
3
14
17
0
4
0
3
3
0
1
0
4
4
0
1
44
141
185
8
21
52,5
177
229,5
10
26
Total général
107
77
2].
4
5
214
265,5
La figure 6 donne une image de 1 ‘ensemble des anixnaux recaptures
(dans et autour des carrés délimitant lee préleva.ts quantitatifs). On no-
te l’absea e de migration des endogés hors de l’aire d’accueil (c’est—à-
dire une migration inférieure a 50 cm pendant l’expérience). On constate
aussi une recapture plus forte dans lee carrds A ou lee emigration -s sont
mieux compensdes par des i nigrations que dane is carré de bordure B. En
utilisant toutes lee données de recapture au dehors de l’aire de iãcher
on peut constater (fig. 7) w retard a Ia migration due probablement a
l’effet hivernal sauf pour L. castaneus et deux N.zcodrilus juveniles. La
calcul de la vitesso de migration des pionniers oYcserv4e peut étre tentée
(tableau 6) pour lee Nicodrilus. Ces vitesses, A partir de l’aire d’ac—
cueil, ne préjugent pas du trajet effectivement parcouru par les animaux,
ii s’agit donc de la vitesse minixnale c&lculée sur la distance inaximale
observ-ée.
Z’évoiution des captures des anlmaux non marques dane l’aire de
prélèvement pendant la pdriode d’échantillonnage indique une diminution
constanta de i’effectif estimé (y) en fonction du temps en jours Cx) A
partir de fin février (y = — 15,7 x + 0,33), la diminution de 1,57 mdi-
vidus/jours/m 2 est significativement différente de 0 au seuil de 0,01.
Le rapport formol/formol—béche set relativement constant sauf en juin
lorsque la sécheresse ].iaite l’efficacité de la méthode au formol. En hi-
ver, Le basses temperatures (2 A 4 C) on? contribué & limiter les cap-
tures par toutes méthodes. En dehors des deux premiers prélêvements hi—
vernaux (froid) et du dernier préj.èvement estiva]. (sécheresse) la métho—
696
-------
TABLEAU 4
Grignon. Ddplacements. Liaisons entre les captures (Xl) et le temps (X2).
Sp : coefficient de correlation des rangs de Spearnian. D : dur e du sé—
jour. C : evolution chronologique des prdlëvements. %L : pourcentage par
rapport aux lãchds des recaptures dane les surfaces C et Ext. %R : pour—
centage par rapport . tous les recaptures de ceux des surfaces G et Ext.
%Bg : méme pourcentage pour N. g-iardi. A : rapport entre la densitd de
capture dens la surface PM et celie dans la surface C, pour 1 ‘ensemble
des animaux. P n : inéme rapport pour les non colorés. ° significatif au
seuil 0,01. x significatif au seuil 0,05.
XI
X2
Sp
nombre d’observations
%L
D
(3,87°
9 (deCDa 1D)
C
—
0,87°
.R
0,65
C
0,45
A_-
0
O, 59
8 (de CD a io
sans le 2B)
An
D
-0,69’
%Rg
C
0 ,71 ”
7 (de CD a 2B)
—
La densitd de capture des animaux non colords est toujours plus
grande daiis la surface G que PM (tableau 3, An c 100 ) ; cette différeri-
ce est significative au seuil de 1 S (test binomial : probabilité criti-
que 2. 10 ). Ces animawc ont donc disparu plus fortement dens la zone
de lAcher. Enf in, le rapport A (tableau 3) des effectifs par 52 des 1cm—
briciens captures (toutes categories) de PM/C décroit d’abord jusqu’au
premier mois, ii semble ensuite remonter aux trois derniers prélèveinents.
En definitive, l’apport ponctuel d’une population allochtone en
surnombre conduit A - une migration partielle des allochtones A peu de
distance du lAcher,
— une diminution des autochtones au lieu de ].Acher,
— un tree lez t retour & l’équilibre avec une sorte
d’onde de déplacement, cette emigration étant
probablement accompagnée d’une mortalitd induite
(Cf. Citeaux) (fig. 5).
695
-------
FIGURE 4 Densité globale de capture au in 2 , par zone de prélèvement. La
surface des rectangles est proport±onnej le au nonibre de ca tures.
Nombres ; Densités, ° L’aire de la surface Ext a été estiinée
a 1,2 n 2 .
nsIt
Cipturn

Surface •
Description. schéinatique ‘ e l’évolutjon dans le mps de La densité
de capture dane las surfaces PM et G. A : rapport entre lee densi-
tés de capture dane les surfaces PM et G, pour tous lec animaux
( —— ) et pour las non colorég f——-4). (n nombre d’individus.
d : distance au lieu d’introductjo des niinaux marques).
FiGURE 5
‘ I
d
p
I I! III
p
p
II III I v
69’+
Temps
L
d
FIGURE 5
G
9Cr
I
-------
Globalement, Ia migration s ‘observe sur 258 animaux recaptures
dent 69 seulement L’ont été hors de la surface centxale PM (fig. 4)
pour un sejour moyen de 3 mois et demi, seulemen . 27 % des mazqués ont
migré hors de l’aire centrale. La migratton est done faible et celle
hors de l’ajre d’expéiience Cenviron 2,3 m 2 ) a donc dQ tre réduite.
Le résultat en fonction du temps t ..ableau 3) perniet de inettre en
evidence une emigration prog ess ’ie des aninaux marques (tableau 4). Dans
lee surfaces G et Ext. le nombre de recaptures crort dans le temps (en
moyenne Dar jour) de 0,12 % des animaux lâchés. La pente de La droite de
zdgression est diffdrente de 0 au seuil 5 % (equation : y = 0,123 x + 0.994
y = % ; x = durée en jours). Cette augmentation se fait malgré une sur-
face de recapture peut-être trcp petite, les insuffisances de l.a méthode
au formo]. et la mort .ilité avec le temps.
TABT EMJ 3
Grignon. Evolution dans le tempo des recaptures par surface de prélêve—
ment. D durée de jour. PM, G et Ext : surfaces des prélêvemer’ts (voir
fig. 1). % L recaptures dans lee surfaces G et Ext, en pourcentage du
nombre d’ animaux ldchés. % R : mémes recaptures en pourcentage du nombre
total. d’animaux recaptures a La znême date. An pourcentage de densité de
capture dans la surface PM par rapport a celle dans La surface G pour lee
non colorés seuls. A : méme pourcentage par rapport aux colorés et non co—
lorés ensemble. Rd : rapport ntre la densité de recapture dane l.a surface
PM et celle dane La surface PM + G. MG : N. giardi. LT L. terrestris.
3 1 : donnée indicponible.
lots
D
nombre
P ’
de
G
recaptu
Ext
res
TOTAL
HG
% R
LT
TOTAL
I L
TOTAL
An
A
Rd
CD
22
6
2
0
8
0
29
25
1,8
76
113
1,77
lB
27
26
2
1
29
7
50
10
2,4
58
88
2,19
3A
37
25
4
2
31
22
0
19
9,8
76
108
2,03
1A
39
12
2
6
20.
23
71
40
5,8
66
91
2,02
2A
47
53
6
0
61
9
29
13
4,7
87
157
2,05
IC
66
26
5
1
32
19
20
19
5,9
53
73
1,97
28
73
24
8
14
46
52
42
48
12,7
*
i
1,77
38
80
4
7
0
11
64
64
15,9
51
54
0,86
10
120
5
6
1
12
58
58
12,7
48
52
1,07
1E
212
5
0
0
5
0
0
0
89
106
2,35
2C I 245
4AJ263
3
0
0
0
0
0
3
0
C’
0
0
58
96
62
96
2,35
TOTAL 188 44 25 258
693
-------
FIGURE 3
Division d’une bande de pré1èveme t en prélevats. Dix prélevats
formol quantitatifg de 0,5 m 2 , cinq prélevats quantitatifs beche
aprês formol de 0,1 rn 2 et sept prélevats externes qualitatifs
au formal.
D ire eot i vo1
bêche ( /1O m 2 ) du Icher
di tins pr*leve I Ii () 1ac rt sire daccu.i1
692
-------
ration par inois ; ces phdnomènes ne peuvent être maiheureusement distin—
gues.
TABLEAU 1
Ctteaux. Conditions et chronologie des recaptures. T teinpérat-.ire du sol
a io cm de profondeur et temperature moyenne mensuelle de l’air (abbaye
de Citeaux) - pP du sol. a io cm de profortdeur. D durCe de sdjour sur le
terrain des animaux recaptures (en jours).
N°
Date
T
sol air
pFI

0
01
11
21
31
02
Décembre 77
11
13 Janvier 78
30
31
27
Février
2
.J_.
4
4
7
3
1
2
I
2,4146
2,4 48
163
64
2,3 91
12
22
32
03
13
28
13
14
Mars
28
29
7
10
71
7
10 I
10 I
2,592
2,2 1105
2,1 1106
2,1 1120
2,2 1121
23
33
04
11
Avril
12
25
10
8
12
2,6 1134
2,2 1135
2,3 148
14
24
22
Mai
14
12
,6
175
34
05
15
23
6 Juin
13
lii—
15
3,0
3,0
190
TABLEAU 2
Evolution dans le temps des recaptures de vers marques et des captures
globales. Regressions lindaires y ax + b. I.C. : interval.les de con-
fiance des coefficients a et b.
,
de Darqu6e recapturd.
par rapp.,rt aux 11ch e
nc bre to a1 de Vera capturdu
(colorda . u flon)
— x
dude de sdjour
6vo1ut 3n chrcnoLoqLq. .
Fquation
y — -0.146 x + 40.3
y — -0.659 a + 3a8
X.C.
(seuil 0.01)
-0.246 a c —0,046
25.8 C b C 54,7
— 1.237 a —0.081
264 C b C 512
69J.
-------
FXGL i : Les aires des trois prélevats de recaptures effectues a chaque
point de lAcher A Crignon.
FIGURE 1
I-
£OIELLE
2 14 S
NE
ft
1
TI
ZI
E
FIGU 2 L’aire de lãcher (aires Zt et Za) et
pour recapture (les bandes hachurées
levees).
FIGURE 2
lea bandes de pré lêvements
ont ét4 effectivement pre-.
-------
pc .is, relãchdS dans tine petite aire de 0,1 m 2 environ ciifférente du lieu
de capture, recapttirés, selori trois zones concentriqueS (fig. 1) l’aire
centrale PM recouvxaflt l’aire de rel cher. Les 3mplaceulertts de Acher
étaient dista. tS de 7 m las uns des autres. Les dates des lAchers et la
durde du sdjour au terrain ont été fort variables.
L’expérieflCe de C!tectux (d partemerit de la Cãte d’Or) a été faite
la prairie servart a la majoritd des etudes fonctionnelles de lombri-
ci s (P. 433). C’e5t une prairie perinanente a sol limono—argileuX a
pseudogley. Lea animaux captures au forniol furertt colorés au VilE aprês
identification en espêces et stades (Nicodrilus nocturnus (Evas, 194o)
N. .Zongus loriguS (Ude, 1886) ; N. loagus ripicola Bouché, 1972 parini les
aneciques ; LumbricUs astaneus (Savigny, 1826) dpigd ; enfin, pour lea
endogés, N. caligirzo3us caliginosu.s (Savigny, 1826) ; Aliolobophora i c—
terics icter.zce (Savigny, 1826) at A. roses rosea (Savigny, 1826)). Au
relAcher, les an maux furent ré—introduits en 165 points en vidant 165
boites ayant reçu 5 662 individus marques. Toutes ces boites ont reçu
uniformément les anéciques mais, faute d’un nonibre stiff isant d’animaux,
seuLement la moitiC d’entre elles ont recu lea autres aniiaaux. D’oü deux
zones différentes dans l’aire de lacher en raison des peuplements intro-
duits, ceux—ci ayant une nature diffdrente (catégorie écologique) et un
niveau different : surcharge moyenne 17 % mais 22 % dans la zone a faune
totale (Zt) et 13 % dar.s la zone & allochtones exclus .vement aridciques
(Za) (pourc ntages établis par rapport a un peuplement autochtone de 200
individus/in’) (voir fig. 2).
Lea prélèvements ont étd effectués avec La méthode formol-béche.
chaque mois, 4 bandes de 5 ni x 1 m ont €té échantillonnées a cheval sur
itaire de l&cher et l’extérieur (2 in & l’intérieur et 3 m & l’extérieur)
de façon a recenser d’Cventuels migrants hors de.l’aire. La disposition
des prélevats eat donnée fig. 3 et la chronologie tableau 1. Les préle-
vats quanti.tatifs sont appel.és A, B, C, D, S a partir de l’axe median de
L’aire, us sont dits qualitatifs si l’on y ajoute lea animaux récoltés
au même niveau par rapport A l’axe median, hors du a 2 délimité pour la
recapture. Lea bandes des préléveinents n’ont pas toutes dté utilis es en
raison d’une saisori autonnale 1978 extrémement sèche.
RESULTATS
L&chers porictuelc rdpdtds Grignon
A Grignon, on observe une baisse de captures des animaux merqués
et non marques en fonction du tempo (tableau 2). Si l’on admet que lea
résidus du mod .e liriéaire utilisé sont des variables aléatoires norma—
lea non corrélées at de même variance (ce que nous n’avons pu verifier),
lea coefficients du modéle sont significativement différents de zero au
seuul 1 % • Ceci permet de préciser le devenir des animaux marques apres
le lAcher 40 % sont recapturables “au formol”, 10 % perdent leur colo-
ration. Lea 50 % restant Sont non extraits du sol ou disparus par mortali—
té et migration. La diminution dans le temps (evolution chronologique) du
nombre de vera marques et recaptures traduit & la fois us depeupleinent
isais aussi souvent l’influence de la sécheresse et 1,7 % de perte de cob-
6a9
-------
QUESTIONS and COMMENTS
P. LAVELLE : I have studied earthworm communities along
a decreasing rainfall gradient in West Africa. I find that
the most humid ecosystems have communities composed of r and
K species. Then, when rainfall decreases K species disappear.
Do you think 5esert ecosy ems could be considered as systems
reducted to r components?
J.A. WALT.MOBK : As far as our present knowledge is con-
cerned, I do inde . d believe that this is the case in hot
deserts. However, I am not sure that this applies equally
to cold deserts; more data must be obtained from these before
any firm conclusions can be drawn.
M.S. GHILARDV : What was the maximum depth of soil layer
you nave eximined? In the desert xnicroarthropods can exist
at significant depths where conditions are rather stable and
selection is of K-type (Examples of larger forms are Hentolepistus
woodlice).
J. . WALLWOI : I sampled to a depth of 14 cm, and I agree
that this procedure may have ncglected deep-dwelling species
which, indeed, may be K-selected. However, my primary interest
was with that part of the soil ecosystem assuciated with the
surface litter and the mineral soil immediately beneath this
litter, for it is here that the major part of organic decompo-
sition is occurring.
M. HASSALL : With respect to your suggestion that the
predatory species you described are not food limited, may
there be a parallel here with the herbivore systems in African
grasslands, described by Sinclair (1975) who found that al-
though primary production of food species was well in excess
of the amount consumed by herbivores, the herbivores were still
food limited because of seasonal discontinuities of food supply.
Is there a possibility that food could similarly be limiting
the predatory species in the desert where prey species are
at a minimum e.g.. during March?
7. . WALLWORK : This is possible, but I don’t think it
is probable. In fact, there is no short answer to this question.
In a global sense. I do believe that herbivores are predator—
limited, rather than food-limited. Again, by the sante token.
predators are limited by their food supply in a global sense.
But the desert system that I have been studying, the absence
of a lag phase in prey and predator population increases does
not suggest a negative feedback at the times of population
recruitment. As M. Hassall rightly points out, however, there
may be periods of the year when predators could experience
food shortage, and limiting effects could then come into the
picture. I would suggest that the predatory species Spini —
-------
bdella cronini responds to this situation in one (or both) of
two ways. Firstly it does not recruit during periods of food
shortage. Secondly, it avoids such periods of f’od stress
by mobilizing food reserves laid down during times of plenty.
While I have not been able to demonstrate that S. cronini does
in fact do this 1 I have established elsewhere that predatory
mites can make this provision. If S. cronini follows this
pattern, it need not experien:e periods of food stress, and
its subsequent fecundity would not be impaired.
B. STEVENSON : Do seasonal “pulses” in annual desert
climate produce changes in carrying capacity (e.g. does rain-
fall increase K for microarthropods)? Is it possible for
arthropods to track (with changes ii . population density)
changes in K?
WALIWORK : My observat...rns in the Mo;ave cannot
provide an answer to this question, for I was not able to
establish what was the carrying capacity of the system. I
am able to say that population densities of microarthropods
are lower than in cool, moist, temperate ecosystems but the
important part to establish, which I did n , was whether
these densities were low in relation to the carrying capacity;
this determines the type of strategy employed, and if my case
rested on this criterion alone, it would be hardly defensible.
However, it does not, and in the event, work in progress has
shown that microarthropod densities will tncrease in artificially
watered plots, and in sites immediately subjected to rainfall.
So. the answer to both your questions is an affirmative: yes.
environmental pulses produce changes in carrying capacity,
and yes, microarthropods can track these changes. This is
an opportunistic strategy.
M.J. MITCHELL : Do you have any information on whether
specific population “r” or “K” characteristics, such as
fecundity or rate of increase have been selected for in the
arthropod populations?
J.A. WALLWORK: No, the scope of my investigation did
not allow for estimates of fecundity or rates of increase in
populations.
-------
ARTHROPODS AND DETRITUS DECOMPOSITION IN DESERT
ECOSYSTEMS
Walter G. Whitford and Perseu F Santos
Nvw Mexira Staie’ L1nit’erst y
USA
INTRODUCTION
The mountain and basin topography of the desert areas of North
America has a profound effect on the distribution and redistribution of
dead plant material (litter). Topography has an effect on deiftity and
species composition uf vegetation especially along water courses and
redistribution of Litter by sheet flcw of water and by wind. Litter
act.umulates under shrubs and along edges of water courses and is buried
in depressions or where snags, rocks or obstructions create wind and
water eddy currents. Santos, DePree and Whitford (1978) have shown
that tile density and diversity of the soil microarthropod community
varies directly with the amount of organic nM.ter present, hence, are
directly related to topography.
Studies of the soil fauna of the worlds’ deserts are limited
(Wa].lwork, 1970. 1972; Wo3d, 19’l; Freckman, Mankau, and Ferris, 1975)
and there have be.-n no quant3.tattve studies ot the role of soil fauna
in decomposition and nutrient release from plant litter. In 1977 we
initiated a series of studies to examine the rolc. of various taxa of
desert soil fauna in decomposition and in mineral release processes.
In this paper we review selected portions of those studies in order
to illustrate the relationships of termites, microarthropods. nematodes
and soil microflora in litter decomposition in North American desert
ecosystems.
STUDY SITES
Most studies were conducted on the New Mexico State University
Experimental Ranch 40 km tiE of Las Cruc e. NM. The study site is an
alluvia]. pediplain (bajada) of Mt. Summerford drained by a large dry
wash (arroyo) and dissected by n erous smaller arroyos which empty
into the main drainage chann. 1. The large arroyo drains into a dry
lake at the base of the water ed. The alluvial fan has a vegetative
cover of approximately 27% of which creosotebush, Larrea tridentata ,
accounts for 89%. The subdominant shrubs are mesquite, Prosopis
1.05% cover; tarbush, Flourensia cernua , 1.00% cover and
snalceweed, Gutierrezia app., 0.652 cover are 1.ocated at the edges of
the a royos. Summer air temperature maxima vary between —5°C and 10°C.
Mean summer (Nay—September) soil temperatures at 10 cm vary between
25”C ard 37°C in the s er months. The 100 year average annual rainfall
7?O
-------
± one standard deviation is 211 77 mm (Houghton, 1972) with m. st of
that rainfall o curring in July-September from convectional storms.
Four additional sitee were used to eompare microarthropods and
bacteriophagic nematodes in North American hot deserts. T e Sonoran
desert site is a sloping alluvial pedipj .ain of the Sierra Estella Mts.
32 km west of Casa Grande, Arizona. The bajada is dissected ‘ y several
small arruyos. The vegetative cover was visually estimated at 2 )% with
a mixture of creosotebush, La-ma tridentata ; palo verde, Zercidium
microphyllum ; sagauro cactus, C. reus giganteus ; and ironvood, Olneya
tesota . Summer te&perature maxima regularly reach 40°C. Average annual
rainfall is about 2J6 zmn with both winter and summer precipitation.
The Coloradan desert site is 3 km east of Clamis, California on
a gravel—rock pavement vi..h a sparse (less than 5%) cover of cresotebush,
ironwood and Encelia farinosa . Here the summer temperature maxima
regularly exceed 40°C and average rainfall is 68 imn with most of that
falling between December and March.
The Mojave desert site is 30 km ESE of Boulder City, Nevada on
a gently sloping bajada dissected by numerous small arroyos. Vegetative
cover is around 20% most of which is creosotebush with Yucca schottii as
subdominant. Summer temperature maxima range between 38°C to 40°C;
the average annual precipitation is 131 mm priinar’ly in the winter months.
METHODS
All of the decomposition studies reported herein utilized fiberglasz ,
mesh bags initially containing 30 gms of litter for surface bags a-id 20
or 30 gas for buried bags. Arthropods were excluded from litter bags by
treating the litter with the insecticide chiordane (TM). The litter was
either mixed litter (termite studies) conr.aining about 60% creosotebush
( Larrea tridentata ) and pieces of grass and forbs or just creosotebush
litter which consisted of freshly piflked, air dried leaves and small
twigs. Bags were placed on the surface under the canopy of creosotebushes
or buried 15 cm below the soil surface under creosotebush canopies.
Microarthropods were extracted in modified Tullgren funnels into
water and counted within 24 hours after extraction was completed (usually
72 hours). Nematodes were extracted from the litter by a combination of
the Cobb sieving mathod and the Oostenbrink cotton—wool filter (Nichols,
1975).
Organic matter loss was determined by ashing oven dried contents
in a muffle furnace and correcting for mean initial organic content of
the sample and organic content of the soil in the area where bags wete
placed. Bacterial numbers were estimated by direct counts of cells of
homogenates of “lant material stained with Acridine orange and counted
with a UV microscope.
m
-------
RES uLTS
In mixed litter during the perioc of peak surface foraging by
the subterranean termites, Gnathamitermes tubiformans , surface bags
in which termitLs foraged as evide 4 ced by galleries helovi the bags
and carton in the bags, lost 57.4 — 7. % of the initial weight, while
bags in which termites were excluded lost 32.3 ± 4.6% of the initial
weight. This experiment was conducted from mid—August through October.
Litter bags buried from the end of July through October lost
42 — 10% of the original organic matter. The microarthropod community
in surface begs during that period was more diverse but the taxa in
buried bags occurred in significantly greater densities (Table 1).
Mixed litter buried for 90 days had a fauna dominated by tydeid and
pyemotid mites and Psocuptera. There we€e no clearly dominant
microarthropods in surface litter (Table 1). However, most of the
surface litter mites were predatory Prostigmata.
TABLE 1. Comparison of microarthropod communities In 30 gms of nu.xed
creosotebush litter in buried and surface bags Jul ’-0ctober. Numbers
are mean nunibers ± standard deviation per bag. Buried N 10, Surface
N = 8.
TA A BURIED SUPIACE
Cryptostiginata +
0ribat id 3.8 — 0.4
Prostigmata +
Tetranychidae + 1.3 0.8
Tydeidee 200 — 35 3.5 — 3.0
Pyemotidae 499 ± 65 +
arsonemidae 9 * 7.6 5.3 — 2.2
Nanorchestidae 7.8 ± 0.8
Bdel].idae 43 ± 1.2
Smaridiidae 1.1 * 0.7
Cunaxidae 0.8 * 0.5
Mesostigma a +
Rhodocaridae 9 - 3.3
Lae lapidae. 3.1 ± 1.4
Psocopt era + +
L.iposcelidae 44.4 — 5.3 3.1 — 1.2
Trogiidae + 7.4 ± 3.2
Collembo la 8.5 — 5.8 0.2 ± 0.2
In experiments in which we examined the effect of eliminating
inicroarthropods on organic matter loss and other components of the
litter decomposer community, we found that the initial mite colonizers
were tydeid mites which entered the buried litter within 5 to 10 days
after burial. After !O days, insecticide treated bags had significantly
higher populations of bacteriophagic nemRtodes, lower numbars of bacteria
and significantly less organic matter loss (Table 2).
m
-------
TABLE 2. The effect of eliminating Tydeidae mites fr ’o b ied litter
on other components of the litter system and on org tic a erter loss
in 30 gas of creosotebush litter buried for 10 da ,s.
Insecticide (chiordane)
— UNTREATED TREATED
— + — +
x - SD x — SD
Tycleidae (no./bag) 85 25 0
Bacteriophagic + +
Neinatodes (no./bag) 109 — 52 600 — 225
Bacteria (no.1gm litter) 3.3 x 2.0 x io6
Organic matter loss 20.7 * 2.3% 5.6 ± 2.5%
Excep in the hottest and driest desert, the Coloradan, we found
that eliminating the microarthropods resulted in a significant increase
in free living nematodes Table 3). Buried creosotebush litter in the
Co].oradan desert also had significantly lower microarthropod populations
tha in the other hot deserts. The faunas ir buried litter in the
Sonoran, Mojave and Coloradan deserts differed from the Chihuahuan by the
absence of tarsonemids which were the most numerous mites in the material
from the Las Cruces, NM area (Table 3). Also liposcelid psocopterans
were absent in the o month buried bags from the Chihuahuan area .ind
predominant in the buried bags from the other deserts (Table 3). However,
liposcelid psocoptexans were present in the iiihuahuan area in three
month buried bags (unpublished data) and were always found associated
with collembolans which were not present in the other descrts.
