&EPA
United States
Environmental Protection
Agency
Office of Pesticide Programs
Field Operations Division
Washington, D.C. 20460
August 1989
INTEGRATED PEST
MANAGEMENT FOR
TURFGRASS AND
ORNAMENTALS
Printed on Recycled Paper
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INTEGRATED PEST
MANAGEMENT FOR TURFGRASS
AND ORNAMENTALS
EDITORS
Anne R. Leslie
and
Robert L. Metcalf
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DISCLAIMER
The opinions, findings, conclusions and
recommendations expressed herein are those of
the authors and speakers and do not necessarily
reflect the opinions of the U.S. Environmental
Protection Agency.
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TABLE OF CONTENTS
Introduction v
Anne R. Leslie
Section I Problems Encountered in Controlling Pests with
Chemical Toxicants
1. Insect Resistance to Insecticides 3
Robert L. Metcalf
2. Ecological Side Effects of Pesticide and Fertilizer Use on Turfgrass 33
Daniel A. Potter, Stephen D. Cockfield and Terry Arnold Morris
3. Current and Future Regulatory Concerns for Lawn Care Operators 45
James F. Wilkinson
4. Societal Problems Associated with Pesticide Use in the Urban Sector 51
Anne R. Leslie
Section II Benefits of an Integrated Pest Management Approach to Turfgrass
and Ornamentals
5. Urban Integrated Pest Management Education and Implementation: Implications
for the Future 57
William Brown, Jr., W. Cranshaw and C. Rasmussen-Dykes
6. Educational, Environmental and Economic Impacts of Integrated Pest
Management Programs for Landscape Plants 77
Michael J. Raupp, Mildred F. Smith and John A. Davidson
7. Integrated Pest Management In the Golf Course Industry: A Case Study and
Some General Considerations 85
Zachary Grant
8. Societal Benefits of Conservation Oriented Management of TUrfgrass In
Home Lawns 93
Anne R. Leslie and William Knoop
9. Lawn Service Industry: Transition in Services 97
Roger Funk
Section III Current Research Towards Understanding the Pest and the Site
10. Detection and Monitoring of lurfgrass Pathogens by Immunoassay 109
S.A. Miller, G.D. Grothaus, F.P. Peterson, J.H. Rittenburg, K.A. Plumley, and R.K. Lankow
11. Biological Management of TUrfgrass Pests and the Use of Prediction Models
for More Accurate Pesticide Applications 121
J.M. Vargas, Jr., D. Roberts, T.K. Danneberger, M. Otto and R. Detweiler
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12. Managing the Scarab Grub Pest Complex In Turfgrass: Some Ecological
Considerations .................................... •• 127
Michael Villani and RJ. Wright
13. Influence of Fertilization and Irrigation Practices on Waterborne Nitrogen Losses
from lurfgrass ...................................... 143
A.J. Gold, W.M. Sullivan, and R.J. Hull
14. Surface Runoff from Turf ................................
M.S. Welterlen, C.M. Gross, J.S. Angle and R.L Hill
15. The Influence of TURFtech Seeding on Soil Compaction In Southeast Iowa
and a Mldsouth Region ................................. 161
Jim Schaefer and Larry Larson
Section IV State of the Art Research on Control of lurfgrass Pests Through
Use of Naturally Occurring Endophytic Fungi
1 6. The Role of Endophytic Fungi in Grasses: New Approaches to Biological
Control of Pests ..................................... 169
Malcolm R. Siegel, Douglas L Dahlman and Lowell P. Bush
17. Utilization of Fungal Endophytes of Grasses: Laboratory Manipulations for
Specific Toxins ...................................... 187
Charles Bacon
18. The Role of Endophytes In Enhancing the Performance of Grasses
Used for Conservation and Turf ............................ 203
C. R. Funk, B. B. Clarke, and J. M. Johnson-Cicalese
Section V State of the Art Research on Use of Entomophilic Nematodes for
Control of Turfgrass Insects
19. Field Effectiveness of Entomophilic Nematodes Neoaplectana and
Heterorhabditls 215
Ramon Georgis and George Poinar, Jr.
20. Entomogenous Nematodes for Control of lurfgrass Insects With Notes
on Other Biological Control Agents 227
David J. Shetlar
21. Biological Control of Social Insects with Nematodes 257
George O. Poinar, Jr. and Ramon Georgis
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Section VI Manual of Current Practices for Control of Turfgrass Diseases,
Insects and Poa Annua
22. Symptomatology and Management of Common lurfgrass Diseases In
Transition Zone and Northern Regions 273
Peter H. Dernoeden
23. Suppression of White Grubs with Microorganisms and Attractants 297
Michael Klein
24. Annual Bluegrass to Bentgrass Conversion with Turf Growth Retardants 307
Milton E. Kageyama and Larry R. Widell
Section VH Evaluation of the Site/Pest Complex: A Starting Point for
Development of an Urban Pest Management System for
Turfgrass
25. Development of an IPM Program for Turfgrass 315
Anne R. Leslie
26. Knowledge Based Systems for Use in Integrated Pest Management:
Requirements, Pitfalls, and Opportunities 319
Jan P. Nyrop, Bernie Huber and Walter Wolf
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IV
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INTRODUCTION
Anne R. Leslie
U.S. Environmental Protection Agency
Office of Pesticide Programs
Field Operations Division (H7506C)
401 M Street SW
Washington, DC 20460
This book is the product of a symposium held during the 194th American Chemical Society
meetings in New Orleans, Louisiana, in September 1987. Entitled "Urban Integrated Pest
Management: An Environmental Mandate", the symposium was sponsored by the Division of
Environmental Chemistry and co-listed by the Division of Chemical Health and Safety. The
symposium was a project of the Integrated Pest Management Unit (IPM Unit) of the United States
Environmental Protection Agency (EPA) to pull together the latest information on alternative controls
for urban pests. An important part of the IPM Unit's mission within the Office of Pesticide Programs
(OPP) has been development of demonstration projects and workshops for technology transfer to
private sector managers. Most of the non-chemical alternatives presented addressed turfgrass and
ornamentals, so this work focuses on turfgrass sites and includes relevant information on integrated
pest management for ornamentals.
Concerns related to the current pesticide practices for turfgrass include:
• increasing problems with resistance to pesticides, which have been documented for
insects, weeds and fungus diseases,
• attitudes of the general public about health effects to occupants when pesticides are
applied to home lawns,
• downstream effects based on the appearance of pesticides in ground and surface water
from agricultural uses.
It is time to evaluate these concerns; to state the evidence for adverse effects and the benefits
of maintaining healthy turf; and to present the best possible alternatives. We believe an integrated
pest management program can be devised that will promote a more sophisticated use of pesticides,
control turf pests and still maintain highest turfgrass quality. Such a program will preserve the useful
life of valuable pesticides, and provide cost savings for those who implement it.
A planned demonstration project based on this program should provide a comparison of the
results of several management methods and information on the extent of movement of pesticides
from turfgrass into groundwater and surface water. This information thus addresses EPA's concerns
that people must reduce pollution of all kinds at the source. Based on sound ecological principles
this program involves conservation of valuable resources.
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Different sites will have different pest problems and different maintenance requirements. For
example:
Home lawns: A healthy stand of the appropriate variety of grass, properly irrigated and fertilized,
will rarely require fungicide treatment, will have minimal insect damage, and will
have a weed population manageable without herbicides.
Golf courses: Because golfers' demands present special grass stress problems, superintendents
need to use fungicide treatments for certain areas to lower disease pressure when
weather conditions indicate potential problems. These chemicals must be applied
before disease is expressed to control certain diseases effectively. The current
practice is to apply fungicides to all vulnerable areas on a calendar basis.anticipating
disease outbreaks at certain times of the year, dependent on weather conditions.
Groundskeepers have experienced difficulties with disease control under this system because
of the toxic effects of fungicides on the turf and the buildup of resistance of disease organisms to
fungicides. If a disease is misdiagnosed, repeated treatment with the wrong chemical can be
disastrous to the turf.
An integrated pest management system advocates careful monitoring, and the chemical
industry, interested in proper application of their products, has now developed diagnostic kits that
are quick, simple to run and very accurate in predicting the outbreak of disease. Superintendents
are finding that they can rely on such products to identify the disease organism and to avoid
unnecessary treatments, thereby preserving the effectiveness of the chemicals. The savings in
treatment costs more than compensates for the cost of the kits, and the chemical industry still
benefits in the marketplace.
The public has expressed concerns about the emphasis placed on chemical control of turfgrass
pests by the professional lawn care operators and about homeowner use of the non-restricted
pesticides registered for turf. The Professional Lawn Care Association of America is concerned
about new State regulations on posting. A number of companies now offer alternative service
programs to their customers and give advice on proper cultural management. The acreage of urban
turfgrass has increased greatly in the last ten years, and the acreage under treatment by lawn care
companies has doubled (see the chapters by Raupp, Potter and Welterlen). We are encouraged
that the industry is taking steps to alter its practices, as shown in the chapters by Jim Wilkinson and
by Roger Funk.
Very few studies have been done to determine the downstream impact of the increased use
of pesticides on the growing urban area. Studies such as those reported by Welterlen take several
growing seasons to complete and can be very complex in design and costly to run. Research on
the impact of urban pesticides on water resources should be considered an important part of the
investigation carried out at land grant colleges as a part of their mission.
In summary, we believe that:
• the turfgrass industry in general can become more sophisticated in their pest control
programs and
• integrated pest management programs are designed to maximize proper use of
pesticides.
Unnecessary use of any chemical is of benefit to no one and is a waste of valuable resources
Our society can no longer afford to ignore such practices.
VI
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The monitoring methods, biological alternatives and cultural practices discussed in this book
will greatly benefit the golf course industry as well as the growing lawn care service industry by
providing information on a number of control methods and how to design the best program for their
needs.
We hope that this book will contribute to a greater understanding of best management practices
for turfgrass and will supplement turfgrass and landscape management courses. We hope that it
serves as a comprehensive source of information for anyone from city managers to homeowners
who wants to learn how to maintain healthy turf.
I acknowledge the gracious cooperation of my authors in providing their material under
sometimes very short deadlines. Especially I would like to acknowledge the expert work of Randy
Bacon, of EPA's print shop, who has made my work easy by his management of the text as it arrived.
Thanks are due to Charles Reese, Chief of the Certification and Training Office of OPP, who
offered to provide funding for the project because he saw the need for material on integrated pest
management in the training program.
I am especially indebted to Diana Home, Chief of EPA's Integrated Pest Management Unit,
who has enthusiastically supported this work through all the administrative travails of the project,
and to Joyce Herbert, who has provided exceptional clerical and secretarial service from the time
the symposium was first planned.
VII
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VIII
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SECTION I
Problems Encountered in
Controlling Pests with
Chemical Toxicants
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INSECT RESISTANCE TO INSECTICIDES
Robert L. Metcalf
Department of Entomology
University of Illinois
Urbana, IL61801
BRIEF HISTORY OF INSECTICIDE RESISTANCE
That insect pests acquire resistance or tolerance to insecticide action has been known for 73
years, since the description of lime-sulfur resistance in the San Jose scale Quadraspidiotus
perniciosus in California (Melander 1914). In 1916, resistance to hydrogen cyanide fumigant was
reported in the California red scale Aonidiella aurantii and in the black scale Saissetia oleae (Quayie
1922). The number of scientifically validated cases of insecticide resistance increased gradually
and by 1946 insecticide resistance was known in a total of 11 species including the codling moth
Cydia pomonella and the peach twig borer Anarsia iineatelia to lead arsenate, the citricola scale
Coccus pseudomagnoliarum to hydrogen cyanide, the citrus thrips Scirtothrips citri to potassium
antimonyl tartrate (tartar emetic), the walnut husk fly Rhagoletis completa to cryolite, and the cattle
ticks Boophiius microplus and EL decoloratus to sodium arsenite dip (Metcalf 1955). This evidence
suggested that the prognosis of the chemical control of insects was poor. However, little scientific
attention was given to insecticide resistance which is nothing more than accelerated microevolution.
Insecticide resistance began to receive the scientific attention that it deserved following the
introduction of DDT after World War II when resistant strains of the housefly Musca domestica
appeared almost simultaneously in Sweden and Denmark in 1946; of the mosquitoes Culex pipiens
in Italy and Aedes solicitans in Florida in 1947, of the bedbug Cimex lectularius in Hawaii in 1947,
and of the human body louse Pediculus humanus in Korea and Japan in 1951 (Brown and Pal 1971).
With the steady proliferation of new insecticides and their increasing use in insect control
programs, the number of scientifically documented cases of insecticide resistance has increased
at an exponential rate, encompassing 224 species in 1970, 364 in 1975, and 447 in 1984 (Table
1, Georghiou 1986). Although most early examples of insecticide resistance were found in insect
vectors of human diseases because of the very widespread use of DDT, lindane and dieldrin in
vector control programs, by 1970 insecticide resistance was demonstrated in 118 pests of
crop, forest, and stored products as compared with 166 pests of humans or animals (Brown 1971).
By 1980, resistance was established in 260 agricultural pests compared to 168 pests of humans
and animals (Georghiou, 1981). These figures probably understate the severity of the resistance
problem worldwide because the susceptibility of many insect pests species has not been studied,
is incompletely characterized, or is not reported adequately in the scientific literature.
Insecticide resistance has been documented in 16 orders of Arthropoda with the distribution
recorded by Georghiou (1981) as: Acarina, 53 (12.4%); Anoplura, 6 (1.4%); Coleoptera, 64 (14.9%);
Dermaptera 1 (0.2%); Diptera, 153 (36.7%); Ephemeroptera, 2 (0.5%); Hemiptera, 20 (4.7%);
Homoptera, 42 (9.8%); Hymenoptera, 3 (0.7%); Lepidoptera, 64 (14.9%); Mallophaga, 2 (0.5%);
Orthoptera, 3 (0.7%); Siphonaptera, 8 (1.9%); and Thysanoptera, 7 (1.6%). These data reflect the
relative numbers of pest species in the individual orders and the amount of insecticide pressure
placed upon them.
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As each new class of insecticides was introduced and widely deployed against insect pests,
the rate of development of resistant species has followed an almost identical pattern of essentially
exponential growth until high-level resistance or legal restrictions slowed further usage. These
curves are best characterized by the doubling times over the middle range. These can be
approximated by the data in Table 2, as DDT/methoxychlor 6.3 years, lindane/cyclodienes 5.0
years, organophosphates 4.0 years, carbamates 2.5 years, and pyrethroids 2 years. Thus these
data show that the doubling time for the development of numbers of resistant species has steadily
decreased with the introduction of each new type of insecticide. This is corroborated by the
decreasing spans of effectiveness of substitute insecticides to such pests as the Colorado potato
beetle Leptinotarsa decemlineata (Forgash 1984), the Agromyzidae leaf miner Liriomyza trifolii
(Parrella and Keil 1984), the citrus thrips (Morse and Brawner 1986) and the house fly (Keiding
1977) as illustrated in Tables 3 and 4. This accelerated development of multiple resistance is a
product of the persistence of R genes in the species genome and of their interactions through a
variety of resistance mechanisms that affect both the detoxication of and the target-site sensitivity
to various insecticides.
RESISTANCE AS AN EVOLUTIONARY PHENOMENON
Insecticide resistance is dependent upon random mutation that establishes an R-allele in the
natural population of the species. Widespread application of the insecticide propagates the R-allele
through preferential survival and it is dispersed throughout the population. As the R-allele becomes
sufficiently common, the effectiveness of the insecticide is reduced. Where the R-allele is partially
dominant, RR homozygotes are rapidly selected that are completely resistant. With recessive alleles
or combinations of genes each conferring low-level resistance, selection is much slower (Sutherst
and Comins 1979).
There is surprisingly little data about the natural frequency of resistance alleles. These are
thought to be present in typical insect populations at frequencies of 10'4 to 10~2 with RR homozygotes
present at 10~8 to 10"4 (Georghiou and Taylor 1986). The most carefully studied example is that of
Anopheles gambiae in West Africa (Hamon and Garrett-Jones 1963). In this vast region, dieldrin
was used as the primary insecticide for WHO malaria eradication programs because of its
persistence on the mud surfaces of dwellings. Initially dieldrin was very effective against A. gambiae
adults with LC50 values as low as 0.02 -0.07% based on a 1 hour exposure to treated filter papers
as producing 24-hour mortality (Armstrong 1958). The corresponding value for DDT was 0.6%.
Dieldrin spraying began in 1954 and dieldrin-resistance was first observed in the Sokoto
Province of northern Nigeria that had been sprayed 3 times over 18 months. Within 2 months after
spraying, large numbers of A, gambiae were observed resting, unaffected upon treated walls and
the LC50 was 2.0% dieldrin (Armstrong et al. 1958). Laboratory colonization produced a RR strain
that was unaffected by 4.0% dieldrin test papers and had resistance-ratios of 800 for dieldrin, 400
for aldrin, 140 for isodrin, 90 for endrin, and 26 for lindane, but no resistance to DDT (Brown and
Pal, 1971). Crossing the R-Ambursa strain with a S-Lagos strain produced RS heterozygotes exactly
intermediate in resistance and the RS, and RR alleles could be distinguished in field populations
by exposure to standard WHO test papers, of 0.4% and 4.0% for 1 hour. By this technique, it was
shown that resistant heterozygotes formed 0.04% of the wild unsprayed A, gambiae ara'biensis
population in Diggi and 6.0% in Sokoto (Armstrong et al. 1958). A single large scale treatment of
lindane (HCH) produced a population of 86% RS and RR genotypes. In Upper Volta in an area
near Bobo-Dioulasso which had been sprayed 4 times with dieldrin, there was 100% RR genotype
No mortality was produced by exposure to 4.0% dieldrin papers, as compared to an LC50 of 0.03%
'o
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in an unsprayed village 40 km. away (Brown and Pal 1971). Areas where A gambiae had high
frequencies of RS and RR genotypes have appeared in Ivory Coast, Ghana, Togo, Dahomey and
Cameroon (Hamon and Garrett-Jones 1963). Surveys have shown 91-100% RR homozygotes in
Liberia, Dahomey, Cameroon.and Republic of Congo. There is evidence that increases in the
frequency of R alleles may be related to the heavy use of dieldrin and lindane on agricultural crops
such as cotton and peanuts. The dieldrin resistant mosquitoes have sporozoite indices as high as
neighboring susceptible populations and dieldrin resistant strains have been found to be larger,
longer-lived, and more stress-resistant than susceptible strains (Davidson 1956,1958; Hamon and
Garrett-Jones 1963). Thus the failure of dieldrin residual spraying has always resulted in the
resumption of malaria transmission.
RESISTANCE MECHANISMS
A. Cross Resistance. This is the most common form of insecticide resistance where a single
detoxication process or an aberrant intoxication process reduces the susceptibility of resistant
alleles of an insect pest species to a chemically related family of insecticides. Cross resistance has
been demonstrated in naturally occurring arthropod populations to discrete groups of insecticides
classified in order of historical appearances as I DDT/methoxychlor, II lindane/cyclodienes, III
organophosphates, IV carbamates, and V pyrethroids. As shown in Table 1, many insect pest
species have successively acquired resistance to these various classes of insecticides. In general,
races of insects resistant to one insecticide in a class exhibit a spectrum of abnormal responses to
all the other members of the class as dictated by their individual stereochemical peculiarities.
B. Multiple Resistance is defined as resistance extending to a variety of classes of pesticides,
unrelated to one another chemically. The mechanisms typically involve target site insensitivity e.g.,
the kdr mechanism that shows reduced sensitivity of the nerve axon to DDT as well as to the
chemically unrelated pyrethroids; and the altered acetyicholinesterase mechanism where both
organophosphates and carbamates fail to react with the modified catalytic site of the enzyme due
to a structural modification that restricts access of the chemical inhibitor. Multiple resistance is now
present in at least 213 arthropod species from 10 orders and 44 families (Table 1). Thus almost
half of all the documented cases of arthropod resistance to insecticides comprise resistance to
several chemically unrelated classes of insecticides: I DDT/methoxychlor, II lindane/cyclodienes, III
organophosphates, IV carbamates, and V pyrethroids. By 1987, at least 19 arthropod pest species
are resistant to all 5 classes of insecticides as identified in Table 5.
This extensive and ever widening pool of species with multiple-resistant genes is the product of the
historical replacement of insecticide as resistance developed, by insecticides of different chemical
types and modes of action. Each new insecticide produces a selection for one or more mechanisms
of resistance and each mechanism selected produces a spectrum of cross-resistance to closely
related insecticides. Thus the sequential use of alternative compounds has led to widespread
multiple resistance and the continued selection pressure favors the retention of resistant genes to
discontinued insecticides. Therefore the presence of alleles for multiple resistance in a pest
population reflects the past history of insecticide use and precludes a return to insecticides
previously used. The devastating effects of cross-resistance and multiple resistance to control
programs for the Colorado potato beetle attacking potatoes and the house fly in Denmark are shown
by the sequences of resistance development portrayed in Tables 3 and 4. Similar portrayals of the
development of multiple resistance have occurred with the serpentine leaf miner and the German
cockroach (Section V-C).
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The past history of selection for resistance may result in an accumulation of mechanisms for
resistance that confer multiple resistance across the various classes of insecticides. For example,
an esterase in the housefly (E.O. 33) selected by exposure to the organophosphate malathion and
trichlorfon confers moderate resistance to the pyrethroids as well (Sawicki et al 1984). However, in
houseflies with the kdr mechanism for resistance selected by exposure to DDT, subsequent
exposure to the pyrethroids resulted in intensification of both the kdr and esterase mechanisms
leading to total immunity to deltamethrin (LD50 greater than 20 ug per fly) (Sawicki et al 1986). Thus
a history of sequential use of DDT followed by OP's produced a genetic history of multiple resistance
that contributed to the rapid failure of a third group of insecticides, the pyrethroids. There is,
therefore, valid concern that the effective lifetime of the pyrethroids may be shorter in developing
countries where their use directly succeeded that of DDT than it will be in developed countries
where the sequence after DDT involved several years of use of OP's and carbamates (Georghiou
1986).
C. Genetic and Biochemical Processes of Insecticide Resistance.
A number of increasingly more generalized mechanisms for insecticide resistance have been
identified in terms of specific genetic control (Plapp 1986). Most of these studies have been made
with the housefly but the types of resistance have been identified in many other insects and there
is little reason to question their generality.
Metabolic resistance involves detoxication of the insecticides by a variety of enzymatic
processes including esterases, mixed function oxidases, glutathione transferases, and
epoxyhydrolases. Genes on chromosome II are the controlling factor and this may be a common
codominant resistance gene controlling a variety of detoxifying enzymes (Plapp 1986). Metabolic
resistance involves DDT, OP's, carbamates, and juvenoids and the specific detoxication enzymes
are typically inhibited by synergists that may act to restore the effectiveness of the pesticide.
Examples include (a) the DDT'ase inhibitor 1,1-bis-(p_-chlorophenyl)-ethanol (chlorfenethol) for
DDT; (b) Q-ethyl, Q-(p-nitrophenyl) phenylphosphonate (EPN-oxon) a carboxyesterase inhibitor for
malathion, (c) S, S, S-tributyl phosphorotrithioate (DEF) for esterases hydrolyzing OP's; and (d)
piperonyl butoxide for mixed function oxidases detoxifying carbamates and pyrethroids.
Kdr or knockdown resistance involves a modification of the target sites for DDT and the
pyrethroids on the nerve axon and is controlled by a gene on chromosome III. The kdr resistance
mechanism confers multiple resistance to all DDT analogues and pyrethroids. Both low level (kdr)
and high level super kdr alleles have been studied.
Dld-r or dieldrin resistance involves another modification of the target site on the nerve axon
and is controlled by an incompletely recessive gene on chromosome IV.
AChE-R or altered acetylcholinesterase involves a change in the biochemical action of the
nerve synaptic regulator acetylcholinesterase that is the target site for OP's and carbamates. The
codominant gene is located on chromosome II and confers multiple resistance to organophosphorus
and carbamate insecticides.
Pen is a resistance mechanism involving decreased penetration of insecticides and is
controlled by a recessive gene on chromosome III. This type of resistance can act in concert with
other resistance genes to further increase resistance levels.
1. DDT'ase. Resistance resulting from the selection of alleles that produce high levels of a
specific enzyme that catalyzes the dehydrochlorination of DDT to the non-insecticidal DDE was
very intensively studied during the 1950's when the insect resistance picture was relatively unique
and simplistic remedies were sought. The enzyme is DDT-dehydrochlorinase or "DDT'ase",and its
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high litre produces DDT resistance in the housefly, in the yellow-fever mosquito Aedes aegypti, the
pest mosquitos Culex fatigans. the malaria vectors Anopheles saccharovi, and A^ subpictus. the
human body louse Pediculus humanus. the triatomid bug Triatoma infestans. the Mexican bean
beetle Epilachne varivestis. the red-banded leafroller Argyrotaenia velutinana. the pink bollworm
Pectinophora gossypiella. and the cotton bollworm Heliothis virescens.
DDTase isolated from DDT-resistant flies (Sternburg et al 1954) appears to be a lipoprotein with a
molecular weight of about 120,000 daltons and consists of 4 subunits. Glutathione is required as a
cofactor for DDT'ase activity (Lipke and Kearns 1960; Dinamarca et al. 1969, 1971). DDT'ase
activity is present in the susceptible (S) housefly to only about 0.03 to 0.3% of that in highly resistant
strains (R), and the level of resistance in houseflies where this mechanisms is present is roughly
correlated with the resistance ratio or RR (LD50R/LD50S) (Lipke and Kearns 1960; Oppenoorth and
Welling 1976; Oppenoorth 1984).
DDT'ase functions by attacking the alpha-H of the DDT molecule in a manner similar to
OH-catalyzed dehydrochlorination, producing an E2-type elimination reaction and the expulsion of
Cl-leading to the formation of DDE or 2,2-bis-(p-chlorophenyl)-1,1-dichloroethylene (Figure 1)
(Metcalfand Fukuto 1968). The rates of reaction of various DDT analogues with DDT'ase are similar
to the OH-catalyzed dehydrochlorination constants and are controlled by the relative availability of
electrons at the H-C bond (alpha carbon) as determined by the polar effects of the p_,p_'-substituents
on the aryl rings. Thus DDT'ase attacks methoxychlor with p,p'-CH3O groups (electron-donating)
at a rate only about 0.2 that of the attack on DDT with p,p_'-CI groups (electron-withdrawing) (Lipke
and Kearns, 1960). The rates of dehydrochlorination by DDT'ase are also dependent upon the
electronic properties of the substituents on the beta carbon, and 2,2-bis-(p_-chlorophenyI)-1,1,1-
tribromoethane is attacked about 4X more readily than DDT. The analogue DDD or 2,2-bis-(p_-
chlorophenyl)-2,2-dichloroethane is attacked about 3.8X more readily than DDT, and the
dibromo-analogue of DDD or 2,2-bis(p-chlorophenyl)-2,2-dibromoethane about 4.6X more readily
than DDD (Berger and Young 1962).
2. DDT'ase Inhibitors as DDT Synergists. Dramatic demonstration of the role of DDT'ase in
DDT resistance has been provided by discovery that certain structural analogues of DDT, although
insecticidally ineffective, could synergize the toxicity of DDT to highly resistant strains of houseflies.
Chlorfenethol or 1,1-bis-(p_-chlorophenol)-ethanol was found by Summerford et al. (1951) to have
asynergistic ratio (SR) or LD^ DDT alone/LD^ DDT plus synergist of 60. Chlorfenethol was shown
to inhibit the in vivo detoxication of DDT to DDE in R flies and when a range of 0.06 to 6.5u9was
applied topically together with a constant amount of 0.65U9 of DDT, the mortality was increased from
2 to 100%, the amount of DDT recovered internally was increased from 9.4 to 77%, and the amount
of DDE formed was decreased from 63 to 12% (Perry et al 1953). Chlorfenethol proved to be an
effective in vivo inhibitor of DDT'ase at a molar ratio of 0.001 that of DDT (Lipke and Kearns 1960).
Many other structural analogues of DDT are synergists for R flies, and synergistic ratios (SR values)
determined for the R super pollard housefly are: 1,1-bis-(p_-chlorophenyl)-ethane SR 100,
bis-(a-chlorophenyl)-chloromethane SR 140, and 1,1-bis-(p_-chlorophenyl)-2,2,2-trifluoroethanol
SR 78-127 (March et al 1952; Metcalf, 1967). The high activity of p_-chlorobenzenesulfon-p_-
chloroanilide SR 108 was described by Speroni (1952) and emphasized the structural similarity of
such compounds to DDT. This led to the development of p_-chlorobenzene-N,N-dibutylsulfonamide
as an oil soluble synergist for DDT (Neeman et al. 1957).
These DDT-synergists clearly fit the active site of the DDT'ase enzyme and act as competitive or
in some cases as irreversible inhibitors thus blocking the dehydrochlorination of DDT. The DDT
synergists such as Chlorfenethol, 1,1-bis-(p-chlorphenyl)-chloromethane, and 1,1-bis-(p-chlorophenyl)-
ethane were used successfully in field experiments to control DDT-resistant houseflies (March et
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al. 1952). However, the DDT-synergist combinations had only temporary effectiveness in housefly
control and eventually treated populations developed "super resistance" to the DDT-synergist
combination (March et al. 1952). The widespread development of an alternative DDT-resistance
mechanism in the housefly, the kdr nerve axon insensitivity which was not responsive to synergistic
action (Oppenoorth and Welling 1976), emphasized the inadequacy of the synergist approach.
3. "Resistance Proof" DDT Analogues. The relatively greater effectiveness of methoxychlor
to DDT resistant houseflies with high DDT'ase activity and the spectrum of activity of DDT'ase
toward a variety of DDT analogues suggested that analogues in which dehydrochlorination was
hindered or blocked might be effective insecticides for DDT-resistant insects. This requirement
posed a nice problem in finding DDT-analogues which had the proper stereochemical configuration
to be active intoxicants but were not DDT'ase substrates. Four distinct mechanisms for "resistance
proofing" of the DDT-type molecule have been identified (Metcalf and Fukuto 1968):
a. Changing the bond strength at the alpha-carbon to substitute alpha-D or alpha-F for
alpha-H. The deuterium isotope effect in OH-catalyzed dehydro-chlorination is 6.8. The
alpha-C-F bond cannot be attacked by DDT'ase.
b. Steric hinderance to interaction with DDT'ase by introduction of an ortho-group of proper
size as in p_-CI-DDT. This reduces OH- catalyzed dehydrochlorination to 0.17.
c. Changing the bond character of the chloromethyl moiety as in 1,1 -bis-(p-chlorophenyl)-2,2-
dichlorocyclopropane.
d. Total replacement of aliphatic halogens by CH3 as in the neopentanes or isobutanes or
by CH3 and NO2 as in the nitropropanes (Coats et al 1977). Examples of the effects of
these changes in the DDT molecule on toxicity to the susceptible and DDT-resistant
housefly are shown in Fig. 1.
Several of these "resistance proof "DDT analogues have had serious consideration for practical
use. DDT-resistant larvae disrupted the Aedes aegypti eradication program in the United States
(Section VI-A). The DDT'ase of Aedes aegypti differs from that of the housefly in effectively
dehydrochlorinating o-chloro-DDT but not alpha-deutero-DDT (Kimura and Brown 1964).
Therefore the use of alpha-deutero-DDT which dehydrochlorinates at a rate of about 0.14 that
of DDT was proposed as a substitute in the eradication program. The relative LC50 values for
aipha-deutero DDT and DDT to S- and R- Aedes aegypti larvae were (Pilai et al. 1963):
DDT
deutero-DDT
S 0.012 ppm
R 31.0 ppm
0.004 ppm
0.40 ppm
However, the substitution of alpha-deutero-DDT at $10 per Ib. for DDT at $0.20 per Ib. posed
an unacceptable reduction in the cost effectiveness of the eradication program.
8
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4. Kgr resistance factor. A totally different mechanism of DDT resistance,the knockdown
resistance or kdr mechanism was first identified in the housefly in 1951 (Winteringham et al. 1951).
The kdr mechanism is a target site insensitivity of the nerve axon and evidence for it is obtained
largely by electrophysiological measurements of nerve physiology together with the absence of
DDT'ase, the inactivity of DDT-synergists (Georghiou 1980) and kdr resistance to DDT analogs
that cannot be dehydrochlorinated (Coats et al 1977). The development of kdr is controlled by a
gene on Crlll and is recessive. Kdr is widespread in the housefly in northern Europe and was found
in practically all populations in Denmark (Keiding 1977). Kdr has been identified in a variety of
mosquito species: Culex fatigans. (X tarsalis, Aedes aegypti. Anopheles albimanus. ^ gambiae.
Ai quadrimaculatus. A^ saccharovi. ^ Stephens!, in the stable fly Stomoxys calcitrans. the horn fly
Haemotobia irritans and the cattle tick EL microplus. Kdr is also found in a variety of armyworms
and bollworms including Spodoptera exigua. a frugiperda. ^ littoralis. and Heliothis armigera(Miller
etal. 1983).
The pyrethroids act at the same general target site in the insect nerve axon as DDT, and the
introduction of residual pyrethroids in Denmark, Switzerland, Germany, and England was followed
by development of high levels of pyrethroid resistance in the housefly within a few months (Keiding
1980; Keiding 1986; Chapman and Lloyd 1981). In contrast, kdr is rare in Japan and pyrethroid
resistance in the housefly did not develop until after 6 years of residual pyrethroid use (Motoyama
1984).
The influence of kdr on multiple resistance of DDT and pyrethroids was demonstrated by the very
rapid emergence of pyrethroids resistance in the horn fly, Haematobia irritans. following the use of
ear tags containing permethrin and fenvalerate on cattle throughout the U.S. DDT has been used
extensively to control the horn fly during the 1950's and resistance appeared about 1960. The
pyrethroid-containing ear tags were introduced in 1980 and within 2 to 3 years widespread
resistance was evident (Quisenberry et al. 1984, Sparks et al. 1985). This resistance resulted from
genetic selection for the kdr mechanism (Roush et al. 1986) that resulted in cross-resistance to
cypermethrin, fenvalerate, permethrin, deltamethrin, and flucythrinate (Byford etal. 1985).
5. Altered AChE resistance factor. The enzyme acetylcholinesterase (AChE) is the target site
of the entire groups of organophosphate and carbamate insecticides which number in the hundreds.
Resistance to these insecticides resulting from a decreased sensitivity of AChE was first identified
in the mite Tetranychus urticae (Smissaert 1964). The development of altered AChE is controlled
by a gene on Crll that is codominant, and has been identified in the mites T. telarius. T. kanzawai.
Typhlodromus pyri. Aphis citricola. the green rice leafhopper Nephotettix cincticeps. the housefly,
the mosquitoes Anopheles albimanus and Culex pipiens. the cattle tick Boophilus microplus, and
the cotton leafworm Spodoptera littoralis (Nolan et al. 1972; Yamamoto et al. 1983; Raymond et al.
1986). Kinetic analyses of the enzymes of S and R races have shown a decrease of about 200-fold
in the bimolecular rate constant ki for the inhibition of housefly AChE by tetrachlorvinphos (Tripathi
and O'Brien 1978) and of about 500-fold for the enzyme in the green rice leafhopper by
ntsee-butylphenyl N-methylcarbamate (Yamamoto et al. 1983). The phosphorylation or carbamylation
constants, k,, were not appreciably altered but the affinity constants Ka were reduced by 300-500
fold; indicating structural alterations in the stereochemistry of the active sites of both fly and
leafhopper AChE, hence the term "altered AChE." In contrast, for both altered enzymes there was
only a 2-3 fold difference in the affinity of ACh for the altered enzyme (Yamamoto et al. 1983). The
altered AChE resistance is particularly destructive to insecticide resources as its appearance results
in wholesale loss of effectiveness of the large groups of OP and carbamate insecticides.
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PERSISTENCE OF GENES FOR PESTICIDE RESISTANCE
Once selected for, resistance genes have very lengthy persistence in wild insect populations.
Although gene frequency of a specific resistance allele may decrease upon removal of insecticide
pressure, the persistence of an apparently changed background of residual inheritance in the
genome causes the strain to regain its resistance as soon as the insecticide is reapplied (Brown
1977). Genes for DDT and cyclodiene resistance in Danish houseflies have persisted for more than
20 years; these insecticides again became ineffective within 2 months after reapplication of the
insecticides. Genes for resistance to diazinon and dimethoate also have shown long persistence
(Keiding 1977). The citrus thrips, Scirtothrips citri has retained its resistance to tartar emetic for
more than 45 years and to DDT for more than 35 years (Morse and Brawner 1986). Multiple
resistance in the cotton leafworm in Egypt showed no signs of regression over an 11-year period
(El-Sebae 1977). There also appears to be no sign of regression of resistance in the multiple
resistance patterns of the Colorado potato beetle (Table 3) and the house fly (Table 4) over periods
of as much as 30 years.
These unpleasant consequences of the segregation of R-genes are predictable from the
Hardy-Weinberg equilibrium which predicts that gene frequencies and genotype ratios in large
biparental populations reach an equilibrium in one generation and remain constant thereafter unless
disturbed by natural selection, new mutations, or genetic drift. This factor, therefore, prevents the
successful long-term reuse of any insecticide in insect populations with resistance alleles, even
though the initial resistance has apparently reverted to full susceptibility (Brown 1971; Georghiou
and Taylor 1976; Keiding 1979).
10
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IMPACT OF INSECT RESISTANCE TO INSECTICIDES UPON PEST
CONTROL
The onslaught of cross and multiple resistance has greatly complicated the chemical control
of individual insect pests (Georghiou, 1981) and jeopardized highly structured eradication programs.
A few examples will suffice to illustrate the severity of the problems.
A. Colorado Potato Beetle, Leptinotarsa decemlineata. This native American insect is the key
pest of the Irish potato and fed on buffalo burr, Solanum rostratum until about 1859 when it was
found attacking the potato SL tuberosum in eastern Nebraska. The beetle rapidly accommodated
to this new host and migrated eastward until it reached the Atlantic Coast in 1874 (Casagrande
1987). Paris green or copper acetoarsenite was found to control this insect in 1865 and was replaced
by lead arsenate as the standard remedy until the introduction of DDT in 1946. Resistance to DDT
developed in New York in 1949, North Dakota in 1952 and Minnesota in 1959. The beetle was
introduced into Europe after World War I and has become a major pest of potatoes there and
resistant genes are now ubiquitous. Subsequently resistance has developed to lindane and the
cyclodienes, to a wide variety of OP's, carbamates, and pyrethroids. Since 1945, at least 12
insecticides have been used on Long Island to control this insect and, as shown in Table 3, all of
them have failed due to the onset of multiple resistance (Forgash 1981). This accumulation of
resistance genes has progressively decreased the interval of effectiveness so that since 1973 no
insecticide has remained effective for more than 2 years. In the words of Forgash (1984) "the fact
is we are rapidly running out of control materials for the Colorado potato beetle in certain areas of
the Northeast....where do we go from here?"
B. Serpentine leaf miner, Liriomyza trifolii. This insect was a minor pest of ornamentals,
vegetables, and cut flowers until the use of the broad spectrum insecticides chlordane and
toxaphene in Florida destroyed its natural enemies and resulted in huge population resurgences,
following the development of resistance about 1957. Since 1975, no insecticide has given effective
control for more than 2-4 years and there is widespread multiple resistance to the cyclodienes,
OP's, carbamates, and pyrethroids. Subsequently, the resistant race was imported into California
(Parrella and Keil 1984), and pest control costs have risen to $6,000 per acre. By 1984, as all
registered insecticides were ineffective, the leafminer problem "had become so serious that it has
threatened the chrysanthemum industry throughout the United States and the celery industry in
Florida"(Parrella and Keil, 1984).
C. German cockroach, Blattella germanica. is the most ubiquitous of urban pests and is
responsible for the great majority of requests for the services of professional pest control operators
(PCO's) as well as for the preponderance of insecticide applications to the interiors of urban and
suburban structures (National Academy of Sciences 1980). Although other species of domestic
cockroaches are household pests including the oriental cockroach Blatta orientalis. the American
cockroach Periplaneta americana. the smoky brown cockroach P. fuligenosa. the Australian
cockroach P.. australasiae and the brown banded cockroach Supella longipalpa: the enormous
populations of the German cockroach and its almost universal exposure to insecticides have brought
about the most acute problems of insecticide resistance.
The German cockroach was initially of only moderate susceptibility to DDT (topical LD50 ca 50 ug
per g, Heal 1953). True DDT resistance was first demonstrated in Trinidad and Panama in 1959,
and in Canada, Germany, France, and England in 1961 (Grayson 1966). Laboratory colonies have
shown DDT resistance ratios (RR values) as high as 200X (Grayson 1953). Chlordane (topical
LD-Q ca 20 ug per g), (Heal et al. 1953), was substantially more effective than DDT and became the
insecticide of choice for cockroach control from 1948-1952 (Kearns et al. 1948). However, a strain
11
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of EL germanica collected in Corpus Christi, Texas in 1952, where control failures with chlprdane
had been experienced, was found to have RR values of 5-6 for DDT, 10-12 for lindane, and 100-200
for chlordane (Heal et al. 1953). By 1953, chlordane resistance had appeared generally in the Gulf
States of the U.S. and sporadically elsewhere and diazinon and malathion were recommended as
substitute insecticides. Cyclodiene resistance was demonstrated in Europe by 1961 and RR values
of 5,000 to chlordane and 6,000 to dieldrin were reported (Green et al. 1961). Chlordane resistant
EL germanica were cross resistant to heptachlor, aldrin, dieldrin, and lindane (Fisk and Isert 1953;
Butts and Davidson 1955) and a strain collected from Hawaii showed RR value for females of
chlordane 322X, dieldrin 194X, lindane 27X, DDT 6X, malathion 8X, naled 3X, and the carbamate
propoxurSX (Ishii and Sherman 1965).
Resistance to diazinon was demonstrated in roaches collected near Owensboro, Kentucky in 1959
(Grayson 1961) and resistance to malathion had apparently appeared by 1959-1960 and was
conclusively demonstrated in 1962 (Johnston et al 1964). Cross resistance among diazinon,
malathion, and fenthion was widespread in major Texas cities by 1964 (Grayson 1965).
Pyethrins resistance at RR levels up to 20-31X was found in a strain of EL germanica collected at
Fort Rucker, Alabama in 1954 (Keller et al. 1956) and three strains collected in Texas in 1963 had
RR values of 10-15X (Grayson 1966).
Resistance to the carbamate bendiocarb appeared in England in 1977 (Barson and McCleyne 1978)
and the roaches were cross resistant to dioxacarb and showed resistance to diazinon, and
malathion, with weak resistance to permethrin (Barson and Renn 1983). A strain of the German
cockroach from Baltimore, Maryland was highly resistant to bendiocarb (RR 90X) and had cross
resistance to propoxur (RR 13X) and resistance to diazinon (4X), malathion (6X), and chlordane
(8X) (Nelson and Wood 1982). German roaches with kdr type resistance to DDT were found to
have resistance to pyrethrins, allethrin, permethrin, fenvalerate, and marginal resistance to
cypermethrin, but none to deltamethrin.
Chlordane resistance in JL germanica has been shown to be stable over 25 generations of
non-exposure and malathion resistance for 13 generations (Grayson 1966). A major consequence
of the widespread multiple resistance in this species has been the introduction of more acutely toxic
OP compounds into human dwellings and the workplace, e.g., the replacement of malathion (rat
oral LD501250 mg per kg) by chlorpyrifos (rat LD50 97) and propetamphos (rat LD50 82).
IMPACT OF RESISTANCE ON VECTOR CONTROL AND
ERADICATION PROGRAMS
The development of DDT and its successful initial uses in controlling the mosquito, louse, and
flea vectors of such dreaded human diseases as malaria, yellow fever, typhus, and plague afforded
remarkable visions of mass public health programs for the abatement and eventual eradication of
these and other vector-borne diseases throughout the world. DDT was safe to humans even when
applied in the intimacy of dwellings, inexpensive and highly persistent in its effectiveness in all sorts
of environmental situations. Thus it was possible to secure financing for major public health
programs that naively promised eradication of disease vectors by the domestic application of DDT
over periods of only a few years. The projected costs of such programs although reckoned in tens
to hundreds of millions of dollars, have proved in retrospect to have been grossly underestimated
and the eventual magnitude of the operations was such that the original goals have been lost and
"eradication" has quietly slipped into oblivion. Vector resistance to DDT and to subsequently
12
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developed cheap and durable insecticides such as lindane and dieldrin has been the principal
technical problem leading to steadily worsening control failures.
DDT resistance appeared in the housefly Musca domestica and in Culex molestus in Italy in
1947, in the human body louse Pediculus humanus in Korea and in Anopheles saccharovi in Greece
in 1955, and in the oriental rat flea in India in 1959. The rapidly increasing number of vector species
for which insecticide resistance was suspected as the cause of control failures are shown as
(Quarterman and Schoof 1958).
1946
1
1947
3
1948
6
1949
12
1950
19
1951
23
1952
26
1953
29
1954
33
1955
37
However, these abundant warning signs were virtually ignored in planning and operating vector
eradication programs with the result that monumental failures have resulted as shown in the
following examples. The ultimate failures of these programs represent an enormous disaster to the
cause of global public health and are the most extravagant economic tolls yet levied by insect
resistance.
A. Aedes aegypti eradication. This domesticated mosquito, the urban vector of yellow fever
and dengue fever, was introduced into the Americas from its native home in Africa before the 16th
century. For hundreds of years, the presence of Ae. aegypti was responsible for devastating
outbreaks of yellow fever in seaports throughout the Americas. By 1930, the mosquito was present
in 19 countries and ranged from Oklahoma and Tennessee in the United States to Buenos Aires
in Argentina and Tecopila in Chile (Gratz 1973). Ae. aegypti is the vector of the several serotypes
of dengue fever virus and the number of reported cases in the Americas reached 503,000 in 1977
and 354,000 in 1982 (Tonn et al. 1982).
The concept of a hemispheric eradication program for Aedes aegypti was first proposed by the 11th
Pan America Sanitary Conference in Rio de Janeiro in 1942, and by 1947, the Pan American Health
Organization (PAHO) officially embarked in the eradication of the mosquito as the solution to the
urban yellow fever problem. By 1960, the United States was the only country in the mainland
Americas that had not initiated an Aedes aegypti eradication program. Strong political pressures
resulted in a Congressional appropriation of $3 million in 1963 for operations the succeeding year.
The major weapon relied upon was the "perifocaP'application of DDT water dispersible suspension
in and around all potential breeding places of the mosquito and to any adjacent wall surfaces within
a radius of about one meter (Gratz 1973).
The eradication effort was thus essentially doomed because DDT-resistance had been
characterized in Aedes aegypti in Trinidad as early as 1950 (Brown and Pal 1971), and a survey
of the mosquitoes' susceptibility throughout 16 countries of the Americas had shown that by 1964
no populations could be found that were susceptible to either DDT or dieldrin (Kerr et al. 1964).
Initial control failures in the U.S. demonstrated that it would be necessary to replace the relatively
cheap organochlorines with more costly and less persistent organophosphorus insecticides and
these economic dislocations resulted in the quiet demise of the eradication program in 1968 after
the expenditure of $54 million. A PAHO report in 1970 estimated that it would cost an additional
$250 million and require another 5 years to eradicate Ae, aegypti from the U.S (Gratz 1973).
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Presently A. aegypti is known to have multiple resistance to DDT, cyclodienes, OP's and pyrethroids
(Georghiou 1981), and it seems most unlikely that eradication can be accomplished by chemical
applications.
B. Malaria Eradication. The onset of insecticide resistance has produced its most deleterious
effects in the control of malaria. Malaria has long been called the king of diseases and before the
advent of DDT annually caused about 300 million illnesses and 3 million deaths. During World War
II, the persistence and efficiency of DDT residual sprays against a variety of mosquito species
entering human habitations suggested that yearly spraying of all dwellings in malarious areas could
eliminate the disease by killing female Anopheles mosquitoes over the 10-14 day period required
for infective sporozoites to develop in the mosquito's body following the ingestion of male and
female gametocytes from a human blood meal. Application of this control measure directed at the
vector Anopheles labranchiae in Italy in 1944 reduced the number of primary cases of malaria from
4800 in 1946 to 81 in 1949 and malaria was considered eradicated in 1950 (Missiroli 1950). A similar
program in Sardinia using DDT spraying at 2 g per m2 on the interior walls of houses eradicated
malaria in 1951 (Logan 1953). In India 3-4 years of DDT residual spraying against the vectors ATL
culicifacies and An. fluviatilis reduced the parasite rate to less than 0.05% of its former level and
by 1954 at least 64 million inhabitants were under protection of DDT spraying. These and successes
in other parts of the world set the stage for the 1955 World Health Organization's program for the
global eradication of malaria to be accomplished by residual house spraying with DDT at 2g per
m2 or with dieldrin at 0.6 g per m2. It was planned that 8 years of continuous operations would be
required for eradication in each national program and the entire global eradication was estimated
to cost $1.3 billion (Brown et al. 1976; Soper et al. 1961).
DDT resistance was first observed in An. saccharovi in Greece in 1950 and was followed by dieldrin
resistance in 1954. The onset of resistance was marked by a deterioration in malaria control that
has continued for more than 30 years, with sporadic epidemics of malaria (Brown and Pal 1971).
Resistance in An. saccharovi is now found in Greece, Lebanon, Iran, and Turkey and multiple
resistance to DDT, dieldrin, malathion, fenitrothion, propoxur, and permethrin has been
demonstrated.
Pronounced DDT resistance appeared in An. Stephens! in Iran and Iraq when full scale residual
spraying operations were begun in 1957-58. Dieldrin resistance appeared three years later, followed
by malathion resistance in 1975 after six years of use (World Health Organization 1976).
In Central America and the Caribbean, dieldrin spraying against An. albimanus was begun in 1956
and widespread resistance appeared in 1958. A return was made to DDT spraying, and resistance
appeared in 1958 and was general by 1960. The effective carbamate propoxur was employed in
Guatemala, El Salvador, Honduras, and Nicaragua in 1970-71, and pronounced resistance had
developed by 1974. ATK albumanus now shows multiple resistance to DDT, dieldrin, lindane,
malathion, propoxur, and permethrin (World Health Organization 1981).
ATL culicifacies is the principal vector of malaria in India, Pakistan, and Sri Lanka. This vector
developed dieldrin resistance in India in 1958 and DDT resistance in 1959 after three years of
spraying, but a widespread malaria eradication program was continued until 1965-66 when both
DDT and BHC failed to control outbreaks of malaria in areas under consolidation and maintenance
(Brown and Pal 1971). Malathion was substituted in 1968 with some success, but widespread
epidemics of malaria were reported in 1975 with 4 million cases as compared to 125,000 in 1965.
In Pakistan, the experience was similar with DDT resistance appearing in An. culicifacies in 1963.
The importance of this resistance was not recognized until outbreaks of malaria began in 1969.
Neither DDT nor lindane was effective. By 1975 malaria cases in Pakistan were reported to number
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over 10 million as compared to 9,500 in 1961. Malathion resistance appeared in An, culicifacies in
1975.
The problems of the rapid development of BHC and dieldrin resistance in An. gambiae in Africa
have been discussed in Section II.
Many other examples of insecticide resistance in Anopheles spp occurred throughout the world,
and by 1981 multiple resistance was present in 52 of the 60 vectors of malaria as shown in Table
6 (World Health Organization 1981).
Malaria eradication through residual house spraying reached a high point in 1974 when the malaria
was considered eradicated in 36 countries; the population in areas in the maintenance phase and
essentially without risk had increased to 797 million or 41.2% of the population in the areas of
endemic malaria (Brown et al. 1976). However, malaria eradication programs in Saudi Arabia,
Somalia, Burma, Cambodia, and South Viet Nam had reverted to organized control programs
covering a population of 168 million. Parasite rates remained high in Africa, Southern Asia, and
parts of Central America involving about 100 million people. Massive epidemics of malaria had
occurred India and in Pakistan. Thus in the areas where multiple resistance in Anopheles vectors
is widespread malaria eradication efforts have almost completely broken down with some countries
recording 30-40 fold increases in the number of cases of malaria from 1968 to 1976 (Agarwal
1979). Bruce-Chwatt (1970) stated that "physiological resistance has become one of the major
threats of the success of global malaria eradication", and as of 1976, WHO quietly abandoned the
concept of global malaria eradication by residual house spraying (WH01978).
DEPLETION OF INSECTICIDE RESOURCES
The widening spread of cross and multiple resistance through the genomes of major pest
insects has severely limited the armamentarium of insecticides effective for the control of insect
pests. The chronology of control failures with the Colorado potato beetle (Table 3) and the house
fly (Table 4) provide dramatic confirmatory evidence (see also Section V). The spread of resistance
has resulted in the wholesale replacement of the organochlorines by organophosphates and these
in turn are being replaced by carbamates and then by pyrethroids. The progressive substitution of
newer and more sophisticated insecticidal molecules has caused escalating costs to the users of
insecticides. On the average, lindane and the cyclodienes cost about 6 times more than DDT,
organophosphates 11 times, carbamates 9 times, and pyrethroids 100 times more than DDT. To
be sure there are substantial dosage differences, e.g. the pyrethroids are generally used at rates
0.05- 0.1 those for DDT. Nevertheless, the cost differential is a major factor for the farmer who is
bound by essentially static farm prices, and it has been disastrous for public health programs such
as the WHO malaria eradication scheme. Based on a cost factor of 1.0 for DDT residual house
spraying at 2 g per m2, replacement with dieldrin at 0.5g per m2 costs 1.7 times more; with lindane
at 0.5g, 5.2 times; with malathion at 2g, 5.3 times; with fenitrothion at 2g, 15.9 times; with propoxur
at 2 g, 20.4 times (Metcalf 1983). With the synthetic pyrethroids costing $50-100 or more per Ib.
and used at 0.1 g per m2; the costs become astronomical. These cost increases are completely
beyond the resources of public health budgets.
During the past 40 years insecticide-resistant pests have been controlled by the simplistic
process of changing to a new type of insecticide to which the pest is susceptible. The widening
patterns of multiple resistance (Table 1) show that this is a dubious long term solution. Pesticide
discovery and development have become increasingly rigorous and costly. In 1956,1800 chemical
compounds were screened per marketable new product; in 1965-3600; in 1969-5040; in 1970-8000;
15
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in 1972-10,000; in 1977-12,000 and in 1984-22,000 (Johnson and Blair 1972, Menn 1980, Storck
1984). Over this same period, the total developmental costs for marketing a new pesticide in the
United States have increased from about $1.2 million in 1956 to about $45 million in 1984 (Fig. 2).
Insecticide resistance has steadily decreased the marketable life of new insecticides and cross
and multiple resistance prejudice the effectiveness of new products even before they are marketed.
Thus cross resistance in An. albimanus in El Salvador initiated by the drift of carbaryl from cotton
fields to aquatic breeding habitats of the mosquito, sharply reduced the effectiveness of the related
carbamate propoxur developed as a replacement for DDT in malaria control by residual house
spraying (Georghiou et al. 1973). Multiple resistance by the DDT-selected kdr mechanism
predisposes insect pests to rapid development of high levels of pyrethroid resistance (Miller et al.
1983, Omer et al. 1980, Priester and Georghiou 1980, Georghiou 1986). There is substantial
evidence that the accumulating genes regulating a variety of biochemical mechanisms for
detoxication and target site insensitivity have progressively shortened the effective lifetimes of
succeeding classes of new insecticides (Tables 1 and 2). Insecticide resistance, therefore, has
played a major role in the precipitous decline in the discovery and development of new synthetic
insecticides that has occurred since 1960 (Table 7).
TACTICS FOR MANAGING INSECT RESISTANCE TO INSECTICIDES
The methodology for insecticide use in agricultural and public health over the past 40 years
has been largely that of endeavoring to suppress insect pest species to unrealistic levels, i.e.
eradication. Pest species exposed to the massive applications of insecticides made to agricultural
crops, to pest breeding sites, and to urban and suburban properties have been under intensive
"natural selection" in the Darwinian sense. Species that survived such onslaughts were forced to
change the nature of the genome by undergoing "accelerated microevolution". Naturally occurring
mutations that favored survival in an insecticide laden environment rapidly become dominant as
described in Section II. As shown in Tables 1 and 2, this process of resistance selection has occurred
with disconcerting rapidity for almost all insect pest species. The persistence of resistance genes
in the insect pest genome (Section IV), has made it impossible to reverse the historical loss of
insecticide effectiveness as portrayed in Tables 3, 4, and 6.
Many tactics for resistance management have been proposed over the past 40 years but few
specific methodologies have been put to practical use. The resistance problem has been addressed
largely by toxicologists and entomologists who have proposed solutions directed solely at insecticide
use, i.e., insecticide management (beeper et al. 1986). Suggested solutions include (a) monitor
insect pests so that primitive susceptibility levels are understood and early detection of specific
resistance is possible, (b) avoid use of mixtures of insecticides, (c) extend the useful life of a
satisfactory insecticide as long as possible, but monitor susceptibility and replace the insecticide
before it fails, (d) choose a sequence of suitable alternative insecticides based on genetic
considerations affecting cross and multiple resistance, and (e) exploit alternative treatments with
insecticides devoid of common major R factors (Metcalf 1980). The frequently proposed remedy of
incorporating synergists to restore insecticide effectiveness is unlikely to be productive in view of
past experience (Section III-B). Resistance can rapidly develop to the combination of insecticide
and synergist or through alternative pathways. The use of mixtures of chemicals is subject to
disadvantageous registration and marketing considerations and to environmental quality problems.
However, resistance is a complex genetic, evolutionary, and ecological phenomenon and
insecticide management is unlikely to produce other than temporary palliation. As we have seen
(Section VII), the technological and economic requirements for successful insecticide management
16
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are likely to exceed available resources. Resistance management tactics are more likely to succeed
if they are directed at reducing the single-factored selection pressure that occurs with conventional
chemical control. Obvious counter measures include (1) reduce frequency of insecticide treatments,
(2) reduce extent of treatments, (3) avoid insecticides with prolonged environmental persistence
and slow release formulations, (4) reduce the use of residual treatments, (5) avoid treatments that
apply selection pressures on both larval and adult stages, (6) incorporate source reduction and
non-chemical methods, such as biological and cultural controls in control programs (Metcalf 1980).
National programs or policies incorporating these principles have been organized against the
housefly in Denmark, and the cattle tick and the cotton bollworm Heliothis armigera in Australia
(Keiding 1986).
The combination of these principles is essentially a blue-print for integrated pest management
(IPM) that is a dynamic framework for insect control practice based around the observance of the
economic threshold before initiating remedial practices, and that seeks to relegate the use of
insecticides to emergency weapons to be applied as last resort. Within the IPM framework there is
opportunity to consider resistance management tactics based on population genetics, i.e., relating
to the frequency of resistant aileles, decreasing the dominance of resistant genes, and minimizing
the fitness of resistant genotypes (beeper et al. 1986). These proposals require manipulations of
the agroecosystem such as the mass release of susceptible insects, the eradication of resistance
foci, the application of insecticides at high rate to reduce dominance by heterozygotes, and reducing
the fitness of resistant genotypes by preserving susceptible homozygotes (Georghiou and Taylor
1977). Whether such theoretically desirable schemes can be implemented within existing economic,
social, and political constraints is an intriguing question. (Miranowski and Carlson 1986).
17
-------
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22
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TABLE 1
Development of Insect Pests with Multiple Resistance to Various Groups of Insecticides1
Year
1938
1948
1954
1970
1975
1980
1984
Resistant DDT
Cyclodlenes
7 0
14 1
25 18
224 42
384 70
428 105
447 119
DDT
Cyclodlenes
Organophosphorus
0
0
3
23
44
53
54
DDT
Cyciodienes
Organophosphorus
Carbamates
0
0
0
4
22
25
25
DDT
Cyciodienes
Organophosphorus
Carbamates
Pyrethroids
0
0
0
0
7
14
17
References
Brown & Pal (1971)
Brown & Pal (1971)
Metcalf (1955)
Brown (1971)
Georghlou & Taylor
(1981)
Georghlou (1981)
Georghiou (1986)
1From Metcalf, R.L The ecology of insecticides and the chemical control of insects, pp. 251-297,
in M. Kogan, ed, "Ecological Theory and Integrated Pest Management Practice", Wiley, N.Y. (1986)
23
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TABLE 2
Approximate Rate of Development of Insecticide-Resistant Insect Species, Worldwide
Year Resistance was Attained1
Resistant pests (no.) DDT/ Undane/ Organophosphates Carbamates
methoxychlor cyclodiens
5 1951 1954 1959 1971
10 1952 1955 1962 1972
20 1955 1956 1964 1974
40 1960 1959 1968 1977
00 1968 1965 1972
160 1974 1971 1976
Average Doubling time -years 6-3 5-° 4-° 2-5
Pyrethrolds
1976
1979
1980
1985
2.0
1Data from Brown & Pal (1971), Metcalf (1955), Brown (1971), Georghiou & Taylor (1977a),
Georghiou (1981), and Farnham (1985).
24
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TABLE 3
Development of Insecticide Resistance in the Colorado Potato Beetle Leptinolasa decemiineata.
island1
Insecticide
Arsenicals
DDT
Dieldrin
Endrin
Carbaryl
Azinphos methyl
Monocrotophos
Phosmet
Phorate
Carbofuran
Oxamyl
Fenvalerate
Permethrin
Year Introduced
1880
1945
1954
1957
1959
1959
1973
1973
1973
1974
1978
1979
1979
Year First Failure
1940
1952
1957
1960
1963
1964
1973
1973
1974
1976
1978
1981
1981
1From Metcalf, R.L. The ecology of insecticides and the chemical control of insects, pp. 251-297,
in M. Kogan, ed. "EcologicalTheory and Integrated Pest Management Practice", Wiley, N.Y. (1986).
Data from Forgash (1984).
25
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TABLE 4
Rates of Development of Insecticide Resistance in the House Fly, Musca domestica. in Denmark.1
Insecticide
PDJ
Lmdane
Chlordane
Diazinon
Coumaphos
Malathion
Ronnel
Fenthion
Dimethoate
Fenitrothion
Dichlorvos
Bromophos
Tetrachlorvinphos
lodofenphos
Bendiocarb
Dioxacarb
Decamethrin
Cypermethrin, penmethrin
Fenvalerate
Year Introduced
1945
1948
1949
1952
1955
1962
1960
1960
1963
1967
1968
1969
1969
1969
1976
1976
1976
1977
1977
Year First Failure
1947
1950
1951
1955
1955
1963
1961
1964
1966
1967
1970
1970
1969
1969
1976
1976
1976
1977
1977
1Keiding 1977, 1978, 1979.
26
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TABLE 5
Insect Pests with Multiple Resistance to Five Classes of Insecticides
Coleoptera
Colorado potato beetle, Laptinotarsa decemlineata
Granary weevil, Sitophilus aranarius
Red Flour beetle, Tribolium castaneum
Dlptera
House Fly, Musca domestica
House Mosquito, Culex pipiens
Horn Fly, Haematobia im'tans
Leaf miner, Liriomyza trifolii
Malaria mosquitoes. Anopheles albimanus and An. sacharovi
Homoptera
Brown plant hopper, Niloparvata lugens
Green peach aphid, Myzus persicae
Pear psylla, Psylla pyricola
Lepldoptera
Armyworms, Spodoptera fruigiperda. &. littoralis
Cotton Bollworms, Heliothis armigera and hL virescens
Diamond back moth, Plutella xylostella
Orthoptera
German cockroach, B|attella germanica
Thysanoptera
Citrus thrips, Scirtothrips citri
27
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TABLE 6
Spread of Insecticide Resistance in Anopheles Mosquito Vectors of Malaria1
Year
Number of
Resistant
Species
DDT
Number of Species Resistant to:
Dieldrin/ Organophosphates Carbamates Pyrethrolds
Undane
1951
1957
1959
1962
1969
1976
1980
8
24
35
39
43
51
12
15
24
34
6
23
34
37
43
47
1
2
10
1Data from Brown & Pal (1971), Georghiou (1981), World Health Organization (1976,1980).
28
-------
TABLE 7
Rate of Discovery and Development of New Broad-Spectrum Insecticides1
Years
1940-45
1945-50
1950-55
1955-60
1960-65
1965-70
1970-75
1975-80
1980-85
Number Patented
3
6
15
19
21
17
10
8
0
1From date of original patent (Merck Index 1983).
29
-------
FIGURE 1
Action of DDT'ase in converting DDT to DDE, and relative toxicity of some "resistance proof" DDT
analogues to susceptible (S) and DDT resistant (R) house flies. (Metcalf & Fukuto 1968).
Cl
H
Q
c
DDT
Cl
Musca domestics
LD50 pg per g
S R
2.0 >5OOO
Cl
DDE
Cl
Cl.
Cl
D
C
C
Cl
2.3
500
36
Cl
Cl
D
c
C
CI-
Cl
9.5
22
4.1
15.5
30
-------
FIGURE 2
Increasing developmental costs for new pesticides. From Johnson & Blair (1972), Metcalf (1980),
Menn (1980), and Storck (1984).
xlO6
50
40
30
20
10
(• I Wj^ | | | | |
I960 I960 1970 1980 1990
31
-------
32
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ECOLOGICAL SIDE EFFECTS OF PESTICIDE AND
FERTILIZER USE ON TURFGRASS
Daniel A. Potter, Stephen D. Cockfleld,
and
Terry Arnold Morris
Department of Entomology
University of Kentucky
Lexington, Kentucky 40546
Turfgrasses, which cover an estimated 8 to 10 million hectares in the United States (Kageyama
1982, Tashiro 1987), are typically the most intensively managed plantings in the urban landscape.
Increasing public demand for dense, uniform, pest-free turf has resulted in a growing number of
lawns, golf courses, and other turf areas being maintained with regular chemical applications (U.S.
EPA 1979, National Research Council 1980, Anonymous 1984). Gross annual sales of the
commercial lawn care industry increased at an average annual rate of 22% between 1977 and
1984, with ca. 13% of single-family households with incomes over $20,000 contracting for
commercial lawn care in 1984 (Anonymous 1984). Total annual expenditures for turfgrass
maintenance in the United States were estimated in 1983 to be about 15 billion dollars (Tashiro
1986), with much of this cost allocated to the purchase and application of insecticides, herbicides,
fungicides, and fertilizers.
Pesticides and fertilizers are versatile and powerful tools of pest management, and there are
many pest problems for which the use of chemicals currently provides the only practical solution
(Metcalf 1975). However, use of chemicals may also have profound effects on the structure, stability,
and resilience of agricultural systems (Pimentel and Edwards 1982). Because pesticides kill
beneficial organisms as well as pests, their use may increase the risk of pest resurgences or
secondary pest outbreaks (e.g. Luck and Dahlsten 1975, McClure 1977, Merritt et al 1983).
Pesticides and fertilizers may also affect energy flow and nutrient recycling by altering primary
production or by disrupting the activity of organisms important to decomposition processes (Edwards
and Thompson 1973, Pimentel and Edwards 1982).
Like many cultivated crops, turfgrass lacks the complexity of natural grassland and forest
systems, and so would be expected to be relatively susceptible to pesticide-induced perturbations.
However, little information exists on the ecological side-effects of pesticide and fertilizer usage on
turfgrass. The purpose of this chapter is to summarize recent research which has begun to clarify
the effects of common turf management practices on populations of potentially beneficial
invertebrates in turfgrass, and how this in turn may affect key processes such as thatch
decomposition and natural regulation of pest populations.
33
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THE TURFGRASS ECOSYSTEM
Turf grass consists of the roots, stems, and leaves of grass plants, together with a tightly
intermingled layer of dead and living roots, rhizomes, stolens, and organic debris commonly referred
to as thatch (Beard 1973). This composite habitat supports a variety of plant-feeding insects and
mites which inhabit the soil, thatch, and/or above-ground portions of the grass plants. These include
a number of familiar pest species that cause injury by consuming roots (e.g., scarabaeid grubs;
billbugs), devouring grass blades and stems (e.g., sod webworms, cutworms, armyworms) or by
feeding upon plant sap and damaging vascular tissues (e.g., chinch bugs, greenbug, winter grain
mite). Biology and host plant relationships of turfgrass insect pests were reviewed by Tashiro (1987).
Turfgrass also supports a diverse community of non-pest invertebrates. In one survey (Streu
1973), 11 taxa of nematodes, 83 arthropod taxa including numerous families of insects and mites,
and numerous kinds of annelids, gastropods, and other invertebrates were collected from a
bluegrass-red fescue turf in New Jersey. Pitfall trap surveys and Tullgren funnel extractions revealed
a similarly rich fauna of free-living predators and soil and thatch inhabiting species from turfgrass
areas in Kentucky. More than 40 species of Staphylinidae (rove beetles), 30 species of Carabidae
(ground beetles), 10 species of Formicidae (ants), dozens of species of spiders and other
predaceous arthropods, and large numbers of nematodes, earthworms, Collembola (springtails),
oribatid mites, and other soil invertebrates have been collected from untreated Kentucky bluegrass
and tall fescue turf (Cockfield and Potter 1984, 1985, Potter et al. 1985, Arnold and Potter 1987).
These pest and non-pest invertebrates form a complex community which interacts with the living
grass, thatch, and soil and contributes to the stability of the turfgrass habitat.
PESTICIDE EFFECTS ON NATURAL REGULATION OF
PEST POPULATIONS
Pesticides that are applied for control of turfgrass pests are generally also toxic to predators
and parasites. For example, a single, surface application of the organophosphate insecticides
chiorpyrifos or isofenphos reduced populations of predatory mites, spiders, and insects in Kentucky
bluegrass by as much as 60% (Cockfield and Potter 1983). Predator populations were still
depressed more than six weeks after the application (Fig. 1). Given their sensitivity to insecticides,
it is not surprising that predatory arthropods were found to be less abundant and less diverse in
high maintenance Kentucky bluegrass sites (i.e., turfgrass that received scheduled applications of
fertilizers and pesticides) than in sites that had been maintained without chemical applications
(Cockfield and Potter 1985, Arnold and Potter 1987) (Table 1). Similarly, spider and ground beetle
populations were found to be 20-30% lower in lawns receiving preventative insecticide treatments
in Florida (Short et al. 1981).
Several authors (Streu and Cruz 1972, Streu and Gingrich 1972, Reinert 1978, Cockfield and
Potter 1984) have cautioned that repeated pesticide treatments could reduce the stability of
turfgrass communities and lead to increased pest problems. Nevertheless, documentation of pest
resurgences or secondary pest outbreaks in turfgrass is somewhat limited. Reinert (1978) observed
that southern chinch bug (Blissus insularis Barber) populations in Florida remained low in untreated
St. Augustine grass lawns where predators and an egg parasite were abundant, while at the same
time reaching outbreak densities on lawns that received repeated insecticidal treatments. Similarly,
resurgence of hairy chinch bug populations following several years of chlordane treatment were
attributed to reduced populations of predatory mites (Streu and Vasvary 1966, Streu 1969, Streu
34
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and Cruz 1972), and possibly predatory hemipterans (Streu 1973). In New Jersey, carbaryl
treatments over several years were accompanied by outbreaks of winter grain mite (Penthaleus
mjior (Duges)) (Streu and Gingrich 1972). These authors suggested that carbaryl may have
reduced populations of mite predators. In Kentucky, outbreaks of the greenbug (Schizaphis
graminum (Rhondani)) appear to be more common on high maintenance lawns than on untreated
turf (Potter 1982).
Short lists of natural enemies associated with various turfgrass pests have been published
(e.g., Bohart 1947, Streu and Cruz 1972, Streu and Gingrich 1972, Tashiro 1973, Reinert 1978,
Cockfield and Potter 1984). Nevertheless, the experimental evidence that predators or parasites
are important in regulating pest densities in turfgrass is very limited. Reinert (1978) observed egg
parasitism and predation upon southern chinch bugs in laboratory trials and in the field. He
suggested that the combined predator-parasite complex may have contributed, at least in part, to
an observed collapse in chinch bug populations in late summer. Cockfield and Potter (1984)
collected sod webworm (Crambus and Pediasia spp.) eggs from field-collected females and
exposed them to natural predation in Kentucky bluegrass. Predators, primarily ants, consumed or
carried off up to 75% of the eggs within 48 hours. Treatment of half of the plots with a single surface
application of chlorpyrifos to kill sod webworm larvae significantly reduced predator- induced
mortality of the eggs for at least three weeks (Table 2), while simultaneously reducing the numbers
of predators moving through the turf. To date, this study is the only experimental demonstration
that natural enemies may be important in reducing pest populations in turfgrass, and that this
process can be disrupted by pesticide applications.
THATCH ACCUMULATION AND DECOMPOSITION
The Greek philosopher and scientist Aristotle called earthworms "the intestines of the earth".
indeed, earthworms and other soil- inhabiting invertebrates including nematodes, millipedes,
oribatid mites (Acari: Cryptostigmata), Diplura and Collembola are known to play a major role in
plant litter decomposition and nutrient recycling in forest and pasture soils. These animals aid the
decomposition process by fragmenting and conditioning plant debris in their guts before further
breakdown by microorganisms (Lofty 1974, Harding and Stuttard 1974, Wallwork 1983). They also
disseminate bacteria and fungi, enrich the soil with their excreta, and help to distribute organic
matter throughout the topsoil layer (Satchell 1967, Lofty 1974). Plant litter decomposition is generally
much faster with the combined influence of soil animals and microorganisms than with
microorganisms alone (Ghilarov 1963). The burrowing action of earthworms and other soil
invertebrates is also critical to air and water infiltration in turfgrass. Charles Darwin, considered an
early authority on earthworms, wrote: "The plough is one of the most ancient and most valuable of
man's inventions; but long before he existed, the land was in fact ploughed, and still continues to
be thus ploughed by earth-worms" (Darwin 1907). This process is especially important in lawns,
golf course fairways, and other turf areas which are "cultivated" mainly as a result of earthworm
activity.
Excessive thatch results from an imbalance between vegetative production and decomposition
at the soil surface (Beard 1973). Problems associated with thatch accumulation include restricted
penetration of fertilizers (Cornman 1952, Nelson et al. 1980), binding of insecticides (Niemczyk et
al. 1977, Niemczyk 1987), reduced water infiltration (Taylor and Blake 1982), and shallow root
growth, with increased vulnerability to heat and drought stress (Beard 1973). Kentucky bluegrass
lawns maintained with multiple applications of pesticides and high rates of fertilizer often develop
35
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a thatch problem within 4 to 5 years (Engel and Alderfer 1967, Meinhold et al 1973, Shoulders and
Hall 1983).
Excessive fertilization encourages thatch accumulation by increasing vegetative production,
but may also indirectly contribute to the problem by affecting decomposition processes. Nitrogen
fertilization commonly results in soil acidification (Pierre 1928) which may in turn inhibit microbial
activity (Starkey 1953, Martin and Beard 1975, Bridges 1983). Furthermore, the repellent nature of
NH4+ can reduce numbers of soil invertebrates, including microarthropods and nematodes, and
earthworms (Marshall 1977, Edwards and Lofty 1977). Earthworms, in particular, are generally
sparse in acidic pasture and forest soils (Satchell 1977, Edwards and Lofty 1977). Several studies
(Starkey 1953, Engel and Alderfer 1967, Meinhold et al. 1973, Smith 1978, Potter et al. 1985) have
indicated correlation between high rates of fertilization and thatch accumulation, although this may
not always occur (Shearman et al. 1980). Potter et al. (1985) sampled earthworm and
microarthropod populations in Kentucky bluegrass plots that had received varying rates of
ammonium nitrate fertilizer (0 to 25 g N m-2) for seven years. Increasing the rate of fertilization
resulted in a significant decrease in soil and thatch pH and in exchangeable Ca and K, and caused
a significant increase in thatch. These changes were accompanied by a significant (33 to 66%)
reduction in populations of earthworms and certain oribatid mites. Although thatch thickness was
correlated with decreased earthworm density and biomass, it is probable that other factors such
as increased plant growth and reduced microbial degradation also contributed to the relationship.
Use of pesticides can also contribute to thatch development. For example, treatment with
certain fungicides may reduce soil pH, which can in turn impair the activity of microorganisms
important to thatch degradation (Smiley and Craven 1978). Alternatively, fungicides may increase
rates of root and rhizome production, further contributing to thatch accumulation (Smiley et al.
1985). Several investigators (Randell et al. 1972, Streu 1973, Turgeon et al. 1975) have reported
correlation between increased thatch and reduction in earthworm populations following treatment
with certain insecticides or herbicides. Many pesticides commonly applied to turfgrass, including
benomyl, ethoprop, carbaryl, bendiocarb, and others, are toxic to earthworms (Ruppel and Laughlin
1977, Karnok 1980, Roberts and Dorough 1984, Potter, unpublished data).
It is generally observed that thatch is rarely excessive where earthworms are abundant, but
until recently, the evidence that earthworms are important to thatch degradation has been largely
correlative. If earthworms and other soil invertebrates are in fact critical to thatch degradation, then
careful consideration should be given to any cultural practice that might reduce their activity.
Experiments currently in progress (Potter and Powell, unpublished data) appear to verify the
contribution of earthworms to thatch degradation in turf. Several hundred pre-weighed pieces of
intact Kentucky bluegrass thatch (8x10 cm; ca. 18 mm thick) were sewn into nylon mesh bags
having different sized openings (50 m, 1.2 mm, or 5 mm), and buried just under the surface of a
Kentucky bluegrass turf. The small, medium, and large mesh sizes were intended, respectively, to
exclude all decomposers except microorganisms, to selectively exclude earthworms while admitting
smaller invertebrates, such as mites, or to admit all components of the soil fauna, including
earthworms. In a companion experiment, thatch pieces in identical large mesh bags were buried
in untreated plots, or in plots that had been treated with chlordane and carbofuran to eliminate
earthworms. Thatch pieces from each experiment were disinterred every 3-4 months to compare
rates of decomposition in the presence or absence of soil invertebrates. Pieces were re-weighed,
analyzed for microbial activity and soil content, and extracted in Tuligren funnels to determine the
invertebrate species present. Dramatic differences were apparent in both experiments after only 3
months. Without earthworms the structure and composition of the thatch remained nearly
unchanged; however, the pieces were broken apart and dispersed when earthworms were present.
The most striking effect of earthworm activity was a significant increase in the amount of soil
36
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incorporated into the thatch (Fig. 2). The effect of this natural process is very similar to that achieved
by core cultivation, a process by which soil is mechanically reincorporated back into the thatch
layer, and which is considered the best method of managing thatch (Beard 1973, Danneberger
1982). Rates of microbial respiration and loss of organic matter were found to be much greater for
thatch pieces that had been "worked" by earthworms than for those from which earthworms had
been physically or chemically excluded. Details of these experiments will be reported elsewhere.
ADDITIONAL CONSIDERATIONS
Two other problems that may be encouraged by repeated pesticide usage in turfgrass are
acquired resistance of pests to insecticides or fungicides, and enhanced microbial degradation of
pesticide residues. Acquired resistance can become a problem when insecticides are applied
repeatedly over a number of years. Acquired resistance has been documented for a number of
turfgrass pests, including webworms, chinch bugs, billbugs, greenbugs, and several species of
white grubs (Tashiro 1982, 1987; Reinert 1982). Judicious use of insecticides, and alternation of
treatments with materials from different chemical classes (e.g., organophosphate followed by
carbamate) will help to prevent or delay this phenomenon.
Enhanced microbial degradation occurs when pesticide residues are degraded more rapidly
than usual by microorganisms. Enhanced biodegradation apparently occurs as a result of
microorganisms becoming adapted to a pesticide to the point of being able to use it as an energy
source (Forrest et al. 1981). This phenomenon has been documented in soil for several insecticides,
including diazinon, carbofuran, fensulfothion, and isofenphos.
Recent experiments (Niemczyk and Chapman 1987) indicate that this alarming pattern may
also occur in turf. When isofenphos was applied to golf course fairways that had a history of
isofenphos treatments, more than 90% of the insecticide degraded within three days. In contrast,
there was practically no degradation in previously untreated fairways. Enhanced microbial
degradation of isofenphos residues in thatch appears to be the cause of at least some reported
cases of poor residual control of white grubs (Niemczyk and Chapman 1987). Even more disturbing
is the report that other insecticides, including diazinon, chlorpyrifos, carbaryl, and isazophos were
rapidly degraded when applied to turfgrass that had been previously treated with isofenphos
(Niemczyk and Filary 1987).
We choose not to here enter the debate concerning the potential acute and long-term chronic
effects of pesticide exposure to humans, pets, and wildlife, or the fate of pesticide residues in the
urban environment, as these are complex biological, social, and political issues that have been
reviewed elsewhere (McEwen and Stephenson 1979, National Research Council 1980, McEwen
and Madder 1986).
37
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CONCLUSIONS
The intent of this chapter is not to support or condemn pesticide use on turfgrass. Rather, our
goal has been to review some of the ways that chemical applications can affect interactions among
turf- inhabiting invertebrates, and to speculate on how these changes may alter the stability and
resilience of the turfgrass ecosystem. There are clearly certain situations in which the use of
pesticides is essential to the maintenance of quality turf. However, like human medicines, pesticide
applications can have some adverse side-effects, and these must be weighed against the overall
benefits that the treatment provides. The available evidence suggests that turfgrass is a complex
system with many buffers. However, we are only beginning to understand the roles of
microorganisms, earthworms, predators, and other invertebrates in maintaining this natural balance.
It does appear that pesticide or fertilizer applications can sometimes aggravate thatch or pest
problems by interfering with the activities of beneficial organisms, or by encouraging the
development of acquired resistance or enhanced microbial degradation. Awareness of these
potential side-effects, together with additional research on basic interactions within the turfgrass
ecosystem may facilitate development of more effective and more environmentally-sound turfgrass
management programs.
38
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LITERATURE CITED
Anonymous. Lawn Care Ind. 1984, 8(6), 1,8.
Arnold, IB.; Potter, DA Environ. Entomol. 1987, 16,100-105.
Beard, J.B. "Turfgrass: Science and Culture"; Prentice-Hall: Englewood Cliff, N.J., 1973, 658 pp.
Bohart, P.M.; Hilgardia; 1947,17, 267-307.
Bridges, B.L "Thatch Control and Effects of Nitrogen on Certain Biological and Chemical Parameters in Kentucky
Bluegrass Turf". M.S. Thesis, Univ. of Kentucky, Lexington.
Cockfield, S.D.; Potter, D.A. Environ. Entomol. 1983,12,1260-1264.
Cockfield, S.D.; Potter, D.A. J. Econ. Entomol. 1984, 77,1542-1544.
Cockfield, S.D.; Potter, D.A. Great Lakes Entomol. 1984,17,179-184.
Cockfield, S.D.; Potter, D.A. Can Entomol. 1985,117, 423-429.
Danneberger, K. Am. Lawn Applic. 1982, 3,24-26.
Darwin, C. "The Formation of Vegetable Mould Through the Action of V\forms with Observations on Their Habits"; D.
Appleton: New York, 1907, 336 pp.
Edwards, C.A.; Thompson, A. Residue Rev. 1973, 45,1-79.
Edwards, S.D.; Lofty, J.R. In "TheSoil Ecosystem";Sheals, J.G.; Ed.; Systematic Association: London, 1969, pp. 237-247.
Engel, R.E.; Alderfer, R.B. N.J. Agric. Exp. Stn. Bull., 1967, 818, 32-45.
Forrest, M.; Lord, K.A.; Walker, N.; Vtoodville, H.C. Environ. Pollut., 1981, A24, 93-104.
Ghilarov, M.S. In "SoilOrganisms";Doeksen, J.; va der Drift, J; Eds.; North Holland: Amsterdam, 1962, pp. 256-259.
Harding, D.J.L.; Stuttard, R.A. In "Biology of Plant Litter Decomposition"; Dickinson, C.F.; Pugh, G.J.F.; Academic Press:
New York, 1974, pp. 489-532.
Kageyama, M.E. In "Advances in Turfgrass Entomology"; Niemczyk, H.D.; Joyner, B.G.; Eds.; Hammer Graphics: Piqua,
Ohio, 1982, pp.133-138.
Karnok, K. Lawn Care Ind.. 1980, 4,16.
Lofty, J.R.; In "Biology of Plant Litter Decomposition"; Dickinson, C.H.; Pugh, G.J.F.; Academic Press: New York, 1974,
pp. 467-488.
Luck, R.F.; Dahlsten, D.L. Ecology 1975, 56, 893-904.
Marshall, V.G.; Commonwealth Bur. Soils Spec. Pub., 1977, no. 3.
McClure, M.S. Environ. Entomol. 1977, 6, 480-484.
McEwen, F.L; Stephenson, G.R.; "The Use and Significance of Pesticides in the Environment"; Wiley: New York, 1979,
538 pp.
McEwen, F.L; Madder, D.J.; In "Advancesin Urban Pest Management"; Bennett, G.W.; Owens, J.M.; Eds.; Van Nostrand
Reinhold: New York; 1986, pp. 25-50.
Meinhold, J.H.; Duble, R.L.; Weaver, R.W.; Holt, E.C.; Agron. J., 1973, 65, 833-835.
Merritt, R.W.; Kennedy, M.K.; Gersabeck, E.F. In "Urban Entomology: Interdisciplinary Perspectives"; Frankie, G.W.;
Koehler, C.S. (Eds.). Praeger: New York, 1983, pp. 277-299.
Metcalf, R.L. In "Introduction to Insect Pest Management"; Metcalf, R.L.; Luckman, W.H.; Eds.; J. Wiley & Sons: New
York; 1975, pp. 235-273.
National Research Council. "Urban Pest Management". Report prepared by the Committee on Urban Pest Management,
Environmental Studies Board, Commission on Natural Resources; National Academy Press: Washington, D.C.,
1980,272pp.
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Niemczyk, H.D. J. Econ. EntomoL; 1987; 80; 465-470.
Niemczyk, H.D.; Krueger, H.R.; Lawrence, K.O. Ohio Rep., 1977, 62, 26-28.
Niemczyk, H.D.; Chapman, R.A. J. Econ. Entomol. 1987, 80, 880-882.
Niemczyk, H.D.; Filary, Z. Proc. N.C.B. Meet., Entomol. Soc. Am.; 1987, (Abstr.).
Pierre, W.H. J. Am. Soc. Agron., 1928, 20, 254-269.
Pimentel, D.; Edwards, C.A. BioScience. 1982, 32, 595-600.
Potter, D.A. Am. Lawn Applic.; 1982, 3, 20-25.
Potter, D.A.; Bridges, B.L; Gordon, F.C. Agron. J. 1985, 77, 367-372.
Randell, R.J., Butler, J.D.; Hughes, T.D. HortScience, 1972, 7, 64-65.
Reinert, J.A. Ann. Entomol. Soc. Am. 1978, 71, 728-731.
Reinert, J. A. In "Advances in Turfgrass Entomology"; Niemczyk, H.D.; Joyner, B.D.; Eds. Hammer Graphics: Piqua, Ohio,
1982, pp. 71-76.
Roberts, B.L; Dorough, H.W. Environ. Tox. Chem. 1984, 3, 67-78.
Satchell, J.E. In "Soil Biology"; Surges, A.; Raw, F.; Eds.; Academic Press: New York, 1967, pp. 259-322.
Shearman, R.C.; Kinbacher,, E.J.; Riordan, T.P.; Steinegger, D.H.; HortScience, 1980, 15, 312-313.
Short, D.E.; Reinert, J.A.; Atilano, R.A. In "Advances in Turfgrass Entomology; Niemczyk, H.D.; Joyner, B.G.; Eds.;
Hammer Graphics: Piqua, Ohio, 1982, pp. 25-31.
Shoulders, J.F.; Hall, J.R. Am. Lawn Applic. 1983, 4, 4-7.
Smiley, R.W.; Craven, M.M. Agron. J. 1978, 70,1013-1019.
Smiley, R.W.; Craven Fowler, M; Kane, R.T.; Petrovic; White, R.A. Agron. J. 1985, 77, 597-602.
Smith, G.S. Agron. J., 1978, 71, 680-684.
Starkey, R.L Golf Course Rep. 1953, 21, 7-14.
Streu, H.T. Proc. Scotts Turfgrass Res. Conf. I. Entomology; 1969,1, 53-59.
Streu, H.T. Bull. Entomol. Soc. Am. 1973,19, 89-91.
Streu, H.T; Vasvary, LM. Bull. N.J. Acad. Sci.; 1966, 11,17-21.
Streu, H.T; Cruz, J.B. Down to Earth, 1972, 28,1-4.
Streu, H.T; Gingrich, J.B. J. Econ. Entomol. 1972, 65, 427-430.
Ruppel, R.F.; Laughlin, C.W. J. Kans. Ent. Soc.; 1977, 50,113-118.
Tashiro, H. In "Advances in Turfgrass Entomology"; Niemczyk, H.D.; Joyner, B.D.; Eds.; Hammer Graphics: Piqua, Ohio,
1982, pp. 81-84.
Tashiro, H.; Bull. Entomol. Soc. Am.; 1973, 19, 92-94.
Tashiro, H. "Turfgrass Insects of the United States and Canada"; Cornell University Press: Ithaca, N.Y., 1987, 391 pp.
Taylor, D.H.; Blake, G.R. Soil Sci. Soc. Am., 1982, 46, 616-619.
Turgeon, A.J.; Freeborg, R.P.; Bruce; W.N. Agron. J., 1975, 67, 563-565.
U.S. Environmental Protection Agency. National Household Pesticide Usage Study, 1976-1977, Report no.
EPA/540/9-80-002, 1979, 126pp.
Wallwork, J.A. Ann. Rev. Entomol.; 1983, 28,109-130.
40
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FIGURE 1
Impact of four turfgrass insecticides on spider populations in Kentucky bluegrass, based on
relative numbers captured in pitfall traps in treated and control plots. Replicated plots were treated
with surface sprays at label rates in late May. Similar reductions occurred for other taxa of
predaceous arthropods, although not all groups were equally affected. Reproduced with permission
from Cockfield and Potter (1983).
120
100
O 80
DC
O 6O
O
u.
O 4O
20
A chlorpyrifos
+ bendiocarb
• trichlorfon
• isofenphos
' ' -4
J_
012345
WEEKS POST-TREATMENT
J.
6
41
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FIGURE 2
Change in the mineral content of thatch pieces buried under Kentucky bluegrass turf for 12
months. Samples depicted in upper graph had been buried in mesh bags having different sized
openings to selectively admit or exclude certain components of the soil fauna (see text). Samples
in lower graph were buried in identical large mesh bags in plots that were either untreated, or that
had been treated with pesticides to eliminate earthworms. Data represent percentage of final
sample weight remaining after incineration, and reflect mainly differences in the amount of soil
incorporated into the samples by earthworms.
60
CD 4°
"5.
CO
CO
M—
o
S 20
o
O
"2
CD
J 60
0
O
CD
A Large Mesh
O Medium Mesh
• Fine Mesh
40
20
A With Earthworms
• Without Earthworms
July
1986
October
1986
April
1987
42
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TABLE 1
Relative number of predatory arthropods captured in pitfall traps at Kentucky bluegrass sites
maintained under a commercial lawn care program ("high maintenance") or under minimal care ("low
maintenance"). Data are based on seasonal captures (22 March -18 October) from 4 institutional
lawns (1-4 ha each) of each type in Lexington, Kentucky. Adapted from Cockfield and Potter (1985).
Mean number trapped per site
High Low
Taxon Maintenance Maintenance
mm mm mm mm mmmmmmimtmm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm mm *•* mm mm mm mm mm mm mm <
Coleoptera
Carabidae 24.8* 200.3
Staphylinidae 774.0 1172.5
Araneida
Lycosidae 29.3 38.8
Erigonidae 394.0* 1017.8
Linyphiidae 60.3* 183.0
^H ^_. ^^ ^^ ^^ ^^ ^^ ^^ ^^ ^^ ^w ^^ ^^ ^^ ^^ ^^ ^^ ^^ •• MM <^» ^Ht ^^ «!• ^^ mm>mmi mm mm mm, mm tmm mm. ^mi mm, mm tmm^mt mm mmmmi mm mm MB mm mm mm mm mm mm mm «•» mm mm mm
*Significantly lower than corresponding mean (P < 0.05)
43
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TABLE 2
Mean percentage of sod webworm eggs eaten or carried off by predators in replicated plots
of untreated Kentucky bluegrass compared to plots that had received a single surface application
of chlorpyrifos at label rate. Based on cohorts of 500 total eggs placed in the field for 48 h at 1,3,
or 5 weeks after the insecticide treatment. Reprinted with permission from Cockfield and Potter
(1984).
Percent missing from
Weeks post- Untreated Treated
treatment plots plots P levela
^"* ^^ ^^ ^* *** ^* ^™' ^* *^ ••» *^ <^* ^^ «^» ^» ^B «• ^M ^M •• *Bm ^^ ^B» ^^ ^M ^^ ^^ ^^ ^^ ^^ ^H» ^IB ^^^IV^IB ^^ «•» ^^ ^^ «•» ^|» ^^ ^^ «M «W «^ ^V ^^ ^^ ^^ ^^ ^W ^^ ^^ ^^ ^^ ^^ ^^ «• ^M ^» ^M «
1 37.7 0.9 P < 0.001
3 17.6 0.1 P < 0.05
5 75.4 61.3 P < 0.08
Probability of a greater t statistic, one-sided paired t test,
44
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CURRENT AND FUTURE REGULATORY CONCERNS
FOR LAWN CARE OPERATORS
James F. Wilkinson, Ph.D.
Director of Regulatory and Environmental Affairs
Professional Lawn Care Association of America
101 Buena Vista Drive
North Kingston, Rl 02852
Pesticide applicators, particularly those applying pesticides in the urban environment, such
as lawn care operators (LCO's), today are confronted with a rapidly changing (and often adverse)
environment. Public perception of pesticides and pesticide applicators is at an all time low. Federal,
state and local regulation of pesticides increases almost daily. Environmental concerns from ground
water contamination to endangered species will continue to generate regulations to be imposed
on applicators for many years to come. And the non-agricultural user of pesticides, those applicators
using pesticides in the urban setting (lawns, trees) or for vegetation management (utilities,
rights-of-way) will face even stiffer rules and regulations. These uses have a perceived lack of
"benefits".In addition, there is often the belief pesticides are not needed in the urban setting.
This paper first will present legislative and regulatory concerns for the LCO both today and in
the future. The Professional Lawn Care Association of America (PLCAA) is currently involved with
most of these issues since the issues will undoubtedly have a major impact on the way in which
pesticides are used (or not used) in the future. Safety, health, certification and training issues will
all play an increasing role and require increased attention from the LCO.
Next, the paper will review the need for LCO's to begin to help formulate reasoned pesticide
public policy. This will involve cooperation with other pesticide applicator groups, decision makers
(legislators and regulators), and environmental activists. LCO's will need to further incorporate IPM
and other techniques into their operations to reduce pesticide use and use pesticides more safely.
Otherwise, future regulations may jeopardize the very existence of the lawn care industry itself.
PERCEPTION OF PESTICIDES/MEDIA ATTENTION
The American public's perception of pesticides and toxic chemicals today, created generally
by the media, environmental groups and a few, but highly effective antipesticide activists, is at an
all time low. Here are the subjects of just a few of the stories which the public hears almost on a
daily basis:
pesticide residues on food
groundwater contamination
farm workers exposed to pesticides
death of Navy Lt. Prior after playing golf
2,4-D, cancer and Kansas farmers
data gaps, chronic effects of pesticides unknown
allergies/sensitivities to pesticides
dioxins, agent orange, Love Canal
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It's no wonder that the public is concerned and feels the way it does about pesticides after a
steady diet of such stories. These stories, especially when highly publicized by environmental
groups such as the National Coalition Against the Misuse of Pesticides, Sierra Club, Audubon
Society, National Wildlife Federation, and Environmental Defense Fund, strike a nerve with the
public. Concern over pesticide use is heightened when pesticides are being used right in their own
back yards for lawn care.
All of this has created a number of broadly defined issues facing the pesticide user industry
in general, and the LCO in particular. These begin with the public demanding their right-to-know
more about pesticide use and health and safety, and could end up with serious impairments to the
way LCO's currently conduct their business.
RIGHT-TO-KNOW
The public's right-to-know has become an important issue among anti-pesticide groups and
government officials. Communication of this right-to-know is taking many different forms as the issue
arises in various locations around the country.
Prenotification of pesticide applications has been proposed in many areas and has already
been adopted in some localities. Proposals often include notification of not only the LCO's
customers, but neighbors as well. LCO's are strongly opposed to notification of everyone in the
immediate areas of an application. They believe it is unjustified, and that it would add tremendously
to their cost of doing business.
Some states (Rl, MA, MD, NY) have adopted regulations requiring prenotification of lawn and
tree pesticide applications as requested by customers and neighbors. This system seems to be
working well, since only a small minority of people actually request prenotification so that it is not
overly burdensome to the LCO.
Posting after lawn and tree care applications is required in at least half a dozen states, and
more are sure to follow. In this case, strong industry input into the drafting of the regulations has
so far led to the use of signs only at the time of application (as opposed to before the application).
Many groups are in favor of "pre"posting (putting up signs one to two days before the application),
and should this type of posting become law, applicator costs will significantly increase.
Central registries of pesticide sensitive or allergic individuals are gaining favor in some areas.
Pennsylvania and Maryland, as well as some local communities, have established registries for
individuals with medical evidence of an allergy or sensitivity to pesticides. The names of individuals
on the registry are then shared with applicators to allow them to prenotify allergic individuals of
impending applications. Industry's reaction to this system has been positive, with a high degree of
compliance by individual companies. The actual number of people placing their names on the
registry has thus far been low.
Health and safety information is frequently required to be passed along to customers, and this
trend is expected to continue in more states. This information generally involves post application
safety precautions, but in some cases labels and MSDS's must be made available.
The newly passed federal Community Right-to-Know Law will also require certain pesticide
applicators to provide material information to local fire departments and other emergency personnel.
Local jurisdiction over pesticides is often an issue which arises out of local right-to-know
concerns. Federal legislation as well as legislation in many states often prohibits political entities
below the state level from regulating the use of pesticides. Numerous applicator alliances have
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challenged the right of local governments to regulate pesticides (Wauconda, IL; Prince Georges
County, MD), and in most cases courts have upheld the right of only the federal and state
government to regulate pesticides. With over 88,000 political entities below state level in the U S
LCO's clearly have a concern over the chaos which would be created if local governments were
given authority to regulate pesticides.
PUBLIC HEALTH AND SAFETY
Public concern over the health effects of exposure to pesticides will continue to generate future
regulations. Chronic risks from low levels of long term exposure, particularly in food residues and
drinking water are a major concern. Dislodgeable residues resulting in potential human exposure
to pesticides after lawn care applications is receiving considerable attention and has been one
justification for requiring lawn care posting.
A recent GAO report alleging inadequate EPA testing of most pesticides will surely speed up
the federal reregistration of many pesticides to bring them up to current registration standards. At
the same time, some states have lost confidence in the EPA's ability to adequately regulate
pesticides and protect the public. Thus, some states (CA, MA) will begin to require their own
registration data. Both of these developments will surely lead to higher pesticide costs and product
loss as manufacturers conclude that the economics of a product simply does not justify continued
registration.
The public also is increasingly hearing the question of risk/benefit analysis on pesticides used
non-agriculturally. Why, some ask, take any risk whatsoever simply to have a green lawn or to
control vegetation that could be controlled mechanically? Non-agricultural users of pesticides have
not done a good job of communicating the benefits of pesticides.
EMPLOYEE HEALTH AND SAFETY
The health and safety of applicators regularly using pesticides is receiving increasing attention.
Proposed and enacted legislation and regulation in this area alone will add huge costs to LCO
operations in the future. Consider the following examples:
• OSHA'S Hazard Communication Standard requiring health and safety information to
be shared with employees;
• a newly proposed EPA worker protection standard requiring health monitoring and
extensive personal protection equipment;
• strengthened certification and training requirements in most states and the adoption
of federal minimum standards for certification and training;
• a narrowly defeated Senate bill which would have required extensive monitoring of the
health of employees occupational^ exposed to toxic chemicals;
• a newly implemented regulation requiring drivers carrying hazardous substances to
carry commercial driver's licenses;
• proposed changes in pesticide labeling which should make them more readable for
applicators, yet create labels which will contain more detailed information than ever.
Employee health issues will undoubtedly increase the cost of doing business, and at the same
time make it increasingly difficult to find and train employees in an increasingly tight labor market.
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ENVIRONMENTAL CONCERNS
Numerous concerns for the environment will place further scrutiny on all pesticide applicators,
not just LCO's. Concern for the impact of pesticides on endangered species is leading to areas
where specific pesticides simply will not be allowed. Wildlife concerns have recently led to the
banning of diazinon on golf courses and sod farms. Problems with disposal of pesticide containers
and wastes (RCRA, Superfund) have led to volumes of regulation.
The "granddaddy" environmental concern for the next decade, however, is groundwater
contamination. As the EPA concludes its current survey of wells around the country, and more trace
amounts of pesticides are found in wells, more and more public misunderstanding, fear, regulation
and product loss and restriction are bound to impact pesticide applicators. LCO's can expect to
encounter more questions and concerns about their use of pesticides around public and private
sources of drinking water.
LEGAL ISSUES
Several legal issues are currently being debated as well. While some of these wouldn't seem
to have an immediate impact on the LCO, their long term impacts could be immense:
• The 1988 amendments to FIFRA (FIFRA 88) significantly expand ERA'S authority to
regulate recall, storage, transportation, and disposal of pesticides. The Agency must
exercise this authority by the study of all aspects of these issues, consultation with
affected and interested parties, and issuing of requirements for storage, transportation,
or disposal of a suspended or cancelled pesticide or its container, rinsates, or other
materials which may be contaminated with such a pesticide. These findings must be
submitted to Congress by December 1990. The new regulations will affect end users
to the extent that they are subject to recall procedures. Details of reporting requirements
will be announced in the Federal Register when they are developed.
• Under FIFRA 88 end users such as pesticide applicators will generally be indemnified
against the costs of disposing of cancelled or suspended pesticides.
• Applicator liability on issues such as ground water contamination is another issue that
was debated but not resolved in FIFRA 88. Farm groups are currently proposing that
their members be exempt from liability should they be able to show they used a pesticide
in accordance with all label directions. If this exemption is allowed, should it be extended
to the non-agricultural user as well?
• Private right of action, or the ability of a citizen to bring suit against an applicator for
pesticide misuse, another issue being debated, could change our thoughts on liability
forever.
• Local regulation of pesticides continues to be debated at the federal level as well as
within many states. Although applicators have won a few battles in the area, the war
is far from over. All pesticide users should easily understand the chaos that would be
created should the more than 88,000 local government entities in the United States
be given the authority to regulate pesticides.
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INDUSTRY/APPLICATOR RESPONSE
LCO's need to be more aware of the public's concerns over pesticides. Whether or not our use
of pesticides creates a hazard is often not the issue. The issue sometimes becomes the fact that
the public perceives a hazardl We must be willing to put ourselves in their shoes and imagine how
we would feel if we believed pesticides were a threat.
Industry's response to many pesticide issues in the past has not been adequate. It is time
industry becomes more proactive in terms of defending the legitimate and safe use of pesticides.
The public must be made more aware of pesticides' benefits; regulators and extension people
must be better educated on the professionalism which already exists within the lawn care industry;
and all of us must work towards reasonable pesticide public policy. Increasing regulation is headed
our way, and we must work hard to keep it reasonable.
The impact of lawn chemicals on ground water is a good example of where to start to educate
decision makers and the media. Research underway at numerous universities is finding that lawn
chemicals do NOT have the same potential to contaminate groundwater as pesticides applied
agriculturally. It is important that decision makers understand this when developing groundwater
protection strategies.
Alliances of pesticide users at the local, state and national levels need to be formed and to
become actively involved in pesticide policy formation. A few state alliances, as well as the national
Pesticide Public Policy Foundation, are already working toward this goal, but the job is immense
and much more work is needed. The opposition, the anti-pesticide forces, are well organized and
funded, and they network extremely well. Pesticide users need to rise up to face their challenge.
A major goal of the Pesticide Public Policy Foundation is to bring together an alliance of all
national urban pesticide user groups (lawn, tree, pest control, landscape, golf, right-of-way) and to
foster the formation and development of state-wide pesticide user alliances. Applicator alliances
must be formed rapidly and in as many states as possible to allow applicators to be heard on the
many important issues facing them today.
At the same time, LCO's need to do all they can to get their own house in order. Applicator
training requires the highest priority, and operations must be run squeaky clean. Applicators also
need to understand that they must adapt to many changes on the horizon such as IPM, new
application equipment, and new products which will change forever the pesticide application
business. LCO's definitely use less pesticide today than in the past, and this trend will continue.
The Professional Lawn Care Association of America is directing an increasing amount of its
resources to regulatory and legislative concerns. PLCAA's goal is to protect the right of their
members to apply pesticides safely, yet at the same time ensure adequate safeguards to protect
employees, customers and the environment.
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SOCIETAL PROBLEMS ASSOCIATED
WITH PESTICIDE USE
IN THE URBAN SECTOR
Anne R. Leslie
U.S. Environmental Protection Agency
Office of Pesticide Programs
Field Operations Division (H7506C)
401 M Street SW
Washington, DC 20460
The stage is set for spring in the Washington, D.C. metropoiitan area. Rows of forsythia paint
a golden backdrop to the ribbons of highway. The silhouettes of bare fruit tree branches glow with
color and then disappear in soft clouds of pink or white blossoms. The birds and squirrels compete
less for seeds around the feeder and more for each other's attention. Homeowners spend warm
days pruning, raking, digging, planting and fertilizing, as they try to realize the fragile dream of a
colorful flower garden framed by a deep green lawn.
Contained within these suburban gardens is a population of life forms which are indicted for
their ability to interfere with the achievement of the dream. My neighbor's yard of wheat colored
zoysia (whose golden color is prized in Japan) is punctuated with green clumps of wild garlic. This
plant is not as obvious amid my lawn of mixed fescue and bluegrass, cool season grasses which
green up earlier than zoysia or bermuda. Yesterday I dug some up to put in my salad as I pulled
out unwanted honeysuckle that was moving from its firm foothold on an old wire fence to take over
the yard, strangling a tree on the way.
In the lawn, a patch of bare earth piled up in mounds attests to activity of ants, and my neighbor
worries at seeing a rat in his garage. The pest control company arrives to set out bait-the neighbor
carries a contract with them to treat for termites, ants and roaches.
My yard has a patch of wild mustard, whose time of flowering is already past, and the seed
heads float above the lawn. Henbit displays tiny purple flowers from a patch of soil the grass
disdained to cover. Should we call a lawn care service, or visit the nursery or hardware store for
some broad-leaf weed killer to clean up the lawn and get rid of these pests-or is there another way?
The appearance of all these life forms is part of the natural ecology. They have found a
favorable niche to live in, and they are not concerned that it is the same niche we live in.
I would gladly pay for some sound advice on the alternatives for my half acre. Is a good lawn
the best choice? Will the henbit and mustard retreat to form a meadow transition to the neighboring
woods? I need to know what effort this will require.
What might I expect over a period of time if I just keep adding organic matter, adjusting the
soil pH as needed, and overseeding with a grass variety that is adapted to my site? The beneficial
spiders, earthworms and the bacteria in the grass thatch can then continue their roles in the system
without the effects of pesticide. And if a damaging level of a pest such as the Japanese beetle
appears, I might put my faith in introduction of their natural enemy, an entomophagous nematode.
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Hand digging of unwanted plants may be enough to control a lot my size. But if my yard were
larger, it would be prohibitively labor intensive. What if I let the grass grow to three inches instead
of one and one-half? The dandelions will have their spring show and be choked out later by the
healthy grass. Crabgrass is an annual. It has left its dead skeletons in patches where its seed can
sprout anew. But I can tip the scales in favor of a chosen variety of grass that may grow vigorously
and inhibit the crabgrass seedlings by shading them out.
The decisions I have to make are similar to those confronting many homeowners in the United
States. Because some homeowners lack time to manage their own lawns and lack first-hand
agronomic experience, choosing a lawn care service seems very attractive. Yet some sectors of
society are objecting to the choices made by others, particularly when a contracted service impinges
on a neighbor's property.
Problems Related to Pesticide Regulation
Environmental and citizen groups have collected information on pesticide use practices and
combined that information with potential health and environmental hazards of individual pesticides.
The public's concern over small amounts of chemicals in ground water is compounded by the lack
of real data on long-term health effects of low level exposure. Detection is now better than ever
because of the improved analytical methods developed by chemists in recent years. Testing for
health effects lags far behind technically. It is an expensive and long-term project, and the regulatory
process that requires and evaluates such studies is complicated and slow moving.
The federal government gives the states and local communities the ultimate responsibility to
control the way registered pesticides are used. Local governments may decide to notify the public
of pesticide use by posting areas being treated, and they draw up requirements for certification of
applicators. However, there are limitations on what these controls can accomplish in the urban area,
given the following facts:
Most pesticides applied to home lawns are not restricted to use only by a certified
applicator, and posting of private residences is not required.
Large rural areas are being rapidly converted to urban land uses, which pose new
problems that may require regulation. The regulatory agencies do not have the
manpower for enforcement of proper pesticide use by private citizens.
Turf is not considered an agricultural crop in some States, and, therefore, does not
receive as much research funding to determine the effects of its management on the
environment. However, it carries a definite economic value, which is used to justify the
application of pesticides in its management, even though a dollar value for an aesthetic
product is difficult to determine.
The very real problem of resistance to pesticides is appearing in insects, as shown in
the chapter by Metcalf; in weeds as detailed in a paper presented by LeBaron (ACS
Symposium Series, in press, 1988), and in fungus as noted in the chapter by
Dernoeden. Resistance buildup leads to use of increasing amounts of pesticide on turf,
just as on agricultural crops.
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Problems Related to Conflicts in Land Use
Conflict exists between people willing to pay for pesticides to achieve high quality turf on their
lawns and people not wanting to have pesticides on their property, or even nearby. And conflicts
exist over other kinds of land development.
Golf courses are a very visible expanse of highly managed turf. Projections of the increase in
the golfing population by the National Golf Foundation (Golf Projections 2000, Golf Summit '86
Research Presentations, October, 1986) call for the opening of one new course per day until the
year 2000. This represents a conservative 2% increase in this recreational land use. People who
have experienced hypersensitivity to pesticides raise objections based on the potential for drift
Environmentalists fight the conversion of wilderness areas and impacts of land development on
endangered species; cities blame the courses for pollution of their water supplies.
Studies on Water Pollution by Pesticides Used on Turf
For the most part, both sides argue from a minimal data base. Studies on groundwater pollution
in natural watersheds, with one exception, have not been carried out. EPA's well water survey
includes only agricultural land. The Cape Cod study carried out by EPA showed positive levels of
nitrogen and traces of pesticides. No similar sampling studies have been run in less permeable soils
than the sandy soil of the Cape. The studies by Gold and Sullivan, reported in chapter 13, include
the most targeted and complete information we have seen to date on waterborne transfer of
fertilizers on home lawns. Controlled studies on pesticides in runoff from turfgrass plots are reported
by Welterlen in chapter 14. Studies by Watschke at Penn State University, Niemczyk at Ohio State
University, and Petrovic at Cornell University substantiate the ability of thick turf to prevent or
minimize pesticide transfer to water. These studies are cited in the above chapters.
More significantly, ground and surface water pollution from runoff of paved areas may be the
largest urban source, since any chemical sprayed near or spilled on paving materials has great
potential to be carried to the watershed. Although pesticides are not deliberately applied in these
areas, they may arrive there carried by trucks, along with other chemicals such as gasoline, oil, dry
cleaning fluids, disinfectants, and structural pesticides. In short, anything that is spilled during
transport or accidental application. Many chemicals are not removed at most existing water
treatment facilities.
Few published studies on water pollution via runoff from paved areas have been reported,
although some companies are running determinations.
The greatest source of water pollution is application of chemicals to agricultural land. Concerns
over contamination of groundwater by pesticides applied to turfgrass are usually based on the
agricultural groundwater studies. Leaching through bare soil is much greater than through grass
and thatch, as shown in the chapter by Welterlen. Agricultural use of pesticides and fertilizers is still
much higher on a per acre basis than on golf courses, although limited areas of golf courses may
use a higher rate. Agriculture employs restricted pesticides which are generally not used on urban
turfgrass.
Direct Health Effects to Applicators and Residents
Pesticides registered for use on turfgrass and ornamentals carry labels indicating proper
handling, protective clothing requirements and disposal instructions. These are based on studies
required by EPA and carried out by the registrant. Restricted use pesticides are available only to
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certified applicators, whether commercial or private. Certification is awarded on evidence that the
applicator knows how to handle the material.
Although it is believed that current regulations adequately protect the applicator, such
regulations may not protect a resident of the treated site. Because nonagricultural use of these
pesticides has increased, EPA's Office of Pesticide Programs is re-examining current requirements
for studies of dislodgeable residues. There is potential for exposure to residents "reentering"the
lawn after treatment. These residents may include a highly vulnerable segment of the
population-either directly, as with children playing on the lawn or indirectly with pets or applicator
clothing coming into the household.
Landowners' Rights versus Society Benefits:
Need for Land Use Planning
Health and environmental effects of turf pesticides are often cited in disputes over urban
development. But the concerns have not always led to productive solutions. The societal issues are
outside the scope of this book. However turfgrass managers who practice more sophisticated
pesticide use through an IPM program will be making a positive step towards resolution.
Cities grappling with such issues need comparative data on the impact of all land development
alternatives to decide on the land use of greatest benefit to society. All residents must keep in mind
that urbanization is taking place regardless of individual preference, and wise planning needs to
be done early to avoid the problems many cities now face.
Limitations of Pesticides and the Need for Realistic Goals
At the other end of the scale, homeowners are often led to expect they can obtain golf course
quality turf solely through greater use of pesticides. And because they lack agronomic experience,
they do not use cultural practices that can support reasonably high quality lawns. With increasing
demands for perfect turf, the cost of chemical use and maintenance of a lawn escalates significantly.
Just as a cockroach inside the home incites much greater urge for chemical control than do
most outdoor "bugs,"a dandelion on a home lawn may incite a desire for pesticide use that would
not be expressed for the same pest density in a park.
In a National Park Service project, stands of grass with different levels of weed infestation
were to be evaluated by people to determine their perception of the grass quality. No satisfactory
scale has yet been established.
Societal conflicts have evolved from urbanization of former agricultural land. Where
development leads to increased pesticide use, land use planners need to consider long-term
consequences. An IPM program can help greatly to reduce these potential consequences.
Education of the public in basic agronomic practices and environmental fate of chemicals can
contribute greatly to their intelligent decision-making for land use, management goals and
conservation of resources. The remainder of this book is devoted to examining some of the best
methods and putting them together in a concerted IPM program.
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\
SECTION II
Benefits of an
Integrated Pest Management
Approach to Turfgrass and Ornamentals
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URBAN INTEGRATED PEST MANAGEMENT EDUCATION
AND IMPLEMENTATION:
IMPLICATIONS FOR THE FUTURE
W. M. Brown, Jr.
and
W. Cranshaw
Colorado State University
Fort Collins, CO 80523
and
C. Rasmussen-Dykes
Jefferson County Cooperative Extension
Golden, CO 80401
Integrated pest management (IPM) programs are underway for many agricultural commodities.
In contrast, few IPM programs are established in urban environments. The reasons for the lack of
functional urban IPM programs vary, but two significant reasons emerge:
• the lack of technology and programs to address the wide variety of plants, cultural
practices and pests encountered in the urban habitat;
• the lack of consistent research and development support for urban programs in pest
management.
This is paradoxical, considering that in 1982 a national Extension Committee on Policy (ECOP)
reported that 7.5% of the total pesticide used in the United States is used by homeowners. An
additional 19.4% is used by urban government and industry (7). Thus, a total of almost 27% of the
pesticides used in the United States are used in our densest population areas, and by predominantly
untrained pesticide users. Concern over pesticide use has triggered right-to-know and pesticide
posting ordinances in several communities in recent years. In Colorado, the city of Boulder recently
voted to establish a pre- and post- pesticide posting ordinance covering lawn spraying. Frequently
anti-pesticide advocates promote "IPM" as a blanket alternative to pesticide use without actually
being fully aware of the lack of a research and implementation base in urban IPM. Therefore, a
critical need exists for comprehensive national urban IPM education, research and program
development. A pilot urban IPM educational and field program has been developed in Colorado and
is described in the following pages.
DISEASE MANAGEMENT
Under good cultural practices, Colorado has few turf and ornamental disease problems. The
problems encountered are frequently in stress situations resulting from unrealistic design, poor
management, intensive use (i.e., golf courses with night watering and heavy traffic), home lawns
with poor site preparation, high nitrogen and excessive pesticide applications or ornamentals
planted in inappropriate sites.
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An exception are the Pythium blight diseases caused by E aphanidermatum. E. ultimum. E
myriotylum. and E torulcsum. all reported pathogens on turfgrass (15) that have been associated
with disease outbreaks in Colorado (13,14).
Little work has been done on biological control of turf diseases. Trials using a known
mycoparasite of Pythium spp., a benomyl tolerant mutant of Trichoderma harzianum (T95) (3,4,5)
and a systemic fungicide specific for Pythiaceous fungi, metalaxyl, were carried out at Colorado
State University and at field sites in Colorado. Tests were conducted on all the above Pythium spp.
found associated with blighted turf in Colorado (13,14).
Each Pythium spp. was parasitized by T harzianum in vitro in much the same manner as
described by Chet et al. (6). Trichoderma hyphae coiled around Pythium hyphae and the latter
collapsed (Fig. 1). Low concentrations (25-200 ppm) of metalaxyl significantly retarded mycelial
growth of Pythium spp. (Fig. 2). Equal concentrations of metalaxyl did not affect mycelial growth
and spore production of T harzianum. although higher concentrations (275-2500 ppm) did (Figs.
3,4). Trichoderma spores produced on media at 750 ppm metalaxyl when streaked onto
non-amended PDA media were viable.
Additional studies showed that other pesticides frequently used in turf disease management
(benomyl, chloroneb, diazinon, Trimec, phenyl-mercuric acetate+thiram and iprodione) did not
significantly affect the population of T. harzianum (Fig. 5)(13).
Work at Colorado State University by Ahmad and Baker (1) has demonstrated that rhizosphere
competent mutants are more efficient in colonizing and subsequently protecting roots from infection.
In addition to suppression of disease causing organisms, T95 also has demonstrated growth
enhancement properties in bluegrass in the absence of known pathogenic organisms, Fig 6
(5,13,14,17). The mechanism responsible for growth enhancement by Trichoderma is not fully
understood (17). The attraction of a biological control agent that is also compatible with fungicides
and provides growth enhancement even in the absence of disease is exciting and more research
must be initiated in this area.
A fluorescent pseudomonad, used as a biocontrol agent, was effective in control of take-all of
Kentucky bluegrass, caused by Gaeumanoyces graminis. Figure 7 shows the effect on bluegrass
growth in pots infested with the take-all fungus. Similar effects of fluorescent pseudomonads on
wheat take-all organism, Gaumanomyces tritici have been reported by Baker, Cook and others (2,
18, 19).
While more work must be done to develop fully integrated Pythium blight or other turf disease
control programs with combined chemical and biological components, the prospect is exciting.
These components must now be field-tested using commercial turf management practices, and
appropriate ways must be developed to deliver Trichoderma or other biocontrol organisms.
INSECT MANAGEMENT
Many of the insect and mite problems common in urban plantings in Colorado are unique to
the region and have not been studied in depth. Lack of information on life history of these pests,
their management and injury potential has significantly contributed to misunderstandings regarding
appropriate controls and the damage assessments. This lack of information has resulted in
excessive or inappropriate pesticide usage habits that are incompatible with IPM strategies.
Consequently, a fundamental research effort at Colorado State University (C.S.U.) has been to
improve our understanding of regional pest species biology and habits and to convey this information
through Cooperative Extension outlets.
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Concurrently, insect management research studies have been conducted to develop effective
IPM technologies. Summaries of recent efforts and future needs are outlined below:
TUrf.
Major emphasis has been to develop insect parasitic nematodes as biological control agents
for thatch and soil infesting insect turf pests. White grubs in the genera Cyclocephala. Phyllophaga.
and Polyphylla have been successfully controlled in our field trials at rates of control equivalent or
sometimes superior to most standard insecticide treatments. In particular, the nematode genus
Heterorhabditis (heliothidis. 'H.p. 88') has been effective in white grub control. Nematodes in the
more commonly commercially available genera Neoaplectana (primarily N, carpocapsae) have
been less effective for white grub control but have shown potential against other common turf pests
such as sod webworms, cutworms, and billbugs (8).
Effectiveness of nematodes against soil insects has been shown by other researchers (8,16)
to be influenced by factors such as soil type and moisture. In C.S.U. studies the importance of thatch
as a barrier to nematode movement has been quantified. Of all the insect parasitic nematodes
studied, only a small percentage of them (8-17%) were able to penetrate through a 1.5 cm thatch
barrier layer. The ability of different strains and species to penetrate thatch varied; Heterorhabditis
proved the species most inhibited by thatch. Trying to "flush"nematodes through thatch with varying
water volumes was ineffective. It is obvious that thatch management will be important in effective
use of insect parasitic nematodes as well as insecticides for soil insect control. Fortunately, insect
parasitic nematodes do not adversely affect earthworms, the most important organisms involved
in organic matter breakdown in turf. Impacts of nematodes on other non-target pest species are in
progress.
Insect parasitic nematodes have also been screened for compatibility with various turfgrass
management chemicals. Soaps and wetting agents appear fully compatible with nematode
applications as are most fertilizers (16). Fungicides, with the notable exception of the mercurials,
show no toxic effects to nematodes. However, mercurial fungicides are devastating to nematodes
and prior use of these compounds may preclude adequate survival of insect parasitic nematodes
at a turf site. Tested insecticides (11) show a range of effects on insect parasitic nematodes with
the toxicity potential ranging chlorpyrifos, bendiocarb, carbaryl, diazinon. However, nematode
species sensitivity to various compounds varies. For example chlorpyrifos is highly toxic to
Heterorhabditis but only moderately toxic to Neoaplectana: carbaryl only showed toxic effects to
Neoaplectana.
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TABLE 1
Summarized results of white grub control with insect parasitic nematodes and Lawn Aerator Sandals
in Colorado State University trials, 1986-1987.
Trial Location Target Pest Treatment
% Control
Lamar, CO
57 Phyllophage. Diazinon 14G
55 Polyphylla Lawn Aerator Sandals
48 H. heliothidis
33 N. carpocapsae
Pueblo, CO
94 Cyclocephala Oftanol 2
47 N. carpocapsae
45 H.-H.P.88"
Grand Junction, CO
0 Cyclocephala
N. carpocapsae
Simple cultural controls also appear to have potential in managing regional turf problems. A
1986 study evaluated the use of a spiked sandal, sold under the trade name "Lawn Aerator Sandal"
for white grub control. Merely walking across plots with this product achieved a level of control
(approximately 50%) comparable to that of the insecticide (diazinon) standard (Table 1). Other
studies are demonstrating that adequate winter watering, a neglected turf maintenance procedure
in the arid West, can greatly limit turf injury by clover mites and sod webworms.
Woody plants.
Spraying trees and shrubs has become a particularly visible and controversial use of
insecticides in urban areas. Technologies to limit these treatments have proceeded along the
following approaches.
Expanded trials developing the use of soil injected systemic insecticides was emphasized in
1987. These treatments involve the use of specialized equipment that rapidly injects the insecticides
into the soil for subsequent root uptake, thus avoiding drift and many non-target problems.
Oxydemetonmethyl (Metasystox-R) is fully labelled for this use and has shown promising levels of
control against aphids, psyllids and mites (Table 2). Unfortunately control of leaf chewing insects
(beetle larvae, tip moths, gall midges) with this product has been erratic. An alternative soil systemic
treatment with great potential is dimethoate. Dimethoate is effective against a very wide spectrum
of woody plant pests. Expanded use of this material is pending labelling developments.
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TABLE 2
Summary of Colorado State University control trial results using soil applied systemic insecticides,
1984-1987.
Target Pest
Honeylocust pod gall midge
Honeylocust pod gall midge
Honeylocust spider mite
Honeylocust plant bug
Honeylocust rust mite
Honeysuckle aphid
Ash leaf curl aphid
Pinyon spindle gall midge
Pinyon tip moth
Hackberry nipple gall
Hackberry bud gall
Elm leaf beetle
Insecticide
Metasystox-R
DiSyston
Metasystox-R
Metasystox-R
Metasystox-R
Metasystox-R
Cygon/Dimethoate
Metasystox-R
Metasystox-R
Cygon/Dimethoate
Metasystox-R
Cygon/Dimethoate
Metasystox-R
Metasystox-R
Cygon/Dimethoate
Metasystox-R
Degree of Control
Fair-Good
Poor
Excellent
Poor
Fair-Poor
Excellent
Excellent
Excellent
Fair-Poor
Excellent
Good
Excellent
Good
Poor
Good
Poor
Various "softlnsecticide treatments also show potential for greatly expanded use in landscape
plant care. Insecticidal soaps are routinely incorporated into CSU trials and have shown fair to good
potential for control of spider mites, eriophyid mites, plant bugs, leafhoppers, and some aphids.
More recently, interest has focused on the horticultural oils for summer foliage uses. These refined
specialty oils appear to be greatly under-utilized at present. Researchers in other areas of the
country have shown an exceptional level of effectiveness of these products against young scales
and whiteflies in foliar applications. C.S.U. trials established efficacy against eriophyid mites and
spider mites.
Elm leaf beetle treatment, the most common insecticide application made to trees in southern
Colorado, demonstrates how several potential alternatives may be developed. Use of insecticide
spot treatment to trunk bands was shown in 1984 studies to be highly effective at controlling larvae
as they move to the tree base to pupate. A number of community spray programs have since
successfully adopted area-wide trunk band applications with a dramatic reduction in insecticide
usage and drift. In addition, new control products are in advanced development. The biological
control Bacillus thuringiensis 'San Diego' shows activity against elm leaf beetle larvae and may be
marketed in 1989. Summer spray oils also were effective in preliminary 1987 studies.
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EDUCATION AND TRAINING
A major thrust of the Colorado urban IPM program is to expand information sources and
delivery. This recognizes that lack of information on proper pest management methods leads to
inappropriate pesticide use. Instruction in diagnosis, damage evaluation, timing of treatments, and
effective pesticide alternatives can produce reductions in inappropriate preventive or "revenge"
treatments. IPM education was especially given a high priority in the 1981 ECOP report on urban
IPM (7). Additionally, increasing public awareness of ecological implications of pesticide use can
promote more thoughtful considerations prior to and during urban pesticide applications.
Expanded IPM education is receiving major emphasis in the Colorado program. Colorado
Cooperative Extension education activities are targeting three distinct audiences: turf and landscape
maintenance professionals, homeowners, and youth.
Colorado State University IPM specialists carry on extensive workshops, field days and field
experiment/demonstrations with parks and recreation, professional lawn care and golf course
personnel. Over 1,000 turf professionals receive IPM training and updating each year. An additional
500-600 commercial landscapers, nurserymen, urban foresters and other urban pest management
professionals also benefit from IPM training sessions. In addition to actual organized training,
Colorado State entomologists and plant pathologists routinely offer informal on-site training through
cooperative field trials, demonstrations, and visits.
A major emphasis has been made to update and develop new materials on regional urban
insect management problems. In particular, publications outlining the proper use of insecticidal
soaps, Bacillus thuringiensis. pheromones and spray oils for regional problems have been popular
and distributed widely. Aides for identification of beneficial insect species and references in proper
use of commercially available biological controls have also been well received.
For example, an atypical Extension publication drawing considerable interest from youth and
adult audiences promotes "butterfly gardening". Implied in "butterfly gardening" is the careful use of
pesticides, further assisting in improving pesticide use habits among urban audiences. By
emphasizing and valuing an overlooked beneficial group of common insects this publication has
directly assisted overall IPM efforts.
The Cooperative Extension Master Gardener program promotes appropriate IPM strategies
for urban situations. Over 10,000 volunteer Master Gardeners have received IPM training and serve
as Cooperative Extension paraprofessionals in Colorado urban communities (Fig. 8). For example,
in 1986 in Boulder County, Master Gardeners fielded over 6,704 client queries. In Jefferson County
(western Denver Metro area), 106 Master Gardener volunteers worked over 3,000 hours. Their
impact in providing educational service to the wider community is outstanding (Table 3). Many of
the Master Gardeners stay with the program and serve as volunteer leaders or in other, more
advanced program capacities.
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TABLE 3
Jefferson County* 1986 Master Gardener Accomplishments
Master Gardener's Trained/Used 106
Volunteer Hours Worked 3-000+
Plant Specimens Examined 1-082
Telephone Queries Answered 14,000+
* West Denver, CO, and adjacent foothill rural areas.
CSU IPM staff developed a special youth educational program, "THE BUG SHOW" using large
insect and vegetable hand puppets (Fig 9). Use of large hand puppets have increased elementary
school students attention and awareness (10). A pilot program consisting of a 15-minute skit
followed by a question and answer period was begun in 1987. Advanced Master Gardeners (those
who have received two or more years of in-depth Master Gardener training in horticulture and IPM)
were trained as puppeteers. CSU Cooperative Extension staff and Master Gardeners have
presented the pilot program to 350 youth (pre-school through third grade) in the Denver Metro area.
This program gives youth an introduction to biology, biological control and pesticide safety. After
the program, teachers and students use CSU prepared activity booklets as supplemental in-class
or at-home study material. Under development is a follow-up video presenting selected information
on biology, pesticide safety, and IPM; each teacher will be provided a copy for further class use and
study.
Information dissemination systems using technical sheets, radio shows, weekly newsletters,
and a special Cooperative Extension pre-recorded phone Teletips weekly Urban Pest Alert are all
operational. The Teletips system uses three-minute pre-recorded tapes to provide current pest
occurrence and management updates. Pest Alert tapes are updated weekly or more frequently if
necessary.
FUTURE IMPLICATIONS
While there is a critical need for development and implementation of urban IPM, major problems
exist.
There is very little plant pest research in urban IPM. Without a strong commodity support base,
little financial support is available for urban IPM research. Minimal available funds are generally
attached to chemical research. Thus, biological and cultural control approaches receive less
attention.
There is a government trend to decrease Cooperative Extension in the cities. This is
demonstrated in both federal budgets (i.e., Reagan Administration FY 87) and in many state budgets
such as Colorado's 1987 and 1988, budgets in which decreases have specifically targeted urban
programs. The critical nature of pest management education and research in urban IPM and its
components must gain recognition, if environmentally sensitive urban programs are to be
developed.
Present laws and confusion between various governmental agencies as to testing of biological
control organisms in the environment must be clarified; provisions must be made for testing. Much
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of the work to be accomplished in development of biological control is done and will be done by
universities and public agencies. To date there is not enough public funding for this essential
research and development.
CONCLUSION
Technology is available that can be adapted to urban IPM programs in turf and ornamentals.
Much more is needed to provide a base for comprehensive urban IPM success. Without adequate
funding, recognition and general education, successful implementation of IPM strategies to urban
situations and the resultant use of pesticide alternatives will not be realized. This has long range,
negative implications for both urban and farm populations.
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LITERATURE CITED
1. Ahmad, U.S., and R. Baker. 1987. Competitive saprophytic ability and cellulolytic activity of rhizosphere-competent
mutants of Trichoderma harzianum. Phytopath. 77:358-362.
2. Baker, K.F. and R.J. Cook. 1982. Biological control of plant pathogens. Amer. Phytopath. Soc., St. Paul, MN. 433 pp.
3. Baker, Ralph. 1985. Biological control of plant pathogens: definitions. Pages 25-39 in: Biological Control in Agricultural
IPM Systems. M.A. Hoy and D.C. Herzog, eds. Academic Press, NY. 600 pp.
4. . 1986. Biological control: an overview. Canadian Journal of Plant Pathology 8:218-221.
5. . 1987. Enhancing the activity of biological control agents. Pages 1-17 from Innovative Approaches to
Plant Disease Control. I. Chet, ed. Wiley and Sons, NY.
6. Chet, I., G.E. Harman, and R. Baker. 1981. Trichoderma hamatum: Its hyphal interactions with Rhizoctonia solani
andPythium spp. Microb. Ecol. 7:29-38.
7. Evans, Burton R., ed. 1981. Urban Integrated Pest Management Programs for State Cooperative Extension Services.
A Report for the Extension Committee on Organization and Policy. Cooperative Extension, Univ. of Georgia,
Athens, Georgia, 30602, 20 pp.
8. Gaugler, R. 1981. Biological control potential of Neoaplectana nematodes. J. Nematol. 13:241-249.
9. Georgis, R. and G.O. Poinar. 1983. Effect of soil texture on the distribution and infectivity of Neoaplectana carpocapsae
(Nematoda: Steinernematidae). J. Nematol. 15:308-
10. Gilfoyle, E.M., and J.A. Gliner. 1985. Attitudes toward handicapped children: Impact of an educational program.
Physiol. and Occupational Therapy in Pediatrics 5:27-41. Haworth Press, NY.
11. Hara, A.H. and J.K. Kaya. 1982. Effects of selected insecticides and nematicides on the in vitro development of the
entomogenous nematode, Neoaplectana carpocapsae. J. Nematol. 14:486-491.
12. Rao, P.S.P., P.K. Das, and G.Padhi. 1975. Note on compatibility of DD-136 (Neoaplectana dutkyi). an insect parasitic
nematode with some insecticides and fertilizers. Indian J. Agric. Sci. 45:275-277.
13. Rasmussen-Dykes, C. 1983. Developing an integrated control program for Pythium blight of turfgrass. M. Sc. Thesis.
Colo. State Univ., Fort Collins, CO. 73pp.
14. , and W.M. Brown, Jr.. 1982. Integrated control of Pythium blight on turf using metalaxyl and
Trichoderma hamatum. Phytopath. 72:975.
15. Saladini, J.L.. 1979. Cool versus warm season Pythium blight and other related Pythium problems. Pages 37-39 in:
Advances in Turfgrass Pathology. P.O. Larsen and B.G. Joyner, eds. Harcourt Brace Jovanovich, Inc. Duluth,
MN. 197pp.
16. Schroeder, W.J. and J.B. Beavers. 1987. Movement of entomogenous nematodes of the families Heterorhabditidae
and Steinernematidae in soil. J. Nematol. 19:257-259.
17. Windham, M.T., Y. Elad, and R. Baker. 1986. A mechanism for increased plant growth induced by Trichoderma spp.
Phytopath. 76:518-521.
18. Wong, P.T.W., and R. Baker. 1984. Suppression of wheat Take-all and Ophiobolus patch fluorescent pseudomonads
from a Fusarium-suppressive soil. Soil Biol. Biochem. 16:397-403.
19. t c. Rasmussen-Dykes, I.E. Perotti and W. M. Brown, Jr. 1982. Occurrence of Ophiobolus patch of
turf in Colorado. Phytopath. 72:976.
65
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LIST OF FIGURES
Figure 1. Trichoderma harzianum isolate T95 coiled around Pythium spp. showing the collapsed
parasitized condition of the latter.
Figure 2. Effect of metalaxyl at varying concentrations on mycelial growth of Pythium spp.
Figure 3. Effect of metalaxyl at varying concentrations on myelial growth of Trichoderma
harzianum isolate T95.
Figure 4. Effect of metalaxyl at varying concentrations on spore production of Trichoderma
harzianum isolate T95.
Figure 5. Recovery of Trichoderma harzianum isolate T95 after various fungicide treatments.
Figure 6. Kentucky bluegrass at left untreated, plants at right treated with Trichoderma harzianum
isolate T95.
Figure 7. Kentucky bluegrass plants in pots from left to right, pots infested with Gaeumannomyces
graminis. G. graminis plus a fluorescent pseudomonad, and uninfested check.
Figure 8. Colorado master gardener class observing solar treatment of soil trials.
Figure 9. Cindy Rasmussen-Dykes with children and bug puppets used for childrens education
IPM programs.
66
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FIGURE 1
Trichoderma harzianum isolate T95 coiled around Pythium spp. showing the collapsed parasitized
condition of the latter.
67
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FIGURE 2
Effect of metalaxyl at varying concentrations on mycelial growth of Pythium spp.
ou
? 25
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«.«
. r . «
'/.'
XV
^
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25 50 100
Metalaxyl (jug/ml)
68
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FIGURE 3
Effect of metalaxyl at varying concentrations on myelial growth of Trichoderma harzianum isolate
T95.
25 50 100 150 187 375 625 750 1250 2500
Metalaxyl (jug/ml)
69
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FIGURE 4
Effect of metalaxyl at varying concentrations on spore production of Trichoderma harzianum isolate
T95.
20
16
o
x 12
1
£ 8
o
I I I I I I III
i iiii
i • •
0 25 50 100 150 187 375 625 750 1250 2500
Metalaxyl (jug/ml)
70
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FIGURE 5
Recovery of Trichoderma harzianum isolate T95 after various fungicide treatments.
35
30
ro
Q 25
X
*O
10 20
CP
15
CP
o
10
0
71
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FIGURE 6
Kentucky bluegrass at left untreated, plants at right treated with Trichoderma harzianum isolate T95.
72
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FIGURE 7
Kentucky bluegrass plants in pots from left to right, pots infested with Gaeumannomyces graminis.
(L graminis plus a fluorescent pseudomonad, and uninfested check.
73
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FIGURE 8
Colorado master gardener class observing solar treatment of soil trials.
74
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FIGURE 9
Cindy Rasmussen-Dykes with children and bug puppets used for childrens education IPM programs.
75
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76
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EDUCATIONAL, ENVIRONMENTAL, AND ECONOMIC
IMPACTS OF INTEGRATED PEST MANAGEMENT
PROGRAMS FOR LANDSCAPE PLANTS
by
Michael J. Raupp, Mildred F. Smith and John A. Davidson
Department of Entomology
University of Maryland
College Park, MD 20742
A landscape plant management pilot program was initiated in 1978 by extension specialists
in the Department of Entomology, in cooperation with a county agent and a community of suburban
Maryland homeowners. The objectives of the program were twofold. The first objective was to
demonstrate the feasibility of the integrated pest management approach for managing landscape
plants. As part of this approach, participating homeowners received regular monitoring of pest
activity by a trained scout. The scout prepared a report that was reviewed by extension personnel.
Management recommendations were sent to each cooperator via a weekly or biweekly newsletter.
In addition to specific management recommendations, homeowners received timely extension
literature on the life cycles and control of insects and diseases, cultural plant care, pest identification
and proper pesticide use. As an educational program, the project provided homeowners with
information that would allow them to deal with their plant problems more effectively. The second
objective was to quantify changes in knowledge, attitudes, skills, and practices brought about by
the program.
The program expanded from about 20 homeowners in the initial year (1978) to 100
homeowners in its final year (1982). At the conclusion of the 1982 program, a comprehensive
evaluation was conducted. The program was evaluated by two methods, a survey of program
participants and a group comparison between participants and their non-participating neighbors.
Analyses were based on the 59 participants and 47 of their non-participating neighbors. Both survey
techniques indicated substantial changes in knowledge, attitudes, skills, practices, and end results.
Table 1 summarizes some of the changes detected by the survey of program participants.