Raphignathidae are the most common predators in the Sonoran, Mojave and
Coloradan deserts (Table 3). There was a great diversity of predatory
mites in the Chihuahuan desert. Raphignathids were part of the predatory
complex in bags buried for 90 days in the Chihuahuan desert area
(unpublished data). The taxon common to all of the deserts in the two
month buried bags was the tydeid mites which are the first colonizer and
apparent nematode predators.
77,
-------
TA3LE 3. A comparison of free living neniatodes and aoL ]. microarthropods extracted from buried 20 gm
creosotebush litter in Ielected North Meri an desert sites. Numbers reported are nuthers per litter
bag. Two litter bags from each site were extracted for nenatodes and three extracted for mircoarthropod3.
Chihuahuan Sonora Coloradan Mojave
Las Crucea, NM Casa Crande, Glamis, Boulder City,
Arizona California Nevada
Nematodea (NT) 50— 161 394— 1050 416—3774 3600- 3878
Nematodee (IT) 1937—2155 6395—11164 968-1050 11800—12408
Tydeidae — 156 ± 36 17.3 ± 4.2 3.3 ± 1.52 8.25 5.56
Taraonemidae — 7345 ± 1681
Raphignathidac 17 ± 5.5 1.3 .57 19.5 13.4
Liposcelidae (Psocoptera) — 153 ± 87 12 ± 2.3 12b ± 75
Other predatory mites — 461 ± 167
Period March 14, 1979 to June 1979.
-------
DISCUSSION
Johnson and Whitford (1975) estimated that on the Jornada
subterranean termites consumed 5.6 x 106 cal.ha 1 and that total
detrital input including cattle dung and rabbit feces was 10.3 x
106 cal.ha . Their estimates were based on paper consumed from
toilet paper roll baits. FowI.er and Whitford (unpublished data)
showed that termites did not uti1iz creosotebush leaf litter.
Data reported here suggests that termites harvested the annual
forb—p’zrts and bits of grass from the mixed litter leavtag the
creosotebush leaves to be broken down by the other desert litter
feeders. Gnathamitejmes tubiforinaus builds gallery tunnels into
surface accumulations of litter and tran3port pieces of litter
material to some unknown depth in the soil. In late suer and
autumn when relative humidity varies between 50% and saturation,
G. tubiformans builds galleries around standing dead vegetation
which is completely harvested. Fowever, since annual forb
production is only around 4 kg .ha 1 - depending on rainfall (Whitford,
1973), organisms that process the leaves of creosotehush must be
more important to the nutrient cycling economy of this system
than the subterranean termites. Data on forage selection of C.
tubiforinana suggests that the consumption :ates estimated from
bait rolls overestimate consumption of natural plant materials.
However, these must be cot.sidered tentative conclusions and must
await additional data on the role of termites on decomposition
processes.
Although there was a higher diversity of microarthropods
in surface litter bags than in buried bags in late s* er,
microarthropods are completely absent from surface litter during
some parts of the year. It is possible that there is a diel
migration of microarthropods from the soil into surface litter
and back into the soil depending upon the moisture and thermal
gradients between soil and litter. The predominance of predatory
mites in surface litter suggests that there may be significant
populations of nematodes in surface litter but this remains to be
doeume’ ted. The predominance of tydetd, tarsonemid and pyemotid
mites in buried litter and the b(gher population numbers probably
result from the more constant end favorable temperature and
moisture conditions of buried litter in comparison to surface
litter.
We have both indirect and direct evidence that tydeid mites
prey on nematodea. In the mite exclusion expim, ..acteriophagic
nematode numbers were 6X greater in the insecticide treated bags
when tydeid mites were excluded. We have observed tydeid mites
feeding on “ “ todea in laboratory culture. We suggest that these
mites affect organic matter breakdown by preying on bacteriophagic
nematodes which reduce the primary decomposers: the becteria.
The reciprocal relationship between mites and nematodes is
comson to the wetter ? erth American deserts but appears to break
down in the driest deserts. At the time of this writing climatological
775
-------
data for the Arizona nd Nevada reporting stations was available
only through March 1979 (National Oceantc and Atmospheric Admin-
istration Climatological Data, National Climatic Center, Ashville,
NC). The March data show Casa Grande, Arizona receiving 30.2 mm
of rainfall above normal, Boulder City, Nevada receiving 28.2 n
above normal and Yuma, Arizona (nearest reporting station to Glamis,
Calitornia) receiving normal rainfall. Rainfall during March—May
on the Joruada was more than 60 mm above average. The differeaces
in mite taunas in the litter buried in these areas from mid—March
through May undoubtedly reflect that rainfall.
It is also possible that the higher temperature in the
Moja; , Sonozan and Coloradan deserts in addition to moist soils
reeulted in rapid decomposition of the creosotebush litter. Santos
and Whit ford (unpublished data) have shown a succession in soil
inicroarthropods associated with the degree of organic matter break-
down. The litter communities in the otheL hot deserts with the
large n mbers of psocoptera are similar to communities found in
litter buried in the Chihuahuan desert f or 90 days in the simmer.
Many of tI’ese questions will be answered when more complete data
are available in a comparison of the hot deserts.
The data presented and discussed here allow us to produce a
tentative picture of the trophic relationships and dynamics of
desert litter processors (Figure 1). Whera present, subterranean
t3rznites probably process a significant proportion oL standing dead
annual3 and grasses as well as the fecal material from cattle and
lagamorphs. The relative amounts and types of litter consumed
require study in other deserts. When termites harvest material from
the surface that material is translocated to some as yet undetermined
depth in the 30i1 where it is converted to termite biomass. The
depth and location of termite colonies in the desert soil thus
determine where these energy ann nutrient sinks are located. Returns
to the shallow soil occur via predation on termite workers by lizards
and ants and by death of alates. We know very little about the size
of these fluxes and although we are currently studying them, it will
be several years before we can make an accurate assecseent of the roLe
of termites in decomposition and nutrient release in desert ecosystems.
The processing of leaf litter on the soil surface is also not
well understood. We know that organic matter loss from surface litter
occurs at rates similar to that of buried litter for the same time
periods and that dur1n wet periods there is a complex mite fauna in
the surface litter. Also we have recent evidence that nematodes are
present in dry mixed creosotebush litter (unpublisned observations in
collaboration with D. Freckman). We hypothesize that the processing
of surface litter is the same as buried litter (Figure 1) and that
there are diel migrations of mites and ne iatodes into and out of the
litter dependent upon moisture conditions in the litter and soil.
Studies are in progress to examine these relationships.
The processing of buried litter and annual roots is the moat
completely studied part of the system (Figure 1). Our data indicate
776
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that the initial decomposition (organic matter loss) is due to
bacterial activity. Although fungi are present the fungi do not
appear to be contributing very much to initi&i. C02 production and
organic matter breakdown. Protozoans and bacteriophagic nematodes
enter buried litter and establish large populations within a few
days after litter is buried. The populations of nematodes are
initially controlled by tydeid mites. After approximately 30% of
the or. ginal rganic matter has disapp. arvA, fungivorous tarsoneinid
and/or pye tid mites begin grazing on the fungi and fungivorous
nematode populations increase. In later stages of decomposition
predatory Gamasina mite populations increase and they reduce the
grazing mite populations as well as the fine living nematodes. In
late stages of decomposition, psocopterans and collembolans make
up a substantial part of the leaf litter community (Figure 1). We
have no data on the trnphic relationships of psc,copterans and
colleinbolans in desert litter communities.
The limited data from the other North American hot deserts
suggests many simflarities in the litter community structure and
processing of dead plant material. We expect the similarities to
bc. great and for the differences to be instructive.
LITERATU CITED
Freckman, D., R. Mankau and H. Ferris. 1975. Nemato.ie
community structure in desert soils. Nemacode Recovery. . NemaLol.
7:343—346.
Johnson, K.A. and W.G. Whitford. 1975. Foraging ecology and
relative importance of subterranean termites in Chihuahuan desert
ecosystems. Environ. Entomol. 4:66-70.
Nichols, W.L. 19Th. The biology of free—living nematodes.
Clarendor , Press, Oxford. 219 pp.
Santos, P.F., K. DePree and 4.G Whitford. 1978. Spatial
distribution of litter and inicroarthropods in a Chihuahuan desert
ecosystem. J. Arid Environ. 1:41-48.
Waliwork, J.A. 1970. Ecology of soil animals. UcGrav—Hull,
Inc., I.ondon.
Wallwork, J.A. 1972. Distribution patterns and population
dynamics of microarthropods of a desert soil in southern California.
3. Anim. Ecol. 41:291— i1O.
Wood, T.G. 1971. The distribution and abundance of Folsomides
deserticola Wood (Collembola: lsomidae) and other microarthropods in
arid populations. Pedobiologia 11:446—468.
ACKNOWLEDGEMENTS
This research was supported by Grant DEB—77—16633 from the
National Science Foundation.
-------
APPENDIX I.
List of scientific names of plants and families of arthropods.
Plants
Cercidium inicro hyllum (Torreynum)
Cereus (Enge1n n)
Encelia farinosa (Gray)
Flourensia cernua (DC.)
Gutierrezia app. (BrI.cton and Rusby)
Larrea tridentata (Coville)
Olueya tesota (Gray)
Yucca schottii (Enge1 ii)
Arthropods
Acari
Bdellidae (Duges)
Cumidae (Thor)
Laalapidae (Berlese)
Nanor hestidae (Grandj ean)
Oribatid (Duges)
Pyeinotid.ae (Oudeuians)
Raphignathidae (Kramer)
Rhodacarida e (Oudemans)
Smaridiid e ((Kramer)
Tarsonemidac (Kramer)
Tetranychidae (Donnadieu)
Tydeldae (Kramer)
insecta
Cnathamitermes tubiformans (Buckley)
Psocoptera
Liposcelidae
Trogiidae
778
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.
SOIL ANIMAL SPECIES DIVERSiTY IN A SEPARATED DUNE
GRASSLAND ECOSYSTEM
Ryszard K. Cykowski
InsIii e of Bio1o y WSP
Poland
INTRODUCTION
Faunal investigations of isolated dune biotopes pro-
vide much important information for rational management of
natural resources. They ensure a better analysis of the
fauna—floristic complexity and the regulation mechanism of
ecosystems productivity.
The purpose of the present investigation was the nalyc s
of:
1) horizontal and vertical distribution of soil fauna de-
pending on its directional exposure and the height of
a grey dune,
2) quantitative and qualitative changes of the developmental
forms (larvae and pupae) of soil ontoniofauna,
3) the structure of dominance and species density of soil
fauna in the isolated dune ecosystem.
METHODS
The investigations in June and July 1976 - 1978 followed
preliminary observations in 1 .975. Soil sampling after Ghilarov
1965 was the method applied here and 144 samples each 05 x
0,5 in by 30 cm deep including the vertical distribution of
0-10, 10—20 and 20—30 cm were collected.
The isolated dune biotope studied is one of the highest
(50 n altitude) in the Czo ptf skie Dunes situated in Saowiz ski
National Park. The flora of this biotope represented a typi-
cal complex of grey dunes called Elymo-Amrnophiletum Festu-
cetosum arenariae by Wojterski (1964).
7 ,9
-------
S
Twelve investigation sites were set up in this eco-
system, 3 each to analyse the north, south, east, and west
sides of the dune; also the foot, the middle and the top
of the isolated dune biotope were sanipled.
RESULTS
No marked differences among the soil faunal comxnuni—
ties of isolated dune biotope ware observed in the respec—-
tive years. Among animal communities coexisting in sandy
dune soil the Coleoptera (95%) dominated over the Lepidoptera
(3%) and Diptera t2%) (Figure 1).
Among developmental forms of soil entomofauna imagines
comprising (81%), Malachius aeneus L.. Philopedon plagiatus
Schall. and Aegialia arenaria Thr. dominated over the 1arv 1
forms (11%) Anomala aenea Deg. plagiatus, Polvphy].la
fullo L. and pupal forms (8%) A. aenea , P. plagiatus forms.
Vertical distribution analysis showed that 81% of
soil fauna was found in 0-10 cm, 17% in 10-20 cm and 2%
in 20-30 cm samples (Figure 1). Malachius aeneus , P. plagiatus
and Coccinella septempunctata L. were the dominant species
in the 0—10 cm samples, while P. p1aq iatus , A. aenea and A.
arenaria in the 10-20 cm samples and . piggiatus and A.
aenea in 20-30 cm strata.
Soil fauna was concentrated mostly at the foot of the
dune biotope (81%) fewer in the middle (11%) and the least
at the top (8%) (Figure 2). At the foot of the dune such
species as P. plagiatus , C. septeznpunctata and A. arenaria
were predominant whereas M. aeneus and . plagiatus in the
middle, and . aeneus , arenaria at the top.
Summing up. the species composition of the following
soil fauna, P. plagiatus (21%). Malachius aeneus (17%), A.
arenaria (14%), C. septempunctata (12%), A. aenea(9%) and
Demetrias monostiqula Sam. (5%) • were the predominant species
(over 5% dominance). These species were found most often in
the south side of the dune (38%), less in the east (33%) and
the least in the west (18%) arid north (11%) (Figure 3).
780
-------
3% Z%
—nfl—--
- a_a_
o . -
%J _J r- 1
0
117%
r
— — I I I

d
I
CONCENTRATION OF SOIL FAUNA, VERTICAL DISTRIBUTION
AND DEVELOPMENTAL FORMS OF SOIL FAUNA IN ISOLATED
DUNE ECOSYSTEM.
Figure 2: CONCENTRATION OF SOIL FAUNA AT THE FOOT (F), IN THE
MIDDLE (M) AND AT THE TOP (T) OF AN ISOLATED DUNE
BIOTOPE (%).
Figure 1:
H
L
]
i(4i%)
I
[ _F ( 1 )
783.
-------
N -
W - 43’.
E — 35’ !.
S — WI.
Figure 3: DISTRIBUTION OF SOIL FAUNA ON THE SIDES OF TEE
ISO LP 1 TED DUNE ECOSYSTEM (%).
Soil fauna density analysis (individuals/rn 2 ) showed
that the density coefficient was the highest, 9, on the souti
side at che foot of dune biotope, 8 in the middle, and . i at
the top. On the east side likewise, 9 at the foot. 5 in the
middle, and 5 at the top. On the west si Ie at the foot the
density coefficient was 6 and 2 in the middle and at the top.
and on the north 2 at all three levels (Figure 4).
Varied species dominance was distinguished when analysing
the directional sides of the dune. Philopedon plagiatus was
dominant on the south, A. aenea on the east, A. Arenaria and
. septempunctata on the north, and A. arenaria on the west side.
782
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1.11::
Figure 4: DENSITY COEFFICIENT ON DUNE SIDES AT THE FOOT, IN
THJ MIDDt ND AT THE TOP OF ISOLATED DUNE ECOSYSTEM
(individuals/rn 2 ).
RECAPITULATION
The investigation gave information about faunal corn—
utunities in sandy soil of a isolated dune grassland ecosy&tem
(Elymo-Ammophiletum). Coleoptera prevailed among soil faunal
communities (95%). Fauna was concentrated mostly in soil 0—10 cm
deep, particularly on the south and east sides at the foot of
the isolated dune ‘ecosystem. On the south side of dune bio—
tope, Philopedon plagiatus was the predominant species where-
as Anomala a nea on the east side, Aecda arenaria on the
west and A. arenaria and C. septempunctata were dominant on
the north side.
The above mentioned faunal communities are determined
by weather conditions such as winds, air—temperature and in-
solation. In spite of d ininance of phytophages (51%) no
deleterious influence dangerous to fauna of isolated dune
ecosystem has been observed so far.
783
-------
ACKNOWLEDc 4ENTS
This study was coordinated with the Institute of
Ecology — Polish Academy of Sciences, Dziekanow Le ny near
Warszawa, Poland.
REFERENCES CITED
Ghilarov, M.S. 1965. Zoological methods in soil diagnostics.
Moskau: “Na a” , pp. 80—96.
Wojterski, T. 1964. Bory sosnowe na wydmach nadmorckich
na Poiskim Wybrzezi. PW?L Poznai(, pp. 180-201.
-------
DIVERSITY TRENDS AMONG THE INVERTEBRATE UTTER
DECOMPOSERS OF A SUBALPINE SPRUCE-FIR SERE: A TEST
OF ODUM’S HYPOTHESES
Lloyd W. Bennett and Richard T. Vett,. r
Utah 5Ia , Lbtivirrsity
USA
In 1969 Eugene Od.um propounded 2 1 e attributes of ecosy-stems which,
theoretically, ui dergo systematic change during succession. The atti-i—
butes are grouped into the following categories: community energe ;ics,
community structure, life history, nutrient cycling, selection pressure
and overall henieostasis. Most of the predicted trends are at least
potentially testable, while a few are basically vague. To date the
testable hypotheses have not been tested en mass on one ecosystem
involving a straightforward, succession. Further, no studies have
addressed them in which essentially all higher taxa have been studied
zimultaneously. Clearly befo e Odum’s hypotheses can form a basis for
understanding suceessinna], trends of ecosystems, their validity must be
determined. Preliminary results of a study of invertebrate litter
decoinposers reported here represent part of a large—scale effort to test
most of Oduin’s hypotheses simultaneously utilizing data on all important
taxa present within a subalpine spruce—fir successional ‘equence.
MP 1 TERIALS AND TH0DS
The study area was located in the Wasatch Mountains of northern
Utah, U.S.A., at elevations between 2550 in and 2600 m. Study plots were
established atop an undissected plateau—like ridge of gentle topography.
Further details of the area were discussed by Schimpf, I{end.erson and.
MacMahon (1980).
The successional sequence studied and believed to be a ebrono—
sequence (Schimpf et al., 1980), began with herb—dominated meadows which
were invaded by quaking aspen ( Popu.].us trcmuloides) . The latter were,
in turn, invaded and replaced by subalpine fir ( Abies iasioc er pa ) which
was succeeded by Engelaann spruce ( Picea engelmannii) . A mixed spruce—
fir forest was the apparent local climax.
Three replicate acres were selected for detailed. study. Within
each sere, plots measuring 20 in by 25 in were established. Each plot
WftB divided with twine into square meter arc .s Each square meter from
which samples were taken was selected. from ‘oordinates generated by a
computer—run, random numbers program. Numbers were generated without
785
-------
replacement so that no square meter was sampled more than once. During
the summer the three replicate.. were sampled on a 3—week rotation. Two
of the replicate seres ver sampled only during snow—free conditions.
One, designated Cattle Gu ’ .rd, was also sampled during winter at 3—week
intervals for the moderate snow depths (1.5 m) which prevailed during
the time interval herein reported. The present report spans the dates
from 14 August 1976 to 16 Augu5 1977. It must be noted that after
11 November 1976, analyses of i11 sample periods for which samples were
collected. were not available.
Samples were collecte’i wtth ‘t band-operated, garden—type coring
device with a cross—sectional area. of 38 cm . Cores extended through
the litter layer, if present, and 5 cm into the mineral soil. The lit-
ter portion was removed by band and placed in a plastic bag. The remain-
ing soil was placed in a separate bag. Four cores were collected from
the centers of the ii quadrates composing the square meter. All litter
thus collected from a square meter was placed in a single bag and mixed.
The soil was treated similarly. For a given sample date, ‘within each
seral stage 5 square meters were sampled. Since the meadows lacked
litter, a given sample date is represented by 35 samples. The samples
were returned t the laboratory and processed immediately.
The samples were first weighed and ve ghed subportions removed
for extraction of nematodes. The remaindar was used for extrsction of
artbropods. Nematodes were extracted by a technique essentially
identical to that of Uhlig (1966, 1968). Other prGcedures, based on
flotation of the neinatodes on various soluticns, were tried ‘out were
found to be ineffective for samples containing appreciable quantities
of litter. Artbropods were extracted. using Tuligren funnels. Extrac-
tions were analyzed by assigning indiiidual ,rganisms to an “opereti.g
taxonomie unit” or species and making counts within each such ‘mit.
This procedure was necescary due to the apparent abunJance of und .escribed
taxa. The data were stored on magnetic tape for subsequent conij 1 uter
analysis. For the prescnt preliminary analysis, data for the litter and
soil portions of each sample were combined. For each acre.]. stage for
each date, and separately for nematodes and artbropods, the total number
of speciea, the Shannon-Wiener index of diversity (H’) and the index of
equitability (3) were calculated. The results are presented graphically
in figures 1-6.
RESULTS AND DISCUSSION
Od mi’s hypotheses eight and nine, respectively, predict that
species diversity (variety component) and species diversity (equit-
ability comr.onent) should proceed from low to high across succession.
The variety comçonent itself is here resolved into two components:
786
-------
total number of species (species richness) and H’, the Shannon—Wiener
information diversity index. For nematodes, the species richness
(figure 1) in the meadows ranged between 6 and 22 and, except for a
slight overlap on two dates, Is clearly less than in the other seral
stages. Species richness in ehe aspen, fir and spruce were similar
and ranged between 26 and For some dates the number were rather
different; however, from one date to another the tree stage with
maxiinum, intormediate and minimum numbers of species changed. The
Shannon—Wiener index for nematodes (figure 2) varied from 0.7 to 1.3
and generally reveals no clear—cut differences between the seral
stages, except possibly that the value for the meadows was somewhat
less. The order of seral stages with maximum to minimum clearly
changed from date to date. The index of equitability, J, (figure 3),
ranged from 0.56 to 0.95. Again, no clear trends were evident with
the oeral stage order of maximum to minimum J varying across the
sample dates.
Species richness for the arthropods (figure 14) varied between
1 and 514. Values in the meadows were consistently less than in other
stages for the same date and did not overlap with them. In the aspen,
fir and spruce stages the numbers were higher with the stage order of
maximum to minimum varying from date to late. H’ (figure 5) varied
from 0.2 to 1.14 with values in the meadows generally lower than in the
other seral stages and much more erratic. Values in the tree stages
were higher and less erratic. Further, the order or maximum to minimum
values in the tree stages varIed across the sampling dates. Equ5tab llity,
J, ranged between 0.0 and 1.0. The values were highly erratic In the
meadows; otherwise no clear—cut trends were evident. The seral stage
order of max 1 ”um to minimum values for all four stages changed across
sample dates.
Species richness for both nematodes and arthropods (figures 1
and 14) were generally lower for the meadows; however, no successional
pattern was evident for the aspen, fir and spruce stages. The values
of H’ (figures 2 and 5) were somewhat lover in the meadows with no
emergent pattern in the tree stages. These results appear to contradict
Odum’s hypothesis concerning the variety component of diversity. The
values of the equitability componeut, J, (figures 3 and 6) for both
neinatodes and arthropods revealed no clear s’tccessional treads. There-
fore, these data seam to contradict Odum’s bypotbesis relating to the
equitability component of diversity. For thcse preliminary analyses
great caution must be exercised in reaching any firm conclusions. Sub-
sequent calculatIons will be performed on the separate soil and litter
faunas. Farther, the effects of varying litter amounts among the
actual sites sampled, water content, temperature and season will be
assessed. It is possible that these more detailed analyses will reveal
more clear—cut trends with which to test Odum’ s hypotheses.
787
-------
FIGURE 1. Species richness for n natodes.
w
2
I
U
U’
w
U
w
0 .
4
50
40
30
20
I0
FIGURE 2. Shannon—Wiener diversity index
3.0
2.5
2.0
1.5
I.0
0.5
0
N
.4
DATE
(H’) for n atodes.
00
...
•* . . ..
_0_ 0
— . .. -d
- .4 -e .
- e - d -4 .4
0
DATE
NEMATODA MEADOW
ASPEN
FIR
SPRUcE —
78R
-------
FIGURE 3. Equitability index, J, for nematodes.
MEADOW
NEMATODA ASPEN —
t.ooo FIR
SPRucE—
aeoo
0.600 \
0.40U
azoo
0 .000 N OO o-
DATE
789
-------
JACCARO C0EFF1C1EtiT
NEP1ATODA,P JANUARY
FIR
0.60
MEAD OW 0.09— ASPEN
0.00 0.34
SPRUCE
JACCARD COEFFICIENTS
ARTHROPODA FE3RUARY
S
FIP
0.29 0.48 .45
IiEADOW 0.31— ASPEN
0. v
SPRUCE
790
-------
FIGURE . Species richness for arthropods.
‘v ‘I ‘
A
F’
:: -—
DATE
— OOOO


FIGURE 5. Shannon-Wiener diversity index (H’) for
3 . 0
tb
2.0
• 1.5
*0
as
arthropods.
-1
-4
z .. .
.4 -1 -4
- -4-4-1
ARTHROPODA
MEADOW
ASPEN
FIR
SPRUCE —
5 .
40
Sc
20
I0
0
-.4 .4 4 -4 -4.4
a’ a’ a’ a’ a’
MEADOW
ASPEN — — ——
ARTHROPODA FiR
SPRUCE
0
-------
FIGURE 6. Equitabi] .ity index, J, for arthropods.
APTHROPODA
I.000
80o
‘ 0.600
0.400
I l
MEADOW
ASPEN —-
Fm —
SPRUCE —
N
0 N
g 0
.4 .9
DATc
-------
LITERATURE CITEt
Odum, E. P. 1969. The strategy of ecosystem development. Science
161e: 262—270.
8chimpf, D. J., 3. A. Henderson and J. A. MacMahori. 1980. Some
aspects of succession in the spruce—fir forest zone of
northern Utah. Holarctic Ecology (in press).