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TABLE 1
Changes Brought About by an IPM Program for Landscape Plants
Response (%)
Impact Increase No Change Decrease
Identify ornamental plants 58 42 0
Inspect plants for problems 58 40 2
Recognize agents causing problems 75 25 0
Select the correct chemical control 75 25 0
Apply the chemical at the proper time 66 32 2
Use controls other than chemicals 53 47 0
Substitute alternatives for chemicals 45 52 3
Knowledge of cultural plant care 78 22 0
Deal effectively with plant problems 83 15 2
In addition to the changes summarized in Table 1, other changes were quantified. Ninety-seven
percent of participants believed that the information received would be useful in future years and
81% thought this approach would save money on pest control in the long run (the average estimated
savings was $53 per year). Furthermore, 93% felt the program was worthwhile and 98% believe it,
or a similar one, should be conducted in the future. Program participants said that they followed
extension recommendations about 71% of the time and were satisfied with their results 81% of the
time.
In the area of pesticide application, participants and their non-participating neighbors were
asked to select the best means of controlling aphids. Possible choices included insecticide,
fungicide, miticide, and soapy water sprays and ladybird beetles. Responses of participants differed
significantly from those of non-participants. The majority of non-participants selected insecticides
as the control method of choice while cooperators selected insecticidal soaps most frequently. This
difference undoubtedly resulted because participants were informed that insecticidal soaps provided
good control of aphids and were an environmentally preferred alternative to insecticides.
Homeowners were asked the same question regarding the control of mites. Non-participating
homeowners chose insecticides as the preferred control tactic while participants selected
insecticidal soaps and miticides most frequently. This difference is especially important because
many insecticides provide little, or no, control of mites. An additional finding of interest was that 15%
of the non-participants said that they had received helpful pest management information from
neighbors who had participated in the program.
The final phase of homeowner program evaluation was conducted in 1985 when approximately
330 former program participants were sent a questionnaire through the mail. Ninety-eight
homeowners returned the questionnaire. Of these, 71% indicated that they still used information
from the program. This compares very favorably with other surveys of information sources used by
homeowners. In 1979, Barrows et al. found that only 17% of gardeners surveyed used information
from the local Cooperative Extension Service. A national survey of homeowners conducted by the
Nursery Marketing Council (1983) revealed only about 16% using agents, universities, and
78
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governments as a primary information source. Several uses of information are summarized in Table
2.
TABLE 2
Information Use by Former IPM Program Participants
Use
Recognize cause of problem
Decide if control is needed
Select proper control
Apply controls at proper time
Use pesticides safely
Continue to Use
85%
84%
84%
84%
78%
Never Use
15%
16%
16%
16%
22%
In addition to these results, 48% of those responding believed this information had helped prevent
plants from dying.
Community managers and grounds maintenance supervisors face problems similar to those
of homeowners with respect to the types of pests affecting their landscape plants. A demonstration
project was conducted within a city of 27,000 people in 1983 and 1984. The demonstration project
in 1983 placed 354 acres inhabited by 1,661 residents under IPM management. In 1984, the
program was expanded to 476 acres, occupied by 3,844 people. Over the two years of the program,
pesticide sprays were reduced by an average of 83% and the overall cost associated with pest
management was reduced by 22% on the average. In 1985, the program was transferred to a private
consultant employed by the city. The program expanded to seven communities. Environmental
impact data is unavailable for the program conducted by the consultant; however, economic
information indicates that costs continued to be reduced under the IPM approach (Table 3). The
average total cost reduction resulting from the adoption of IPM ranged from $4.8 to 21.7/acre. The
mean savings realized was $12.9/acre + 3.99 (standard error).
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TABLE 3
Economic Assessment of Traditional and IPM Programs in Three Communities
Community Cost Acres Cost Reductions $/Acre
1982a 1983b 1984b 1985C 1983 1984 1985
1 2895 784 822 210 131 16.1 15.8 20.5
2 3750 1663 2986 420 56 37.3 13.6 59.5
3 1325 510 401 0 17 47.9 54.4 77.9
Pesticide Total 7970 2957 4209 630 204 24.6 18.4 36.0
Labor Total 0 2505 2779 2920
Total 7970 5462 6988 3550 12.3 4.8 21.7
a. 1982 — Traditional management program, including cover spray,
no monitoring.
b. 1983, 1984 — IPM management program conducted by Cooperative
Extension Service as a demonstration.
c. 1985 — IPM management program conducted by private consultant.
The success of the landscape plant management programs for homeowners and communities
prompted extension specialists in entomology to undertake a demonstration project with a
commercial arborist. The objective of this program was to demonstrate that an arborist could provide
the same approach for managing pests as did the extension based IPM programs. This was a critical
step in transferring technology to the commercial sector.
The program demonstrated the feasibility of the IPM approach conducted in the commercial
sector. Furthermore, it demonstrated that an arborist could reduce unnecessary pesticide use by
94% while maintaining a high level of customer satisfaction with the program. Seventy-eight percent
of the clients said they preferred the IPM approach to traditional cover sprays.
Part of the effort to continue the transfer of IPM technology to the commercial sector has been
an intensive training program. One component of this training has been a technical conference held
each winter at the University of Maryland. This interdisciplinary conference, called the Interstate
Ornamental Plant Management Conference, features nationally recognized plant management
experts from the disciplines of entomology, pathology, agronomy, weed science, botany,
horticulture, and the green industry. In its first three years, this conference has provided training to
more than 700 businessmen, government workers, and extension personnel. Ninety-six percent of
the attendees at the 1985 conference rated the overall quality of the 20 presentations as satisfactory
or excellent.
Other training activities include in-depth workshops conducted over several days during the
winters of 1984 and 1985. These workshops focused on interdisciplinary approaches of pest
management and were limited to approximately 30 participants each year. To determine how IPM
information was being implemented by former workshop attendees, a telephone survey was
conducted during the winter of 1986. The study group consisted of former program participants and
a group of Maryland arborists selected at random. Both groups were asked questions designed to
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reveal their pest management practices. One of the major impacts of the IPM approach is a reduction
in unnecessary pesticide use. When asked if their pesticide spraying had declined in the last ten
years, 83% of program participants were spraying less. Sixty-seven percent of non-participating
arborists were also spraying less. Not only did program participants spray less, but the materials
sprayed were more environmentally acceptable. Pesticides may be categorized according to toxicity
and environmental persistence. Pesticides such as horticultural oils, insecticidal soaps, and the
insect pathogen Bacillus thuringiensis (Bt) are considered biorational insecticides due to their low
toxicity to vertebrates and short environmental persistance. Insecticides used by workshop
attendees were compared to ones used by arborists that had not participated in workshops.
Arborists that had received IPM training were significantly more likely to use biorational insecticides
(Table 4). Furthermore, former program participants were the only ones to suggest non-chemical
controls for pests.
TABLE 4
Control Tactics Used by Arborists for Controlling Insect Pests
Pest
Aphids
Caterpillars
Scales
Spider Mites
Attended IPM
Workshop
Yes
No
Yes
No
Yes
No
Yes
No
Control Method (%)
Non-chemical
11
0
4
0
0
0
6
0
Synthetic
Biorational Organic
28
6
29
7
78
47
35
8
61
94
67
93
22
53
59
92
A second critical component of any IPM program for landscape plants is the regular inspection
of the plants for problems caused by pests or improper culture. Eighty-five percent of the firms that
attended workshops employed at least one person whose primary responsibility was plant
inspection. This contrasts with arborists that had not attended workshops. Only half of these firms
employed plant inspectors. To be effective, monitoring must be performed on a regular, short-term
basis. This means a minimum of ten, or more, visits per growing season. A comparison of the
frequency of inspections by program participants and non-participants revealed that 57% of the
participating arborists conduct ten, or more, regular inspections compared to only 20% of the
arborists that did not attend IPM workshops.
In summary, the demonstration programs have had the following results. First, they have
conclusively demonstrated the feasibility of implementing IPM technologies in non-traditional
settings, such as landscapes. Moreover, they have demonstrated that persons other than farmers,
or farm consultants, can implement IPM programs. This group includes homeowners, grounds
maintenance personnel, and commercial arborists. As educational activities, these programs have
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succeeded in changing knowledge, attitudes, skills, and practices of information recipients. These
changes have had the following economic and environmental impacts. They have reduced the cost
of pest control. The documented savings in the community-based IPM programs averaged
$12.9/acre. More important than the economic impacts are the environmental ones. Documented
reductions in pesticide use in the arborist demonstration program averaged 73 gallons (dilute)/acre.
These studies clearly indicate that IPM technologies have tremendous potential benefits for urban
clientele.
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LITERATURE CITED
Barrows, E.M., J.S. DeFilippo, and M. Tavallali, 1983.Urban community gardener knowledge of arthropods in vegetable
gardens in Washington, D.C.. lo: G.W. Frankie and C.S. Koehler (eds) Urban Entomology: Interdisciplinary
Perspectives, pp. 107-126
Nursery Marketing Council, 1983. Nursery Consumer Profile. 230 Southern Bldg., Washington, D.C. 20005.
83
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INTEGRATED PEST MANAGEMENT
IN THE GOLF COURSE INDUSTRY:
A CASE STUDY AND SOME GENERAL CONSIDERATIONS
Zachary Grant
Formerly Manager of Government Relations
Golf Course Superintendents Association of America
1617 St. Andrews Drive
Lawrence, KS 66046
Building a golf course in the late 1980's involves challenges beyond architecture, engineering,
finances and the demands of the game. In many states, developers of a course must also overcome
forbidding legal and regulatory barriers related to zoning, planning and environmental protection.
One of the most challenging of those regulatory obstacles is Vermont's Act 250 development
law, which requires that proposed developments meet a series of ten separate tests to obtain a
land use permit. These tests, administered by an independent environmental commission, range
from effect on water quality to infrastructure demands to aesthetic value.
For the past four years, Act 250 compliance has been the aim of developers of the proposed
Sherman Hollow golf course, planned for construction near Burlington, Vermont. Along the way, the
Sherman Hollow management team has demonstrated exemplary concern for environmental
interests, in spite of often burdensome and frustrating regulatory requirements.
Over the past four years, vocal opponents of the project repeatedly intervened to stall the
progress of approval for Sherman Hollow. Using slogans such as "Keep Sherman Hollow", the
protesters at one time appeared capable of bringing the development to a halt. Today, through a
series of positive and progressive steps, much of the opposition to Sherman Hollow has subsided.
However the Sherman Hollow permit was denied by the State Act 250 Commission. The Vermont
Pesticide Advisory Council is now drawing up a comprehensive protocol for golf course permitting,
and the Sherman Hollow case has been granted a new hearing.
A key component of the Sherman Hollow response to Act 250 inquiries was development of
an integrated pest management (IPM) plan to govern the use of pesticides on the proposed golf
course. Thought to be the first of its kind in the United States, it was hoped that this IPM plan could
serve as a model for the golf industry in its efforts to contribute ever more effectively to the
enhancement and protection of our natural environment. Meanwhile Cornell University Extension
Service has been developing a detailed IPM manual for golf courses in the northeast that embodies
ail the concepts put forward in the Sherman Hollow plan. The manual should be available in the fall
of 1989.
This essay explores the general nature and advantages of IPM to the golf course turf industry
and outlines some of the specific features of the Sherman Hollow IPM plan.
WHAT IS INTEGRATED PEST MANAGEMENT?
Integrated pest management (IPM) has been defined in various ways by various authors, which
has led to some confusion about the precise meaning of the term. From the perspective of golf
course turf management, one enlightening definition was provided by Victor A. Gibeault and others
of the University of California, Riverside.
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They suggest that "IPMis defined as multiple tactics used in a compatible manner in order to
maintain pest populations below levels that cause economic or unacceptable aesthetic injury without
posing a hazard to humans, domestic animals, or other non-target life forms."
The decision-making process inherent within this definition involves setting up tolerance levels
for pest populations, monitoring turf areas for pest incidence, maintaining accurate records of
monitoring data and taking appropriate actions with regard to the information collected through
monitoring.
An important point to note is that IPM is not itself a tactic for controlling pests, but rather it is
a system for understanding various strategies and tactics of pest control. It serves to guide the
pest manager in recognizing and selecting among various tactics. Further, it requires that such
selections be hazard-efficient.
One of the objectives of IPM is to use chemicals less, but it is a misconception that IPM
programs always replace chemical control. Rather, IPM encourages the pest manager to use
chemicals more wisely, which can mean less often. In a study of tree care reported by Dr. Michael
J. Raupp, an entomologist at the University of Maryland, pesticide use was reduced by more than
90% when IPM was utilized. Studies of household pest control have shown pesticide use reductions
of 80% and more in controlling cockroaches.
To implement the IPM approach, superintendents must be prepared to establish thresholds
for unacceptable economic or aesthetic injury based upon some reliable system of measurement.
Before resorting to the use of any chemical pesticide, it should be established by actual monitoring
of the turf that injury thresholds - or action levels related to such thresholds - will be exceeded
unless chemicals are used. Until these thresholds are crossed, use of alternative methods should
be attempted as feasible.
Because IPM is inherently site specific, explicit thresholds and the means of measuring injury
cannot be standardized for the golf industry. However, this should not deter experienced
professionals from drawing upon their best judgement in making such determinations.
Sheila Daar, IPM consultant and Executive Director of the Biointegral Resource Center,
explains "golfers and superintendents at different courses will have different tolerance levels for turf
injury. And differing maintenance regimes will result in different degrees of injury from the same
number of pests. The setting of injury thresholds just isn't subject to uniform standards."
SHERMAN HOLLOW: THE SETTING
Sherman Hollow is in Huntington, Vermont, 18 miles southeast of Burlington, and 20 minutes
from the Burlington International Airport. It is within 30 minutes of the Stowe, Sugarbush and Bolton
Valley ski areas and 25 minutes from Lake Champlain.
Sherman Hollow occupies 1,200 acres of land in the foothills of the Green Mountains. The
golf course is part of an overall development plan that will include a 70 room inn, conference facilities,
indoor tennis courts, a complete sport fitness center, 72 luxury townhouses, a live theatre, a chapel,
and 40 kilometers of cross-country ski trails.
The development will be arranged in a clustered "village" occupying only 20 acres. The golf
course will be built on an adjacent 120 acres.
Sherman Hollow, Inc. President Paul Truax and his family have lived on Sherman Hollow land
for many years. Paul and his wife Colleen purchased the core farm in 1961 with an eye toward
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recreational development. Their residency is an important factor in the environmental sensitivity
exhibited throughout the development.
"We've left a lot of land open, clustered the village and set a limit on the size of the project,"
noted Truax, "We want to make a profit, but life-style is important. After all, we live here."
The Golf Course
Sherman Hollow's golf course promises to be one of the finest in Vermont. Designed by
architect Charles Ankrom and golfer Raymond Floyd, the par-72 layout will measure 6,849 yards.
Ankrom already has a number of fine layouts to his credit, including the TPC course at Monte
Carlo and the Tower Club and Crane Creek in Martin Downs, Florida.
In designing Sherman Hollow, Ankrom recognized the need for a solid environmental design.
Even with the natural plateaus and terracing of the property, the course drops vertically more than
300 feet from start to finish.
From a design standpoint, Ankrom indicated that his key environmental concerns included
erosion control - especially during clearing and construction --and good water management.
"We are doing a variety of things to control erosion," Ankrom said. "The layout parallels the
natural terrain, creating terraces to reduce runoff. We've used birming, water retention areas, natural
watersheds -- the works. We have no interest in soil leaving the property, so we've been very careful."
An extensive erosion control plan, detailing every square foot of the construction site, has
been submitted to the Act 250 commission.
Ankrom also noted that good water management would play an essential role in pest
management. An extensive irrigation and drainage system is planned to interface with a series of
five lakes.
Floyd, who counts the 1986 U.S. Open crown among his five major tour victories, is consulting
designer for the project. He will bring to the project his expertise as a well-travelled golf professional.
Commenting on the environmental effect of the project, Floyd referred favorably to the
proposed IPM plan: "We play golf to enjoy and enhance our environment. If we can provide top
quality playing conditions with reduced chemical applications, that is going to be good for the game.
The specific pest control plan is outside my area of expertise but, as a player, I appreciate the
philosophy behind it."
Pesticide Use Plan
The protracted battle for Act 250 approval has involved dozens of public hearings concerning
the proposed golf course. The Sherman Hollow management team sought assistance from a variety
of outside authorities, including a hydrogeologist, toxicologist, agronomist, environmental scientists
and others.
Late in the spring of 1987, Sherman Hollow Superintendent Garry N. Crothers, CGCS,
contacted GCSAA's office of government relations for assistance. Through GCSAA contacts, a
working relationship between Sherman Hollow and the U.S. Environmental Protection Agency (EPA)
was established.
Anne Leslie, of EPA's Integrated Pest Management Unit, and Unit Chief Diana Home, had
indicated to GCSAA representatives earlier that year that they were looking for golf courses to serve
as IPM demonstration sites. Given Sherman Hollow's interests and needs, it was determined that
a possible compromise could be arranged.
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By early summer, discussions between Sherman Hollow and the EPA had solidified an
agreement in principle to implement a comprehensive IPM plan. Leslie appeared at a local permit
hearing in Vermont to discuss the proposal. Shortly there-after, the local Green Mountain Audubon
Society withdrew its objections to the golf course plan, a move that "stunned opponents of the
project", according to a report in the Burlington Free Press.
In a letter to Truax, Craig S. Sharf, chairman of the Green Mountain Audubon Conservation
Committee, wrote that "the information you presented to us has satisfied our concerns and provided
us with the assurance we felt is necessary."
Sharf said in a recent interview that some local Audubon members oppose any development
whatsoever at Sherman Hollow. Others, including himself, see some form of development as
inevitable. In that context, he sees the golf course as an "acceptable"alternative.
On July 29, Sherman Hollow representatives travelled to Washington, D.C., along with Kenneth
E. Bannister of the Vermont Department of Health, to meet with EPA representatives, and observers
from the staff of U.S. Senator Patrick Leahy, a Vermont Democrat and chairman of the Senate
Committee on Agriculture, Nutrition and Forestry. This meeting produced a formal outline of the
agreement to participate in an IPM demonstration project.
During the day long meeting, it was agreed that the overall goal of the IPM project was to
reduce dependency on pesticides while maintaining a high quality golf course. The EPA supports
the project to promote IPM for turfgrass and to demonstrate that good results can be achieved
when the best IPM practiceaare put to use.
"Weare pleased to be able to take a leadership role in protecting the future of the environment,"
Truax said. "We are particularly pleased to have the benefit of EPA's research and input in
implementing this plan. GCSAA has been instrumental in securing our good relationship with EPA
and other interested parties."
Leslie, of the EPA, pointed out that the Sherman Hollow IPM project is not expected to be an
experiment per se, but rather a joining of the very best of various individual techniques to see how
well they work within a comprehensive IPM approach.
"We will be looking for good preventive maintenance, such as selecting well adapted varieties
of grass, proper irrigation, fertilization, aerification, mowing and so forth," Leslie said. "And we will
recommend biological controls and other alternatives as advisable. Monitoring, record keeping and
setting thresholds will be the key to chemical treatments."
IPM ADVANTAGES
/
A dedicated IPM program can help superintendents do a better job of managing turf pests and
using various means of pest control -- including chemicals - as widely as possible. For those who
take IPM seriously, the rewards can be great. In the case of Sherman Hollow, IPM may spell the
difference between having a golf course and none at all, if the opposition of environmentalists and
concerns of regulators can thus be resolved.
Better Control
To individual superintendents, equally important advantages may result from adoption of an
IPM approach. By encouraging the natural predators of turfgrass pests, for example, more effective
control can be achieved. Further, the superintendent will not inherit the work of beneficial predators
that might be killed off by the overuse of non-selective chemical pesticides.
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Dr. Don Short, extension entomologist at the University of Florida, recently reported that, in a
three year study in south and central Florida, spot treatment with pesticides and weekly monitoring
of the turf resulted in good control of chinch bugs and webworms.
"This is primarily due to the fact that we are not killing off beneficial organisms that may be
providing more control than pesticides," Short concluded.
Where overdependence on chemical controls has substantially reduced non-target beneficials,
the stage is set for a dramatic resurgence of the unwanted pest. This is similar to the unchecked
expansion of exotic pests in areas where they have no natural enemies, such as introduction of the
mole cricket from South America in the early 1900's.
Avoiding Pest Resistance
Recent experience with various control failures illustrates the logical extension of this boom
and bust cycle. Where dependency on chemical solutions is great, pest populations can develop
resistance to pesticides.
Selection pressures are exerted by pesticide use, because genetically superior pests, which
are less susceptible to the pesticide, will survive the application and pass their superiority to the
next generation. With each successive treatment, greater resistance is encouraged. Eventually, the
pesticide itself will no longer provide effective control.
James F. Moore, mid-continent director of the USGA Green Section, observed this same trend
in a recent issue of the USGA Green Section Record.
"Combine excessive chemical use with improper turf grass selection and superintendents find
it necessary to make more and more pesticide applications a year," Moore noted. "Onthese courses,
it is only a matter of time until resistant organisms develop or the turf overdoses on the chemicals."
Healthy Turf
Moore's use of the word "overdose"is well chosen. Similar to a person addicted to drugs, a
golf course that is over-dependent on chemicals may be addicted to pesticides. In both cases,
chemicals become necessary for short term survival but counterproductive to overall health.
Used wisely, both drugs and pesticides can have medicinal or therapeutic value. A seasoned
physician addresses illness by adjusting diet, exercise, environment and various treatment
interventions, including Pharmaceuticals. Likewise, a good superintendent maintains healthy turf
through appropriate cultural practices, fertilization, irrigation and various pest controls, including
chemical pesticides.
Experienced superintendents realize that misuse of chemical pesticides can itself increase
turf stress. Each additional application carries the small, but significant, risk of mishaps or
misapplications that may radically degrade turf quality. These can include improper mixing or
calibration, accidental use of the wrong chemical, spillage or equipment failure -- the list goes on.
USGA's Moore sums up the idea well by noting that chemicals "are not a substitute for good
agronomics. By far the best chemical pest control programs are those that are as simple as possible."
Safety and Cost Factors
Minimizing hazards to humans, domestic animals and other non-target life forms is a part of
IPM by definition. This does not universally translate into reduced use of chemicals, but often fewer
applications do result.
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For every application avoided, the associated human and environmental risks are avoided.
Risks may also be reduced by use of chemicals that are more highly selective in attacking only the
target pest, or by more selective applications, such as spot treatments.
The direct cost savings of reduced pesticide use also can be substantial when the price of
single applications may be several thousand dollars.
The independence and judgement of individual superintendents considering an IPM alternative
is essential in this respect. Because the use of pesticides is a cost factor in golf course maintenance,
a superintendent has no monetary incentive to apply chemicals unnecessarily. Every treatment
avoided is money in the bank.
The trade-off between resource intensive chemical controls and labor intensive alternatives
may involve transitional costs. However, actual cost savings have been demonstrated in some pilot
programs.
"Our experience has consistently shown the long term costs of IPM are less than with
preventative chemical spray routines," says Daar.
Professionalism
One of the most important advantages of integrated pest management is that IPM recognizes
the agronomic insight and management skill of the superintendent. The turf manager's judgement
in balancing aesthetic, environmental, agricultural and human factors is the key to effective IPM.
The level of responsibility and professionalism involved exceeds sheer dependency on chemical
solutions.
Further, IPM is important from the perspective of good stewardship. Superintendents have a
powerful interest in the long term viability of the land they manage. The challenge to do everything
possible to preserve the integrity and productivity of the land logically includes a personal
commitment to IPM.
"A superintendent with the vision to effectively administer such a system is obviously a very
valuable asset to his employer," concludes GCSAA director William Roberts, CGCS. "It is, very
simply, the smart way to manage pest problems."
A Word of Caution
Cultural techniques, such as proper aerification, thatch control, good drainage and careful
irrigation have long been used by golf course superintendents to maintain healthy turf.
"We have been using IPM practices," notes Dr. Leon Lucas, Professor of Plant Pathology at
North Carolina State University, "but many haven't called them 'IPM'".
Yet, there is a difference between the use of practices consistent with an IPM approach and
actual adoption of IPM as a system of pest control.
Because of the positive public image associated with minimizing pesticide use, there is some
temptation to appropriate the language and trappings of IPM prematurely, without a commitment
to meaningful changes in behavior. Doing so reduces IPM to a hollow shell surrounding the same
old methods of pest control.
"Even where essentially benign techniques are being used," Daar said, "if there is no monitoring
program, no record keeping, no known tolerance level -- then there is no IPM."
The danger is that IPM will lose its credibility and appeal as an alternative to increasingly
unpopular traditional methods. Where there is even the suspicion that IPM has been used to
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whitewash continued overdependence on chemical pesticides, its value in resolving the emotional
debate over environmental issues will be lost.
To preserve the genuine advantages of integrated pest management, it is important that the
approach be understood and implemented with sincere appreciation for its intrinsic merit. In that
vein, the work of progressive projects, such as Sherman Hollow, should be encouraged and
supported.
The Bottom Line
Ultimately, the Sherman Hollow IPM plan represents a very creative and progressive response
to an increasingly common -- and increasingly complex - set of problems facing proposed golf
course developments. By exhibiting an extraordinary level of professionalism and environmental
concern, Sherman Hollow has set an important example for others in the golf industry.
As the Selectmen of the Town of Huntington testified during Act 250 hearings, issuing permits
for Sherman Hollow would allow "flexibility in efforts to preserve the delicate balance between open
spaces and developmental pressures."
As long as golf course construction and management continue to set a high standard for
environmental awareness, the golf industry will remain a preferred development option.
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SOCIETAL BENEFITS OF CONSERVATION ORIENTED
MANAGEMENT OF TURFGRASS IN HOME LAWNS
Anne R. Leslie
U.S. Environmental Protection Agency
401 M Street SW
Washington, DC 20460
and
William Knoop
Texas A&M University
Research and Extension Center
17360 Colt Road
Dallas, TX 75252
This chapter shows how communities can benefit when homeowners choose an IPM approach
to turfgrass management and city management is supportive through recycling programs. Although
healthy grass is generally viewed as an aesthetic asset rather than a cash crop, evidence is
accumulating for its positive health and environmental contributions. Balanced against all of this is
the potential risk from the pesticides that may be applied. So an IPM program that emphasizes
proper pesticide application without sacrificing turf quality is especially important. Reductions in air
and water pollution can be realized through maintenance of this quality groundcover. Some recycling
of urban solid waste is even possible, and as shown below, this can be an economic benefit to the
community.
Healthy turf can act as a buffer to delay or prevent movement of chemicals and soil from
agricultural sites to watersheds. Grass is used in orchards to absorb pesticides and minimize
erosion. Grassland experiences 84 to 668 times less erosion than areas planted to wheat or corn.
Studies show that an average golf course of 150 acres absorbs 12 million gallons of water during
a three-inch rainfall, and thick, carefully managed turfgrass has 15 times less runoff than does a
lower quality lawn (Watschke, personal communication). By comparison, parking lots, streets, and
other paved residential areas load nearby waters with hazardous pollutants carried in runoff from
road surfaces, gutters and catch basins.
Healthy turf can flourish with IPM techniques that also recycle sewage sludge, and detoxify air
and water pollutants. Using recycled sewage sludge compost to fertilize golf courses helps mitigate
groundwater pollution effects of waste disposal sites. Homeowners can purchase such materials
to use on their lawns so long as they grow no food nearby. Some of these materials are discussed
in the chapter by Vargas.
A healthy lawn can detoxify air pollutants. The capacity of grass is comparable to the same
leaf surface area contained in trees. In addition, turf is an excellent groundcover to diminish loss of
soil as dust, a significant air pollutant. Finally, a lawn can provide cooling to the home and lower the
energy consumption for air conditioning in the summer.
Communities having limited landfill space have built incinerators to dispose of solid waste. In
this technology the burning of organic matter such as lawn clippings, which have a high water and
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nitrogen content, results in increased emission of the oxides of nitrogen. Reducing the quantity of
garden plant material to this solid waste disposal stream will help reduce air pollution.
The Lawn Waste-Saver Program carried out in Piano, Texas addresses the problem of limited
landfill space. William E. Knoop of Texas A&M University Research and Extension Center at Dallas,
reports in Grounds Maintenance Magazine the only quantitative study of its kind that we are aware
of. The plan has since been implemented in other communities, including Fort Worth, Texas. It was
presented to the EPA Municipal Solid Waste Task Force in May 1988. This presentation included
recent data from Wichita Falls, TX, and a report, "Turfgrass Management Practices and Their
Influence on Pests," given by Philip F. Coibaugh of Texas A&M at the ACS symposium in New
Orleans, August 1987. The latter report shows how this system is part of an IPM program that
results in improved turf as well.
The original article by Knoop is reproduced here to show how the program was implemented
by the City of Piano. (Reprinted with permission from the November 1982 issue of Grounds
Maintenance 1982, Intertec Publishing Corp., Overland Park, KS 66212.)
WASTE-SAVER LAWN CARE PROGRAM
Landfill space is at a premium for most cities. It is expensive to obtain. It is also expensive to
maintain. Cities surrounded by other cities often have used up all possible landfill space and must
find land in other areas. Few residents are eager to allow any city to develop a landfill next to them.
These considerations make it highly desirable to make the most out of the currently used landfill.
Piano, Texas, north of Dallas, is a bedroom community of about 80,000 people. To make the
city government run as efficiently as possible, the management created a Productivity Department
in the spring of 1980. It reviewed Piano's solid waste disposal system. During one week in mid-June
1980, productivity staff members rode each garbage truck on every route and recorded the number
of garbage bags containing grass clippings and the number of bags containing other garbage.
The city officials found that 29.1 percent of all garbage bags picked up during the 1980 Piano
sampling period were filled with grass clippings. A bag of grass clippings weighs approximately 40
pounds, so Piano homeowners were placing nearly 700 tons of grass in the landfill. Because bags
of grass clippings weigh more than an average bag of other garbage, it was estimated that about
40 percent of the garbage truck's load (by weight) was grass clippings.
If analyzed on the basis of their dry weight, the 33,000 bags of grass clippings collected each
week contain approxi-mately 2 1/2 tons of nitrogen, 1/2 ton of phosphorus, 1 ton of potassium and
all the remaining essential plant nutrients. When placed in a landfill, their value has essentially
ended; their only function is to possibly become a future source of ground-water pollution.
EDUCATIONAL PROGRAM
A cooperative public educational program between the city of Piano and the Texas Agricultural
Extension Service was begun in April 1981 in an effort to reduce the amount of grass clippings
reaching the landfill. This educational program used the local newspaper, area TV and radio, and
a flyer that the city mailed to each of its nearly 19,000 homeowners. The goal of the program was
to encourage proper fertilization, watering and-most importantly-proper mowing. Homeowners
were advised that the management of golf courses (with the exception of greens), athletic fields
and other high-quality turf areas does not include the process of picking up grass clippings.
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The results of the program, summarized in the accompanying table, were encouraging.
Although the number of bags of other garbage increased by 12 percent, the number of bags of grass
clippings decreased by 11 percent, for a projected overall decrease of 23 percent. The percentage
of bags containing grass clippings was reduced from 29.1 percent in 1980 to 24.7 percent in 1982.
The total saving to the city was over $100,000. Perhaps more importantly, the burden on the landfill
was reduced.
How unique is this problem? Piano is an upper middle-class city whose homeowners place
very high aesthetic value on their homes. As word of the success of the program spread, mainly
through city-government-oriented publications, more than 100 cities from 27 other states wrote
asking for details of the Piano program. A director of public works from an Ohio city indicated that
approximately 50 percent of the solid waste collection in summer was grass. He thought that 95
percent of homeowners bagged their grass clippings, indicating that the bagging of grass clippings
may be a more universal problem than first considered. It might be hard to find a city without a
landfill problem and grass clippings may be a part of that problem.
How did all this bagging of grass clippings get started? Perhaps we homeowners became
more and more lazy about mowing practices. Instead of removing no more than one-third of the
leaf surface area each mowing and letting the growth rate dictate the mowing frequency, we tended
to let the calendar dictate mowing frequency. As a result, the heavy layer of clippings on the lawn
presented a real management problem. Raking clippings certainly is not a pleasant task and
mowers that collected the clippings in a container that could be emptied into a garbage can or plastic
bag became highly desirable.
We homeowners may have compounded the problem by also placing such a great value on
dark green lawns. Such lawns require fairly high applications of nitrogen, which tend to increase
growth rates. Promoters have never emphasized turfgrass varieties that produce reasonable growth
rates at low nitrogen rates.
HOMEOWNERS RECEPTIVE
Perhaps it is now time to provide homeowners with good, basic turfgrass management
information that encourages such practices as proper mowing. The experience in Piano indicated
that most people did not know they did not have to bag grass clippings. They assumed that, because
the mower had a bagging attachment, there was no alternative. The program demonstrated to
homeowners that if mowing frequency was increased to once every 5 days, then the need to bag
was ended. Most homeowners felt this increase in mowing frequency was far more desirable than
bagging clippings. The program also demonstrated the value of a 3-1-2 fertilizer ratio and the value
of a slow-release nitrogen source in slowing growth rates without any sacrifice in lawn quality.
Mulching mowers can be expected to play an important part in a non-bagging lawn
maintenance program. More research with mowers in controlled-management situations is needed.
Our energy as a turf industry has been concentrated in areas that benefit relatively few people.
Now we must consider a larger issue, such as the bagging of grass clippings and its effect on
landfills.
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TABLE 1
SUMMARY OF THE PLANO, TEXAS
WASTE-SAVER LAWN CARE PROGRAM
YEAR
Number of homes
Number of stops for garbage
Number of stops that had bags
of grass
Number of bags of grass
Number of bags of other
garbage
Total bags of garbage
Truckloads of garbage
1980
18,771
29,025
9,894
33,625
81,852
115,477
141
1981
21,074
31,740
9,133
30033
91,462
121,495
123
CHANGE
+12%
+ 9%
-8%
-11%
+12%
+ 5%
-13%
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LAWN SERVICE INDUSTRY: TRANSITION IN SERVICES
Roger C. Funk
The Davey Tree Expert Company
1500 N. Mantua Street
Kent, Ohio 44240
The lawn care industry has experienced unprecedented growth in the last decade and the
demand for our services is still growing.
The recent pesticide controversy has raised questions concerning the safety of pesticides and
our current practices. It has also increased consumer awareness of our industry, expanding the
market for quality-conscious lawn care operators. There has never been greater opportunity for
those willing to accept the challenge.
Lawn care operators are developing an image problem. We are being perceived not as an
industry that maintains the health of turfgrass but rather as an industry that applies pesticides. Of
course we do apply pesticides but only as one of the many services that we provide.
Although several factors could contribute to the public's perception of our industry, the most
important are media coverage, high market visibility and the overuse of pesticides. This perception
can be changed only if we recognize that education is an integral part of the services we provide
and that we must limit our use of pesticides through monitoring and selective applications and the
use of alternative materials whenever possible.
One of the best methods of educating the public is through an educated media. Too often we
take a combative or defensive attitude toward the media since they usually fail to present balancing
viewpoint about lawn pesticides. It is their objective to report what they consider to be newsworthy.
Unfortunately for us, the application of pesticides to millions of lawns without a single incident is
not considered newsworthy. However, the perceived or alleged injury to just one person from those
millions of applications is news and would be reported.
The high visibility of the lawn care industry has also contributed to our image as pesticide
applicators. Because of the demand for our services, the lawn care industry has been highly
successful. And because of our success, we're highly visible in the urban and suburban
environment. There are estimates as high as 40-60% if the homeowners in any given market having
a commercial applicator do their chemical lawn maintenance.
As success and visibility increase, questions and concerns about the effect of our applications
on health and the environment also increase. Do-it-yourselfers use the same fertilizers and
pesticides we use, but they maintain a lower visibility in the neighborhood.
The noticeable odor of pesticide applications is largely the result of the overuse of pesticides.
Most lawn care operators apply pesticides to the entire lawn if pesticides are needed on any portion
of the lawn. Some may apply the same granular or liquid formulation to all of the lawns serviced
within a geographic area based on the predicted pests for that time of year. This practice leads to
the unnecessary application of pesticides and contributes to the concern of pesticide exposure. In
addition, "shot gun" applications are not an economically or agronomically sound practice since no
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benefit is derived from a pesticide application if a pest is neither present nor anticipated within the
residual period of the pesticide.
In order to change the public's perception of our industry, we must change the way we do
business. Change is seldom easy, particularly for an established company with a growing market
share. Change, however, is an integral part of any successful company. One definition of success
is to find out what the public wants and then give it to them. When the lawn care industry first started,
our customers wanted green, weed-free lawns. They still want the same thing but with less
pesticides applied to achieve it.
Last year, insecticides and herbicides in Davey lawn care services in selected territories were
effectively reduced 40% to 50%, respectively, through the use of the patented Davey Customizer.
The Customizer is specially designed for spot application of pesticides. Pesticides are not
tank-mixed, but are secured in a separate reinforced tank and are injected in the fertilizer line only
as needed. Another feature of the Customizer is its specially designed no-drift nozzle.
In a five-area representative sample of Davey lawn care operations (Akron, OH; Charlotte,
NC; Minneapolis, MN; Rochester, NY; and Washington, DC), 1987 results show that 4,800 gallons
of herbicide were used in 1985 compared to 2,260 gallons in 1987 with the use of the Customizer.
(Fig 1). In addition, insecticide use was reduced from 1,020 gallons to 600 gallons. (Fig 2). This
represents a 52.9% reduction in herbicides and a 41.1% reduction in insecticides.
Based on our field experience in the five test markets, we are projecting a company-wide
reduction in lawn pesticide use in 1988 of almost 10,000 gallons-without any increase in insect or
weed problems.
Petrochemical pesticide use can be reduced in other ways. Alternative materials such as soap
and citric oil are being researched. Both materials are effective insecticides and currently are used
in other industries. Biological controls may prove practical.
Milky spore disease has reportedly been reformulated and is more effective on Japanese
beetles. Tests are under way for nematode control of grubs and fungal control of chinch bugs.
Electrostatic sprays may reduce drift of conventional pesticides by electrical attraction of spray
particles to plant surfaces. This allows the rate of application to be reduced.
Micro-encapsulation of pesticides can potentially reduce the toxicity of pesticides while
reducing odor.
Our industry should investigate alternative methods of pest management and discuss possible
solutions with university personnel and material equipment manufacturers. We should not be
committed to any material or method of application - only to provide the quality of service the
customer wants and has a right to expect.
In summary, the lawn care industry is partially responsible for the pesticide controversy due
to our high visibility in residential areas and the overuse of pesticides. The news media has
contributed by reporting only "newsworthy" items that sensationalize and distort the risks from
pesticide exposure. We can, however, improve the quality of our service through education, and
through alternative materials and methods of application. Controversy almost always results in
change... and with change comes opportunity.
Editor's note: A more technical treatment of how the Davey Co. has responded to the need
for change is presented in the following section dealing with ornamentals.
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DAVEY'S PLANT HEALTH CARE
Pest management is an important service offered by Arborists to protect trees and shrubs in
the landscape. Concerns for public health and the environment, however, have resulted in increased
insurance costs and restrictions in the use of pesticides. Many tree care companies are weighing
the benefits of a pest management service against the risks involved in the continued use of
pesticides.
In January 1985, the Davey Company scheduled our first Plant Health Care (PHC) Seminar
to discuss a comprehensive approach to improving tree health through proper selection, planting,
and care. Since the concept of PHC emphasizes preventative maintenance, the health of the tree
(not pest control) became the central focus of our service.
Neilsen (Reference #2) defines a similar concept and provides a framework for implementation
in the November, 1986 issue of the Journal of Arboriculture.
One of the objectives of our PHC concept was to reduce the use of traditional pesticides.
Horticultural oil was an obvious and underused alternative and we began testing its use for
foliage-feeding insects. In addition, we began testing reduced rates of the registered insecticides
in combination with soaps, horticultural oil, vegetable oils, and citric oils. More recently, we have
begun testing Neem oil, diatomaceous earth, and detergents.
Our earliest successes were with soap plus reduced rates of insecticides. After two years of
laboratory and field testing, we introduced the approved combinations in five test markets in 1987
and implemented the "program"through our U.S. market in 1988. We anticipate a 75% reduction in
pesticide use this year with further reductions by 1990. Additional reductions are projected through
the increased use of alternatives, selective spraying and improved methods of application.
EFFICACY TESTING
Preliminary research with Safer Insecticidal Soap indicated that soap alone would satisfactorily
control most soft-bodied insects and mites, but provided no residual effect. Testing was begun on
reduced rates of the petrochemical pesticides in combination with soap to determine efficacy for
sucking as well as chewing insects and mites.
in most cases soap was found to enhance the control achieved with reduced rates of
pesticides. This was particularly true with sucking insects and mites, but also with Japanese beetle.
Tempo, a synthetic pyrethroid, was sprayed on linden leaves in the field. Leaves were also treated
with Safer soap and Tempo plus soap. Foliage was collected one week later. During this period,
rainfall was approximately 1-1/2 inches. Japanese beetles were introduced onto the foliage in the
laboratory. After a feeding period of two days, mortality rates were recorded. The results are in the
following chart:
99
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Table 1.
Japanese Beetle on Linden
Insecticide Rate/100 gal. % Control
(Residual)
Tempo 0.5 oz. 17
Soap 128oz. 0
Tempo + Soap 0.5 oz. + 128 oz. 92
Tempo alone at 1/4 the recommended rate and soap alone at 1/2 the recommended rate did
not control the beetles. The same rates of Tempo and soap when combined, however, provided
92% control.
In another experiment, Tempo and soap were tested for contact control of aphids. Rose of
Sharon twigs infested with aphids were brought into the lab, placed in individual vials of water and
sprayed. Results of this experiment are given in the chart below:
Table 2.
Aphids on Rose of Sharon
Insecticide Rate/100 gal. % Control
(Contact)
Tempo 0.5 oz. 40
Soap 64 oz. 90
Tempo + Soap 0.5 oz. + 64 oz. 98
The combinations of Tempo plus soap again outperformed either component individually
applied. The tests demonstrated that the rate of Tempo can be reduced significantly when combined
with soap for the control of aphids and Japanese beetles. Tests with other insecticides, such as
Dursban, Orthene, and Sevin, have shown similar results in combination with soap or horticultural
oil, although the effective rates vary. In one test, Dursban at 1/16 the recommended rate in
combination with horticultural oil (1 gal/100) provided mite control equal to Dursban at full rate.
COMPATIBILITY TESTING
The current soaps which are registered for ornamentals are strongly alkaline and may react
differently with different insecticides or in different water sources. For example, in some of our
markets, soap causes Sevin to deactivate within several hours of mixing and turn a brown to
reddish-brown color -- which stains! In these situations, additives are necessary to combine soap
with the insecticide. Davey researchers are working with soap manufacturers to alter the formulation
of soaps so that additives may not be necessary in the future.
100
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PHYTOTOXICITY TESTING
There are a number of plants listed as being injured by Safer's soap. (Reference #3) In addition,
we have found that drought-stressed trees are more susceptible to injury from soap than standard
pesticides and that, under certain conditions, the new growth of evergreens may be injured. In
most cases, we did not find that the addition of a reduced rate of pesticide altered the occurrences
or severity of the pnytotoxicity. Although precautionary statements regarding phytotoxicity from
horticultural oil persist, Johnson (Reference #1) has not observed injury when light, superior oil is
applied to deciduous foliage, provided that the proper rate is applied and that the tree is not under
moisture stress. Injury which we observed occurred only when oil was combined with Sevin and
may have been related to drought stress and/or excessive heat and pressure.
SELECTIVE SPRAYING
Selective spraying involves monitoring to determine the presence and population levels of
insects, and spraying only those trees and shrubs that have a pest problem. Pheromone traps are
a useful tool in determining the most effective timing for control of clearwing moth borers. Traps
have also been used successfully in identifying species of pine tip moth. This is particularly useful
when first starting a monitoring program or when opening a new market.
Personnel training and resource information is essential to the success of our PHC programs
since the person making the application normally determines which trees and shrubs will be sprayed.
The Technical & Research staff developed pest/host timing charts for each of our field offices which
are continuously being refined with the assistance of an on-site PHC trainer. (Figures 1 & 2) The
charts provide guideline for anticipated insect and disease problems. In addition, the trainers attend
week-long classes at our headquarters in Kent, Ohio, each year to enable them to train and monitor
the effectiveness of the technician in the field. Extension courses developed in-house are part of
the training supervised by the PHC trainer. The Technical staff also visits each territory each year
to further train and motivate the field staff.
Educating clients is necessary, not only as a potential participant in the monitoring process,
but also to accept the concept of selective spraying. Clients who have been on a program where
all the trees and shrubs have been sprayed are often reluctant to accept selective sprays. Literature
which explains Davey's approach to Plant Health Care is provided to clients as well as Fact Sheets
which discuss any major problems on the property. Information is also available to help clients
select the proper plants for site conditions and the proper transplant procedures and cultural
requirements for those plants.
Application techniques can reduce the potential for drift and reduce the volume of pesticide
used.
Davey researchers tested various pressures and disc sizes to determine the effect on drift.
Trees should be sprayed with a large disc or nozzle and only sufficient pressure at the gun to reach
the top of the tree. A ball valve or similar control at the spray gun will allow the technician to adjust
the flow rate and pressure at the nozzle without returning to the truck.
Excess spray volume applied to trees and shrubs is a common problem, particularly with new
technicians. Guidelines were developed by Davey researchers indicating the spray volume needed
for coverage of different size canopies. For example, a tree 50-ft. high and 60-ft. wide would require
25 gallons of spray mix. This gives the technician and his manager a tool for comparing the actual
with the estimated material usage.
101
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A survey of all field managers was conducted in 1987 to estimate material savings from the
improved application techniques. Although the actual material savings varied, depending upon the
pest problem and the experience of the technician, the least savings reported was 5%.
In summary, Davey's Plant Health Care program enabled us to reduce our use of traditional
pesticides by 75-80% in five test markets in 1987. Fifty percent of the savings was achieved through
the use of alternative materials, 25% by selective spraying, and 5% by improved application
techniques. Based on our findings we are projecting a reduction in use of over 20,000 gallons of
pesticides in 1988 for our tree care markets-with no reduction in the quality of service to our
customers.
102
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Literature Cited
Johnson, W. J., 1980. Spray Oils as Insecticides. Journal of Arboriculture. 6(7); 169-174.
Neilsen, D. G., 1986. Planning and Implementing a Tree Health Care Practice. Journal of Arboriculture. 12(11): 265-268.
Safer, Inc. Phytotoxictty Information. May 8,1984.
103
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FIGURE 1
<
o
LAWN CARE
HERBICIDE REDUCTION
IN FIVE-AREA REPRESENTATIVE SAMPLE
OF DAVEY OPERATIONS
'85 '87
Total
'85 '87
Akron,
OH
'85 '87
Charlotte,
NC
'85 '87
Minneapolis,
MN
'85 '87
Rochester,
NY
'85 '87
Washington,
D.C.
104
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FIGURE 2
LAWN CARE
INSECTICIDE REDUCTION
IN FIVE-AREA REPRESENTATIVE SAMPLE
OF DAVEY OPERATIONS
1,050
'85 '87
'85 '87
'85 '87
Total
•Minneapolis, MN does not have a high insect control problem
Akron,
OH
Charlotte,
NC
Minneapolis,
MN
'85 '87
Rochester,
NY
'85 '87
Washington,
D.C.
105
-------
106
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SECTION III
Current Research Towards
Understanding the Pest and the Site
107
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108
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DETECTION AND MONITORING OF TURFGRASS
PATHOGENS BY IMMUNOASSAY
S. A. Miller, G. D. Grothaus, F. P. Peterson,
J. H. Rlttenburg, K. A. Plumley, and R. K. Lankow
Agri-Diagnostics Associates
2611 Branch Pike
Clnnaminson, NJ 08077
An integrated pest management (IPM) strategy for crop protection and production seeks to
achieve maximum yields while minimizing crop damage, cost to the grower, and environmental
hazards (1). For any crop, an effective IPM program must include the accurate and timely detection
of pests and pathogens. For most plant diseases, few tools have been available to the grower or
crop consultant for this crucial aspect of disease management, resulting in a reliance on
symptomatology for disease diagnosis (11). However, symptom expression can be highly variable,
depending on the crop variety, maturity, environmental conditions, and other factors. In addition, a
number of pathogens may cause similar symptoms on the same plant variety. Reliance on
symptoms usually precludes the early detection of pathogens, which may hinder the implementation
of preventive management practices.
Recent advances in biotechnology are being applied to plant pathogen systems to provide
diagnostic tests directly applicable to pathogen detection at the grower level (8,9). For broad
acceptance among crop managers, these assays must be sensitive, specific, reliable and
user-friendly. These criteria can be met by immunoassay-based diagnostic systems. Agri-
Diagnostics Associates have developed immunoassays for the detection of three fungal pathogen
complexes in turfgrass: Pythium Blight, Rhizoctonia Brown/Yellow Patch, and Dollar Spot. The
basic concepts of immunoassay technology are described, focusing on the Pythium Blight assay
and its effectiveness in detecting the disease in golf course turfgrass.
Immunoassays are tests in which antibodies are used as analytical chemistry reagents (7).
To a large extent, the antibody is responsible for the specificity and sensitivity of the immunoassay,
and two major types (polyclonal and monoclonal) are employed. Polyclonal antibodies are produced
and secreted in experimental animals by a large number of B-cell clones which proliferate in
response to recognition of chemical structures or determinants presented by the injected antigen.
Polyclonal antisera can be produced in commercial quantities by immunizing large numbers of
small animals or a few large animals such as sheep and goats in a relatively short time frame (3-6
months), and usually provide a robust antibody population due to the variety of immunoglobulin
types in the sera. The generalized specificity of a polyclonal antiserum to a number of determinants
on an antigen can be advantageous. If the target analyte is heterogeneous and somewhat variable
in structure or the relative ratios of its various components, a polyclonal antiserum may provide a
certain amount of "recognition buffering".
Monoclonal antibodies are now finding considerable application in immunoassay by providing
a very high level of specificity as well as a potentially unlimited source of uniform antibody (4,5,6).
Monoclonal antibodies are produced by fusing antibody-producing cells isolated from the spleen of
109
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an immunized animal with "immortaJ"myeloma cells from tissue culture. The cells are transferred
to a selective medium that will only support the growth of hybrid cells, called hybridomas. Individual
hybridomas are subcloned and allowed to divide and produce antibody. Antibody secreted into the
cell culture medium is then tested for desirable antigen-binding characteristics. Since each
hybridoma cell line produces only one type of monoclonal antibody, it is possible to select antibodies
with the specificity and sensitivity required for specific applications. Hybridomas may be stored
frozen in liquid nitrogen and recovered at any time to continue reproducible production of the
antibody.
For practical application of the unique properties of antibodies in a diagnostic assay, the user
must be able to determine whether the antigen/antibody reaction has taken place. A variety of
visualization and detection methods have been designed for this purpose. Enzyme immunoassay
(EIA) is probably the immunoassay technology most widely applied today (7,9). One widely used
EIA is the double antibody or "sandwich" immunoassay (2,3), in which an untagged or capture
antibody is bound to a solid phase, such as beads, membranes or the wells of a microtiter plate.
The test sample and enzyme labeled antibody are added sequentially, and unbound components
are removed by washing after each incubation. Enzyme labeled antibody is detected by the addition
of a color-producing substrate. The capture antibody is particularly useful when the test sample
consists of a complex mixture of materials, such as a plant extract. The capture antibody binds the
target antigen, while other components of the sample, which could interfere with subsequent steps
in the immunoassay, are washed away.
One of the simplest immunoassay formats uses a dipstick as the solid phase (7). The dipstick
is moved from one reagent to the next and the assay result is determined by examining the dipstick.
Visualization of the bound enzyme-labeled antibody occurs when the enzyme converts the substrate
to an insoluble colored product that binds to the dipstick. Quantitative results can be obtained
through the use of an inexpensive field-adaptible reflectometer that measures the color intensity
on the dipstick.
KIT CHARACTERISTICS
The Agri-Diagnostics turfgrass disease detection kits employ the dipstick format for performing
a double antibody sandwich immunoassay. The assay requires no specialized equipment and can
be completed in less than 4 hours.
The turfgrass sample is ground on an abrasive pad which is placed into the sample extraction
buffer. The grinding homogenizes the sample, breaks up the fungi, and presents a controlled
amount of sample (material trapped within the abrasive surface) into a fixed volume of extraction
buffer. In the next step a fixed volume of enzyme-tagged antibody, specific for the pathogen, is
added into the extraction solution. Then the dipstick, with antibody specific to the pathogen
immobilized to its surface, is placed into the reaction mixture. During this step, the antibody on the
dipstick captures any pathogen in the sample, and the enzyme-labelled antibody simultaneously
tags the pathogen. After washing away any material not specifically bound, the dipstick is placed
in a substrate solution which forms a colored precipitate in the presence of enzyme. The assay is
quantitative, yielding a color endpoint, the density of which is directly related to the amount of
pathogen in the turfgrass sample.
110
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The graph in Figure 1 shows the dose response curve for the Pythium detection assay. The
sensitivity limit based on fungal protein material is approximately 20 ng protein/ml. A reflectometer
was used to quantitate the intensity of the reaction zone on the dipsticks.
The specificity of the immunoreagents used in the dipstick assay was determined using a
"multiwell-'EIA format. Dilutions of soluble extracts of isolates of fungi known to occur as pathogens
or saprophytes on turfgrass were tested in a direct double-antibody EIA using standard protocols
(3). The second ("tag") antibody was conjugated with horseradish peroxidase, and ABTS
(2,2'-Azinobis(3-ethylbenzthiazolinesulfonic Acid) was the substrate used.
The reactivity of nine Pythium spp. associated with turfgrass as pathogens or saprophytes
with the assay immunoreagents is shown in Table 1. All of the Pythium species associated with
Pythium-induced disease, including P. aphanidermatum. P. ultimum. P. graminicola. P. aristosporum.
£. arrhenomanes. and P. myriotylum are detected by the assay. Species described as weak
pathogens or saprophytes of turfgrass, including R, torulosum. FL vanterpooliir and H rostratum are
not detected. Other genera of turfgrass pathogens or saprophytic fungi associated with turfgrass
also are not detected. Among the genera tested were Rhizoctonia, Sclerotinia. Fusarium.
Drechslera. Bipolaris. Laetisaeria. Limonomyces. Curvularia. Rhizopus. Typhula. Trichoderma and
Mortierella.
FIELD RESULTS
The Pythium detection assay was evaluated on a southern New Jersey golf course in 1986
and 1987. The 1986 test was of limited duration, carried out during an outbreak of Pythium blight
on several of the course's fairways and greens in July of that year. Environmental conditions were
conducive to Pythium blight for the duration of the testing period. The data resulting from tests on
the green and fairway with the most severe disease are presented. The green that was studied
(Green 4) contained bentgrass and a small percentage of annual bluegrass. Pythium blight occurred
primarily on the collar, and samples were taken from this part of the green. The fairway studied
(Fairway 7) consisted of perennial ryegrass, and was severely damaged by the disease. In order
to determine the relative concentration of the pathogen at various stages of disease progression,
samples were taken from the middle and edge of patches or streaks caused by Pythium spp., as
well as from symptomless areas in proximity with the symptomatic areas. Samples of turfgrass from
areas tested with the Pythium kit were also plated out on a selective medium for Pythium spp.
isolation (10).
Pythium spp. were detected in both asymptomatic and symptomatic perennial ryegrass and
bentgrass samples from the same green or fairway (Table 2). Pythium assay results were usually
higher for symptomatic samples than for asymptomatic samples, as were Pythium spp. isolation
frequencies. For all five of the asymptomatic samples shown in Table 2, Pythium spp. were detected
by the immunoassay, although they were isolated from only three of the five samples. Since the
samples were tested when environmental conditions were optimal for Pythium blight and prior to
the application of Pythium control fungicides, Pythium spp. may have been present in the
asymptomatic turfgrass samples at a high enough level to be detected but were not causing
symptoms. Meter readings for Pythium assays of samples taken during conditions not conducive
to Pythium blight development, or when the disease is well under control as a result of fungicide
application, are usually in the 0-10 range (see Figure 4,5, below).
111
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In general, the highest meter readings for blighted turf were obtained by sampling at the edge
of patches or streaks (Figure 2). While Pythium spp. could usually be detected in dead grass in the
center of a patch, high levels were detected more consistently at the leading edges.
Pythium spp. were detected on Fairway 7 and Green 4 throughout the testing period. A
fungicide effective against Pythium spp. was applied on July 10, which was followed by a decrease
in meter readings for samples taken from both the green and the fairway. Meter readings continued
to decrease for samples taken from the green, while the readings for fairway samples increased to
pre-fungicide application levels. These results reflect the amount of disease development on the
green and fairway; Pythium blight damage was somewhat localized on the green, which had begun
to recover by the end of the testing period. The damage on the fairway was extensive in the area
that was tested, and the ryegrass turf did not recover quickly.
In 1987, a monitoring program was initiated on Green 4 and Fairway 7, beginning in late May
and extending through the summer until termination at the end of August. Six subsamples were
collected from the green and its collar, bulked separately, and thoroughly mixed. On the 7th Fairway,
an area surrounded by trees and approximately 150 yards from the green was sampled. Six
subsamples were taken from an area no larger than a green and bulked. Two dipstick assays were
run for each bulked sample. Leaf blades were plated onto Pythium-selective medium as described
above. Designated areas were sampled before mowing in the morning to maximize the amount of
foliage that could be sampled, as well as to permit visual detection of pathogen signs (mycelium),
if present.
As a result of the damage caused by Pythium blight to the greens and fairways during 1986,
the golf course superintendent instituted a rigorous fungicide spray program in 1987. Beginning in
late May, greens and fairways were sprayed on a weekly basis with three fungicides effective against
Pythium spp. in rotation. As a result, no symptoms of Pythium blight were observed throughout the
testing period, even during periods when the environment was highly conducive to disease
development. Results of the monitoring program using the Pythium detection assay are presented
in Figure 4. Conditions favorable for Pythium blight first occurred on May 29; low positive readings
were observed for the sample from the collar of Green 4, which was taken from the area most
severely affected in 1986. Results were negative for the samples from the Green 4 and from Fairway
7. The first fungicide application was made on May 29 after the sample was taken; all subsequent
Pythium detection assay results were negative for Green 4 (including its collar) and Fairway 7.
Thirty isolates of Pythium spp. were recovered during the testing period, five of which proved to be
pathogenic in standard pathogenicity tests.
The negative results obtained with the Pythium detection assay were clearly correlated with
the lack of symptoms of Pythium blight on the greens and fairway tested. With the exception of the
low positive reading observed for the collar of Green 4 on May 29, Pythium spp. did not reach
detectable levels at any time during the testing period. These results, especially when compared
to the results of the 1986 trial, attest to the efficacy of currently available fungicides in controlling
Pythium blight. However, the use of fungicides in this instance appears to have been excessive;
our data (not shown) indicate that fungicide applications may not be required until meter readings
reach 10-15, depending on the disease history of the turfgrass in question. By monitoring greens
and fairways on a regular basis using the Pythium detection assay, increasing populations of
Pythium spp. can be detected, and superintendents may more precisely time the application of
fungicides.
112
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CONCLUSIONS
The sensitivity and specificity of the dipstick assay system will make it possible for golf course
superintendents and other turf managers to a) correctly diagnose turfgrass disease, b) detect
pathogens at an early stage of disease, before symptoms appear, and c) monitor the development
of pathogens in established turfgrass stands during periods of disease risk. An effective disease
monitoring program will include a determination of the baseline readings for particular stands (i.e.
greens, fairways, tees) during periods of low risk, followed by regular monitoring during the season.
This capability will enhance the effectiveness of currently used disease control measures and
promote an integrated approach to disease management in turfgrass.
113
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REFERENCES
1. Andrews, J. 1983. Future strategies for integrated control, in: Challenging Problems ]n Plant Health, ed. I
Kommedahl, P. H. Williams. American Phytopathological Society, St. Paul, MN. pp.431-440.
2. Clarke, M. F. 1981. Immunosorbent assays in plant pathology. Ann. Rev. Phytopathology 19:83-106.
3. Clarke, M. F., Adams, A. N. 1977. Characteristics of the microplate method of enzyme-linked immunosorbent
assay(ELISA) for the detection of plant viruses. J. Gen. Virol. 34:475-483.
4. Galfre, G., Milstein, C. 1981. Preparation of monoclonal antibodies: strategies and procedures. Meth. Enzymol. 73:
3-46.
5. Coding, J. W. 1983. Monoclonal Antibodies: Principles and Practice. Academic Press Ltd., London. 276 pp.
6. Halk, E. L., DeBoer, S. H. 1985. Monoclonal antibodies in plant disease research. Ann. Rev. Phytopathology 23:
321-350.
7. Lankow, R. K., Grothaus, G. D., Miller, S. A. 1987. Immunoassays for crop management systems and agricultural
chemistry, in: Biotechnology in Agricultural Chemistry, ed. H. M. LeBaron, R. O.Mumma, R. C. Honeycutt, J. H.
Duesing. ACS Symposium Series 334:228-252, American Chemical Society, Washington, D.C.
8. Miller S. A. 1988. Biotechnology-based disease diagnostics. Plant Disease 72:188.
9. Miller, S. A., Martin, R. R. 1988. Molecular diagnosis of plant disease. Ann. Rev. Phytopathology 26:409-432.
10. Schmitthenner, A. F. 1962. Isolation of Pythium from soil particles. Phytopathology 52:1133-38.
11. Strandberg, J. 0.1986. Disease and pathogen detection for disease management, in: Plant Disease Epidemiology.
ed. K. J.Leonard, W. E. Fry. MacMillan Publishing Co., New York. pp. 153-179.
114
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TABLE 1
Reactivity of isolates of Pythium species associated with turfgrass In a double antibody
immunoassav using anti-Pythium aphanidermatum antibodies. Extracts of each isolate were
standardized at a protein concentration of 1.0 ug/ml. Absorbance values (405 nm) are represented
as the mean of all isolates tested.
Pythium species Number of Isolates Mean Absorbance
Tested (405 nm) *
E- aphanidermatum 10 >2.00
E- graminicola 1 >2.00
P. ultimum 2 >2.00
P. myriotylum 2 >2.00
P. aristosporum 1 >2.00
P. arrhenomanes 4 >2.00
P. torulosum 2 0.12
E. vanterpoolii 1 0.00
P. rostratum 1 0.09
1 Absorbance readings > 2.0 are off-scale.
115
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TABLE 2
Detection of Pythium spp. in perennial ryegrass and bentgrass golf course turf by the Pythium
detection assay and isolation from leaves using a selective medium. All samples were taken prior
to application of fungicides for control of pythium blight.
Turfgrass Symptoms*
Type
Pythium Kit Pythium Isolation
Meter Reading Frequency2
Bentgrass
Bentgrass
Bentgrass
Ryegrass
Ryegrass
Bentgrass
Bentgrass
Bentgrass
Ryegrass
Ryegrass
Pythium blight
Pythium blight
Pythium blight
Pythium blight
Pythium blight
None
None
None
None
None
37
25
43
28
36
22
20
26
22
15
5/8
0/8
3/8
3/8
.. 3 / 8
0/8
1/8
2/8
1/8
0/8
1 Asymptomatic turf grass samples were taken from areas within 10 ft
of symptomatic turfgrass.
2 Indicates the number of leaves/total plated on selective medium from
which Pythium spp. were observed to grow out.
116
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FIGURE 1
Dose response curve for the Pythium detection assay. The sensitivity limit of the assay, based
on fungal protein of Pythium aphanidermatum. is approximately 20 ng protein/ml.
200
.01
.1 1
[Fungal protein] tig/ml
10
100
117
-------
FIGURE 2
Prevalence of Pythium spp. in blighted patches and surrounding asymptomatic perennial
ryegrass during a severe outbreak of Pythium blight, determined using the Pythium detection assay.
In most cases, levels of Pythium spp. were highest at the edge of patches and lowest in the center
of patches. Asymptomatic ryegrass samples taken from areas in close proximity to symptomatic
areas also contained detectable levels of Pythium spp.
CD
c
-6
fC
0
cc
G
o
0
o
c
O)
03
50 -i
40 -
Middle
Edge
>2" Away
10 -i
7/12
7/13
7/14
7/14
7/15
7/18
Date in 1986
118
-------
FIGURE 3
Detection of Pythium spp. in perennial ryegrass (Fairway 7) and bentgrass (Green 4) using the
Pythium detection assay. Values represent the mean of two to four samples. Environmental
condition remained highly favorable for Pythium blight development through the testing period. An
application of a Pythium control fungicide was made on 7/10; Green 4 began to recover in the latter
part of the testing period, but symptoms persisted on Fairway 7. The dotted line in the figure
represents the threshold of positive detection for the assay.
O)
c
5
(0
o
cc
0
**
o
tf)
o
4-<
V)
o
c
O)
(0
50
40-
30-
20-
10-
-13— FAIRWAY 7
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co
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—3
O)
T
CM
T~
00
•*
>
-r
LO
T-
|
>
13
00
>-
DATE in 1986
119
-------
FIGURE 4
Results of a monitoring program for the detection of Pythium blight on Green 4 and Fairway 7
in 1987. Conditions favorable for Pythium blight occurred initially on May 29, and continued
intermittently until late July. Pythium spp. were detected by the assay on the collar of Green 4 on
May 29; however, regular application of Pythium control fungicides kept the pathogens at a
non-detectable level. No symptoms of Pythium blight occurred during the testing period. The dotted
line in the figure represents the threshold of positive detection for the assay.
50
O)
c
•O
«J
0)
DC
0)
40 -
30 -
to
o
1 20 H
o
c
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CO
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<
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—o — GREEN 4 (COLLAR)
—••—• GREEN4
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3 fe
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O O
DATE in 1987
120
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BIOLOGICAL MANAGEMENT OF TURFGRASS PESTS
AND THE USE OF PREDICTION MODELS FOR MORE
ACCURATE PESTICIDE APPLICATIONS
J. M. Vargas, Jr.; D. Roberts; T. K. Danneberger;
M. Otto & R. Detweller
Departments of Botany and Plant Pathology, and the Pesticide Research Center
Michigan State University
East Lansing, Ml 48824
Biological management of turfgrass pests, including some fungal diseases, insects, and weeds
is now possible. These management tools consist of cultural practices to encourage natural
predators as well as the direct application of beneficial organisms that are antagonistic to the fungal
pathogens.
Necrotic ring spot (MRS), caused by Leptosphaeria korrae. is a serious disease of Kentucky
bluegrass (Poa pratensis) in the northern areas of the cool season grass growing region. The
disease was formerly referred to as Fusarium blight and mistakenly believed to be caused by either
Fusarium roseum or Fusarium tricinctum. Koch's postulates were never completed for this disease
with either F. roseum or F. tricinctum. as all attempts to produce patch or "frog eye "symptoms in the
greenhouse or the field failed. Further investigation revealed a root pathogen associated with these
disease symptoms which was eventually identified as L korrae. Koch's postulates were completed
in both greenhouse and field Inoculation studies with L. korrae where actual patches and "frog eye"
symptoms were produced, providing the final proof of the true cause of this patch disease on
Kentucky bluegrass in the northern areas of the cool season grass growing region.
L. korrae is pathogenic to P. pratensis over a wide temperature range (15-28 degrees C.). L.
korrae attacks the root systems of Kentucky bluegrass plants primarily during the cool weather of
the spring and fall. The patches range in size from 7-8 cm up to 1 m in diameter. When the disease
occurs in cool weather, red and straw colored blades are intermingled in the infected area of the
patch. When the disease symptoms occur during the warm weather, the infected turf originally
appears as wilted turf, later turning to straw color.
Necrotic ring spot is currently managed by high rates (compared to rates normally used to
manage foliar turfgrass diseases like dollar spot or anthracnose) of the following fungicides:
benomyl, thiophanate, thiophanate-methyl, iprodione, and fenarimol.
IRRIGATION AND BIOLOGICAL MANAGEMENT
Studies of the environmental conditions necessary for necrotic ring spot symptom development
indicated low soil moisture was important. An irrigation study was established to determine the
effects of irrigation on necrotic ring spot. The treatment included a daily irrigation treatment
(1/107day), an 80% pan treatment (replacing 80% of the moisture lost from an evapro-pan twice a
week), and a no supplemental irrigation treatment. Each replication included three sub-treatments:
a muck sod, a mineral sod, and a seeded blend of three JEL. pratensis cultivars (Baron, Victa, Bristol).
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In 1986 and 1987 necrotic ring spot symptoms developed In the muck and mineral sod 80%
pan treatments and non-supplemental irrigation plots. No symptoms occurred in the daily irrigated
plots. This is believed to be due to the increase in the beneficial microbial populations. There was
an increase in the number of beneficial fungi, the number of actinomycetes (known producers of
anti-fungal compounds) and beneficial bacteria. The effect of these various organisms on the
development of necrotic ring spot is being investigated. Similar results have been observed in the
reduction of melting-out, caused by Dreschlera poae and leaf spot, caused by Biopolaris
sorokinianum in other irrigation studies. This disease reduction has been correlated to an increase
in microbial populations. Two other pests that have been reported to be managed by irrigation are
the chinch bug and bill bug. The possibility of managing five £L pratensis turfgrass pests biologically
through the cultural practice of irrigation now appears feasible.
BIOLOGICAL MANAGEMENT PRODUCTS
In May 1984 a curative study was established on a heavily diseased P, pratensis sodded area
in Novi, Michigan. The study was laid out with three replications of 1.83 x 2.44 m2 plots in a
randomized block design. The condominium site at Novi was irrigated with an automatic irrigation
system and in 1984 received, in addition to our treatments, the same four fertility and herbicide
treatments as the rest of the complex, including a total of 180 kg N/ha. In 1985 and 1986 this area
did not receive any additional fertilizer treatment other than those we applied. Green Magic and
Soil Aid were applied using a CO2 small plot sprayer at a volume of 454.2 I/ha., equipped with a
.914 m boom. Lawn Restore was applied by hand to individual plots. The results of Green Magic
plus Soil Aid and Lawn Restore when compared to a nitrogen check can be seen in Table 1. They
show complete recovery in the Green Magic plots when treatments were applied three times a year
in May, July, and September at a 480 kg/ha rate. The amount of necrotic ring spot increased 303%
during the same period of time.
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TABLE 1
Mean percent reduction3 in necrotic ring spot patches from 5/23/84 to 8/14/86 at Novi, Michigan.
Treatment Month of Application 8/14/86 meansep.c
mean % redb
Green MJO 100 a
Magic
Lawn MJS 100 a
Restore
Check AS -303 b
(46)0)0)
a Calculated by subtracting number of patches per plot on 8/14/86 from the number on 5/23/84,
dividing this by the number present on 5/23/84, and multiplying by 100.
b Percent disease reduction. Mean of three replications.
Means followed by the same letter are not significantly different by LSD (.05).
c
Biological management of soil-borne disease through the use of microbes can act through two
mechanisms. The first is competition for nutrients in the thatch and soil between the beneficial
microorganisms and the pathogens. By utilizing available nutrients, they can deny the pathogens
the nutrients needed to stimulate germination of resting structures (spores or sclerotia) and, after
germination, they can deny them the nutrition needed to grow saprophytically to reach the root of
the host plant for infection. The second feasible mechanism is the production by beneficial
microorganisms of substances that are antagonistic to the germination and growth of soil-borne
pathogens. The latter has been demonstrated under laboratory conditions with the microorganisms
in Lawn Restore. Replicated studies conducted by Michigan State University over the past six years
with Lawn Restore, Green Magic, and Strengthen and Renew have shown significant reduction in
the amount of necrotic ring spot disease compared to the untreated controls.
There are two general categories of products involved in the biological management of necrotic
ring spot. One category of products improves the thatch and soil environment to encourage higher
levels of beneficial microbial activity and the other adds the beneficial microorganisms to the thatch
and soil. Products developed by the Agro-Chem Corporation of Franklin Park, Illinois are in the first
category. Soil Aid is designed to flush thatch and soil of substances that are toxic to sustaining high
levels of microbial activity. It is an enzymatic type wetting agent. This treatment is followed by Green
Magic or Strengthen and Renew, which are products that contain major and minor nutrients as well
as plant and microorganism extractions. They have been shown to reduce the growth of L korrae
in laboratory culture work and increase natural microbial populations in the field. The use of Green
Magic or Strengthen and Renew have been shown, under field conditions, to allow existing necrotic
ring spot patches to recover and to prevent the development of new ones when used on a regular
basis.
The Ringer Corporation, of Minneapolis, Minnesota, produces a product in the second
category. It is an organic fertilizer consisting of bone meal, feather meal, soybean meal, and other
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protein sources. This is supplemented with Actinomycete fungi and bacteria in the genus Bacillus,
The product is called Lawn Restore. The microorganisms in Lawn Restore have been shown to
produce substances in laboratory culture tests that are antagonistic to L. korrae. Lawn Restore has
been shown to promote the recovery of necrotic ring spot patches and to prevent the development
of new ones under field conditions when used on a regular basis.
Leptosphaeria korrae. the cause of necrotic ring spot in turfgrass, is a soil-borne pathogen
that has been successfully managed by the use of beneficial microorganisms. It must be
remembered that these products are not like fungicides that can be applied one time, halting the
spread of the fungus and allowing the grass to recover. In order to be effective, Lawn Restore,
Green Magic, and Strengthen and Renew must be applied on a regular basis, either monthly or
bi-monthly, throughout the growing season to change the biological makeup of the thatch and soil
environment.
POA ANNUA MANAGEMENT
Poa annua (annual bluegrass) is composed of two types: Poa annua c.v. annua. a true annual
type, and Poa annua c.v. reptans. a perennial type. Both types are considered weeds in turfgrass
stands. P. annua is the number one weed problem on golf courses in the northern United States.
The annual type is managed mainly with pre-emergence herbicides, whereas the perennial type is
primarily managed by post-emergence herbicides like the arsenicals. Neither chemical has been
very successful in preventing the encroachment of FL annua into the species that were originally
planted, in addition, the arsenicals are highly toxic compounds that present a hazard to both people
and the environment. Xanthomonas campestris has been successfully tested under laboratory
conditions for the management of EL annua. The bacterium infects the xylem tissue of the P. annua
plant where it interferes with the uptake of water and nutrients. The infected plants wilt and die from
the lack of water and nutrients. The bacterium is very specific for P. annua and all attempts to infect
other grass species have been unsuccessful. The new biological control for the management of EL
annua will certainly be safer for people to use, to play golf on after application, and safer for the
environment. Hopefully, it will be more effective in managing P. annua than the pesticides that are
currently being used.
ADVANCEMENT OF COMPUTER MODELS
More precise models for the prediction of disease development are being developed today
because of advancements in computer technology and weather-gathering equipment. Most
turfgrass diseases occur under certain environmental conditions, provided there is a susceptible
host and a virulent pathogen present. The environmental parameters are: air temperature, soil
temperature, soil moisture, leaf wetness, and relative humidity. Although not all of these
environmental factors are involved in the development of every disease, at least two of them are
involved in ail disease development. Mathematical models to predict disease occurrence can be
developed by measuring these factors, recording them over a period of time, and correlating them
with disease outbreaks. These models can then be used to make more accurate fungicide
applications based on environmental conditions, rather than applying them on a calendar or
preventive basis.
Most golf course superintendents would like to apply fungicides at the most appropriate time
to achieve maximum disease control for the least amount of money. This not only involves the
money spent on fungicide, but labor cost to apply them, plus the wear and tear on the spray
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equipment. Another consideration that has to be taken into account when applying pesticides is the
environment. No one wants to put more pesticides into the environment than necessary.
COMPUTERIZED DISEASE MODELS
These disease models were developed by collecting hundreds of thousands of data points,
analyzing them in various ways to determine which correlate best with disease development. This
would be impossible to do without the use of a computer, which is one of the reasons effective
disease prediction models have only recently been developed. Once the computer analyzes the
data and it is determined which information is pertinent, a mathematical model is developed. This
prediction model is first tested under controlled environmental conditions in the laboratory where
appropriate adjustments are made. Then the prediction model is tested under field conditions for
validity. It usually requires a minimum of two seasons, with three being preferred.
Once the model has been validated and any necessary corrections made, it is ready for the
end user. This can be a time consuming process if the data must be collected from several different
weather-measuring instruments, put into the formula and analyzed by the computer. However, if the
model is placed in a microprocessor that can record all the weather and environmental data, analyze
it and incorporate it into the model, then the task is much more quickly completed.
Although this sounds like science fiction from the 21st century, this technology is here today.
Neogen Corporation's PestCaster has a Pythium blight model, an anthracnose model, and an
annual bluegrass seedhead-emergence model. This microprocessor will collect the weather
information, assimilate it into the models, and indicate when it is necessary to make a fungicide
application.
ANTHRACNOSE DEVELOPMENT
Anthracnose, caused by Colletotrichum graminicola. is a devastating disease of annual
bluegrass that can cause severe turf loss on golf course greens, tees, and fairways during the warm
weather of July and August. To prevent this from occurring, golf courses normally treat their fairways
three to four times a year on a preventive or calendar basis to prevent the disease from occurring.
However, depending on location, anthracnose does not occur every year, nor do out-breaks occur
all season long every year. Sometimes anthracnose outbreaks only occur once during a two to three
month period in any summer. However, without a reliable system to predict the occurrence of
anthracnose, the golf course superintendent has little choice but to treat the greens, tees, and
fairways on a preventive or calendar basis. The same can be said about fungicide treatments for
Pythium blight. It is too devastating a disease not to treat it on a preventive or calendar basis, unless
one has access to an accurate predictive model. With these two models, fungicides can be applied
only when needed, only when environmental conditions are present for disease development. This
will result in more accurate treatment of these two diseases, more cost effective treatment of these
diseases, and less fungicides being applied to ^environment. This mathematical model was
developed from over 150,000 individual data points. It has now been field tested for over six years.
It has a 95% plus accuracy rate in predicting anthracnose outbreaks.
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PYTHIUM BLIGHT MODEL
The second model is for Pythium blight, caused by Pythium aphanidermatium. which can be
a devastating disease when it occurs. Pythium blight is a fast developing disease which can wipe
out the majority of the turf on a golf course in a 24-hour period if environmental conditions for disease
development are optimum. Because of this, most golf courses treat Pythium blight on a preventive
basis. However, in many areas of the United States the disease does not occur every season.
Even in areas where it does occur every season, it does not occur all season long. But, in an attempt
to prevent Pythium blight from occurring and to maintain their jobs, often superintendents make
unnecessary applications of fungicides. The use of the Pythium blight model can eliminate
unnecessary fungicide application, reduce the cost of treating for Pythium blight, and reduce the
amount of fungicides being applied to the environment. Other disease prediction models are being
developed for other diseases, which will allow turf managers to apply fungicides only as needed for
these problems as well. Hopefully, the day will come when all fungicides are applied based on
disease models, which should reduce the cost of application by eliminating unnecessary treatments,
while giving the desired level of disease control. This will also result in a significant reduction in the
amount of fungicides being applied to the environment.
SUMMARY
Root pathogens like k korrae and weeds like FL annua can now be managed biologically.
Fungicides can be applied based on computer prediction models for diseases such as anthracnose
and Pythium blight, which will reduce the amount of fungicides being put into the environment. The
turfgrass area has already made great strides in reducing fungicide usage and, hopefully, this trend
will continue in the future.
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MANAGING THE SCARAB GRUB PEST COMPLEX
IN TURFGRASS:
SOME ECOLOGICAL CONSIDERATIONS
M. G. Villani and R. J. Wright
Department of Entomology
NYSAES/Cornell University
Geneva, New York 14456
INTRODUCTION
The scarab grub complex attacks a variety of crops in the Northeast including turf and grassy
pastures, and woody ornamentals. The Japanese beetle, Popillia japonica Newman (JB), is the
most abundant and widely distributed species of the group, but other important species include the
European chafer, Rhizotrogus majalis (Razoumowsky) (EC), Oriental beetle, Anomala orientalis
Waterhouse (OB), Asiatic garden beetle, Maladera castanea (Arrow) (AGB) and Northern masked
chafer. Cyciocephala borealis Arrow (NMC). All species cause considerable damage as immatures
and at least one, the Japanese beetle, causes heavy damage to a wide variety of agricultural and
horticultural crops through adult feeding (41 and citations within). Historically, insecticides have
been the major control tactic used against these insects, however, because many of the plants
attacked by these grubs are grown in urban or suburban areas (golf courses, parks, home lawns
and gardens, landscaping around commercial buildings) the potential for human exposure to
insecticides through application or environmental contamination is great. Pesticide contamination
of groundwater (from undetermined sources) has occurred in several areas of the Northeast (e.g.,
aldicarb, oxamyl and carbofuran on Long Island) and there have been instances of bird kills
associated with use of diazinon on golf courses. Effective long-term control of the scarab grub
complex was achieved with organochlorine and cyclodiene insecticides until their use was
discontinued through insect resistance and government intervention; less consistent control has
been achieved with organophosphate and carbamate insecticides (2, 45) and with a variety of
biological agents (nematodes, fungi, bacteria and viruses) (27,46, 49).
One reason for this inconsistency may be the lack of basic understanding in the interaction of
the control tactic (chemical, biological or genetic), the cropping system, the target insect, and the
soil physical and biotic environment (soil moisture, temperature, texture, compaction, and microbial
flora etc). While each of these factors has been independently studied to varying degrees by basic
and applied researchers, their interdependence has largely been ignored. If we assume that a
combination of management tactics (IPM) will be required to effectively and safely manage scarab
grubs in turfgrass in the future then the nature of specific interactions between target insect
population(s), control agent(s) and the soil environment must be examined. In this chapter we will
focus on the management of the scarab grub complex in turfgrass and discuss how 'ecological'
approaches to this problem may help control scarab grubs more effectively.
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SCARAB GRUB BEHAVIOR
C. R. Harris in reviewing the problems of controlling soil insects with insecticides in general
(21) and soil insects in turf in particular (22) suggests:
"During the past 20 years this problem (lack of efficacy of short residual insecticides in
controlling soil insects) has received considerable attention and a number of factors have
been shown to influence insecticide activity in the soil including: the physiochemical
properties of the insecticide; soil and climactic factors; insect susceptibility to insecticides
and insect behavior in the soil...a factor that has received little attention, other than in a
very general sense, is the way insect behavior will influence the effectiveness of soil
insecticides...for the immediate future, the most promising research possibilities are in the
area of soil insect ecology. With greater comprehension of the factors influencing the
behavior and development of soil insects, it would be possible to utilize insecticides far
more effectively"
Much of the available literature on the impact of soil physical properties on the movement
behavior of members of the scarab grub complex has recently been reviewed by Tashiro (41 and
references within [1, 8, 11,12, 14, 15, 16, 17, 18, 19, 20, 24, 25, 35, 37 ,38, 43]) Although previous
research has often been qualitative or anecdotal some interesting patterns do emerge. Briefly we
would like to outline what is known about five species of scarab grubs (JB, EC, OB, NMC, AGB)
which are of major economic importance in the Northeast and share similar life history patterns. All
five species have somewhat similar seasonal patterns of vertical movement of grubs in response
to gross temperature changes. After hatching, larvae feed at or near the soil surface from
mid-summer to late fall. As surface temperatures cool grubs migrate down into the soil and
overwinter as late instar larvae below the frost line. In the spring grubs migrate back to the surface
again in response to temperature changes, complete feeding and move down again into the soil
profile to pupate and eclose. Field observations indicate that EC grubs remain at the soil surface
later in the fall and return to the soil surface earlier in the spring than do the other four grub species.
Confounding this yearly temperature moderated movement pattern there may be more localized
response to changes in soil moisture as well. Grubs have been reported to move deeper in the soil
in response to decreasing soil moisture. Most of the observations concerning response to moisture
are anecdotal. Even under 'favorable conditions' of soil moisture and temperature, field reports
indicate that different grub species tend to be found at different soil levels; for example, EC and
AGB tend to feed further below the soil surface than either JB or OB grubs. The differences in
preferred feeding depths of different grub species have an effect on the types of plant tissues
attacked. Grubs such as the EC, which feed for a longer period of time, have a greater potential
effect per grub than do other grub species that leave the surface earlier in the fall and return later
in the spring. AGB are normally less destructive than JB or OB grubs to turf, in part due to the
tendency of these grubs to feed at greater depths which results in less damage (however due to
their greater depth AGB may be much more difficult to manage with non-mobile chemical
insecticides).
Information concerning the behavior of soil insects is anecdotal in most instances due to the
difficulty in studying insect behavior under 'natural' conditions. There is a general perception that
such research, if not impossible, is difficult, tedious, and cost ineffective when compared with similar
studies of above ground insects. This attitude toward soil insect research has resulted in a situation
where the soil ecosystem is treated as a 'black box' in which the consequences rather than the
processes of insect behavior are measured. While there have been many studies looking at the
movement of soil insects over long periods of time (3, 4, 5, 7, 10, 13,, 23, 29, 30, 31,) the studies
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tend to lump the soil insects found in the top 5 cm as being at the surface layer. It is clear from
insecticide movement studies in turfgrass systems that the details of grub movement within the top
5 cm over relatively short periods of time can have a profound effect on management.
Villani and Gould (44) have developed an x-ray technique that makes it possible to study soil
insect movement and behavior within heterogeneous soil blocks.We have expanded this technique
to include studies with several species of scarab grubs in larger arenas (up to 35 cm by 12 cm by
43 cm) and with field-collected soil blocks. Soil blocks retain their field characteristics (compaction,
heterogeneity, endemic floral and faunal communities) and therefore allow for the careful monitoring
and manipulation of the system for long periods of time. During the past year we have been gathering
data from both simulated field soils (soil profiles created in the laboratory through the use of a variety
of field soils) and actual field soil blocks extracted from turfgrass pasture plots (see 47 for details
of experimental design and analysis for studies concerning radiographs outlined below).
Work in our laboratories with radiography indicates there is a species-specific response of
scarab grub species to changes in moisture and temperature in the soil profile (47). These studies
simulated the effects of irrigation and drought and temperature flux on populations of several scarab
grub species. NMC, JB and OB and EC grubs all showed a strong trend for moving downward into
the soil profile as soil moisture declined at the soil surface and turf root zone and movement back
to the root zone when irrigated with the equivalent of 1 cm. of distilled water; EC grubs exhibited the
least sensitivity to drying soil which may be related to their ability to rapidly escape from extreme
conditions.
There were significant differences among grubs (EC, JB, and OB) in their responses to
fluctuating temperatures. Shifts in soil temperature (decreasing from 20 to 5 C over 5 week period)
had very little impact on the position of EC grubs. This relative unresponsiveness to temperature
flux conforms to field observations (41, M. G. V. personal observations) which indicate that EC grubs
are often found in the turf root zone well into early winter and early spring, and at times feeding In
the root zone under snow if this zone is not frozen. In contrast, there was a marked response to
shifting temperatures with the other two scarab species. JB grubs fed in the root zone in the stable
temperature regime (constant 20 C) while in the shifting temperature regime grubs moved from the
root zone downward with the onset of cooling soil (14 C) and returned to the surface as temperatures
increased back up to 20 C. OB grubs appeared more variable but there was a clear population trend
for grubs to remain at the root zone in the stable treatment (constant 20 C) and to respond to lower
soil temperatures (8 C) by moving down into the soil profile . An increase in soil temperatures
appeared to move a portion of the OB grub population back to the root zone while not affecting the
median population value.
These studies demonstrate species-specific differences in scarab grub response to changing
temperature and moisture conditions in simulated turf systems which conform to reported field
reports. These differences involved both changes in the population median and the overall
population distribution. Increased knowledge of species-specific movement patterns of scarab grubs
in turfgrass in response to these and other soil environmental factors will have practical applications
in developing more effective management systems for these soil insects in that they will help
determine the probability of overlap of a specific grub species with a specific control agent in space
and time, suggest depth to which sampling for grubs must occur in sampling and monitoring
programs and indicate the 'hidden1 population of grubs when sampling within the turfgrass root zone.
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IMPACT OF IRRIGATION ON SCARAB GRUB BEHAVIOR AND
INSECTICIDE MOVEMENT, PERSISTENCE, AND EFFICACY
Understanding the behavior of soil insects found in turfgrass is important considering the
difficulty in moving soil insecticides down into the root zone of established turf. Physical factors that
result in the movement of target insects as little as 1 cm into the soil profile may put these insects
out of the effective active zone of chemical and biological control agents. Conversely, highly mobile
soil insecticides will move beyond the root zone and will again be ineffective in controlling soil insect.
Several studies (39, 28, 33) have shown that, unlike the cyclodiene soil insecticides, the less
persistent organophosphate and carbamate insecticides degrade quickly, leaving little time for
movement into the soil and roots. Diazinon applied to turf degrades so rapidly that < 1% of the
original concentration is present in the root zone 14 days after treatment (39). Chlorpyrifos is
considered one of the more persistent OP insecticides but Kuhr and Tashiro (28) found < 1% of the
original concentration of this pesticide could be recovered from the thatch-root zone 56 days after
application. These results indicate that there is a relatively narrow window in which turf insecticides
can be applied to obtain consistent control. Niemczyk (32, also 33,34) reports that virtually no
insecticide applied to turf for scarab grub control actually reaches the soil surface if appreciable
levels of thatch are found at the surface. The generally low persistence, low solubility and high
organic binding properties of soil insecticides labelled for turf insect control have led to a situation
where soil insecticides may not be reaching the target population in the field.
It has been noted that soil insecticides are more effective in controlling scarab grubs in turfgrass
when they are irrigated into the soil with at least 1 cm of water. It has been assumed that this irrigation
helped move the active compound off the turfgrass and from the soil surface to the root zone where
scarab grubs were feeding. Recent studies by Niemczyk (32) and Niemczyk et. al (34) suggest that
little if any active material is moved into the soil through irrigation. A study (see 47 for detail on
experimental design and analytic procedures) reviewed below, proposes an alternative hypothesis
to explain increased insecticide efficacy with the use of irrigation: irrigation moves scarab grubs up
to the surface rather than moving the insecticide down to the grubs in the soil profile.
Studies were conducted in plexiglass arenas (35 cm by 5 cm by 43 cm) filled with sieved loamy
sand soil. Arenas were seeded with grass seed and ten third instar EC grubs were placed at the top
of each arena; grubs which did not dig into the soil within 1 h were replaced. There were eight
replications of each of the following treatments:
Treatment Isofenphos (Oftanol 1.5G) Amount of water added
1 2.24 kg (Al) per ha 50 ml {= 0.33 cm irrigation)
2 2.24 kg (Al) per ha 150 ml (= 1.0 cm irrigation)
3 none 50 ml
4 none 150 ml
Arenas were x-rayed at 0,24, 96,166, and 360 h posttreatment. Residue samples were taken
at 24 h posttreatment from additional infested and treated arenas receiving treatments 1 and 2.
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Grub condition (normal, moribund or dead) and location (depth below soil surface) was
recorded at the end of the study (360 h posttreatment). Soil moisture was measured gravimetrically
at this time by taking samples at intervals through the soil profile from all arenas. Residue samples
were taken from the soil surface and at intervals through the soil profile of treated arenas and
analyzed by standard analytic procedures.
The results indicate that there was little movement of insecticide past the 0-2.5 cm level of
soil regardless of the irrigation applied (Table 1). There was a significant loss of active material
(percent recovered) in the high moisture treatment after 360 h when compared with the dry condition.
A significant portion of the insecticide recovered remained on the soil surface unavailable for insect
control in both treatments. Percent control was identical in both treatments after 15 days. However,
there was a higher proportion of morbid grubs in the higher moisture treatment; morbid grubs will
die within 14 days in most cases (M. G. V., unpublished data). These results confirm that insecticides
are not moving into the profile in response to simulated irrigation and suggest that grub mortality
will be higher in high moisture plots despite lower total insecticide recovery.
Figure 1 shows the shift in the soil moisture profile for the high and low moisture treatments
over the duration of the experiment. Twenty-four h after water was added to the low moisture arenas
the percent moisture in the soil profile remained fairly uniform with a slight (but important) rise in the
first 2.5 cm; the soil continued to dry up to 360 h when a strong moisture gradient was observed.
Twenty-four h after moisture was added to the high moisture arenas there was a strong trend for
decreased moisture with increased soil depth. Soil moisture remained uniformly high but there was
a slight (but important) drop in the top 2.5 cm of soil. Data on grub position in each treatment (Fig.
2) were grouped at levels which are important with regards to the observed pesticide movement in
the arenas (Table 1); 0-2.5 cm deep (high insecticide concentration), 2.5-5 cm and greater than 5
cm (no insecticide detected [< or equal to 045 ppm]). The following points can be made based on
these data. First, addition of water brought grubs to the surface in all treatments (data at 24 h).
Second, the activity of the insecticide (as indicated by the general lack of grub movement in
response to changing soil factors when compared with non-treated boxes) becomes apparent in
both moisture regimes between 96 and 166 h. There is a slight difference in grub population
distribution within moisture regimes between control and treated arenas. Third, differences in grub
population distribution between moisture levels in the control arenas begin to occur at 96 h ; i.e.,
grubs in low moisture control arenas begin to move down in the profile while those in high moisture
regime remain near surface, potentially in contact with insecticide. And finally, grubs in high moisture
control plots begin to respond to a slight decline in soil moisture at 166 h. Note that moisture levels
at 360 h in these arenas are greatest in the greater than 5 cm level. Clearly soil moisture flux within
the profile had a profound effect on both insecticide persistence and EC grub movement patterns
in this study and these effects influenced the efficacy of isofenphos in the soil.
SPECIES-SPECIFIC SUSCEPTIBILITY OF SCARAB GRUBS TO
TURFGRASS INSECTICIDES
Many factors, including soil pH, organic matter, moisture, thatch, insect behavior and microbial
degradation of insecticides influence the efficacy of currently registered insecticides, (6,21,22,28,
33, 36, 42 47 48). One factor contributing to the variable control of scarab grubs in the field is the
presence of mixed-species populations of grubs, which may exhibit species-specific insecticide
susceptibilities. Although field insecticide efficacy studies against mixed populations of scarab grubs
have been reported (e.g.,9, 50), significant treatment effects can be demonstrated only for the
most abundant grub species,because secondary species are often present at low densities and
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their distribution is patchy. Previous work by Baker (2) has demonstrated among- and within-species
variation in susceptibility of New York populations of Japanese and Oriental beetle larvae to
chlorpyrifos, bendiocarb and isofenphos. Additional research in New York State (45) was done to
provide more information on the susceptibility of three economically important scarab grub species
to five currently labelled turf insecticides (diazinon, chlorpyrifos, isofenphos, bendiocarb and
ethoprop). This laboratory study indicated that, in general, EC grubs are less susceptible to soil
insecticides than the other two scarab grub species (Table 2). This finding agrees with reports from
extension agents and turfgrass and sod producers in New York State. Several statistically significant
interactions were found which indicated the need to study each species-insecticide combination
separately. The most striking insecticide - scarab grub species interactions involved diazinon and
chlorpyrifos. Diazinon provided good control of OB and EC grubs, but very poor control of JB larvae.
However, chlorpyrifos provided good control of JB and OB, but very poor control of EC grubs. Since
behavioral differences among grub species (i.e., their characteristic position in the soil profile in the
field which may influence exposure to insecticides) have been eliminated in these studies,
differential mortality of JB and EC grubs to diazinon and chlorpyrifos may reflect species-specific
tolerances to these compounds (if testing of additional populations give similar results) or localized
insecticide resistance. The relatively low level of mortality observed with all grub species in the
isofenphos treatments may be attributed to a number of causes including: loss of activity of the
compound through microbial degradation due to an 'activated' test soil, insufficient initial product,
and insufficient time for mortality to be apparent; discrimination tests undertaken in future studies
should be done with higher rates of this product. Ethoprop treatments induced uniformly high
mortality with all scarab grub species tested indicating either similar tolerance to this material or
application rates too high for discrimination among species.
The results of these studies indicate the need to develop species-specific insecticide
recommendations for the scarab grub complex, and to encourage those responsible for insecticide
use in turf to be aware of the scarab grub species present in their areas. Although single species
infestations occur in some areas of New York, mixed populations of JB and EC grubs (western
section of state) or JB and OB grubs (Long Island) and other scarab grub species are the rule rather
than the exception. Our results suggest that, with some insecticides (e.g., diazinon and chlorpyrifos),
intermediate levels of control of the overall scarab grub population may reflect high mortality of one
species and little or no mortality of one or more co-existing species. Depending on the relative
abundance of each species at a given site, percent control achieved with each insecticide may vary
widely. Differences in insecticide susceptibility among species of the scarab grub complex need to
be considered, as well as the possibility of insecticide resistance, microbial degradation, or
inadequate application procedures, as a possible reason for control failures after use of turf
insecticides.
BIOLOGICAL CONTROL OF SCARAB GRUBS: PATHOGEN/INSECT
INTERACTIONS
Development of biological controls for soil insects such as scarab grubs would provide an
alternative to the use of chemical insecticides and would alleviate many of the problems associated
with insecticide use (development of insecticide-resistant pest strains, environmental pollution).
We have found it useful to group pathogenic agents used to control soil insects in turf based on
their mobility and their reproductive behavior. The first are agents that interact with the soil
environment and the target species much like a soil insecticide, an example of this type of agent is
Bacillus thuringiensis (Bt) toxin. The material is non-mobile (passive movement through profile only)
132
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and non-replicating, therefore contact between toxic agent and target insect is determined by
passive movement of the agent and activity of the target. The second class of control agents are
those that are non-mobile but replicating (e.g. Bacillus popilliae. Beauveria bassiana and
_Metarrhizium anisopliae). Unlike soil insecticides and Bt, the behavior of the target insect is vitally
important to the spread of the pathogen: infected grubs, which respond to environmental conditions
and/or pathogen induced aberrant behavior, may move the control agent out of the range for
effective control by moving the site of agent replication outside of the normal range of the target or
the optimal range of agent replication. If for example scarab grubs infected with milky disease move
down into the soil profile in response to environmental conditions and then die, this movement
would effectively reduce milky disease spore levels from the upper soil profile. Since it is only in the
upper profile that grubs would be actively ingesting spores (needed for infection) and where soil
temperatures are sufficient for spore replication (see 41) this movement would effectively halt
significant disease spread and insect control. Finally, there are those agents that are both mobile
and replicating such as entomogenous nematodes (e. g. Steinernema feltiae) which have been
discussed at length in previous chapters of this book (insect parasites and predators can be
generally included in this third class of agent). These agents are interesting ecologically because
infection and replication depend on the interaction of the soil environment on both agent and target.
Initial infection and subsequent spread through the target population depends upon the overlap of
agent and target in both space and time within the soil environment. We believe that this class of
control agent has great potential for controlling soil insects when incorporation of control agent is
not possible (47, 49).
CONCLUSIONS
The relative lack of success in predicting scarab grub damage in turfgrass and the costs
involved in achieving satisfactory control dictates a more systematic and comprehensive research
effort. Paramount to such an approach is the ability to monitor grub response to static and dynamic
soil factors and to manipulate these factors to determine changes in insect response. Understanding
the fundamental differences in behavioral response among the various grub species within the
complex to a variety of typical soil factors will enhance our ability to predict the stress each species
will inflict in turf and other horticultural plant species. An understanding of the interaction of the
control agent (biological or chemical),with the target insect species and with the soil environment
will lead to changes in current management practices which will allow for greater overlap in agent
and target leading to a greater potential for effective management.
133
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134
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TABLE 1
Residue analysis and effect on EC larvae of surface applications of isofenphos (Oftanol 1.5G)
under two different moisture regimes.
Isofenphos residues
EC larvae
Treatment Time Depth
Dry
Moist
Dry
Moist
(h) (cm)
24 0-2.5
>2.5
24 0-2.5
>2.5
360 0-2.5
>2.5
360 0-2.5
>2.5
ppm
2.78
ND3/
1.92
ND
2.67
ND
1.07
ND
% Recovered %on surface
62.50
74.00
65.25 47.38
26.75 47.53
% Control % Normal
28.4 56.8
28.4 33.3
3/ ND = non-detectable (< 0.045 ppm).
Source: Vfflani and Wright (1988b)
135
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TABLE 2
Efficacy of five turf insecticides against last stage larvae of three scarab grub species in a
laboratory soil bioassay; insecticides were incorporated into soil at one-half labelled rates. Analysis
of variance of percent control (angular transformed) of grubs after five weeks indicates significant
differences among insecticides (df=4, F= 13.201, P < 0.001) and grub species (df=2, F=6.066, P <
0.01). There was also a small but significant insecticide by grub species interaction (df=8, F=3.255,
P<0.05).
Treatment Percent Mortality
QB JB EC
Chlorpyrifos 74 91 21
Bendiocarb 75 70 37
Ethoprop 100 99 95
Diazinon 93 25 78
Isofenphos 26 38 11
Source: Villani et. al. 1988
136
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FIGURE 1
Soil moisture profile for high and low moisture treatments at beginning and end of study of
interaction of soil moisture and isofenphos persistence and efficacy against scarab grubs. Histogram
bars indicate (left to right) % moisture at the 0-2.5, 2.5-5.0, 50.-7.5, 7.5-15.0, 15.0-22.5 and
22.5-30.0 cm soil depths.
LOW MOISTURE
ui
c
i
10
UJ
a
360
D 9-12
tlm*
HIGH MOISTURE
360
D 9-12
time
-------
FIGURE 2
The distribution of EC grub populations in arenas maintained at high and low moisture levels
with and without addition of isofenphos to the surface. Histogram bars indicate (left to right) percent
of EC population at the 0-2.5, 2.5-5.0 and greater than 5.0 cm depth.
LOW MOISTURE/TREATED
HIGH MOISTURE/CONTROL
100
24 96 166 360
DEPTH
• 0-1
D 1-2
E3 >2
time
166
360
LOW MOISTURE/CONTROL
HIGH MOISTURE/TREATED
100
DEPTH
• 0-1
n 1-2
E3 >2
24 96 166 360
tlm0
100
Q.
2
m
E
O
20-
360
138
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24. Hayes, W. P. 1918. Studies on the life histories of two Kansas Scarabaeidae. J. Econ. Entomol. 11:136-144.
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32. Niemczyk, H. D. 1987. The influence of application timing and posttreatment irrigation on the fate and effectiveness
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80:465-470.
33. Niemczyk, H. D. and H. R. Krueger. 1982. Binding of insecticides on turfgrass thatch, pp. 61-63. in H. D. Niemczyk
and B. G. Joyner [eds.], Advances in Turfgrass Entomology. ChemLawn Corp., Worthington, Ohio.
34. Niemczyk, H. D., Z. Filary, and H. Krueger. 1987. Movement of insecticide residues in turfgrass thatch and soil.
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soil temperature and rainfall patterns. Environ. Entomol. 10:793-797.
36. Racke, K. D. and J. R. Coats. 1987. Enhanced degradation isofenphos by soil microorganisms. J. Agric. and Food
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37. Regniere, J., R. L Rabb, and R. E. Stinner. 1981. Popillia japonica: seasonal history and associated Scarabaeidae
in eastern North Carolina. Environ. Entomol. 10:297-300.
38. Schwardt, H. H. and W. H. Whitcomb. 1943. Life history of the European chafer, Amphimallon majalis. J. Econ.
Entomol. 36:345-346.
39. Sears, M. K. and R. A. Chapman. 1982. Persistence and movement of four insecticides applied to turfgrass. pp
57-59. In Niemczyk, H. D. and B. G. Joyner [eds.], Advances in Turfgrass Entomology. ChemLawn Corp.,
Worthington, Ohio.
40. Smith, W. G. and G. M. Wilson, [eds.] 1987. 1988 New York State Pesticide Recommendations. Chemicals-
Pesticides Program, College of Agric. and Life Sciences, Cornell University, Ithaca N. Y.
41. Tashiro, H. 1987. Turfgrass Insect of the United States and Canada. Cornell University Press, Ithaca N.Y.
42. Tashiro, H. and R. J. Kuhr. 1978. Some factors influencing the toxicrty of soil applications of chlorpyrifos and diazinon
to European chafer grubs. J. Econ. Entomol. 71:904-907.
43. Tashiro, H., G. G. Gyrisco, F. L. Gambrell, B. J. Fiori, and H. Brertfeld. 1969. Biology of the European chafer,
Amphimallon majalis (Coleoptera:Scarabaeidae) in northeastern United States. New York State Agric. Exp. Sta.
Bull. 828, 71 pp.
44. Villani, M. G. and F. Gould. 1986. Use of radiographs for movement analysis of the corn wireworm, Melanotus
communis (Coleoptera:Elateridae). Environ. Entomol. 15:462-464.
45. Villani, M. G., R. J. Wright, and P. B. Baker. 1988. Differential susceptibility of Japanese beetle. Oriental beetle,
and European chafer (Coleoptera:Scarabaeidae) larvae to five soil insecticides. J. Econ. Entomol. 81: in press.
46. Villani, M. G.and R. J. Wright. 1988a. Entomogenous nematodes as biological control agents of European chafer
and Japanese beetle (Coleoptera:Scarabaeidae) larvae in turf. J. Econ. Entomol. 81:484-487.
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47. Villani, M. G.and R. J. Wright. 1988b. Use of Radiography in Behavioral Studies of Turfgrass Infesting Scarab Grub
Species (Coleoptera:Scarabaeidae). Bull. Entomol. Soc. Am. (in press)
48. Vittum, P. J. 1985. Effect of timing of application on effectiveness of isofenphos, isazophos, and diazinon on
Japanese beetle (Coleoptera:Scarabaeidae) grubs in turf. J. Econ. Entomol. 78:172-184.
49. Wright, R. J., M. G. Villani, and F. Agudelo-Silva. 1988. Steinernematid and heterorhabditid nematodes for control
of larval European chafers and Japanese beetles (Coleoptera:Scarabaeidae) in potted yews. J. Econ. Entomol.
81:152-157.
50. York, A. C. [ed.] 1986. Insecticide and Acaricide Tests. Vol. 11. Entomological Society of America. College Park Md.
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INFLUENCE OF FERTILIZATION AND IRRIGATION
PRACTICES ON WATERBORNE NITROGEN LOSSES
FROM TURFGRASS
A.J. Gold, W.M. Sullivan, and RJ. Hull
Departments of Natural Resources Science and Plant Sciences
Contribution Number 2445 From the Rhode Island Agrlc. Exp. Sta.
University of Rhode Island
Kingston, Rl 02881
INTRODUCTION
Nitrogen constitutes the largest chemical input routinely applied to well maintained turf.
Nitrogen fertilizers are applied in a variety of forms, ranging from slow release types, such as
methylene urea, to quick release formulations, such as ammonium nitrate. Regardless of the
formulation applied, nitrogen not taken up by growing plants or soil microorganisms is readily
transformed to nitrate-nitrogen. Figure 1 summarizes the nitrogen cycle in a turfgrass environment.
Nitrate-nitrogen is a mobile anion that has the potential to move rapidly from the rootzone to the
groundwater. Percolation of water from the rootzone is the major pathway for water discharged from
turfgrass (Morton et al. 1988). Several researchers have found that selected fertilization and
irrigation practices can generate substantial leaching of nitrate-N from the rootzone of turfgrass
(Owen and Barraclough, 1983;Rieke and Ellis, 1974; Morton et al., 1988).
Nitrate-N is a drinking water contaminant with a U.S. Drinking Water Standard of 10 mg/L
(USEPA, 1976). Nitrogen inputs to coastal bays and estuaries, such as the Chesapeake Bay, have
been found to accelerate eutrophication. Water quality degradation can result from concentrations
of nitrogen much less than the drinking water standard of 10 mg/L (Ryther and Dunstead, 1971).
Various turfgrass management strategies have been evaluated for their capacity to reduce
nitrogen leaching losses from turfgrass. In this chapter, several options will be highlighted:
• Nitrification inhibitors to slow the formation of the mobile nitrate anion.
• Irrigation scheduling to reduce leaching to groundwater.
• Fertilizer source selection to minimize the pool of nitrate in the rootzone.
• Fertilizer application rate and timing to optimize plant uptake.
Our discussion will concentrate on practices typically used to manage home lawns or turf used
for outdoor recreation.
NITRIFICATION INHIBITORS
Most nitrogen fertilizers and all natural processes of organic matter cycling introduce nitrogen
into the soil solution in the ammonium form (Figure 1). This reduced cationic nitrogen is immobilized
on cation exchange sites in the soil and readily absorbed by microorganisms and plant roots.
Consequently, ammonium is not readily leached from the soil even when appreciable hydraulic flux
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occurs. Hesketh (1986) generally found less than 1.0 mg/L of ammonium-nitrogen in the soil solution
collected in suction lysimeters from the root zone (20 cm depth) of Kentucky bluegrass turf. At the
same time, soil solution nitrate-nitrogen often exceeded 20 mg/L. It appears that if the transformation
of fertilizer nitrogen to nitrate-N could be inhibited and nitrogen retained in the ammonium form, the
potential for nitrogen loss through leaching would be minimized.
In field crop production, nitrification inhibitors have been used successfully to stabilize
ammonium-nitrogen and increase nitrogen use efficiency (Huber et al. 1969; Prasard 1976; Warren
et al. 1975). In these studies, the inhibiting compound was mechanically incorporated into the soil
usually with the nitrogen fertilizer. Nitrification inhibitors used to improve the nitrogen use efficiency
of turfgrass have yielded few positive results. Waddington et al. (1975) found no benefits from
including the nitrification inhibitor nitrapyrin (2-chloro-6-(trichloromethyl) pyridine) with nitrogen
fertilizers applied to turf. Hesketh (1986) evaluated nitrapyrin at two rates, terrazole (3-ethoxy-3-
trichloromethyl-1,2,4-thiadiazole) and DCD (dicyandiamide) for their ability to enhance nitrogen use
efficiency in urea-fertilized Kentucky bluegrass turf. Turf quality, clipping yield, clipping nitrogen
content, and the nitrate and ammonium concentration in soil water were measured. No consistent
evidence of improved nitrogen uptake was obtained when nitrification inhibitors were present.
In these studies, fertilizers and inhibitors were applied to the surface of turf and washed into
the sod with irrigation water. No mechanical incorporation of the inhibitors into the soil was attempted
nor has any practical way of accomplishing this in established turf been proposed. Because nitrogen
leaching appears to be minimal on urea fertilized turf (Hesketh, 1986; Hull et al., 1987; Morton et
al., 1988) nitrification inhibitors may not generate substantial effects. However, because there was
no evidence of delayed nitrification when urea was applied with an inhibitor, Hesketh (1986)
concluded that the inhibitors probably were adsorbed in the overlaying thatch and never reached
the soil depths where nitrification was most active.
To determine if nitrification inhibitors can be effective in stabilizing ammonium-nitrogen when
nitrogen fertilizers are applied at the time of turfgrass seeding, nitrapyrin and DCD were disked into
the soil along with urea just prior to seeding Kentucky bluegrass (Hull et al. 1988). All parameters
measured exhibited a beneficial response to DCD, applied alone or combined with nitrapyrin, but
no response from nitrapyrin was noted. The nitrogen recovered in late season turfgrass clippings
doubled in response to DCD incorporation but this constituted only 10 percent of the fertilizer
nitrogen applied. It appears that the potential for nitrate leaching at the time of turfgrass seeding is
significant. However, it can be reduced somewhat by incorporating a water soluble nitrification
inhibitor.
IRRIGATION SCHEDULING
The potential for off-site nitrate-N losses depends on the concentration of nitrate in the rootzone
and the frequency and quantity of water percolation through the soil profile. Irrigation has been
shown to significantly increase nitrate-N leaching (Snyder et al., 1984; Endelman et al., 1974).
Morton et al. (1988) found that overwatering increased nitrate nitrogen transport to the groundwater
six fold from turfgrass, independent of fertilization rates. Home lawns are typically watered with little
regard for soil moisture status or the water holding capacity of the soil. Where irrigation is
automatically controlled with timers on permanently installed systems, rates are often selected to
meet maximum evaporative demands, regardless of weekly rainfall and climatic conditions (Snyder
et al., 1984). Excessive watering will increase antecedent soil moisture, thereby promoting additional
leaching from natural storm events or from the supplemental water alone.
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Supplemental water should be added judiciously in metered quantities to avoid drought stress
and to reduce losses from the rootzone to the groundwater. Efficient scheduling of irrigation water
requires an understanding of soils, plant physiology, and meteorology. Several approaches are
used to determine when turfgrass is in need of irrigation:
• Direct measurement of soil moisture status,
• Direct measurement of plant water status, and
• Estimation of cumulative evaporative demand from evaporation pans or climatic data.
Soil moisture measurements can be obtained with inexpensive tensiometers placed 7 to 15
cm into the rootzone. In a given climate, plants have been found to exhibit drought stress at the
same soil moisture tensions, regardless of soil texture. As soil dries the soil water tension increases.
At a predetermined "critical tension" irrigation is initiated. Studies relating drought stress to soil
moisture tensions have been performed on a range of turfgrass species. In a greenhouse
experiment, Aronson, et al. (1987) found that fine-leaved fescues could maintain acceptable quality
at tensions greater than 1 bar, while Kentucky bluegrass quality was found to decline markedly after
the soil had reached 0.6 bars. To reduce unneeded irrigation and avoid drought injury, additional
research is required to establish critical tensions for other turfgrass and grass mixtures.
Recently, Throssell et al. (1987) have suggested monitoring canopy temperature with an
infrared thermometer to detect plant water stress. Several researchers have found that canopy
temperature in turfgrass increased in response to drought stress. Other researchers have
established the relationship between evapotranspiration from well watered turfgrass and moisture
use predictions based on climatic measurements (Aronson et al. 1987; Pochop et al., 1977). Daily
tabulation of the expected water loss along with soil moisture characteristics of a particular site can
generate estimates of soil moisture status and critical tensions.
Determining the appropriate depth of irrigation is essential to avoid excess water draining from
the rootzone. The proper application depth of water requires knowledge of the upper and lower
limits of the available water in the soil and the depth of the rootzone. The lower limit of available
water in the soil is the amount that can be extracted from the rootzone by turfgrass before drought
stress occurs. Field capacity, the upper limit, is the soil water content that occurs after all
gravitational water has drained from a previously saturated soil. Ideally, enough water should be
applied to bring the entire rootzone to field capacity without promoting percolation. Since cultivated
turf has a shallower rootzone than commonly irrigated field crops, drought stress may occur earlier
in turf, while percolation from the rootzone could occur from the application depths used in field
crop irrigation. Most of the data necessary to develop recommended application depths is available;
however, the information needs to be evaluated and tailored to turfgrass.
FERTILIZER SOURCE SELECTION
Synthetic fertilizers, manures, animal and plant residues, by-products and a host of other
materials can supply nitrogen to the turfgrass plant. The requirement for continued access and
utilization of turf requires that turfgrass fertilizer products be easy to handle, of uniform quality,
inconspicuous after application, readily effective, and impart no offensive odor. The general visual
and functional expectations of modern turfgrass management practically eliminates use of
non-processed fertilizer materials (Beard, 1973). The choice of one fertilizer over another
traditionally has been based on turfgrass performance ratings (Waddington and Duich 1976;
Wilkinson 1977; Nelson 1980). More recently, nitrogen loss to the environment has been considered
(Snyder et al. 1981; Wesely et al. 1988)
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Turfgrass management practices employ N fertilizer products that belong to three general
classes. They are the synthetic inorganic, synthetic organic and natural organic nitrogen sources
(Table 1). The differing properties of nitrogen containing fertilizers determine where and when the
fertilizer N enters the soil nitrogen cycle (Figure 1).
Turfgrass fertilizer management ideally provides plant available nitrogen in the soil solution
as plant demand arises. Turfgrasses absorb most nitrogen as nitrate, however ammonia which is
less abundant in the soil solution is also absorbed. The three classes differ in the rate at which the
applied N becomes available to the growing plant. The transformation of the fertilizer product to
absorbed plant nutrient may involve only dissolving the fertilizer product in soil water or it may be
dependent on exacting soil water, aeration, temperature and microbiological conditions (Hays and
Haden, 1966).
The concept of nutrient release period refers to the rate with which the fertilizer increases the
ammonium and nitrate concentration in the soil solution. The 'fast' or 'quick' release products are
generally soluble salts and contain N in the ammonium or nitrate form at application.
The 'slow' or 'controlled' release fertilizer products require additional physical, chemical and/or
biological processing after application for the nitrogen to reach the water soluble form required for
plant utilization. These products range from urea and urea solutions to sulfur or resin coated urea
to complex polymers of urea and formaldehyde. Barriers to solubilization and transformation are
achieved through a number of different methodologies. Nitrogen release and transformation of these
products will vary with the polymer length, coating thickness and integrity, and the environmental
conditions into which they are placed. Sulfur coated urea and similar coated products such as
OsmocoteR, have coatings of limited or reduced permeability that restrict the movement of water
and nutrient from the granule. Methylene urea and urea formaldehyde are low molecular weight
compounds that require microbiological activity to mineralize the nitrogen. IBDU (isobutylidene
diurea) has controlled release properties due to its chemical structure and the particle size of the
product used. These 'slow' release synthetic organics produce their metered solubility characteristics
and reduced nitrification rates via different mechanisms. The methylene-ureas, IBDU and SCU
products have solubility characteristics that are inversely proportionally to molecular weight and
granule size (Hays and Haden, 1966; Hughes, 1976).
The major source of the natural organic fertilizer class is activated sewage sludge. The best
known product comes from the Milwaukee municipal system and is called MilorganiteR. Milorganite
and comparable materials contain the nitrogen in complex organic molecules. The rate of N release
is dependent on the microbiological activity in the soil. The predominant factor influencing N release
from this fertilizer class is soil temperature and aeration. The rate of N availability to the plant is
regulated by soil temperature as it effects mineralization and subsequent nitrification by soil
microbes.
The N in synthetic inorganic products, for example, ammonium nitrate, calcium nitrate, and
ammonium sulfate, is water soluble, rapidly available to plants and highly susceptible to leaching.
Synthetic inorganic N fertilizers have generated excessive N losses to the groundwater (Bredakis
and Steckel, 1963; Brown et al. 1977; Snyder et al. 1981). Nitrate-N concentration up to 200 mg/L
and total losses of over 15 percent of the applied fertilizer have been reported from turf fertilizers
with synthetic inorganic N (Brown et al. 1977).
In contrast to synthetic inorganic fertilizers, the natural and synthetic organic products have
been found to generate very low N losses to the groundwater. Bredakis and Steckel (1963), Snyder
et al. (1981), Starr and DeRoo (1981) and Brown et al. (1982) all document limited release of
nitrate-N from synthetic organic product used in the turfgrass environment. The highest nitrate-N
146
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concentration leaving the turfgrass rootzone were 2 and 18 mg/L when ureaformaldehyde and
activated sewage sludge were applied in a study conducted by Brown and colleagues (1977).
The most common nitrogen form now used for turfgrass fertilization are the synthetic organic
products. Urea is the most common N source of the synthetic organic class. Turfgrass response is
excellent and off site losses are low when urea is used as the N source. Mean annual nitrate-N
concentration below the turfgrass rootzone following urea application never exceed 6 mg/L in
studies conducted by Morton et al. (1988) or Wesely et al. (1988).
APPLICATION RATES AND TIMING OF FERTILIZER
Unlike field crops, annual fertilizer applications to turfgrass can be easily split and applied in
small increments throughout the growing season. In the Northeast U.S., commercial lawn care
companies almost exclusively use urea or urea formaldehyde as the nitrogen source. Applications
may occur monthly, from late spring through late summer, with a final large application in late fall.
Morton et al. (1988) found no evidence of increased nitrate-N leaching following late fall or late
spring applications of urea/urea formaldehyde. In the late fall, the cool temperatures slow the
enzymatic hydrolysis of urea to ammonium and the subsequent biological oxidation of ammonium
to the mobile anion nitrate. Plant uptake may match the generation of ammonium and nitrate,
reducing the pool of teachable N in the rootzone. More research is need to define the relationship
between the rates of nitrate production and uptake by roots. The lack of nitrate-N in soil leachate
following late spring applications of urea may result from the vigorous turf growth that occurs during
this period. Plant uptake may be well suited for absorbing moderate nitrogen applications at this
time of year. Again, we believe research on turfgrass nutrient budgets is essential to fully understand
this situation.
Morton et al. (1988) observed high concentrations of nitrate-N in soil water leachate following
late summer applications of urea. Cisar (1986), through analysis of leaf growth and N content of
clippings, found that N uptake by Kentucky bluegrass declined in late summer. Applying nitrogen
fertilizer when plant uptake is reduced could generate excessive amounts of soluble nitrogen in the
rootzone and could increase the potential for waterborne nitrogen losses from the rootzone.
A dense turfgrass sod constitutes a substantial sink for topically applied synthetic organic
nitrogen. This was dramatically demonstrated by Hull et al. (1987) when urea was applied as a
single treatment at 288 kg N/ha to five turfgrass species during mid-May. Over the next four months,
the nitrate-nitrogen content of soil water collected at a 60 cm depth never exceeded 1.0 mg/L.
During the growing season, less than 0.4 kg N/ha leached from these plots while 58 percent of the
applied nitrogen was recovered in clippings.
However, the soil water from Kentucky bluegrass plots which had received over 350 kg
N/ha/year as urea for 14 years sometimes contained more than 10 mg N/L below the root zone and
more than 50 mg N/L within the rootzone (Hesketh, 1986). At this high fertility level, approximately
22 kg N/ha were lost through leaching during the growing season which was equivalent to 6 percent
of the nitrogen applied. It appears that the rate of nitrogen application may influence the quantity
of nitrate leaching from turfgrass sod, but this is most likely to be a problem with turf that has been
subjected to long term intensive fertilization rates.
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CONCLUSIONS
Because no significant crop is removed from a turfgrass sod unless the clippings are collected,
there is little mechanical or cultural nitrogen loss. If fertilizer nitrogen is repeatedly applied at elevated
rates (greater than 200 kg/ha/year) the soil-plant system may become "nitrogen saturated" and
generate substantial nitrate leaching. To reduce the potential for groundwater contamination, turf
managers would be well advised to maintain their grass with less than 150 kg/N/ha/year, to utilize
slow-release organic formulations, and to carefully control supplemental irrigation.
148
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LITERATURE CITED
Aronson LJ, A.J^Gold, and R.J. Hull. 1987. Cool-season turfgrass response to drought stress. Crop Science
Aronson, L.J., A.J. Gold, RJ. Hull and J.L. Cisar. 1987. Evapotranspiration of cool-season turfgrass in the humid northeast
Agron. J. 79:901-905.
Beard, J.B. 1973. Turfgrass: science and culture. Prentice-Hall, Englewood Cliffs, NJ.
Bredakis, E.J. and J.E. Steckel. 1963. teachable nitrogen from soils incubated with turfgrass fertilizers. Agron J. 53:
145-147.
Brown, K.W., J.C. Thomas, and R.L. Duble. 1982. Nitrogen source effect on nitrate and ammonium leaching runoff losses
from greens. Agron. J. 72:947-950.
Brown, K.W., R.L. Duble and J.C. Thomas. 1977. Influence of management and season on fate of N applied to golf greens
Agron. J. 69:667-671.
Cisar, J.L. 1986. Cool season turfgrass response to moderate fertility. Ph.D. diss. Univ. of Rl, Kingston.
Endleman, F.J., D.R. Kenney, J.T. Gilmour, and P.G. Saffigna. 1974. Nitrate and chloride movement in the plainfield loamy
sand under intensive irrigation. J. Environ. Qual. 3:295-298.
Hays, J.T. and W.W. Haden. 1966. Soluble fraction of ureaforms nitrification leaching and burning properties. J. Ag. Food
Chem 14:339-341.
Hesketh, E.S. 1986. The efficiency of nitrogen use by Kentucky bluegrass turf as influenced by nitrogen rate, fertilizer
ratio and nitrification inhibitors. M.S. Thesis, Univ. of Rl, Kingston Rl, p. 88.
Huber, D.M., G.A. Murray, and J.M. Crane. 1969. Inhibition of nitrification as a deterrent to nitrogen loss. Soil Sci. Soc.
Amer. Proc. 33:975-976.
Hughes, T.D. 1976. Nitrogen release from isobutylidene diurea: soil pH and fertilizer size effects. Agron. J. 68:103-106.
Hull, R.J., E.S. Hesketh, and A.J. Gold. 1987. Factors influencing nitrate leaching from lawn turf to ground water.
Completion Rept., Rhode Island Water Resources Center, Kingston, Rl 24 p.
Hull, R.J., E.S. Hesketh, and H. Liu. 1988. Can nitrification inhibitors increase nitrogen use efficiency by turfgrasses?
Agron. Abstracts, In press.
Morton, T.G., A.J. Gold and W.M. Sullivan. 1988. Influence of overwatering and fertilization on nitrogen losses from home
lawns. J. Environ. Qual. 17:124-130.
Nelson, J. 1980. Summer and fall color retention of Kentucky bluegrass receiving varying amounts and timing of inorganic
or inorganic-organic combinations of nitrogen. Can. J. Plant Sci. 69:1015-1021.
Owen, T.R. and D.Barraclough. 1983. The leaching of nitrates from intensively fertilized grassland. Fert. Agric. 85:43-50.
Pochop, L.O., J. Borelli, J.R. Barnes, and P.K. O'Neill. 1978. Water requirements and application rates for lawns. Wyoming
Water Res. Rsch Int., Wat. Res. Series No. 71.
Prasard, M. 1976. Nitrogen nutrition and yield of sugarcane as affected by N-Serve. Agron. J. 68:343-346.
Rieke, P.E. and B.G. Ellis. 1974. Effects of nitrogen fertilization on nitrate movement under turfgrass. p. 120-129. In:
E.D. Roberts (ed.) Proc. Int. Turf. Conf., Blacksburg, VA. 19-21 June 1973. ASA, Madison, Wl.
Ryther, J.A. and W.M. Dunstan. 1971. Nitrogen phosphorus and eutrophication in the coastal marine environment. Science
171:1008-1013.
Snyder, G.H., B.J. Augustin, and J.M. Davidson. 1984. Moisture sensor-controlled irrigation for reducing N leaching in
bermuda grass turf. Agron. J. 76:964-969.
Snyder, G.H., E.G. Burt and J.M. Davidson. 1981. Nitrogen leaching on bermuda grass turf: Effect of nitrogen source and
rates. Proceeding of 4th Intern. Turfgrass Conf. Guelph, Canada: 313-324.
149
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Starr, J.L. and H.C. DeRoo. 1981. The fate of nitrogen fertilizer applied to turfgrass. Crop Science 21: 531-536.
Throssell, C.S., R.N. Carrow, and G.A. Milliken. 1987. Canopy temperature based irrigation indices for Kentucky bluegrass
turf, crop sci. 27:126-131.
USEPA. 1976. Quality criteria for water. U.S. Gov. Print. Office, Washington, DC.
Waddington, D.V. and J.M. Duich. 1976. Evaluation of slow-release nitrogen fertilizers on Pennpar creeping bentgrass.
Agron.J. 68:812-815.
Waddington, D.V., E.L. Moberg, J.M. Duich and T.L. Watschke. 1976. Long-term evaluation of slow-release nitrogen
sources on turfgrass. Soil Sci. Soc. A. 40:593-597.
Waddington, D.V., T.R. Turner, and J.M. Duich. 1975. Response of cool-season turfgrasses to liquid applications of
fertilizer. Progress Rept. 350, Pennsylvania State Univ. Agric. Exp. Sts. Univ. Park, PA p. 31.
Warren, H.L., D.M. Huber, D.W. Nelson, and O.W. Mann. 1975. Stalk rot incidence and yield of corn as affected by
inhibiting nitrification. Agron. J. 67:655-660.
Wesely, R.W., R.C. Shearman and E.J. Kinbacher. 1988. 'Park' Kentucky blue response to foliarly applied urea. Hort.
Science 23:556-559.
Wilkinson, J.F. 1976. Effect of IBDU and UF rate, date and frequency of application on Merion Kentucky bluegrass.
Agron.J. 69:657-661.
150
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TABLE 1
Classification, burn potential, leaching potential, low temperature response and residual
effect of common turfgrass nitrogen sources.
Fertilizer N content
Source %
Burn Leaching Low Temp Residual
Potential Potential Response Effect
Synthetic Inorganic
Ammonium
nitrate
Calcium nitrate
Ammonium
sulfate
Synthetic Organic
Urea
Urea solutions
Sulfur coated
urea
Isobutylidene
diurea
Methylene
ureas
Ureaformaldehyde
Natural Organic
Activated
sewage
sludge
34
16
21
45
30
35
30
42
30
6
High
Very High
Very High
High
High
Low
Low
Low
Low
Very Low
High
High
Mod. High
Mod. Low
Mod. Low
Low
Mod. Low
Low
Low
Very Low
Rapid
Rapid
Rapid
Rapid
Rapid
Moderate
Moderate
Low
Low
Very Low
Short
Short
Short
Short
Short
Moderate
Moderate
M-Long
Long
Long
151
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FIGURE 1
Turf grass Nitrogen Cycle
CLIPPINGS
t
N,
DENITRIFICATION
TURFSOD
A
GAS
LOSSES
ROOT UPTAKE
VOLATILIZATION
TURFSOD
PLANT-AVAILABLE NITROGEN
NITRIFICATION
NH
NO;
'MINERALIZATION
ORGANIC
MATTER
LEACHING
FERTILIZER
NITROGEN
NO
GROUND WATER
ROOT UPTAKE
152
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SURFACE RUNOFF FROM TURF
M. S. Welterlen
Grounds Maintenance Magazine
P.O. Box 12901
Overland Park, KS 66212
formerly, Dept. of Agronomy
University of Maryland
College Park, MD 20742
and
C.M. Gross, J.S. Angle, R.L Hill
Department of Agronomy
University of Maryland
College Park, Maryland 20742
Nonpoint source pollution of waterways has received considerable attention in recent years
as a result of a decline in water quality of these waterways and subsequent declines in desired
resources derived from them. In assessing the impact of nonpoint source pollution of waterways the
quality and quantity of surface and ground water emanating from various aspects of the watershed
must be critically evaluated.
Sensitive areas such as the Chesapeake Bay, which is one of the most productive estuaries
in the world, are particularly vulnerable to impacts by actions throughout their watersheds.
Watersheds such as the Chesapeake Bay are comprised of various land uses such as forestation,
urbanization and crop production. Surface characteristics as well as fertilizer and pesticide loading
on these areas have been shown to affect the quality and quantity of water emanating from the
watershed. Consequently, land use has been more critically reviewed in sensitive areas in recent
years.
Urbanization with associated suburbanization has increased dramatically in the Northeast
United States, Urbanization results in an increase in impervious surfaces which accelerate surface
runoff from watersheds. In addition, an increase in the amount of turf acreage has also occurred
with urbanization as residential lawns, parks, highway roadsides and other turf areas are
established. Surveys conducted by the Maryland Department of Agriculture (1987) indicated an
increase in Maryland turf acreage from 346,871 in 1979 to 614,024 in 1986. The increase in turf
acreage has prompted public concern as to ecological impacts of turf management, since turf makes
up a growing proportion of the watershed in urban areas.
This chapter will discuss research relating to the effects of turf on surface water movement. A
discussion of the effects of turf on ground water quality is included elsewhere in this text.
PHYSICAL CHARACTERISTICS OF TURF
Turf is composed of many closely spaced individual plants that form a closed canopy over the
soil surface. Turf density, leaf texture and turf canopy height are primary physical factors relating
to dissipation of impact energy of rain droplets and resistance to surface movement of water over
turf. Approximately 80 percent of the extensive fibrous root system of turfgrass is located in the
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upper 5 cm of soil. The protective nature of both the turf canopy and the root system are responsible
for the soil stabilizing effects of turf.
Turf density varies depending on inherent characteristics, environmental conditions and
management. Creeping bentgrass (Agrostis palustris Huds.) which is used as an intensively
managed turf, may exhibit density as high as 1,700 plants dm-2, whereas Kentucky bluegrass (Poa
pratensis L.) density may be as low as 100 plants dm-2 and tall fescue (Festuca arundinacea Shreb.)
less than 100 plants dm-2 (Beard, 1973). Cultural factors that increase shoot density include close
mowing, adequate moisture and nitrogen fertility (Roberts, 1965).
Leaf texture refers to the width of turfgrass leaf blades and varies among turfgrass species
and varieties (Table 1) as well as management and seeding rate (Table 2). In order to maintain turf
uniformity, seeding mixtures are formulated with turfgrasses of compatible texture.
Optimum canopy height of maintained turf depends on the species and intended use.
Residential lawns are typically maintained at heights ranging from 2 to 8 cm. Highway roadsides
are generally maintained at 8 to 13 cm, and golf course fairways are mowed at 1.3 to 3.8 cm
depending on the species.
RUNOFF CHARACTERISTICS OF TURF
Research conducted on the effects of grasses, in general, and turfgrass, in particular, on
surface runoff has been documented, and more research is currently underway. Numerous studies
have shown that grass buffer strips are quite effective in reducing runoff and the sediment and
nutrients carried with it (Gross et al., 1987; Hayes et al., 1978; Tollner, et al.,1977; U.S. E.P.A.,
1983a and 1983b; and Young et al., 1980). Most of the work conducted over the past 25 years
pertaining to the pesticide content of surface waters draining from agricultural fields has been
reviewed by Pionke and Chesters (1973) and Wauchope (1978). In cases where water quality has
declined due to nutrient and pesticide movement in water or eroded sediment, the use of grassed
buffer strips between treated fields and the receiving bodies of water have significantly reduced t^e
problem. The Cooperative Extension Service in the Chesapeake Bay area currently recommends
the planting of grass filter strips as well as natural vegetation filter areas for reducing runoff from
field crops (Extension Services of the Chesapeake Basin, 1985). Doyle, et al. (1977) evaluated the
effectiveness of forest and grass buffer strips in improving water quality of manure polluted runoff.
The authors determined that both forest and grass buffer strips of approximately 4 meters were
found to be effective in reducing levels of fecal bacteria from manure treated plots. Total soluble
NH4-N, NO3-N, P and K levels were also reduced by the buffers.
Studies relating to surface runoff from turf are currently underway at the University of Maryland
(Gross et al, 1988, unpublished data). Another study conducted on a Sassafras sandy loam with a
slope of 8% at the University of Maryland (Gross et al, 1988, unpublished data), evaluated the effects
of rainfall intensity and turfgrass seeding rate (density) on runoff initiation time, runoff rate and
sediment loss. Three rainfall intensities (3.0 inches per hour, frequency of once every two years;
3.7 inches per hour, frequency of once in every 5 years and 4.7 inches per hour, frequency of once
in every 20 years) were imposed with a rainfall simulator. Under a rainfall intensity of 4.7 inches per
hour, runoff rate was reduced by 50% with tall fescue, seeded at 10 Ib. per 1,000 sq. ft. one year
prior to testing, in comparison to bare ground (Fig. 1). Runoff initiation time was positively correlated
with rainfall intensity and seeding rate (Fig. 2). Under a rainfall intensity of 3.7 inches per hour,
sediment loss was reduced from 1.1 g m-2 min-1 (bare ground) to 0.1 g m-2 min-1 (on turf originally
seeded at 10 Ib. seed per 1,000 ft.-2) (Fig. 3). Researchers in Pennsylvania (Harrison et al, 1988)
154
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showed that only 5% of applied water (6 in./hr) ran off slopes with Kentucky bluegrass sod, whereas
approximately 20% of applied water ran off slopes established by seeding. Consequently, by
sodding critically-sloped areas during initial stages of construction, runoff can be further reduced.
These studies indicate general trends in the effects of turf and rainfall intensity on surface water
and sediment movement; however, it is important to note that specific values may vary depending
on soil type, terrain, turfgrass species, turf quality and naturally occurring rainfall in the area.
Research conducted by the University of Maryland (Gross, et. al. 1987) at the Chesapeake
Bay Foundation Research Farm in Upper Marlboro, Maryland showed that surface water runoff
volume, sediment loss, total N movement and phosphate movement were dramatically lower in turf
in comparison to conventional tobacco (Table 3) under natural rainfall. Under simulated rainfall
intensities, turf was also shown to be superior to corn in terms of stabilizing soil (Table 4). With an
intense rainfall occurrence of 4.7 inches per hour, turf was 133 times more effective in stabilizing
soil in comparison to corn. These studies also indicated that annual runoff volume from tall fescue
was five times less than from conventionally planted tobacco. Sediment loss was 4,730 kg ha-1
from tobacco versus 5.8 kg ha-1 from turf. Total N was 11.7 kg ha-1 from tobacco versus 0.11 kg
ha-1 from turf and ortho-P loss was 0.42 kg ha-1 from tobacco versus 0.03 kg ha-1 from turf.
The ability to project amounts of pesticides in surface waters emanating from a turf site
depends on several factors including: amounts and rates of degradation of specific pesticides to
be applied, pest pressure, rainfall intensity at the site, topography and landscape design. Since
pesticides vary in their chemical characteristics, they differ in their rate and mode of degradation
(by microbial, photochemical and hydrolytic means), soil adsorptive tendencies, and volatilization.
A thorough review of these characteristics is presented in several sources (Farm Chemicals
Handbook, 1988; Herbicide Handbook, 1983; Saltzman and Yaron, 1986).
SUMMARY
The stabilizing effects of turf must not be overlooked in developing land use strategies. In
developing such strategies, turf is often equated with impervious surfaces, which is far from the
conclusions that have been documented by research. Before alternative ground covers are adopted
for sensitive sites, we must first consider the environmentally beneficial aspects of turf and determine
whether the alternative ground cover will provide improved results.
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LITERATURE CITED
Beard, J. B., 1973. Turf grass science and culture. Prentice-Hall Publishing Co. Englewood Cliffs, NJ.
Doyle, R. C., G. C. Stanton, and D. C. Vtolf. 1977. Effectiveness of forest and grass buffer strips in improving the water
quality of manure polluted runoff. Proceedings of the 1977 Winter Meeting of the American Society of Agricultural.
Paper No. 77-2501.
Extension Services of the Chesapeake Basin. 1985. Best management practices for nutrient uses in the Chesapeake
basin. Bulletin 308 College of Agriculture, University of Maryland, College Park, MD.
Farm Chemicals Handbook. 1988. Meister Publishing Co. Willoughby, Ohio.
Harrison, S., T. L Watschke and G. Hamilton. 1988. Turfgrass runoff update. ASPA News, American Sod Producers
Association.
Gross, C. M., J. S. Angle, R. L. Hill and M. S. Welterlen. 1987. Natural and simulated runoff from turfgrass. Agron.
Abstracts. 79:135.
Hayes, J. C., B. J. Barfield and R. I. Barnhisel. 1978. Rltration of sediment by simulated vegetation II. Unsteady flow with
non-homogeneous sediment. Transactions of the ASAE: 21 (10): 1063-1067.
Maryland Department of Agriculture. 1987. Maryland turfgrass survey, 1987. Maryland Department of Agriculture and
Maryland Turfgrass Council. Annapolis, Maryland.
Pionke, H. B. and G. Chesters. 1973. Pesticide-sediment water interactions. J. Environ. Qual. 2:23-45.
Roberts, E. C. 1965. A new measurement of turfgrass response and vigor. The Golf Course Reporter. 33:10-20.
Saltzman, S. and B. Yaron. 1986. Pesticides in soils. Von Nostrand Reinhold Co., New York.
Tollner, E. W., B. J. Barfield, C. Vachirakornwatana and C. T. Haan. 1977. Sediment deposition patterns in simulated
grass filters. Transections of the ASAE 20 (4): 940-944.