Uhlig, G. 1966. Untersucb’ungen ZUr bctraction d.er vagilen Milaro—
fauna aus marinen Sedimenten. Zool. Ariz., Supp].. 29:.L51—15T.
Ublig, G. 1968. Quantitative methods in the study o interst. tial
fauna. Trans. Amer. Micros. Soc. 87:226—232.
QUESTIONS and COMMENTS
3. CURRY: Could you comment on the biological sig-
nificance of H’ as a measure of diversity in view of the
rather anomalous results it appears to give in your data
‘when the meadow community is compared with those in the
spruce—fir sites?
L.W. BENNETT: H, an ir’formation index of t1iversity,
is not especially intuitive in a biological sense. It
requires much more thought to make an adequate response.
J.A. ADDISON : Were all your sites at the same elevation
or were you looking at changes along an elevational gradient?
L.W. BENNETT : All sampling sites were within Ca. 100 m
of 2,500 m elevation.
. FRECIQIAN : Sample size? determinati of extraction
efficiency? Does your method select for certain TG? What
does TG (community structure) look like?
LW. BENNETT : Sample size: ca. 38 cm 2 of soil, to a depth
of 5 c m and through whatever depth of litter. Samples were
taken from 5 randomly chosen square meters froni each seral
stage on a 3 week rotation. Extraction efficiency: Rough
estimates at present suggest approximately 75% efficiency
for most nematode groups using the Uhlig method. (Community
structure will be discussed in subsequent papers).
793
-------
. STEVENSON : It would seem to me that changes in the
components of B’ (equitability and richness) would vary
annually due to organic matter decomposition. Did you analyse
and/or control for these c ianges?
! .3!. BENNETT : Data for such analyses were collected but
have not yet been fed to th computer I They will be very soon.
! BU iTA : I can give some additional information. We
have investigated the effects of clear—cutting on soil animal
communities in Finland. Coleoptera and Araneae were identified.
After clear-cutting the diversity in the spider con w.unity
was increasing in southern Finland but decreasing in northern
Finland. The diversity of the coleopteran community was de-
creasing in southern Finairid but increasing in northern Fin-
land. No conclusions could be made.
BENNETT : It is quite possible that species richness
for a given taxocene may increase or decrease depending on
local conditions and the species available for colonization.
-------
SYNECOLOGY OF FOREST SOIL ORIBATID MITES OF
BELGIUM.
I. ThE ZOO SOCIOLOGICAL CLASSES.
Georges Wauthy and Philippe Lebrun
Labonif sire dEcologie Generak LI &perarirntalc
&lgnirn
This article is the first part of a synecological analysis
carried ouL on thirty taxocenoses of Oribatid mites living in
the olganic horizons of the soiis of deciduous forests in )3e1gium.
Any synecological analysis requires, first of all, representatiVe
and sufficient information about the physiognomical structure of
the taxocenoses. The first chapter of this article shows how we
got the information and how we presented it in the form of zoo—
sociological relcvéa.
Then, any synecological step includes the delimitation of relevSs
groups which have the same zoological composition and form zoo—
sociological classes. Finally, a list of species results from
this collection of relev s. These z.p cies are influenced by the
same environment and define an original combination of species
which forms an ecological group ( GOUNOT. 1969 ).
The second chapter of this article deals with the de].imi—
tatiun of the moosociological classes of relevds.
CHAPTER 1 . — THE RELEVES .
1. The bjo eocenoses .
Before beginning the analysis, we decided to choose sites
which were comparatively undamaged and not very fnfluenced by
man. These sites we have chosen tend to show the .liversity of
the deciduous vegetation of Belgium. In this way, our conclusions
will be generalized to the whole taxocenoacs of Oribatids of the
organic horizons of deciduous vegetation of the country.
As the figure 1 shows it, the organic horizons we have met
can be divided into four principal types according co their
morphological structure and a few pbysico—chemica.l characteristics
considered to be significant ( KUBIENA, 1950 and DELECOUR, 1978 ).
The organic horizons with calcic mull, are found on calcareous
outcrops or chalks. The soils where they are f,wid always have
a good chemical fertility and undergo a long period of drought
in summer. The studied calcicole vegetations, all of thorn being
medio—european climax beechwoods of the Façion , are located in
Thynes ( nr.i ; plateau of the Coridroz ; 160 in ), Rémersdael
( 2 ; Entre—Vesdre-et—Meuse ; 215 in ), Crupet ( , ; Condroz
19 ’ in ), Dourbes ( 4 ; Famenne ; 160 m ) and Ilarche-les-Dames
(5; Neuse trench ; 120 in ).
The organic horizo 1 ns with non—calcic mull such as those
with modor—mor can be found on soils presenting a wide range of
fertility and moisture conditions. However, the decomposition
processes ( in the widust sense ) of the organic matter are more
rapid for the first ones than for the second ones, for there is
a Fm horizon, in the BABEL’s meaning ( 1971 ).
Some vegetations arc climax phytoceneses of the Farion arid
uercion . The first ones are situated in ! larneffe ( 9 ; Ilesbaye ;
169 in ), Nont—St—Aubert ( 11 ; hainault loessic re( ion ; 88 in ),
Bouyet ( 13 ; Fainonne ; 24 2 ”m ), Bohan C 1-4 ; southern Ardenne ;
315 in ), Annevoie ( 15 ; Condroz ; 246 in )7 Fouron_St_Ilartin
( 21 ; En-tre-Veadre-et—Meuse ; 250 m ), Eupen (22 ; Hertogenwald,
northern Ardenne ; 420 in ). The second ones have been found in
795
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N DROUS
I N&IURI
—
Ipsoetoo,ca 1 (
I GL*551S
[ caTEaoR l I
I NUMUB
- Grouping of sites nccordini to the humus category,
the pedologicul close, f ,rttlity and the hydrous
nature of the soil. Ncntiozt of the phytosociologiccil
and chorological position of their phytoconosis. —
Podological class C, catcimagnosic ; 11, bydro—
morphic ; 8, brown ; ND, not very developed ; PD,
podsolie brown ; P, peat. — Hydrous evaluation : GD,
coed internal drair.ing D I), defi ieut internal
draining ; F, fluctuatin’ nydrous conditions ; N,
moist.— Phytosociolcgy $ F, Fagion ; C, Carpinton
PC, Fraxinio-Carpinion Q, Quercion Atnion
jlutinosae ; !, Vaccinio-piceiofl. — CboroloCy $ A,
association of the atlantic province ; j, associa-
tion of the inedio-europO fl province.
Pii!ure 1 .
L I ____
I PI4YYO-
SOCIOLOOT
1
- - — JL_ a ] [ j . ] [
1
: ]( =

MEIOTROPMIC ] Muo OUOOYPOPrnC (
‘ = f L] : ::çj ; cH 4cN3
CALCIC MULl. if aO l CALCIC MUlL MOoSS-MON
=

OLIOOT SOPHIC
‘U:
] PLAY -
-------
7 j aire 2 . — Recinrocal averaging of 30 r•lev4s out of 357 eco-
logical species of hernie 1aphic Oribatids. Plan of
the axo. 1 and 2.— Th. numbers indicate the origii .
of the reT.v ..— The categorie, of bunus are
designated by a symbol.
P MO7 MULL
Y I I
797
-------
Cul—des—Sarts ( 23 southern Ardenn ; 359 in , Ham—sur—
Houre ( 211 ; hainault alluvial region ; 177 in $, Angleur ( 26
Coridroz ; 170 in ), Ruien ( ; coarse—loamy Flanders ; 127 m 5.
The other ve etations are edaphic cl wax and fall into the
Carpinion or the Querci in . The first ones arc located in Habay—
la—Vieille ( 6 ; LoEraiaie ; 303 in ), Arquenflcs ( 1.; brabant
loesaic region 107 m ) Froidchapelle ( 8 ; Fc gne of the Entre—
Sambre-et—l4cuse ; 235 m 5, Angre C 12 ; hainault loessic region ;
88 in ), Tarcicnnes ( 12 ; brabant loessic recion ; 230 in ), Sadzot
( 16; western Ardenne ; 370 in ), Waillet C 17 ; Fanenne ; 22b in ),
Eugie!l 18 ; hainault loessic region ; 138 ii ). The second ones
can be fo iiid In Grand—L.ecz ( 19 ; licebaye ; 173 in ), Houtbulet
( 20 ; coarse—loamy Flanders ; 15 in ), Courrière (25 ; Condroz ;
267 ), Eupen ( 28 ; Brachkopf, northern Ardenne ; 545 m
In this last biogeocenosis, the humu5 is a peculiar mor ; the
thickness or the organic horizons does not exceed 5 cm and moreover,
the C/N rati.o is rather weak ( + 16 ), this is why the humus of
tI.is site bears a resemblance t the moder.
Theiwo peat organic horizons we have met belong to biogeo—
cenoses whose botanical composition offers great differences.
This is due to the fact that the site of )Jalempré ( 29 ; central
Ardenne ; 425 m ) is full of ferruginous water a trea iets whereas
in the site of Rownont ( 30 ; central Ardenne ; 4 i in ) the surface
horizons of the aoi l are only fed with the water of rains and snow.
Let us point out that two phytocenoses are enclaves of
atlantic groups in the medio—european province. The phytocenoses
in question are nr. and nr. 29. In both cases, particular edaphic
conditions ( moist and gleyified lumen on the surface in the site
nz 23 ; permanent runnels on the surface in the site nr. 29 ) can
pro the transgrfssionz ( S0U NEZ, 197 14 ).
2. Ecological species of Oribatids ,
The definition of the systematic units we have retained,
units which we think to be the smallest taxonoinical entities
presenting an ecological unity ( TUFFERY & VERNEAUX, 1968 ), is
based on the neotenic concept of the Acarida developed by GRANDJEAII
( 1938 ). We associate to the phylogenetic independence between
adults and immatures proved by this author ( 19147 a ) an eculo-
gical independence pointed out by TRAVE ( 1964 ).
Larvae, nymphs and adults are full ecological species.andwe cssign
a distinct zoosociolugical part to them. There are 357 ecological
species of Oribatids.
3. Sampling .
The releviSs constituting has been realized in accordance
with the “ petiten faunes “ method of CRANDJEAN ( 1947 1 ). Th .
method advocates the concentraticn of the collecting places in
sniali areas which hnve been chosen with care.
Our knowledge does not enable us to estimate the biotic hoinoge—
neity ( GOUNOT, 1969 ) of any taxocenosis of Oribatids. This
is why we decided to reduce surface of the sampling areas
to a minimum. In this way, we hoped to meet biotopes whose life
conditions were not very heterogeneous ( C/.NCEL.A DA FONSECA &
VANNIEP, 1969 ). in view of the dimensions of the Oribatid mites
and the parcelling of the hcrbaceous tapetwn of our forests,
we decided the sampling area of each site to be a small area of
798
-------
herbaceous vegetation typical of the phytocenosis.
In each sampling area, we have distinguKshed the tazoce—
noses of the ‘ litter “ habitats from those of the “ humus “
habitats. In the non-peaty forests, the “ litter “ habitat
consists of surface holcrGanic layers including the or 7 micro—
layer ii it Lxists. The “ humus “ habitat consists e r n ie Oh or
surface micro—layers ( + 1 cm thick ) according to the humus
categories. In peaty forests, we hsve chosen the fl layer as
“ litter • habitat sad the surface part of the Ilhtorizon as
“ humus “ habitat because these two horizons exhibit a morpho—
.‘.ogieal discontinuity state similar to the one observed between
the “ litter “ and “ humus “ habitats of the other non—peaty
biogeocenoses.
The sampling has been made in spring and in fall. We have
chosen these two seasons for we observe a density forester
optimun in summer and in spring for the “ litter “ habitats and
in fall for the “ humus habitats ( LEBRIJN, 1964 ).
4. The three types of relevjs .
On the whole,tweniysarnples have been taken in each area.
Thy specific and au srical lists of these samples have been put
together to form three relevds by biogeocenosis a “ litter
relevë, a “ humus “ relevd and a “ homiedaphic “ relevJ concerning
the Oribatids living both in the “ litter “ and “ humus “ habitats.
The “ hemusdaphic “ relevJ is a kind of zoosociological reference
standard since important variations of the morphology and of the
physico—chemical composition of the forester organic horizons
have been recorded. Thus, the “ humus “ habitat of a mull organic
horizon is more mineral than the one of a moder organic horizo .
Besides, the decomposition of the organic matter follows different
biogeochemical processes according to the composition of the
mineral sub—soil ( TOIJTAIN, 1974 ).
Since the relevés include much information, it will be easy
to generalize the results deriving from their comparisons.
CHAPTER 2 . - THE ZOOSOCIOLOGICAL CLASSES .
The zoosociological class concept fs based here on the
individualistic conception of the sociological categories
( WIIIT7AKER, 1956 ) which recognizes the existence of the ecolo-
gical continuum of the taxocenoses. This implies the approximate
repetition { except for the uncertain variations ) of the salute
specific combinations when the environment ( in the widest sense )
is about the sante .
Consequently, the me 1 ological similarity of the biotopes can be
associated with the similarity of the specific and numerical
profiles b;t.ween the relev s. The purpnse of this association
is to dete mine the mesological frame which is necessary for the
Oribatid ecological groups to develop and to remain.
1. Nethod .
The quantization of the similarities bctwoen the relevds
has been realized with tho help of the reciprocal averaging
( BEKZ1 CRI & al., 1973 ). The similarity function is a distance,
called distance, which is determined from the •:onditional
799
-------
frequencies on the specific numbcrs of individuals.,
Then. thc method describes the information put on the relcvs
table accoreiini to seveal linear orders by means of represen-
tations made of axes and points.
We think that thaso ordinations arc of great ecological iiuportrineo
because the points corresponding to two rclcvés which have about
the same distribution of individuals through tne same species.
mingle in the factorial hypciespaCe.
The algorithm which has been used is the one of LEDART & .
( 1977 ).
2. The tuesolo ical frame .
The figure 2 shows the dispositions of the hermedaphic
relevés—points in the space of the first two factorial axes..
An assembly of relev s—points which refer to taxocenoses living
in the inodox--mor and non—calcic mull organic horizons focuses
close co the center of gravity. The first axis is a segregation
axis of the reLevés—points dealing with the taxoceroses which
develop in the peat organic horizons. The second axis is a segre-
gation axis of the relev s—points indicating taxocenosas living
in the organic horizons of soils with a high biogen elements content
and, among others, caleuc mull soils.
In relation to the third factorial axis ( figure 3 ), the
hemiedaphic relevés—points are divided into two groups. The group
on the let i of the center of gravity is almost totally made of
re1ev s—points relating to taxocen050s located in the north of
the Sainbre—I’Ieuse trench while the other group consists of relevés
points relating to taxocenoses situated in the south of this trench.
In fact, the third axis seems to prove ( exc.ept for points 2, 3,
24 and 25 ) that there is an excellent chorological para lleTis
E tween tie taxocenosea of Oribatids and the phytocenoses
sheltering them.
The ‘ourth and following axes could not be interpreted on
account at the ecological parameters we analysed.
The ordination of the hemedaphic relevés—points which we
have Just described is about the same than the one of the “ litter “
relev s—pointa alone or the “ humus a relevés—points alone, accor-
ding to the directions defined by the factorial axes nr.i and 2.
In accordance with thc direction of the third axis, the same macro—
climatic antagonism can only be found with the analysis of the
U litter • relev4s —points. In the case of the “ humus “ releves—
points, this antagonism is present for all the points except for
those, indicating the nuoder—mor organic horizons.
Nevertheless, the convergence of the results of the three reci-
procal averagings is unde iiable.
Therefore, we come to the conclusion that, generally, there is
an exci’Ulent physiognoinical identity between the 3axocenoses of
the • litter “ habitats and the ones of the “ humus “ habitats.
Indeed, the exclusive ( LEDRUN. 1971 ) or indifferent ( LIONS,
1972 ) species are very few. Futhcrmore, our rosultz state preci- .
ely the existence of an identical mesologfc.al frame which has
en influence on the spccific combinations of the “ litter °
and “ humus “ habitats. This frame consists of two components s
the first one is an edaphic component which reveals the influence
of the category or humus, this is to say the morphological and
phyeico-cheinicai organization of the organic horizons on the
800
-------
Iii
i+0
, .IJ.e po
0
D O ti’.
. 1.0. 10
3O 0 0 ,1
0
n
r 0 • P
‘1 •;dJ.I .0I.0
•0 ••
P
I’ P i • 4
• f+ef •G
9
P P0 J. 0

‘.0.
04
fl0d •
P
‘1 •0
81 V
I .a .’ —
o 0 4 0 I. ’ .
• 1
•ao

(3
• so
r’ .
•s
cl n 0
• 0P
P ‘+0
g p . o.
P I•-•
S
p. ,
• o+
P
P P
I.S.O Ot I .
on, • S
0 1.0. .3
I-’ Ii
I i
*
c i
*
c J
1
L J
u J
r J
0
3
• Peat
calcic Mull
non ca1cic Mull
Moder-Mor
-------
Oribatid groups ; the other one is a climatic component which
shows the int3.uence of the climate of the atlantic or subatlaritjc
type.
. ‘ elirnitation of the zoosociolni ical clnssaa ,
With the heLp of the natural subdivisions of the two com-
ponents, we can define six homogeneous , ub—assemblies of relevi a,
this ie to say dealing with taxocenose i whose species seem to
have about the same reaction towards the incriminated ecological
factors. Those sub—assemblies form zoosociological classes.
As the figure 4 shows it, the first class corresponds to
the sub-asseitibly made of the two relevós—points referring to
the taxocenosea of the peat organic horizons. Thus, these taxo—
cenoses can be found in biotopes which are a .s’ost permanently
wet. The action of water on the taxoccnoses of Oribatid mites
has been pointed out by KNULLE ( 1957 ).
The second class consists of the relev s referring to the
organic horizons taxocenoses of ca3.cic mull soils where calcium
takes a leading part in the biogeochemical cycles. The direct
influence of calcium on the Oribatids has not been proved.
However, since the quantity of ectoskeletal calcium ( GIST &
CROSSLEY, 1975 ) is important, there is probably vital physio-
logical needs for this ion.
The third clasi corresponds to the relovds established from
the taxocenoses of the organic horizons of non—calcic mull soils.
These taxocenoses have a great zoosociological plasticity since
their physiognomy recalls the one at the taxocenosos found in
celcic mull horizons, when they are in organic horizons of soils
with a high biogen elements content. In soils with a low biogen
elements content, their physiognomy recalls the physiognomy of
the texocenoses which develop in moder—mor organic horizons and
from which the relovés form the fourth zoosociological class.
The last two classes deal ith the climatic component one
of them consists of the relev s relating to the taxoccnoses of
the atlantic territory. Thus, it is subject to a climate which
is less hard than in the s’ batlantic territory whose rel.evés
form the sixth zoosociological class.
çNCLUSIONS .
The ecological connection between the deciduous phyto—
cenoses and the taxocenoses of Oribatids of the organic horizons
cannot be admitted. Ifldeed, the deciduous phytocenoses are mainly
influenced by the climati factors while the taxo”enoses of
Oribatids they shelter are above all condioned by the edaphic
factors and, secondarily, by clitnatic factors.
Now, we still have to work out the specific composition of each
ecological group and to reveal the relations between the groups,
the two inesological components and other ecological data.
-------
EDAPHIC MESOLOGICAL COMPONENT
4 ZOOSOCIOLOGICAL CLASSES
NON CALCIC MULL
0I
-
0I
) 3 Oh
MODER
CLIMATIC MESOLOGICAL COMPONENT
2 ZOOSOCIOLOGICAL CLASSES
Pi ure 4 . — The zoosociological cl&sses. Designation of the
— p.dolo ical horizons : 113., dead peat mosses almost
undamaged i Hf, peat mo ies which are less structured
Rh, peaty niaT ers ; Ah, mineral hemiorganic horizoi ;
I, almost undamag.dT.aves ; Of, more and more
i 1itted up leaves ; Oh, very splitted ur and hutnified
substance..
PEAT
CALCIC MULL
ATLANTIC CLIt 1ATE SUBATLANTIC CLIMATE
603
-------
REFERENCES .
BABEL. U. ( 1971 1.
Gliecerung und Beschreibung des Humusprofils In mittc.1europ is en
Waldern.
GEOD. 5 : 297-324.
BENZECR • J.P. 1 CONTRIBUTORS ( 1973 ).
L’analyse des données. Volume 2.
Dunod, Paris • 616.
CANCELA DA FONSECA, J.P. & VANNIER, G. C 1969 ).
Echantillonna e des Nicroarthropodes du sol.
In “ Probl ines d’Ecoloj ie : L’écbantillonnaf!e des peuplements
animaux dos milicux terrestrea “.
Nasson, Paris . 207 - 236,
DELECOUR, F. ( 1978 ).
Initiation a la pédologie.
Service de is Science dii eel, Gembioux . 69.
GIST, C.S. & CROSSLEY, D.A. ( 1975 ).
The litter arthropod community in a southern Appalachian hardwood
toreet numbers, biomass and mineral element content.
All, MIDL. NATURALIST . 93 t 107 — 121.
GOUNOT, N. ( 1969 ).
)l6thodes d’6tude quantitative de is v gétation.
Nasson, Paris . 314.
GRANDJEAN, F. ( 1938 ).
Au eujet de la néotdnie chez lea Acariena.
£.R. SEANC . AC. SCI. 207 ; 131.7 — 1351.
GRANDJEAN, F. ( 1947 a ).
Sur is distinction de deux sortes de temps en biologie 6vohutive
et aur l’attribution d’une pbyiog. nèse particuli re ii chaque
4tat statique de l’ontogdnèse.
C.R. SEANC . . . 225 $ 612 — 615.
GRANDJEAN, F. C 1947 b ).
Etude sur lea Smarieidae et quelques autres Erythroidos ( Acariens ).
ARCH. ZOOL . EXP. GEN. 85 (i ) : t — 126.
KNULLS, v. ( 1957 ).
flje Vertejlun 9 der Acari Oribatei im Boden.
Z. MORPH . U. OKOL. TIERE . 46 397 — 432.
KUBXENA, V.L. ( 1950 )
Bestimmungsbuch md Systematik der Baden Europas.
Enke, Stuttpart • 392.
LEBART, 1.,, NORINEAU, A. & TADARD, ; . ( 1977 ).
Techniques de is descrirtion statistique.
Dunod, Paris . 351
LEBRUN, Ph. C 1964 )
Quelques aspects de la ph nolegie des populations d’Oribates
( Acari $ Oribatei ) dane le aol forostier en floyonnc Bei ique.
DULL. ACAD . ROY. I) BELG]QUE • 50 : 370 — 392.
8o
-------
LEDHUN, Ph. ( 1971 )
Ecu1ujii ci, Bioc notiquo do quciques pcuplcuiicnts d’Art’iropodos
édnpliiqucs.
lEM. INST . !. SC. NAT. hl U.IA IQUE • 165 i 1 — 203.
LIONS, .i.c. ( 197 ).
Ecolorie des Oribatce ( Acaric is ) de la Sainto Baume ( Var ).
Thène Doct. Sci. Not. Thir oi11e.
n° A.0. 72118 ). Inédi . 5 1e9
SOUGNEZ, N. ( 1974 ).
Lea ch naies ailicicoles de De1 que ( Quercion robori—petraeae
( Ilaic. 1929 ) P.r. — Bi. 1932 ). In “ Collogues phytosocio1o guos.
III Lea rorats acidiphiles. Lille 1974 “ • 1811 — 2119 • 11 t.
TOUTAXN, F. ( 1974 ).
Etude écologique de l’humidification dana lee hêtraies acidiphiles.
These de doctor-at llniversitê da Nancy ( N° C.N.R.S . : A.O. 9650 ).
Inédit • 124.
TRAVE, J. ( 1964’).
Impo tance dee stases imsatures des Oribatea en syst4matique
at en êcologie.
ACAROLOGIA FASC . H. S. 1964 . 4 - j4.
T1JFFERY, C,. & VERNEA !(, 3 ( 1968 ).
)léthode de d termination de la qualit4 biologique des eaux
courazites.
C.E.R.A.P.E.R., Paris • 21.
VHI ITA3CER, R.H. ( 1956 ).
Vegetation of the C’eat Smoky Mountains.
ECOL. P4ONOGR . 26 1 — 80.
QUESTIONS and COMMENTS
14.B. BOUCIth : Quel eat le pourcentage d’explication de
chacun es quatre principaux axes de votre analyse factorielle?
C. WAUTEY : These percentages are respectively 15.50,
11.35, 8.11 and 7.37 for the first four axes of the reciprocal
of the heiniedaphic releves. As Lebart et al. (1977) note
these percentages permit an appreci3tion of the confidence
associated with each ordination. In our case the percentages
seem high enough for the first four axes. For the fifth
and sixth axis the percentages (respectively 5.85 and 5.60)
are lower and approximately the same.
8o
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POPULATION DYNAMIC AND METABOLIC
CHARACTERIZATION OF COLLEMBOLA SPECIES IN A BEECH
FOREST ECOSYSTEM
Henr ing Petersen
Moislaboratorirt Femri ltor
DenrnarL
INTRODUCTION
Soil ecological studies carried out within the frame-
work of the International Biological Programme (IBP) mostly
focused or. population size and production biology of larger
taxonoirdc units without much emphasis on the role of indivi-
dual species. The increasing knowledge about the structure
and function of natural ecosystems,however, has during the
recent years stimulated the interest in species diversity
a: d community structure. The soil and litter fauna is often
e tremely diverse, but attempts to explain the co-existence
of the many species in terms of fundamental niches have been
so disappointing that it has led to the formulation,”The
enigma of soil animal species diversity” (Anderson 1975).