U.S. Environmental Protection Agency. 1983. Reducing runoff pollution using vegetated borderland for manure application
sites. USEPA Rep. 600/52-83-022. U.S. Government Printing Office, Washington, D.C.
U.S. Environmental Protection Agency. 1983. Swine manure and lagoon effluent applied to fescue. USEPA Rep.
600/S2-83-078. U.S. Government Printing Office, Washington, D.C.
Wauchope, R. D. 1978. The pesticide content of surface water draining from agricultural fields: A review. J. Environ.
Qual. 7:459-472.
Weed Science Society Of America. 1983. Herbicide Handbook. W.S.S.A.
Young, R. A., T. Huntrods and W. Anderson. 1980. Effectiveness of vegetated buffer strips in controlling pollution from
feedlot runoff. J. Environ. Qual. 9 (3): 483-487.
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TABLE 1
Comparison of leaf texture of turfgrasses mowed at 3.8 cm (Adapted from Beard, 1973)
Textural Category
Very Fine
Fine
Medium
Coarse
Leaf Width
-mm--
Less Than 1
1-2
2-3
3-4
Very Coarse
Greater than 4
Turfgrass Species
Creeping red fescue
Velvet bentgrass
'Emerald1 zoysiagrass
Rough bluegrass
Kentucky bluegrass
'Meyer' zoysiagrass
Annual bluegrass
Annual ryegrass
Redtop
Centipedegrass
Tall fescue
St. Augustinegrass
Bahiagrass
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TABLE 2
Effects of seeding rate on leaf texture of 9 month old tall fescue mowed at 6 cm in Silver Spring,
Maryland (Welterlen, 1984, unpublished data).
Seeding Rate Width of Second Leaf
Ib./1,000ft2 -mm-
2 5.7 a*
4 5.5 ab
6 5.3 be
8 5.3 be
10 5.3 be
12 5.2 cd
14 5.1 d
16 5.0 d
Means followed by the same letter are not significantly different at the 0.05 level according to
Bayes Least Significant Difference.
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TABLE 3
Comparison of tobacco versus tall fescue turf in surface movement of water, sediment and
fertilizer (Gross, et al., 1987).
Crop Runoff Volume Sediment Total-N P04-P
Lx103ha'1 kg ha-1 kghff1 kghr1
Conventional 334.0 4730 11.7 0.42
Tobacco
Tall Fescue 74.5 5.8 0.11 0.03
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TABLE 4
Sediment loss from com versus tall fescue (Gross, et al. 1987).
Sediment Loss
Rain Intensity fall Fescue Turf Corn
In. hr1 —- gm nv2 mln-1 —
4.7 0.18 24.0
3.7 0.12 14.1
3.0 0.08 10.0
* Rainfall was imposed with a rainfall simulation device. Rainfall intensities of 4.7, 3.7, and 3.0
inches per hour correspond to 30 minute rainfall events which occur every 20, 5 and 2 years,
respectively.
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THE INFLUENCE OF TURFtechtm SEEDING
ON SOIL COMPACTION IN SOUTHEAST IOWA
AND A MID-SOUTH REGION
BY
Jim Schaefer
and
Larry Larson
Research and Development Department
Soil technologies Corp.
51 West Adams
Fairfleld, IA 52556
INTRODUCTION
TURFtech is a commercial microbial product composed of chlamydomonas, chlorella and
cyanobacteria. The purpose of the product is to provide a seeding of viable dormant microorganisms
at the rate of 18.2 x 109 cells acre-1, per application, to a turf's soil surface, thereby establishing
an artificial advantage for these selected strains, and culturing the organisms for three to five
weeks. The artificially induced large population of microbes then act as sources for the production
of biopolymers or microbial polysaccharides, an organic soil-aggregating agent. These microorganisms
grow on soils and secrete quantities of polysaccharides (Kroen, 1984). The addition of microbial
polysaccharides to soil generally improves aggregate development and stability (Lynch and Bragg,
1985). Lewin (1977) and Melting (1986) collected empirical evidence suggesting these same
microbes as efficacious agents for beneficial alteration of soil structure.
Considerable evidence is published which suggest that soil compaction of various forms
seldom favors the economics of turf production and generally works against it (Gill, 1971). Soil
structural degradation has been blamed by various researchers for plant growth reductions (Baver
and Farnsworth, 1941; Lawton, 1945; Quastel, 1952; Gill and Miller, 1956; Hagin, 1952; Voorhees
et al, 1975). This paper will report field results where bearing ring cone penetrometer readings were
collected at sites which were seeded with the TURFtech product.
MATERIALS AND METHODS:
Two experimental regions were established for test sites for 1987 and one region for 1986.
The regions were distinguished as having similar soil origins and climactic conditions. The regions
were called Southeast Iowa (north of Highway 34, and south of I-80 and east of Knoxville) and the
Mid-South (Eastern Arkansas and the northwest 1/4 of Mississippi). Each represented a single
experimental area. Each test site belonged to a cooperating TURFtech customer. The operators
purchased and applied the TURFtech product, which consists of single cells uniformly dispersed
in a dry, suspendable, clay based powder. This material was mixed with water and applied with
conventional spray equipment at the rate of 4 ounces with between 30 to 60 U.S. gallons of water
per acre. Seeding, or application, was done in the spring. In each case, for 1986 in Southeast Iowa
and for the Mid-South in 1987, the treated areas were receiving their first seeding with TURFtech .
Southeast Iowa treated areas were treated again in 1987. A seeded and non-seeded area (or plots)
161
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were located side by side at each site. The experimental measurement area was within this area.
Each test or measurement area was 45m2 with one half of the area the seeded area and the other
half the non-seeded area. Each measurement area was selected for uniformity of soil type, slope,
drainage pattern, and cultural history.
For compaction data collection a Soiltest bearing ring cone penetrometer was used. The cone
had a cross sectional area of 2.54 cm2 and had a 30 degree angle. Twenty subsample data sites
were randomly selected, for each the seeded and non-seeded areas for probing. Each of the 80
Southeast Iowa and 38 Mid-South sites were probed one time, approximately 6 weeks after the
TURFtech seeding. The twenty subsample measurements were integrated to produce a mean for
each the seeded and non-seeded areas, and all measurements were adjusted to U.S.
pounds/inch2 for each replicate. Measurements were taken at the two and four inch depths in 1986
and 1987. A one inch soil core to the four inch depth was taken at every fourth to tenth subsample
data site for each replicate. Gravimetric moistures were analyzed on each soil sample. The 2 to 5
gravimetric subsample moistures for each the seeded and non-seeded areas were integrated
producing a percent moisture mean for each the treated and non-treated area of the replicate.
Each measurement area, containing a treated and non-treated plot, represented a replicate
or block. Thus, the statistical design was that of a randomized complete block, with each
measurement area or test site treated as a replication.
RESULTS
The bearing ring cone penetrometer measurements for all test sites are presented in Table 1.
For all test sites the TURFtech seeded area had significantly less penetrometer resistance to both
the two and four inch depths. The soil water content difference between the seeded and non-seeded
areas was not significant.
DISCUSSION
Certain soil organisms produce polysaccharides that have a mucilaginous nature and may
cement mineral particles together. Rennie et al. (1954) found that the addition of only 0.02g of an
extracted and purified soil polysaccharide material to 100g of soil increased the water-stable
aggregates > 0.1mm in diameter from 44g to 60g. Chesters et al. (1957) on analysis of a large
number of soils, indicated that per unit mass, the polysaccharide fraction was more effective in
stabilizing the mineral particles into structural units than was the non-polysaccharide portion of the
soil organic matter.
In experimental work, it is frequently desirable to evaluate soil structure issues because the
most suitable management practices may depend on the extent to which structure affects the
growth of plants. With the advent of synthetic, organic soil-aggregating agents, with only small direct
effects on the microbiological population and nutrient status of soils, structural effects on plant
performance could be measured. It has been observed that in some cases the improvement of
structure through field application of a synthetic organic soil-aggregating agent did not improve plant
growth (Clement, 1961) and in other examples a definite improvement in plant growth could be
attributed to structural improvements associated with the addition of the aggregating agent (Boekel,
1963). It is generally agreed that improved soil structure is beneficial to soil as a medium for plant
growth.
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Within one season, with four TURFtech seedings, the measurement of force required to
displace or shear soil with a bearing ring cone penetrometer was significantly reduced at both the
two and four inch depths, (Table 1). The measurement of greater comparative reductions at the two
inch depths versus the four inch depths, is probably due to the majority of the microbial produced,
organic, soil-aggregating agent being tied up with the soil mineralogy in the upper zone of the
measurement depth. Each test site used a different type and design of spray equipment to seed
soils with the product. The total number of sites should have minimized any bias in the data due to
inconsistence in the equipment calibration. An inconsistent number of soil moisture readings per
site was calculated. However, the total number of moisture evaluations was high and the moisture
bias in the penetrometer calculations was statistically insignificant. These measurements appear
to produce a correlation between the seeding of surface soils with a microbial product, a presumed
biological source for an organic, soil aggregating agent, and decreases in surface soil compaction.
It is at least suggested by this work that a soil response may be associated with the TURFtech
seeding of certain surface soils, possibly more so with those identified in need of structural
improvement.
ACKNOWLEDGEMENTS
I wish to thank Rick Cruse, Ph.D. Department of Agronomy, Iowa State University, Ames, Iowa,
for his guidance with regard to the experimental design in this report.
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TABLE 1
Bearing ring cone penetrometer measurements at two and four inch depths.
Depth Replicates
inches (a) Region (b)
2/86
2/87
2/87
4/86
4/87
4/87
80/SEIA
80/SEIA
38/MS
80/SEIA
80/SEIA
38/MS
lbs./inch2 % Moisture Ibs./inch2
Seeded Seeded Non-
Mean Mean Seeded
Mean
40.63 (c)
33.57 (c)
47.96 (c)
95.29 (c) 15.7(d)
94.23 (c)
1 56.98 (c) 12.08(d)
58.24
45.79
71.67
125.78
117.79
193.30
% Moisture
Non-
Seeded
Mean
16.0
11.90
(a) Depth in inches per year.
(b) Each replicate treated as a randomized complete block.
SEIA = Southeast Iowa and MS = Mid-South.
(c) Significant at 1% level.
(d) Insignificant at 5% level.
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REFERENCES
Barber, Stanley A. 1959. The influence of alfalfa, bromegrass, and corn on soil aggregation and crop yield Soil Sci Soc
Am. Proc. 23:258-259.
Baver, L.D. and R.B. Farnsworth. 1941. Soil structure effects on growth of sugar beets. Soil Sci. Soc. Amer. Proc. 5:45-48
Boekel, P. 1963. Soil structure and plant growth. Netherlands J. Agr. Sci. 11:120-127.
Chesters, G., O.J. Ahoe, and O.N. Allen. 1957. Soil aggregation in relation to various soil constituents. Soil Sci Soc Am
Proc. 21:272-277.
Clement, C.R. 1961. Benefit of leys-structural improvement or nitrogen reserves. J. British Grassland Soc. 16:194-200.
Gill, W.R. 1971. Economic assessment of soil compaction. In: Compaction of Agricultural soils. K.K. Barnes, W.M. Carlton,
H.M. Taylor, R.I. Throckmorton, and G.E. Vanden Berg (eds.) Am. Soc. Agri. Eng. St. Joseph, Ml.
Gill, W.R. and R.D. Miller. 1956. A method of study of the influence of mechanical impedance and aeration on the growth
of seedling roots. Soil Sci. Soc. Am. Proc. 20:154-157.
Hagin, J. 1952. Influence of soil aggregation or plant growth. Soil Sci. 74:471-478.
Kroen, W.K. 1984. Growth and polysaccharide production by the green alga Chlamydomonas mexicana (Chlorophyccae)
on soil. J. Phycol. 20:616-618
Lawton, K. 1945. The influence of soil aeration on the growth and absorption of nutrients by corn plants. Soil Sci. Soc.
Am. Proc. 10:263-268.
Lewin, R.A. 1977. The use of algae as soil conditioners." Centres. Invest. Baja Calif., Scripps Inst. Oceanogr. 3:33-35.
Lynch, J.M., and E. Bragg. 1985. Microorganisms and soil aggregate stability. Adv. Soil Sci. 2:133-171.
Melting, B. 1986. Dynamics of wet and dry aggregate stability from a three-year microalgal soil conditioning experiment
in the field. Soil Sci. 143:139-143.
Quastel, J.H. 1952. Soil Conditioners. Annual Rev. Plant Physiol. 5:75-92
Rennie, D.A., E. Truog, and O.N. Allen. 1954. Soil aggregation as influenced by microbial gums, level of fertility and kind
of crop. Soil Sci. Soc. Amer. Proc. 18:399-403.
Vborhees, W.B., D.A. Farrell, and WE. Larson. 1975. Soil strength and aeration effects on root elongation. Soil Sci. Soc.
Am. Proc. 39:948-953.
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166
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SECTION IV
State of the Art Research on
Control of Turfgrass Pests
Through Use of Naturally Occurring
Endophytic Fungi
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THE ROLE OF ENDOPHYTIC FUNGI IN GRASSES:
NEW APPROACHES TO BIOLOGICAL CONTROL OF
PESTS
Malcolm R. Slegel, Douglas L. Dahlman and Lowell P. Bush
Departments of Plant Pathology,
Entomology and Agronomy,
University of Kentucky
Lexington, KY 40546-0091
The infection of grasses by consistently symptomless nonsporulating endophytic fungi has
been known for many years, but only recently attracted attention because of the economic
importance associated with animal toxicoses and resistance to insect predation. Since the initial
work of Bacon et aL (2) in 1977 and Fletcher and Harvey (11) in 1981, which established the
respective associations of animal toxicosis with endophyte-infected tall fescue and perennial
ryegrass, researchers have come to further understand the relationship between fungal endophytes
and their host grasses. Recent studies have addressed the origin and incidence of endophyte-
infected grasses, modes of dissemination of the fungi, identification of the chemicals responsible
for mammalian and insect toxicoses, and the significance of ecological and physiological
relationships between grass hosts and endophytes.
In this chapter, we will present a general review dealing with the biology, ecology and
physiology of the host-fungus interaction as well as some specific information on the nature of the
biological control of insects and diseases by endophyte-infected grasses. The aspect of biological
control of pests deals with the potential use of infected turfgrasses in the urban environment.
Introduction of these grasses could result in reduction of pesticide usage and the undesirable
ecological side effects of chemicals used on turf. However, the successful use of endophyte-
improved turfgrass cultivars depends on a number of factors which are related to the nature of the
host-fungus interaction.
In addition to the information presented here, there are other chapters in this book by Bacon
(Chapter 17) and Funk et aL (Chapter 18) that detail further the production of specific toxins in
endophyte-infected grasses and endophyte-enhanced performance of turfgrass, respectively.
Because there are a number of recent reviews on fungal endophytes (1,3,8,26,36,37), we will only
reference those statements which represent new information or those which need further emphasis.
TAXONOMY, BIOLOGY AND ECOLOGY
The term endophyte, in regard to infection of grasses, was defined previously by Siegel el aL
(37) as a fungus which is contained or growing (entirely) within the substrate plant, spending aH or
nearly all of its life cycle in the host. Almost all of the grass endophytes are grouped or related to
fungi in the tribe Balansiae (genera; AtkiDSoneila, Balansia, Blansiopsis, Myriogenospora and
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Epichloe) of the family Clavicipitaceae. They are common biotrophic inhabitants of grasses, which
have a C-3 type photosynthetic pathway, and sedges. Other non-related endophytes (Phialophora-
like and Gliocladium-like spp.) have been described as well (17).
A generalized life cycle of the grass endophytes is illustrated in Fig. 1. In relation to this life
cycle, it is germane to emphasize those endophytes which remain symptomless versus those which
produce sporulating fructifications and prevent flowering. The mycelia of both symptomless and
symptom-producing endophytes grow intercellularly (10,13,35), infecting meristems, leaf sheaths,
and sometimes blades. In addition, the symptomless endophytes infect seed, growing in association
with the aleurone layer and seed embryo. Unless symptoms are produced, the plant appears to be
undamaged and the fungus becomes incorporated into the plant's reproductive system. The only
known means of dissemination of symptomless endophytes is through maternal transmission of
infected seed (solid arrow, Fig. 1).
It is the group of systemic seedborne fungi for which no sexual state has been found (often
called symptomless parasites), as well as related fungi in the genus Epichloe that currently offer
new approaches to biological control of pests of turfgrass. Epichloe typhina is a common pathogen
of grasses producing the striking symptom of mycelium surrounding the emerging flower
inflorescence, with the subsequent prevention of flowering and seed production (called choke
disease). This fungus is found on important grass genera, in primarily the Poaceae (e.g., Agrostis,
Bromus. Dactylis. Festuca. Holcus. Hordeum. Lolium and Poa). There has been debate recently
about the taxonomy of the anamorphic state (asexual) of E typhina. Originally classified as
Sphacelia typhina. it now has been reclassified by Morgan-Jones and Gams (23) and confirmed
by White and Morgan-Jones (49) as Acremonium typhinum. Other important symptomless,
seedborne endophytes found in grasses for which there are no known teleomorphic states (sexual)
are now also classified in the same genus Acremonium sec. Albo-lanosa. While this classification
implies morphological relatedness, Johnson et a! (15) have also demonstrated serological
relatedness among some Acremonium spp. and EL typhina isolated from different grasses. The list
of named Acremonium endophytes is shown in Table 1. It should be pointed out that by staining the
mycelium in vegetative tissue and in seed, numerous endophytes have been found in grasses of
the Poaceae but remain as yet unnamed (19,29,41,46).
The emergence of A^ typhinum at flowering depends on the biology of the grass-fungus
association, which will be discussed shortly. When choke symptoms occur, conidia of >V typhinum
are produced on the stroma (broken arrow, Fig. 1). Whether the sexual ascomycetous state of E
typhina occurs depends on simple bipolar heterothalism (two mating types present) and insect
transmission of conidia, which act as spermatia (43). While it has been suggested that species of
the Balansiae producing external spores infect healthy plants via the stigma and style to the ovule
(9), it is also possible that spores infect tillering buds of grasses as well. There is some uncertainty
as to the role of ascospores in the life cycle of these organisms as well as to the mode of infection.
It has been known, since the work of Sampson (30), that EL typhina may remain symptomless
for long periods and be seed disseminated in certain host grasses (12,29). Consequently, Siegel et
ai (37) and Bacon and Siegel (3) consider E, typhina to exist as different biotypes in various host
grasses. The existence of fungal biotypes suggests that there is a continuum within the symbiotic
association as it relates to the compatibility of the partners (22,38). Some biotypes enter into
agonistic (parasitic-pathogenic) interactions whereas others, like the symptomless Acremonium
spp. infecting Festucoideae grasses, enter into mutualistic (beneficial) relationships.
White (42) has differentiated into three types the associations between E typhina and related
Acremonium endophytes, and their grass hosts (Table 2). The biology and ecology of the
associations are important in understanding the distribution of infected plants in the population and
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dissemination of the endophytes. In type 1 associations, infected plants produce stromata fan
external mat of mycelium bearing fructifications) on nearly 100% of the flowering panicles
Populations of plants in this association tend to remain small, spreading primarily as the grass clone
spreads vegetatively. All of the plants in this clonal population are infected. Type 2 like type 3
associations, have been found only in the Festuciodeae. The differences between these two
associations are relatively minor and involve the identity of the fungus and the distinction between
the low level (0 vs. 1-10%) of flowering panicles showing stromata. The spread of endophytes in
type 2 and 3 associations is primarily by seed dissemination, however, ascospores may also be
important in the former association.
The percent of the population infected in type 2 and 3 associations may depend on whether
the grass is present in recent or older cultivations or is from native species. One would expect high
levels of infection in the population of wild grass species as it has been hypothesized that the
endophytes co-evolved with their hosts (37,42). High percentages of infected plants have been
reported to occur in various Lolium and Festuca spp. growing in the wild in the U.S. and Europe
(19,34,42). Populations of older cultivated grass species appear to be highly infected whereas
others from recently introduced cultivars or new cultivation have low levels of infection. For example,
58% of the tall fescue plants, grown on 14 million hectares, in the U.S. have been reported to be
infected with A. coenophialum (31); nearly 100% of the perennial ryegrass plants, grown on 6 million
hectares, in New Zealand are infected with ^ Mi (19,37). Seed of perennial ryegrass (19) and fine
fescues (29) collected from old pastures and turf in Europe also had high levels of infection.
It is now clear that the seedborne and symptomless nature of the endophytes of type 2 and 3
associations has unintentionally resulted in their worldwide distribution along with their cultivated
hosts. The reasons for the differences in levels of infection of cultivated grasses (old vs. new cultivars
or plantings) may have more to do with the commercial methods of handling of seed than with a
failure of the grass to remain infected.
Seed-borne endophytes survive for indefinite periods at low temperatures (0-5C), but generally
lose their viability in much shorter storage periods (1-2 yr) at 20-30C and high seed moisture levels
(40). Grass seed may be stored in the U.S. at ambient temperature for up to 18 months before it is
sold; consequently, seed lots can contain infected seed with different levels of endophyte viability
that result in reduced numbers of infected plants.
GRASS-ENDOPHYTE INTERACTIONS
Symptomless and seed disseminated Acremonium spp. and E typhina (type 2 and 3
associations) can be considered as obligate biotrophs (20). That is, they cannot exist outside the
host (except in laboratory culture) and additionally are not known to be capable of re-infecting, by
natural means susceptible grasses. As discussed earlier, these endophytes are also mutualistic
symbionts, whereas EL typhina of type 1 associations and other specific endophyte species in the
tribe Balansia are agonistic (parasitic) symbionts producing disease. The grass endophytes that are
mutualistic symbionts receive benefit from the association with their hosts in the form of long term
protection and enhanced survival and dissemination (via seed). These endophytes are of great
interest because of the benefits they impart to the hosts. They cause or induce in many instances
improved growth and persistence of the host plants, tolerance to herbivore feeding (animal and
insect) and possible disease resistance. As will be discussed later, these endophytes can be
manipulated for the production of improved turf-grass cultivars.
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Improved plant growth and persistence
Acremonium endophytes confer improved growth performance to some infected cultivars and
clones of perennial ryegrass and tall fescue. Plants of an infected perennial ryegrass clone had
more dry matter, total leaf area, tiller number and growth of roots than plants of the non-infected
clone (18) as well as improved seed set, germination and seedling growth (7). While it has been
suggested that growth and survival are enhanced when field-grown infected tall fescue plants were
grazed (27), experiments in Kentucky with Kenhy tall fescue showed no significant differences in
plant growth and seed production between infested and non-infested mowed plots (34). However,
in greenhouse tests, Bush et aL (6) have shown that infected tall fescue plants performed better
(greater number of tillers, daily photosynthesis and net carbon fixed, and water use efficiency) than
non-infected plants. Belesky ei aL (5) have also reported greater tiller production and net growth in
some tall fescue clones grown under controlled conditions. However, in these experiments, net
photosynthesis rate was lower while stomatal resistance tended to be greater in infected than
non-infected plants. These data support the hypothesis that infected cultivated grasses would have
an adaptive growth advantage over non-infected plants in environments with abiotic stresses
(deficient water and nutrients, high temperature and competition with weed species).
The reason for possible changes in growth patterns of endophyte-infected plants remains
obscure, although it has been suggested that endophytes localized in stem base and sheaths of
plants utilize reserve photosynthate (i.e., fructosans) (5). This utilization may impart source-sink
dynamics, altering the production and partitioning of photosynthate and, hence, growth in infected
plants. In addition, members of the Claviciptaceae may produce auxins or other plant growth
regulators, or they may alter the hormone metabolism of their host. These are distinct possibilities
when one considers that symptoms of infection by E, typhina and other members^of the tribe
Balansia include not only the inhibition of flowers and seed, but also enhanced plant growth,
dwarfism or deformation of the flag leaf (1,8,9). Auxin-like indole compounds have been isolated in
vitro from cultures of Claviceps pupurea and Balansia epichloe (25). The production of these indole
compounds may reflect an alteration of nitrogen metabolism and assimilation in the infected plant
(1).
Insect resistance
One of the most striking effects produced by endophyte-infected grasses is resistance to insect
attack. This subject has been extensively reviewed and will be discussed in detail by Funk et aL
(Chapter 18). An up-to-date list of species of insects reported to be affected by endophyte-infected
Festuca and Lolium species of grasses has been presented elsewhere (37 -see Table 1). In addition,
Pedersen et aL (24) reported that there were lower populations of the spiral (Helicotylenchus
dihystera) and stubby root (Paratrichodorus christiei) nematodes in pots containing infected tall
fescue than in those containing non-infected plants.
Acremonium and E^ typhina-infected grasses produce an array of chemicals that have a wide
range of biological activity. The chemistry and synthesis of these chemicals will be discussed by
Bacon (Chapter 17). Table 3 summarizes the current information available concerning these active
chemicals. Of notable interest is peramine, an insecticidal compound originally recovered from /L
join-infected perennial ryegrass. This compound has also been found in many grasses infected with
A, coenophialum or E typhina (33). However, not all biotypes of E. typhina produce peramine, as
the compound was not recovered from the naturally infected cultivar Ensylva (Festuca rubra rubra)
or from Dawson (R rubra litoralis) artificially infected (via seedling wounding) with an JB typhina
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isolate from an unidentified cultivar of R rubra grown in New Zealand (Siegel el aL unpublished
data). Ergot alkaloids originally found in A, coenophialum-infected tall fescue have also been
recovered from various E typNna-infected grasses (Bacon and Siegel, unpublished data) as well
as perennial ryegrass infected with A, lolii (28).
The number and quantity of compounds found in endophyte-infected grasses may play an
important role in determining the spectrum of insecticidal activity as well as affect the potential for
the development of insect resistance. Of the types of compounds listed in Table 3, only loline
alkaloids are found in high concentrations in the plant. The reputation for a high level of insect
resistance by infected tall fescue may be based, in part, on the concentration of loline as well as
the presence of the other toxic chemicals. On the other hand, the compounds found in infected
perennial ryegrass are present at ca. 250 fold less than the loline alkaloids but still exert a
considerable spectrum of activity (37). The ability of certain fungal symbionts (e.g.. A. coenophialum
and A.ipJii) to produce at least three biologically active compounds likely contributes to an improved
spectrum of activity. If one hypothesizes that insects would become resistant to these compounds
by different mechanisms, then potential for the development of resistance by the insect is negligible.
From these aspects of the synthesis of insecticidal compounds in endophyte-infected grasses one
might speculate that the level of the chemical may be less important than the number of chemicals
produced by the host-fungus association.
While the topic of this chapter involves the nature of endophyte-infected grasses, endophytes
from tall fescue and perennial ryegrass used in pasture have been removed to improve animal
performance. These endophyte-free cultivars do not contain any of the biologically active
compounds found in infected grasses. However, because the fitness of the partners in the
grass-fungus association involves mutualism, some questions have been raised about whether
these endophyte-free cultivars would be able to survive over long periods of cultivation (32,37). It
is quite clear that removing the endophyte from perennial ryegrass in New Zealand resulted in loss
of stands by predation of the Argentine stem weevil and animal overgrazing. Whether attack by
insects, poorly managed grazing practices, reduced plant vigor and survival during periods of abiotic
stresses will also cause loss of recently established endophyte-free tall fescue pastures in the U.S.
is currently unknown. However, small plots of Ky 31 and other tall fescue cultivars containing low
levels of infected plants have existed in the transition zone of the southeastern U.S. for many years
(31,34).
We have devised laboratory assays to test for activity of some of the chemicals produced in
infected plants. Figure 2 A,B illustrate one such assay system (14). The plastic cup contains a piece
of dental cotton (holds 300 ml of water), one sunflower seed and five Oncopeltus fasciatus (large
milkweed bug) nymphs (1-12 days old). Test chemicals in water or water alone are applied to the
cotton and the nymphs are allowed to feed. At intervals the percent mortality is determined. The
data in Table 4 indicate that N-formyl loline, ergotamine (peptide type of ergot alkaloid) and
ergonovine (clavine type of ergot alkaloid) had ED50 values after 6 days of exposure of
approximately 7.81 ug/ml. Higher concentrations produced more rapid onset of death. Ergocryptine
(peptide type) was toxic only at 1 ug/ml. Ergovaline (peptide type), the predominant ergot alkaloid
(40-70%) recovered from endophyte-infected tall fescue, was not available for testing.
The broad spectrum activity of N-formyl loline was evaluated via preliminary contact studies
with a number of other insect species. Loline was toxic to the cat flea (CtenocephaHdes fejis),
oat-birdcherry aphid (Rhoaajoslphum padi), greenbug aphid (Schizaphis graminum), American
cockroach (Periplaneta americana), adult face flies (Musca autumnaiis), larvae of Japanese beetle
(PapM japonica). and eggs of the tobacco budworm (Helkfe Mescens). Chrome exposure to 1
ug/ml In waJeTdurlng the entire life of the milkweed bug in the assay previously described resulted
173
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in delayed development and reduced fecundity. In addition, 1 ug applied topically in acetone to
adult milkweed bugs is sufficient to kill 50% of the test insects after 4 days of exposure, the dose
being somewhat dependent upon the age and weight of the individual adult. An injected dose of 1
ug/adult results in approximately 50% mortality. The catbird cherry and greenbug aphids can also
be killed by ingesting lolines either from within infected tall fescue stems and leaves (the compounds
are not present on the surfaces of the plant; Eichenseer, unpublished data) or from non-infected
stems that had previously taken up the alkaloids from water (Siegel, unpublished data).
In summary, various insects were very sensitive to purified N-formyl loline in several different
assay systems (contact, ingestion and injection). Eventually, all the toxic chemicals produced in
infected plants will be similarly assayed and their modes of action determined. This information will
aid in understanding further the host-endophyte interaction and how this interaction can better serve
the needs of man as he uses grasses for aesthetics and conservation.
Disease resistance
Resistance to plant diseases by endophyte-infected grasses has not been reported. However,
agar plate antibiosis assays have indicated that antifungal compounds were produced in vitro by
isolates of Acremonium spp., Phialophora-like sp. and E. typhina from various grasses (44,45, Latch
and Siegel, unpublished data). An example of the kind of antibiosis experiment conducted by Latch
and Siegel is shown in Figure 2 C,D. Zones of inhibition of growth of the test grass pathogen by a
soluble factor(s) from the endophyte colonies are clearly evident. This experiment and others
indicate that a diverse range of antibiosis exists among isolates of E. typhina and various
Acremonium species. Both the spectrum and amount of antifungal activity appears to be endophyte
isolate dependent. In part, this dependency suggests the presence of fungal biotypes existing within
the same grass cultivar or species.
Reasons for the lack of expression of antibiosis (disease resistance) in pasture and turf Festuca
and Lolium spp. are unknown. It is possible that the antifungal compound(s) is produced, but not
in sufficient quantity to control the pathogens.
MANIPULATION OF GRASS ENDOPHYTES FOR USE IN TURF
The use of the Acremonium endophytes in turfgrasses as agents of plant protection and
improvement has certain unique advantages. As previously discussed, the natural association
between the grass hosts and these endophytes is one of mutualism (benefits). In addition, the
endophytes are propagated with the plant by vegetative means through tillers and by
seed-dissemination. Thus, the endophytes can be regarded as compartments of maternally-
inherited genetic information that can be removed, manipulated, and re-introduced into the grass
plant. Genes contained within this compartment include those that direct or affect production of
loline, ergot, and peramine alkaloids and lolitrem toxins, and other compounds (not yet identified)
which directly or indirectly provide enhanced resistance to insects, plant pathogens and improved
plant growth and survival.
Production of improved endophyte-infected grasses can be achieved by plant breeding
(maternal line selection) (12) or by artificial (wounding) introduction of the endophyte into seedling
meristem (synthetic complexes or combinations of endophyte and host grass) (16). The latter
method is illustrated in Figure 2 E,F,G and can be used with naturally occurring or genetically
modified endophytes.
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Use of naturally occurring endophytes
A number of endophyte-infected grass cultivars have been developed for insect resistance
by maternal line selection (12,29, see Funk, Chapter 18). In most cases, the endophyte is already
present in the grass cultivar, usually at a low level of infection. It then becomes a matter of selection
and increasing the number of infected tillers and plants. However, in some cases, the endophyte
must be transferred from one cultivar to another within the same plant species. The resulting cultivar
must not only contain the endophyte but also have desirable characteristics for turf use.
One of the current problems with the use of naturally occurring endophytes is the presence of
biotypes which produce less of the desired beneficial chemicals. For example, it has been
demonstrated that a biotype of IE typhina infecting Ensylva neither produces any of the known
compounds (lolines, peramine and ergot alkaloids) responsible for insect resistance, nor can insect
resistance be demonstrated using an aphid bioassay (Siegel, unpublished data). Biotypes of A
coenophialum exist which do not produce ergot alkaloids (4). Likewise, we have shown that biotypes
of Acremonium spp. exist which apparently produce varying levels of antifungal chemical(s) in
culture.
It is clear that considerable screening and characterization of the host-endophyte interaction
will be necessary in order to ensure that all the required chemicals are produced. By using artificial
inoculations one may be able to ensure that specific biotypes exhibiting superior performance in
one plant can be introduced into others of the same species.
Use of genetically modified endophytes
Endophytes modified by recombinant-DNA techniques may be used to (i) enhance already
existing beneficial characteristics; (ii) introduce foreign genes which are of benefit to the plant (these
may include genes for the synthesis of antibiotics antagonistic to insects and causative agents of
grass diseases, genes for the detoxification of herbicides, or factors that enhance growth and
persistence of the host grass); and (iii) gain further understanding of how fungal-plant mutualistic
relationships are established so that the genetic potential of endophyte genomes can be
manipulated for crop improvement. Manipulation and improvement of grass endophytes by genetic
means will require elucidation of the function(s) and role(s) of secondary compounds produced in
the host-fungus interaction, particularly with regard to biosynthetic pathways and effects of
chemicals on livestock, insects, microbes and plant growth. In addition, it will be necessary to
develop DMA-mediated transformation systems and associated techniques of cloning, gene
replacement and complementation. Development of a transformation system will, in turn, require a
knowledge of the nature and requirements of gene expression in the endophyte as well as gene
expression of the host in response to infection, expression of disease (choke) and synthesis of
secondary metabolites.
CONCLUSIONS
The mutuaiistic relationship between grasses and the Acremonium fungal endophytes provides
an excellent model system for studying the nature and expression of biologically active secondary
metabolites, molecular genetic studies, and improvement of agriculturally important grasses. These
fungi do not produce disease in their host grasses, are obligate biotroph.c symbionte, grow in the
meristems leaf sheaths and leaf blades of their hosts, and are seed-disseminated. Because of
175
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their ecological role and life cycle, the Acremonium endophytes are ideal agents for biological control
of insects and possibly diseases of turfgrasses and for basic studies of mutualism.
New endophyte-infected turfgrass cultivars with enhanced resistance to insects are now
available. Whether they are commercially successful depends on factors discussed elsewhere in
this book. However, because the potential is so great for turfgrass improvement, it seems that future
use of infected cultivars will be assured, particularly if endophytes with genetically modified genomes
are developed.
ACKNOWLEDGEMENT
We wish to thank authors for providing unpublished information and copies of manuscripts in
press. Research was supported, in part, by USDA Competitive Research Grant 85-CRC-1-1533.
This chapter is Kentucky Agricultural Experiment Station Journal Series Paper 88-11-7-3-50.
176
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grasses: A
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Environ. Microbiol. 34:576-581 . -**-
3. Bacon, C. W., Siegel, M. R. 1 988. Endophyte parasitism of tall fescue. J, Prod. Agric. 1 :45-55.
4. Bacon, C. W. Procedure for isolating the endophyte from tall fescue and screening isolates of it for ergot alkaloids
Appi Environ. Microbiol. 54:261 5-261 fl
5. Belesky, D. P., Devine, O. J., Pallos, J. E., Jr., Stringer, W. C. 1987. Photosynthetic activity of tall fescue as
influenced by a fungal endophyte. Photosynthetica 21 :82-87.
6. Bush, L P., Gay, S. L, Johnson, M. C. 1 986. Growth and water use of endophyte-infected and endophyte-free tall
fescue. Amer. Soc. Agron. Ann. Meetings. Agron. Abstr. p. 140.
7. Clay, K. 1987. Effects of fungal endophytes on the seed and seedlings biology of Lolium perenne and Festuca
arundinacae. Oecologia 73:358-362.
8. Clay, K. 1986. Grass endophytes. In Microbiology of the Phyllosphere (J. Kokkena and J. van den Heuvel, eds.),
pp. 188-204. England: Cambridge University Press.
9. Diehl, W. W. 1950. Balansia and the Balansiae in America. Agric. Monogr. 4. Washington, D. C.: US Dep. Agric.
10. Fineran, B. A., Harvey, I. C., Ingerfeld, M. 1983. Unusual crystalloids and aggregates of tubules in the Lolium
endophyte of ryegrass leaf sheaths. Protoplasma 117:17-23.
11. Fletcher, L. R., Harvey, I. C. 1981. An association of a Lolium endophyte with ryegrass staggers. H* 2L Vet. sL
29:185-186.
12. Funk, C. R., Halisky, P. M., Ahmad, S. Hurley, R. H. 1985. How endophytes modify turfgrass performance and
response to insect pests in turfgrass breeding and evaluation trials, in Proc. Fifth Int. Turf Res. Conf. Avignon,
(F. Lemaire, ed.) pp. 137-45, Versailles: INRA.
13. Hinton, D. M., Bacon, W. C. 1985. The distribution and ultrastructure of the endophyte of toxic tall fescue. Can. JL
Bot. 63:36-42.
14. Johnson, M. C., Dahlman, D. L., Siegel, M. R., Bush, L. P., Latch, G. C. M. et ai 1985. Insect feeding deterrents
in endophyte-infected tall fescue. Appl. Environ. Microbiol. 49:568-571 .
15. Johnson, M. C., Siegel, M. R., Schmidt, B. A. 1985. Serological reactivities of endophytic fungi from tall fescue and
perennial ryegrass and of Epichloe typhina. Plant Disease 69:200-202.
16. Latch, G. C. M., Christensen, M. J. 1 985. Artificial infection of grasses with endophytes. Aum Appl. Bjoi 1 07:1 7-24.
17. Latch, G. C. M., Christensen, M. J., Samuels, G. J. 1 984. Five endophytes of Lolium and Festuca in New Zealand.
Mycotaxon. 20:535-550.
18. Latch, G. C. M., Hunt, W. F., Musgrave, D. R. 1985. Endophytic fungi affect growth of perennial ryegrass. N, "L vL
Agric. Res. 28:165-168.
19. Latch, G. C. M., Potter, L R., Tyler, B. F. 1987. Incidence of endophytes in seeds from collections of Lolium and
Festuca species. Ann. Appl. Bjol 1 1 1 :59-64.
20. Lewis, D. H. 1 973. Concepts in fungal nutrition and the origin of biotrophy. BjoL Revs, 48:261 -278.
21 . Lewis, D. H. 1 974. Micro-organisms and plants: The evolution of parasitism and mutualism. 24th Symp, Soc, Gea
Microbiol. pp 367-392, England: Cambridge University Press.
22. Lewis D H 1985 Symbiosis and mutualism: Crisp concepts and soggy semantics. In JM Biology of Mutualism
(D.'n. Boucher, ed.), pp. 29-39, New York: Oxford University Press.
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23. Morgan-Jones, G., Gams, W. 1982. Notes on Hyphomycetes, XLI. An endophyte of Festuca arundinacea and the
anamorph of Epichloe typhina. new taxa in one of two new sections of Acremonium. Mycotaxon 15:311-318.
24. Pedersen, J. R., Rodrigues-Kabana, R., Shelby, R. A. 1988. Ryegrass cultivars and endophytes in tall fescue affect
nematodes in grass and succeeding soybeans. Agron. J. 80:811-814.
25. Porter, J. K.f Bacon, C. W, Cutler, H. G., Arrendale, R. F., Robbins, J. P. 1985. In vitro auxin production by Balansia
epichloe. Phytochemistry 24:1429-1431.
26. Pottinger, R. P., Barker, G. M., Prestidge, R. A. 1985. A review of the relationships between endophytic fungi of
grasses (Acremonium spp.) and Argentine stem weevil (Listronotus bonarienses Kuschel). Proc. 4th Australas.
Conf. Grassl. Invert. Ecol. Lincoln Coll.. Canterbury, pp. 322-331.
27. Read, J. C., Camp, B. J. 1986. The effect of the fungal endophyte Acremonium coenophialum in tall fescue on
animal performance, toxicity, and stand maintenance. Agron. J.. 78:848-850.
28. Rowan, P. P., Shaw, J. G. 1987. Petection of ergopeptine alkaloids in endophyte-infected perennial ryegrass by
tandem mass spectrometry. N. Z. Vet. J. 35:197-198.
29. Saha, P. C., Johnson-Cicalese, J. M., Halisky, P. M., van Heemstra, M. L, Funk, C. R. 1987. Occurrence and
significance of endophyte in fine fescues. Plant Pis. 71:1021 -1024.
30. Sampson, K. 1933. The systemic infection of grasses by Epichloe typhina (Pers.) Tul. Trans. Br. Mycol. Soc.
18:30-47.
31. Shelby, R. A., Palrymple, L. W. 1987. Incidence and distribution of the tall fescue endophyte in the United States.
Plant Pis. 71:783-786.
32. Siegel, M. R., Bush, L. P., Pahlman, P. L. 1987. What am I losing by removing endophyte from tall fescue. Proc.
43rd South. Past. Forage Improv. Conf. pp. 41-44, USPA/ARS Nat. Tech. Infor. Ser., Springfield, VA.
33. Siegel, M. R., Fannin, N., Bush, L. P., Rowan, P. 1987. Synthesis of peramine and loline alkaloids in fungal
endophyte-infected grasses. Ann. Meet. Mycol. Soc. Amer. Ottawa. Abstr. 38 (p. 69).
34. Siegel, M. R., Johnson, M. C., Varney, P. R., Nesmith, W. C., Buckner, R. C., et ah 1984. A fungal endophyte in
tall fescue: Incidence and dissemination. Phytopathology 74:932-37.
35. Siegel, M. R., Jarlfors, U., Latch, G. C. M., Johnson, M. C. 1987. Ultrastructure of Acremonium coenophialum.
Acremonium loll! and Epichloe typhina endophytes in host and non-host Festuca and Lolium species of grasses.
Can. J, Bot. 65:2357-2367.
36. Siegel, M. R., Latch, G. C. M., Johnson, M. C. 1985. Acremonium fungal endophytes of tall fescue and perennial
ryegrass: significance and control. Plant Pis. 69:179-183.
37. Siegel, M. R., Latch, G. C. M., Johnson, M. C. 1987. Fungal endophytes of grasses. Ann. Rev. Phytopathology
25:293-315.
38. Starr, M. P. 1975. A generalized scheme for classifying organismic associations. Symbiosis Symposia Soc. Exper.
Biol. 29:1-20.
39. Weedon, C. M., Mantle, P. G. 1987. Paxilline biosynthesis by Acremonium lolii: a step towards defining the lolitrem
neurotoxin. Phytochemistry 26:969-971.
40. Welty, R. E., Azevedo, M. P., Cooper, T. M. 1987. Influence of moisture content, temperature and length of storage
on seed germination and survival of endophytic fungi in seeds of tall fescue and perennial ryegrass.
Phytopathology 77:893-900.
41. White, J. F., Jr. 1987. The widespread distribution of endophytes in the Poaceae. Plant Pis. 71:340-342.
42. White, J. F., Jr. 1988. Endophyte-host associations in forage grasses. XL A proposal concerning origin and
evolution. Mycologia 80:442-446.
43. White, J. F., Jr., Bultman, T. L. 1987. Endophyte-host associations in forage grasses. VIII. Heterothalism in Epichloe
typhina. Amer. J, Bot. 74:1716-1721.
44. White, J. F., Jr., Cole, G. T. 1985. Endophyte-host associations in forage grasses. III. In vitro inhibition of fungi by
Acremonium coenophialum. Mycologia 77:487-89.
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45. White, J. F., Jr., Cole, G. T. 1986. Endophyte-host associations in forage grasses. IV. The endophyte of Festuca
versuta. Mycologia 78:102-107.
46. White, J. F., Jr., Cole, G. T. 1986. Endophyte-host associations in forage grasses. V. Occurrence of fungal
endophytes in certain species of Bromus and Poa. Mycologia 78:846-850.
47. White, J. F., Jr., Cole, G. I, Morgan-Jones, G. 1987. Endophyte-host associations in forage grasses. VI. A new
species of Acremonium isolated from Festuca arizonica. Mycologia 79:148-152.
48. White, J. F., Jr., Morgan-Jones, G. 1987. Endophyte-host associations in forage grasses. VII. Acremonium
chisosum. a new species isolated from Stipa eminens. Mycotaxon 28:179-189.
49. White, J. F., Jr., Morgan-Jones, G. 1987. Endophyte-host associations in forage grasses. IX. Concerning
Acremonium typhinum. The anamorph of Epichloe typhina. Mycotaxon 29:489-500.
50. White, J. F., Jr., Morgan-Jones, G. 1987. Endophyte-host associations in forage grasses. X. Cultural studies on
some species of Acremonium Sect. Albo-Lanosa, including a new species, A. starrii. Mycotaxon 30:87-95.
179
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180
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TABLE 1
Acfemonium FungaJ Endophytes of Grasses.
Fungus Grass Refa
Epichloe typhina Lolium. Festuca. Agrostis. Dactylis, (9,23,
(Acremor.ium typhinum) Holcus. Hordeum. Poa. etc. 49)
A. coenophialum £. arundinacea, P_. autumnal is (23,50)
A. lolii L. perenne (17)
A. huerfanum ][. arizonica (Colorado)0 (47)
A. chisosum Stipa eminens (48)
A. starrii £. arizonica (Texas)0, (50)
"" Bromus anomalus, F_. obtusa,
F. subulata
* References for name of fungus and species of infected grass.
b Fungus isolated from the populations found in Colorado or Texas.
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TABLE 2
Characterization of the association between Epichloe typhina and related Acremonium
endophytes and their grass hosts3.
Z flowering
Association panicles shoving
No . symptoms Fungus
1 I 98 E. typhina
2 1-10 E. typhina
3 0 Acremoniun spp.
Z
Type of population
Association infected
Pathogenicb > 98
Pathogenicb 50-70
or mutualistic
Mutualistic * 90
Fungal
dissemination0
Spread by clonal growth
of host and ascospore
infection
Spread by clonal growth
of host , seed and
ascospore infection
Spread by seed and
clonal growth of host
grass
Grass
host
Several sub-
families of
Poaceae and
sedges
Festucoideae
only
Festucoideae
only
8 Adapted from White (42).
b Same as parasitic in the sense of Lewis (21) and Siegel et al. (37). The term agonistic is now suggested by
Lewis (22).
c Listed in order of importance.
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TABLE 3
Biologically active compounds isolated from endophyte-infected Festuca and Lolium species
of grassesa.
Origin
Chemical (grass)b
Ergot alkaloids TF.PRG,
HF.CF
Loline alkaloids TF
Peraaine alkaloids TF.PRG,
HF.CF
Lolitreras & PaxillineS PRG
Tetraenone steroid TF
• Summary of data from Ref. 1,3,
b Abbreviations: TF, tall fescu
(L. perenne) ; CF, Chewings and
coenophialum; A.I., A. lolii,
Average Distribution in
amount (pg/g) plant6 Produced
Orig1n drv wt — - . . i..
(fungus)b»c in plantd Roots Stems Leaves culture toxicity
A.c.,A.l., 3-10 (TF) ND
A.c. 2,000 (TF) +f
A.C..A.1., 5-25 (PRG)
E.t., E.t.
A.I. 3-25 (PRG) ND
A.c. ND ND
4,37 and unpublished data of Siegel,
e (F. arundinacea); HF, hard fescue
creeping fescue (F. rubra coramutata
E.t., Epichloe typhina.
+ + Yes Insect & mammalian
+ + No Insect
+ +• Yes Insect
+ 4- No, Yes Insect & mammalian
ND ND Yes Microbial & mammalian
Latch and Bacon.
(F. longifola); PRG, perennial ryegrass
and F. rubra litorales); A.c., Acremonium
c Refers to the fungus which infects the grass listed in the previous column; i.e., A.c. infects TF, E.t. infects
HF, etc.
d Average amount in the grass listed in parenthesis, includes vegetative parts and seed.
e ND, not determined; -, not present; +, present.
f 10-15Z of total loline found in plant (Bush, unpublished data).
8 Paxilline is a precursor of lolitrem B and is produced in both culture and the plant, whereas only lolitrem B has
been detected in the plant (39).
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TABLE 4
Percent mortality of Oncopeltus fasciatus (large milkweed bug) offered either N-formyl loline
or various ergot alkaloids in water3
Concentration (Mg/ml)
Day
2
4
6
2
4
6
2
4
6
2
4
6
Compound 1000
N-Formyl Loline
80
100
100
Ergotamine
90
100
100
Ergonovine
50
85
95
Ergocryptine
5
45
65
125
55
100
100
65
90
95
30
55
80
0
0
5
31.25
10
70
90
35
75
90
30
35
40
0
5
5
7.81
10
20
55
0
35
50
15
25
40
0
0
0
Control
10
10
10
Methods used the same as in Johnson et al. (14).
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FIGURE 1
Generalized life cycles of grass endophytes. Question Mark (2); indicates that uncertainty
exists as to the role of ascospores in the life cycle of these organism (e.g. E. typhina) as well as to
the mode of infection (via stigma) (adapted, in part, from Ref. 1). Solid arrows: endophytes that are
seedborne as in the Festucoideae grasses and in cleistogramous Balansiae-infected seeds. Broken
arrows: transmission of endophytes via spores, in the case of Ephicioe typhina ascospores, from
stromata of infected plants.
Fungus Ge
Through Sti
Endophytic
Mycelium
In Seed
Fungus Germ
Tube
Enters Stigma (?)
Endophytic
Mycelium
into Ovule
Active Mycelium
Infects
Grass Seedling
Germinating Spore
Endophytic
Mycelium
Enters Flower
Stem
Sporulating
Fructifications
(Ascospores, Conidia)
at Flowering (?)
Active Endophytic
Mycelium in Seedling
(Stem Tissue and
Leaf Tissue)
185
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FIGURE 2
A, component parts of milkweed bug (Oncopeltus fasciatus) antibiosis assay (plastic cup, plug
of dental cotton and cardboard top). B, assembled assay, includes 5 nymphs. C and D, antibiosis
assay for chemical activity of various endophyte isolates. Photographs are of the underside of agar
plates. Test grass pathogen growing from center of the plate, Rhizoctonia cerealis. Endophyte
isolates of Acremonium coenophialum place on the periphery were isolated from tall fescue: 9, Ky
31; 10, Kenhy; 11, Fawn; 12, Alta; 13, unknown tall fescue cultivarfrom NZ; 14, Ky 31. Acremonium
lolii isolated from: 15, Nui. Acremonium starrii isolated from: 16, Festuca arizonica. E, F, G: Artificial
inoculation of one week old seedlings. Arrows indicates position of the meristem, wounded meristem
and meristem inoculated with mycelium of the endophyte. Seedlings grown on water agar (2%) and
wounding operation done under a stereo microscope using a scalpel, with disposable blade (see
Ref. 16 for the detail).
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UTILIZATION OF FUNGAL ENDOPHYTES
OF GRASSES:
LABORATORY MANIPULATIONS FOR
SPECIFIC TOXINS
Charles W. Bacon
Toxicology and Mycotoxlns Research Unit
USDA/ARS
Richard B. Russell Agricultural Research Center
P.O. Box 5677
Athens, Georgia 30613
The ecological necessity for an intimate association of a fungal endophyte with a grass is
suggested by the widespread occurrence of these two vastly different organisms as a composite
system (1,2,3). Fungal grass endophytes include species of Acremonium. Epichloe. and Balansia
(Clavicipitaceae , Ascomycetes) that live within and are associated intimately with various species
of grasses and sedges. The compatible nature of this relationship (4,5), as well as data from various
laboratories led Siegel et al. (6) and Bacon and Siegel (7) to conclude that this association was a
mutualistic symbiosis. The fungus receives nutrients from the grass, and is protected and
disseminated. Infected grasses benefit by increased growth (8,9,10), reduced predation from
vertebrate and invertebrate herbivores (11,12,13), and drought tolerance (14). Additional benefits,
while observational, include disease resistance and stress sparing mechanisms (15,14). Before
we can completely define the symbiotic nature and ecological success of endophyte-infected
grasses, field data reflecting physiological responses of infected grasses to strenuous environmental
stresses are needed. Nevertheless, it is the use of ecological benefits derived from the association
that is the current focus of research.
Researchers are attempting to transfer endophytic fungi into grasses, primarily conservation
and turf grasses, many species of which are not natural hosts. Benefits from these infections are
expected to include increased pest resistances, improved appearance, and tolerance to
environmental stresses. There are many potential uses for such symbiotic systems, but they may
be grouped under two broad classes: biological controls for grass growth, stamina and appearance;
and biological control for pests on grasses. Fungal endophyte-infected grasses are unique in that
they are one of few biological controls that can be used, in addition to deterring pest, for controlling
the morphology and stamina of a group of plants so essential to man's environment and health.
Use of infected grasses requires complete understanding of the in vitro and in vivo
requirements for the fungus relative to predicting its performance when transferred to non-host
grasses. After having accomplished infecting non-host grasses, experiments designed to determine
agronomic performances of the infected grasses should pose no problem. However, when we try
to attribute specific performance aspects of infected grasses to either the grass, fungus, or both
we are faced with an experimental dilemma. The problem is compounded when we want specific
information related to the fungus as a potential for forage improvement. Working with isolated fungus
involves problems of defining and maintaining in vitro the desired in vivo characteristics. Thus, there
is a need to 1) develop laboratory techniques for culturing the endophyte in vitro ; 2) develop media
which will characterize and maintain useful specific physiological strains of the endophyte; and 3)
develop techniques for transferring the endophyte to the desired grass species.
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It is my intention to discuss the first of these two research needs, and to describe results of
studies which established that while these fungi are varied and genetically unstable upon isolation,
their in vitro culture may still be used to experiment with in situ resistance mechanisms after transfer
to grasses. The infection of grasses, developed by Latch et al. for grass seedlings (16, and see
companion chapter by Siegel et al. this proceeding), will not be covered. The discussion will center
mainly around the endophytes of tall fescue and/or perennial ryegrass since these two are of
considerable economic importance, and are the major focus of attention by various endophytologists.
A more detailed discussion on morphology and taxonomy, and host parasite relationships of these
two endophytes as well as other species of endophytes can be found in recent reviews (6,7,17,18)
and in the chapter by Siegel in these proceedings.
ISOLATION OF FUNGI
The fungi (Table 1) may be isolated from either recently collected field or greenhouse grown
material. Most endophytic fungi are located in the sheath portion of a grass leaf and it is an inner
sheath that should be used since it is relatively free of debris and saprophytic fungi. For those fungi
that are not located in leaves, it would behoove one to use the inner, least exposed plant tissue
since it too will be free of debris. Material intended as a source for endophytes should be used
immediately or stored under refrigeration (4 C) in tissue paper dampened with sterile water, but
only for a few hours.
Small sections of sheaths are sterilized in full strength commercial bleach, rinsed in sterile
water, cut into smaller sections (Table 2) and placed in either liquid medium or agar isolation media
(Table 3). Additional isolation procedures have been reported for other endophytes and include
such starting material as ascospores (19), and seed (16). The speed of isolating the fungus from
grass tissue depends on tissue type and its preparation, genetic characteristics of each fungus and
isolation media. The total time will vary from as early as 2 weeks on the liquid medium to as late
as 6 weeks on the agar medium. Agar medium is solid and on solid media nutrients are more limited
due to reduced diffusion of growth requiring compounds. Generally fungi producing choke symptoms
(see chapter by Funk, this proceeding) will grow faster than nonchoke inducing species. This
possibly reflects a difference in the nutritional fastidiousness of the two basic groups.
Once isolated, grass endophytes can be stored on either corn meal-malt agar or M102 medium
(Table 3). Fungi may be stored under refrigeration only if they are freshly isolated and producing
spores. Spores can survive the storage temperatures frequently used to preserve fungi (-20 to 0
C). Older nonsporulating isolates can be safely stored under warmer temperatures (4 to 10 C), or
at room temperatures (20 to 26 C). Storage at room temperature is particularly recommended for
those isolates that are nonchoke inducing as they rapidly loose the ability to produce spores. I have
had no success with storage of endophytes on substrates traditionally used for fungi, i.e. silica gel,
soil, etc.
The exact in vitro growth requirements of endophytic fungi have not been established. Most
media are nondefined and complex and at best semisynthetic (19,20,21). One isolate of the
endophyte of fescue was induced to grow on defined and relatively simple media after it was
maintained in the laboratory for a considerable period of time (20,21). In another group of
endophytes, Balansia which are associated primarily with weed grass species, a defined medium
has been used to culture five species (22). I have not had any success using these defined media
for initially isolating fungi from grasses. However, once endophytes have been isolated using a
complex media of choice, defined media (20,21, 22) may be tried.
Regardless of the media selected, shake culture of liquid media is favored over stationary
culture when it is desired to obtain a rapid growth of fungus. Once maximum amount of growth is
188
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produced, the culture may be continued as stationary cultures where several secondary products
are produced (see below).
CULTURE
After an endophyte is isolated, it may be tested for the synthesis of specific substances on a
specific culture medium. If one is trying to determine whether an isolate is toxic to cattle, or to
insects, the procedure to follow should include a two-stage fermentation (Table 4) with the addition
of specific substrates which are considered possible precursor for inducing the synthesis of specific
metabolite, e.g. tryptophan for ergot alkaloids (Table 4). An alternative is to use either liquid or agar
media to culture endophytes and use it directly to determine toxicity using one of many insect feeding
bioassays (11,12,13). Of course negative bioassay results need not mean that an isolate is
biologically inactive. Rather, it may mean that the in vitro requirement is not met. An in vitro test of
isolates should be taken to mean that under test conditions they are either producing or not
producing the desired compound. However, work on species of Balansia established that qualitative
production of ergot alkaloids occurred both in vivo and in vitro (19). This same corollary was
established for the endophyte of tall fescue (23,24,25), and is suggested from the work of Rowan
et al. (13) for the production of peramine by the ryegrass endophyte. Concern for only mammalian
need only be considered if the intended endophyte is for agronomic improvement of forage grasses
and not conservation and turf grass species.
The competence of an endophyte to produce the desired biologically active compound should
be done on the initial isolate as this ability may not be stable in culture, e.g. ergot alkaloids, Table
5. It is not known if in fact this loss in biosynthetic potential for a substance is restored to an isolate
upon re-infecting it into grass material. Work on this aspect of the endophytes is being done (Siegel
and Bacon, unpublished). An alternative procedure for working with endophytes is to obtain single
spore isolates of the initial fungus. This procedure, while tedious, might lead to the selection of
colonies that are superior or equal to the initial isolate, and contain one basic nuclear type. Such
colonies should be stable for a considerable period of time, allowing for strain improvement using
any of the processes, e.g. protoplast fusion, mutagenesis.
SECONDARY METABOLISM
This section will center on the production of several biologically active compounds which are
secondary metabolites and whose intended use makes grass endophytes economically attractive.
These compounds consist of a variety of chemically complex and structurally unrelated substances
that have been associated with grasses, fungi and endophyte-infected grasses (Table 6). For the
most part, compounds produced by endophytic fungi are alkaloids and they may or may not have
the same biogenetic precursors since they have such diverse chemical structures. Of course there
may be many more unknown secondary metabolites than currently reported, but the ones that are
known are all produced from only a few biochemical intermediates of primary metabolism (Table
6). The compounds selected for inclusion in this table are those that were either studied in the past
and related to some aspect of cattle toxicity, synthesis by the fungus in culture, or associated with
some economic aspect of the infected grass.
Control of the biosynthesis of compounds availability of precursors. As is the case for the in
situ origin of the final infected grass product, the origin of intermediates used in their biosynthesis
might priginate from the grass and/or the fungus. It must also be considered that the fungus might
produce one portion of the molecule, and the grass chemically modifies it, as suggested for the
synthesis of the neurotoxin, lolitrem B, found in infected perennial ryegrass (31). Table 6 lists, where
possible, the class of compounds grouped according to the precursor biosynthetic origin for fungal
189
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secondary metabolites following Turner's scheme (32) which may be useful for adding inducer
substrates when formulating media to test for biosynthesis of specific classes of compounds.
Only recently have attempts been made to demonstrate whether substances are produced
by the fungus independently of the grass and the reverse. Table 6 also lists those compounds that
have been reported to occur in grasses whose infection status was unknown. Attempts to
demonstrate that endophytes alone can make some of the major biologically active compounds in
culture have failed, but these negative data may only mean that the culture conditions have not
been met. It has been established that one of these, loline, is produced only in infected tall fescue,
while another, perloline, is produced by both infected and noninfected grasses.
The media used for isolating and growing endophytes all have a high carbon to nitrogen ratio,
and this ratio can vary within a range of 100 to 10, particularly for vegetative growth. I have found
that this ratio is not optimum for the production of classes of secondary metabolites that are, at least
partially, under nutritional control. One such class of compounds is the ergot alkaloids in which the
qualitative and quantitative levels produced on media occur when the carbon to nitrogen ration is
reversed in the direction of higher nitrogen. In addition to this ratio, media may be used where the
form of nitrogen supplied is such that the rate of its utilization is slow. This suggest that the control
mechanism for this class of compounds may involve nitrogen catabolite repression (27), as has
been suggested for the mechanism for ergot alkaloid synthesis by a closely related fungus Claviceps
sp. (28).
As indicated above, a characteristic of media useful for detecting secondary metabolites is the
very slow growth rate. Slow growth rate is not only a factor of media, but also an inherent quality
of each isolate. For the most part, ergot alkaloid-producing isolates that grow the slowest, but
sporulate the most are the highest ergot alkaloid producers. This statement is based on data using
endophytic species of Balansia (19,22). Information is not available one other endophytes to
supports this generality.
Yates (29) has reviewed and he is indeed a leader in the research on the isolation and chemical
identification of alkaloids and other substances isolated from tall fescue grasses. Garner et al. (30)
have developed useful cattle toxicity bioassays for determining the activity of most compounds
reported by Yates. In addition to these excellent reviews, a spectrum of biological activities for these
and other compounds, as well as current bioassays can be found in the chapter by Siegel et al. (this
book).
In the grass-fungus situation the environment is also expected to influence both the production
of secondary metabolites and hence any associated animal pest, or fungus disease defense
mechanism. Such environmental influences on the accumulation of secondary metabolites by plants
(33,34), and in endophyte-infected tall fescue (13) are documented. These studies have only
examined the effects of nitrogen and its interaction with soil moisture on the accumulation of ergot
alkaloids, but similar effects should exist for other economically interesting metabolites. It has not
been established which essential plant nutrient is more responsible for a particular metabolite
associated with a desirable feature of infected grasses. A complex interaction is probably
responsible for the reaction of infected grasses to any stressful situation.
The performance of infected grasses for any stress sparing mechanism should be measured
under severe environmental conditions. Most studies have measured the performance of infected
grasses under greenhouse conditions of constant temperature and moisture. Such ideal conditions
will never differentiate between survival values and other effects of the endophyte on grass
performance. Studies of infected grasses under severe environmental conditions can establish the
value of an endophyte for use in other forages. A word of caution concerning this theoretical
190
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approach is that The ecological success observed in naturally infected hosts may not be realized
in synthetically infected hosts. It may be simpler to select naturally infected grasses and improve
these for whatever desired character. Nevertheless, once identified, specific endophytes can be
isolated and studied as described above; the continued use of specific endophytes will establish
the utilitarian value of each endophyte for improved performance of nonhosts.
It is also important to use several cloned infected and noninfected grass material if at all
possible since studies of such material might indicate differences due to infection, and not to the
genetic makeup of different seed sowed seedlings. Studying cloned material should also identify
grasses with superior tolerances to severe environmental factors, and which when infected by
endophytes might produce an even better grass. Furthermore, it is important to study the
performance of a variety of clones, since the work of Arechavaleta et al. (13) suggested and Belesky
et al. (35) established that for each environmental factor, the behavior of each cloned will differ. The
important point to remember is that the fungus apparently influences or exaggerate the basic genetic
makeup of each grass.
CONCLUSIONS
The most important outgrowths of research devoted to etiologies of pasture grass toxicity (for
review see 17) was establishing that the nature of the relationship of a fungus and its grass hosts
was nonpathogenic, and that the fitness of infected grasses was improved. If indeed the fungus
only modifies the basic physiology of the grass, it implies that there is in the basic genetic makeup
of each grass species, a cultivar that is inherently superior without an endophyte.
Improved fitness observed in endophyte infected grasses indicates that ecologically we find
yet another example of a mutualistic symbiosis. The nature of the benefits are still circumstantial,
but then too so are many other mutualistic symbioses. The association of endophytes and grasses
fits Smith and Douglas's definition as an interceliullar mutualistic endosymbiosis (36). This is a
purely morphological definition and its use here reflects what is currently known with complete
certainty.
Research should continue into the use of endophytes as biological controls for pests and for
improved performance of grasses under stressful conditions. It is very seldom that such a biological
system presents itself that will confer both pest resistant and stress resistant mechanisms. The fact
that such a system is self-perpetuating, contained, and stable is all the more reason to use it. The
present information on the variety of natural pest deterrents produced within the association predicts
that there are obvious benefits derived from identifying the responsible agent, defining the nature
of any stress sparing mechanisms, and using these for control processes in other plants.
191
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REFERENCES
1. W. W. Deal. 1950. Balansia and Balansiae in America. Agriculture Monograph No. 4. U.S. Department of Agriculture.
U. S. Government Printing Office, Washington, DC, 82pp.
2. G. C. M. Latch, M. J. Christensen, and G. J. Samuels. 1984. Five endophytes of Lolium and Festuca in New Zealand
Mycotaxon 20: 535-550.
3. J. F. White and G. T. Cole. 1985. Endophyte-host associations un forage grasses. I. Distribution of fungal endophytes
in some Lolium and Festuca sp. Mycologia 77: 323-327.
4. D. M. Hinton and C. W. Bacon. 1985. The distribution and ultrastructure of the endophyte of toxic tall fescue. Can.
J. Bot. 63: 36-42.
5. M. R. Siegel, U. Jarlfors, G. M. C. Latch and M. C. Johnson. 1987. Ultrastructure of Acremonium coenophialum.
Acremonium lolii. and Epichloe typhina endophytes in host and nonhost Festuca and Lolium species of grasses.
Can. J. Bot. 65: 2357-2367.
6. M. R. Siegel, G. M. C. Latch and M. C. Johnson. 1987. Fungal endophyte of grasses. Ann. Rev. Phytopathology 25:
293-315.
7. C. W. Bacon and M. R. Siegel. 1988. Endophyte of tall fescue. J. Production Agric. 1: 45-55.
8. G. C. M. Latch, W. F. Hunt and D. R. Musgrave. 1985. Endophytic fungi affect growth of perennial ryegrass. N.Z. J.
Agric Res. 28:165-168.
9. J. C. Read and B. J. Camp. 1986. The effect of the fungal endophyte Acremonium coenophialum in tall fescue on
animal performance, toxicity and stand maintenance. Agron. J. 78: 884-850.
10. K. Clay. 1987. Effects of fungal endophytes on the seed and seedling biology of Lolium perenne and Festuca
arundinacea. Oecologia 73:358-362.
11. D. L. Gaynor and W. F. Hunt. 1983. The relationship between nitrogen supply, endophytic fungus and Argentine
stem weevil resistance in ryegrasses. Proc. N. Z. Grassland Assoc. 44: 257-263.
12. M. C. Johnson, D. L. Dahlman, M. R. Siegel, L. P. Bush, G. C. M. Latch, D. A. Potter, D. R. Varney. 1985. Insect
feeding deterrents in endophyte-infected tall fescue. Appl. Env. Microbiol. 49: 568-571.
13. D. D. Rowan and D. L. Gaynor. 1986. Isolation of feeding deterrents against Argentine stem weevil from ryegrass
infected with the endophyte Acremonium loliae. J. Chem. Ecol. 12: 647-658.
14. M. Arechavaleta, C. W. Bacon, C. S. Hoveland and D. E. Radcliffe. 1988. Effect of the tall fescue endophyte on
plant response to environmental stress. Agron. J. Accepted.
15. J. F. White and G. T. Cole. 1985. Endophyte-host association in forage grasses. III. In vitro inhibition of fungi by
Acremonium coenophialum. Mycologia 77:487-489.
16. G. M. C. Latch and M. J. Christensen. 1985. Artificial infection of grasses with endophytes. Ann. Appl Biol 107'
17-24.
17. C. W. Bacon, P. C. Lyons, J. K. Porter and J. D. Robbins. 1986. Ergot toxicity from endophyte infected grasses: a
review. Agra. J. 78:106-116.
18. K. Clay. 1986. Grass endophytes. Pp. 188-204 in: N. J. Fokkema J. van den Heuvel, eds., Microbiology of the
Phyllosphere. Cambridge University Press, London.
19. C. W. Bacon, J. K. Porter and J. D. Robbins. 1979. Laboratoryproduction of ergot alkaloids by species of Balansia
J. Gen. Microbiol. 113:119-126. '
20. N. D. Davis, E. M. Clark, K. A. Schrey and U. L. Diener. 1986. In vitro growth of Acremonium coenophialum. an
endophyte of toxic tall fescue grass. Appl. Environ. Microbiol. 52: 888-891.
21. R. K. Kulkarni and B. D. Nielsen. 1986. Nutritional requirements for growth of a fungus endophyte of tall fescue
grass. Mycologia 78: 781-786.
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22. C. W. Bacon. 1985. A chemically defined medium for the growth and synthesis of ergot alkaloids by species of
Balansia Mycologia 77:418-423.