The present paper does not pretend to solve this enigma but
will emphasize the dissi ” ilarities between some collembolan
species living together in a Danish beech forest soil as re-
gards various aspects of their population dynamics and pro-
duction biology.
The results suggest that several of the ecological
characters separating collembolan species are combined into
sets of properties which relate to the depth distribution of
the species. A classification of the collembolan fauna based
on these ecological characters therefore parallels and mostly
coincides with the classical morphological life—forms described
by Gisin (1943).
The information of this paper is extracted from a coxu—
prehensive study of collembolan population ecology and energe—
tics which will be published in more details elsewhere. The
work was conmienced as part of the “Hestehave beech forest
ecosystem project” which i a major Danish contribution to the
IBP.
The research site covers 1.5 ha of a pure c. 95 years
old beech stand. The surface soil has the character of a typi-
cal mull. There is a sharp separation between the litter layer
(L) and the mineral soil. F and H layers are not distinguish-
able, but the humus content of the minex al soil decreases gra-
dually with depth. The forest floor is through the spring and
the summer more or less completely covered by a field layer
dominated by Anemone nentorosa L, Melica unifloraRetz,Asperuia
806
-------
odorata L , and Carex silvatica Huds. More information about
the site and theproject may be found in Yeates (1972) and
Thamdrup,Nielsen and Petersen (1975).
METHODS
1. Field Population Estimation . 28 plots distributed in a stra-
tified random pattern were sampled each month through nearly
biannual period. In each plot a litter sample (86.6 cm sur-
face area) and a core (10 cm surface area) were sampled. The
core was subdivided into L layer and two 3 cm thick layers
of the mineral soil. A core to 15 cm depth was sampled seaso-
nally. The sample units were extracted in high gradient ex-
tractors (Petersen 1978). Specimens mounted in slides were
identified to species and as far as possible to se and stage
of reproductive development (Petersen,in press). The body
lengths of the mounted specimens were measured by means of an
ocular micrometer and converted to ‘i’ y weight by the use of
allometric regressions (Petersen 1975)
2. Culture Experiments . One to several eggs of some of th com-
mon species from the fie 1 site were transferred from stock
cultures to small culture chambers kept at constant temperatu-
res or at field temperatures (Petersen 197].,a). The size of
specimens were mt asured regularly from eclosion to death by
means of micro-photography (Petersen op. it.). The cultures
were mostly examined twice per week in order to check survival,
and the production of exuviae and eggs. A yeast, Candida sp.,
extracted from the soil of the field site and cultured on
agar plates, was in most cases used as food.
3. Respiroinetry . Measurements of oxygen consumption were car-
ried out on single individuals by means of an open gradient
diver method (NexØ, Hamburger and Zeuther. 1972) modified for
terrestrial microarthropods (Petersen, in prep.). The method
is based on the gradual sinking of a small aivtpulla containing
the experimental animal in a linear density gradient made from
a sodium—sulphate solution (FIGURE 1). The lower part of the
ampulla contains 0.1 normal NaOH. The decreasing buoyancy of
the ampulla caused by the respiraticn o the animal makes the
ampulla sink at a rate proportional to the oxygen consumption.
The movement of a control diver is used to correct for changes
in temperature and atmospheric pressure. The changes in diver
positions have been recorded by means of a time—lapse camera.
807
-------
FIGURE 1. Open gradient diver respirometiy.
a. Measuring cylinder with density gradient of
Na SO solution
b. Ain u)ia divers
c. Control diver
d. Density standards (glass beads)
e. Experimental animal
f. Porous material (polystyren)
g. 0.1 n NaOH
808
-------
RESULTS
1. Size and Composition of the Totai Co].lembolan Population .
FIGURE 2 illustrates the density fluctuations of the total
collembolan population through the biannual period (L +
0-6 cm mineral soil). It will be noted that the population
reach maximum density during summer and autumn but was
low during winter and early spring. A depression durinq
late summer and early autumn of 1969 which coincided with
a dry and hot period reduced the mean annual density of
1969 to about half of the mean density recorded in the fol-
lowing year. The total range of variat...on through the
biannual period !s 19. x 103 to 67. x io3 specimens per m 2 .
The biomass of the total collembolan population varied
between 76 and 160 mg dwt. per m 2 in 1970.
The composi .ion of the collembolan fauna is listed
in APPENDIX A. About 60 different species have been iden-
tified from the so.J. and litter within the rather homo-
geneous area of 1.5 ha. Several of these, however, have
been found only o casional1y. Others have been found
regularly, but in low numbers. The two most abun-
dant species Tulibergia macrochaeta (most common member of
the T.krausbaueri species group; see footnote at APPENDIX A)
and I.minor constitute together about 50% of the total
number of Collembola . In terms of biomass,however, the
dominance ranks are quite different with T.flavescens as
the most dominant species fb11 , by L.lignorum .
2. Vertical Distribution . FIGURE 3 shows the mean annual depth
distr1butior of some of the most important species.In APPEN-
DIX B the specit’s have been classified into subjectively
defined groups according to their depth distribution pattern.
Juvenile spe intens which generally constitute a major frac-
tion of the average annual density have in all species a
deeper distribution than adults. This has a special influ-
ence on the average c .nnual depth distribution of the two
sminthurid species D.rninuta s.l. and S. aureus because
adults of these species are more or less completely missing
in the soil and litter during summer and early autumn.
D.minuta seems to migrate from the forest floor to the tree
canopy during early summer. The population of S.aureus may
largely survive the summer as eggs.
The two species which have the highest dominance
values in terms of biomass, i.e. L.li9norum and T. flavescv.ns
are more or less confined to the litter layer (epedaphic).
T. macrochaeta and I. minor which strongly dominate the
collembolan fauna in terms of den ity clearly belong to the
euedaphic group of species. The hemiedaphic category inclu-
des the majority of species ccurring ifl the forest floor.
3. Reproductive Periods . FIGURE 4 and 5 exemplify two different
patterns of seasonal changes in the size structure of col—
809
-------
! IGURE 2.
80
70
>-50
40
U i
Q 30
20
10
Density of the total colleinbolan population in the
L layer and uppermost 6 cm of the mineral soil +
(March 1969 to February 1971) .Arithmetric means-
standard errors.
JFMAMJJASON OJFMAMJJASONOJFMA
1969 1969 1970 1970 1971
-------
FIGURE 3. Vertical distribution of selected species. Verti-
cal axes indicate the litter layer (L) and 5 . 3 cm
layers of the mineral soil. H’ rizontal Lar3 illu-
strate the percentage contribution of each horizon
to the total density of the species.
L.l : Lepidocyrtus 11 gnoruzn ; T. f. : Tontocerus flavescens ;
D.m.: Dicyrtomina minuta s.l.; F.n.:Folsomia nana ;
I.n.: Isotoma notabilis ; O.f.: Onychiurus furcifer ;
0. p.: Onycniurus pseudovanderdrifti ; I .m. Isotoiniella
minor ; Tk: Tulibergia krausbaueri s.l.
L.L.
L
- I
27 1
1.21
6
If.
— 58
D.m .
36 1
I
15
53 1
En .
LI 34 1
6
LI
I I
P
15
I.n.
15
56 I
6
15’
___O.f.
21. I
L25 1
70
7L
6
7J
6
15
1
L
O.p.
15’
1.m.
1 J
6
71 I
T.k.
15
811
-------
leinbolan populations which reflect the occurrence of re-
production through the year. The I.notabilis population
(FIGURE 4) includes throughout the year members of the
smallest juvenile size classes. Thus, the reproductive
period appears to cover most of the year. A similar pat-
tern is shared by I.xninor and T. krausbaueri s.l., i.e.
the two most important euedaphic species. The epedaphic
species T. flavescens (FIGURE 5) on the other hand has a
more confined reproductive period. Most juveniles hatch
in June and July, whereas the recruitment to the popula-
tion in August, Septemb r,and October is less significant.
Similar restricted reproductive periods are characteristic
for the sminthurids D. mi iuta s.l. and S. aureus which
mainly reproduce during late winter or very early in the
spring. 0. fur ifer and W. anophthalma which are classified
among the hnmiedaphic sp cies have also rather restricted
recruitment periods culminating in June and August,re—
spectively. The epedaphic L. ].ignorum has a more extended
reproductive period from March to August. The he’niedaphic
species F.nana seems to reproduce regularly from May to
Nove’nber.
Although each species of the beech forest floor may
have a special reproductive phenology it seems justified
to suggest a relationship between the depth distribution
of the species and the extension of the reproductive period.
Thus, it may be typica. that euedaphic species reproduce
more or less continuously through most of the year whereas
the epedaphic species being more exposed to environmental
fluctuations typically have se sona1ly restricted repro-
ductive periods. Species with intermediate depth distri-
butions cover a range from seasonally well defined repro-
duction (O.furcifer,W.ano hthalma) to continuous repro-
duction through the year ( I.notabilis) .
4. Mode of Reproduction. Bisexual and Parthenogenetical
Populations . The sex identification of the specimens from
tie field samples which was mainly based on the deve]op—
ment of the genital aperture unveiled that several of the
most abundant collembolan species in the Hestehave soil
existed as pure female populatic ns thus suggesting a par—
thenogenetic mode of reproduction (Petersen, in press).
Parthenogenesis was confirned for two of the species I.nota—
hilis and T.krausbaueri by means of culture experiments
(Petersen 1971, b). The hestehave beech wood populations of
the following seven abundant species can safely be attri-
buted obligatory parthenogenetic reprc duction : Willemia
anophtha].ma, Tuilbergia macrochaeta,T. sylvatica, T.calli—
pygos, Isotomiella minor, Isotoma notabilis,and Megalothorax
minimus but at least B additional less abundant species
should probably be included among them. Thus,parthenogenetic
reproductton comprise about 72% of the mean annual number of
Collembola in the beech forest soil.
-------
FIGURE 4. Isotoma notabilis . Size structure of the population
December 1969 tc November 1970. Horizontal axes
define body length classes in rnm.Vertical arnes show
number of specimens per m 2 in the litter layer (up-
wards from the horizontal axes), and the 0-6 cm
horizons of the mineral soil (downwards).
813
-------
a- doç - -
:—:
— — — 17 10-70 —
U may-70
T11 d Lr jiini-70 —
j

,
._r j{ftL q’— juLy -70
• aig.-70
- se t.-70 —
100
ir oct-70 2
- ._ 1 - 1 -, rrrh_ n0 .-70__
— - - - a:— . —
1 4OCERUS FLAVESCENS
FIGURE 5. ToniocerUs flavesCens . Size structure of the pop 1a-
ion December 1969 to November 1970.FOr explanation
see FIGURE 4.
814
-------
female or male with “open” genital aperture and the smallest
juvenile, o. between fe’nales containing eggs and the smal-
lest juvenile is considered. This sequence of species
rather closely parallels the sequence of species ranked ac-
cording to vertical distribution. Thus the epedaphic spe-
cies are characterized by n extended development before
maturity is reached, or if expressed inversely: th progeny
of the apedaphic species is small compared with the smallest
sexually mature adults. The euedaphic parthenogenetic spe-
cies on the other hand produce progeny which is relatively
large compared with the smallest ugg producing females.
The hemie iaphic species produce progeny of intermediate
relative size.
The postinature growth which is illustrated by the
ratios between the largest and the smallest females or miles
shows relatively small differences between species and seems
not related to the depth distribution.
6. Metabolic Rate . Results from respiration measurements of some
of the most significant collembolan species in the Hestehave
beech forest floor (Petersen,in prep.)(FIGURE 9— 11) suggest
that the metabolic rate is related to the depth distribution
of the sipecies. The relation between dry weight and oxygen
consumption is described by the formula:
R = a .
where R Is oxygen consumption per individual per hour,
W is dry weight per individual
and a and b are constants.
The exponent b (pooled between temperatures) varies from
0.78 in O.furcifer to 0.96 in T.flavescens .
At all three temperatures and throughout the weight
range D. minuta s.l. has the highest oxygen consumption
followed by L. lignoruin.The euedaphic I.minuta has at the
three temperatures the lowest oxygen consumption of the mea-
sured species. The hemiedaphic species I. notabilis,
F. quadrioculata s.l., and 0. furcifer have intermediate
respiratory rates. The metabolism of T. flavescens is more
difficult to relate to the other epedaphic species,but the
large adults have a high metabolic rate whereas the respi-
ration of the small juveniles is relatively low.
815
-------
Two characters obviously unite the parthenogenetic
species: They are relatively small, and they live in the
more protected strata of the forest floor. Only I.notabilis
and especially W. anophthalma disagree with the euedaphic
depth distribution by having a relatively large proportion
of their populations in the litter layer. The populations
of all epedaphic and most heutiedaphic species,however, in-
clude 30% to 50% males and seem restricted to a bisexual
mode of reproduction.
5. Relative Size of Offspring . The size of newly hatched ju-
veniles and sexually mature adults was estimated from
examination of the mounted specimens from the fie]d samples,
and from measurements of specimens kept in culture (FIGURE
6 — 8)
Adults mounted on slides can be recognized by the
development of the genital aperture (Petersen,in press). A
aist. Inction can often be made between “closed” and “open”
gei:ital apertures which indicates that the individuals were
in a reproductively inactive or a reproductively active
stage, respectively. In females possessing “open” genital
apertures eggs n ay occasionally be recognized inside the
mounted body. In males with “open” genital apertures an
ejaculatory Iuct is usually distinct. The stages with “open”
and “closed” genital apertures seem to alternate riore or
less regularly thrrughout the reproductive period of the
animals (Mayer 1957, Snider 1973).
In the material of mounted specimens from the field
samples the stage of reproductive maturity, however, is
most safely defined by the smallest specimens with “open”
genital apertures or witi. eggs visible within the ovaries.
In the culture experiments reproductive maturity was de-
fined by the first oviposition. The size of newly hatched
individuals was measured within the first four days after
eclosion.
FIGURL 6 - 8 illustrate the frequency c 1 f occurrence
of the aifferent developmental stages in three typical spe-
cies. I. notabi].is (FIGbRE 7) exemplifies a type of 4evelop—
ment characterized by the occurrence of maturity in spc3ci—
mens which are only little larger than the newly hatched
juveniles. T. flavescens (FIGURE 8) exemplifies the other
extreme in which maturity is not reached until a conside-
rable growth haz occurred. O.furcifer (FIGURE 6) exemplifies
an intermediate type.
APPENDIX C presents the weights of characteristic
stages during the development from newly hatched juveniles
to the largest adult specimens of some of the most impor-
tant species in the Hestehave forest floor.In APPENDIX D
the ratio between some of these values have been ranked
according to the ratio between the smallest female (A) or
male (B) and the smallest juvenile. The species maintain
principally the same rank if the ratio between the smallest
816
-------
FIGURE 6
O ychiurus furcifer . Size structure and the occur-
rence of various developmental stages in the field
population and in cultures. The frequency distri-
bution of the field population 13 based on the cu-
mulated results from 11 samples (December 1969 to
November 1970).
T juveniles.In the diagram representing
culture experimer 1 ts: Juveniles 0—4 days old
-isex or stage not identified
r q males “closed” genital apertures see text
—ma1es “opens genital apertures.For cultures;
males coupled with females producing their
first egg batch.
females “closed” genital apertures
females “open” genital apertures
females containing (producing) eggs.For
cultures:females few days after first
oviposition.
U)
LU
C-)
LU
0 .
U .’
Li-
0
LU
I
z
BODY LENGTH mm
-------
I. not abilis
culture
LI.
02 04 0:6 0.8 10 1.2
10
5
02 0 O 0.8
60
20
•02 0.4
I.
02
1
6
4
2
- I 9
: o 1.2
0.6 0.8 1.0 1.2 14
sex not identified
mainly juverules
0.6 0.8 1.0 1.2 1/.
BODY LENGTH mm
FIGURE 7.
Isotoma notabilis . Size structure and the occur-
rence of various developmental s+’ges in the field
population and in cultures.For e :lanation see
FIGURE 6.
3C
20
10
U)
z
I
U
U,
Li-
C
w
300
250
150
100
50
818
-------
T.flovescens
21 culture
Ii ’ -
20 3:0 4.0 5 . 0
10
U,
2
Lii 5
I
C-)
(I )
LL
15
110
5
FIGURE 8. Tomocerus flavescens . Size structure and the occur-
rence of various developmental stages in the field
population and in cultures • For explanation see
FIGURE 6.
160
30
20
10
n
V 20
ir
1.0 20
4.0 SC
sex not identified
mainly juveniles
fli i
3.0 4;o 5O
BODY LENGTH mm
9
3.0
0’
819
-------
FIGURE 9. Relation between dry weight and oxygen consumption
rate r er individual in several co]lembolan species.
1000
FIGURE 10. 1 XX
I-
F
110
1000
jig
For identification of abbreviations referring
to species see FIGURE 3.
820
10°C
,.f.
f.
1 10 100
DRY WEIGHT
-------
L
C
b
z
2ioo
0
C-)
z
LU
1Q
x
0
1
FIGURE 11
1
Relation between dry weight and oxygen consumption
rate per individual in several collen bolan species.
15 0 C.For identification of abbreviation referring to
species see FI( URE 3.
821
15°C
T.f.,
*
1 10 100
DRV WEIGHT
-------
DISCUSSION
The results presented above suggest that various as-
pects of collembolan population dynamics and eriergetics
are interrelated and characterize groups of species with
a conmion depth distribution. The relationship between
these ecological characters and the depth distribution is pa-
ralleled by a relationship betweefl sets of morphologicaL
and sensory physiological adaptations which were described
and classified as °Lebensformen by Gisin (1943). Thus,
acccx ding to this classification the typical “Euedaphon”
differ from the “Hemiedaphon” and the “Atinobios” by small
size, reduction of ].imbs,antennae and furcula, lack of
pigment, lack of scales and other specialized setae,re—
duction of ommatidlae and in return a strong development
of chemical sensory organs. The ecological characters
described in this p.aper may have a direct functional re-
lationship with morphological characters such as body
size and the development of locomotory organs. The eco-
logical characters may also be mutually dependent so that
one character automatically is a consequence of another.
At the present state of insight, however, it is only pos-
sible to speculate about the causal relationships and
adaptive values of these characters.
A govering ecological factor is without doubt the
increasing environmental stability with depth. Dayly and
seasonal fluctuations in temperature and moisture are
leveled out. This will allow reproduction,egg development
and growth through a large part of the year in the deeper
soil layers where in contrast conditions for these acti-
vities near the surface are only favorable in restricted
periods dependent on the actual climate, but in broad
outline fixed by seasonal climatic changes.
Williams (1975) discussed the general occurrence of
asexual and sexual reproduction in organisms and concluded
that asexual reproduction is expected to be the optimal
mode of reproduction in stable environmerts with mild
natural selection whereas sexual reproduction is an adap-
tation to unpredictable environmental conditions and
intense natural selection. The importance of parthenoge-
nesis among the euedaphic species in the Hestehave forest
might well be explained in the light of this hypothesis.
However, another possible explanation is that the collem—
bolan indirect spermatophore transfer mechanism is too in-
efficient to work among Individuals of several species
which probably live widely scattered in the complex system
of soil interstices (Petersen,in press).
It is not yet possible to draw definite conclusions
about the population dynamic consequences of the differen-
ces found between the size of progeny and the first repro-
ductive adult stage. Preliminary data from cultures suggest
that the small relative size of the first reproductive
stage found in euedaphic species does not mean a very short
-------
generation time in compazison with the generation time
of hemiedaphic species. Further, the first ovipositions
of the euedaphic species T. macrochaeta and I. notabilis
comprise very few eggs (mostly 1-2) compared with the
number of eggs produced in the first oviposition by the
heniedaphic 0. furcifer (13—18 eggs). The average number
of eggs per oviposition during the whole life time appears
also to be lower in T. macrochaeta and I.. notabilis than
reported for heiniedaphic and euedaphic species (Gregoire-
Wibo 1977, Hale 1965) .Although it is less well documented
that the total average egg production per female is lower
in euedaphic than in hemiedaphic and epedaphic species
it seems fairly certain that the small size at which egg
production begins in these small euedaphic species is not
equal to a higher reproductive potential than found in
hemiedapnic and epedaphic species.
The small individual size at the start of the
reproductive period combined with a small number of eggs
per oviposition may be an adaptation to the narrow space
t,f the interstices • The low number of eggs per oviposition
is compensated for by an extended period of reproduction
with repeated ovipositions which is favoured by the con-
stant environmental conditions in the deeper layers of the
soil. The differences in metabolic rate betweer euedaphic,heniiedaP iC
and epedaphic species probably reflect the general level
of activity of the specLes. Epedaphic species move a lot
more about than euedaphic species in order to escape
from predators or quickly changinq environmental conditions
or in search for food.
Ccllembolan spncies living superficially have ac-
cording to Bödvarsson (1970) a higher percentage of fungal
hyphae and spores in their guts than species living deeper
in the soil. Fewer specir ens of the surface forms than
of the deeper living forms, however, have their guts filled
with consumed material. T ese results have largely been
confirmed by preliminary observations of the gut contents
of the Collembola from the Hestehave beech wood.The obser-
vati ns may be interpreted in the following way based on
Bödvarsson (op .cit.): The euedaphic species are obliged to
feed more or less continuously on a poor food, whereas the
epedaphic species as the other extreme must spend much time
and energy in search for better quality foods. In this way
the feeding biology may help to explain the different levels
of metabolic avtivity.
823
-------
CONCLUSIONS
The relationships between various ecological characters
of Colleinbola which have been described and discussed above
are summarized in the following somewhat idealized scem tical
list in which general properties of superficially living
(epedaphic) Collembola are contrasted with the corresponding
properties of thi rue interstitial soil spe ies (euedaphic
species). The hemiedaphic speci.es will in general terms have
intermediate characters.
F edaphic Euedaphic
vertical distribution surface,litter soil interstices
size of specimens large small
( bisexual parthenogenetical
J small progeny large progeny
reproduction ) many eggs(?) few eggs(?)
seasonally defined throughout the
year
metabolic activity high low
food ‘ high quality low quality
I dispersed omnipresent
SUMMARY
The paper presents results extracted from a comprehensive
study of collembolan ecology and energetics in a DaniEh beech
wood. 3 3
The population density varies from 19 . 10 to 67 . 10
per in 2 through a biannual period. The 2 biomass varies through
one year from 76 to 160 rng dwt. per m • About 60 species were
found within the research site of 1.5 ha.
The most abundant species are classified according to
their vertical distribution patterns as epedaphic (surface and
litter species) heuu. daphic (populations concentrated around the
soil—litter interface), and euedaphic (populations concentrated
in the minera.tl soil interstices).
The variations in size structure of different species
populations show that epedaphic and some heiniedaphic species
have seasonally well defined reproductive periods whereas other
82
-------
hemiedaphic and the euedaphic species reproduce through
most of the year. Parthenogenetical reproduction is typical
for euedaphic species in contrast to most hemiedaphic and epe-
daphic spec-it s which reproduce bisexueliy. The small euedaphic
species produce large progeny whch only weighs four to six
times less than the smallest reproductive adults. Epedaphic
species in contrast produce rclatively small juveniles which
need to increase many tim s in weight before maturity is
reached. Hemiedaphic species produce progeny of intermediate
size.
Results from respirometry experiments c ’xried out by
means of an open gradient diver method suggest that the rate
of oxygen uptake decrease from epedaphic through hemiedaphic
to euedaphic species of C. 1lembola .
The increase of environme:ital stability w .th depth is
considered a governing factor responsible for the differences
found between colleu’.bolan species attached to different hori-
zons of the soil. Further, the influence of the narrow space
in the soil interstices is included as a signiftcctnt factor.
The mode of reproduction and type of dewlopment from juvenile
to reproductive adult are discussed in the light of these
environmental properties.
The high metabolic rate of the epedaphic species seems
to have relation to the general locomotory activity of the
species including the feeding biology which involves search
for dispersed high quality food items.
LtTERATURE crrED
Anderson, J.M. 1975. The enigma of soil animal species diver-
sity. Pages 51—58 in: Vanek,J.(ed.):Progress in Soil
Zoology. Proc.5th Int.Coll.Soil Zool. The Hague:
W.Junk and Prague:Academia.
Bödvarsson, H. 1970. Alimentary studies of seven common soil—
inhabiting Collembola of Southern Sweden.Ent.scand.
1:74—80.
Gisin, H. 1943. Okologie und Lebensgemeinschaften der Collem-
bolen im Schweizerischen Exkursionsgebiet Basels.
Rev. suisse Zool. 50:131—224.
Gisin, H. 1960. Collembolenfauna Europas. Museum d’Historie
Naturelle. Genéve.3 2 pp.
Gregoire_Wibo,C. 1977. Aspects bio co1ogiques du cycle vital
de Folsoinia guadrioculata (Insecte :Collembole).
Annales Soc.r. ool. Beig. 107:11-24.
Hale, W.G. 1965. Observations on the breeding biology of
Collembo].a ( IX) .Pedobio].ogia 5:161-1/7.
825
-------
Mayer,H. 1957. Zur Biologie und Ethologie einheimischer
Col].einbolen. Zool. Jb. Syst. 85:501—570.
NexO, .A.,K.Hamburger and E. Zeuthen.1972. Simplified
microgasometry with gradient divers .Compt. Rend.
Trav.Lab.Carlsberg 32:139—153.
Petersen, H. 1971 a. Methods for estimation of growth of
Collembola tn cultures and in the field,exeapli-
fied by preliminary results for Onychiurus furcifer
(Börner) .IV.Colloq.Pedobiol. ,Dijon 1970.Ann.Zool.
Ecol.An.(hox:s s rie): 235—254.
Petersen,H. 1971 b. Parthenogenesis in two common species of
Collembola: Tuilbergia kcausbaueri (Börner) and
Isotoma notabilis Schäffer. Rev.E o1.Bio1.So1 VIII,1:
Petersen,H. 1975. Estimation of dry weightfresh wei ght and
calorific content of various coilembolan species.
Pedobiologia 15: 222—243.
Petersen,H. 1978. Some propexties of two high-gradient
extractors for soil inicroarthropods,and an attempt
to evaluate their extrar tion efficiency.Natura
Jutlandica 20:95—121.
Petersen,H. In press. Sex—ratios and the extent of partheno—
genetic reproduction in some collembolan popula-
tions.Proc.of a meeting on Apterygota.Pontignano,
Siena,September 1978.
Rusek,J. 1971. Zur Taxonomie der TuJ.lbergia (I4esaphorura)
krausbaueri (Börner) und ihrer Verwandten (Collenibola).
Acta ent.bohemoslov.68 :188—206.
Rusek,J. 1974. Zur Taxonomie der Tullbergii.nae (A erygot ’:
Collembola). Vest.Cs.spol .zool. 38:61—7C..
Rusek,J. 1975. Zwei neue Tullbergiinae—Gattungen A ’tery—
gota:Coliembola). Vest.Cs.spol.zooL. 39:23’.—240.
Rusek,J. 1976. New Onychiuridae (Collembola) from V ncouver
Island.Can.J.Zool. 54:19—41.
Snider,R. 1973. Labnratory observations on the biology of
Folsomia candida (WI] lem) (Col1ei ibola: Isotomidae).
Rev.Ecol.Biol.Sol 10:103—124.
Thamdrup,H.M., Overgaard Ntelsen,B. & Petersen.H. 1975.
The Hestehave Project. Pages 24—33 in: Vik,R. ed.
International Biological Progranmie . Final Report.
Scandinavian Countries ,Denmark, Fin1a d, rw,
826
-------
Sweden Oslo.
Williams,G.C. 1975. Sex and Evolution. rinceton Univ.Press.
Princeton, New Jersey.200 pp.
Yeates,G.W. 1972. Neniatoda of a Danish beech forest.I.
Methods and general analysis.Oikos 23:178—189.
ACKNOWLEDGEMENTS
The author wishes to thank dr. Kirsten Hamburger,
dr. Bjørn Andersen NexØ and professor Erik Zeuthen, The
Biological Laboratory of the Carlsberg un,Copenhagen,
for their instruction in the use of the gradient diver method.
Mrs. Hanne Vitus Joensen,Mrs. Gertrud Poulsen,and Mrs. Inger
Gotthardt are thanked for technical assistance at various
stages of the investigation,and Mrs. Gertrud Poulsen further
for typing the manuscript.
82?
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APPENDIX A
Density dominance rank of collembolan species found
in the Hestehave research site December 1969 to November
1970. Litter and uppermost 6 cm of the mineral oi1. The
taxonomy is mainly based on Gisin (1960).
dominance %
1. Tuilbergia krausbaueri (B6rner)+s.1. 37.1
2. Isotomiella minor (Schäffer 1896) 21.5
3. Isotoina notabilis Schäffer 1896 6.9
4. Folsomia nana dI in 1957 5 .3
5. Megalothorax nilnimus Willem 1900 4.2
6. Lepidocyrtus lignorum (Fabricius 1775),Gisin 1964 3.1
7. Sminthurinus aurous (Lubbock 1862) 2.6
8. Onychiurus furcifer (BBrner 1901) 2.5
9. Pseudosinella a].ba (Packard 1873) 2.4
10. Willentia anophthalma Börner 1901,H ither 1962 1.9
11. Tullbergia ca11ip gos Börner 1902 ++ 1.6
12. Dicyrtoma minuta (O.Fabricius 1783) s.1. 1.5
13. Onychiurus pannonicus Haybach 1960 1.3
14. Tomocerus flavescens (Tullberg 1871) 1.3
15. Onychiurus arinatus (Tu11berç ) Gisin 1952 1.1
16. Folsomia guadrioculata (Tullberg 1871) ,Gisin 1957 1.0
17. Onychiurus pseudovanderdrifti Gisin 1957 1.0
18. Frieseamirabilis (Tullberg 1871) 0.5
19. On yçhiurus absoloni (B rner 1901) 0.5
20. Isotoma sp.1 1ivacea group) 0.5
21. Anurida pyqinaea (Börnec 1901) 0.4
22. Xenylla grisea Axelson 1900 0.2
23. X boerneri Axelson 1905 0.2
24. Tulibergia denisi (Bagnall 1935) 0.2
25. Folsomia andida Willem,Lawrence 1973 0.2
26. Folsomia inonosetosa Rusek 1966 0.2
27. Neanura inuscoruin (Templeton 1835) 0.1
28. Willemia aspinata Stach 1949,, Hüther 1949 0.1
29. Orchesella flavescens (Bourlet 1839) C 0.1
30. Neelus minutus Folsom 1901 C 0.1
31. Willemia intermedia Mills 1934,Hüther 1962
32. Onychiurus serratotuberculatus Stach 1933
33. Isotoma sensibilis (Tullberg 1876)
34. Dicyrtoina fusca (Lucas 1842)
35. Proisotoma minima (Absolon 1901) 1
36. Eminthurinus flainmeolus Gisin 1957
37. Tomoceruslongicornis (MUller 1776)
38. Hypogastrura puxpurescens (Lubbock 1867)
9. Pseudachorutes dubius Krausbauer 1898 “
40. F 1somia Cf. spinosa I(seneman 1936
Accidental species. (Not ranked after dominance).
Hypogastrura cf. denticulata ( 3agna11 1941)
Friesea clavisetaAxelson 1900
Tuilbergia ( Warkeliella) peterseni Rusek 1975
-------
Isotoma cf. cinerea (Nicolet 1841)
IsotoMa viridis Bourlet 1839
Isotomurus palustris (MUller 1776)
Entomobrya corticalis (Nicolet 1841)
Orchesella cincta (Linné÷ 58)
Willowsia migroraculata (Lubbock 1873)
Se±ca doinestica+++ (Nicolet 1841)
Ileteromurus nitidus (Templeton 1835)
Lepidocyrtus lanuginosus (Gmelin 1788) .Gisin 1 4
Lepidocyrtus violaceus Lubbock 1873,Gisin 1964
Pseudosinella petterseni Börner 1901
Sminthurides puxnilis (Krausbauer 1898)
Sminthurides ma1mg eni (Tullberg 1876)
Arrhopalites caecus (Tullberg 1871)
Bourletlella bicincta (Koch- 1840)
Entomobrya multifasciata (Tullberg 1871)
+ Tuilbergia krausbaueri s.l.: According to Rusek (1971,
. .974,1976) this taxon is a composite group of species.
The Hestehave material is mainly composed of T.macro —
chaeta (Rusek 1976) but includes also T.krausb ri
(Börner) sei su Rusek 1971 and T. sylvatica Rusek 1971.
++ Dicyrtomina mirauta s.1. The material mainly agree with
D. saundersi (Lubbock 1862) but include a number of spe-
cimens identified as D. minuta (0. Fabricius 1783) and
D. ornata (Nicolet 1841). The ide . - cf these taxa as
separate species is questiox
+++ The appearence of these synantz r p specic.. in the
extracted samples may be r ue to a cidenta1 iII.LI.igration
frczn the laboratory duri’ig extraction.
829
-------
APPENDIX B
Important collexnbo].an species ranked according to ver-
tical distribution. Percent annual mean density in litter (L)
and the two uppermost three cm layers of the mineral soil.
(Definition of terms: epedaphic : Distribution concentrated
in or at the surface of the L layer; hypere4aphic : Main distri-
bution on plants above the soil and litter; hemiedaphic:Main
distribution around the soil—litter interface; ew’daphic :
Main distribution in the mineral soil).
L 0-3 cm 3-6 cm
epedaphic L.lignorum 64 27 9
T. flavescen3 58 35 7
juv. :hemidaphic D.minuta 5.1. 36 51 12
ad. :epedaphic S. aure s 27 56 17
to hyperedaphic
I W. anophtha].ma 44 51 5
I F.guadrioculata 40 58 2
hemiedaphic F. nana 34 56 10
I. notabilis 25 68 7
0. furcifer 24 71 6
0.pseudovand drifti 18 71 11
P. alba 14 66 20
M. ininimus 5 66 29
I. minor 2 58 40
euedaphic O.armatus s.str. 3 52 45
T. callipygos 3 44 53
T.krausbaueri s.l. < 1 42 57
0.pannonicus < 1 30 70
830
-------
+ ++ see appendix A.
APPENDIX C
Dry weights ( ig) of characteristic developmental stages in the
collembolan life cycle. Weights calculated from body length d3ta according
to Petersen 1975. Data from analyses of field popi.lations.
Suffix C: genital ,rif ice closed. Suffix 0: genital orifice open
Suffix e: eggs visible Inside body of cleared specimens.
min.juv.
min.2 c.
min.9 o
iitin.9 e
max. 9
(=max.
specimen)
min.d c
min.5 0
0. furcifer
o . pseudovanderdri fti
+
T.krausbaueri. s .1.
T.callipygos
F.nana
F.quadrioculata
I.minor
I. notabilis
L. lignorum
P. flavescens
D. minuta
max.
0.59
0.76
0.058
0.42
0.09
0.15
0 • 10
0.22
0.21.
0.66
1.11
4.85
5.27
0.11
2.51
0.70
1.06
0.44
0.70
4.00
27.4
15.5
0.27
2 • 51
1.29
3.11
0.58
0.87
14.4
0.31
3.11
6.05
1.18
1.06
9.35
176.
34.7
50.5
1.50
21.9
8.46
14.95
3.63
8.02
82.7
424.
317.
4.85
4.65
0.87
1.29
4.00
36.8
15.5
8.24
10.7
0.87
1.90
4.00
104.
18.0
21.9
30 • 0
4.14
7 • 60
54.2
293.
199.
+++ mm. 9 e from culture experiment mm. 9 e from cield datai 21,9.
-------
APPENDIX D
Ratios between dry body weights of characteristic deve1r nrnenta1
stages in the colleinbolan life cycle. Data from analysis of field
populations. (For explanation see APPENDIX A)
A: Female ratioE, ranked according to mm.? C r tio
min.juv. a
mi i i .?
c
mm.?
o
mm.?
e
max.?
max.?
max.
9
mtn.j
uv.
min.j
uv.
min.j
uv.
min.juv.
mm.?
mm
9 e
T.flavescens 42. 267. 642. 16. 2.4
L.lignorum 19. 45. 394. 21. 5.8
D.munuta s.l. ++ 1.4. 286. 21.
O.furcifer 8.2 — 27t 59. 7.1 2.2
F.nana 7.8 14. 35. 94. 12. 2.7
‘ F.quadrioculata 7.1 21. 40. 100. 14. 2.5
O.pseudovanderdrifti 6.9 19. 67. 9.6 3.5
T.callipygos 6.0 6.0 52. 8.7 —
I.m nor 4.4 5.8 12. 36. 8. 3.1.
I.notabilis 3.2 4.0 4.8 37. 12. 7.6
T.krausbaueri s.i. 1.9 4.7 5.3 26. 14. 4.8
+ ++ see appendix A.
+++ miii. 9 e from culture experimcnt
-------
APPENDIX D cont.
B: Male ratios ranked according to min. c ratio.
iiiln .juv.
mm • J
c
mm.
o
max. J
0
max. d
min.j
uv.
min.j
uv.
min.jU
V.
min.d o
T.flavescens 82. 158. 444. 2.8
L.lignoruin 19. 19. 258. 14.
D.minuta s.l. 14. 16. 179. 11.
O.pseudovanderdrifti 9.7 14. 40. 2.8
F.riana 9.7 9.7 46. 4.8
F.quadrioculata 8.6 13. 51. 4.0
O.furcifer 8.2 14. 37. 2.7
-------
ACTIVITY OF SOIL BIOTA DURiNG SUCCESSION FROM OLD
FIELD TO WOODLAND
Amyan MacfacJven
The New Unic’ers fly of Lilsier
Norih,rn Irdanj
INTRODUCTION
The purpose of this study, carried out in 1966 cud 1967 at
Molalaboratoriet, JutlElzd, Denmark, was two-fold. Firstly as a contribution
towards a survey of the ecological conditions tn the estate which surrounds
the Mole laboratory and secondly, in the context of the International
Biological Programme, to test the usefulness of “soil respiration” (carbon
dioxide emission from the Boil) as a general index of decomposition
activity in the soil. Since the work was done much has been published on
the latter topic but very little of it concerns relations between soil
respiration and succession, especially those features which follow changes
in agricultural practice. Also there are probloms and assumptions about
the interpretation of soil respiration methods which remain controversial
and for which additional data may be helpful. In what follows I shall
discuss briefly the features of the study area and the implications of
the survey results and then some devaild of the technique used and its
strengths and weaknesses in the context of preliminary surveys.
ThE STUDY AREA
The Mole Laboratory estate of some 150h.a. is fully described by
Thamdrup (1947). From the point of view of this study the main features are
that it is largely covered by an acid sandy soil much of which has been
cultivated in the past but has been allowed to revert to heath and woodland.
At the time of the study almost half the area was being maintained as meadows
for grazing or haymaking, dominated by Agrostis tanuis, Alepocurus pratensis,
Festuca elatior and Holcus lanatus with some other grasses in local areas.
The remaining sites were chosen in tiie region of Simmons Havsti and showed
stages of c succession (following abandrilent of cultivation) through bare
sand, Corynephrus canescens and lichens 2 to Calluna vulgaris( 6 ) followed
by invasion by shrubs, including Barothamnus Cytisus) scoparius (believed
to be a more vigorous variety from Southern Europe) and Juniper 9 communis (8)
and by treos, especially Pinus sy]veatrie 9 and Quercus uetraea’lO).
Two sets of sampling areas were chosen to represent the meadows and
the Calluna series and are numbered 1. — 5 and 6 - 10 respectively in this
paper. With the help of maps and air photographs loaned by Professor Thamdrup
and the recollections of Her Clausen Koch and Her Lauersen the dates nf last
cultivation of four meadows were eat abliehed.
631i.
-------
In the tables which follow data are given in the order:-
1. Krumehalden (3 years since cultivation).
2. Kj ilinge-Agre (nearly pure Corynephrua) .
3. Langbakke (6 years).
4. Kallebodder (5 years).
5. Horsehuller (over 6 years$.
(For details see Thamdrup 1947).
Of these areas, KJ&elliuge —Agre was vegetated with Corynephrus c aescens
and thus represented the first stage of the succession through Calluna to
woodland. In each meadow three widely spaced localities were selected and
a transect line established, along which three sets of three aujacent bi-
monthly samples were taken randomly. Thus 45 samples were taken on five
occasions; total 225 • In addition, the October/November cinpies were used
to test the value of allowing a “settling period” before taking readings (see
below).
In the case uf the Calluna succession series, samples were taken on
four occasions in addition to the extra series used to test the disturbance
effect.
The measuring techniq
The method used for measuring”soil respiration” was briefly described
in Brown & Maofadyen (1989) and is basically that of Anderson (1973), whose
paper includes a useful survey of the history and characteristics of the
method. Basically it cerives fr m Jiaber’s (1958)and Witkamp’s (1966a, b) tech-
niques and from Conway’s micro—diffusion method (1950) and consists of
insertion of small open-ended plastic cylinders (25cm 2 area by 10cm height)
into the soil where they normally remain for a period of months. When a
reading is to be taken an airtight cap is fitted from which a small glass
dish is suspended. Usually Sal. of approximately N/1O Potassium hydroxide
solution containing excess Barium chloride and phenolphthalein/thymolphthalein
indicator is supplied to the dish through a small hole, otherwise covered
by a greased glass plate. After a measured period of one or two hours the
alkali is back titrated rapidly in the field with Hydrochloric acid using
a light portable aicroburette designed for the purpose. The amount of carbon
dioxide is calculated from the reduction in strength of the alkali after
allowing for the results of blank determinations.
On each occ: gion temperatures are taken at the beginning and end of
the absorption period by thermistor thermometer between each triplet of
samples at the soil litter interface and respiration dgta are calculated
both with and without e “temperature correction” to 10 C. In other words
tce corrected readings gre multiplied by a factor ghich assumes a Qio of 2,
the factcr being 2 at 0 C, 1 at 10 C and 0.5 at 20 C and proportionately at
intermediate temperatures according to the formula
log 10 Qio = 2 = 1O(log Ti — log Y 2 ) x 1
835
-------
in which Y 2 is the standard unit rate at x 2 = 10°C and Y 1 is the intermediate
temperature.
The consistency of the “corrected temperatures” over the annual cycle
pz’ovides a direct indication of the extent to which “spot” readings might
pro e of wider application as an index of respiration for a particular site.
The choice of Qio = 2 is Justified by experiments both in the laboratory
and the field and is usually accepted by other authors (e.g. Anderson 19 7 3)and Reinerg
(1968) bu see Withamp (186Gb) for contrary results and Minderinian & Vulto (1973).
Shade from direct sunlight is provided by aluminium foil if necessary. All
readings were started betwem 1100 and 1300 bra. This procedure adequately
deals with the needs of the local survey, but in the broader context of
testing the method for wider use in unknown habttats it is also desirable to
know whether readings taken immediately after insertion of the cylinders
bea ’ a consistent relationship to those after long exposure because this
might perrd.t a surveyor to complete readings in a single visit and operate
with far fewer cylinders. Therefore, in addition to the readings made as
above, additional ones were made in October and November by inserting fresh
cylinders into undisturbed soil and immediately commencing the absorption
procedure. The rationale behind this was simply that previous experiments
had shown a rise in “respiration” over about aix days followed by a fall
to about one—third of the peak level by the end of two weeks. Also it is
well—known that a burst of microbial activity follows disturbance of soil
in laboratory respirometer experiments. In fact, as shown below, there
proved to be a rather consistent relationship between the “disturbed” and
the “undisturbed” readings on the same dates.
Special treatment was required in the case of the Pinus site because
the very deep and long-leaved litter under theme trees was impossible to
manage in the normal respirometer tubes. Readings in these areas were
therefore taken by removing the litter from an area of 100cm 2 and measuring its
carbon dioxide emission separately in a glass dish covered with a sheet of
glass • The normal cylinders were then inserted into the P & H layers and
soil below the litter and treated in the usual way. Reault were expressed
both as the separate component contributions and as the total of the two;
correcting for the larger area of litter and for the disturbance effect.
RESULTS
The “soil respiration” data for the ten vegetation types (numbered
in the order of the five meadows followed by the succession series through
Calluna to Oak ( 10)) are summarised in Table 1 and Figure 1. These
figures all refer to cores which were “undisturbed” • that is were allowed
to settle and measurements made by carefully placing lids on the tubes
without moving these in the soil.
836
-------
TABLE 1.
Si—monthly soil respiration data from the ten vegetation types. Each
figure is the mean of nine readings (three ad.1acent cores at three distinct
sites) on each occasion. On each occaaio the crude data are ml 00 2 /25cm 2 /br
and the corrected figures are adjusted by a Q 10 = 2 function to 10°C. The
Columns 9* and 9b refer to soil and litter under pine respectively (see text).
Temperatures °C in brackets are means of nine readings.
Grassland Sites ‘Succession” series
SiteNo.
1
2
3
4
5
6
7
8
9*
9b
10
Oct.
(4•30
(3•90
(4.0 )
(4.10)
(4.00)
(4.90)
(5.5 )
(7.30)
C.40)
(8.5 )
Crude
Corrected
159
237
102
155
145
219
166
250
146
221
145
205
173
244
249
313
186
231
375
203
251
320
Jan.
(—0.2
( O. 2
:—o.2
:_O. 2 C
—O.2
(1.40)
(i.d0)
(2.20)
(j•94)
(2.2 )
Crude
Corrected
116
236
102
207
112
226
130
271
104
230
113
204
150
268
192
330
144
252
313
169
147
252
April
(6.60)
(L1.6
(730)
(730)
( 78 C
(6.20)
(5.90)
(5.90)
(5.40)
(6.7 )
Crude
Corrected
304
401
419
390
357
420
358
434
365
419
181
236
234
311
226
301
212
291
119
64
278
350
June
Crude
Corrected
August
Crude
Corrected
( 20 • 20) ( 261 C
327 229
155 65
(1G.2 (22.0
813 632
501 286
:2l.5
248
109
18.3
772
437
2l.4
407
192
19.2
1029
539
336
144
(16.3
1041
618
( 21 3 a
424
194
213 C
616
280
2 l.CQ
627
293
:lO.Tc
584
296
269
145
(20.6°)
671
321
The two sets of figures refer to the crude estimate (of ml CO 2 per 25cm 2
sample per hour) and to temperature corrected estimates derived by applying
the Qio function to the crude data using t &e mean oX the temperature at the
soil-litter interfage at the beginning and end of the sampling period. The
correction is to 10 C. It will be observed that the “corrected” vs.lues give
a much more consistent seasonal picture in the case of the succession series.
Analysis of variance of the corrected, undisturbed data for the ten
plant types demonstrates significant differences between the plant type. on
each occasion whether based on the “between triplets” or the “discrepance”
values.
To arrive at a realistic value for the pine soil it is probably best
to add to the soil estimates (column Oa) a further amount to represent the
837
-------
—— I-. — —.— — ——
Grasslanc ‘e.ries
Site
1
1
Site
2f
Site
3
Site
4
1
Site5
,ite
FIGURE 1.
The same data is in Table 1, corrected values only. Considerable
differences between monthly values for grassland contrast with very
consistent results in the succession series. The former perhaps linked
with root activity and desiccation in June. Rank order within each series
remains the same.
Succession Series
_______ SiteS
__ 7 L
_______ SiteS
___________ Site Ba I Site 9b I
Sitw 10
6
7 1
8
9a (9b
10 I
6
I
•i I
Ba
10
1
I
2
—
I
3
1
4
I
October
January
april
June
August
5
— I I I I I I I U
0 1 2 3 4 5 6 7 0 1 2 3 4 5
838
-------
- .----- -.-- .- - - - -- - — -- -- .--—- -
overlying litter. This 1 however 1 was inevitably disturbed when placed in
the glass respiration vessels (see methods). As a rou.h indication,
therefore 1 the cc.rrectjon factor of 0.54 can be applied to the litter measure-
ments, giving values of 203, 169, 64 and 145 Zor the October, January, April
and June sanpies reape tive1y. These can be added to the soil figures to
give totals of 4 4, 421, 365 and 341 units respectively. It may be noted
that these considerably exceed the values for all the other sites, also that
the seasonal pattern reflects that of seasonal leaf—fall.
If the seasonal patt’rn of the corrc.cted respiration figures for the
different vegetation types is e emined t will be seen that, by eliminating
temperature (which has been demonstrated by most authors to be the dominating
determinant of respiration rate - s e discuesi .a) we are still left with
rather a consist ut seasonal pattern in the case of the grassland sites but
not in the others. Various hypotb ’ses come to mir i. For instance the open
meadows on sandy soil are subject to considerable desiccation which could wel]
reduce both decoapositiotL and root respiration in the summer months. On the
other hand the April 55E of activity might be connected with rapid root
activity in April. phenumenon wh±c 1 was also detected in a more thorough
seasonal study in a grass area at Sesivangen (unpublisned).
TABLE 2.
A comparison beLween undisturbed (U) and disturbed (D) re .dings
taken in the ten vegetation types on successive occasions, 15 dcys apart
(October/November 1976). Disturbed readings were from rings placed immediately
prior to measurement. All figures are unite of p1 C0 2 /cm 2 /hr. To convert
to gC/m 2 /year multiply by 20. These are tb mean of reagings at three
adjacent positions (within 5cm.) and are corrected to 10 C. The vegetation
area numbers are the five meadows followed by the Calluna succession series
in the order listed in the text. Figures for site 9 ( Ptnuc ) apply to the
soil fraction only.
VegetationArea 1 2 3 4 5 6 7 8 9 10
Undisturbed 241 144 247 287 211 213 202 270 256 332
272 142 188 185 219 225 267 349 240 311
197 180 223 280 234 179 263 332 216 319
mean 236 155 219 250 221 205 244 313 231 320
Disturbed 382 226 360 484 424 383 416 533 389 682
447 223 426 452 435 387 444 626 468 662
379 301 359 495 433 402 492 680 453 628
mean 403 250 381 477 430 390 450 612 436 657
Ratio U/D .58 .62 .58 .52 .51 .53 .54 .51 .53 .49
Table 2 provides the data of the “disturbance” experiment conducted in
October/November 1976. Figures are the means from three adjacent respiration
tubes corrected for temperature. It will be observed that the ratio of
83
-------
undisturbed to disturbed readings is rather consistent, despite the very
different vegetation types with an overall value of 54%.
This figure iS used ‘o obtatn an apprco.imate value for the (disturbed)
pine litter and is referred to in the discussion.
DISCU8STON
The Local Survey
The results shown in Pig. 1 and Table 1 do not indicate any significant
difference among the grassland sites other thaxi Kj l1ivge—Agre which is
dominated by the pioneer grass Cozynephrus canes cens and which, as might
be expected has very low values. Prom this it appears that there was no
detectable 4 ’ ”ge in “respiration” between the three year and over six year
fields.
On the other hand the series correspondtng to a succession from Corynephrus
via Calluna and shrubs to the woodlind exhibits a three to four fold increase
in “respiration” which is roughly ranked in the order of the above—ground biomass
of the dominant vegeta’1o i. Subject to the reservations expressed below this
would appear to indicate a reasonable relationship with primary production
by the plants and serve as an encouragement to persue such methods especially
in order to establish the productivity status of other plant communities in the
region.