23. J. K. Porter, C. W. Bacon and J. D. Robbins. 1979. Ergosine, ergosinine and chanoclavine I from Epichloe typhina.
J. Agric. Food Chem. 27:595-598.
24. P. C. Lyons, R. D. Planner, and C. W. Bacon. 1986. Occurrence of peptide and clavine ergot alkaloids in tall fescue.
Science 232: 487-489.
25. S. F. Yates, R. D. Plattner and G. B. Garner. 1985. Detection of ergopeptine alkaloids in endophyte infected toxic
tall fescue by mass spectrometry/ mass spectrometry. J. Agric. Food Chem. 33:719-721.
26. R. A. Prestidge, D. R. Lauren, S. G. van der Zijpp and M. E. Di Menna. 1985. Isolation of feeding deterrents to
Argentine stem weevil in cultures of endophytes of perennial ryegrass and tall fescue. N. Z. J. Agric. Res. 28:
87-92.
27. J. D. Bullock, R. W. Detroy, Z. Hostalek, and A. Munim-al-shakarchi. 1974. Regulation of secondary biosynthesis
in Gibberella fujikuroi. Trans. Br. Mycol. Soc. 62:377- 389.
28. J. Kybal, E. Kleinerova and V. Bulant. 1976. Ergot alkaloids.VI. Nitrogen metabolism during the development of
sclerotium of Claviceps purpurea. Folia Microb. 21:474-480.
29. S. G. Yates. 1983. Tall fescue toxins. Pp. 249-273 in: M. Recheigel, ed., Handbook of naturally occurring food
toxicants. CRC Press, Boca Raton, Fl.
30. G. B. Garner and C. N. Cornell. 1878. Fescue foot in cattle. Pp. 45-62 in: T. D. Wyllie and L G. Morehouse, eds.,
Mycotoxic Fungi, Mycotoxins, Mycotoxicoses, vol. 2. Marcel Dekker, Inc., N. Y.
31. W. M. Christopher and P. G. Mantle. 1987. Paxilline biosynthesis by Acremonium loliae: a step toward defining the
origin of lolitrem neurotoxins. Phytochemistry 26:969-971.
32. W. B. Turner. 1971. Fungal Metabolites. Academic Press, N. Y. 446 pp.
33. G. C. Marten, A. B. Simons and J. R. Frelich. 1974. Alkaloids of reed canary grass as influenced by nutrient supply.
Agro. J. 66:363-368.
34. G. R. Waller and E. K. Nowaki. 1978. Alkaloid Biology and Metabolism in Plants. Plenum Press, N. Y. 294pp.
35. D. P. Belesky, O. J. Devine, J. E. Pallas, Jr., and W. C. Stringer. I987. Photosynthetica 21: 82-87.
36. D. C. Smith and A. E. Douglas. 1987. the Biology of Symbiosis. Edward Arnold Publishers, London 302pp.
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TABLE 1
Choke inducing and nonchoke inducing grass endophytes cultured on media and which may
be useful for transferring to agronomically important grass species.
Endophytes* Grass Hosts**
Epichloe typhina Festuca rubra
E. typhina F. longifolia
E. typhina F. ligulata
E. typhina Lolium perenne
E. typhina Spenopholis obtusata
Acremonium coenophialum Festuca arundinacea
A. lolii L. perenne
Acremonium sp. F. versuta
'Most species of Epichloe are considered choke inducing when infecting their hosts (and see chapter by Funk, this book).
**Natural hosts.
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TABLE 2
Procedure for Isolating Grass Endophytes
A. GRASS TISSUE-ENDOPHYTE, 2.54 cm sections
B. STERILIZE, FULL-STRENGTH BLEACH, 5 min
C. RINSE, ASEPTICALLY CUT TISSUE INTO 0.5 cm SECTIONS
D. MACERATE TISSUE AND PLACE ON MEDIUM
E. INCUBATE UNTIL ENDOPHYTE DEVELOPS*
*The two basic endophytes, Acromonium typhinum and A., coenophialum. may be identified on
media following published descriptions(2).
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TABLE 3
Media Used to Isolate and Culture Endophytes
Isolation Agar
CMM
Malt extract
Yeast extract
Corn meal agar
Chloramphenicol
Distilled water
Medium,
10.0 g
1.0 g
17.0g
0.05 g
1000 ml
Isolation
Medium,
Sucrose
Malt extract
Peptone
Yeast extract
MgSO
KCI
KHPO
Liquid
M102
30.0 g
20.0 g
2.0 g
1.0 g
0.5 g
0.5 g
1.0 g
Chloramphenicol 0.05 g
Distilled water
1000 ml
pH adjusted to 6.0 with NaOH
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TABLE 4
Two stage fermentation procedure for choke inducing and nonchoke inducing fungal
endophytes of grasses.
Fescue Tissue-Fungus
Complex Medium, e.g. M102, and 4 wks Shake Culture, 24 C
Alkaloid Producing Medium:
Sorbrtol 50 o g
Glucose 10.0 g
Glutamic acid 10.0g
KH PO 0.5 g
MgSO 0.3 g
Yeast extract 1.0 g
Tryptophan 0.8 g
Distilled water 1000 ml
pH 5.6 adjusted with 10 N NaOH; incubate first as shake cultures at 24 C, then as stationary cultures (15-24 C) for 2 to
4 months.
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TABLE 5
Stability of Ergot Alkaloid Producing Strains of Tall Fescue Endophyte during Culture
Total Ergot Alkaloid (mg/l)*
Subculture
Strain Initial 5 10 15 25
347
338
351
357
524
214
18
0
487
517
20
0
382
114
0
0
400
93
0
0
390
1.5
0
0
'Values are means of four replicates
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TABLE 6
Major Classes of Secondary Metabolites Isolated from Toxic Grasses whose Endophyte
Infection Status were or were not Known at Time of Chemical Isolation.
Chemical Class*
Examples
Source
A. Indole derivatives
1. Simple indoles
"N'
H
Erythro-1 -(3-indolyl)propane-1,2,3-triol, 3-indole Species of Balansia
acetic acid, ethyl-3-indole carboxylate, indole ethanol,
w-indole acetamide (also see single amino acid
derivities)
2. Lysergic acid amides
12
Ergovaline, ergotamine, ergosine, ergosinine,
ergonovine, etc.
Balansia spp., endophytes
of tall fescue, perenial
ryegrass, and these infected
grasses
3. Prenylated indoles
Lolitrems A, B, C, and D, Paxilline
Perennial ryegrass
(lolitrem B)
*Chemical classes following the scheme of Turner (32).
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Chemical Class*
Examples
Source
B. Triterpens and Steriods
1/. C& Sterols
Ergosta-4,6,8(14),22-trien-3-one,
ergosta-4,6,8(14),22-tetraen-3-one,
ergosterol peroxide
Infected fescue and cultures
of A- coenophialum
C. Pyrrolizidlne alkaloids
N-formylloline, N-acetylloline, and demethyl-N-
acetylloline
Infected tall fescue
D. Amlno acid derivatives
1. Single amino acid
Harmane, perlolyrine, norharmane, Halostachine Tall fescue
(hannane)
2. Two amino acid derivatives
8 7
(1) R = H
(2) R = Ac
(peramine)
Peramine
A. lolii. A. coenophialum.
infected tall fescue and
perennial ryegrass
'Chemical classes following the scheme of Turner (32).
-------
Chemical Class*
Examples
Source
D. Amino acid derivatives (Continued)
3. Miscellaneous amino acid derivatives
perlolidine, perloline
Infected and noninfected
tall fescue and perennial
ryegrass.
OCH,
*Chemical classes following the scheme of Turner (32).
201
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202
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ROLE OF ENDOPHYTES IN ENHANCING THE
PERFORMANCE OF GRASSES
USED FOR CONSERVATION AND TURF
C. R. Funk, B. B. Clarke, and J. M. Johnson-Cicalese
New Jersey Agricultural Experiment Station
Rutgers University
New Brunswick, New Jersey 08903
Grasses used for turf and conservation are exceedingly important in our efforts to enhance
and beautify the environment, preserve and improve our precious soil resources, and provide
recreation and enjoyment for all people. Improved cultivars are currently being developed to produce
attractive, durable, and persistent turfs with reduced establishment and maintenance costs. Grasses
exhibiting increased stress tolerance, improved insect and disease resistance, reduced pesticide,
fertilizer, water, and mowing requirements, and better turf forming properties will also be of great
benefit. We also need grasses adapted to poor soils, shade, heavy wear, close mowing, and other
specialized uses and environments.
Turfgrass breeders have recently begun utilizing endophytic fungi (primarily Acremonium spp.)
in their efforts to develop grasses with improved insect resistance and increased stress tolerance.
In many instances, Acremonium endophytes living within the tissues of tall fescue (Festuca
arundinacea Schreb.), perennial ryegrass (Lolium perenne L), hard fescue (FL longifolia Thuill.)
Chewings fescue (F. rubra L. subsp. commutata Quad.), and perhaps many other grasses have
significantly modified host plant performance. Although plant scientists have been aware of the
presence of endophytes in many grasses for over 100 years, endophytes received very little
attention until recently when a number of sign iicant discoveries were made. These included: (1)
instances of poor performance when animals g< azed on endophyte-infected perennial ryegrass and
tall fescue, (2) reports of insect resistance in many endophyte-containing grasses, and (3)
suggestions of improved growth, summer survival, and stress tolerance of grasses containing
endophytes.
Animal health problems associated with endophyte-produced toxins have prompted programs
to eliminate the fungus from new cultivars and seed lots of tall fescue, an important pasture grass.
On the other hand, dramatic instances of improved insect resistance, persistence and performance
have been observed in endophyte-containing plants. Thus, the Acremonium endophyte is generally
considered to be a desirable attribute in grasses grown for turf and conservation.
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INSECT RESISTANCE
New Zealand scientists (Prestidge et al., 1982) were the first to report that an endophytic
fungus, Acremonium lolii Latch, Christensen, and Samuels, was associated with resistance to the
Argentine stem weevil, Listronotus (= Hyperodes) bonahensis Kuschel in perennial ryegrass.
Several toxins have since been associated with the presence of endophytes and are believed to
be responsible for the enhanced insect resistance (Bacon et aL (Chapter 17). Larvae of the
Argentine stem weevil, a small billbug-like insect, can cause extensive damage to perennial ryegrass
and many other grasses used for pasture, turf and conservation in New Zealand and several other
countries of the southern hemisphere (Stewart, 1986 and 1987). Larval damage is especially severe
during hot, dry summer months resulting in extensive tiller loss, apparent drought stress, and slow
fall recovery. In fact, endophyte-free plants seldom persist in old pastures and turfs in many parts
of New Zealand because they are crowded-out and replaced by perennial ryegrass plants containing
the Acremonium endophyte.
Although adult Argentine stem weevils cause only minor damage to established grasses, they
can inflict severe damage during the seedling establishment stage. Again, the Acremonium
endophyte confers a high level of resistance. Interestingly, even old ryegrass seeds containing
nonviable endophyte, produce seedlings resistant to stem weevil feeding for a few days following
germination and emergence (Stewart, 1985).
Resistance of perennial ryegrass to lepidopterous sod webworms has also been associated
with the presence of the Acremonium endophyte. This important insect pest damages many turf
and conservation grasses, especially in regions with warmer summers. The larvae spend the
daylight hours protected in silken underground tunnels. During the night they feed extensively on
grass leaves, primarily during late summer and early autumn. In a New Jersey trial (Funk et al,
1983), perennial ryegrasses rated as highly resistant to sod webworms were shown, through
microscopic examination and enzyme-linked immunosorbant assay (ELISA), to contain a very high
percentage of endophyte-infected plants. Ryegrasses exhibiting substantial injury from larval
feeding, however, were free or mostly free of the endophyte. Field resistance to sod webworms
was expressed both as a 10-fold reduction in larval feeding and a nearly complete absence of larvae
from the soil beneath endophyte-containing plants. The maternal transmission of sod webworm
resistance was very striking in that single-plant progenies descending from the same mother line
were either all resistant or all susceptible. Maternal transmission of endophyte-mediated pest
resistance occurs because almost all seed produced from an endophyte-infected plant contains the
endophyte. We have not observed any evidence of pollen transfer. The role of endophytes in
conferring resistance to various species of sod webworm in other grasses needs further study.
Billbugs (Sphenophorus spp.) can seriously damage many grasses used for turf and
conservation, especially under conditions of drought stress during mid-summer. Adult billbugs, like
the Argentine stem weevil, lay their eggs in the base of grass tillers during early summer. Upon
hatching, the young larvae feed within the tiller and later upon adjacent plants immediately below
the soil surface. Subsequently, wilted or dead grass tillers can be easily pulled from the soil exposing
insect frass and feeding injury at the base of each tiller. Billbug injury, while easy to diagnose, is
frequently mistaken for summer drought or disease injury. Moreover the more open turf and
subsequent warmer, drier microclimate created by billbug damage makes conditions very favorable
for additional damage by chinch bugs (Blissus leucopterus hirtus Montandon). Endophyte-enhanced
resistance to billbugs has been observed in a number of perennial ryegrass field trials in New Jersey
(Ahmad et al., 1986). Resistance to billbugs in these trials was primarily associated with the
presence of the Acremonium endophyte. However, evidence of a limited level of genetic resistance
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was apparent in selected ryegrasses. As a result, optimum billbug resistance would seem to require
at least a moderate level of genetic-mediated resistance enhanced by an effective endophyte.
Endophyte-enhanced resistance to chinch bugs has been observed in New Jersey turf trials
of perennial ryegrass, hard fescue, and Chewings fescue (Funk et al., 1985; Saha et al., 1987). At
least two factors appear to be involved; (1) an intrinsic resistance to the chinch bug enhanced by
various Acremonium endophytes, and (2) a less favorable environment for chinch bug development
resulting from a healthier denser turf. This second factor may either be the result of
endophyte-enhanced stress tolerance or from less damage caused by billbugs and other insects
in high endophyte turfs.
STRESS TOLERANCE
Funk et al. (1985) reported striking differences in persistence, recovery from summer stress,
and ability to resist weed invasion during the early fall of 1983 in perennial ryegrass and tall fescue
turf trials conducted in North Brunswick, New Jersey. These tests, seeded in 1976, were irrigated
and maintained at moderately high fertility with frequent close mowing (2-cm) until June 1981. At
that time, the mowing height was raised to 5-cm, irrigation and weed control treatments were
discontinued, and fertility applications drastically reduced. A substantial amount of crabgrass
(Digitaria spp.) invaded the test by midsummer 1982 and produced an almost complete ground
cover on the ryegrass trial. The tall fescue test also sustained moderate crabgrass invasion during
this period.
By 1983, most perennial ryegrass entries exhibited 95 to 100 percent turf loss and were almost
completely replaced by crabgrass and other weeds. However, several entries persisted with over
90 percent ryegrass turf cover. Indications of maternal inheritance of this dramatically improved
persistence and resistance to weed invasion suggested that turfgrass endophytes were involved.
It was later confirmed, through laboratory analysis, that 98 percent of all ryegrass tillers sampled
from surviving plots contained the Acremonium endophyte. Unfortunately, remnant seed from this
test had been discarded making it impossible to assess endophyte levels in the ryegrasses that
failed to survive. However, since all 15 surviving ryegrasses were highly infected with endophyte,
it seems unlikely that progenies free of endophyte could have survived. On the other hand, it is
possible that some progenies with endophyte did not survive.
Optimum performance may well require a combination of non-endophytic sources of pest
resistance and/or stress tolerance enhanced by an effective endophyte. It would seem likely that
endophytes vary as much as other biological organisms in their ability to enhance pest resistance,
stress tolerance, and plant persistence. Good performance may also require a high frequency of
endophyte-infected plants within a cultivar.
Endophyte-enhanced performance was also strikingly apparent in the adjacent trial of tall
fescue cultivars and single plant progenies(Funk et al., 1985). The 32 single-plant progenies that
had the best performance contained an average of 98 percent infected tillers. Progenies exhibiting
poor fall recovery and extensive weed invasion contained an average of only eight percent
endophyte-infected tillers. This strongly suggests that the dramatic differences in persistence,
resistance to crabgrass invasion, and recovery from summer stress of the tall fescues were
associated with the presence of an Acremonium endophyte.
Enhanced resistance to sod webworms, billbugs and perhaps other insect pests was
undoubtedly a contributing factor in the survival of the endophyte-containing perennial ryegrasses
in this test. In another turf trial at Adelphia, NJ, many of the endophyte-free turf-type ryegrasses
205
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were able to completely recover from prolonged defoliation by sod webworms. However, in this trial
crabgrass was not present. The severe crabgrass competition at North Brunswick undoubtedly
reduced the recovery of plants weakened by insects and environmental stress. It is likely that
endophytes did more than just enhance insect resistance to produce the observed response. Insect
populations and apparent insect damage did not appear sufficient to account for the great
differences observed. Either the insects escaped our attention, or the improved performance and
persistence of endophyte-infected ryegrasses and tall fescues were associated with physiological
factors related to improved stress tolerance and competitive ability.
It has been our experience that endophytes appear to have little if any effect on turf
performance when conditions are favorable. The endophyte-free ryegrasses Tara' and 'Gator1 have
performed well in a four year national testing program and have an excellent reputation in the
turfgrass industry. Observations of endophyte-enhanced performance have normally occurred
under conditions of severe stress or attacks by some, but not all, insect pests. Thus turfgrass
endophytes may be similar to insurance, of little value when everything is favorable but of great
value under certain conditions of biological and/or environmental stress. It also appears that the
favorable effects of endophytes occur more frequently and are more significant in perennial ryegrass
than in tall fescue, at least under field conditions in New Jersey.
Field studies near Dallas, Texas (Read and Camp, 1986) demonstrated that endophyte-
enhanced performance is common in tall fescue pastures growing ir+^an area with significantly
higher summer temperatures than in most other areas of tall fescue usage. Endophyte-free tall
fescue pastures and lawns have generally performed well in limited short term studies in New
Jersey, Kentucky and Alabama. Although tall fescue is noted for its good overall insect resistance,
deep root system and good heat and drought tolerance, there is some concern that the increased
use of endophyte-free cultivars may result in greater pest problems. Moreover, previously
unimportant insect and nematode species may be able to increase and thrive on endophyte-free
grass. Loss of stress tolerance and persistence could also occur in especially stressful environments
and in long-term plantings.
Fortunately, a number of stress physiologists, ecologists, botanists, and agronomists are now
studying the role of endophytes in grasses of economic importance. Controlled studies have
demonstrated that Acremonium endophytes in perennial ryegrass and tall fescue can increase plant
yield and vigor (Clay, 1987; Latch et al., 1985), enhance root growth (Ellis, 1987), and modify water
relations (Ellis, 1987; White and Comeau, 1987). However, this situation is very complex and is not
fully understood at present. Interactions between host plant genotype, biotype of the endophytic
fungus, plant nutrition, drought stress, and temperature are commonly detected in these studies.
The possible role of endophytic fungi in enhancing disease resistance also needs to be studied.
Research has shown that many biotypes of Acremonium endophytes isolated from tall fescue and
perennial ryegrass will inhibit the growth of a number of plant disease-inducing fungi in vitro(White
and Cole, 1985; Bayaa et al., 1987). However, this has yet to be demonstrated in the field.
DEVELOPING TURFGRASS CULTIVARS WITH ENDOPHYTE- ENHANCED
PERFORMANCE
Turfgrass breeders are currently using traditional plant breeding procedures including
backcrossing, recurrent selection, and other population improvement methods to incorporate
desirable endophytes into existing cultivars and elite breeding populations. This germ plasm is being
used to develop new cultivars with both endophyte-enhanced performance and genetic
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improvements in turf quality, pest resistance and stress tolerance. Increased knowledge of turfgrass
endophytes is making breeding and evaluation programs much more efficient.
Large amounts of time and money were wasted in past breeding and evaluation programs as
efforts made to improve and evaluate animal performance, pest resistance, and stress tolerance
were confounded by the unrecognized effects of endophytic fungi. As a result, our most efficient
approach to long-term cultivar development may well be to (1) remove endophytes from existing
breeding populations, (2) select for genetic improvements in insect resistance, stress tolerance,
etc., and (3) then incorporate the best available endophyte to enhance performance wherever
appropriate. Concurrent with the plant breeding efforts, biologists should identify and/or develop
endophytes tailored to specific host populations and uses. Recent and anticipated advances in
molecular genetics may prove to be useful in endophyte selection and improvement programs.
Perennial Ryegrass
Tremendous progress has been made in the genetic improvement of perennial ryegrass for
turf usage during the past quarter century. Each cycle of breeding has resulted in a stream of new
cultivars with better stress tolerance, increased resistance to many of the most important diseases,
a lower growth profile, and a more attractive appearance. Useful Acremonium endophytes are
currently being incorporated into an increasing percentage of new perennial ryegrass releases. An
estimated 10 million pounds of turf-type perennial ryegrass seed containing a high percentage of
endophyte was harvested in 1987. Perennial ryegrass cultivars containing at least 70 percent
Acremonium endophytes in some seed lots include: 'Regal', 'Pennant', 'Airstar', 'Repell', 'Omega
II', 'Citation II', 'Dasher II', 'Sunrye 246', 'SR-4000', and 'SR-4100'. Additional perennial ryegrasses
with high endophyte levels will be available after the 1988 seed harvest. They will include 'Pinnacle',
'Commander', 'Sherwood', and 'Dandy'.
Turfgrass managers desiring the benefits of endophyte-enhanced performance must be careful
in their selection of seed. Endophyte viability declines during seed storage, especially under hot,
humid conditions. Therefore, seed harvested in June or July should maintain a high level of viable
endophyte as long as it is stored under cool dry conditions and used before or during the following
spring. At present, seedlings produced from a grow-out test must be examined to determine the
viability of the endophyte. This can be done through either microscopic examination of properly
stained plant tissues or by an ELISA test conducted by a well-trained laboratory technician. A
number of states are currently offering this service. A dated seed label showing percent viable
endophyte would also be useful.
It is also important to recognize that different seed lots of the same cultivar may vary in initial
endophyte concentrations. For example, in a few of the older cultivars some seed production fields
were established with old seed containing non-viable endophyte. When this occurred the benefits
of endophyte-enhanced performance were lost.
Normal fungicide applications made to established turfs usually have little or no effect in
reducing the level of endophyte.
Hard Fescues
Hard fescues are receiving increased attention in the turfgrass industry. Improved cultivars of
this valuable species can produce a dense, disease resistant, attractive and fine-textured turf on
poor soils with little or no supplemental fertilization or irrigation. The greatest weakness of hard
fescues, however, may be their slow recovery from excessive wear or insect damage. Acremonium
endophytes have been identified which enhance both summer performance and resistance to chinch
bugs (Saha et al., 1987). Turfgrass breeders are currently utilizing these useful endophytes in their
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cultivar improvement programs. To date commercial seed production has been initiated on
'SR-3000', a hard fescue with a high level of endophyte.
Chewings Fescues
Turfgrass breeders in Europe and the United States have developed a number of attractive
turf-type cultivars of Chewings fescue. They are especially useful for medium-to-low maintenance
turfs, in moderate shade and in regions with cool summer climates. Useful Acremonium endophytes
have been identified in Chewings fescue which can enhance summer stress tolerance and increase
resistance to chinch bugs (Saha et al., 1987). Turfgrass breeding programs at Seed Research of
Oregon, Pure-Seed Testing, Pickseed West, E. F. Burlingham, Rutgers University and the University
of Rhode Island are attempting to develop improved cultivars of Chewings fescue with high levels
of useful endophytes.
Other Fine Fescues
Acremonium-type endophytes have been discovered in strong creeping red fescue (E. rubra
L. subsp. rubra). blue fescues (FL glauca Lam.), and sheeps fescue (R ovina L) (Saha et al.,
1987). Studies are currently underway to assess their usefulness in enhancing insect resistance
and turfgrass performance. Current sources of endophyte in strong creeping red fescue have failed
to produce peramine, a toxin shown to be responsible for insect resistance, and have reacted
negatively (less than or equal to 10% dead) to an aphid bioassay test (Siegel et sL Chapter 16).
Acremonium endophytes in perennial ryegrass, Chewings fescue and hard fescue, however, have
been shown to produce this compound and have given positive results on the aphid bioassay.
Breeders are currently looking for endophytes in strong creeping red fescue that will produce
peramine and thus enhance insect resistance. It would also be of interest to determine whether
non-peramine producing endophytes have other mechanisms that might enhance resistance to
insects and stimulate turfgrass performance.
Tall Fescue
Tall fescue has been widely used for pasture, conservation and turf purposes during the past
four decades, with Kentucky 31 the primary cultivar grown. Significant genetic improvements in
color, texture, and disease resistance during this time led to the development of many improved
turf-type tall fescues. These cultivars are rapidly increasing in popularity in many parts of the United
States and southern Europe. Many, including 'Adventure', 'Apache', 'Mustang', and 'Rebel II', have
characteristics that could also make them very useful pasture grasses in various regions. However,
only seed lots completely free of viable endophyte should be used for forage establishment in order
to avoid livestock toxicoses.
Selected Acremonium endophytes would undoubtedly be useful in enhancing turf performance,
insect resistance and stress tolerance of turf-type tall fescues, especially in highly stressful
environments and low maintenance turfs. However, to date, seed companies and plant breeders
have been somewhat reluctant to develop tall fescue cultivars with high levels of endophyte since
there is always the possibility that they might be used for pasture establishment. This is especially
likely to occur with poorer quality seed that fails to meet certification standards. Therefore, until
appropriate seed labeling and educational programs are in place, breeding for high endophyte-
containing turf-type tall fescues is likely to be delayed. Current progress in developing
lower-growing, "dwarf-type"tall fescues may encourage breeders to incorporate useful endophytes
since such premium turfgrasses would be less likely to be used for non-turf purposes.
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Kentucky Bluegrass
Kentucky bluegrass (Poa pratensis L.) is often considered the Cadillac of lawn grasses in
temperate climates of North America. It is hardy, attractive and widely adapted. The development
of lower-growing, turf-type cultivars with good resistance to the Helminthosporium leaf spot and
melting-out disease has made Kentucky bluegrass even more useful as a turfgrass in humid regions.
Moderate levels of genetic resistance to billbugs, sod webworms, greenbug aphids (Schizaphis
graminum Rondani) and chinch bugs have been identified in Kentucky bluegrass.
Endophyte enhancement of this genetic insect resistance would be very useful; however,
attempts to find a non-choke-inducing endophyte in Kentucky bluegrass have been unsuccessful
to date. Likewise, there are no reports of a successful inoculation of an Acremonium endophyte
from other genera of grasses into this valuable turfgrass species. Even if inoculation were
accomplished, it is questionable whether the intergeneric transfer of an endophyte would be
successful in enhancing insect resistance and stress tolerance. Endophyte-host interactions are
likely to be very specific as a result of a long period of coevolution into a mutually beneficial
relationship (Clay, 1988). If this is the situation, then additional efforts should be made to find useful
endophytes in Kentucky bluegrass and other closely related species of Poa. Successful inoculation
of such endophytes into leading cultivars of Kentucky bluegrass may well prove to be very beneficial.
Because of apomictic reproduction and high levels of heterozygosity present in all elite cultivars of
Kentucky bluegrass, inoculation techniques will be of greater immediate value than the transfer of
endophytes through hybridization techniques.
Most elite Kentucky bluegrass cultivars originated as the progeny of a single, highly apomictic
plant. This results in essentially all plants of a given cultivar being genetically identical to each other
as well as to the original parental plant. Successful inoculation of only one plant would, therefore,
be sufficient to incorporate a useful endophyte into such a Kentucky bluegrass cultivar. Because
of the highly heterozygous genotype in Kentucky bluegrasses, the backcross technique cannot be
used to transfer endophytes or genetic characters into a given cultivar. Hybridization and a modified
backcross technique could be used, however, to generate highly heterogeneous and highly
heterozygous populations of Kentucky bluegrasses containing useful endophytes. Elite, new and
unique, and highly apomictic cultivars containing useful endophytes could eventually be selected
from such populations.
Endophytes in Other Grasses
Endophytes are also being discovered in many other grasses used for turf and conservation.
White (1987) examined over 800 herbarium specimens in 93 genera of grasses and found
endophytic fungi present in 43 grass species in the following 11 genera: Agrostis. Bromus. Cinna.
Elymus. Festuca. Lolium. Melica. Poa. Sitanion and Stipa. These grasses were collected from Africa,
Argentina, Canada, Europe, India, Mexico, New Zealand and the United States. Many of the
endophyte-containing grasses examined were species "native"to the continental United States.
Additional work is needed on the possible significance of endophytes in these other grass species.
In conclusion, utilizing endophytes to enhance the performance, insect resistance and stress
tolerance of turf and conservation grasses has considerable potential, and is highly compatible with
goals for reduced pesticide usage. Moreover, an increasing awareness of the role of endophytes
is making cultivar evaluation and genetic improvement programs much more efficient. As our
knowledge of endophytic fungi expands, including a better understanding of their genetic diversity
and how they interact with both plants and the environment, they will become even more useful to
the turfgrass breeder and ultimately to all who enjoy and benefit from improved grasses.
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REFERENCES
1. R. A. Prestidge, R. P. Pottinger, and G. M. Barker. 1982. An association of Lolium endophyte with ryegrass resistance
to Argentine stem weevil. Proc. N.Z. Weed and Pest Control Conf. 35:119-122.
2. C. W. Bacon. 1988. (Chapter 17).
3. A. V. Stewart. 1986. The effect of endophyte on perennial ryegrass turf performance. Rutgers Turfgrass Proceedings
I7:I20-I26.
4. A. V. Stewart. 1987. Plant breeding aspects of ryegrasses (Lolium spp.) infected with endophytic fungi. Ph.D.
dissertation, Lincoln College, Univ. College of Agric., Canterbury, N. Z.
5. A. V. Stewart. 1985. Perennial ryegrass seedling resistance to Argentine stem weevil. N.Z. J. of Agric. Res.
28:403-407.
6. C. R. Funk, P. M. Halisky, M. C. Johnson, M. R. Siegel, A. V. Stewart, S. Ahmad, R. H. Hurley, and I. C. Harvey.
1983. An endophytic fungus and resistance to sod webworms: Association in Lolium perenne L Bio/Technology
1:189-191.
7. S. Ahmad, J. M. Johnson-Cicalese, W. K. Dickson, and C. R. Funk. 1986. Endophyte-enhanced resistance in
perennial ryegrass to the bluegrass billbug Sphenophorus parvulus. Entomol. Exp. Appl. 41:3-10.
8. C. R. Funk, P.M. Halisky, S. Ahmad, and R. H. Hurley. 1985. How endophytes modify turfgrass performance and
response to insect pests in turfgrass breeding and evaluation trials, p. I37-I45 in: F. Lemaire, ed., Proc. 5th Int.
Turf Res. Conf., Avignon, France.
9. D. C. Saha, J. M. Johnson-Cicalese, P. M. Halisky, M. I. Van Heemstra, and C. R. Funk. 1987. Occurrence and
significance of endophytic fungi in the fine fescues. Plant Disease 71:1021-1024.
10. J. C. Read, and B. J. Camp. 1986. The effect of the fungal endophyte Acremonium coenophialum in tall fescue
on animal performance, toxicrty, and stand maintenance. Agron. J. 78:848-50.
11. K. Clay. 1987. Effects of fungal endophytes on the seed and seedling biology of Lolium perenne and Festuca
arundinacea. Oecologia 73:358-362.
12. G. C. M. Latch, W. F. Hunt, and D. R. Musgrave. 1985. Endophytic fungi affect growth of perennial ryegrass. N. Z.
J. Agric. Res. 28:165-68.
13. D. Ellis. 1987. Effect of Acremonium lolii infection on water relations in perennial ryegrass. Masters Thesis, Rutgers
Univ., New Brunswick, NJ. 173 pp.
14. R. H. White and M. Comeau. 1987. Tall fescue leaf gas exchange and water relations as influenced by endophytic
fungi. Agronomy Abstracts, p. 140.
15. J. F. White, Jr. and G. T. Cole. 1985. Endophyte- host associations in forage grasses. III. in vitro inhibition of fungi
by Acremonium coenophialum. Mycologia 77:487-489.
16. B. O. Bayaa, P. M. Halisky and J. F. White, Jr. 1987. Inhibitory interactions between Acremonium spp. and the
mycoflora from seeds of Festuca and Lolium. Phytopath. 77:II5.
17. M. R. Siegel. 1988. (Chapter 16).
18. K. Clay. 1988. Fungal endophytes of grasses: A defensive mutualism between plants and fungi. Ecology
69:(1):10-I6.
19. J. F. White, Jr. 1987. Biological and taxonomic studies on Acremonium section Albo-Lanosa. Ph. D. dissertation,
Univ. of Texas, Austin.
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SECTION V
State of the Art Research on
Use of Entomophilic Nematodes
for Control of Turfgrass Insects
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FIELD EFFECTIVENESS OF
ENTOMOPHILIC NEMATODES
NEOAPLECTANA AND
HETERORHABDITIS
Ramon Georgls
Blosys
1057 East Meadow Circle
Palo Alto, CA 94303
and
George O. Poinar, Jr.
Department of Entomological Sciences
University of California
Berkeley, CA 94720
INTRODUCTION
High levels of pest resistance to conventional pesticides together with growing public concern
about potential health and environmental hazards associated with chemical pesticides, are forcing
the industry and public to seek less toxic pest management methods. Entomophilic nematodes of
the genera Neoaplectana (=Steinernema) (Family: Steinernematidae) and Heterorhabditis (Family:
Heterorhabditidae) are regarded as having excellent potential as biological control agents (Kaya
19S5, Poinar 1986). The broad host range and high virulence of these nematodes make them
attractive candidates for industrial development. Extensive testing has demonstrated a lack of
mammalian pathogenicity, and the U.S. Environmental Protection Agency has subsequently
exempted these nematodes and their associated bacteria Xenorhabdus from registration and
regulation requirements. There are a number of described species of Neoaplectana and
Heterorhabditis (Poinar 1979, 1986, 1987), however, to date, most studies have been conducted
with WL carpocapsae (SL feltiae) and K heliothidis.
BIOLOGY
The ensheathed third-stage juvenile of R carpocapsae and it heliothidis (approximately 500u
long and 20u wide) is the invasive form which locates new hosts, initiates infection and is the only
stage in the nematode's life cycle that occurs outside the host in the soil. Besides persisting in the
soil environment without taking in nourishment, the infective stage searches for insect hosts using
sensory organs that are capable of detecting insect excretory products, temperature gradients and
carbon dioxide (See Kaya 1985). These/ nematodes are characterized by their mutualistic
association with bacteria in the genus Xenorhabdus (Poinar 1979, 1986). The infective juveniles
enter the hosts via natural body openings (mouth/' anus or spiracles), exsheath and penetrate
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mechanically into the hemocoel (Poinar 1979). Heterorhabditids can also enter directly through the
host's cuticle (Bedding & Molyneux 1982). The infectives liberate the bacteria causing septicemic
death of the host 24-48 hours later. The nematodes feed on the multiplying bacteria and the dead
host tissues, passing through several generations in which their numbers increase tremendously.
Eventually, ensheathed infectives, carrying the mutualistic bacteria in their gut, emerge from the
depleted insect cadaver. Depending on the temperature the complete life cycle in most insects takes
10-20 days.
FIELD EFFICACY
Above-ground applications: In general, attempts to control foliar insects with JSL carpocapsae
have been discouraging, with low host mortality, insignificant population reduction, or inadequate
crop protection (Kaya 1985). Poor control has been attributed to the failure of the nematodes to
survive drying of the spray deposit. Recent developments in inducing infective nematodes to enter
anhydrobiosis (Table 4) may increase the survival of nematodes and subsequently achieve
successful control (Georgis 1987, Ishibashi et al 1987b, Wojcik & Georgis 1987). Other factors
limiting the use of nematodes on foliage are solar radiation (Gaugler & Boush 1978) and temperature
extremes (Schmiege 1963). The most successful use of nematodes has been against insects which
spend part of their life cycle in protected habitats avoiding harsh environmental exposure. Insects
such as wood borers in the family Sesiidae (Deseo 1986), the artichoke plume moth, Piatyptilia
carduidactyla (Bari & Kaya 1984), and beet armyworm, Spodoptera exigua in chrysanthemum
production beds (Begley 1987), were successfully controlled with these nematodes.
Soil applications: Soil inhabiting insects are a logical target for control by these nematodes.
The nematode naturally occurs in moist cryptic environments, especially soil. In the soil they have
advantages over pesticides and microbial pathogens by virtue of their attraction and mobility towards
an insect host. Field applications of hL carpocapsae and HL heliothidis with conventional sprayers
frequently have shown that infective nematodes possess high efficacy for controlling a wide range
of insects that affect man, such as imported fire ants (Poole 1976; Quattlebaum 1980), turfgrass
(Table 1), vegetables (Table 2), ornamentals, shrubs, flowers and caneberries (Table 3). In many
situations, the efficacy of the nematodes will depend on their persistence in the soil. Nematodes
introduced into the soil are capable of remaining infective for weeks or even months (Harlan et al
1971, Miller 1987, Georgis & Hague 1988), more than sufficient time to find a host and cause
mortality; but in some situations persistence may be adversely affected by lack of moisture, extreme
temperatures, soil texture and natural enemies (Molyneux & Bedding 1984, Ishibashi & Kondo 1987,
Ishibashi et al 1987a). Infectivity of nematodes is mostly influenced by soil texture (Georgis & Poinar
1983a, Molyneux & Bedding 1984), temperature (Molyneux 1984, Simons & Van der Schaaf 1986),
and moisture (Molyneux & Bedding 1984, Kondo & Ishibashi 1985). Differences in field efficacy
exist between neoaplectanid and heterorhabditid nematodes and their various species and strains
(Tables 1, 3). For example, heterorhabditids are highly effective against Japanese beetles and
billbugs (Table 1), but provide extremely poor results when mole crickets are challenged. In contrast,
J^L carpocapsae are effective against mole crickets but provide only modest control of Japanese
beetles. Differences in field efficacy in part may be related to the vertical distribution of the
nematodes in the soil after application. N. carpocapsae seem to show a preference for soil near the
surface (Moyle & Kaya 1981, Georgis & Poinar 1983a), and therefore may be best adapted to attack
insects like mole crickets and cutworms which feed at the soil litter interface or on the soil surface.
Heterorhabditids have a greater tendency to move downwards (Georgis & Poinar 1983b) and has
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superior host seeking abilities (Gaugler & Campbell, in press), making them efficacious against
Japanese beetles, billbugs and root weevils which are present at the root zones of their host plants.
APPLICATION CONSIDERATIONS
For successful application of nematodes, the following steps should be taken into
consideration:
1. Nematodes should be applied to moist soil. Pre and post-application irrigation and moderate
soil moisture are essential for the movement and persistence of these nematodes. According
to Poinar (1986), most nematodes applied to dry soil will perish; however, if they are applied
to damp soil which later becomes dry, many will survive for some period because of their ability
to withstand gradual desiccation. Field applications of nematodes to dry turf with 0.64 cm
pre-treatment irrigation followed by 0.64 cm post-treatment irrigation with normal rainfall
resulted in Japanese beetle grub control comparable to a standard insecticide (Shetlar 1987).
Non-irrigated turf showed less control. Nematodes are less effective in soils close to the
saturation point (very wet) (Molyneux & Bedding 1984).
2. Soil temperature between 18-309C is adequate for nematode survival, movement and host
infection. Temperatures above 30QC and below 18gC (Tables 1, 3) may reduce nematode
effectiveness (Schmiege 1963, Molyneux 1984). For effective field control at temperatures
below 18QC, cold-active strains of N. carpocapsae such as the Umea strain (Pye 1987) or the
HL81 isolate of Heterorhabditis sp (Simons & Van der Schaaf 1986) are required.
3. To avoid the effects of solar radiation (Gaugler & Boush 1979) and temperature extremes
(Schmiege 1963), application in the early morning or early evening is recommended.
4. Concentrations exceeding 2.5 billion nematodes/hectare (1 billion/acre) are needed to ensure
that a sufficient population will come into contact with the insect to provide consistent pest
control. A high concentration is needed to overcome the impact of soil environment, pathogens,
predators and other factors that can form an ecological barrier to nematode effectiveness. High
concentrations are required against certain insects such as root maggots which only remain
for a few days in the soil before tunneling in roots (Table 2) or those which are not highly
susceptible to nematode infection (Tables 2, 3) because of their small size (i.e., early immature
stages of mole crickets, root maggots and root weevils).
5. The spray volume needed depends upon characteristics of the turfgrass or soil being treated.
In order to penetrate the deeper thatch (thatch is a tightly bound layer of dead and living roots
and stems that accumulates between the soil surface and green vegetation in turfgrass), or
denser turfgrass a high spray volume may be needed to incorporate nematodes to the depth
frequented by the target insect. Under these conditions, 4 to 5 gailons/1,000 ft2 (0.2 liters/m2)
is usually acceptable. It is well known that both moisture and pore size influence the movement
of soil nematodes (Wallace, 1963). A nematode cannot move between soil particles when the
pore diameter is less than the width of the nematode. Although Mi carpocapsae can migrate
through clay soil, movement will be much less than in sand and sandy loam (Georgis & Poinar
1983a). In most field tests, 150 gallons/acre (230 liters/hectare) appears to be adequate, but
research is needed to determine the proper spray volume in relation to the soil type and insect
activity at the application site.
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6. When nematodes are applied against root-feeding insects such as white grubs, mole crickets,
billbugs, and root weevils, it may take 10-30 days before the insect population is significantly
reduced (Shetlar 1987, Cobb & Georgis, in press); but against lepidopterous larvae such as
cutworms and sod webworms, which can be found on or close to the soil or turf surface, control
can be achieve 2-5 days after treatment (Lossbroek & Theuissen 1985, Shetlar 1987).
7. More than one application of nematodes may be required for acceptable control when soil
environments are not adequate for nematode persistence. Repeat applications may be needed
against insects that feed over a two-month period (i.e., root weevils and mole crickets), and
against insects with more than one generation/year (i.e., root maggots).
8. Nematodes can often be applied with the same equipment used for the application of
conventional pesticides. Neoaplectanids can withstand application pressures up to 300 psi.
Accordingly, nematodes have been applied with small pressurized sprayers, mist blowers,
electrostatic sprayers and helicopters (Kaya, 1985). The infective stages are resistant to shear
but cannot easily pass through a screen with openings less than 50u in diameter. Also, some
pumping equipment produces a considerable amount of heat, and should the temperature rise
above 32QC, the nematodes could be damaged (Poinar 1986).
APPLICATION METHODOLOGY
As with chemical insecticides, soil surface spraying of nematodes is the method most often
used in response to insect attack. The broadcast approach is quick, easy, and gives good coverage,
but in most cases high concentrations are needed to ensure that sufficient numbers of nematodes
will come close to the active site of the insect. In some situations nematodes were found to have
potential when applied at planting time (Georgis et al 1983, Pye & Pye 1986, Bari unpublished);
but in certain soil environments that require nematode persistence 4-6 weeks before the appearance
of the target insect stage, (i.e., corn rootworm, Diabrotica spp and crucifer flea beetle, Phyllotreta
crucjferae), insect damage was not prevented (Munson & Helms 1970, Morris 1987), probably due
to inadequate soil moisture and the non-susceptible nature of some early larval stages. Other
methods of delivering nematodes to the soil are by means of injection (Glaser, & Farrell 1935), baits
(Georgis et al. 1989) and alginate capsules (Kaya & Nelson, 1985). Practical implementation of
these techniques will require further investigation. It is expected that these application strategies
will require fewer nematodes for effective control and will provide better protection for nematodes
from extreme environments. Nematodes may also be applied by drip irrigation (Reed et al 1986),
and overhead sprinkler systems (Kaya 1985). Further research may establish these techniques as
practical for nematode applications. Against wood-boring insects, neoaplectanids and heterorhabditids
have been delivered into galleries with a syringe, cotton swab plug, oil can, and back pack sprayer
(Deseo 1986). Application of nematodes to nylon pack cloth bands lined with pellon fleece or terry
cloth and placed around tree trunks are control tactics used for the control of late stage gypsy moth
larvae Lymantria dispar (Reardon et al 1986), or for overwintering codling moth prepupae Cydia
pomonella (Kaya et al 1984). Such tactics may be useful if nematodes are to be used in concert
with other control measures. Preliminary investigations have suggested that certain formulations
provide an efficient delivery system, and these results should provide an impetus to attempt control
programs against insects that were previously thought to be difficult or impractical to control with
these nematodes (Table 4).
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CONCLUSION
Neoaplectana and Heterorhabditis nematodes have emerged as the only alternative
candidates to chemical insecticides for the control of a wide host range of soil-inhabiting insects.
While the efficacy of the nematode can be affected by undesirable biotic or abiotic factors, the
potential benefits (safe to vertebrates, reduced insecticide use, no environmental contamination)
are great. Recent development in the mass production of nematodes through a liquid fermentation
process, and the ability to induce anhydrobiosis in nematodes may enable them to be used
economically in the management of insect pests in different habitats (Tables 1 -4). Given our rapidly
developing understanding of nematodes and our increasing ability to manipulate them (e.g., genetic
improvement, application techniques, formulations), it would be surprising if they did not eventually
fill an important role in crop protection.
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TABLE 1
Summary of the field trials with Neoaplectana and Heterorhabditis nematodes against selected
turf grass insects (1984-1987).
Nematode8: Number ofb % Control Reduction
billion/hectare tests range average
Japanese beetles, popillia japonica
Hh: 2.5-12.5 12 27 - 90 61
HP88: 2.5-12.5 7 55 -100 76
Nc: 2.5-12.5 8 18-72 47
Standard insecticide 16 29 - 98 77
Northern masked chafer. Cvclocephala borealis
Hh: 2.5-12.5 7 12-95 53
HP88: 2.5-12.5 2 14-74 44
Nc: 2.5-12.5 5 9-61 43
Standard insecticide 6 39-99 65
June and May beetles. Phvllophaga spp
Hh: 1.0-12.5 4 48-81 61
Nc: 2.5-12.5 4 39-62 53
Standard insecticide 3 35-72 54
European chafer, Rhizotrogus maialis
Hh: 2.5-12.5 2 54-61 57
HP88: 1.2-12.5 3 56-70 63
Nc: 1.2-12.5 2 36-52 44
Standard insecticide 4 36-68 59
Mole crickets, Scapterjscus spp
Hh: 2.5-12.5 3 3-12 8
Nc: 2.5-12.5 6 42-73 62
Standard insecticide 6 52-79 69
Black cutworms. Agrotis ipsilon
Hh: 1.2-5.0 3 56-92 76
Nc: 2.5-12.5 3 44 -100 84
Standard insecticide 3 68 -100 89
Armyvorms, Pseudaletia unipuncta
Hh: 2.5-12.5 2 68-95 81
Nc: 2.5-12.5 2 74 -100 87
Standard insecticide 2 75 -100 96
Bluegrass billbuq, Sphenophorus parvulus
HP88: 2.5-7.5 4 61-79 77
Nc: 2.5-7.5 4 55-65 56
Standard insecticide 3 71-88 84
a: Hh = Heterorhabditisheliothidis. HP88 = Heterorhabditis sp HP88
isolate, Nc = Neoaplectana carpocapsae All strain.
b: Biosys, unpublished reports. Plots were 9-36 sq. meters, 4-5
replicates, moderate to high insect pressure. Soil temperature &
moisture varied from 13-27 & from 16-27% (w/w) respectively
throughout the test periods.
218
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TABLE 2
Summary of Neoaplectana carpocapsae All strain field trials (2.5 billion/hectare) applied at
planting or 2-3 weeks after planting against selected important soil-inhabiting vegetable insects
(1985-1987)a
Insect
Host
Field Efficacy0 Remarks0
Banded cucumber
beetle, Diabrotica
balteato
Black cutworm
Aarotis ipsilon
Curcurbits
Lettuce,
tomato,
corn
Fair - moderate
Moderate - high
Neonate larvae
relatively
unsusceptible
Time of appli-
cation is very
critical.
Flea beetles
Epitrix spp
Root maggots
Delia spp
Wireworms
Limonius spp
tobacco, Fair - moderate
sweet potato
Cabbage, bean Fair - moderate
onion, turnip
sugar beet, Fair - moderate
sweet potato
Neonate larvae
relatively
unsusceptible
Neonate larvae
relatively
unsusceptible -
short exposure
time
between larvae
and
nematodes.
Larvae rela-
atively
unsusceptible.
a: Based on 4-7 tests. Biosys, unpublished reports. Rows 10-20 M long,
4-5 replicates. Soil temperature ranged between 16-28°C and kept moist
throughout the test periods.
b: Low to moderate insect pressure.
c: Fair: Reduction in plant damage over control but crop protection
inadequate. Nematodes are probably useful in an Integrated Pest
Management (IPM) program.
Moderate: 50-80% crop protection. Useful in an IPM program if
complete protection is mandatory.
High: Over 80% crop protection.
d: Unsusceptible insects:
conditions.
LD50 above 50 nematodes/larva under laboratory
219
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TABLE 3
Summary of the trials with Neoaplectana and Heterorhabditis against important soil-inhabiting
insects of ornamentals, shrubs, flowers and caneberries (1985-1987)a
Condition
Nematode:dosage
Results0
Remarks
Greenhouse,
potted plants
Outdoor,
potted plants
(average)
Fieldd
16°C
Greenhouse,
potted plants
Greenhouse,
potted plants
Black vine weevil. Otiorhvnchus sulcatus
Strawberry root weevil, O. ovatus
Hh, Nc: 50-100/cm2 Moderate - high
Moderate control
obtained when
early stage larvae
(less susceptible
than later stages)
are highly present
in pots.
Hh, Nc: 50-100/cm2 Moderate - high Soil temperatures
Hh, HP88: 300-
600/cm2
Nc: 300-600/cm2
Japanese beetles.
Moderate - high
Moderate
Popillia naponica
above 16 C
Soil temperatures
above
(average)
Hh, HP88: 90/cm
Nc: 100-500/cm2
High
Low - moderate
Hh & HP88 were
equivalent to
standard
insecticides
European chafer. Rhizotrogus maialis
Hh, HP88: 90/cm
Nc: 100-500/cm2
Moderate
Low
Hh & HP88 were
equivalent to
standard
insecticides
a: Based on 4-8 tests. Biosys, unpublished reports, Stimmann et al 1985,
Klingler 1986, Rutherford et al 1987, Wright et al 1988, Shanks &
Agudelo-Silva 1987.
b: Hh: H. heliothidis; HP88 = Heterorhabditis sp. HP88 isolate; Nc: = N_._
carpocapsae All strain.
c: Low = under 50% control; Moderate: 50-80% control; High: Above 80%
control.
d: Low control was obtained at soil temperatures below 14°C (Rutherford et
al 1978, Biosys unpublished reports).
220
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TABLE 4
Recent investigations in applications technology of Neoaplectana carpocapsae
System
Application Site
Target Insects Results
Ref.
Anhydrobiotic
nematodes
mixed with
sucrose
Anydrobiotic
nematodes
mixed with
bran bait
Anhydrobiotic
nematodes
mixed with
antides iccants
Anhydrobiotic
nematodes in
alginate
capsules
Nematodes in
alginate
capsules
(slow release
system)
Nematodes in
alginate
capsules
(delivery
system)
Nematodes on
specific
moist pads
in traps
Laboratory,
plastic containers
Laboratory,
plastic containers
Laboratory, plant
seedlings
Laboratory/ petri
dish lined with
moist foam
Laboratory,
capsules contain-
ing tomato seeds
in soil
Laboratory, petri
dish (moist
environment)
Laboratory/
plastic
containers
90-100%
infection
(n=20)
70-100%
infection
(n=20)
Carpenter ant,
harvest ant,
Western yellow-
jacket (adults)
Black cutworms,
mole crickets,
house crickets,
vagrant grass-
hopper (late
stages).
Tomato hornworm, 50- 90%
beet armyworm, infection
imported cabbage
worm, corn ear-
worms (various
larval stages).
German cock-
roach (male)
Root-feeding
insects (e.g.,
corn rootworms,
cabbage maggot
Imported fire
ants
Georgis,
1987
Georgis
1987;
Georgis,
et al,
1988
Georgis,
unpubl.
German cock-
roach (various
stages), house
fly adults
60%
infection
(n=12)
high
infection
of wax
moth larvae
Adult ants
carried
capsules
to mounds
70 - 100%
infection
Georgis,
unpubl.
Kaya et
al 1987
Biosis,
unpubl.
Renn et
al 1985,
Georgis
unpubl.
221
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ENTOMOGENOUS NEMATODES FOR CONTROL OF
TURFGRASS INSECTS
WITH NOTES ON OTHER
BIOLOGICAL CONTROL AGENTS
David J. Shetlar
Research Scientist, Entomology
ChemLawn Services Corporation
Research and Development
P.O. Box 85-816
Columbus, OH 43085
The lawn care industry grew exponentially in the 20 years prior to 1985-86, with major changes
in usage of equipment, chemicals and personnel. In general, small single owner businesses which
operated out of garages or sheds have yielded to large multi-state corporations. The industry passed
the $2 billion receipt marker in 1985 and has continued to grow. Increasing buy outs, consolidation
of companies, and a slowing of total growth have marked the 1985 to 1987 years.
Many early programs utilized more fertilizer and pesticides, especially insecticides, than what
was probably needed for quality turf. Applications were usually applied in a dilute liquid form sprayed
over the entire lawn. As research information was accumulated, environmental concerns were
expressed, and business competition required cost savings, considerable reductions in chemical
usage and changes in application have occurred. To maximize profits while satisfying customer
expectations, most lawn care companies now provide complete fertilization, annual grass and
broadleaf weed control and insect control. Many southern and western markets also require
fungicide usage in order to maintain quality turf.
Though there had been increasing numbers of activist groups raising concern over lawn care
chemicals, no major effects were noted until 1985 to 1987. During these years, national media
began to exploit the sensationalism provided by these environmental activists. Many states have
begun to more actively regulate the industry and the way lawn care is delivered. Many states have
enacted regulations on applicator training and certification, customer right to now, pre and post
application notification and posting of treated lawns. Unfortunately, the scientific data base is
inadequate to fully answer the questions raised about long-term chemical exposure, synergistic
effects of chemicals and possible water contamination. Though there is little scientific information
to support claims of damage there is also little information available which has proved that damage
can not occur. This raises the problems of risk and risk assessment. Some people want no risk in
life while others can accept reasonable risks. This dilemma is difficult to resolve with reason.
Because of perceived changes in customer wants and a desire to provide safe and effective
alternatives to standard lawn care treatments, ChemLawn Services Corporation and its research
and development staff have been investigating alternative controls and systems for the last five
225
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years. In order for alternatives to be used, they must be easy to use, effective and comparable in
cost. Unfortunately, the few alternatives available for insect pest control have been, historically,
costly and/or marginally effective.
Insect parasitic (entomogenous) nematodes have been studied since the 1920's, but they
were difficult and expensive to produce and did not produce lasting effects. From 1929 to 1940, R.
W. Glaser et al. (1940) detected, reared and field tested an entomogenous nematode, Neoaplectana
glaseri Steiner. Possibly because of the war effort and discovery of synthetic organic insecticides,
little work on entomogenous nematodes for control of Japanese beetle grubs was subsequently
undertaken. Glaser attempted to produce N. glaseri in large numbers using a veal pulp medium but
this was labor intensive, difficult and did not provide sufficient nematodes for applications to large
areas. Recent interests in entomogenous nematodes have yielded better culture techniques for N.
carpocapsae Weiser and Heterorhabditis heliothidis (Khan, Brooks and Hirschman) (Dutky et al.
1964, Bedding 1981, Wouts 1981). Recently, a new venture capital company, Biosys (Palo Alto,
CA), had developed additional improved rearing procedures so that commercial production of these
nematodes (Neoaplectana spp. [=Steinernema] and Heterorhabditis spp.) was possible and field
evaluations could be undertaken. This paper contains information derived from research on these
nematodes as well as some comparative studies with other alternative products such as Bacillus
thuringiensis (Bt) strains.
LAWN INSECT PESTS AND THEIR CONTROL
The major turfgrass pests include: a) surface feeding insects such as chinch bugs, sod
webworms, cutworms, armyworms and greenbugs; as well as, b) soil or root feeding insects such
as white grubs, billbugs and mole crickets. These pests are appropriately discussed by, Niemczyk
(1981), Baker (1982), Shetlar et al. (1983), and Tashiro (1987).
The white grubs (Japanese beetle, Popillia japonica Newman; masked chafers, Cyclocephala
spp; May-June beetles, PhyHophaga spp; European chafer, Rhizotrogus majalis [Razoumowsky];
Oriental beetle, Anomala orientalis Waterhouse; Asiatic garden beetle, Maladera castanea [Arrow];
and, green June beetle, Cotinis nitida [L]) are, by far, the most troublesome widespread turfgrass
pests. The highly mobile adults seek out quality turf and lay eggs in the soil. The larvae, white
grubs, come to the soil surface to feed on plant roots and other organic material included in the
thatch. Since most turf insecticides are easily bound to the living and dead turf tissue (Niemczyk
and Krueger 1982; Sears and Chapman 1979; Niemczyk 1987), white grubs are difficult to challenge
without considerable irrigation following an insecticide spray and reduction of the thatch layer. Even
when white grub populations are below damaging levels, mammal predators such as raccoons,
skunks, opossums and moles can severely damage turf in their search for an arthropod meal.
Since the Japanese beetle is one of the most important turf damaging grubs in the eastern
United States, extensive research has been undertaken to control this pest using many tactics
(Fleming 1976). Considerable work on biological controls, especially bacterial milky diseases (Klein
et al. 1976), has been undertaken for control of Japanese beetle grubs as reviewed by Fleming
(1968). Bacillus popilliae has been proven effective but the lawn care industry has made little use
of this product. This is probably because of difficulty of application, reliability in cool soils, expense,
lack of availability of large quantities of spore powder and long time of establishment. Similar
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experience has been met with the other biological controls such as parasitic wasps (Tiphia spp.),
parasitic flies (several Tachinidae), and fungal diseases (Metarrhizium spp. and Beauveria spp.).
Because of these problems with white grub biological controls, we were most interested in
concentrating our nematode research in this area.
Mole crickets (tawny mole cricket, Scapteriscus vicinus Scudder; southern mole cricket, &
acletus Rehn and Hebard; and short wing mole cricket, £L abbreviatus Scudder) are the most
troublesome and damaging turf insects in Florida as well as surrounding southern states (Walker
et al. 1984). These pests damage turf by uprooting plants during tunneling and direct feeding.
Mature nymphs and adults can easily dig deep into the soil and thus avoid short residual, surface
applied insecticides. Insecticide laced baits have been used effectively in some cases, but these
baits rapidly decompose or lose their feeding attractiveness in periods of rainfall. As with the
Japanese beetle, imported mole crickets have not responded well to control by biologicals. Because
of these problems, we were interested in the possibility of using parasitic nematodes as an
alternative biological control measure.
We placed less emphasis on development of entomogenous nematodes for control of surface
insects because surface applied insecticides such as diazinon and chlorpyrifos are so effective at
low rates.
Our early research using entomogenous nematodes was a multifaceted approach. We
performed laboratory evaluations of nematode species and strains for infectivity against Japanese
beetle and northern masked chafer (CX boreal is Arrow) grubs. At the same time we investigated
irrigation requirements essential to the establishment of nematodes into soil covered by turfgrass
and evaluated the compatibility of the nematodes with the liquid lawn care system.
WHITE GRUB CONTROL STUDIES
Nematode Strain Evaluations
There are four species of Neoplectana (=Steinernema) (N. giaseri Steiner. N. bibionis Bovien,
N. carpocapsae Weiser and N. intermedia Poinar) and numerous recognized strains (Poinar 1986a).
Several species of Heterorhabditis. including undescribed ones, have been evaluated for insect
control. The common species are K heiiothidis (Khan, Brooks & Hirschmann), K bacteriophora
Poinar, and tL spp. "HP88".Biosys was able to collect and maintain cultures of all of these species
as well as numerous strains.
In 1983, Keith Kennedy (former ChemLawn Services Research Scientist; now Senior
Entomologist, S.C. Johnson & Son, Inc.) and his research associate, Jeff Rodencal, performed initial
evaluations of nematode strains for control of Japanese beetle and northern masked chafer grubs.
These tests were performed in PVC cylinder micro plots, a technique initially developed by Kennedy.
The micro plots are 20.5 cm (8-inch) long pieces of 15.3 cm (6-inch) diameter polyvinyl chloride
(PVC) drain pipe driven into the soil to a depth of 15.3 cm. Each cylinder has a bottom screen which
allows drainage but prohibits insect escape. A 15.3 cm golf course cup cutter can be used to take
turf plugs from established turf. The plugs, consisting of the turf with 8-10 cm of soil, are placed in
the cylinders. Field collected white grubs, usually third instars, are used to infest each turf plug. In
most cases, ten white grubs are placed head down into small holes produced by forcing a 8.0 mm
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sharpened wooden dowel through the thatch. Any grubs not digging in within 1-3 hours are replaced
with fresh grubs. The grubs are allowed 2-3 days to acclimate before control substances are added
to the cylinders.
Initial strain evaluations against Japanese beetle grubs are presented in Table 1. From this
test it appeared that N. carpocapsae 'Breton' and N. glaseri could produce moderate and excellent
control respectively. A similar study using lower rates of nematodes indicated a definite rate
response (Table 2). This was also seen when northern masked chafers were challenged with low
rates of nematodes (Table 3). These three tests indicated that nematodes could control white grubs
if high rates were used.
In 1984, we continued strain evaluations but decided that a smaller laboratory screen might
give more consistent results. Third instar white grubs were placed in 2.5 cm diameter by 10 cm long
plastic vials filled with sterilized potting soil to a depth of 7 cm. Two Japanese beetle grubs or one
northern masked chafer grub was placed in each vial and treatments (approximately 250 infective
nematodes per vial) were replicated six times. The vials were examined at 2, 4 and 7 days after
treatment (DAT).
Mortalities at 2, 4 and 7 DAT are presented in Table 4 for Japanese beetle grubs and Table 5
for northern masked chafers. From these studies, it appeared that the northern masked chafer might
be less susceptible to nematode attack. The K spp. 'HP88' provided adequate mortality for both
grub species. However. N. carpocapsae '42' (='Bretonf x 'DD136') and N. c. 'Breton' produced the
best control of Japanese beetle grubs while R c^ 'Italian' worked best on northern masked chafers.
This experiment was performed again with larger vials (5.0 cm diameter x 10.0 cm deep) using
four Japanese beetle grubs per vial. The grubs were allowed to acclimate for 48 hours and inactive
grubs were replaced before the 450 infective nematodes per vial were added. The vials were rated
at 7, 14 and 21 DAT. The mortality data are presented in Table 6. It appeared that JH. heliothidis
'NC' and K spp. 'HP88' produced the higher mortality, 76% and 82% respectively, at 21 DAT.
Most of the N,. carpocapsae strains, except for hL a 'Breton x DD136', did not provide reasonable
mortality.
Application Evaluations
By 1985, we had decided that entomogenous nematodes should be field tested on small plots
for control of white grubs. We also wanted to know if the nematodes were compatible with the liquid
lawn care application system and chemicals. Of most concern, was knowing if fertilizers, herbicides
or insecticides would adversely affect the infective juvenile nematodes.
Nematodes were added to sample tank mixes containing water, water + fertilizer (nitrogen,
phosphorus, potassium), water + fertilizer + broadleaf herbicide, water + fertilizer + broadleaf
herbicide + insecticide, and water + fertilizer + broadleaf herbicide + preemergence (crabgrass,
etc.) herbicide. These mixtures were agitated continuously on a shaker tray and samples were
withdrawn at 1, 2, 3, 5, 8, 12 and 24 hours. By five hours only the preemergence mix had caused
significant nematode mortality. By 12 hours the fertilizer, fertilizer + broadleaf herbicide and fertilizer
+ broadleaf herbicide + insecticide had mortality no greater than nematodes in water. In fact, the
fertilizer alone had significantly less mortality. By 24 hours the insecticide mix had caused
considerable mortality. When nematode infectivity was bioassayed (with wax moth larvae), only the
water, fertilizer and fertilizer + broadleaf herbicide had not caused a significant reduction by five
hours. The water or fertilizer mixes remained equally benign at 12 hours. In summary, the
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nematodes are compatible with liquid fertilizers and commonly used broadleaf herbicides. This was
encouraging because the nematodes would most likely be used when preemergence herbicides
would not be used and supposedly insecticides would not be necessary.
Effect of Irrigation
Another concern with applying nematodes was their requirement for establishment into the
turf and soil. Entomogenous nematodes are highly intolerant of environmental extremes, especially
moisture and temperature (Gaugler 1981). Jackson et al. (1983) greatly increased establishment
of K bacteriophora in pasture soil for white grub control if applications were made during rain or
followed with irrigation. We wanted to know if irrigation was needed and if so, how much, when the
ChemLawn nozzle was used. The ChemLawn nozzle, a low pressure showerhead type which
delivers 0.16 liter/m2 (=4 gal/1000 ft2) is the liquid lawn care standard.
The previously described PVC microplots were used in a greenhouse. Turf plugs were taken
from a two year old stand of Kentucky bluegrass grown on Blount silt loam (32% sand, 36% silt,
32% clay) with pH's of 6.5-8.0. Each plug had an average of 0.75 cm of thatch. The greenhouse
was maintained at 20QC (±59C) and the turf was allowed to acclimate for seven days. The turf was
then given a water drench and allowed to dry to the wilting point (soil moisture = 18.5%). Small holes
were drilled radially around the soil plug at two levels (5 holes at each level of 2.5 cm and 5.0 cm).
Each turf plug was inoculated with approximately 24,000 infective nematodes (=12.35 x 109/ha; =
5.0 x 109/a) in 3.2 ml of water. JSL carpocapsae 'Mexican', NL glaseri and hL heliothidis 'NC' were
used. Treatments were followed with 0.0, 63.0,126.0 or 252 ml water/cylinder irrigation (=0.0, 0.25,
0.50,1.0 inch). The cylinders were then capped with aluminum foil to reduce evaporation. A greater
wax moth larva (Galleria mellonella L.) was placed in each of the holes and restrained for 48 hours
at 3,5 and 11 DAT. The larvae were then removed, incubated for five days, and dissected to check
for nematode infection.
The data indicated that there were few differences between the nematode species so the data
were pooled for each irrigation amount in each bioassay (Shetlar et al. 1988). These data are
graphically presented in Figure 1. From this graph one can readily see that at least 0.64 cm (=0.25
inch) of irrigation is needed to establish nematodes for up to five days after treatment. At least 2.5
cm (=1.0 inch) irrigation is needed to sustain the nematodes to 11 DAT in dry soil.
Small Plot Grub Tests -1985
On 28 August 85, two areas with Japanese beetle grubs were selected beside two fairways
at a country club in central Ohio. The soil (a Blount silt loam) was at the turf wilting point and was
thinly covered by Kentucky bluegrass mixed with small amounts of fine fescue and crabgrass. hL
carpocapsae 'Mexican' was used because of availability. Each treatment was replicated five times
in each area (A and B) in a randomized complete block design using 6.1 x 6.1 m treatment blocks.
Treatments were: 1) 12.35 x 109 nematodes (nemas)/ha with a ChemLawn nozzle at 0.16 liter/m2
(=4 gal/1000 ft2); 2) 6.18 x 109 nemas/ha with a ChemLawn nozzle; 3) 12.35 x 109 nemas/ha with
an eight pinhole nozzle boom at 0.16 liter/m2; 4) Isozophos 4E (=Triumph,, Ciba-Geigy Corp.)
Insecticide at 2.24 kg (Al)/ha with a ChemLawn nozzle; and 5) water treated check (0.16 liter/m2).
Area A was treated 9 September and no irrigation was applied after treatment. Area B was treated
10 September and treatments were irrigated with about 0.64, cm water immediately following
application. A trace of rainfall occurred the night of 9 September but this was not enough to wet the
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soil. Area A was evaluated on 2 October, 23 DAT, and Area B was evaluated on 9 October, 29
DAT. Grub populations were assessed by taking four 0.09 m2 (1.0 ft2) samples at random from
each treatment block. Only traces of rainfall had occurred during the experiment and the soil was
very dry (16-18% moisture) at the end of the experiment.
The data for Area A and Area B are presented in Table 7 (Shetlar et al. 1988). From these
data it is evident that irrigation increased grub control and possibly increased infection. However,
good control was not achieved in either area when compared to an insecticide. We felt this was
most likely due to the extremely dry conditions.
Small Plot Grub Test -1986
In 1986, we repeated the field test of nematodes using irrigation before and after nematode
applications. We were also able to obtain sufficient quantities of H. heliothidis 'NC1 to be included.
On 10 September 86, an area with Japanese beetle grubs was treated beside a fairway at a
central Ohio country club. Treatment blocks were 1.2 x 1.5 m and each block was irrigated before
application with 22.7 liter water (=0.64 cm). Treatments were: 1) 12.35 x 109 nemas/ha of N.
carpocapsae 'Mexican'; 2) 12.35 x 109 nemas/ha of H. heliothidis 'NC': 3) Isofenphos 21 (=Oftanol,
Mobay Chemical Co.) at 2.24 kg (Al)/ha; and, 4) water treated checks. Treatments were applied in
7.6 liter water from watering cans using shower head nozzles and each block was irrigated after
treatment with 15.1 liter water (=0.64 cm total). Pretreatment grub counts were taken from four
blocks in the area and posttreatment counts were taken 39 DAT using three 0.09 m2 samples in
each treatment block.
The data from this experiment are presented in Table 8 (Shetlar et al. 1988). This field test
demonstrates that adequate grub control (> 70%) can be achieved using entomogenous nematodes
though this control may be significantly less than using an insecticide. Also indicated is that
Heterorhabditis spp. may be better suited than hL carpocapsae.