There is a considerable contrast between the seasonal patterns in the
grassland as against the shrub and woodland sites, the former showing a uniform
peak in April and decline again in June whilst the latter are much more consistent
through the year. This is discussed below.
The General Validity of Soil Respiration techniques
This topic has been extensively discussed in the literature in which views
on the usefulness of the technique vary from the optimistic (e.g. Coleman 1973a,
1973b, Lundgardh 1927, Virso de Santo et al 1976, Wanner 1970) to the guarded
(Anderson 1973, Witkamp 1966a, 1966b, 1969) to the condemnatory !inderman &
Vulto 1973). The general relevance is discussed by Tlacfadyen (1976).
In principle carbon dioxide can be contributed ‘;o the soil from:
1. Decomposition of litter derived from above ground.
2. Decomposition of roots.
3. Respiration of ‘rhimosphere” organisms deriving nutrients mainly
rom “leakage” of soluble materials from roots.
4. Respiration of mycorrhima whose carbon supplies are also derived
from roots (see Rarley 1973).
-------
5. Respiration of the roots themselves — but less carbon dioxide
translocated by the plant to above—ground parts (see Walter and
Haber 1957).
Of these sources perhaps Only the first two should be thought of as
part of the decomposer industry of an ecosystem and only the last is
unequivocally part of primary production. However it seems not unreasonable
to consider the rhizosphere metabolism as part of decomposition and the
mycorrhizal respiration as a symbiotic extension of the plant’s physiology and
thus to draw a line between items 3 and 4. The problem which has so far
remained insuperable is to draw ouch a line in practice.
Further difficulties arise over losses of carbon as soluble components
of the soil leachate and as carbon dioxide and other gases in the soil solution.
Short term effects have also been postulated, and sometimes demonstrated
involving expulsion of soil gases by changes in atmospheric pressure, water
table etc.
The extent to which these problems invalidatc. “soil respiration”
methods in practice clearly depends on the magnitude of the effects and
the level of accuracy required in particular studies.
Perhaps one of the most useful attempts to quantify the problem is
that of Chapman 197S, who workec’ in a Calluna heath and used a modelling
approach simiLar to that of Douglas & Tedrow (1959). chap ” first used a
rospirometer which permitted repeated electrolytic titration within the
covered vessel (1971) out later moved to terminal titration in a syringe
(1976) which has the advantage of greater accuracy but is otherwise quite
similar to the technique of the present study. ills approach was to model
the flows of carbon between the different compartments of roots, litter, root
zone humus and sub root zone humus and to f.Lt the results obtained by’ means
of a regression equation. In this way he concluded that 70% of th. total
carbon dioxide emission was derived from the roots. He makes no separate
estimate for mycorrhizae which, in the Danish heath were extremely evident
by their fruiting bodies and which Harley (1973) has postulated to be
capable of producing up to 30% of total soil carbon dioxide output. Presumably
this source would in fact be included in the “root respiration” of Chapman’s
study. The approach of Sunnell et al (1975) ii somewhat similar.
At the time of the Moislaboratory work the potential importance of
mycorrniza was certainly not appreciated and no estimate of their relative
prevalence in different vegetation types was made: inasmuch as it is
Juatiftabie o regard them as part of the primary production component
however th a should not iiavalidete the results obtained and it could go some
way towards explaining the very variable estimates of the importance of root
respiration which have been published (from 17% by Coleman 1973b in successional
grassland and oak forest, 35% by Edwards and Sollins (1973) in forest soil
through 40% Kucera and Kirkhaa 1971 in prairie to 70% by Chapman (1979) and
by Minderman and Vulto (1973) and by Wiant (1967) in forest soils.
8I1 3.
-------
Clearly, by far the most important factor limiting the usefulness
of “soil respiration” is that of the proportion of carbon dioxide derived
from “root respiration” in the broad sense of including mycorrhizal
respiration. The most urgent need if the methods are to be extended is
that greater insight should be obtained into ie relative roles of roots
in a range of ecosystems. This can be approached in a number of ways.
Experimentally Witkamp (1966b) com .ired me ’surements in which carbon
dioxide was prevented rom moving between soil layers as did Edwards and
Sollins 1973. Witkamp et al (1969) used other methods to physically
separate tbe different components. Technical problems due to disturbance
were not easily overcone in these studies but in general 1 wer estimates
of root respiration were arrived at. Physical separation of components
and the use of a respirometer to determine root respiration in grassland
was tried by Coleman (1973b) for old field and ‘ orest soils producing low
estimates for root respiration whilst in grassland (1973*) he detected
higher root activity. The extensive use of isotopic tracers for this
purpose still appears to be an untri r,d possibility.
In the meanwhile it is worth considering whether there is any value
in these simple techniques as a primary survey method. It would appear
from the present account that “spot” readings on a single occasion and
without allowing for settlement, consistently give approximately double
the estimate that would be obtained after a two week or more settlement
period. Also that “correction” to a atandard temperature permits some
generalization from one occasion to a seasonal average. The fact that the
seasonal pattern of the grassland readings contrasts so strongly with that
in the other sites, may well indicate a major seasonal effect of root
activity and even suggests that most of the “springtime peak” could Se
attributed to this factor whilst winter values represent decomposition
only.
LITERATURE CITED
Anderson, 3. M. 1973. Carbon dioxide evolution from two temperate deciduous
woodland soils. 3. appi. Ecol. 10, 361-378.
Brown, A. & Macfadyen, A. 1969. Soil carbon dioxide output and small scale
vegetation pattern in a Calluna heath. Oikos, 20, 3—15.
Bunnell, F. L. & Scoullar, K. A. 1975. ABISKO—lI a computer simulation of
carbon flux in tundra ecosystems. In: Structure and Punction of
Tundra Ecosystems : Ecological Bulletin 20 . Stockholm. pp.425—448.
Chapman, S. B. 1971. A simple conductimetric soil respirometer for field
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Chap ’ a , S. B • 1976. Production ecology and nutrient budgets. In:
Chap” ”, B. B. (Ed.) Methods in Plant Ecology. BlacIwell, Oxford .
pp. 157—224.
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Cbapmnn, S. 9. 1979 • Some interi alationships between coil and root
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Coleman, D. C. 1973a. Compartmenta] analysis of “total soil respiration”,
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Coleman, D. C. 1973b. Soil carbon balance in a successional grassland.
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Conway, E. J. 1950. Microdiffusion and volumetric error . C. Lockwood.
London. 391pp..
Douglas, L. A. & Tedrow, 3. C. F. 1959. Organic matter decomposition rates
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Saber, W. 1958. Oekologiache Untersuehimgen der Bodenatmnng. Flora,
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Nancy, J. L. 1973. Symbic sis in the ecosystem. J. Nat. Sci., Council
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Kucera, C. L. & Kirkham, D. R. 1971. Soil respiration studJ. s in tall grass
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Macfadyen, A. 1970. Soil metabolism in relation to ecosystem energy flow
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and microbes. Pedobiologia, 13, 337-343.
Phillipson, 3., Putnan, B. J., Steel, J. &Woodell, S. B. J. 1975. Litter
input, litter decomposition and the evolution of carbon dioxide in
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Reinens, W. . 1968. Carbon dioxide evolution from Ihe floor of three
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Thandrup, N. M. 1947. The Mols laboratory, an ecological laboratory ani its
working progr e. Natura Jutlandica, 1, 67-134.
&4.3
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Virso do Santo, A., Alfani, A. & Sapio, 8. 1976. Soil metabolism in beech
forests of Monte Taburno, (Campania, Apenines). Oikos, 27, 144-152.
I.
Walter, H. & Haber, V. 1957. Ube die tntensit5t der Bodenatiuung nit
Bernerkungen su den Lundegardachen Werlen. Her. dt. bet. Gee. 70,
275.
Wanner, H. 1970. Soil respiration, litter fall and productivity of tropical
rain forest. 3. Ecol. 58, 543—547.
Wiant, H • V. Jr. 1967. Influence of moiBture content on “soil re,piration”.
3. Forestry, 65, 902-903.
Witkamp, M. 1986a. Decomposition of leaf litter in relation to environment,
isicroflora and microbial respiration. Ecology, 47, 194-201.
Witkamp, M. l966b. Rates of carbon dioxide evolution from the forest floor.
Ecology. 47, 492-404.
Wi taamp, N • 1969. Cycles of temperature and carbon dioxide evolution from
£i’ter and soil. Ecology, 50, 922—924.
Witkamp, N. & Frank, U. L. 1969. Evolution of CO from litter, humus and
subsoil of pine stand. Pedobiologia, !. 358-365.
AcENOWLEDGEMErt’rS
The field work for this study was performed during my tenure of
a gues: professorship at the Mole laboratory. I am extremely grateful to
the colleagues who asaieted my work there and discussed results with me
and, in particular, I wish to thank Professor H. N. Tbamdrup for hts,
generous patronage and the Natural History Museum and Uni ‘ersity of Aarhus
at whose field station I conducted the research.
QUESTIONS and COMMENTS
MITCHELL : How important is the solubility of CO 2
in water in affecting the utilization of CO 2 flux rates as
a measure of e il metabolism?
A. MA F’ DYEN: I’m afraid I have not adequately considered
this problem. Certainly there are many chemical and physical
reactions which might influence CO 2 emissions. These should
be studied in particular soils but I know of no qualitative
as opposed to speculative data.
M. BASSALL : Please could you comment on the possible
value of recent advances in soil sterilizatiofl techniques for
‘ Ii ’
-------
isolating the contribution made by plant roots to the total
soil metabolism.
A. MA FADYEN : I have not succeeded in that kind of
technique altiiough I have tried some. I hold out greater
hope for tracer techniques in order to discriminate between
carbon derived from the plant directly and that from decomposition.
B. AUSMUS : The length of equilibration and incubation
greatly affects the variance and sensitivity of the measures.
What did you choose to use and why?
A. MACFADYEN : I am afraid I misled you. The “incubation
time” (i.e. the time of exposure of alkali) is one or two
hours. The period of two weeks which I mentioned is the
acclimatization time (the period during which open cylindets
should be in the field before closure and absorption measurement).
M.S. GRILPjROV: What is the contribution of soil animals
to co 2 evolution from the soil?
A. MACFADYEN : The best estimates of which I ant aware in-
dicate that the animals account for between 5% and 10% of the
microbial respiration.
8 1 e5
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SESSION X: CLOSING
Moderator: Daniel L. Dindal
SUNY CESF. USA
&1.7
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r WORMS AND K WORMS: A BASIS FOR CLASSIFYING
LUMBRICID EARTHWORM STRATEGIES
I. E. Satchel!
MerI, o jj Pj,ggrch Station
UK
The development of the idea of dividing earthworms into two
groups, surface—living red—pigmented. forms and soil dwelling, non—red-
pigmented tomes leading to Bouchê’B (1977) classification into ‘epig ’,
‘endogé’ and ‘anecique’ life—forms is reviewed. It is suggested that
the contrasting behaviour, morpholo r and physioIo r of the two forma
represent evolutionary poles arising front r and. K selection. Characters
acquired in response to adaptive radiation into a variety of habitats
are interpreted as secondary- to those reflecting position along the
r/X gradient.
Introduction: the &evelopment of an ecological, classification of earthworms
The first recorded functional classification of eatrthworms appears
to be that of Dan Juliana Berners, prioress of Sopvell Minnery, who in
11.85, in the first printed book on angling recommended as bait for eels
‘the great angle tvytei’ and, for all. other fish, ‘red worms’. Little
oi further vermicologjc .i interest occurred. until the late eighteenth
century when Linnaeus (1758’), 0. F. Muller (i771 ) and Fabricius (1780)
laid the foundat3 .ons of modern earthworm taxonomy. After a further century-,
a basic edaphic distinction was drawn for the first time by P. E. Muller
who in i88 e drew attention to the abundance of earthworms in mull soils
and their absence, as he thought, from mor. The idea was notably expanded
half a century later by his fell w countryman Borr ebusch who in 1930
distinguished the lumbricid faunas of six types of soil and vegetation in
Danish forests and heaths. Two of his most contrasting types were
a) fresh mul]. soil with Lwnb icua t92’2’sBWia,, AUoiobophora ongaj
OctoZaeium cyaneum, Aiiolobopho2’a turgida., A. trapeaoidee, A. chiorotica
and Eisenia roeea, and b) beech raw humus with Dendr’obaena octoedra, and
more rarely, Lwnbricua rubeUus , L. ccz8tW2euB and Dendrobaena ‘borea. ‘
To this background of edaphic and distributional classification
and their own studies on agricultural habitats, Evans and Guild in
l9 7—55 added extensive data on life histories and behaviour of the common
species, distinguishing between a) the deep dwelling species which form
well—defined burrow systems, cast on the surface or in soil spaces and
generall,y aestivate during the sier, and b) the surface—dwelling non-
burrow—forming species which neither aestivate nor form s-.arface worm casts.
Their data and, his own observations were then s ’nmmrized. by Graff (1953)
who divided the common lumbricids (Table 1) into a) red .gmented surface—
living species, which occur prt dominantly in habitats with organic surface
horizons, produce many cocoons, mature rapidly and may produce several,
generat ions in a year and b) those without red pig. . nt which live in tbe
mineral soil, occupy cli agricultural habitats except c nrpost, have a iative]y
low rate of cocoon produntion, mature slowly, aestivate and produce only
one generation each year.
“Throughout this paper, species names and spellings are those of the
authors cited.
848
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TABLE ].
Distribution arid reproductive rate of common earthworms (from Graff, 1953)
Arable Grasslaiid Forest Compost Cocoons Hatching Maturation Offspring
per year time time per year
er worm (weeks) (weeks) per worm
Bed pi nted
Lwnbi’icue terreatr e ++ ++ + 0 1.0 50 35
Lwnbricue rubellue 0 +++ ++ + 914 10 140 80
Dendrobaencz aubrubiôunda 0 + ++ ++ 95 14 15 110
Eiaen! a foetida 0 0 +++ +++ 1140 3 9 350
Not red pi nented
‘ Alioiobophora
++ + 0 35 12 50 30
aaiginoaa
AUoiobophora
++ + 0 21 12 50 18
roeea
AT.Zoiobophora
+ 1+ 0 0 31 7 29
ohiorotica
-------
The functional significance of the red pigmentation has been
interpreted as a protective adaptation against injury by ultra-violet
light (Zielinska 1913, Merker 1926a, 926b); as a. mechanism for
controlling the extent of exposure during surface movement (Svendzen
1957 based on Eenc1925); end as a cryptic adaptation to predation
(Satchell, 196Th).
Perel (1975, 1977) emphasiaed the different feeding habits or
the surface—living and. burrowing types and within each distinguiehed
three groups of species occupying different horizons.
During the 1950s and 60s, many further differen es, morphological,
behavioural and pkiy-siological, were demonstrated between the pigmented
and unpigmented groups or representative pairs of them. Surface—living
species were found to have a grasping tanylobic or closed epilobic
cephalic lobe (Semenova 1966); pennate fibres in the longitudinul
parietal musculature (Perel and Semenova 1968); to be small and
mechanically unsuited to burrowing (Arthur 1965); to have a thin cuticle
(Semenova 1966). a cylindrical intestine a. d a simple unfolded typhlosole
(Semenova l96 .). Soi: dwelling species tended to be epilobic or
proepilobic; to have bundle-like fibres in the parietal muscles; to be
larger and to have a thicker cuticle, a beaded intestine and a folded
typhlosole.
In general • the surface—living species • when compared with the
burrowing species were found to be more tolerant of soil acidity
(Satchell l955 Laverack 1961); more berisitive to ultra—violet light
(Stolte 1962); FInd more mobile over the soil surface (Svendsen 1957).
Haughton t a (1958) demonstrated differences between Lwnbricua terreeti-ia
and. A7.Zoiobophora trrestria in the o rgen dissociation curves of the blood and
Needliam (3.957) showed thnt L. texrieatria excreted nitrogen at a substantially
higher rate than A. caliginosa. Semenova (1967) observed that the chiora—
gogenous tissue is unistra.tous in surface dwellers and multi—stratous in
soil dwel1e s and considered that the ability to accumulate glycogen in
chioragogenous tissue facilitated diapause.
In an nportant contribution on the respiration rates of earthworms,
yzova (1965 then shoved that a more intensive metabolism is characteristic
of litter dwcl].ing and surface active specieB. She demonstrated first that
the mean rato of oxygen consumption of pigmented species tends to be higher
than that of unpigmented species of about the same size and that, in most
pigmented spicies, oxygen consumption is strongly dependent on body size whereas
in unpigment d soil dwelling species e.g. Eieenia roaea and AUoiobophora
caiiginoaa, .he two parameters are only slightly correlated. In her
discussion o’ these results, yzova noted that the pigmented species with
a higher met bolie level penetrate further to the forth than non—pigmented.
ones • the distribution of Dendrobae’2a octaedxa for example extending to
the shrub tundra where under the prevailing conditions of low temperatures
and short vegetation period it lives as an ephemeral.
A further distinction between the bio1o r ot the pigmented and
unpigmented species was made by Satchell (1967) who used the data of
Evans and Guild (19 1 e8) to show the striking relationahip between the numbers
of cocoona produced by the different species and the severity of their
environments. For example, the deep burrowing non-pigmented species A. ionga.,
A. nocturna and. Octolaaion cyanewn which are most ‘rotected from desiccation
and temperature fluctuation produced 3—13 cocoons per annum whereas the
pigmented Lwnbricua rube 4 ue, L. oaataneue and Dendrobaena eubrubicunda
which live near the soil surface and. are most exposed to heat, drought an
predation produced 1 2—lO6 cocoons in a year.
850
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Bouch ’s i.gnopsis
From this background and his own field experience, Bouché (1971,
1972, 1977), has proposed an ecoiogical classification of arthvorms
arouni three generalised lifeforms, “epigê, endogé and anecique”. These
axe baisi ally the surface—dwelling red—p 4 ginented worms and soil-dwelling
aon—red—piginented worms of earlier authors but distinguishing as axiecics
(from Greek, which come up) those species which have deep burrows hut come
to the surface to feed or defaecate. The characteristics of these groups
can be summarised from Bouch (1977) (Table II).
An alternative interpretation
The system now proposed utilises most of the attributes listed by
Bouché (Table II) and some others and suggests axi evolutionary- rationale
for selecting them.
Selection pressures in earthworm evolution
Stephenson (1930) suggests that adaptive radiation in terrestrial
annelids proceeded concurrently with the spread of the angiosperins in the
Cretaceous. It seems likely, in view of the basically aquatic form of
organization, that the first lumbricids were mud—dwellers, perhaps similar
in habit and form to Re odz’ilua occulatue, with a low reproductive rate,
low metabolic rate, low population density and low-grade organic matter
as their ‘ood-source. From this form of organization it is purhaps a short
evolutionary step to that of a soil—dwelling earthworm, a vi v consistent
with that of other workers Ghilarov l9Ii9, Wileke 1955) that the early
lubricids ver soil dwellers and that the main phylogenetic trend thereafter
was to life on the soil surface.
Since the most nutritious and abundant food occurs in the surface
organic horizons rather than in the mineral horizons, selection pressures
seem likely to I’ave favoured forms which could actively seek out and
consume surface organic matter. Colonizing species would require a high
metabolic rate sufficient to maintain the m bility required for food searching,
and it would have been advantageous to deve.Lop sensory mechanisms for selecting
these food sources and behaviour patterns serving to keep t. population in
their vicinity.
Organic horizons are best developed today in regions with severe winters,
at high altitudes and at high latitudes 1!j tundra and boreal vegetation.
Colonizing earthworms in earlier epochs vou d have encountered similar habitats
and their ability to exploit surface organic matter as a food resource would
have depended 1arg ly on their success in surviving freeziné,. Hubta (1978)
describes the effect on lumbricid populations of winter temperatures in Finland.
Animals living in soil or litter were usually protected against low temperatures
by snow but when this was thin or absent, populrtions of Dendrobaena octaedra
and Lwnbricus rubelius fell tc 10% or less. These observations are consistent
with those of earlier woriters in the US& (Hopp & Lin ier, 19147) and Denmark
(Larsen, .L9 1 9) who reported reduced population densities after cold winters,
and, with those of Bengston et oi. (1979) who r uid that T•. 2 ”UbeZiuB and
A. caiiginoea survived in litter bags under 20 cm of sn•Jw in Iceland.
Persson and Lohm (1977) £o’md the biomass of Dend2’obaena octaedz’cz the same in
winter as in suamer, the worms moving downwards to a depth of 10 cm. Their
site at 600 latitude was however much tarther south than Iluhta’s. Ghiliarov
(pars. comm.) reports that Eieenia nordenakiol.di&, known only from the
Pusaian tuntha (Mnt’v-eyeva et al, 1975), survives freezing and at least a
proportion of earthworms in northern latitudes, if acclimated, appear to
survive temperatures down to about —3°C. At lower tempe.ratures and in
851
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TABLE XI
Summary of characteristics used by Bouch to distinguish
ecological types
Epigeics Endogeics Axiecics
Related to burrowing habit
1. Burrowing muscles Reduced Developed Strongly
deve1op d
2. Longitudinal contraction Nil Nil to feeble Important
3. Hooked chetae Absent Abs it Present
14• Weight Small Small to large Often large
(10-30mg) (adults
200—1100)
Related to surface habit
5. Sensitivity to light Feeble Strong Moderate
6. Response to irritation: Positive Positive Positive
mobility Rapid Feeble Moderate
7. Skin moistening Developed Slight Strongly
developed
8. Pigmentation Homochromic Absent Dorsal and
(red brown anterior
or green) (dark brown)
9. Regeneration Ni]. Important Important
variab].e)
Other characteristics
10. Fecundity High Limited Lim.,.ted
11. Maturation Rapid Moderate I’ oderate
12. Pespiration rate High Feeble Modest
13. Survival of adverse
conditions As cocoons By qa1el. cenc True d. .apause
lie. Food size Mesopha.ge Microphage Macroph ge
.L5. Intestinal traxsit Slow Rapid Var& ib1e
852
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populations not acclimated to freezing, few worms, if any-, survive and
populations overvinter as cocoons, — a strate r requiring the metabolic
capacity to grow and reproduce rapidly during the favoarable season.
Since surface feeding carries the penalties of exposure to pred tors,
ultra—violet irradiation and desiccation it would have been advantageous
to develop cryptic colouration, nocturnal surface activity, surface
movement during rain, and means of moistening tile respiratory sur ace
with secretions. Tolerance to the acidity of maz’.y types of iitt:-’ layer
would also have been reauired.
As the group spread and competition for food intensified, adaptations
to pioneer conditions will tend to have been replaced by new adaptations to
survival on the lower grade food material of soil organic matter and by the
return of the burrowing habit. Survival through the cold season be ow
the soil surface creates the possibil: ty of extending the life span beyond
one season. A high biomass can then exisi throughout the year ready to
exploit the available food supply whenever temperature and nr isture
constraints p2rmit. The need for rapid maturation and reproduction declines
and the reduction in mortality from surface hazards reduces the rate at
which cocoons must be produced to maintain the population density. Once
the need to seek out a nitrogen—rich food source in order to produce a big
seasonal batcb of cocoons ceases, it becomes possible to conserve ener
by reducing the rate of body metabolism and to adopt a more sedentary life.
By the operation of surface lairs, reducticu in metabolic, rate permits an
increase in body size and hence the power to form burrows. Subsurface
feeding on soil organic matter can +,hen be combined with feeding on urface
plant remains from below ‘.r collecting materials on the surface close to
burrow openings. 1xelusivel,y subsurface feeding patterns may also develop,
including subsoil feeding. It then beccwnes prudent, so to speak, to
mañmise resource conservation by onibining low metabolic rate with ‘ugh
Longevity. Adaptive radiation irto a variety of niches in both organic
and mineral horizons could be expected to produce specialists in cop ph gc as,
corticolous, aubsoil, amphibiotic and other habitats.
It seems therefore that the Lumbricidae may have evolved from lire in
the soil to life on the surface and back again and that species with
adaptations to soil dwelling are not necessarily older than species adapted
to life on the soil surface. Wide differences in ecolo r between npecies
in the same genus provide support for this view. Eieeni foet(4iz and H. roeea
and 8imaotoe eieen and B. mjldali show totally different modes of Life
as, according to Perel (1971 , do Dcndi’obaena attemei and D. al$r a.
Although revisions in nomenclature may eliminate some of these examples,
others, for example in the genus Tz4mbr cue, seem incontrovertible.
DiffeLentiation within species at the present time, e.g. in AUolobophora
chiorctica (Satchell, 196Th) seems also to support the view that much of
the adaptive radiation to be observed in the Lunibriei&ae is relatively recent.
In the northern hemisphere, the most important recent event in
lumbricid evolution is the obliterasion of the endemic populations of large
areas by glaciation and the post—glacial recolonization cf these areas by
peregrine species. It can be inferred from the absence of post-glacial
end.emics that these events are too recent for new species to have evolved.
Nevertheless, the changing selection pres3mes exerted on the exiating stock of
species as the tundra—ilk. babitats of the immediate post—glacial period were
succeeded by temperate ecosystems determined the species compoaition of
the present—day ].umbricids • Se1e tion pressur-s “avouring initially the
short, fast life style of the surface feeder must have swung as the clisate
ameliorated to favour the slow, resource-conserving life-stile of the soil
dweller. The earthworm’ a answer to the question of whether it is better to
853
-------
live like a lion for a. day or a lamb forever is, on this interpretation,
partly historical and partly geographical.
Earthworm strategies as responses to r and K selection
It seems desirable in principle to harmonize ideas in soil zoolo r
with concepts already established in genera]. ecological theory. The division
of earthworm lire styles into these two basic types is paralleled by the
concept of r and ic selected species, already well established in evolutionary
theory in 1967 by MacArthur and Wilson. The terms r and K are taken from
the Verhulst- ’Pearl equation
dN N
= r C’, - N
where N is the population !ensity
r is the intrinsic rate of nature], increase
and K is the carrying capacity of the environment.
Discussing what happens to pcpulations that invade ialand. environments,
MacArthur and Wilson coined the terms ‘r selection’ and K selection’ to
describe the different ways in which populations might function to survive
in uncrowded and crowded environments. In an environment vith no crowding,
genotypes which harvest the most or the best food will rear the largest
families and be most fit, evolution favouring productivity, but in a crowded
environment, genotypes which can at least replace themselves with a 8 = i 1
family at the lowest food level will win, the food deisity being lowered so
that large families cannot be fed. Where climates are rigorously seasonal
and winter survivors recolonize each spring in the presence of abundant food,
r se1e -tion will operate favouring high productivity but where seasons are
more unifoi-ml.y benign , K sd action favouring efficiency of conversion
of f” od iz 1 to offspring will result. Newly colonizing species will be subject
to r selection but, once safely established will tend to become K selected.
While emphasising the imrortance of se ore wilLtera in generating
r selertion, MacArthur and Wilson explicitly recognized constraints on food
and feeding as the crucial evolutionary pressure. Thus, in habitats with
surface organic matter horizons and winter temperatures too low to permit
feeding, r life strategies wiU be expected and where these horizons are
lacking or transitory and soil becomes the main habitat, IC strategies will
prevail. In mediterranean or arid climates, the hot season imposes a similar
constraint on earthworm feeding and only species which have evolved methods
of combating desicea,cion survive. If a consequence of the hot season is
an accumulation of surface litter ana if this is not destroyed by fire but
is available as food. in the fouowing vet season, r strategists may be
expected to evolve no less than in high latitudes. But if the hot seison
accumulation of litter disappears before feeding is again curtailed ny winter
cold or si e.r drought, soil dwelling LC strategies may be expected to prevail.
Southwood et a (19714) and Southwood, (1977) discuss the stability of
the environment as the arbiter of r and IC selection, discontinuous distribution
of food sources in space and time generating r s 1ection. Stahility in
the earthwort environment is determined partly by food distribution but
perhaps more importantly by variability in the conditions permitting feeding.
Coprophogous and corticolous species encounter .3Datiel diecoLtinuaty in t ie
distribution of their food. sources and l ster feeders encolmter seasonal
fluctuations ii, supply. Soil organic matter provides a relatively stable
food source and the oi1 en,ironment is substantially buffered against the
variations in moist’Are and temperature which limit feeding in surface—living
rpecies. Surface habitats cend therefore to be r-selecting and nub—surface
habitats K-selecting.
8511.
-------
Attributes of r and K life forms
Piazika (1970) lists a numbe- of correlates of r and K selection
(Table III) of which all but relative abundance (which does not apply to
species but to groups of Bpec .eS) are zelevant to r— and K—selected
earthvcrm&i. There are unfortunately very few data available for earthworms
on several of these correlates but in general there is a clear correspondence
between the characteristics of Burface—liv3.ng pi nented species and of
r selection and between those of burrow-forming, non—pi nented species and
of K selection. Specifically, no data are available on mortality such as
might show density dependence althcrugh Tomlin and Miller (1980) have shown
in Eieenia foef.i.da that growth and fecundity are related to population density.
The pattern of 3urv’ivorahip is know i for very few species but in Lwnbricua
terz’eBtria it is undoubtedly of the type 3 pattern (Deevey (19147) with
heavy mortality in early growth ata. es (r.a ’iani and Satchell, 1970) and in
this respect it appears to be r selected. Population size, though perhaps
rarely constant in any earthworm species, is apparently more constant in the
burrowing than in the surface living fornis, post-embryonic stages of L. eaetaneue,
for example, disappearing entirely in some years during the simimer (Bouehd, 1977).
No eat1m teB have been made of the carrying capaeit of earthworm environments,
of the extent to which earthworm conmunities are saturated or of the intensity
of competition. Recoloni-.ation each year by surface-living forms occurs in
the sense tha the popuirtion is annually replenished after reaching its
aeasozial].y 1 west 11m2 ta by a new generation of pont—embryonic worms, soil—
dwelling species maintaining post-embryonic populations through adverse seasons
by vertical migration and. quiescence. For the remaining characters in Table III
the correspondence between surface—living worms and. r selection and between
soil—dwelling worms and K selection is generally well established.
Southwood (1977) has added a number of other concepts to this list.
Nigh levels of dispersal and fecundity, listed as attributes of r selection,
are veil—established characteristics of the surrace—a*elling species as their
converses are of burrowing species. Low and high levels of investment in
defence and other interspecific competition mechanisms, listed respectively
as r and IC characteristics, may- not be applicable to earthworms although it is
too early to assert this positively until earthworm pheromones have been
further investigated.
In discussion of body size, Soixthvood(1977) and Southwood at ai (19714)
interpret the large size of K—selected species as conferring survival
advantage as a means of defence against attack. The idea of a retaliatory
earthworm, however large, seems unsustainable de ’pite t.be popular concept of
the worm turning. A large worm atta.ked by a bird may lose a few segments
and survive when a i ) 1 worm would be consumed, nevertheless econo in ener r
metabolism and the mechanical capcity to burrow appear to be more important
benefits of size. With some few exceptions attributable to the peculiarities
of annelids, the characteristi s distinguishing surface-living and soil-dwelling
earthworms are not special to the group but are widely paralleled in similarly
contrasting groups of r and K selected species throughout the plant and
nn4m i kingdoms.
As e1ated to earthworms, the attributes distinguishing r and K
lifeforms may be considered as those concerning repeoduetion and productivity;
those related to the feeding behaviour associated with different levels of
productivity, including adaptations to surface living or burrowing; and those
which may- be adaptive or may- be associated with different metabolic rates
as either causes or effects. They are s” ” ised in Table IV.
855
-------
TABLE Ill
Some of the correlates of r- and. K—selection (Pianka 1970)
z - cleet ion
K— selection
Climate
Mortality
Survivorship
Population size
Intra & interspecific
competition
Relative abundance
Selection favours
Length of life
Variable and/or unpredictable;
uncertain
Often catastrophic, non—directed,
density independent
Often Type III (Deevey l9 47)
Variable in time, non-equilibrium;
usually well below carrying capacity
of environment; unsaturated
co mnunitiee or portions thereof;
ecological vacuuma recolonization
each year
Variable, often lax
Often does not fit MacArthur’s broken
stick model (King 196)e)
1. Rapid development
2. High max
3. Early reproduction
s. Small body size
5. Seme]parity: single reproduction
Short, usually less than 1 year
Fairly constant and/or predictable;
more certain
More directed, density-depentlent
thiually Type I and Ii (Deevey l9 e7)
Fairly constant in time,
equilibrium; at or near carrying
cepacity of the environment;
satura ed communities; up recolonization
necebsary
Usually keen
Frequently fits MacArthur model
(King 1961e)
1. Slower development, greater
competitive ability
2. Lover resource thresholds
3. Delayed reproduction
ii . Larger body size
5. Iteroparity: repeated reproduction
Longer, usually more than 1 year
Leada to
Productivity
Efficiency
-------
— ...._,“._,- -—_
A3IJE I V Sumi” ’y o . attributes of r and K selected eaxthworma
A. Direct1 related to fec.undity and, length of life cycle:
r K
1. Nimther of COCOOflB produced per worm Higher Lover
2. Number of embryos produced per cocoon Higher Lover
3. Inci bation time of cocoons Shorter Longer
1 . Maturation time froz i hatching Shorter Longer
5. Duration of reproductive life Shorter Longer
6. Time distribution of mortality Shorter Longer
7. Form of 5u2-v’ivorsbip curve Type III Type I or II
8. Seasonal stability of population density Lower Higber
B. Belated to the feeding behaviour required to sustain different
reproductive rates:
9. Surface or subsurface dwelling Surface Subsurface
10. Metabolic rate Faster Slower
1],. Mobility Higher Lover
12. Sensitivity to p5 Lower Higher
13. Sensitivity to light Higher Lover
1I&. Pi entation Pi uented Unpi nented
15. Avoidance of desiccation Quiescence Diapause
i6. Size Sm i1er Larger
17. Morphological adaptations to burr,ving Poorly Well developed
developed
18. Form of prostomium Tanylobic Epilobie or
proepilobic
19. Form of typhiosole Smaller, Larger, folded
unfolded
C. Related to metabolir rate
20. Nitrogen excretion rate Faster Slower
2],. InteLtina]. transit rate Faster Slower
22. Oxygen affinity of haenoglobin Lower Higher
857
-------
—7—
Characters not included in this list but noted. by Bouch6 (Table 11)
include food size and response to irritation. Insufficient publishel data
is available on either of these to permit their inclusion. Field observations
of responses tc ver1nifuges are difficult to interpret because size of
burrow openings and other confounding factors affect vermifuge penetration.
More direct ata are needed.
Intestinal transit rate is also difficult to interpret. Like nitrogen
excretion rate it may have adaptive significance or it may be a fvnction of
metabolic rate. The characteristics of the haemoglobin may- also distinguish
the two extremeB of life form but interpretation of its significance awaits
evidence from additional species.
Avoidance of desiccation in the surface feeding species is facilitated
by their high mobility, their habix of moving during rain showers and to some
extent by nocturnality. Summer diapause occurs in endemic species of regions
south of the limits of glaciation and perhaps evolved much earlier. The
regeneration of lost segments during diapause seems of doubtful ecological
significance although Bouchd (1977) consideru it an adaptation to predation.
Adaptive radiation within r and K Btrate ies
Within the confines of the r strategy several variations in life
style are possible (Table V). Dendi’obaena octaedrcz and Bieiraetoe eieoni,
living in forest or heathiand litter layers are seen as predominantly r-selected.
lumbrious castaneue occurs in litter layers but more abundantly in grassland
where it is adapted o exploitation of ephemeral ä ung pats. Eieenia foeti4a,
originany a corticc ,lous litter-layer species (Graff, 1971e) is now also
adapted to man—made h oitats in nitrogen—rich organic matter. Lirbricua
i’ubel2ijs,, primarily an r strategist, lives in fcest litter or in grassland
as a partial coprophage. In acme sites with a thin litter lay-sr it burrows
into the mineral soil and seems part way along the route to a IC strategy.
Zwnbrioua tarreetr e,, further along the same route, has the reproductive
features of a K life form but, having retained the r selected habits of
feeding and nating on the surface, also retains the pigmentation of the
r strategist. Riaeniel .ia tetraedva is perhaps an r strategist that has
become semi—aquatic.
Predominantly K-selected types are AiZoZ.obcphora caUginosa, living
in the A horizon of mull soils, reproducing slowly and maintaining a high
biomass throughout the year, and Eieenia i’oaea with similar habits.
Al.Zol.obophora chiorotica, also a mull soil dweller, lives just below the
soil surface where it is much exposed to bird, predaticn. Its pigmentation,
thought to have cryptic value, is of in entirely different: composition
(Kalmus, SatcheU and Boven 1955, Satchell 196Th) from that of r strategists.
A. ionga and. A. nocturna are two typical IC strategists which in their
exploitation cf the full depth of the A horizon have developed the behaviour
of defaece.ting on the surface. Their distal pigmentation is also of a
differen cozposition from that of r strategists. Oc’tol.c.w”t cyanewn and
0. iactmirn are K strategists edapted to exploitation of p z v ently moist
subsoil. The latter has a weak ability to diapause b .t is ‘nt o1ed ty a well—
developed network of subcuta.ieoua blood vessels and a high concentration of
haemoglobin to inhabit poorly aeiated soils (Perel, 1977).
858
-------
TABLE V Adaptive radiation of some peregrine earthworms
_____________ I C __
Surface feeders
Litter la ere D. c’ctaedra
Litter and • eiaeni
subcortical D. eubrubicunda
Litter and
clung pats L. 8t(D2ez48
Litter and E foetida
dung heaps
Surface and subsurface feeders
Semi-aquatic E. tetraedra
Litter, dung
pats and subsurface L. rubeUu8
Litter and soil
organic matter z. terreetria
Subsurface feeders
Surfac!e soil A. chiorotica
Soil organic A. noctia’na
matter and A. ionga
litter
Soil organic A. c. Uginoea
matter roeea
Ac uatic muds i. ocuiatue
and subsoil B. miiidaii
Subsoil 0. cya’zewn
O Zactewn
859
-------
—8—
Witnin the main d vi.sions of r and K strategists, many forms or
adaptive radiation a e thus seen to be possible and this can b expected
to apply also to endemic species. Where winter temperatures or suz er
drought do not permit survi val of post-embryonic worms r life-forms may
be expected, — where adult or juvenile orins can survive throughout the
year, a v’uiety of adaptations within the K life for.a will occur.
ir. the Megascolecidae, Lavelle ‘1979 fo.i.ad that small species
living close to the surface have a high multiplication rate and are the
most productive (P/B) and. the least efficient (P/I) and that large species
living deep in the soil are less produc! ive and more efficient. It seems
therefore that although some dive.cge!’I e may be found from the suites of
r and K a tributes appropriate to the Lvn bricidae the t4egascolecidae and
possibly other earthworm groups may also be capable of analysis in terms
of r and K seleci iori.
Acknowled ent
I e m indebted to Dr. T. G. Piearce for contrib.ating a number of points
of substance on earthworm evolution.
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-------
QUESTIONS and COMMENTS
M.B. BOUcHE : Just a remark about resistance by cocoons.
When I discovered this phenomena (in Lumbricus castaneus
Savigny) that was not during the cold season but in dry
r.uxnmer. To the best of my knowledge until n w resistance
by cocoons is the equivalent of quiescence or diapause during
drought.
J.E. SATCI LL : Yes, thank you. Although I have devel-
oped the theme of r—selection in earthworms primarily in
relation to colonization of regions with cold climates, it
could also be developed in relation to the seasonally avail-
able resources in hot climates. Cocoon survival through dry
sunmters would then be equivalent to cocoon urviva1 through
cold winters as one of the means by which populations persist
through adverse seasons.
GHILAROV : You have pointed out that earthworms
cannot survive freezing. But . octaedra and . nordenskioldii
do survive such freezing which is line vitrification.
J.E. SATCBELL : It is true that some earthworms can
survive freezing in the extreme northern limits of their range
and this may be by acclimation in for example D. octaedra or,
possibly an evolutionarily recent adaptation in E. norden—
skioldii . The point is not critical however since even in
these species they appear to suffer a severe reduction of
population in the winter. r—selection will therefore operate
to favour a high rate of population recovery in the spring.
.S. GEILAROV : You suggest that there are quite different
evolutiorary trends in colourless and pigmented Luinbricids.
But Eisenia nordenskioldii is found invariably pigmented as
w€ll as colourless in some localities.
I.E. SAT LL : In general the more K-selected geophagous
species are less pigmented than the more r—se].ected species.
However, polymorphic species can be found exhibiting inter-
specific differences in relaticn to the r-K gradient. Allolo—
bophora chlorotica may be interpreted in this way as having
a green pigmented form which is perhaps more r—selected than
the K-selected unpigniented form.
MS. GHILABOV : Earthworms were often found in winter in
frozen soil layers. They can be in the overcooled state 3!id
even active in the “vitrified” soil, as MN. Gorizontova,
L.A. Krasnaya and T.S. Perel (Uchenye Zapiski Moskovekogo
Gorodskogo Pedagogicheskogo Institute, LVI: 161-178, 1957) have
observed near of Moscow on L nbricus sp. (juv.) and Nicodrilus
caliqinosus . But they can also be quite frozen as B.A.Ticho-
mirov (Priroda, No. 5, 1957) observed on Novaya Zeinlya. There
were also did records of living earthworms frozen into the ice
(I. Recker, Zool. Cluz. Bd. 19:3-4. 1896; E. Sekera, ibid. 159).
There are also some data on “vitrification” of earthworms, but
not correctly analyzed.
86
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SOIL FAUNA STUDIES FOR SOLVING PROBLEMS OF
BIOGEOGRAPHICAL CONNECTIONS
M. S. Gbilarov
USSR ,caiowy of Scksc,s
Moscow. USSR
Soil animals are exclusively appropriate to elucidate
biogeographical as well as paleogeographical connections of
various territories, principally those taxonomic groups.
with representatives that have feeble potencies to disper-
sal.. Of especial interest with this respect are earthworms.
woodlice, millipedes, centipedes and higher insects whose
larvae develop in the soil whereae imagines are not or are
little capable of flight. Activ ’ly flying insects and vari-
ous invertebrates adopted to anemochory or ernithochory are
of minor value for su].ving biogeograpbical. problems.
Certainly biogeographical problems are to be solved
when studying territories minim .lly influenced by man where
the possibility of anth opochory is practically excluded.
Some examples taken froa the author’s own experience are
as follows.
En the red—coloured soils on limestone rocks of the
South Crimea coast the majority of larger soil invertebrates
belongs to species distributed in the Mediterranean, espe-
cially in the East—Mediterranean area whereas in other soil
types in the same locality Mediterranean species do not occur
or their percentage is manj times lower.
As examples. typically Mediterranean species may be
found such as Haploembia solier.i Ramb., Dilar turcicus Hag.,
Licirius silphoides Rossi, Ophonus subcruadratus Dej, Blape
mucronata Latr. and many others ccuunon to the Crimean red
soils. As such species do inhabit “terra rossa” in the
Mediterranean province, red—colou, .’d soils of the South
Crimean coast are to be identified as nowadays forming
“terra Rossa” (Ghilarov, 1956), because their regime cor-
responds to ecological, demands of various Mediterranean soil
invertebrates, which proves that these soils are the re-
sult of the contemporary soil formation. This excludes
the assumption of some pedologists that Crimean red soils
are fossil ones exposed by erosion.
865
-------
These data prove also that an, already disap-
peared, land connections of the South Crimea with Asia
Minor and the Balcan peninsula occurred in the Tertiary.
Another example is the study of “bald summits” of
calcareous mountains in the North—West Caucasus situated
above the belt of beech and oak forests (altitude 800—1100 m).
These summits are covered with steppe—like vegetation cover
(Stipeto-Festuceta or Fe ’ituceta herbosa) and the soil fauna
there is very similar to that in steppes of the Ukrainian
plains. Such a group as tenebrionids is represented by 0pat
sabulosum L., Pedinu . feinoralis F., Codescelis polita Sturm.,
and vlindronotus breviocollis Kust; though each of these
species may not be regarded as an indicator of steppe con-
ditions, the combination of species of this “taxocenose” is
characteristi.. of steppes. The same is true for Scarabaeidae-
Pleurosticti ( Amphimallon solstiti.ale L., Rhizotroqus
aestivus 01., Rhizotroqus aeautnoctialis Berbst, Pentodon
idiota Herbst). And the typical steppe genus Dorcadion was
represented by . caucasicum Kust.
Such ground beetles as zabrus spinipes F., and }Iarpalua
flavicoxnis Dej. or such weevils as Otiorrhynchus fullo Schrnk.,
Stomodes tolutarium Bob., Brachycerus junix Licht.. are common
to Ukrainian virgin steppes, though being of the Mediterranean
origin.
The cockroach ( Ectobius duskei Adel.), t ’e japygid
( Confusus rumaenus Silv.), the millipede ( Chromatoiulus
rossicus Tim.), the centipedes ( Escarvus retusid grnatus
FoLlcm., and Clinopodea flavidus escherichii Ver.), the
sowbug tracheoniscus q .iarovi Borutzki) and others are
typical to plain steppes of the steppe zone (Gbilarov and
Arnoldi, 1969). The occurrence of such sp cies with a neg-
ligible potency to dispersal shows the relic and not a sec-
ondary character of these mountain steppe ecosystems; the
penetration of these steppe elements upward into the mountain
through the forest belt is quite improbable. Not only steppe
vegetation but also the whole ecosystem of the studied summits
prove their immediate connection with plains in the xero—
thermic period before glaciation.
S
A soil faunal study was presently applied also to solve
the problem of the history of some juniper forests inside
the Transcasp an Desert.
866
-------
In this desert (West Thr3auenia) the western branches
of the Kcpetdag Mountain range are ending. This range is
now connected with other mountain systems 3f the Central Asia.
To the northwest front Kcpetdag separated from it by the
very dry Karakouxn Desert there are two isolated small moun-
tain ranges — the Small Balkhan and more remote and the
higher (alt. 1880 m) Big Balkhan. The southern slope of
this last range is covered with desert vegetation whereas
on the steep northern one there are Junipereta. Junipereta
in West Turkmenia represents isolat d arboreal communities
in mountains and are considered as those of humid type
(Korovin, 1961).
Northwestward from Kopetdag the northern slope of Big
Balkhan is the only site where juniper forests are growing
(surrounded with desert vegetation). On a steep slope
undergoing erosion, if growth conditions are favourable for
the edificator plant species, it is rather arbitrary to draw
a conclusion whether the vegetation cover is of a recent
origin (due to the possible passive transportation of saeds
by wind or birds) or of an ancient relic one. In the case
under study the arboreous juniper species both on the Big
Ba].khan and on the Kopetdag northern slopes is Juniperus
tuzkomanica , which is rather close to a more occidental one —
J. po1yca pos growing in Transcaucasus, whereas eastward in
Tien—Shan Mountain system it is substitut i i by turkestanica .
To solve the nature and age of Big Balkhan Junipereta the
data on soil fauna composition are of real interest.
In the Junipereta of Big Balkhan many soil animal species
were found common to Kopetdag Junipereta too. auch are e.g.
the earthworm Allolobophora Mich., described from
Iran, centipedes Lithobius icis 2alesskaya, known only from
Big Bal]chan and Kopetdag Junipereta and Henia bicarinata Mein..
found during our many decades of studies in juniper forests
of Kopetdag. the Transcaucasus, the South Crimean and the
Northwest Caucasus. Only in the 3unipereta of Big Balkhan
and of Kopetdag a new species of Pachvmeritmt was found which
is yet to be described.
In Big Balkhan there was found the ground beetle
Dvschirius beludsia Tschitasch.., described from Beludjistan.
Cockchafer ( Miltotrogus) aschhabadensis Nonv. and its white
grubs were sampled both in Big Balkhan and Kopetdag under
juniper cover.
867
-------
Such tenebrionids as Zo hohe1ops steinhargi G. Meclv.
and . arvatensis G. Medv., described and known from Kopetdag
only, were found also in a Juniperetum of Big Balkhan. The
same concerns also Blaps seriata ‘.—W. and the ant, Aphaeno—
gaster fabulosa K.Arn.
All these species are to be regarded as mesophilous
e. ements ct the soil population common to Junipereta in
West Turkmenia. absent under the xerophilous vegetation in
surrounding deserts.
- Korovin (1961) indicates that the penetration of the
Junipereta into t}’e Middle Asia occurred jr the Tertiary.
The occurrence in the Junipereta of Big Balkhan of the
above mentioned soil animal species common to Kopetdag (and
in some cases also to IChorasan, Elburs and the Transcaucasus)
proves the ancient (Tertiary) connections of juniper forest
biocenosea of Big Balichan with those of Kopetdag and other
southern territories (Girkan province).
Such connections could not have been established in
the dry Quarternary. Beginning from the early Paleocene,
Big Balkhan was a territory, acquiring during the sea trans-
gressions an insular position.
With this peculiarity of the history of Big Balkhan
the existence of many endemics (not mentioned in this communica-
tion) is connected.
But ntesophilous soil friunal species common to Big Balkhan
and Kopetdag prove that there were ancient immediate relations
of these mountain ranges dating from the early Miocene. In
the Mesozoicum the whole territory of the contemporary Trans-
caspian Turkmenia was under the sea. In the Eocene, Big
Balithan was an isle. P’ d in the early Miocene there was a
sea regression, and there was an immediate land connection
between Big Ba].khan and Kopet ag. In the late Miocene a new
sea transgression (the Sarmatian one) tc ok plmce; Big Balkhan
and Kopetdag bocame isles. In the upper Pliocene (Akchagyl
transgression) the aquatic innunclation became still greater.
In the Quarternary there was established a dry desert climate,
and the land bridge between the mountains of Big Balichan and
Kopetdag was unsuitable for the distribution of mesophilous
soil animals. But evidently of the Quarternary origin, some
868
-------
Big BaUthan dry suimr it inhabiting rodents are known in this
country besides only from Kopetdag and partly inhabiting
Transcaucasia ( Ochotona rufescens Gray. Meriones persicus
Blanf, Ellobius fuscocapillus Blyth. and others).
Thus during early Miocene was the only geological period
when there were possibly an immediate connection ano. exchange
between mesophilous soil faunal elements of Kopetdag and Big
Balkhan Junipereta. This is just the period when represent-
atives of the genus Juniperus supposedly invaded the terri-
tory of Middle Asia..
The existence of niesophilous soil faunal complexes
conunon to the Big Ballthan and Kopetdag (as well as Elburs and
other area8) proves this that Big Ba].khan was surrounded by
sea during the other periods of the Tertiary. Therefore,
from the biogeographic viewpoint it is clear that it is
necessary to appreciate the western limits of the mountain
system of Middle Asia not as coinciding with those of Kopetdag,
as it is generally accepted (Gerasiiuov. 1968). not with
Small Balkhan as it was suggested by L.S. Berg (1952). but
ending with Big Balkhan.