Discussion of Use of Nematodes for White Grub Control
Entomogenous nematodes appear to show promise as a biological control agent to manage
white grubs in turfgrass. The nematodes are compatible with the materials (at least fertilizer) and
equipment used by liquid lawn care applicators. For soil insect control, irrigation and soil moisture
seem to be the most critical factors for success of the nematodes. The nematode species and strains
also exhibit a considerable range of activity. In our tests R heliothides 'NC' and K spp. 'HP88'
appear to be more useful than the N. carpocapsae strains. Unfortunately, N. glaseri, the first species
identified for grub control (Glaser et al. 1940), remains difficult to culture and thus difficult to evaluate.
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CONTROL OF TURF LEPIDOPTERA
Screening of Nematodes and Other Biologicals
Surface feeding turf Lepidoptera such as sod webworms (Pyralidae: Crambinae) and the
armyworm-cutworm (Noctuidae) complexes are periodic pests. Though these are easily controlled
with low rates of insecticides, we are very interested in biological alternatives. The literature indicates
that these pests should be susceptible to entomogenous nematodes (Poinar 1986b) as well as other
biologlcals such as Bacillus thuringiensis (Bt) (Ignoffo and Gregory 1972; Krieg and Langenbruch
1981) and Beauveria or Metarhizium (Perron 1981). Since the nematodes were available and Bt
was commercially marketed, we undertook numerous tests to evaluate the efficacy of these agents
for caterpillar control.
In the fall of 1984, an outbreak of sod webworms (mainly the tropical sod webworm,
Herpetogramma phaeopteralis Guenee) occurred in the Boynton Beach, Florida area. Larvae were
field collected and shipped to Columbus, Ohio for testing. The larvae were maintained on
bermudagrass clippings until they were about 1.0 cm long. In the first test, glass petri dishes (20 x
80 mm) were lined with two pieces of 80 mm diameter fijter paper wetted with 2.0 ml distilled water.
Several leaf blades of bermudagrass were added and dishes were inoculated with about 800
nematodes in 1.0 ml water. Four larvae were placed in each dish and treatments (N. carpocapsae
'Breton', N. a 'Agriotos1 and water check) were replicated three times. By 4 DAT most of the larvae
had spun webbed tunnels along the upper surface of the petri dishes. Apparently, this behavior
effectively isolated the larvae from the nematodes. Out of 12 larvae per each treatment the following
mortalities were recorded: two in the checks, seven in the NL c^ 'Breton' and eight in the NL a
'Agriotos'.
A second test was established using 5.0 x 10.0 cm snap cap vials filled with 2.5 cm of potting
soil upon which were placed six blades of bermudagrass. Four sod webworms and about 800
nematodes were added and the treatments (NL a 'Breton', NL c^ 'Agriotos', NL c. 'Italian' and water
check) were replicated five times. The vials were evaluated 3 DAT and the larvae were dissected
to confirm nematode infection. Fewer larvae sheltered themselves above the soil and the infection
rate is presented in Table 9.
A petri dish test in 1985 using the armyworm, Pseudaletia unipuncta (Haworth), provided
excellent control within seven days. Though all larvae subjected to nematodes had been killed, the
percent of larvae with active infections was dramatically different. JSL c^ 'Breton' had 100% infection
and N, glaseri had 87% infection but no nematodes were recovered from the hL heliothidis treated
larvae.
PVC cylinder micro plots were used in 1986 and the parasitic nematodes were compared to
commercial preparations of Bt (Thuricide and Javelin, Sandoz, Inc.) and surface insecticides. In the
first two evaluations, armyworms were laboratory reared on artificial diet until they were
approximately 2.0 cm long. Each turf plug was infested with eight larvae and irrigated with 60 ml
water 24 hours before treatment. Each cylinder was covered with a screen top to prohibit armyworm
escape or predator/parasitoid contamination. Each treatment was replicated five times and
evaluations were made 3 DAT for nematode treatments and 7 DAT for Bt and water control
treatments. Chlorpyrifos (Dursban 4E,, Dow Chemical Co.) was used as a standard surface
insecticide. The results of these two tests are presented in Tables 10 and Table 11.
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In the first test, the nematodes gave excellent control and the NL carpocapsae. strains were
not significantly different (P < 0.05, df = 6)than the chlorpyrifos treatment. K heUothidis 'NC' was
evaluated as providing good control (> 70%) though it was significantly lower than the chlorpyrifos
treatment. The Bt treatments did not provide adequate control and all the turf was eaten by the end
of the study.
The second test was somewhat the same though K heliothidis 'NC' provided inadequate
control (< 70%). NL bibionis was also considered inadequate. This may have been caused by the
lower soil moisture. Soil moisture in the first study was 26% by weight while the second study had
only 18% moisture. The Bt treatments, even at 4X rates, still did not provide control of armyworm
larvae. This is partially due to the large size of the larvae and some soil Lepidoptera seem to be
refractive to Bt toxins.
DISCUSSION ON BIOLOGICALS FOR CONTROL OF TURF CATERPILLARS
Our initial screenings indicate that entomogenous nematodes appear to have excellent
potential for control of turf lepidopterous pests. £L carpocapsae strains seem to be the most active
nematodes. Tests with commercial Bt preparations indicate that problems exist concerning soil
Lepidoptera species controlled and timing, or size of larvae to be controlled. In other words, Bt
does not seem to have a broad spectrum of control when compared to entomogenous nematodes.
MOLE CRICKET CONTROL
Field Evaluations
Preliminary screening of entomogenous nematodes for infectivity to mole crickets was
performed by Ken Lawrence (Associate Research Scientist, ChemLawn Services R&D, Boynton
Beach, FL) in soil filled cups or petri dishes in 1984. He noted that mole crickets (Scapteriscus
acletus and £L vicinus) could be infected and killed though nematode reproduction was often
sporadic.
In late 1985, Ken Lawrence and Richard Miller (Entomologist, Biosys, Palo Alto, CA) performed
another bioassay of parasitic nematodes for mole cricket infectivity. £L carpocapsae 'Mexican' and
'All1 and M, bibionis 'SN' were applied to moistened filter paper in 15 x 100 mm plastic petri dishes.
A single adult £L acletus was placed in each petri dish and mortality was recorded at 4 and 6 DAT.
Dead mole crickets were removed and placed on sterile moistened filter paper in fresh dishes for
72-120 hours for incubation. After incubation the insects were dissected to evaluate nematode
reproduction. These data are presented in Table 12. The higher rates of NL carpocapsae strains
were able to achieve 100% mortality and nematode reproduction was more successful than with
N. bibionis.
In 1985, we undertook a series of field applications of parasitic nematodes to attempt to control
mole crickets. A Boynton Beach, FL golf course driving range was selected. This area was well
populated by mole crickets as evidenced by numerous trails and mounds which were easily
232
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assessed in the short cut bermudagrass. Area A consisted of treatment blocks 9.1 x 9.1 m replicated
five times in a randomized complete block design. Area B consisted of large unreplicated treatment
blocks, 15.2 x 24.4 m. Area A was evaluated by counting all the mole cricket tunnels within each
treatment block while Area B was evaluated by counting ail the tunnels in a 9.1 m wide transect
running the length of the blocks. A pretreatment flushing determined that most of the mole crickets
were adults and most (> 70%) were S, vicinus. The nematodes were applied using a ChemLawn
nozzle calibrated at 0.16 liter/m2. Both areas were irrigated through the golf course system the
evening following applications.
Mole cricket activity was evaluated a week after treatment and the data are presented in Table
13 and Table 14. These data indicate that hL. carpocapsae was effective in reducing adult mole
cricket activity and there was a definite rate response. Unfortunately, nematode infected mole
crickets were not recovered using a soap flush a week after treatment and mole cricket activity
resumed in all plots within four weeks after treatment.
A summer application of nematodes was made to bermudagrass containing numerous
nymphal mole crickets (1.5-2.5 cm long) using the design of Area A (above). These data are
presented in Table 15. At this time no significant control was achieved using nematodes or
insecticides.
Discussion on Using Parasitic Nematodes for Mole Cricket Control
Our experiences indicate that entomogenous nematodes have the ability to attack mole
crickets. However, there seems to be some problem with the nematode's ability to enter mole
crickets in field conditions. This may be due to the almost constant mole cricket activity or the dense
covering of hydrophobic hairs. We feel that better control may be achieved if a bait containing
nematodes can be developed.
MISCELLANEOUS TURF INSECT CONTROL
Bluegrass Bill bug
The bluegrass billbug, Sphenophorus parvalus Gyllenhal, is an important pest of cool season
turf across the northern states (Niemczyk 1983, Tashiro & Personius 1970). This pest is especially
difficult to control because the adults are highly migratory and are susceptible to surface insecticides
for a short time during the spring (Niemczyk 1982). Soil insecticides are often effective against the
larvae when they emerge from turf plants. However, the larvae may emerge over an extended
period.
In 1983, a ChemLawn Services branch in Boise, Idaho applied NL carpocapsae 'Breton' to six
lawns with active billbug larvae. The nematodes were applied at a 7.75 x 108 nemas/ha (= 3.1 x
108 nemas/a) using the ChemLawn nozzle at 0.16 liter/m2. Mark Mahady (Associate Research
Scientist, ChemLawn Services Corp., Monterey, CA) supervised the application and subsequent
sampling. Sampling at 14 and 21 DAT revealed a majority of dead larvae (creamy yellow in color),
some moribund larvae (slow moving) and few normal larvae. Dead larvae were collected and
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shipped to George Poinar, Jr. (Univ. California, Berkeley, CA) for evaluation. Positive nematode
infection was confirmed. By 28 DAT, no live billbug larvae were found on the treated lawns, but by
35 DAT two lawns contained fresh young larvae and displayed new injury. This test indicates that
R carpocapsae is able to infect and control the bluegrass billbug larva.
Crane Flies
The European crane fly, Tipula paludosa Meigen, or 'leatherjacket' is a northwestern Europe
native which has become established in the Pacific Northwest (British Columbia, Washington and
Oregon) (Jackson and Campbell 1975). This pest can cause considerable damage to turfgrass.
An European test of nematodes for control of the European crane fly indicated that the larvae are
susceptible to infection (Lam and Webster 1972).
In 1986, Patrice Suleman (Research Associate, ChemLawn Services Corp., Columbus, OH)
located an area of golf course turf with significant damage apparently due to a native (range) crane
fly (Tipula spp.). Larvae were field collected and transported to the laboratory for a petri dish test.
Glass petri dishes (15 x 80 mm) were lined with filter paper and five larvae per dish were distributed.
Each dish received 2.0 ml distilled water and 1.0 ml aliquot containing 200 or 400 nematodes. Four
nematode strains plus a water check were evaluated with three replicates. Mortality was recorded
at 2,4 and 8 DAT and dead larvae were examined for nematode infection. The data for this test are
presented in Table 16. The data indicate that this crane fly larva is susceptible to all the strains
evaluated.
SUMMARY
Our present day knowledge of the susceptibility of turfgrass insect pests to entomogenous
nematodes indicates that this may be the first biological control agent with a broad spectrum of
activity. We have laboratory and field data confirming activity against surface insects such as sod
webworms, cutworms, armyworms and crane fly larvae. We also have laboratory and field data
confirming activity against soil insects such as white grubs (Japanese beetles and northern masked
chafers), mole crickets, and billbug larvae. The only major pest not evaluated has been chinch
bugs. This pest is probably too small for successful infection but a trial test should be performed.
Other sporadic and minor pests not likely to be controlled by parasitic nematodes are greenbug,
winter grain mite, Bank's grass mite, bermudagrass mite and several scales and mealy bugs.
Future challenges include: 1) identification of soil conditions most conducive to nematode
survival and activity; 2) refinement of application techniques (sprays, irrigation, baits, etc.); and 3)
improved mass production which maintains the nematodes1 hardiness and infectivity while lowering
cost.
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REFERENCES CITED
Abbott, W.S. 1925. A method for computing the effectiveness of an insecticide. J. Econ. Entomol. 18:265-267.
Baker, J.R. (ed.) 1982. Insects and other pests associated with turf: Some important, common, and potential pests in the
southeastern United States. North Carolina Agr. Ext. Serv. AG-268:108pp.
Bedding, R.A. 1981. Low cost in vitro mass production of Neoaplectana and Heterorhabditis species (Nematoda) for field
control of insect pests Nematologica. 27:109-114.
Duncan, D.B. 1955. Multiple range and multiple F tests. Biometrics. 11:1-42.
Dutky, S.R., J.V. Thompson and G.E. Cantwell. 1964. A technique for the mass propagation of the DD-136 nematode.
J. Insect. Pathol. 6:417-422.
Perron, P. 1981. Pest control by the fungi Beauveria and Metarhizium. pp 463-482. In H.D. Surges (ed), Microbial Control
of Pests and Plant Diseases 1970-1980. Academic Press, London.
Fleming, WE. 1968. Biological control of the Japanese beetle. United States Dept. Agr., ARS Tech. Bull. 1383:78pp.
Fleming, W.E. 1976. Integrating control of the Japanese beetle - A historical review. United States Dept. Agr., ARS, Tech.
Bull. 1545:65pp.
Gaugler, R. 1981. The biological control potential of neoaplectanid nematodes. J. Nematol. 13:241-249.
Glaser, R.W., E.E. McCoy and H.B. Girth. 1940. The biology and economic importance of a nematode parasite of insects.
J. Parasitol. 26:479-495.
Ignoffo, C.M. and B. Gregory. 1972. Effect of Bacillus thuringiensis B-exotoxin on larval maturation, adult longevity,
fecundity, and egg viability in several species of lepidoptera. Environ. Entomol. 1:269-272.
Jackson, D.M. and R.L. Campbell. 1975. Biology of the European crane fly, Tipula paludosa Meigen, in western
Washington (Tipulidae:Diptera). Wash. State. Univ. Tech. Bull. 81:23pp.
Jackson, T.A., B.W. Todd and WM. Wouts. 1983. The effect of moisture and method of application on the establishment
of the entomophagous nematode (Heterorhabditis bacteriophora) in pasture. Proc. 36th N.Z. Weed & Pest
Control Conf. pp 195-198.
Klein, M.G., C.H. Johnson and T.L Ladd, Jr. 1976. A bibliography of the milky disease bacteria (Bacillus spp.) associated
with the Japanese beetle, Popilliae japonica. and closely, related Scarabaeidae. Bull. Entomol. Soc. Amer.
22:305-310.
Krieg, A. and G.A. Langenbruch. 1981. Susceptibility of arthropod species to Bacillus thuringiensis. pp 837-896. In H.D.
Burges (ed.), Microbial Control of Pests and Plant Diseases 1970-80. Academic Press, London.
Lam, A.B.Q. and J.M. Webster. 1972. Effects of DD-136 nematode and of a B-exotoxin preparation of Bacillus thuringiensis
var. thuringiensis on leatherjackets, Tipula paludosa, larvae. J. Invertebr. Pathol. 20:141-149.
Niemczyk, H. 1981. Destructive Turf Insects. HDN Books, Wooster, OH. 48pp.
Niemczyk, H.D. 1982. Chinch bug and bluegrass billbug control with spring applications of chlorpyrifos, pp 85-89. In H.D.
Niemczyk and B.J. Joyner (eds.), Advances in Turfgrass Entomology. Hammer Graphics, Piqua, OH. 150pp.
Niemczyk, H.D. 1983. The bluegrass billbug: a frequently misdiagnosed pest of turfgrass. Amer. Lawn Appl.,
May-June:4-7.
Niemczyk, H.D. 1987. The influence of application timing and posttreatment irrigation on the fate and effectiveness of
isofenphos for control of Japanese beetle (Coleoptera: Scarabaeidae) larvae in turfgrass. J. Econ. Entomol.
80:465-470.
Niemczyk, H.D. and H.R. Krueger. 1982. Binding of insecticides on turfgrass thatch, pp 61-63. In H.D. Niemczyk and
B.J. Joyner (eds.), Advances in Turfgrass Entomology. Hammer Graphics, Piqua, OH 150pp.
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Poinar, G.O. 1986a. Recognition of Neoaplectana species (SteinernematidaerRhabditida). Proc. Helminthol. Soc. Wash.
53:121-129.
Poinar, G.O. 19866. Entomogenous nematodes. In H. Franz (ed.), Biological Plant and Health Protection, Fortschritte
der Zoologie, Bd. 32. G. Fischer Verlag, Stuttgart, New York. pp. 95-121.
Sears, M.K. and R.A. Chapman. 1979. Persistence and movement of four insecticides applied to turfgrass. J. Econ.
Entomol. 72:272-274.
Shetlar, D.J., P.R. Heller and P.O. Irish. 1983. Turfgrass insect and mite manual with an index of registered materials.
Pennsylvania Turfgrass Council, Bellefonte, PA. 63pp.
Shetlar, D.J., P.E. Suleman and R. Georgis. 1988. Irrigation and use of entomogenous nematodes, Neoaplectana spp.
and Heterorhabditis heliothidis (Rhabditida:Steinernematidae and Heterorhabditidae), for control of Japanese
beetle (Coleoptera:Scarabaeidae) grubs in turfgrass. J. Econ. Entomol. 81(5): 1318-1322.
Tashiro, H. 1987. Turfgrass Insects of the United States and Canada. Cornell Univ. Press, Ithaca, NY 391pp.
Tashiro, H. and K.E. Personius. 1970. Current status of the bluegrass billbug and its control in western New York home
lawns. J. Econ. Entomol. 63:23-29.
Walker, T.J. (ed.), R.I. Sailes, J.A. Reined, D. Boucias, P. Busey, R.L. Kepner, T.G. Forrest and W.G. Hudson. 1984(1985).
Mole crickets in Florida. Florida Agr. Exp. Sta. IFAS Bull. 846:54pp.
Wouts, W.M. 1981. Mass production of the entomogenous nematode Heterorhabditis heliothidis (Nematoda:
Heterorhabditidae) on artificial media. J. Nematol. 13:467-469.
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TABLE 1
Japanese beetle larval control in turfgrass plugs with entomogenous nematodes, Milford
Center, OH.
Treatment Rate X larvae/cylinder % control
(13/V/83) (nemas/ha) 10 DAT
Check
N. c. 'Breton' 14.1xl09
N. c. 'HOP' 14.1X109
N. c. 'Mexican' 14.1xl09
N. g. 14.1X109
H. spp 'HP88' 14.1X109
N. c. = Neoaplectana carpocapsae ; N.
Heterorhabditis .
8.2 a
2 . 5 cd 69
3.8 be 53
7.8 a 4
0.8 d 90
6.0 ab 27
g. = N. alaseri; H. =
Equivalent to 5.7xl09 nemas/a.
Ten 3rd instar larvae per cylinder; N = 6; means followed by
the same letter are not significantly different (P = 0.1;
Duncan's [1955] multiple range test).
Calculated by Abbott's (1925) formula.
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TABLE 2
Control of 2nd and 3rd instar Japanese beetle larvae with varying rates of Neoaplectana
carpocapsae and NL glaseri. Milford Center, OH, 1983.
Treatment
(21/ix/83)
N. carpocapsae
1 Breton '
N. alaseri
Triumph 4E
Check
Rate X larvae/cvlinder
(nemas/ha) 14 DAT
1
2
5
10
1
2
5
10
2.24
.25x10*
.50x10*
.00x10*
.00x10*
.25x10*
.50x10*
.00x10*
.00x10*
kg(AI)/ha
—
6.8
6.2
5.8
5.7
6.8
5.7
6.0
4.8
3.2
7.0
ab
ab
ab
ab
ab
ab
ab
be
c
a
% control
2
12
17
19
2
19
14
31
55
-
Equivalent to 0.5, 1.0, 2.0 and 4.0 x 10* nemas/a,
respectively.
Ten 3rd instar larvae/cylinder; N = 6; means followed
by the same letter are not significantly different (P
0.1; Duncan's [1955] multiple range test).
Calculated by Abbott's (1925) formula.
238
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TABLE 3
Control of Northern masked chafer larvae with two rates of Neoaplectana carpocapsae "Breton1
and N. qlaseri. Mllford Center, OH 1983.
X larvae/cvlinder
Treatment
(5/X/83)
N. alaseri
N. carpocapsae
N. alaseri
N. carpocapsae
Triumph 4E
Oftanol 2F
Check
Rate Top 2"
(nemas/ha) of soil
5.5x10*
5.5X108
10.9x10*
10.9x10*
2.24 kg(AI)/ha
2.24 kg(AI)/ha
6.2 a
7.2 a
8.0 a
7.0 a
1.5 b
0 b
7.0 a
14 DAT % control
Entire Top 2"
soil plug of soil
6
8
9
9
1
0
8
.2 b 11
.0 ab 0
.5 a 0
.0 a 0
.8 c 86
.2 c 100
.2 ab
Entire
soil plug
24
3
0
0
79
97
^™
Equivalent to 4.4 and 2.2x10* nemas/a respectively.
Ten 3rd instar larvae cylinder; N = 4; means followed by
the same letter are not significantly different (P = 0.1;
Duncans [1955] multiple range test).
Calculated by Abbott's (1925) formula.
239
-------
TABLE 4
Mortality of Japanese beetle grubs caused by parasitic nematode strains.
Nematode Strain
X of surviving larvae (% control)
2 DAT 4 DAT 7 DAT
N.
N.
N.
N-
N.
N.
N.
N.
H.
c.
c.
c.
c.
c.
c.
c.
c.
spp
1 Agr iotos '
'All'
' Breton '
'Breton x DD1361
'DD136'
•HOP'
'Italian'
'Mexican'
. 'HP88'
Check
0.
0.
0.
0.
1.
1.
1.
1.
1.
1.
83
83
67
50
16
50
16
33
00
33
(38)
(38)
(49)
(62)
(12)
(00)
(12)
(00)
(24)
(")
0.
0.
0.
0.
0.
0.
0.
0.
0.
1.
83
67
16
16
83
83
50
33
67
33
(38)
(48)
(88)
(88)
(38)
(38)
(61)
(75)
(48)
( — )
0.
0.
0.
0.
0.
0.
0.
0.
0.
1.
50
67
16
16
50
67
50
33
33
33
(61)
(48)
(88)
(88)
(61)
(48)
(61)
(75)
(75)
(— )
N. c. = Neoaplectana carpocapsae; H. = Heterorhabditis; 250
nemas/vial.
Calculated by Abbott's (1925) formula.
240
-------
TABLE 5
Mortality of northern masked chafer grubs caused by parasitic nematode strains.
Nematode Strain
X of surviving larvae (% control)
2 DAT 4 DAT 7 DAT
N.
N.
N.
N.
N.
N.
N.
N.
H-
c.
c.
c.
c.
c.
c.
c.
c.
spp
'Agriotos1
'All1
1 Breton '
'Breton x DD136'
'DD1361
'HOP1
'Italian'
'Mexican'
. 'HP88'
Check
0.
0.
0.
0.
1.
0.
0.
0.
1.
1.
83
83
83
67
83
83
83
67
00
00
(17)
(17)
(17)
(33)
(17)
(17)
(17)
(33)
(00)
( — )
0.
0.
0,
o.
0.
0.
0.
0.
0.
1.
83
67
50
67
83
67
16
50
67
00
(17)
(33)
(50)
(33)
(17)
(33)
(84)
(50)
(33)
( — )
0.
0.
0.
0.
0.
0.
0.
0.
0-
1.
67
50
50
67
67
67
16
50
33
00
(33)
(50)
(50)
(33)
(33)
(33)
(84)
(50)
(67)
( — )
N. c. = Neoaplectana carpocapsae; H. = Heterorhabditis; 250
nemas/vial.
Calculated by Abbott's (1925) formula.
241
-------
TABLE 6
Mortality of Japanese beetle grubs caused by parasitic nematode strains.
Nematode Strain
fi.
M.
H.
M.
H.
E.
M.
H.
H.
H.
H.
H.
c.
c.
c.
c.
c.
c.
c.
c.
c.
h.
spp
b.
'Agriotos'
'All1
1 Breton '
•Breton x DD1361
•DD136'
'HOP1
•Italian'
'Mexican'
•PYE'
'NC'
. 'HP88'
Check
N. c
. = Neoaolectana
X
7
2
2
2
2
2
3
2
3
3
2
1
3
3
of surviving larvae (%
DAT
.0
.3
.8
.8
.3
.0
.6
.0
.0
.3
.8
.3
.6
(44)
(36)
(22)
(22)
(36)
(17)
(27)
(17)
(17)
(36)
(50)
( 8)
(")
carpocapsae ; H.
heliothidis; H. = Heterorhabdi
tis ?
14
2.
1.
1.
1.
2.
2.
1.
2.
2.
1.
1.
2.
3.
DAT
0
5
8
6
1
6
8
8
5
0
0
0
3
(39)
(55)
(46)
(52)
(36)
(21)
(46)
(15)
(24)
(70)
(70)
(39)
(~)
control)
21 DAT
1.
1.
1.
1.
1.
2.
1.
2.
2.
0.
0.
1.
3.
2
5
6
0
6
5
5
5
5
8
6
5
3
(64)
(55)
(52)
(70)
(52)
(24)
(55)
(24)
(24)
(76)
(82)
(55)
( — )
h. = He t er orhabd itis
H. b. =
H
. bacter iophora ;
450 nemas/vial.
Calculated by Abbott's formula.
242
-------
TABLE 7
Average number of normal ±sd (% control) and nematode infected grubs per 0.09m2 per
treatment in Areas A and B.
Treatment
X Grubs (%)
X Infected
Area A (not irrigated)
12.35xl09/ha
w/CL nozzle
6.18xl09/ha
w/CL nozzle
12/35xlO»/ha
w/ph nozzle
Isozophos
15.8± 8.9 ( 6%)a 2.1±2.6a
15.1+ 5.7 ( 7%)a
15.7+10.1 (10%)a
Area B (irrigated)
12.35 bill/ha
w/CL nozzle
6.18 bill/ha
w/CL nozzle
12.35 bill/ha
w/ph nozzle
Isozophos
2.24 kgAI/ha
Check
11.4+ 2.2 (25%)a
13.5+ 1.6 (ll%)a
3.8+ 2.6
15.2+ 6.4
(76%) b
( )a
0.5±0.4 b
0.2+0.3 b
2.24 kg(AI)/ha
Check
4.0+ 2.0 (76%) b
16.8+ 4.8 ( )a
0.0+0.0 b
0.0+0.0 b
10.0+ 3.5 (34%)a 1.9+1.6a
1.9+1.4a
1.4±0.8a
0.0+0.0 b
0.0+0.0 b
Means in the same column for each area followed with the
same letter are not significantly different (P = 0.05;
Duncan's [1955] multiple range test)
CL = ChemLawn shower head nozzle
ph = Pinhole nozzle boom
243
-------
TABLE 8
Average number ±sd of Japanese beetle white grubs per 0.09m2 per plot 39 DAT with
entomogenous nematodes and insecticide followed with irrigation.
Treatment X Grubs/0.09m2 (% control)
N. carpocapsae
12.35xl09/ha 7.8+3.9 b 55%
H. heliothidis
12.35xl09/ha 4.5±3.3 c 74%
Isofenfos 2F
2.24 kg(AI)/ha 1.3+1.5 d 93%
Check
1.27cm water 17.3+5.9a
Means followed by the same letter are not significantly
different (P = 0.05; Duncan's [1955] multiple range test).
percent control determined using Abbott's (1925) formula
(pretreatment counts =16.9 grubs/0.09m2).
244
-------
TABLE 9
Sod Webworm mortality when subjected to various parasitic nematode strains 3 DAT.
Treatment # Alive # Dead # Infected % Infected
Water Check 11 9 0 0
N. c. 'Breton1 3 17 17 85
N. c. 'Agriotis' 3 17 15 75
N. c. 'Italian1 1 19 12 60
N. c. = Neoaplectana carpocapsae
245
-------
TABLE 10
Control of armyworm (Pseudaleta unipuncta) larvae using entomogenous nematodes and
Bacillus thuringiensis products.
Treatment
17/vii/86
N. c. 'All1
H. c. 'Mexican1
E. h. 'NC«
Thuricide®
Javelin®
Chlorpyrifos 4E
Control
Rate _
(nemas/ha) X
12.5X109
12.5X109
12.5X109
2.4 1/ha
2.4 1/ha
1.1 kg(AI)/ha
—
Larvae/cy 1 inder
0.0 A
0.4 A
1.8 B
6.6 C
7.2 CD
0.4 A
8.0 D
(% control)
(100)
(95)
(78)
(18)
(10)
(95)
—
12.5X109 nemas/ha = S.OxlO9 nemas/a; 2.4 1/ha = 1 qt/a; 1.1
kg(AI)/ha = 1.0 lb(AI)/a.
Numbers followed by the same letter are not significantly
different (P = 0.05; Duncan's [1955] multiple range test).
Calculated by Abbott's (1925) formula.
246
-------
TABLE 11
Control of armyworms (Pseudaleta unipuncta) larvae using entomogenous nematodes and
Bacillus thuringiensis products.
Treatment
5/viii/86
H. h. 'NCf
N. b.
Javelin®
Thuricide®
Chlorpyrifos 4E
Control
Rate X
12.5X109
12.5X109
9.5 1/ha
9.5 1/ha
1.1 kg(AI)/ha
—
Larvae/ cyl inder
3.0 B
4.8 C
6.2 D
7.0 DE
0.0 A
7.8 E
(% control)
(61)
(31)
(21)
(10)
(100)
—
12.5xl09 nemas/ha = 5.0xl09 nemas/a; 9.5 1/ha =1.0 gal/a; 1.1
kg(AI)/ha =1.0 lb(AI)/a.
Numbers followed by the same letter are not significantly
different (P = 0.05; Duncan's [1955] multiple range test).
Calculated by Abbott's (1925) formula.
247
-------
TABLE 12
Percent mortality and percent confirmed infection of adult SL acletus confined on filter paper
innoculated with various rates of NL carpocapsae "Mexic
R&D Center, Boynton Beach, FL, 26 Dec 85.
Treatment
N. c. 'Mexican'
N. c. 'All'
N. b. 'SN'
N. b. 'SN'+X77
Check
Rate Replicate
(nemas/dish)
10,000
5,000
1,000
100
10,000
5,000
1,000
10,000
5,000
1,000
100
1,000
8
9
10
10
5
5
5
9
8
9
10
7
10
an"or "AlP'or N.
bibionis "sn".ChemLawn
s % Mortality %
4 DAT
100
89
60
70
80
100
60
56
63
67
50
100
10
6 DAT
100
89
60
70
100
100
60
56
75
78
60
100
10
Infected
88
67
50
40
80
80
60
56
38
89
20
14
—
N- c. = Neoaplectana carpocapsae. N. b. = N. bibionis
Based on dead insects with various stages of nematodes in body
cavity compared to number of replicates.
X77 = Ortho X-77® spreader, Chevron Chemical Co., 0.3 ml/1.
248
-------
TABLE 13
Application of entomophageous nematodes to area A for mole cricket control, 11/.V/85 and
evaluated one week later. -, «iu
Treatment
H. h.
H. h.
N. c.
N. c.
Check
H. h
'NC'
'NC'
'Mexican'
'Mexican1
^— tI^4"^>"^M
• JL At* V^ >?^L ^^ J
Rate
nemas/ha
12.4X109
2.5X109
12.4X109
2.5X109
rhabditis
X Mole Cricket
Pre-treat
96
64
89
60
83
heliothidis; N. c.
Mounds/ Plot
7 DAT %
87
63
42
42
85
= Neoaplectana
Control
9%
2%
53%
30%
carpocapsae
2.5xl09 nemas/ha = l.OxlO9 nemas/a; 12.4X109 nemas/ha = 5.0xl09
nemas/a
Calculated using Abbott's (1925) formula.
249
-------
TABLE 14
Application of entomophagous nematodes to area B for mole cricket control, 12/iv/85, and
evaluated 6 days later.
Rate X Mole Cricket Mounds/Transect
Treatment nemas/ha Pre-treat 6 DAT % Control
H. h. 'NC1 7.4X109 53 53 0
N. c. 'Mexican' 7.4xl09 28 15 42
Check 28 26
H. h* = Heterorhabditis heliothidis; N. c. = Neoaplectana
carpocapsae
7.4xl09 nemas/ha = 3.0xl09 nemas/a
Calculated using Abbott's (1925) formula.
250
-------
TABLE 15
Application of entomophagous nematodes for mole cricket control, 27/iv/85, and evaluated
11 and 19 days later.
Treatment
Rate
nemas/ha
X Mole Cricket Mounds/Plot
Pre-treat 11 DAT 19 DAT
% Control
N. c. 'Mexican'
N. c. 'Mexican1
Isofenphos 21
Check
12.4X109
4.9X109
2.24 kg(AI)ha
51.4
61.6
35.6
70.0
62.4 72.4
67.2 78.0
55.2 34.2 4
60.6 74.0
N. c. = Neoaplectana carpocapsae; Isofenfos = Oftanol® (Mobay
Chemical Company)
12.4xl09 nema/ha = S.OxlO9 nemas/a; 4.9xl09 nemas/ha = 2.0xl09
nemas/a; 2.24 kg(AI)ha =2.0 lb(AI)/a
Calculated using Abbott's (1925) formula.
251
-------
TABLE 16
Petri dish evaluation of entomogenous nematodes for infection of a range crane fly (Tipula
spp.) larvae.
Treatment
23/iv/86 Nemas/dish
N. b.
N. c. 'Mexican1
N. c. 'All'
H. h. 'NC1
Check
200
400
200
400
200
400
200
400
% Mortality (N =
2 DAT 4 DAT
20
0
0
20
0
0
0
20
0
20
20
40
40
20
40
40
40
0
= 15)
8 DAT
80
100
100
100
80
100
100
100
0
N.
= Neoaplectana
Heterorhabditis heliothidis.
N. c. = N. carpocapsae; H. h. =
262
-------
FIGURE 1
Pooled average wax moth larval mortality (N=5) for 3, 5, and 11 days after treatment (DAT)
at two soil depths (2.5 and 5.0 cm) followed by different amounts of irrigation (cm).
4 -
CO
CO
*
<
2 -
0
5DAT 2.5cm
3DAT 5.0cm
3DAT 2.5cm
5DAT 5.0cm
1 1DAT 5.0cm
11 DAT 2.5cm
0.00
0.64 1.27
Irrigation Applied (cm)
2.54
253
-------
254
-------
BIOLOGICAL CONTROL OF SOCIAL INSECTS WITH
NEMATODES
George O. Polnar, Jr.
Department of Entomological Sciences
University of California,
Berkeley, CA 94720
and
Ramon Georgls
Biosys
1057 E. Meadow Circle
Palo Alto, CA 94303
INTRODUCTION
For the present review, social insects are meant to comprise bees, wasps and ants of the order
Hymenoptera and termites of the order Isoptera. Various diverse groups of nematodes are
associated with these insects in nature (Poinar, 1975, Bedding, 1986), either as phoretics,
facultative or obligate parasites. However, our discussion will be restricted to those nematodes
which show potential in regulating these insects in specialized habitats and which can be
manipulated by man to serve as biological control agents. The nematodes which fit these categories
today belong to the genera Neoaplectana and Steinernema of the Steinernematidae and
Heterorhabditis of the Heterorhabditidae.
TERMITES
In the world today, there are some 2000 species of termites that are distributed into six families.
On the basis of their habits, termites have been placed into ecological groups which include the
drywood termites (Kalotermitidae) which live in dry wood and have little or no contact with soil, the
dampwood termites (Hodotermitidae) which live in buried timber or rotting logs and the subterranean
termites (Rhinotermitidae) which construct their nests in the soil and build protective shelter tubes
when searching for food above ground (Edwards & Mill, 1986). Since the subterranean termites
rely principally on the soil for moisture, they are potential hosts for steinernematid and
heterorhabditid nematodes. Laboratory studies showed that Neoaplectana carpocapsae could kill
workers of Coptotermes. Nasutitermes and Termes (in Poinar, 1979) and Georgis et al (1982)
reported 96-98% mortality (N=10) of Zootermopsis and Reticulitermes three days after being placed
in standard petri dishes with 2000 infective stage N. carpocapsae (Breton strain) (Fig. 1, 2) as well
as Heterorhabditis heliothidis. respectively.
The next step was to test the effectiveness of these nematodes in the field. Some initial studies
using the DD-136 strain of hL carpocapsae against the Formosan termite Coptotermes formosanus
255
-------
were reported by Reese (1971). In these studies, large numbers of termites were trapped, infected
with nematodes, and returned to the colonies. The lack of success was attributed to the large
number of termites in a single colony, and because the termites in some colonies would recognize
infected workers, then collect and isolate them behind earthen barriers. This behavior was only
observed in some colonies however and it is not known if such actions constitute serious threats
to the use of nematodes against subterranean termites.
In 1981, Bedding and Stanfield reported that by baiting with a species of Heterorhabditis
obtained from Australia, large laboratory colonies of Mastotermes were totally eradicated within a
week. Nematode suspensions were applied to termite-infested Pinus carabea plantations near
Darwin. Nematode-infected termites were recovered from neighboring untreated trees within one
week after treatment. Each termite cadaver yielded about 10,000 nematodes and dead termites
were not walled off sufficiently to prevent exit of nematode progeny nor eaten by other termites or
associated mites. However, the investigators noted that there was a tendency for the termites to
vacate trees that had received nematode applications.
In 1985, Mix reported studies conducted by R. Beal in Mississippi. Beal placed nematodes at
rates of 5,000 to 40,000/foot2 in a pine forest and placed pine boards over the treated area. The
area was heavily infested with subterranean termites and as the termites were attracted to the
boards, they would encounter the nematodes. The boards were examined after one and two months
and the damage rated as percent of termite attack to the pine boards (see table 1). Although no
chemical treatment was applied for this experiment, the results reveal two interesting points. The
results are variable, however there is evidence that some nematode species and strains are more
effective against termites than others. This variability in susceptibility was also demonstrated using
Neoaplectana carpocapsae (All strain) and Heterorhabditis heliothidis (NC strain) in petri dish
experiments against Reticulitermes hesperus. Using a similar dose. N. carpocapsae killed the same
number of termites twice as quickly as hL heliothidis (Mangan & Miller, 1986). Secondly, although
Mix said that "There was no kill," the 40,000 applications of the Breton strain of N. carpocapsae
definitely did exhibit some "kill"and although it was not complete, it was better than the untreated
control. Also, it should be noted that even a dose of 40,000 nematodes per square foot is extremely
low to be used against an infinite supply of termites coming out of the soil.
When used against subterranean termites attacking dwellings, some success with the
nematodes was reported. Olkowski et al (1985) reported on data supplied by Post and Drucker, two
pest control operators who distributed SAF-T-SHIELD, a product composed of Neoaplectana
carpocapsae. On the basis of treating 4000 structures, they reported that the success rate for the
nematodes was about 80%, compared to a 92% maximum success rate with chlordane. Post
emphasized that it was very important to use a high dose, have adequate moisture and to position
the nematodes as close to the structure as possible. Hall (1986) reported the experiences of Paul
Leek, a pest control operator in Pennsylvania. Leek treated some 38-40 houses with nematodes
and had a call back rate of only 13 percent (87% success).
Using a Heterorhabditis isolate from Darwin, Australia, Danthanarayana and Vitarana (1987)
successfully controlled the live-wood tea termite, Glyptotermes dilatatus infesting tea plants in Sri
Lanka. The nematodes were applied to 50 tea bushes with a pipette inserted into the galleries inside
exposed stems at a rate of 240,000 nemas per bush. At periodic intervals, the plants were uprooted
and examined to count living and nematode-infected individuals (see Table 2). Equally good results
were obtained using a pressurized knapsack sprayer with a hypodermic needle in place of the
nozzle. About 1000 infective stage juveniles were produced in each of 32 parasitized termites after
256
-------
8 days. The authors concluded that the nematodes from such cadavers parasitized healthy termites,
thus establishing a chain infection. Termite colonies were annihilated within 2-3 months with a
single nematode application, thus convincing the authors that these nematodes could be used to
control the tea termite in Sri Lanka.
A recent study tested the efficacy of Neoaplectana carpocapsae against foraging workers of
Reticulitermes tibialis in a pasture in Colorado (Epsky & Capinera, 1988). The nematodes were
applied to the soil at a rate of 1 x 107 per m2 directly beneath the baited traps. There was a significant
decrease in number of termites per trap between treated and untreated traps and protection was
provided for a period of 2-3 weeks.
A general assessment of the above reports concerning the effect of nematodes on
subterranean termites suggests several points. First, that it is difficult to compare results obtained
experimentally in field conditions (often with infinite numbers of termites) with situations associated
with controlling termites in structures (where the number of termites may be large, but finite).
Second, that although results reported by pest control operators who understand how to work with
biological organisms and apply adequate numbers of nematodes in choice areas, appear promising,
quantitative data on the number of termites killed and colony reduction is still lacking. Such data is
necessary before any official statement can be made regarding the effectiveness of neoaplectanid
nematodes in controlling subterranean termites in structures.
FORMICIDAE
Ants, as Aculeate Hymenoptera, have the ability to sting and this fact, coupled with damage they
do in constructing their nests in human dwellings, is why control measures are sometimes
necessary.
Early studies showed that under laboratory conditions, Neoaplectana carpocapsae was able
to infect adults of the fire ant, Solenopsis geminata. larvae and adults of Camponotus spp., larvae,
pupae and adults of the parasol ant, Acromyrmex octospinosus (Reich) (Kermarrec, 1975; Laumond
et al, 1979) and workers of Myrmica and Camponotus (Bedding, 1984). (Figure 3).
Some interesting aspects of the association between hJ.. carpocapsae and A. octospinosus
were discussed in a later work (Kermarrec et al, 1986). There appeared to be some host resistance
to nematode penetration in mature pupae and adult ants. Besides a decline in penetration, there
was also a decrease in nematode development. Whereas penetration and development to the adult
stage occurred in 95-100% of the third and fourth stage larvae, penetration in older pupae dropped
to 5% and only 10% of these parasitized pupae contained nematode adults. Although adult ants
were killed none contained developing stages of the nematodes. When three million infectives of
N. carpocapsae were introduced into the fungus gardens of the ants, intense social grooming,
together with cleaning and building activities resulted in the elimination of the nematodes after ten
days.
Kermarrec et al (1986) point out some aspects to consider when infecting ants with nematodes.
If the ant contains an infra-buccal filter, then this device may retain nematodes in the infra-buccal
pocket and not allow them to enter the pre-pharynx. Such a filtering device is usually absent in ant
larvae. If this device is effective in adult ants, then the nematodes would have to enter the buccal
area and force themselves through the pharyngeal glands to enter the hemocoel. Aside from
opening size, other barriers hindering nematode infection in adult ants could be spinules in the
spiracular chamber, closure of the mouth and pilosity around the anus.
257
-------
In 1976, Poole completed a study on the use of Neoaplectana carpocapsae (=NL dutkyi) to
control the fire ants, Soienopsis richteri and S.. invicta in Mississippi. Reproductives and brood of
both species were susceptible to infection. Under laboratory conditions after 48 hrs, a mean dose
of 20 nematodes/inch3 resulted in 50% larval mortality, a mean dose of 31 infective juveniles/inch3
resulted in 50% pupal mortality and a mean dose of 109 nematodes/inch3 produced 50% mortality
of winged males and females. Poole found that the workers were less susceptible than the other
stages and could only achieve 50% mortality of media workers when a mean dose of 880,000
nematodes/inch3 was used. A dose of 9,100,000 nematodes/inch3 was required to produce 50%
mortality of the minor workers after 48 hrs. It was concluded that the nematodes entered the adult
ants per o_s_.
Using a concentration of 1 million nematodes per mound in the fall, the nematodes were
capable of causing 35% mortality (12% worker infection) up to 90 days post-treatment, reducing the
mound size by 18%. With the same concentration in the spring, 80% mortality was recorded (22%
worker infection) and the mound size was reduced by 28%. Greater colony mortality was achieved
against smaller colonies. In field tests against fL richteri. the nematodes destroyed 80% of the
mounds in the spring and 36% of the mounds in the fall.
Reasons why the workers were infected less than other stages were their greater overall
activity and grooming behavior. Also, workers regurgitated introduced nematodes to the alates and
larvae. A single winged male or female ant could produce up to 3,000 infective stage juveniles.
Poole concluded by stating that Neoaplectana would be an effective biological agent in the
control of the imported fire ants if timing of the application, mound size and climatic conditions were
taken into consideration.
In 1980, Quattlebaum reported on tests with the DD-136 strain of NL carpocapsae and the
NC strain of HL heliothidis on mounds of the red imported fire ant, S, invicta and the black imported
fire ant, & richteri. in Boykin and Bounan Counties in South Carolina. Quattlebaum used a 2-gallon
compressed air sprayer calibrated to deliver 300 ml/20 sec. in applying the nematodes to the
mounds. A vertical hole 2 inches in diameter and 12-24 inches deep was made into the center of
the mound. The sprayer wand was inserted into the mound and discharged for 20 sec. Check
mounds were sprayed with water. Assays were based on ant and mound mortality or the percentage
of inactive mounds in a plot. Mounds were considered active if any living ants were found associated
with them. Mortality was determined by holding fire ants from treated mounds in large vials 24h
post-treatment and recording the number that died after 4 days. Control ants were taken from the
water-treated mounds. The results of two years' tests are shown in Tables 3 and 4.
Quattlebaum (1980) concluded that both N. carpocapsae (DD-136) and H. heliothidis (NC-19)
were able to reduce field populations of the red imported fire ant (S. invicta). Of the two nematodes,
R carpocapsae gave the best control. Quattlebaum (1980) felt that this might be the quicker
reproductive cycle of Neoaplectana in the nest, thus releasing more infective nematodes. He also
noted that results varied under conditions of different soil texture (sand versus silt) and it would be
desirable to note this condition in further field testing. In combining NL carpocapsae (DD-136) with
various insecticides (Sevin, Pennwalt, Knox-out and Orthene) in field tests against S, invicta.
Quattlebaum (1980) found that a synergistic interaction often occurred between insecticides and
nematodes. In these experiments a mound mortality of only 37.5% was recorded when the
nematodes (N, carpocapsae DD-136) were used alone at a rate of a 1 X 106 per mound. Recent
studies by Georgis (1987) show that desiccated nematodes (N. carpocapsae All) in a sugar solution
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were infective to carpenter and harvester ants. Such formulations might be successful against fire
ants also.
BEES AND WASPS
Bees and wasps of the Aculeate Hymenoptera have the ability to sting and it is primarily this
character which necessitates their occasional control. It is mainly the social species of bees and
wasps that cause concern, the latter especially are attracted to food and produce.
Bees
Bees are beneficial to man and are tested with biological insecticides for compatibility studies
so that the agents could be used against insect pests in the bee's environment.
Whereas original reports indicated that honeybee adults were resistant to Neoaplectana
carpocapsae (Dutky & Hough, 1955; Cantwell et al, 1972), Hackett & Poinar (1973) showed that
adult worker honeybees could be parasitized and killed when infectives of NL carpocapsae were
added to sugar solutions, honey or a fruit concentrate which were fed to bees. The authors
suggested that nematode baits placed outdoors for yellowjackets should be unattractive to
honeybees. Kaya et al (1982) tested N. carpocapsae against worker and brood stages by spraying
infective juveniles on frames in bee hives. They observed adult worker mortality but larvae and
pupae were not infected. Absence of parasitism in the brood was attributed to temperature ranges
between 33.3 and 35.2 C, which was detrimental to the infective stages. Desiccation of the infectives
under hive conditions of high temperature and low relative humidity (40-78%) was also considered
to act as a nematode mortality factor. The conclusions of the study were that general spraying of
nematodes in the vicinity of the hive and even direct spraying of the hive might kill some bees but
would not be detrimental to the colony. If some worker bees did become infected, they would be
removed and the nematodes would not be able to recycle in the hive. To reduce exposure of bees
to nematodes applied to the environment, applications could be done at times when the bees were
still in their hives (early morning or in the evening).
Yellowjackets
Representatives of the subfamily Vespinae of the family Vespidae include yellowjackets and
hornets of the genera Vespula and Paravespula. Yellowjackets in particular can constitute a serious
problem because of their attraction to foodstuffs (sweet sources or high protein substances
depending on the season). Although human deaths from yellowjacket stings in the United States
are rare (Parrish, 1963), the discomfort felt, especially by hypersensitive individuals, may be
considerable. In 1968, an estimated loss of $200,000 due to the action of Vespula spp. in agricultural
operations was reported just in California (Hawthorne, 1969). Although natural infections of
Vespinae by rhabditid nematodes would be unexpected, Bedding (1984) reports discovering a
queen Vespuia germanica infected with hL carpocapsae. hibernating beneath Eucalyptus bark in
Tasmania.
Initial studies showed that workers of Vespula pennsylvanica. V, rufa atropilosa and \A vulgaris
are killed by the infectives of several strains of JSL carpocapsae as well as K heliothidis (Poinar &
Ennik, 1972; Gambino, 1984).
There are two basic methods of applying neoaplectanid nematodes to control yellowjackets.
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One is to apply the nematodes directly to the nest, the other is to attract yellowjacket workers to
nematode-treated baits.
Preliminary studies relating to the latter method were reported by Poinar and Ennik (1972)
when they showed that the workers of V, pennsylvanica and V, rufa atropilosa from California and
Vespula sp. from the Netherlands could be killed when they Ingested infective stages of NL
carpocapsae (Agriotos strain) placed in a fruit concentrate or on sugar cubes. In order to avoid
attracting honeybees, the bait could be composed of a protein base such as tuna or other pet foods.
Such baits containing insecticides have been successful in controlling yellowjackets in the field
(Ennik, 1973; Reid & MacDonald, 1986). If contamination was a problem, then utilizing synthetic
lures to attract the yellowjackets might be feasible (Davis et al, 1973).
The problem of nematodes drying out and dying in the baits could be alleviated by using
desiccated nematodes that revive when ingested by the hosts. Such desiccated nematodes have
been shown to be infective to \A pennsylvanica workers (Wojcik & Georgis, 1987).
Introduction of aqueous suspensions of R carpocapsae into colonies of mixed populations of
\A pennsylvanica and E. vulqaris in California were performed by removing some of the overlying
soil and making a hole in the exposed nest envelope (Gambino & Pierluisi, 1987). The water
suspension of infective nematodes was poured in through the hole. Thirty-six hours after treatment,
the authors caught insects that were being carried out of the treated colonies by yellowjacket
workers. Seventy percent of these insects (both adults and larvae) had been parasitized by NL
carpocapsae. Prompt removal of infected individuals by healthy nestmates would eliminate recycling
of the nematodes and reduce their effectiveness.
CONCLUSION
The use of nematodes for the control of social insects is beset with two difficulties. The first is
how to introduce the nematodes into the colony which may be concealed (termites, wasps) or have
a relatively small opening (ants). The other is how to establish cycling of the nematodes in diseased
members of the colony when the instinct of the workers is to avoid the diseased forms (termites)
or to remove them from the nest (wasps, ants).
Thus, either a heavy dose must be used in or near the colony in order to kill enough of the
workers or brood to reduce and hopefully eventually eliminate colony activity or a nematode-treated
bait be used that the workers will take and feed to the developing brood. Attempts at killing the
queen may be difficult and successful only in single queen colonies where new queens are not
readily produced. New types of formulation, such as embedding the nematodes in calcium alginate
together with an attractant (Poinar et al., 1985) or utilizing desiccated nematodes in baits (Georgis,
1987) may result in innovative delivery systems that could be used against social insects.
The success of these efforts will depend on the ingenuity of the researcher in understanding
the biology and behavior of the insects involved in order to utilize the nematodes effectively in any
control program.
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REFERENCES
Bedding, R.A. 1984. Nematode parasites of Hymenoptera. In: Nickle, WR. "Plantand Insect Nematodes."Marcel Dekker
N.Y. 755-795.
Bedding, R.A. and M. Stanfield. 1981. Nematodes for insect control. Mastotermes. In: CSIRO Division of Entomoloav
Ann. Rpt. 1979-80.
Cantwell, G.E., T. Lehnert and J. Fowler. 1972. Are biological insecticides harmful to the honey bee? Amer Bee J
112:255-258.
Danthanarayana, W. and S.I. Vitarana. 1987. Control of the live-wood tea termite, Glvptotermes dilatatus using
Heterorhabditis sp. (Nemat.). Agr., Ecosyst. Environ. 19:333-342.
Davis, H.G., R.W. Zwick, W.M. Rogoff, T.P. McGovern and M. Beroza. 1973. Perimeter traps baited with synthetic lures
for suppression of yellow-jackets in fruit orchards. Environ. Entom. 2:569-571.
Dutky, S.R. and W.S. Hough. 1955. Note on a parasitic nematode from codling moth larvae, Carpocapsa pomonella.
Proc. Ent. Soc. Wash. 57:244.
Edwards, R. and A.E. Mill. 1986. Termites in buildings. Rentokil Ltd., 261 pp.
Ennik, F. 1973. Abatement of yellowjackets using encapsulated formulations of Diazinon and Rabon. J. Econ. Entomol.
66:1097-1098.
Epsky, N.O. and J.L. Capinera. 1988. Efficacy of the entomogenous nematode Steinernema feltiae against a
subterranean termite. Reticulitermis tibialis (Isoptera: Rhinotermrtidae). J. Econ. Entomol 81:1313-1317.
Gambino, P. 1984. Susceptibility of the western yellowjacket Vespula pennsylvanica to three species of entomogenous
nematodes. IRCS Medical Sci. 12:264.
Gambino, P. and G. J. Pierluisi. 1987. Eusocial Paravespula wasps remove diseased nestmates from the colony.
Unpublished report. 9 p.
Georgis, R. 1987. Nematodes for biological control of urban insects. Amer. Chem. Soc.-Div. Environ. Chem. 194th Natl.
Mtg., New Orleans, LA 27:816-821.
Georgis, R., G.O. Poinar, Jr. and A.P. Wilson. 1982. Susceptibility of damp-wood termites and soil and wood-dwelling
termites to the entomogenous nematode, Neoaplectana carpocapsae. IRCS Med. Sci. 10:563.
Hackett, K.J. and G.O. Poinar, Jr. 1973. The ability of Neoaplectana carpocapsae Weiser (Steinernematidae:
Rhabdrtoidea) to infect adult honeybees (Apis mellifera. Apidae: Hymenoptera). Amer. Bee Journal 113:100.
Hall, R. 1986. Down but not out. Pest Control 54:60-62, 91-92.
Hawthorne, R.M. 1969. Estimated damage and crop loss caused by insect/mite pests - 1968. California Dept. of
Agriculture. Bureau of Entomology, unpublished report, 11 pp.
Kaya, H.K., J.M. Marston, J.E. Lindegren and Y.-S. Peng. 1982. Low susceptibility of the honey bee, Apjs mellifera L
(Hymenoptera: Apidae) to the entomogenous nematode, Neoaplectana carpocapsae Weiser. Environ. Entomol.
11:920-924.
Kermarrec, A. 1975. Etude des relations synecologiques entre les nematodes et la fourmi-manioc: Acromyrmex
octospinosus ReiclvAnn. Zool.-Ecol. Anim. 7:27-44.
Kermarrec, A., G. Febvay and M. Decharme. 1986. Protection of leaf-cutting ants from biohazards: Is there a future for
microbiological control? In: Fire Ants and Leaf-Cutting Ants. Eds. C.S. Lofgren & R.K. Van der Meer. Westview
Press, Boulder, pp. 339-356.
Laumond, C., H. Mauleon & A. Kermarrec. 1979. Donnees nouvelles sur le spectre d'hotes et le parasitisme du nematode
entomophage Neoaplectana carpocapsae. Entomophaga 24:13-27.
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Mangan, D. and R. Miller. 1986. Biosys unpublished report. 2 pp.
Mix, J. 1985. Seal's research shows nematodes don't control subterranean termites. Pest Control 53:22-23.
Parrish, H.M. 1963. Analysis of 460 fatalities from venomous animals in the United States. Amer. J. Med. Sci. 36:129-140.
Poinar, Jr., G.0.1979. Nematodes for biological control of insects. CRC Press, Boca Raton, Florida. 277 pp.
Poinar, Jr., G.O. and F. Ennik. 1972. The use of Neoaplectana carpocapsae (Steinernematidae: Rhabditoidea) against
adult yellowjackets (Vespula spp.. Vespidae: Hymenoptera). J. Invert. Path. 19:331-334.
Poinar, Jr., G.O., G.M. Thomas, K.C. Lin and P. Mookerjee. 1985. Feasibility of embedding parasitic nematodes in
hydrogels for insect control. IRCS Med. Sci. 13:754-755.
Poole, M.A. 1976. Survey and control efficacy of endoparasites of Solenopsis richteri Forel and Solenopsis invicta Buren
in Mississippi. Ph.D. thesis. Mississippi State University, Mississippi State. 83 pp.
Reese, K.M. 1971. Navy fights Formosan termite in Hawaii. Chem. & Engineer. News (Oct. 11). p.52.
Reid, B.L. and J.F. MacDonald. 1986. Influence of meat texture and toxicants upon bait collection by the German
Yellowjacket (Hymenoptera: Vepsidae). J. Econ. Entomol. 79:50-53.
Wojcik, W.F. and R. Georgis. 1987. Infection of selected insect species with desiccated Steinernema feltiae (Nematoda).
Abst. Soc. Invert. Path. 20th Ann. Meeting, July 20-24,1987, Gainesville, Florida, p.77.
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TABLE 1
Percentage of damage caused by subterranean termites to pine boards placed over areas
treated with Neoaplectana and Heterorhabditis. respectively (modified from Mix, 1985).
Nematode
Dosage
(sq. ft.)
Percent of Damage
1 month 2 months
Heterorhabditis sp.
(HP88)
N. carpocapsae
(Breton)
N. carpocapsae
(Mexican)
ft
•I
5,000
60
80
Untreated Control
20,000
40,000
5,000
20,000
40,000
5,000
20,000
40,000
•••
60
80
40
20
20
40
80
80
40
60
100
100
100
60
80
100
60
100
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TABLE 2
Mortality of the live-wood tea termite, Glyptotermes dilatatus after applying Heterorhabditis sp.
to tea bushes at a rate of 240,000 nemas per plant (modified from Danthanarayana and Vitarana
(1987)).
Treatment
Control
Days after
application
Total number
of termites
per plant
Percentage
dead
Total number
of termites
Percentage
dead
10
15
31
50
95
354
291
379
9
6
92
76
81
100 380
100 773
-
-
-
16
17
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TABLE 3
Mortality of fire ant (£L invicta) mounds treated with the DD-136 strain of fL carpocapsae
(approximate figures obtained from Figures 6 and 7 of Quattelbaum (1980)).
% Mortality Z Mortality
(nematodes/mound) after 30 days after 180 days
Control 7A (5)B 15 (9)
0.5 x 106 57 (55) 72 (81)
1 x 106 85 (68) 93 (86)
2 x 106 100 (97) 99 (98)
A * numbers represent 1978 tests.
B * numbers in parentheses represent 1979 tests,
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TABLE 4
Mortality of fire ant (S, invicta) mounds treated with the NC-19 strain of Heterorhabditis
heliothidis (approximate figures obtained from Figures 8 and 9 of Quattelbaum (1980)).
Dose % Mortality Z Mortality
(nemat odes /mound) after 30 days after 180 days
Control 6* (5)B 12 (9)
0.5 x 106 - (40) - (52)
1 x 106 64 (69) 64 (70)
2 x 10° 89 (80) 89 (82)
A • numbers represent 1978 tests.
B » numbers in parentheses represent 1979 tests
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FIGURE 1
A worker of Reticulitermes surrounded by infective stages of Neoaplectana carpocapsae.
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FIGURE 2
Developing stages and adults of Neoaplectana carpocapsae removed from the body cavity of
an infected Reticulitermes.
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FIGURE 3
Fire ant queen surrounded by developing stages of Neoaplectana carpocapsae removed from
the host's hemocoel. Specimen courtesy of Brad Vinson, under whose direction the fire ant control
program with entomogenous nematodes is being conducted.
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270
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SECTION VI
Manual of Current Practices for
Control of Turfgrass Diseases,
Insects and Poa Annua
271
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SYMPTOMATOLOGY AND MANAGEMENT OF COMMON
TURFGRASS DISEASES IN TRANSITION ZONE AND
NORTHERN REGIONS
Peter H. Dernoeden, Ph.D
Department of Agronomy
The University of Maryland
College Park, MD 20742
INTRODUCTION
Most turfgrass diseases are caused by pathogenic fungi that invade leaves, stems and roots
of plants. As a result of the injurious effects of a disease, the plant will exhibit various symptoms
such as leaf spots, root rots or death of leaves, tillers or entire plants. Sometimes these fungi
produce visible signs such as mushrooms; white powdery mildew; white, fluffy mycelial growth; pink
gelatinous mycelial growth; red or black pustules on leaves, etc. Mycelium is the vegetative body
of a fungus that is composed of a network of fine tubes that often appear cottony. It is through the
use of these symptoms and signs that disease problems are diagnosed. Time of year and turfgrass
species also provide important clues in diagnosing diseases. For example, brown patch and Pythium
blight are seldom a problem when night temperatures fall below 65F, and Pythium blight does not
cause severe injury to mature stands of Kentucky bluegrass. Conversely, dollar spot tends to be
more damaging under conditions of cooler nighttime temperatures in late spring and early fall than
during the hottest weeks of summer. Summer patch is strictly a high temperature, summer disease
of Kentucky bluegrass, fine leaf fescues and annual bluegrass. Species such as perennial ryegrass,
creeping bentgrass and tall fescue are resistant to summer patch.
Most turfgrass diseases are caused by fungi rather than bacteria or viruses. In the pages to
follow, the most common fungal diseases of turfgrasses, as well as plant parasitic nematodes, are
described and cultural and chemical approaches to their management are outlined. A more complete
list of turfgrass diseases, hosts and pathogens is provided in Table 1.
SPRING AND FALL DISEASES
DOLLAR SPOT
The dollar spot pathogen (Sclerotinia homoeocarpa) is widespread and extremely destructive
to turfgrasses. The disease is known to attack most turfgrass species including annual bluegrass,
bentgrasses, red fescue, Kentucky bluegrass, perennial ryegrass, bermudagrass, zoysiagrass,
centipedegrass and St. Augustinegrass. The symptomatic pattern of dollar spot varies with turfgrass
species and management practices. Under close mowing conditions, as with intensively maintained
bentgrass or zoysiagrass, the disease first appears as small, circular, straw-colored spots of blighted
turfgrass about the size of a silver dollar. With coarser textured grasses such as Kentucky bluegrass
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or perennial ryegrass suited to higher mowing practices, the blighted areas are considerably larger,
irregularly-shaped, straw-colored patches three to six inches in diameter. Affected patches
frequently coalesce and involve large areas of turf. Grass blades often have straw-colored or
bleached-white lesions shaped like an hour glass. The hour glass banding on the leaves is often
made more obvious by a definite narrow brown, purple, or black band which borders the bleached
sections of the lesion from the remaining green portions. When the fungus is active and moisture
is present, a fine, cobwebby mycelium may cover the diseased patches during early morning hours.
Disease severity has peak periods in late spring-early summer and again late summer-early fall. In
the upper Midwest, however, the disease tends to be most damaging during autumn. Dollar spot
can remain active during mild periods throughout fall and into early winter in some regions.
There are at least two strains of the dollar spot fungus, (referred to tentatively as species of
Moellerodiscus and Lanzia) which may account for the ability of the disease to be damaging during
cool and warm periods. Presently, the taxonomy of the two strains is imperfectly understood. Dollar
spot tends to be most damaging in poorly nourished turfs, particularly if soils are dry but when
humidity is high or when a heavy dew is present. Avoiding drought stress, watering deeply during
daytime hours, maintaining a balanced N-P-K fertility program, and controlling thatch and
compaction are cultural approaches that minimize dollar spot injury. Except for maneb, mancozeb
and thiram, most fungicides effectively control dollar spot.
HELMINTHOSPORIUM LEAF SPOT and MELTING OUT
Many of the fungi that cause leaf spotting and melting-out diseases of turf grasses were once
assigned to the genus Helminthosporium. Today, these fungi are more appropriately referred to as
species of Drechslera or Bipolaris. but the common name of the diseases they cause remains
Helminthosporium leaf spot, melting-out or netblotch.
Among the most important spring and autumn diseases of Kentucky bluegrass is leaf spot,
which is caused by Drechslera poae. This disease is not as devastating as it once was because of
the development and widespread use of resistant bluegrass cultivars. South Dakota, Kenblue, Park
and other "common"types of Kentucky bluegrass are very susceptible to leaf spot. The common
types, which generally survive extreme environmental stresses, are still used today as components
of bluegrass blends in some regions of the U.S. because they lend genetic diversity to the stand.
Drechslera poae is a cool weather pathogen that is most active during the spring (especially
April and May), autumn (especially September and October), and throughout mild winter periods.
CX poae causes disease that may occur in two phases: the leaf spot phase, and the melting-out
phase. Typically, distinct purplish-brown leaf spot lesions with a central tan spot are produced on
the leaves of affected plants. In a heavily infected stand, the turf appears yellow or red-brown in
color when observed from a standing position. During favorable disease conditions, lesions may
increase in size to encompass the entire width of the blade causing a die-back from the tip. Leaf
spot lesions are initially associated with older leaves, which die prematurely as a result of the
invasion. If favorable environmental conditions for disease continue, particularly overcast, cool and
drizzling weather, successive layers of leaf sheaths are penetrated, and the crown is invaded. Once
the crown is invaded the disease enters the melting-out phase. During this phase, entire tillers are
lost, and the turf loses density. Hence, it is the melting-out phase that is most damaging to the sward.
Net-blotch disease of tall fescue and perennial ryegrass is caused by another of the
helminthosporia, Drechslera dictyoides. IX dictyoides is also a cool, wet weather pathogen that
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attacks turf primarily during cool and moist periods of spring and fall. Initially, symptoms appear as
minute, purple-brown specks on leaves. As the disease progresses, a dark brown, net-like pattern
of necrotic lesions develop on tall fescue. These net blotches may coalesce, leaves turn brown or
yellow, and die-back from the tip. On leaves of perennial ryegrass, numerous oblong, brown lesions
are produced. Under ideal environmental conditions the fungus may invade crowns and roots,
causing a melting out of the stand. Both diseases can be active during relatively warm, rainy periods
of winter.
Cultural practices that minimize injury from leaf spot or melting-out diseases are as follows:
raise the mowing height; avoid spring and summer applications of water soluble nitrogen fertilizers;
avoid light, frequent irrigations; control thatch; overseed with resistant cultivars; and avoid the use
of broadleaf, phenoxy herbicides during periods when these diseases are active. Fungicides that
effectively control leaf spot disease include anilazine, chlorothalonil, iprodione and maneb.
SPRING DEAD SPOT
Spring dead spot (SDS) is perhaps the most damaging disease of bermudagrass turf and is
caused by Leptosphaeria korrae and possibly other fungi. As the name implies, SDS injury becomes
apparent in the spring. The actual infection, however, may begin as early as autumn, but root injury
by the pathogen becomes rapid prior to spring green-up, during late winter or early spring. As
bermudagrass breaks dormancy, circular patches of brown, sunken turf two inches to three feet in
diameter become conspicuous. Rhizomes and stolons from nearby, healthy plants eventually
spread into and cover the dead patches. This filling-in process is slow, a period which may last four
to eight weeks following spring green-up. The slow filling process is believed to be due to toxic
substances generated in the soil below the dead patches. Weeds commonly invade the dead
patches. These weeds should be controlled to reduce competition with the bermudagrass and
thereby speed up the recovery process.
Spring dead spot is most commonly associated with mature bermudagrass turfs older than
three years. The disease, however, may appear the spring following sprigging with stolons from sites
that previously had SDS. SDS injury is most likely to occur where thick thatch layers exist and where
nitrogen fertilizers have been heavily applied during late summer. Benomyl and fenarimol applied
in late September help alleviate SDS. Ammonium sulfate (applied at 1.0 Ib N/1000 ft) and other
water soluble nitrogen fertilizers plus potassium (applied at 1.0 Ib K/1000 ft) applied on monthly
intervals from mid-May to mid-August speed the recovery of turf injured by SDS.
NECROTIC RING SPOT
Necrotic ring spot (MRS) is a newly described disease of Kentucky bluegrass and is caused
by Leptosphaeria korrae. Although newly described, MRS probably has been around for some time,
but has been confused with Fusarium blight.
Necrotic ring spot was first suspected as being a new disease in Wisconsin, where the fungicide
triadimefon had been applied unsuccessfully to control what was believed to be Fusarium blight.
Unlike Fusarium blight, NRS primarily is a cool, wet weather disease of spring and fall. Fusarium
blight and another recently described patch disease that mimics Fusarium blight, summer patch,
are both high-temperature diseases of summer. The confusion over NRS, summer patch and
Fusarium blight has occurred because all three diseases can appear as rings of dead grass with
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living turf in the center. To date, NRS has been observed mainly in Kentucky bluegrass turf grown
in the Northeast, upper Midwest and Pacific Northwest regions.
Currently, there is no information regarding cultural control of NRS or cultivar susceptibility to
the disease. Early spring applications of fenarimol and propiconazole have been reported to control
NRS.
STRIPE SMUT and FLAG SMUT
Stripe (Ustilago striiformis) and flag smut (Urocystis agropyri) are diseases that occur primarily
in mature Kentucky bluegrass stands and occasionally in bentgrass and perennial ryegrass turf.
Symptoms are most conspicuous during the cool, moist seasons of spring and fall. Infected plants
are often stunted and pale green or yellow in color. Narrow, silvery or gray-black streaks will appear
on the leaves. These streaks are fruiting structures (sori) in which large masses of spores
(teliospores) are produced. When sori mature, the cuticle and epidermis rupture, and the leaves
shred and curl releasing the teliospores. During summer months, infected plants may appear
amazingly healthy if properly maintained. In spring or autumn, however, badly infected stands may
appear chlorotic and in need of nitrogen fertilizer. During winter, leaves that had been shredded by
matured fruiting bodies develop a gray-brown, desiccated appearance.