These data show that soil faunal studies do help to
solve some difficult problems of historical biogeography.
REFERENCES CITED
Berg L.S. 1952. Natural Zones of the USSR. Vol. II. Moscow
(in Rissian).
Gerasimc,v I.?. (Ed.). 1968. Middle Asia. “Nauka” Pubi.
House. Moscow (in Russian).
Ghilarov M.S. 1956. Soil fauna investigation as a method
in soil, diagnostics (the South Crimean Terra rossa
taken as an example). Boll. Lab. Zool. Gener.Agraria
F. Silvestri DcX:574—585..
Ghilarov M.S. and Ky. Arnoldi, 1969. Steppe elements in
the soil arthropod fauna of Ncrth—West Caucasus Moun-
tains. Main. Soc. Entoin. Italians XLVIII:103-112.
Korovin E.P. 1961. Vegetation of Middle Asia and Kazakhstaxi.
Pubi. House CJzbek Acad. Sci. Tashkent,
869
-------
QLJESTIQNS and COMMENTS
74.9. BOUCBE : When was the last (i.e. the most recent)
biologically possible contact between the c,roup of Balkhan
and the Kopetdag mountains?
If that means a separation since around 13 million
years ago (13 M.A.) I am surprised, at least for the earth-
worm Allolobophora persiana by the absence of morphologically
noticeable divergent evolution. As you know (my book 1972),
I prove a close relation between historical area pattern
and systematic hierarchy. For instance, the genus Scliero—
theca split off into two subgenera around 60-40 M.A. (opening
of Biscayne Bay); in the subgenus Scherotheca ( Scherotheca) ,
a species ( . ductin ) differentiated in the French Alps, and
these mountains formed in the Miocene (13 M.A.).. In turn,
this last species migrated later to Corsica thanks to a short
event - the drying up of the Mediterranean Sea (6 M.A.).
Today a peculiar subspecies is clearly differentiated in Cor-
sica (S. dugin breviselLa) . So, I think it is strange that
an earthworm species could remain unchanged (without diver-
gence) since Miocene.
GHILAROV : Though the territory of Big Balkhan and
Kopetdag separated in the Miocene, the territorial conditions
were very similar. The distribution of the Juniperata in
Middle Asia is dated from Miocene, and probably the whole
coimnunity is developing quite parallel. Existence of endemic
Big Balkhan species related to those of Kopetdag prove that
in some cases changes did occur e.g. the occurrence in the
South Crimea of ilaploenibia solieri , a species of older times
which had no possibility of later invasion.
870
-------
LIST OF PARTICIPANTS
Bo,uw.e 7. Abi&am
SUNY CESF
Syra use, NY 13210 USA
Jaiie.t A. AddLoopz
Department of Zoo’ ogy
University of Alberta
Endmonton, Alberta, CANADA
Caopa4 Andejroen
Royal Veterinary and Agricultural
University
Zoological Institute
O!( 1870 Bulowsvej 13
Copenhagen, DENMARK
OLo Andieat
Oer.artment of Ecology and
Envi rorinental Research
Siedish University of Agricultural
Sciences
S—75007 Uppsal a, SWEDE4
Ma g Appe ho
Kalamazoo Nature Center
121 E. Van Hoesen
Kalamazoo, MI 49002 USA
M ekey Atthw
Battelle Columbus Laboratories
505 ICing Avenue
Columbus, OH 43201 USA
Seuvziy S. Aiuma&
Battelle Columbus Laboratories
505 KIng Avenue
Columbus, OH 43201 USA
Ui oLe a a ue.t
Universite de I’rovence
rue H. Poincare
11397 Marsellle Cedex 4 FRANCE
DonaLd F. BeWLend
Vice President, Acadenic Affairs
SUNY CESF
Syracuse, NY 13210 USA
Cec.LZ& &Lpa2te de Moiw2eo
Instituto de Ecologla-Univ.
Mayor de Sar. Andres
Casilla Postal 20127
La Paz, BOLIVIA
G.i.Ue4 8e,ie .t
Laboratoire d ‘Ecologie
Geruerale et Appi.
Universite Paris 7
2 P1. Jussieu
75005 Paris, FRANCE
Go’w.n Bengb,.son
Animal Ecology Department
Ecology Building
Helgonavagen 5
S-223 62 Lund. SWEDEN
Uoyd IU. Bennet.t
Biology Department
Utah State University
Logan, UT 84322 USA
Pao2 Be’t.thLt
Universite Catholique de
Louva In
5 P1. CroIx du Sud
Bl348 Louvain Ia Neuve,
BELGIUM
ZI 8t4 8e4.W 66On
Department of Ecology and
Envi rotinental Research
Swedish University of
Agricultural Sciences
S-75007 Uppsala, SWEDEN
Jc.s.n-MojtJj &.toch
Laboratoire d’Ecologle
Ge ieral e
Museum National d ’Histoire
Naturel le
4 Av. du Petit-Chateau
S1800 Brunoy, FRANCE
871
-------
MeLoon Beye..t
Patuxent Wildlife Research Center
Laurel, lID 20611 USA
Tamttuj 8hattLte.haft!fa
School of Life Sciences
Visva-Bharati University
Santiniketan West Bengal, INDIA
Entomolgisches Inst.
ETH-Zentrwn
CH-8092 Zurich, SWITZERLAND
WLUAam &ock
Life Sciences Division
British Antarctic Survey
Madingley Road
Cambridge CB3 OET ENGLAND
MwieeZ Souckt
INRA
17 rue SuUy
Dijon F-21034, FRANCE
A. B’wce. Bicoo4bent
University of Guelph
do Agriculture Canada Research
Institute
University Sub P.O.
London, Ontario NM 5B7 CANADA
biLge P. Canaa1 a da. Fon&e a
Laboratotre de Biologie Vegetale
Route de la Tour Dennecourt
Fontal nebi eau 77300 FRANCE
Ma.n Co
Department of Soil Science
University of British Columbia
Vancouver, B.C. V6T 1W5, CANADA
Ken*e.th Ck t.L&t2anoe,t
Crinnell College
Grinnell, IA 50112 USA
0av4d C. CoZema i
Nature! Resource Biology
Laboratory
Colorado State University
Ft. Collins, CO 80523 USA
V. A. C’wutey, .1k.
Department of Entomology
University of Georgia
Athens, GA 30602 USA
James Cu/tAg
University College of Dublin
Dubl1 , IRELAND
Ry4mkd K. Cyiwwa
Department of Biology WSP
Ui Arciszewskiego 22
76-200 Slupsk, POLAND
Ve,iLeZ L. VLndaZ
Department of Forest Biology
SUNY CESF
Syracuse, NY 13210 USA
Ktaith H. Pomoah
Department of SoiP Biology
Federal Agriculture Research
Center
Bundesalle 50
Braunschweig D300 (FRfr
WES1 GERMANY
Catlwjtjjte E. Eeobncjt
Illinois Natural History
Survey
172 Natural Resourctc
Building
Urbana, IL 61801 USA
AnZtzn I.. Edgat
Alma College
W. Superior Street
Alma, MI 48801 USA
872
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C. A. Ed&’zi da
Rothamsted Exp r1menta1 Station
Harpenden, Herts, EP LAND
HeJirr a ELJ6aeb.et6
Rljkslnstltuut v. Natuurbeheer
mnper erger weg
Arnh n, HOLLAND
S. E-V A. Fa.4zq
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Zamalek, Cairn, EGYPT
MWzae.L FL6hv
SUNY CESF
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KeLth FZLtC.hVL
Ro.hamsted Experimental Station
Harpenden, Herts, ENGLAND
V. PauL F’w t t
Arete Vennlcoinp Inc.
4355 Lake Heights
Canton, OH 44708 USA
V ,ut (U. Fxethaait
Department of EfltO’T!oi oq_y
University 0 f California
Riverside, CA 92521 USA
14ene Gaicay
Ecole Nonnale Superleur
Laboratoire Zoologle
Universite Paris VI
46 rue d’Ulun
Paris 75007, FRANCE
lM.eczg .taw Goduty
Institute of Soil Science
Agricultural University
ul. Rakowlecka 26/30
02528 Warsaw, POLAND
Fned Gould
North Carolina State University
Entcm 1 ogy Department
Ra eigh, NC 27650 USA
P. 3. M. G&wtalade
CSIRO Division of Soils
Glen Omiond 5, S.A.
AUSTRALIA 5000
PeiwJ ope Gi&wtaeadt
South Australian Nusewn
Adelaide, S.A. AUSTRALIA 5000
Kwtht A. Gn4m,w
Department of Zoology
Michigan State University
Biology Research Center
E. Lansing, MI 48824 USA
(ILUAAm E. ffamZton
Ohio State University and
Ohio Agricultural Research
and Developmental Center
Wooster, OH 44691 USA
Man
School of Continuing
Education
SUNY CESF
Syracuse, NY 13210 USA
Me wLy S. OkLLa*cv
Institute of Animal
and Morphology
Acadeny of Sciences
Lenin Av. 33
Moscow 117071. USSR
Evolution
of the USSR
Roy Nwiten ttht
SUNY CESF
Syracuse, NY 13210 USA
McvLk Hao6aU
School of Envirorriental
Sciences
University of East Anglia
Norwich, Norfolk tlR4 7111 U K
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Stua B. K U
P0 Box 301 MacDonald College
McGill University
Ste. Anne of Be 1evue
PQ H9X ICO, CANADA
Jane Hoeche’i
SUllY CESF
Syracuse, NY 13210 USA
Sa2Lg G. HonrLo L
SUllY CESF
Syracuse, NY 13210 USA
Jame6 B. Hog
Department of Entomological
Sciences
Un1versit y of California
Berkeley, CA 94720 USA
Ve.j.hko Hukta
Department of Biology
University of Jyvaskyla
Yllopistonkatu 9, SF-40l00
Jyvaskyla 10. FINLAND
Vau id L. Kaplan
Environmental Protection Group
U . Ansy Research and Develop-
ment Coniiand
Natick, MA 01760 USA
VLLZO K4.tLzZc.uiz
Department of Biology
University of Occupational and
Environmental Health
Iselgaoka, Yahata Nishi-ku
Kitakyushu 807, JAPAN
Geo’cge E. KLee
Kent State University-Stark
Campus
6000 Frank Avenue NW
Canton, OH 44720 USA
E. C. Ko6.Ce,zmegen.
Department of Entomology
Washington State University
Pullman, WA 99164 USA
CknAM a F. U. Knappvi.
Universidade do Vale do Rio
dos Sinos
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H vLrnu.t H. KoekLe*
University Brwien
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Seppo Kapcne,t
Department of Zoology
University of Turku
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V. A. VJJJ.JOSJJtA Lg
A.N. Seventzov Institute of
Evolution and Morphology 74
Lenin av. 33
117071 Moscow W 71 USSR
Jan Lagen.Lo
Department of Ecology and
Environmental Research
Swedish University of Agri-
cultural Sciences
5-75007 Uppsal a 7. SWEDEN
Pa.t 2ck Laue2Le.
Labo’atolre de Zoologle de PENS
46 rue d’Ulm 75230
Paris, Cedex 05, FRANCE
Ph4 Up Lebicwt
Ecologle Animale
Place Croix du Sud, 5
1348 Louvain-La-Neuye BELGIUM
K. E. Le.e
CSIRO Division of Soils
Private Bag No. 2
Glen Osmonc • SA 5064 AUSTRAL IA
87k
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John W. Lee.tham
Natural Resource Biology
Laboratory
Colorado State University
Ft. Collins, CO 80523 USA
Jean•Ce ’ude L1on6
Laboratoire d’Ecologle-St. Jerome
Rue Henri Poincare
13397 Marsellle Cedex 4 FRANCE
Vwjte Là ng6.tc te
Co’liers Earthworm CompostThg
Systen
P0 Box 2910
Santa Cruz, CA 32211 USA
V&thA.e R. Lone
University of Tennessee
Apt. 303, 222 North Purdue
Oak Ridge, TN 37830 USA
S.teue.n 3. LO4A.ng
Departuent of Zoology
Michigan State University
203 Natural Science Building
E. Lansing, MI 48824
$Jny Ln ?I.o4 4zdye.n
New Univer lty of Ulster
Culeraine Co.
Londonderry 8152 1 SA N. IRELAND
SpylLo6 MOt 1 çe.ta4
Ecole t4onnale Superleure-Lab.
d’Ecnl.
46 Rue d’Ulm
75005 Paris. FRANCE
V4v d MaLLow
Department of Zoology
Michigan State University
E. Lansing. MI 48824 USA
Zahe.t Maa4oud
C N R S V4usetrn National
4 Avenue du Petit Chateau
Brunoy 91800, FRANCE
amea M. M 1Lua. ,t it.
SUNY CESF
Syracuse, NY 13210 USA
LouA4 .1. Me2z
USDA Forest Service
Southeastern Forest
Station
P.O. Box 12254
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Mykon J. MLtckeZL
SW1Y CESF
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John C. Moofte
Department of Zoology
Michigan State University
E. Lansing, MI 48824 USA
Eda vLd F. ?Jeuku4eft
SUNY CESF
Syracuse, NY 13210 USA
Roy No,c.ton
SUNY CESF
Syracuse, NY 13210 USA
Ma.t6 0L6oon
Department of Forest Soils
Swedish University of Agri-
cultural Sciences
Box 7001
S—iSO 07 Uppsala, SWEDEN
Venn Pwth. noon
Department of Biology
University of Calgary
Calgary, Alberta 1211 lN4
CANADA
Mak.tiii Pwtht6o
SUNY CESF
Syracuse, NY 1S l0 USA
Experiment
875
-------
8.LU. PwP.60fl6
Department of Biology
University of Calgary
Calgary, Alberta T2N 1N4
CANADA
Henn2ng Pe.te’ 6en
Mol si aboratorlet
FeimiØlley
DK 8400 Ebel toft DENMARK
Dau d A. Pke.taon
Department of Biological Sciences
North es tern University
Evanston, IL 60201 USA
Ktmte6k PwtJ JitL
Institute of Forest Zoology
University of Goettingen
34 Goettingen
Busgenweg 3 (FRfr) WEST GERMANY
A. Ro j A
Zaktad Biologil
Wielkopolska str. 15
Szczecin, POLAND
R. ManteL Reeuao
Department of Entomology
University of New Hampshire
Durham, NH 03824 USA
VLv d E. ReA .ghZa
Envirormental Sciences Division
Oak Ridge National Laboratory
PD Box X Bldg. 1505
Oak Ridge, TN 37830 USA
A. .7. Re2necke
Department of
Potchefstrocsn
Potchefstrooin
J g RemtzcZt
Department of Botany
University of Liege
Sart-Ti iman
4500 Liege, BELGIUM
KtauA 0. R cht,VL
John Graham and Company
1110 Third Avenue
Seattle, WA 98101 USA
RonaLd F. P.omLg
West Chester State College
RD #1
Chester Springs, PA 19425 USA
Stan G. Rwidgxen
Helglnov 5
22363 Lund, SWEDEN
PexoetL F. San.to 6
Department of Biology
New Mexico State University
Box 3AF
Las Cruces, 114 88001 USA
.7. E, Sa.tckeZt
Institute of Terrestrial
Ecology
Nerlewood Research Station
Grange-over-Sands
Cumbria, LA1l 6JUI U K
Gewige Sch&nk
Arete Vermicomp, Inc.
6180 Apulla Road
Tully, NY 13159 USA
Thotna4 ScMLe4e,i
University Bremen
Achterstr. NW 2
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WEST GERMANY
DonaLd P. &hwe*.t
Geology Department
North Dakota State University
Fargo, ND 58105 USA
John F. &imeone
Environmental and Forest
Biology
SUNY CESF
Syracuse, NY 13210 USA
Zoology
University
2520 RE. S. AFRICA
876
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Reiw.te M. SvJileii.
Department of Zoology
Michigan State University
E. Lansing, MI 48824 USA
R1e.hwLd 1. Sn4deic
The Museum
Michigan State University
E. Lansing, MI 48824 USA
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Ministry of Agriculture and
Fisheries
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SliMY CESF
Syracuse, NY 13210 USA
BenjainLn L S,tLIuwA
University of Georgia
Athens, GA 30602 USA
JUAILp SubagjLL
Department of Zoology
Michigan State University
E. Lansing, MI 48824 USA
A. .1. SZLLJeCk.L
Warsaw Agricultural University
02-526 Warsaw, Rakowlecka 26/30
POLAND
Mohoen .5. Tadwa
Faculty of Agriculture
Tanta University ARE
333 Ramsls Str.
Abbassla, Cairo, A.R. EGYPT
Ma.’th F.
SUNY CESF
Syracuse, NY 13210 USA
Ata.n V. Tomt2n
Research Institute
Agriculture Canada
University Sub P.O.
London, Ontario NSA 587 CANADA
Guy Ilann2e’t
C N R S Ecologie Generale
4 Av. du Petit Chateau
Brunoy 91800 FRANCE
G. K. Vwtei h
Department of Entomology
University of Agricultural
Sciences
Hebbal • Bangal ore 560024
Karnataka, INDIA
John P. VJ.awne/L4tedt
Ohio Agricultural Research
and Developmental Center
Wooster, OH 44691 USA
M4AtLna Vo -Lag e’LZund
Department 0 f Soil Science
Finnish Forest Research Inst.
Unioninkatu 40 A
00170 HelsinkI 17, FINLAND
Ma*eg A. Wdauv.
SUNY CESF
Syracuse. NY 13210 USA
El2zabeth wc2doFid
Deparbnent of Zoology
Louisiana State University
Baton Rouge, LA 70803 USA
John A. WaZbuo,Lk
Zoology Department
Westfield College
London M 3 1ST U K
Je4 n.ey H. Waugh
SIJNY CESF
Syracuse, NY 13210 USA
Geonge& Wau.thy
University of Louvain
Place Croix du Sud, 5
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John M. YiwoMkg
School of Continuing Education
SUNY CESF
Syracuse, NY 13210 USA
87 ?
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LIST OF ADDiTIONAL CONTRIBUTORS
JUN- ICH! AOKI
Institute of Environmental
Science and Technology
Yokohama National University
Yokohama, JAPAN
0. ATUVTNYTF
Institute of Zoology and
Parasitology
Academy of Sciences,
K. Pozelos 54
Vilnius 232500
LITHUANIAN SSR
VALERiE M. BEHAN
Department of Entomology
Macdonald College of McGfll
University
Ste. Anne de Bellevue, P.Q.
H9X lCO CANADA
L. BiGOT
Centre Scientlfque de Saint-
Jerome
13397 Marsefile
Cedex 4 - FRANCE
PATRICK 8LAt4DTN
Ecole Noniiale Superieue
Laboratoire de Zoologie
46 Rue d’ulm
75230 Paris-Cedex 05 FRANCE
W. BROCV)WJ
University of Breinen
P0 Box 334440
0 28 Brenen, WEST GERMANY (FRG)
J. C. SUCKERFIEW
CSIRO, Division Of Soils
Adelaide. SOUTh AUSTRALIA
P. WWGEI4
Department of Botany
University of Liege
Sart Tflman 8-4000
Liege, BELGIUM
MART E-MA1)ELETNE COLrEAUX
Museum National d’Historfe Naturelle
4 Avenue du Petit Chateau
91800 Brunoy (Essonne) FRANCE
R. N. VAN 1EL 30N
Department of Biology
The University of Calgary
Calgary, Alberta, T2N 1114 CANADA
.1. L. VODV
Natural Resouce Ecology Laboratory
Colorado State University
Ft. Collins, Colorado 80523 USA
AIZSON P. FRATER
Department of Zoology
Westfield College
University of London
London NW3 1ST EN8LAND
S. A. GAKEEN
Faculty of gr1cu1ture
University of Tanta
Cairo, EGYPT
ELiZABETH A. HAVES
University of British Columbia
Vancouver, B.C. V6T lW5 CANADA
EEVA !KONEN
University of Helsinki
Institute 0 f Zoology
Department Morphology and Ecology
P-Rautatlek 13
SF 00100 Helsinki, FINLAND
V. C. JOY
Department of Zoology
Visva Bharati University
Santlniketan, 731 235 INDIA
A. KAJAK
Polish Academy of Science
Institute of Ecology
Dziekanow Lesny near Warsaw
P.O. Lomianki, POLAND
878
-------
0. KEITh MCE. KEVAN
Macdonald College
McGill University
Ste. Anne of Beflevue
PQ H9X 1CO. CANADA
G. KILl V%EV1CTUS
Research Institute of’ Forestry
Vilnius, LITHUANIAN SSR
TAKASHZ KITAZAWA
Department of Biology
University of Occupational and
Environmental Health
Iselgaoka, Yahata Nishi—Ku
Kitalçyashu 807, JAPAN
.5. EL KRAVY
Faculty of Agriculture
University of Tanta
Cairo, EGYPT
GENICH! IGIRIKZ
Department of Btol og.y
Tohoku Dental University
Kohrlyama, JAPAN
SAl-HO I UAM
Department of Biology
The Chin2se University of Hong Kong
Shatin, HONG KONG
L. M. LALIKUL ICH
University of British Colwnbia
Vancouver, B.C. V6T 1W5
CANADA
(U. K. LAURENROTH
Natural Resource Ecology Laboratory
Colorado State University
Ft. Collins, Colorado 80523 USA
A. LUGAUSKA.S
InstItute of Botany
Academy of Sciences,
K. Pozelos 54
Vilnius 232600
LITHUANIAN SSR
.3. V. MAJER
Department of Biology
Institute of Technology
South Bentley, WA 6102
WESTERN AUSTRALIA
3. J. MILLER
Research Institute
Agriculture Canada
University Sub Post
London. Ontario NSA
G. PARMEHTIER
Department 0 f Botany
University of Liege
Sart Tilman 6—4000
Liege, BELGIUM
SMNISLALU PERLINSKI
Warsaw Agricultural
02— 526 Warsaw
Rakowlecka 26/30 POLAND
ASVEL-FA1TAH S.A. SMV
Faculty of Cotton Sciences
Heiwan University
Alexandria, EGYPT
T. 3. MCNARY
Natural Resource Ecology Laboratory
colorado State University
Ft. Collins, Colorado 80523 USA
M..3. MACI7ONAW
Department of Biological Sciences
University of Aston
Gosta Green, Birmingham 84 lET
ENGLAND
STANISLAW MAZUR
Warsaw Agricultural University
02-526 Warsaw
Rakowlecka 26/30 POLAND
Office
5B7 CANADA
University
13.3SF. PUGH
Department of Biological Sciences
University of Aston
Gosta Green, Birmingham
64 7ET ENGLAND
879
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ROGER SCMEFER
Laboratoire d’Ecologle Vegetale
University de Paris Xl
91400 Orsay FRANCE
U. R. SIN H
Laboratory of Ecophysiology and
Pedoecol ogy
V.S. Mehta College of Science
Bharwarl • All a ba bad - 212201
INDIA
SEPPO SIIIELA
Institute of Zoology
University of Helsinki
SF 00100 Helsinki FINLAND
LAWRENCE 8. SLO&)VKIH
Department of Biological Sciences
SUNY at Stony Brook
Stony Brook, NY 11790 USA
ThOMAS P. SMiTH
Departh*nt of Lands and Forests
P.O. Box 68
Truro, B2t1 588, Nova Scotia
CANADA
BOUBACAR SOW
Station d’Ecologle Tropicale de
Lainto
B.P. 28
N’Douci, IVORY COAST
VERONICA SUNII4AN
Institute of Zoology
University of Helsinki
SF 00100 Helsinki FINLAND
JAN SZYSZKO
Warsaw Agricultural University
02-526 Warsaw
Rakowlecka 26/30 POLAND
CHARLES E. TAYLOR
Natural and Agricultural Sciences
University of California-Riverside
Riverside, CA 92521 USA
&IENRYK TRACZ
Warsaw Agrir. j1tural University
02- 526 Warsaw
Rakowiecka 26/30 POLAND
N. TUPROS
Faculty of Agriculture
University of Tanta
Cairo, EGYPT
RICfIAIW 1. Veirtic
Department of Blologj, UNC 45
Utah State Ur iverslty
Logan, Utah 4322 USA
PEKKA V1LKAMAA
Institute of Zoology
University of Helsinki
SF 00100 Helsinki FINLAND
F. A. YISSER
Department of
Potchefstrooni
Potchefstroom
RE. S. AFRICA
S. VISSER
Department of Biology
The University of Calgary
Calgary, Alberta, T2N 1114
CANADA
TUULA WARTZOVAARA
Institute of Zoology
University of Helsinki
SF 00100 Helsinki, FINLAND
WALTER 0. WHTTFORV
Department of Biology
New Mexico State Univeilty
Las Cruces, M I 88003 USA
MIM-HWJG M
Department of Biology
The Chinese University of Hong Kong
Shatir., HONG KONG
J. ZAK
Department 0 f Biology
The University of Calgary
Calgary, Alberta, T2N 1114 CANADA
Zoology
University
2520
880
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!smpla A. OTS Document Clearancu Form
I. T0e SI Oocvmsnt No. sg RRfl
Soil Biology as Related to Land
Use Pract1ces:Procee fings of the
VII International_Colloquium of
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This report is the Proceedings of the VII International Soil Zoology Colloquium
of the International Society of soil Science, which was held in Syracuse, New
York (USA) on July 29 to August 3, 1979. Over 100 scIentists from 27 countries
participated jn the nine general sessions which covered several aspet.ts of soil
zoálogy dealing with the Interrelationships of soil systems and human activities.
Irciuded are the results of studies of the effects of mining, forestry, and
agr1cu tural operations on soil biological systems and the ability of soil
systems to detoxify a variety of human—generated chemicals and wastes.
$ I
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