Stripe and flag smut are most damaging to infected plants during periods of heat and drought
stress. If properly irrigated and fertilized, however, badly smutted stands often survive, exhibiting
only a decrease in turf quality and some thinning during stressful summer months. These smut
diseases most commonly occur in mature (two to four years and older) stands that have been
managed with high levels of nitrogen fertilizer. Merion, Windsor and Fylking Kentucky bluegrasses
are among the most susceptible cultivars. Recently introduced cultivars are less susceptible to these
diseases, which has led to a reduction in the occurrence of stripe and flag smut. Using a balanced
N-P-K fall fertilizer program, increasing the mowing height in summer and deep irrigation at the first
sign of drought stress are effective management practices that greatly minimize smut injury in
Kentucky bluegrass. Hence, cultural control of smut diseases is aimed at blending disease resistant
cultivars, avoiding excessive use of nitrogen fertilizer, controlling thatch and preventing severe
drought stress of infected turfs. Smut diseases are effectively controlled with a spring or fall
application of a systemic fungicide such as benomyl, fenarimol, propiconazole, or triadimefon.
RED THREAD
Red thread (Laetisaria fuciformis) is a common disease of turfgrasses, and its development
is favored by cool (65-75F), wet and extended overcast weather of spring and fall. Red thread may
also occur during warm to very cold weather in the presence of plenty of surface moisture or at
snow melt in winter. This disease may become widespread among turfgrass species during mild
winters.
Red thread is most damaging to perennial ryegrass, common-type Kentucky bluegrasses, and
the fine leaf fescues. Red thread may also attack improved cultivars of Kentucky bluegrass, tall
fescue, bentgrass, and bermudagrass, but generally does not cause a significant level of injury to
these species when they are sufficiently fertilized with nitrogen.
The symptoms and signs of red thread are distinctive and unmistakable. In the presence of
morning dew or rain, a coral pink or reddish layer of gelatinous fungal growth (mycelium) can easily
be seen on leaves and sheaths. The infested green leaves of these plants soon become
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water-soaked in appearance. When leaves dry, the fungal mycelium becomes pink in color and is
easily seen on the straw-brown or tan tissues of dead leaves and sheaths. During the final phase
of disease activity, bright red, hard and brittle strands of fungal mycelium called "red threads" or
sclerotia may be seen extending from leaf surfaces, particularly cut leaf tips. These red threads fall
into the thatch and serve as resting structures for the fungus by surviving long periods that are
unfavorable for growth of the pathogen. From a distance, affected turf has a straw-brown, tan or
pinkish color. Symptoms are concentrated in circular or irregularly shaped patches two inches to
three feet in diameter that frequently coalesce to involve the whole sward.
Red thread is generally most injurious to poorly nourished turfs. Frequently, the disease is
best controlled by an application of 0.5-1.0 Ib nitrogen/1000 ft. Application of nitrogen during periods
too cool for turf growth will not aid in reducing disease severity. This is because nitrogen alleviates
red thread disease symptoms by stimulating plant growth and vigor. The nitrogen-stimulated plants
are able to replace damaged tissues more rapidly than the fungus can inflict injury. Fungicides that
control red thread are anilazine, chlorothalonil, iprodione and triadimefon.
POWDERY MILDEW
Powdery mildew (Erysiphe graminis) is a disease confined to shaded environments. The
presence of grayish-white mycelium and spores on the upper surfaces of leaves is a conspicuous,
diagnostic sign of the disease. The lower, older leaves of the plant are generally more heavily
infected than upper, younger leaves. In heavy infestations, leaves appear to have been dusted with
ground limestone or flour. The abundant surface mycelium absorbs nutrients from the epidermal
cells and the leaves turn yellow. Eventually leaves and tillers may die and the turf will exhibit poor
density. The fungus seldom kills plants; however, its presence severely weakens plants and
therefore can predispose them to injury from environmental stresses or other diseases.
Powdery mildew can be found at almost any time of year, but peak activity normally occurs in
the fall. Spores are produced in abundance on leaf surfaces and they move rapidly to adjacent,
healthy leaves. The spores germinate rapidly, even in the absence of dew or water. Disease activity
is most prevalent during cool, humid and cloudy periods of spring and fall. Because shade is the
primary predisposing factor for powdery mildew, reducing shade and improving air circulation is a
cultural, but often impractical approach to reduce damage. Planting or overseeding with
shade-tolerant cultivars, increasing mowing height, avoiding drought stress and using a balanced
fertilizer program will promote turfgrass growth and help to minimize injury from powdery mildew.
Fungicides should be applied in situations where the disease is yellowing plants and thinning the
stand. Some effective fungicides are benomyl, propiconazole and triadimefon. Tank mix a leaf spot
fungicide with the mildewcide.
RUST
Rust diseases in turf are caused by several Puccinia spp. and they are most damaging to
poorly nourished turfs and turfs grown under a low mowing height. Stem rust (P± graminis) of
Kentucky bluegrass, crown rust (P, coronata) of perennial ryegrass, and zoysiagrass rust (IL
zoysiae) are most commonly observed during cool, moist periods of fall. Rust-affected turfs exhibit
a yellowish or reddish-brown appearance from a distance. Close inspection of diseased leaves
reveals the presence of conspicuous red, black, orange or yellow pustules. Sterol inhibiting
fungicides (such as propiconazole and triadimefon) effectively control rust. Contact fungicides (such
as chlorothalonil, maneb and mancozeb) will help somewhat to alleviate injury. A balanced fertility
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program may be preferred to fungicides in situations where rust is damaging poorly nourished turfs.
Also, irrigate early in the day to insure leaf dry ness prior to nightfall, water deeply but infrequently,
increase mowing height and increase mowing frequency. By increasing mowing frequency, leaves
bearing immature spores are removed and this reduces the potential for more leaf infections.
SUMMER DISEASES
BROWN PATCH
Brown patch is caused by Rhizoctonia solani and it is a common, summertime disease of
turfgrasses. In southeastern states. R. zeae may also cause symptoms typical of brown patch. The
pathogen attacks nearly all grasses used as turf, but is most damaging to tall fescue, perennial
ryegrass, creeping bentgrass and annual bluegrass. Kentucky bluegrass, zoysiagrass and other
species are only occasionally injured by Rhizoctonia solani. The symptoms of the disease vary
according to host species. On closely mown turf, affected patches are roughly circular and range
from three inches to three feet or greater in diameter. The outer edge of the patch may develop a
one to two inch wide smoke ring. The smoke ring is blue-gray in color and is caused by mycelium
in the active process of infecting leaves. Smoke rings are not always present and patches may
have an irregular rather than circular shape. Close inspection of leaf blades reveals that the fungus
primarily causes a dieback from the tip down, to give affected turf its brown color. In tall fescue and
perennial ryegrass turfs, affected areas are frequently irregularly shaped and smoke rings are only
occasionally present. EL solani produces distinctive and often greatly elongated lesions on tall
fescue leaves. The lesions are a light, chocolate brown color, and are bordered by narrow, dark
brown bands of tissues. In perennial ryegrass, smaller leaf lesions are produced and tip dieback
commonly occurs. During early morning hours, when the disease is active, the cobweb-like
mycelium may be observed on leaves in the presence of water or heavy dew.
Environmental conditions that favor disease development are day temperatures above 85F
and high relative humidity. A night temperature above 68F is perhaps the most critical environmental
requirement for disease development. Although textbooks underscore the importance of high
surface moisture or high soil moisture in disease severity, the disease can be very damaging to
wilted tail fescue and perennial ryegrass if the relative humidity is high. Summer application of
fertilizers, in particular water soluble N fertilizers, may enhance disease injury from brown patch.
Avoiding nitrogen when the disease is active and irrigating early in the day are the only cultural
practices that may help alleviate brown patch. Benomyl, chlorothalonil, iprodione, maneb,
mancozeb, propiconazole and the thiophanates effectively control brown patch.
PYTHIUM BLIGHT
Pythium blight is among the most destructive turfgrass diseases. During periods of high relative
humidity, nighttime temperatures above 70F and abundant surface moisture, the disease may
progress rapidly, destroying large turf areas within 24 hours. The disease often is first observed in
areas that are shaded, low lying and adjacent to water where air circulation is poor. While there are
several species capable of causing the disease, P. aphanidermatum and P± ultimum are the most
commonplace.
It is a general misconception that Pythium blight is a common, widespread disease. Although
Pythium spp. can cause damping-off of any seedling species, it rarely, if ever, attacks mature lawns
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comprised of Kentucky bluegrass, tall fescue, fine fescue or zoysiagrass. Pythium blight is most
likely to attack creeping bentgrass or perennial ryegrass grown under the high management
conditions commonly found on golf courses.
On closely mown bentgrass putting greens, the disease kills turf in circular patches, rings or
streaks that follow the water drainage pattern. During morning hours when the disease is active,
bentgrass turf displays an orange-bronze color and there may be a gray smoke ring on the periphery
of affected patches. In low lying areas where water collects the patches are brown and all plants
are often killed. In perennial ryegrass, affected foliage develops a dark-gray color and leaf blades
have a water soaked appearance. Blades then collapse, mat together and turn brown.
A cottony web of mycelium covers the grass leaves and is visible during early morning hours
when leaves are wet. Pythium spp. are capable of producing an abundance of mycelium in a few
hours, which bridges leaf blades, giving turf the cottony appearance. The fungus primarily spreads
over a turf by rapid mycelial growth or by movement of mycelial fragments in rain or irrigation water.
Pythium species also produce motile spores called zoospores, which also serve to spread the
disease.
Water management may greatly influence disease severity. It is therefore helpful to water early
in the day to avoid a moist foliage prior to nightfall. Improving water and air drainage will help reduce
disease development, but these cultural measures are often expensive and difficult to achieve. A
fall fertilization program using a balanced N-P-K fertilizer, avoiding the use of lime in alkaline soils
and avoiding nitrogen fertilizers during summer stress periods may help to reduce disease incidence
and severity.
While fungicides are not generally used in lawn care for Pythium blight control, they are
considered a necessity in golf course management in most regions of the U.S. Before the advent
of systemic fungicides targeted for Pythium blight in the early 1980's, the disease was combatted
with short residual chemicals such as chloroneb and etridiazol. Metalaxyl was registered for use
on turf in 1981 and provides over 20 days of control and can be used either preventatively or
curatively. The widespread reliance and continuous usage of metalaxyl on golf courses has led to
reduced effectiveness and in some cases the selection of Pythium spp. biotypes resistant to
metalaxyl. Reduced residual effectiveness is attributed to a build-up of microorganisms that degrade
the active ingredient of the fungicide. Propamocarb and fosetyl-AI are other fungicides that provide
long, residual Pythium blight control, but they should be applied preventatively and they are
expensive to use.
To avoid the build-up of fungicide resistant biotypes and to avoid reduced residual
effectiveness of compounds due to microbial build-up, fungicides should always be rotated and
they should be applied in tank-mix combinations whenever economically feasible. Recent research
indicates that the aforementioned problems can be avoided by tank mixing reduced rates of
metalaxyl and propamocarb or reduced rates of metalaxyl + propamocarb + fosetyl-AI. Tank mixing
metalaxyl with mancozeb is also believed to help reduce the probability of resistant Pythium biotypes
from dominating. Alternating systemics with contact sprays, although the latter may only provide
three to seven day control, will also help to reduce these potential problems from occurring.
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SUMMER PATCH
Summer patch is incited by Magnaporthe poae and is a most destructive disease of Kentucky
bluegrass and annual bluegrass turf. Symptoms of summer patch initially appear as wilted,
dark-green areas of turf. Initially the straw-brown dead patches resemble the symptoms of dollar
spot disease, but these patches soon increase in size and may take on crescent shapes, elongated
streaks, or circular patches. Healthy turf may persist in the center of blighted patches producing
rings or "frog eye" symptoms. The frog eye symptom, however, is only occasionally observed and
the dead patch symptom is more commonplace. Affected regions may coalesce, and large areas
of turf are destroyed within a seven to ten day period. There are no distinctive leaf lesions associated
with the disease, but leaves generally dieback from the tip.
Summer patch most commonly occurs in Kentucky bluegrass turfs that are three years of age
or older. To date, the disease has principally been a problem in Kentucky bluegrass, annual
bluegrass and fine leaf fescues. Environmental conditions play a significant role in the predisposition
of turf to the disease. The disease generally appears in late June or early July when daytime
temperatures above 90F prevail. The disease is most severe on sunny, exposed slopes or other
heat-stressed areas of lawns such as those adjacent to paved walks and driveways. The disease
most frequently occurs following a period of drought stress. Turf allowed to enter drought-induced
dormancy is often severely damaged. Mysteriously, the disease may flair up following rainy periods
in late summer and September. Other predisposing factors include: spring applications of high
levels of nitrogen fertilizer, accumulation of thatch, frequent light irrigations or rain storms, and
compaction. The most important environmental factor required for disease development is for root
zone temperatures to exceed 86F. For home lawns, increasing mowing height to 3.0 inches in late
spring, applying water deeply and only at the onset of wilt and use of a slow release nitrogen fertilizer,
such as sulfur coated urea, are the best approaches to minimizing summer patch. Preventative
applications of triadimefon, or curative applications of benomyl or iprodione drenches may provide
a satisfactory level of control on close-cut Kentucky bluegrass fairways, but no fungicide program
is known to control the disease in annual bluegrass on putting greens. Fungicides are ineffective if
turf is allowed to enter drought induced dormancy.
FUSARIUM BLIGHT
Fusarium blight was first observed in the late 1950's, but is a controversial disease that primarily
attacks Kentucky bluegrass. A complex of Fusarium culmorum and R poae were implicated as the
incitants of the disease. Fusarium blight occurred in California primarily as a severe crown rot;
whereas in the eastern U.S., the foliage blight symptom is most commonplace. Early symptoms first
appear as scattered, light-green or wilted patches two to six inches in diameter. Over a period of
36-48 hours, under high-temperature stress conditions, patches fade to a tan or light-straw color.
Affected areas may take on crescent shapes, elongated streaks or circular patches. Healthy turf
may persist in the center of blighted patches, producing rings of frog-eye symptoms. Leaf blades
may develop bleached white lesions that appear similar to dollar spot lesions. Fusarium species
can be isolated from the lesions.
In California, the disease typically occurs in the absence of foliar blighting. Patches appear
when foliage dies as a result of the destruction of crowns and attached roots by F. culmorum. The
pinkish mycelium of the pathogen can be seen on crown surfaces when soil moisture is high. Stem
bases and crown tissues eventually develop a dark brown or black, firm rot.
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Currently, the name Fusarium blight is retained to describe foliar blight, crown rot and root rot
symptoms in situations where signs of Fusarium spp., such as spores and pink mycelial growth, are
abundant. Two additional diseases, described previously, are now recognized as summer patch
and necrotic ring spot, where Fusarium spp. are not involved and roots bear dark-brown, runner
hyphae. The control measures for Fusarium blight are the same as those described for summer
patch.
MELTING-OUT
In summer, Kentucky bluegrass, fine leaf fescues and other grasses may decline due to
invasion by IL sorpkiniana. This fungus also may cause a leaf spot and melting-out phase. JL
sprpkiniana is normally most severe when temperatures exceed 85F and humidity is high. This
disease is generally aggravated when turf is subjected to drought stress. Today, the fine leaf fescues
are frequently more severely damaged in summer by this fungus than Kentucky bluegrass. Again,
this is principally related to the development of resistant cultivars of Kentucky bluegrass; whereas,
highly resistant cultivars of fine leaf fescues are not yet available. Also during warm, dry periods EL
cynodontis may become a severe crown, stolon and root rot pathogen of bermudagrass. See the
"Helminthosporium and Melting-Out" section for management of melting-out.
FAIRY RINGS
Fairy rings may be caused by any one of 60 or more species of fungi. The activity of these
fungi in the thatch and soil results in rings or arcs of dead or unthrifty turf, or rings of dark green,
luxuriantly growing grass. The most destructive rings are classified as Type 1 rings. Type 1 rings
are very common, especially in old pasture turfs or any mature turf with a lot of thatch. Type 1 rings
normally appear as circles or arcs of dark green, fast growing grass. The most common fungus
known to cause Type 1 fairy ring is Marasmius oreades. These rings are distinguished by three
distinct zones: an inner/lush zone where the grass is stimulated and grows luxuriantly; a middle
zone where the grass may be dead; and an outer zone in which the grass is stimulated. The distance
from the inside of the inner zone ta the outside of the outer zone may range from a few inches to
one or more feet wide. The dead zone is due to a massive build-up in the thatch and soil of fungal
mycelium. It accumulates in such large amounts to form a hydrophobic barrier that prevents entry
of rain or irrigation water, thus killing the plants by drought. The formation of the three zones is
noticeable from early spring to winter.
Control of fairy rings is made extremely difficult due to the impermeable nature of the infested
soil. Chemical control has been ineffective because the fungus grows deeply into the soil and lethal
concentrations of fungicide do not come into contact with the entire fungal body. Suppression is the
most practical approach to combating fairy rings in most situations. The suppression approach is
based upon the premise that fairy rings are less conspicuous and less numerous where turf is well
watered and fertilized. This method of control involves a combination of aeration, deep waterings
and proper fertilization. Aeration is beneficial, as it aids in the penetration of air and water. The
entire area occupied by the ring, to include a two foot periphery beyond the ring, should be core
aerified on two to four inch centers. The area should then be irrigated to a depth of four to six inches.
Use of a wetting agent should help improve water infiltration. The ring area should be retreated in
a similar fashion at the earliest indication of drought stress; that is repeat the process whenever the
dark green grass turns blue-gray and begins to wilt. When an aerator is not available, a deep root
feeder with garden hose attachment may be useful to force water into the dry soil. About 3.0 to 4.0
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Ib N/1000 ft should be applied to cool season turfgrass species in three to four applications during
fall or late winter.
There are two methods of eradication: fumigation and excavation. Both methods are laborious,
costly and not always successful. To fumigate, the sod must be removed from an area two feet to
the inside and at least two feet to the outside of the rings. It is essential not to spill any soil or sod
onto the healthy grass. The most commonly used fumigants are methyl bromide and metam.
Fumigation with methyl bromide must be carried out by a licensed pesticide applicator. Special
precautions must be taken to insure that children or pets do not come into contact with these
fumigants. The second alternative to fairy ring eradication Is to carefully dig out and discard all
infested soil in the ring. This would involve removal of soil to a 12-inch depth, and the excavation
should be wide enough to extend at least two feet beyond the outer most evidence of the ring. The
excavation must then be filled with fresh, uncontaminated soil and the area reseeded or sodded.
Hence, the eradication approach for fairy ring control is impractical and seldom performed.
WINTER DISEASES
SNOW MOLD DISEASES
Snow protects dormant turfgrass plants from dessication and frost, but also provides a
microenvironment conducive to development of some low temperature, pathogenic fungi. Like
most other disease problems, there is no shortage of fungal species that are capable of damaging
turf during cold periods between late fall and early spring. The most common low temperature
fungal diseases are pink snow mold (Microdochium nivalis). and gray snow mold (Typhula incarnata
and T ishikarensis). Other diseases known to be active under snow cover or during winter months
include red thread (Laetisaria fuciformis) and leaf spot (Drechslera spp.). During cool moist periods
of late fall or early spring, cool temperature brown patch (Rhizoctonia cerealis) is a common disease
of putting green turf.
Snow mold fungi are remarkable in being active at temperatures slightly above freezing. Snow
molds are damaging when turf is dormant or when growth of turf has been retarded by low
temperatures. Under these conditions, turfgrasses cannot actively resist fungal invasion. Although
known as snow molds, these fungi can attack turf with or without snow cover. In general, these
diseases develop whenever temperatures are cool (32-60F) and there is an abundance of surface
moisture.
Conditions favoring pink snow mold include low to moderate temperatures; plenty of moisture;
prolonged deep snow; snow fallen on unfrozen ground; lush turf stimulated by late season
application of excessive amounts of nitrogen fertilizer, and alkaline soil conditions. Symptoms of
this disease appear as small water soaked patches two to three inches in diameter that may increase
in size to one to two feet in diameter and coalesce. The pink coloration of affected turf at the edge
of the patches is produced by the pinkish color of the mycelium. The mycelium mats the leaves,
and plants eventually collapse and die. Mycelium on the leaf blades produce fruiting bodies
(sporodochia) upon which spores are borne in prodigious numbers. These spores are easily spread
by machinery and foot traffic. When damage occurs under snow the extent of injury is usually more
severe than without snow cover. The pathogen, once known as Fusarium nivalef is able to survive
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unfavorable environmental conditions as spores and as resting mycelium that remain viable in plant
debris.
Pink snow mold attacks a wide range of turfgrass species under snow including perennial
ryegrass, Kentucky bluegrass, bentgrass and the fescues. This disease is generally most
destructive to annual bluegrass and bentgrass. For many years the standard fungicidal control has
been phenyl mercury acetate or mercurous plus mercuric chloride. The soluble mercuric chloride
provides quick disease suppression and the insoluble mercurous chloride provides persistent
protection. Mercury-based fungicide may only be applied to putting greens and tees, and only for
the purpose of snow mold control. Pentachloronitrobenzene (PCNB), benomyl, iprodione and
triadimefon also provide good control. Fungicidal control is best achieved with a preventative
application prior to the first big snow storm of the year. Subsequent applications should be made
during mid-winter thaws and early spring snow melt in areas where the disease is a chronic problem.
Gray snow mold, or Typhula blight, is also a serious disease of turfgrasses as well as cereals
in North America and Europe. Initially, symptoms appear as light brown or gray patches two to four
inches in diameter enlarging to two feet in diameter and coalescing. Gray snow mold also occurs
with and without snow cover; however, damage is usually minimal in the absence of snow. Like
pink snow mold, Typhula blight is more damaging under prolonged deep snow, particularly when
heavy snow accumulates on unfrozen ground.
Gray snow mold initially begins its disease cycle as a saprophyte colonizing dead organic
matter. Under snow, however, the fungus moves onto living leaves, sheaths and may ultimately
invade the crown. Normally, Typhula spp. do not completely kill crowns so plants generally recover
during the spring. Conversely, pink snow mold more frequently invades crown tissues and kills turf.
Typhula spp. survive unfavorable environmental conditions as sclerotia. Sclerotia are compact
masses of fungal mycelium covered with a dark colored, protective rind. Sclerotia are chestnut brown
or black in color and are less than 1/8 inch in diameter. When cool, moist weathers conditions return
in late fall, these sclerotia germinate to produce fungal mycelium or a specialized fruiting body upon
which spores are borne. All species of Typhula that attack turf produce similar symptoms. Sclerotial
color is one of the primary characteristics pathologists use to differentiate between the two species
of Typhula known to cause gray snow mold.
Gray snow mold, like pink snow mold, is best controlled using a mercurial applied on a
preventative schedule. Iprodione and triadimefon as well as cadmium based fungicides also provide
effective control of the disease. Cadmium (like mercury)-based fungicides, however, may only be
applied to golf course greens and tees. Snow mold prevention with fungicides is generally only
warranted for golf course turf in most regions of the U.S.
Researchers in Canada have shown that the fungus Typhula phacorrhiza applied on grain
inoculum suppressed gray snow mold on creeping bentgrass greens by 44% to 70%. Although not
yet commercially available, these Canadian researchers believe that this biological control agent
can be formulated into pellets and be applied by standard fertilizer spreaders.
Snow mold injury can be reduced by applying a balanced N-P-K fertilizer in fall. Ammonium
sulfate use was associated with reduced pink snow mold injury in Washington. Continue to mow
late in the fall to insure that snow does not mat a tall canopy. On golf courses, snow fences and
windbreaks should be used to prevent snow from drifting on chronically damaged greens. Avoid
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compaction of snow by skiers and snow mobiles on greens. Also avoid the use of limestone where
soil pH is above 7.0, as alkalinity may encourage pink snow mold.
Cool temperature brown patch, also known as yellow patch, is a disease of bentgrass, annual
bluegrass and perennial ryegrass turf. It is most frequently observed on putting greens producing
rusty-brown and yellow rings, or yellow patches a few inches to one or more feet in diameter.
Damage is generally superficial but significant thinning of turf may occur during prolonged, wet and
overcast weather of late winter and early spring. A broadspectrum fungicide such as anilazine,
chiorothalonii or iprodione will prevent severe thinning, but no fungicides or cultural practices are
known which help to prevent the formation of rings and patches.
FACTORS ASSOCIATED WITH FUNGICIDE USE
Arriving at the decision of whether to apply a fungicide to any turf area is often difficult and
generally based upon economic considerations. Aside from cost, the primary determinants in using
a fungicide are the prevailing environmental conditions, host species and cultivars present, and the
pathogen. The environmental factor has unique implications in turf grass pathology because the
intensity and nature of turf grass management greatly influences plant vigor and therefore the
incidence and intensity of diseases.
Promoting vigorous growth through sound cultural practices is the first step in minimizing
disease injury. Frequently, however, environmental stresses, traffic and poor management weaken
plants, predisposing them to invasion by fungal pathogens. When disease symptoms appear, it is
imperative that a rapid and accurate diagnosis of the disorder be made. The prudent manager also
attempts to determine those factors that have led to the development of the disease. The most
common cause for extensive disease injury in lawn turf can frequently be related to poor
management practices by the homeowner. Abusive practices include frequent and close mowing;
light and frequent irrigations; and inadequate or excessive nitrogen fertility. The development of
excessive thatch layers, shade, poor drainage and traffic also contribute significantly to disease
problems. A good case in point is Helminthosporium diseases, which are particularly damaging
when turf is mown too closely, given light and frequent irrigations, and when turf is excessively
fertilized. Despite hard work and adherence to sound management practices, diseases often
become a serious problem. This normally occurs when environmental conditions favor disease
development, but not plant growth and vigor. For example, summer patch and brown patch are
most damaging when high summer temperatures stress plants and impair their growth and
recuperative capacity. In this situation, fungicides may be recommended in conjunction with cultural
practices that promote turf vigor.
Fungicides may be applied preventatively (i.e. before anticipated disease symptoms appear)
or curatively (i.e. when disease symptoms first become evident). Applying a fungicide after the turf
has been damaged significantly is generally a waste of time, money and effort. Curative applications
are more economical and environmentally wise, but only if the disease can be treated rapidly. In
general, a single or possibly two, properly timed applications will provide effective control of most
disease problems encountered on home lawns. Contact fungicides are less expensive and provide
good control. Contact fungicides, however, may only provide 7-14 days of control under high disease
pressure conditions. Where sudden and severe, or chronic disease problems occur, a systemic
alone, or a systemic plus contact may be needed. Systemic or local systemic fungicides will provide
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14-21 days protection during high pressure disease periods. Tank mixing a systemic plus a contact
fungicide provides a longer residual effect and a wider spectrum of control. Frequently, a fungicide
may only be needed to help the turf better survive a high pressure disease period. Favorable
changes in weather such as alternating hot-humid and cooler periods, however, provide the most
effective means of reducing or eliminating disease problems in the summer.
THE FUNGICIDE DILEMMA IN LAWN CARE
Proper utilization and selection of fungicides is too difficult and complicated for most
homeowners. Because of this, only lawn care companies can provide the most reliable lawn disease
service. Fungicides, however, should not become a part of a normal application schedule. As a
general rule, use of fungicides is not encouraged in most home lawn situations because (a) proper
diagnosis and proper fungicide selection is difficult, (b) it is generally too late to achieve the economic
and aesthetic benefits of a fungicide once extensive injury has occurred, (c) lawn care companies
capable of only dry or granular applications do not have the proper spray equipment or they cannot
obtain the desired fungicide(s) in granular form, and (d) it may be less expensive, and better in the
long run, to overseed a damaged turf area in the autumn with disease-resistant cultivars.
There are several disease situations of lawn turf that are best controlled through a preventative
fungicide application. These disease situations are: (1) Kentucky bluegrass lawns injured in previous
years by summer patch, necrotic ring spot, stripe smut and perhaps dollar spot, (2) perennial
ryegrass lawns injured in previous years by Pythium blight, brown patch or dollar spot, and (3) tall
fescue lawns chronically damaged by brown patch. Many diseases, however, are effectively
controlled with curative fungicide applications when disease symptoms first appear. For example,
leaf spot in lawns of common-type Kentucky bluegrasses (e.g., Kenblue, Newport, Park, South
Dakota, etc.) and fine leaf fescue (e.g., Pennlawn and Jamestown), and brown patch in perennial
ryegrass can be effectively controlled with a curative fungicide application. Dollar spot disease is
extremely common and if allowed to go unchecked, may cause extensive injury to Kentucky
bluegrass, perennial ryegrass, red fescue and zoysiagrass lawns. When diagnosed in its early
stages, however, dollar spot is also effectively controlled by fungicides. Given these situations, it
becomes obvious that effective fungicide programs hinge upon (a) knowledge of past disease
problems in a particular lawn or neighborhood, (b) ability to distinguish between turfgrass species
and sometimes cultivars within a species, and (c) ability to diagnose turfgrass diseases. Hence, in
addition to the expense of fungicides and logistical problems associated with sending trucks to
specialized fungicide accounts, the lawn care company must also educate its employees to
diagnose diseases. This educational process is best achieved by in-house training programs. This
knowledge must be reinforced by encouraging employees to attend turf workshops and conferences
held by state universities and other organizations, as well as maintaining subscriptions and reading
articles in trade magazines. Expecting the employee to be proficient by reading alone is not realistic,
even for highly motivated individuals.
In Table 2, the most common lawn diseases are listed, as well as their primary season(s) of
occurrence, and those species that are most commonly damaged. Remember, once a disease has
severely reduced stand density, fall overseeding with resistant cultivars is normally suggested.
Fact sheets describing the disease and a list of cultural practices that will help minimize disease
injury should be provided by the lawn care company to homeowners.
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THE FUNGICIDE DILEMMA ON GOLF COURSES
Where extremely high quality turf is desired, fungicides will be needed in most years, and in
nearly all areas of the U.S. The indiscriminate use of fungicides or employment of numerous,
preventative applications of fungicides for many diseases should be discouraged. Other than
economic restraints, reasons why repeated fungicide applications may not be desirable include:
1. Fungicides may reduce the population of beneficial microorganisms in the soil, which could
lead to excessive thatch build-ups.
2. Fungicides may disturb a delicate balance among microorganisms that compete with and
antagonize disease-causing fungi. This may explain why some diseases recur more rapidly
and cause more injury in turfs previously treated with fungicides.
3. A fungicide may control one disease, but encourage other diseases.
When used repeatedly, certain fungicides have been shown to enhance thatch accumulation.
Benzimidazole fungicides, such as benomyl and the thiophanates, and sulfur-containing fungicides
such as mancozeb, maneb and thiram can cause thatch to accumulate by acidifying soil. The effect
of these fungicides is indirect, that is they inhibit the thatch decomposition capacity of beneficial
microorganisms by lowering soil pH. Cadmium fungicides and iprodione also may enhance thatch
accumulation. In the case of these latter two compounds, thatch build-up is attributed to direct
toxicity of microorganisms that degrade thatch. Fungicides may also contribute to thatch build-up
by being toxic to earthworms. Earthworms help reduce thatch by mixing soil with organic matter.
Benomyl, mancozeb, anilazine, chlorothalonil and various nematicides have been shown to be toxic
to earthworms.
Turf managers have observed that some diseases may recur more rapidly and severely in turfs
previously treated with fungicides, as compared to adjacent untreated areas. Dollar spot is probably
the most common disease to exhibit this phenomenon. Data, recorded in a Maryland study, showed
that red thread was more severe in the spring of 1983 in Manhattan perennial ryegrass plots last
treated with benomyl in July, 1982. These phenomena are attributed to non-target effects of
fungicides, i.e., the fungicide(s) were toxic to microorganisms which antagonize and help keep
disease-causing fungi in abeyance.
The development of fungal strains resistant to fungicides has been well documented. Resistant
strains of the dollar spot fungus first developed as a result of repeated usage of cadmium based
fungicides and benomyl on golf courses. Thiophanates, anilazine, and iprodione resistant strains
of the dollar spot fungus have also been reported. The development of resistant strains of fungi
likely occurs in response to a selection process that eventually enables a small, but naturally
occurring population of resistant biotypes to predominate in the fungicide-treated turf grass
microenvironment. It is very unlikely, however, that occasional fungicide use on home lawns would
lead to the development of fungicide-resistant biotypes.
Fungicides applied to control one disease may encourage other diseases. As previously noted,
benomyl can encourage red thread. Benomyl has also been shown to enhance Helminthosporium
leaf spot and Pythium blight. Thiophanate-methyl may increase crown rust in perennial ryegrass,
iprodione can increase yellow tuft, and maneb may enhance dollar spot. Encouragement of disease
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in these situations may again be attributed to offsetting the delicate balance between antagonistic
and pathogenic microorganisms in the ecosystem.
The phytotoxicity that accompanies the usage of some fungicides is generally not severe.
Most phytotoxicity problems occur when fungicides are applied to bentgrasses, particularly during
periods of high temperature stress. Repeated applications of sterol-inhibiting fungicides such as
fenarimol, propiconazole or triadimefon may elicit a blue-green color in foliage of creeping bentgrass
and other turf grass species.
It should be noted that many of the harmful side effects just described were either isolated
events or occurred only after repeated use of one fungicide over the course of several years.
Experienced turfgrass managers have long recognized that tank mixing fungicides and rotating
fungicides greatly minimizes these potential problems. The importance of rapid and accurate
disease diagnosis, and the judicious use of fungicides are integral in management programs where
fungicides are commonly employed.
NEMATODES
Nematodes are known to cause extensive injury to turfgrasses in warm temperate and
sub-tropical areas in the U.S. In northern climates, the loss of turfgrass that can be attributed to
nematodes is unknown. However, nematodes may be more troublesome in the transition zone and
Mid-Atlantic area than is commonly believed. This would be particularly true following a mild winter.
In general, nematodes most actively feed on turfgrass during environmental periods favorable for
growth of the grass. Hence, feeding would be more active on cool season species in spring and
fall, while on warm season grasses heaviest feeding would occur during summer. The injurious
effects of this feeding, however, may not become noticeable until turf is subjected to environmental
stresses in mid-to late summer.
Nematodes are very small eel-like worms, ranging from 1/50 to 1/8 inch in length. Nematodes
reproduce by eggs, which hatch to liberate larvae. Larvae molt four times before reaching adult size.
Each female is capable of producing hundreds of eggs and the entire life cycle is completed in five
to six weeks under suitable conditions for most species. Because plant pathogenic nematodes are
obligate parasites, they must feed on living tissues in order to grow and reproduce. Most nematodes
are capable of attacking a wide range of plant species, and can survive on weeds in the absence
of turfgrasses. Most nematodes store large quantities of food, which enables them to survive long
periods in soil in the absence of suitable plants. Many also survive in frozen soils and may overwinter
in living roots or in dead plant tissues.
Literally millions of nematodes can inhabit a few square feet of soil, but most nematodes are
non-pathogenic. Some non-pathogens, may actually perform a beneficial service in soil by helping
to degrade organic matter. Although there are thousands of species, only about 50 species are
known to parasitize turfgrasses. All plant parasitic nematodes bear a hollow, spear-like structure
called a stylet. The stylet is similar to a hypodermic syringe, and is used to inject enzymes into plant
cells. Simultaneously, partially digested food is withdrawn. Plant pathogenic nematodes are grouped
according to feeding habit. Endoparasitic nematodes partially or totally burrow into plant tissues
and feed primarily within; whereas, ectoparasitic nematodes feed from the plant surface, although
a small portion of the body may be embedded. The ectoparasitic are more commonly injurious to
turfgrasses than endoparasitic nematodes. Nematode activity is favored by warm and moist soil
conditions. Nematode populations generally peak in June or July and again in late August or early
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September. Their activity is also enhanced in light textured soils and reduced in compacted or heavy
soils where aeration becomes restricted. Nematodes are unable to move more than a few millimeters
in soil, but they may be transported over larger distances by moving water and soil.
The symptoms of nematode injury include yellowing, stunting, wilting or early signs of drought
stress, and thinning of the stand. These symptoms are related to the injury nematodes inflict upon
the root system. Therefore, symptoms of injury may not become noticeable until water becomes
limiting. Due to the similarities between environmental stress symptoms and nematode injury, the
source of the problem is difficult to diagnose. Like many so-called weak or secondary fungal
pathogens, nematodes may not cause much of a problem until environmental extremes reduce the
vigor of a turf. There is often no pattern to nematode injury, but generally affected areas may appear
in streaks or oval-shaped areas. Severe infestations may result in a nearly total loss of grass plants,
which are soon replaced by weed species. Inspection of roots may or may not reveal some indication
of nematode feeding. Roots may exhibit one or more of the following symptoms: swellings, red or
brown lesions, excessive root branching, necrotic root tips and root rot. Some of the more common
plant parasitic nematodes, which are known to injure turfgrasses, are listed in Table 3.
Turfgrass areas damaged by nematodes do not respond readily to an application of fertilizer
or fungicides. This lack of response may be a good indicator of a nematode problem. In this situation
a soil sample should be sent to a nematologist for analysis. Soil should be collected from a dozen
or more areas at the edge or interface between healthy and injured turf. Sampling from severely
thinned areas may yield unreliable results, because these obligate parasites will not survive in large
populations in the absence of living plants. Soil samples should also be collected in the root zone
region, normally the upper three to six inches in heavy soils, but six to twelve inches or deeper in
sandy soils. The samples should be combined, as in a routine soil-fertility sample, and at least a
pint of soil is needed. Samples should also be taken from nearby, healthy turf so that the
nematologist can compare numbers and species of nematodes between the two areas. The soil
must be kept moist and given to the nematologist as soon as possible. Refrigerate the sample, but
do not freeze it, if there will be a delay in transport to the lab. In the laboratory, various methods for
extraction are used. Unfortunately, there are no reliable data correlating nematode number per
sample and expected degree of turf injury in the field. The nematologist, however, will generally be
able to make a relatively good management recommendation based on species and number of
nematodes present in a sample.
An absolute determination of a nematode problem from visual symptoms and even soil analysis
is difficult. Frequently, the best indication of a nematode problem is a positive response from a
nematicide. It should be pointed out, however, that turf green-up invariably occurs following a
nematicide application, presumably because of the death of nematodes as well as other
invertebrates which liberate nitrogen upon decay. Nematicides are highly toxic, organophosphate
derivatives. They must be handled with extreme caution and used only according to the procedure
and at the rates given on the label. Because the target of a nematicide is in soil, it is essential the
chemical be thoroughly watered-in, and aerification prior to application will facilitate the downward
movement of the chemical. Ethoprop is the only nematicide registered for use on home lawns, but
it must be applied by a certified pesticide applicator. Other nematicides include fenamiphos and
fensulfothion. All three are available in granular form. Fumigants are of little practical value because
they kill turf as well as all other living organisms they come into contact with. Obviously, fumigants
would only be used prior to establishing a turf or if total renovation is desired.
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Because nematodes may only be injurious in northern regions during summer stress periods,
cultural practices that alleviate stress may help minimize injury. Such practices would include
judicious irrigation, increasing the mowing height, and use of a balanced fertilizer. Application of
soluble nitrogen fertilizer during environmental stress periods of summer will place an additional
(and perhaps lethal) stress on an already dysfunctioning root system under attack from nematodes.
There are some research data indicating that use of organic forms of nitrogen fertilizer (e.g. sewage
sludges) can discourage development of high populations of some parasitic nematodes, when
compared to the use of inorganic forms. Currently, researchers are evaluating a dried, granular
chitin-protein material called Clandosan, which is obtained from crab and shrimp shells, for control
of nematodes. The mode of action of Clandosan presumably is to stimulate growth of soil
microorganisms that produce enzymes such as chitinase. These enzymes also degrade the cuticles
and eggs of plant parasitic nematodes, thereby providing an indirect, biological means of nematode
control. To date, however, there is insufficient data and information regarding the effectiveness of
Clandosan in turf.
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REFERENCES
Burpee, L.L., L.M. Kaye, L.G. Goutty and M.B. Lawton. 1987. Suppression of gray snow mold on creeping bentgrass by
an isolate of Typhula phacorrhiza. Plant Disease 71:97-100.
Dernoeden, P.M., J.J. Murray and N.R. O'Neill. 1985. Non-target effects of fungicides on turfgrass growth and
enhancement of red thread, pp 579-593 Jn F. Lemaire (ed.) Proc. Rfth Intern. Turf. Res. Conf. Avignon, France.
Smiley, R.W. 1983. Compendium of Turfgrass Diseases. American Phytopathological Society, St. Paul, MN.
Smiley, R.W. 1981. Non-target effects of pesticides on turfgrasses. Plant Disease 65:17-23.
Smiley, R.W. and M.M. Craven. 1978. Fungicides in Kentucky bluegrass turf: Effect on thatch and pH. Agron. J.
70:1013-1019.
Smiley, R.W. M.C. Fowler, R.T. Kane, A.M. Petrovic and R.A. White. 1985. Fungicide effects on thatch depth, thatch
decomposition rate, and growth of Kentucky bluegrass. Agron. J. 77:597-602.
Vargas, J.M. 1981. Management of Turfgrass Diseases. Burgess Publishing Co. Minneapolis, MN.
290
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TABLE 1
The most frequently encountered diseases of lawns, golf courses, athletic fields, and other turf areas
in transition zone and northern regions of the U.S.
Disease
Primary Hosts
Pathogen
PATCH DISEASES CAUSED BY ROOT INVADING PATHOGENS
Summer Patch ABG, FLF, KBG
Necrotic Ring Spot
Take-All Patch
Spring Dead Spot
II. FOLIAR DISEASES
Dollar Spot
Red Thread
Pink Patch
Brown Patch
Leaf Spot
(Helminthosporium)
Gray Snow Mold
Cool Temperature Brown Patch
(Yellow Patch)
Gray Leaf Spot
White Blight
KBG, ABG, FLF
CBG
Bermudagrass
All species except TF
Most species
CBG, PRG
PRG, TF, CBG
All species
All species
ABG, CBG, PRG
St. Augustine
TF
III. FOUAR/STEM OR ROOT DISEASES
Pythium Blight ABG- CBG- PRG
Pink Snow Mold
Anthracnose
All species
ABG, CBG
Magnaporthe poae
Leptosphaeria korrae
Gaeumannomyces graminis var.
avenae
Leptosphaeria korrae
Sderotinia homoeocarpa
Laetisan'a fuciformis
Umonomyces roseipellis
Rhizoctonia solani
Drechslera or Bipolaris spp.
Typhula incarnata and
ishikarensis
Rhizoctonia cerealis
Pyricularia grisea
Melanotus phillipsii
Pythium aphanidermatum, £.,
ultimum
Microdochium nivalis
Colletotrichum araminicola
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Disease
Primary Hosts
Pathogen
III. FOUAR/STEM OR ROOT DISEASES-(Contlnued)
Pythium Induced Root Dysfunction ABG, CBG
Nematodes Most species
Melting-out KBG- FLF- PRG
Fusarium Blight
KBG, FLF
Pythium spp.
Many species
Drechslera or Bipolaris spp.
Fusarium culmorum and F. poae
IV. DISEASES CAUSED BY OBUGATE PARASITES
Stripe Smut
Flag Smut
Powdery Mildew
Rust
Yellow Tuft
KBG
KBG
KBG in shade
PEG, KBG, Zoysia
All species
Ustilago striiformis
Urocystis agropyri
Erysiphe graminis
Puccinia spp.
Sderophthora macrospora
V. DISEASES CAUSING HYDROPHOBIC THATCH OR SOIL, OR THATCH SHRINKAGE
Fairy Ring
Yellow Ring
Superficial Fairy Ring
Localized Dry Spot
All species
KBG
Putting greens
Putting greens
Many Basidiomycetes
Trechispora alnicola
Basidiomycetes
Unknown Basidiomycetes
VI. SEEDLING DISEASES
Damping-Off
Hosts: ABG = annual bluegrass
KBG = Kentucky bluegrass
CBG = creeping bentgrass
PGR = perennial ryegrass
FLF = fine leaf fescue
TF = tall fescue
All species
Pythium spp.
Fusarium spp.
Rhizoctonia solani
Bipolaris spp.
Drechslera spp.
Curvularia spp.
Others
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TABLE 2
Common diseases of transition zone and northern lawn grasses, the primary season of
occurrence, and the primary grasses most likely to be damaged.
Disease
Primary Season
of Occurrence
Primary
Lawn Grasses Damaged
Helminthosporium Leaf Spot, Spring and Fall Summer
Melting-out and Net-blotch
Red Thread
Necrotic Ring Spot
Dollar Spot
Spring and Fall
Early Spring to Early Winter
Early Spring to Early Winter
Brown Patch June, July, August
Summer Patch and Fusarium June, July, August
Blight
Pythium Blight
Stripe Smut
Rust
Powdery Mildew
Fairy Rings
June, July, August
Spring and Fall
Spring and Fall
Spring and Fall
Spring to Early Winter
Common-type Kentucky bluegrass,
Fine leaf fescues, Perennial
ryegrass
Perennial ryegrass, Fine leaf
fescues, Kentucky bluegrass
Kentucky bluegrass
Perennial ryegrass, Kentucky
bluegrass, Fine leaf fescues
Perennial ryegrass, Tall fescue
Kentucky bluegrass, Fine leaf
fescues
Perennial ryegrass
Kentucky bluegrass
Perennial ryegrass, Kentucky
bluegrass, Zoysiagrass
Kentucky bluegrass, Fine leaf
fescues
All species
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TABLE 3
Common plant pathogenic nematodes known to be injurious to turfgrasses.
Nematode Common name/
genus
Feeding group
Turfgrasses injured/root
symptoms
Lesion
(Pratylenchus spp.)
Lance
(Hoplolaimus spp.)
Ring
(Macroposthonia spp.)
Endoparasitic
Endoparasitic
Ectoparasitic
Spiral
(Helicotylenchus spp.)
Stunt or stylet
(Tylenchorhynchus spp.)
Root-knot
(Meloidogne spp.)
Ectoparasitic
Ectoparasitic
Endoparasitic
Stubby root
(Trichodorus spp.)
Sting
(Belonalaimus spp.)
Dagger
(Xiphinema spp.)
Pin
(Paratylenchus spp.)
Ectoparasitic
Ectoparasitic
Ectoparasitic
Ectoparasitic
Cool and warm season grasses
are injured. Root lesions initially
minute and brown, but enlarge
and may prune the root system.
Warm season grasses and annual
bluegrass are injured. Causes
swelling of roots followed by
necrosis and sloughing of cortical
tissues.
Especially important in
centepedegrass, also injured are
Kentucky bluegrass, bentgrass,
bermudagrass, and zoysiagrass.
Roots are stunted; produces brown
lesions on roots.
Cool and warm season grasses
injured. Roots are poorly developed
with premature sloughing of cortical
tissues.
Warm and cool season grasses
injured. Roots shortened, shriveled,
brown; no lesions evident on roots.
Warm season (especially
zoysiagrass) and cool season
grasses (especially bentgrass)
injured. Galls (i.e. swellings or
knots) on roots. Galls may be
small and difficult to see.
Warm season grasses, Kentucky
bluegrass and tall fescue injured.
Large brown lesions on roots;
swelling of root tips.
Bermudagrass, zoysiagrass and
St. Augustinegrass are injured.
Lesions evident, especially root
tips.
Warm season grasses (especially
zoysiagrass) and perennial
ryegrass are injured. Root lesions
are reddish brown to black and
sunken.
Kentucky bluegrass, fine and tall
fescues are injured. Tillering and
rooting increased, but fewer lateral
roots. Distinct lesions on roots.
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TABLE 4
Trade Common Chemical
Name* Name
Mocap ethoprop
Nemacur fenamiphos
Dasanit fensulfothion
Nematicidal Rate
(Formulated)
2.3 Ib. of 10B/
1000 ft2 or 100
16/A.
2.3 - 4.6 Ib of
10B/1000 ft2 or
1.5 - 3.0 Ib of
15G/1000 ft2 or
68-134 Ib/A
Comments
Only the 10G formulation is
registered for use on bahia,
bermuda, centipede, fescue,
Kentucky bluegrass, St.
Augustine and zoysia grass
turfs, labelled for control
of dagger, lance, lesion,
ring, root-knot, spiral
sting, stubby root, stunt,
and other nematodes. May
be used at lower rates to
control some insects, use
on established turfs only.
Can be used on home lawns
by a certified applicator.
Only the 10G formulation is
registered for use on ber-
muda, 100-200 Ib 16/A.
centipede, bluegrass and
bentgrass turf. Do not
use on residential lawns
or public recreation
areas other than golf
courses. Do not use on
newly seeded areas and do
not apply more than twice
per year. Turf should
not be cut for sod for 21
days after treatment.
Only the 15G formulation is
registered for use on com-
mercial (i.e., sod farms,
golf courses, cemeteries)
turf grasses. Turf should
not be cut for sod for 30
days after treatment.
May be used for control
of white grubs.
* Nematicides may only be applied by commercial or professional certified
pesticide applicators.
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REFERENCES
Burpee, L.L., LM. Kaye, L.G. Goulty and M.B. Lawton. 1987. Suppression of gray snow mold on creeping bentgrass by
an isolate of Typhula phacorrhiza. Plant Disease 71:97-100.
Dernoeden, P.H., J.J. Murray and N.R. O'Neill. 1985. Non-target effects of fungicides on turfgrass growth and
enhancement of red thread, pp 579-593 Jn F. Lemaire (ed.) Proc. Fifth Intern. Turf. Res. Conf. Avignon, France.
Smiley, R.W. 1983. Compendium of Turfgrass Diseases. American Phytopathological Society, St. Paul, MN.
Smiley, R.W. 1981. Non-target effects of pesticides on turfgrasses. Plant Disease 65:17-23.
Smiley, R.W. and M.M. Craven. 1978. Fungicides in Kentucky bluegrass turf: Effect on thatch and pH. Agron. J.
70:1013-1019.
Smiley, R.W. M.C. Fowler, R.T. Kane, A.M. Petrovic and R.A. White. 1985. Fungicide effects on thatch depth, thatch
decomposition rate, and growth of Kentucky bluegrass. Agron. J. 77:597-602.
Vargas, J.M. 1981. Management of Turfgrass Diseases. Burgess Publishing Co. Minneapolis, MN.
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BIOLOGICAL SUPPRESSION OF WHITE GRUBS IN TURF
Michael G. Klein
Horticultural Insects Research Laboratory
Application Technology Research Unit
USDA - Agricultural Research Service
Ohio Agricultural Research and Development Center
Wooster, Ohio 44691
The term white grubs, as used here, refers to larvae of beetles in the family Scarabaeidae.
Tashiro (1987) notes that there are 10 species of grubs in five subfamilies that are pests of turfgrass
in the United States. Scarab grubs are the most serious pests of turfgrass in the Northeast, major
pests throughout the Midwest (Tashiro 1987), and of increasing importance in warm season turf
(Cobb 1988). Both introduced and native Scarabs are turfgrass pests. Grubs in two native genera,
Cyclocephala and Phyliophaga. cause problems in almost all areas of the country. Introduced
species are most prevalent in the Northeast, where the Japanese beetle, Popillia japonica Newman,
the European chafer, Rhizotrogus majalis (Razoumowsky), the oriental beetle, Anomala orientalis
Waterhouse, and the Asiatic garden beetle, Maladera castanea (Arrow), in that order, all are pests
in the urban environment (Tashiro 1987).
The Japanese beetle is the most serious turf pest in the United States (Tashiro 1987). Fleming
(1972) reported that 22 states east of the Mississippi River, and Iowa and Missouri to the west, had
Japanese beetle infestations in 1972. Since that time, beetles have moved into Alabama, and within
one county of the Florida border (Hall 1987). In addition, isolated infestations of beetles have been
found in Wisconsin, Oregon, and twice in California (both eradicated). Ahmad et al. (1983) estimated
the losses caused by Japanese larvae to be 240 million dollars per year. This included $78 million
for control costs and an additional $156 million for replacement of damaged turf. Unlike most of the
white grub complex, the adults of the Japanese beetle are also serious pests. Fleming (1972) lists
almost 300 plants fed on by the beetles. New additions to this list will be made as beetles move into
new areas and as their feeding behavior is further studied. It is estimated that damage and control
costs are at least as great for the adults as that reported for larvae.
Fleming (1976) summarized the components available for control of the Japanese beetle in
1976. This included a variety of both chemical and biological agents. However there has been little
effort at a truly integrated program of suppression against the Japanese beetle or other white grub
species. Recently, states such as Massachusetts (Vittum 1987) and Maryland (Hellman 1988) have
developed turf and ornamental IPM efforts. Vittum (1988) states that "several standard insecticides
give acceptable levels of control for most grub species". However, concerns about grub control and
environmental safety persist. Villani et al. (1988) note that the organophosphate and carbamate
insecticides now in use are less effective than materials previously available. Factors as diverse
as insect resistance, microbial degradation of insecticides, the importance of pH and moisture, and
the role of the thatch or organic matter in preventing movement of the insecticides to the target
organisms have been reported by several authors as explanations for the reduction in insecticide
effectiveness (Villani et al. 1988, Niemczykand Chapman 1987, Niemczyk 1980). In addition, there
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is an increasing concern about the fate of insecticides in the environment and the potential of
pesticide runoff causing water contamination (November 1988, Watschke et al. 1988). All of the
above factors make the use of biological agents in the suppression of turf insects more attractive.
I will examine the biologicals that are available and access their place in suppression programs.
MICROORGANISMS
Several recent reviews and books examine the role of microorganisms in pest management
(Surges 1981, Samson et al. 1986, Fuxa 1987, Fuxa and Tanada 1987). Fleming (1968) reviewed
the history and status of biological control of the Japanese beetle up to 1968. In addition, Klein
(1982, 1988) reported on the state of biological suppression of turf insects in 1982, and pest
management of all soil-inhabiting insects with microorganisms in 1988. These sources will give the
reader additional details on those subjects. Bacteria are the most important microorganisms
available for biological suppression of white grubs. Protozoa and fungi are important natural
microorganisms in regulating grub populations, but neither is commercially available at the present
time (Klein 1988a).
Milky Disease Bacteria
The value of Bacillus popilliae Dutky and its role in the regulation of white grubs has been
examined in several recent book chapters (Klein 1988a, 1981a). This bacterium, EL popilliae. has
been used in the suppression of the Japanese beetle for over 50 years (Fleming 1968), and was
the first microbial insecticide registered in the United States. When the bacteria develop in the
hemolymph of Japanese beetle larvae, they produce billions of refractile spores and parasporal
bodies thus turning the infected grub a milky white and giving rise to the common name of the
disease (Fleming 1968). Between 1939 and 1951, Federal and State agencies produced and
distributed about 90 tons of spore powder at 132,299 sites in 15 different eastern states (Fleming
1968). At the present time, there are three commercial brands of milky disease products available.
Doom(R) and Japidemic(R) are manufactured as a powder containing 100 million spores/g by
Fairfax Biological Laboratories, Clinton Corners, NY. Reuter Laboratories, Manassas Park, VA
produces a powder and granular formulation under the brand name Grub AttackTM. For many
years, milky disease products were made by collecting Japanese beetle larvae from the field,
injecting them with IL popilliae. and harvesting spores from infected larvae (Fleming 1968).
However, more recently, Fairfax has been collecting naturally infected Japanese beetle larvae in
the field (Chittick 1987), and Reuter Laboratories intends to produce the bacteria in artificial media
(Obenchain 1988).
An application rate of 10 Ib/acre is recommended by both manufacturers. This is normally
accomplished by placing about 2 g of spore powder in spots in a grid on four foot intervals. When
large areas of turf are to be treated, a reduced rate of 2 Ib/acre (10 foot intervals) has been
registered. Community wide treatment programs have been the most successful in reducing larval
damage and adult populations (Fleming 1968, Fleming and Ladd 1979, Ladd and Klein 1982).
However, since the milky disease bacteria spread naturally in the field (Fleming 1968), it can be
beneficial to treat only a portion of the beetle infested area. Application of spore powder to portions
of two fairways of a Northeastern Ohio golf course resulted in the finding of milky larvae throughout
the course after two years (Klein 1978). Several years can elapse between application of milky
disease bacteria, and suppression of Japanese beetle populations (Fleming and Ladd 1979, Ladd
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and Klein 1982). The disease builds up and spreads as larvae ingest spores, become infected, die,
and release 1-2 billion spores back into the soil (Fleming 1968). Although one might expect that the
use of the granular material distributed over the whole area would speed up the larval suppression,
that may not be the case. Even though the broadcast treatment uses twice as many spores per
acre (Klein 1982) as the spot treatment, the spores may be spread so thinly that the larvae do not
become infected more quickly.
Soil temperatures may have a greater impact on larval suppression by milky disease bacteria
than does the application method (Klein 1988a, 1981a). Although temperatures of at least 16° C.
are necessary for development of the disease, temperatures of 21° C. are required for optimal
development (Fleming 1968, Fleming and Ladd 1979). Concerns about low soil temperatures have
caused State personnel in several New England states question the value of milky disease bacteria
in their areas. It should be noted however, that Fairfax Biological Laboratory obtains its naturally
infected milky grubs in these same areas (Chittick 1987) so the disease is working to some degree.
Daar (1988) has recommended quadrupling the dosage in areas above latitude 40° to speed up
development of the disease. More information is needed about the role of milky disease in the
northern ranges of the Japanese beetle. It is also possible that if B. popilliae can be grown on artificial
media that strains could be isolated that will be effective at lower temperatures. There is also a
concern about the persistence of EL popilliae spores in the environment (Klein 1988a). Although
spores are clearly present in soil that was last treated 25-30 years previously, it is not clear if that
is due to persistence or periodic replenishment as subsequent larvae become infected and die.
Production of EL popilliae on artificial media may also help to expand the host range of
commercial products to other white grubs. Although Grub Attack is listed as being effective on
certain May and June beetles, oriental beetle, and rose chafer in addition to Japanese beetle,
numerous studies indicate that each species is most susceptible to its own strain of EL popilliae
(Fleming 1968, Klein 1981a, 1982, 1986, 1988). Masked chafers (Cyclocephala spp.) are serious
turf pests nation wide, but are not infected by the commercial milky disease formulations (Klein
1981a, Warren and Potter 1983). EL popilliae infections are credited with holding Cyclocephala
paraliela Casey to sub-economic levels in Florida sugarcane fields (Boucias et al. 1986). Since
Cyclocephala strains of EL popilliae have grown on artificial media (Obenchain 1989), it may be
possible to produce a product for masked chafers. However, the costs in registering such a product
may not be supported by the potential market. In addition, although it is common to find high
incidences of natural milky disease in Cyclocephala larvae in turf areas, the true value of the disease
in population suppression has not been assessed. I have seen repeated turf damage in an area
following 50+% milky larvae the previous fall. The black turfgrass ataenius, Ataenius spretulus
(Haldeman) is another potential target for a milky disease product produced on artificial media.
These larvae have several strains of milky disease bacteria that build-up too late in the season to
have the full impact on the population (Tashiro 1987, Klein 1981a). Introduction of the spores into
the population earlier in the season may improve the situation.
Concerns about the attenuation of EL popilliae spores in Connecticut are still being expressed
(Hanula and Andreadis 1988). Although Tashiro (in 23) found in the laboratory that about 75% of
larvae became infected when placed in soil from Connecticut, Hanula and Andreadis (1988) noted
an incidence of only 3.5% milky larvae during extensive field surveys.
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Other Bacteria
Bacillus thuringiensis Berliner is the most widely used microorganism in commercial production
(Klein 1988a). Although it makes up at least 90% of the bioinsecticides on the market, it still makes
up less than 1% of the $13 billion pesticide market. EL thuringiensis products have been used
primarily against lepidopteran pests of forests and ornamentals. Strains of IL thurinaiensiswith
activity against Coleoptera have been isolated (Klein 1988a) giving rise to suggestions of using
them against the Japanese beetle (Bio Integral Resource Center 1987). However, recent tests
have shown that the coleopteran strains have no activity against either Japanese beetle larvae or
adults (Klein 1988b). It may be possible to isolate or create strains with activity against the Japanese
beetle or other Scarab adults. However, because of the short persistence of EL thuringiensis activity
in a soil environment ((West et al. 1984) it is unlikely that it will be an important microorganism
against the white grubs in the near future.
Bacteria in the genus Serratia have been associated with a disease of the grass grub,
Costelytra zealandica (White) in New Zealand (Jackson et al. 1986). The bacteria cause the grubs
to turn an amber or honey color by colonizing the gut, resulting in the starvation of the larvae and
depletion of the fat bodies. Commercial production of the bacteria is moving forward in New Zealand
(Jackson 1988). Similar honey colored Japanese beetle larvae have been observed in the United
States, and Serratia species have been isolated from them (Jackson 1988). The potential exists to
develop certain Serratia species for control of white grubs in the future.
Other Microorganisms
In addition to the bacteria, fungi and protozoa influence white grub populations. There are no
commercial fungal preparations available for use against Scarab beetles or larvae. Species of
Beauveria and Metarhizium are associated with insect mortality world wide (Klein 1988a), and have
been isolated from dead white grubs in this country (Tashiro 1987, Fleming 1968, Hanula and
Andreadis 1988). Work in Europe with the cockchafer. Melolantha melolantha (L.)r has shown that
a Beauveria species is effective when applied to the soil or to swarming females (Keller 1986). We
have a great deal to learn about the potential of fungi to aid in the suppression of white grub
populations.
Several genera of protozoa, in particular Nosema and Adelina. have been isolated from Scarab
larvae (Fleming 1968, Hanula and Andreadis 1988). Very little is known about the true effects of
these protozoa on white grub populations, and they are often overlooked. Recently a new protozoan
has been described from the Japanese beetle in Connecticut (Hanula and Andreadis 1988,
Andreadis and Hanula 1987). Ovavesicula popilliae Andreadis and Hanula was found infecting up
to 90% of Japanese beetle larvae locations (Hanula and Andreadis 1988). This microorganism has
the potential to be more fully utilized in the suppression of the Japanese beetle in the Eastern United
States.
ATTRACTANTS
The vast majority of work on attractants for Scarab species has been done with the Japanese
beetle. Fleming (1969) has summarized the work on Japanese beetle attractants from shortly after
the discovery of the beetle in New Jersey in 1916 up to 1969. Although chemical attractants have
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been noted for several other Scarab beetles, none have been developed commercially. Black lights
are available to attract several night flying beetles.
Japanese Beetle Attractants
At the present time, seven companies are producing Japanese beetle traps and lures. The
best lure is a combination of the synthetic female sex attractant, Japonilure, (Tumlinson et al. 1977)
and three sweet smelling floral or food type lures: phenethyl propionate, eugenol, and geraniol in a
3:7:3 combination (Ladd et al. 1981). Even though the sex attractant captures only male beetles
when used alone, when exposed in the presence of the floral lures it causes increased captures of
both male and female beetles (Ladd et al. 1981, Klein et al. 1981).
Although large numbers of beetles can be captured by Japanese beetle traps, the best uses
for the traps is still being studied. Klein (1981b) reported on several studies where traps were used
to reduce infestations of beetles. However, most workers agree that traps cannot be depended
upon to protect specific plants from beetle feeding (Fleming 1976, Ladd and Klein 1982, Fleming
1969). Recent studies involving heavy populations of beetles in Kentucky showed that there was
an increased damage to plants in the vicinity of Japanese beetle traps (Gordon and Potter 1985,
1986). The use of traps did not increase the population of larvae in near by turf. It has been
suggested that an antifeedant material such as neem may be applied to foliage to protect it when
traps are used in an area. A commercial product, Margosan-O (W. R. Grace, Co., Fogelsville, PA),
has recently been made available for testing. It is still to early to establish the value of such a
product. Since the material is an antifeedant for the Japanese beetle, and not a repellent, it would
appear that there is little future in spraying it on turf to discourage adult egg laying as had been
suggested (Bio Integral Resource Center 1987).
Other Attractants
Sex attractants have been demonstrated for the northern and southern masked chafers,
Cyclocephala borealis Arrow, and & immaculata (Oliver) (Potter 1989). More recently, both a sex
attractant and an aggregation pheromone have been found in the green June beetle, Cotinus nitida
(L) in Arkansas (Domek and Johnson 1987,1988). In addition, a chemical attractant, butyl sorbate
was shown to be an attractant for males and females of the European chafer(Tashiro 1987).
Commercial development of these will await the identification of the pheromones involved and a
demonstration of the value of the attractants.
CONCLUSIONS
Bacillus popilliae is the most important commercially available microorganism available for
suppression of white grub species. Its value should increase in the next few years if the promise of
production on artificial media is realized. We need more information about the value of other
microorganisms such as the fungi and protozoa so that they can be integrated into suppression
programs. Attractants for the Japanese beetle will continue to be available to consumers who wish
to use them. More information is needed on the value of all attractants for scarab beetles so their
full potential can be reached.
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2-10.
T. G. Andreadis, and J. L. Hanula. 1987. Ultrastructural study and description of Ovavesicula popilliae N.G., N. Sp.
(Microsporida: Pleistophoridae) from the Japanese beetle, Popillia japonica (Coleoptera: Scarabaeidae). i
Protozool. 34:15-21.
Bio Integral Resource Center. 1987. Least Toxic Lawn Management. Bio Integral Resource Center, Berkeley, CA, 38 pp.
D. G. Boucias, R. H. Cherry, and D. L Anderson. 1986. Incidence of Bacillus popilliae in Ligyrus subtropicus and
Cyclocephala parallels (Coleoptera: Scarabaeidae) in Florida sugarcane fields. Environ. Entomol. 15:703-706.
H. D. Surges. 1981. Microbial Control of Pests and Plant Diseases 1979-1980. Academic Press, London, 949 pp.
D. Chittick. 1987. Fairfax Biological Laboratory, Clinton Corners, NY. Personal communication.
P. P. Cobb. 1988. Warm season turf insect pests. Am. Lawn Appl. 9(7): 24-25.
S. Daar. 1988. Japanese beetles, an integrated approach to protecting your lawn. Fine Gardening 1(1):52-55.
J. M. Domek, and D. T. Johnson. 1988. Demonstration of semiochemically induced aggregation in the green June beetle,
Cotinis nitida (L.) (Coleoptera: Scarabaeidae). Environ. Entomol. 17:147-149.
J. M. Domek, and D. T. Johnson. 1987. Evidence of a sex pheromone in the green June beetle, Cotinus nitida (Coleoptera:
Scarabaeidae). J. Entomol. Sci. 22:264-267.
W. E. Fleming. 1968. Biological Control of the Japanese Beetle. Technical Bulletin No. 1383. U.S. Department of
Agriculture. U. S. Government Printing Office, Washington, DC, 78 pp.
W. E. Fleming. 1969. Attractants for the Japanese Beetle. Technical Bulletin No. 1399. U.S. Department of Agriculture.
U. S. Government Printing Office, Washington, DC, 64 pp.
W. E. Fleming. 1972. Biology of the Japanese Beetle. Technical Bulletin No. 1449. U.S. Department of Agriculture. U. S.
Government Printing Office, Washington, DC, 129 pp.
W. E. Fleming. 1976. Integrating Control of the Japanese Beetle-A Historical Review. Technical Bulletin No. 1545. U.S.
Department of Agriculture. U. S. Government Printing Office, Washington, DC, 64 pp.
W. E. Fleming, and T. L. Ladd. 1979. Milky Disease for Control of Japanese beetle Grubs. Leaflet No. 500. U.S.
Department of Agriculture. U. S. Government Printing Office, Washington, DC, 6 pp.
J. R. Fuxa. 1987. Ecological considerations for the use of entomopathogens in IPM. Ann. Rev. Entomol. 32:225-251.
J. R. Fuxa, and Y. Tanada. 1987. Epizootiology of Insect Diseases. Wiley, NY, 555 pp.
F. C. Gordon, and D. A. Potter. 1985. Efficiency of Japanese beetle (Coleoptera: Scarabaeidae) traps in reducing
defoliation of plants in the urban landscape and effect on larval density in turf. J. Econ. Entomol. 78: 774-778.
F. C. Gordon, and D. A. Potter. 1986. Japanese beetle (Coleoptera: Scarabaeidae) traps: evaluation of single and multiple
arrangements for reducing defoliation in urban landscape. J, Econ. Entomol. 79:1381-1384.
L A. Hall. 1987. Fort Valley State College, Fort Valley GA, Personal communication.
J. L Hanula, and T. G. Andreadis. 1988. Parasitic microorganisms of the Japanese beetle (Coleoptera: Scarabaeidae)
and associated Scarabaeidae larvae in Connecticut soils. Environ. Entomol. 17:709-714.
J. L. Hellman. 1988. University of Maryland, College Park, MD, Personal communication.
T. Jackson. 1988. MAFTech, Lincoln, New Zealand. Personal communication.
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T. A. Jackson, J. F. Pearson, and G. Stucki. 1986. Control of the grass grub, Costelytra zealandica (White) (Coleoptera:
Scarabaeidae) by application of the bacteria Serratia spp. causing honey disease. Bull. Entomol. Res. 76:69-76.
S. Keller. 1986. Control of May beetle grubs (Melolontha melolontha L) with the fungus Beauveria brongniartti
(Sacc.)Petch. Pp. 525-528 in: R. A. Samson, J. M. Vlak, and D. Peters, eds.. Fundamental and Applied Aspects
of Invertebrate Pathology. 4th International Colloquium of Invertebrate Pathology, Wageningen, The
Netherlands, 711 pp.
M. G. Klein. 1978. Unpublished data
M. G. Klein. 1981a. Advances in the use of BacjJJus pjjpilia® for pest control. Pp. 183-192 in: H. D. Rurges, ed., Microbial
Control Of Pests aM Plant Diseases 1970-1980. Academic Press, London, 949 pp.
M. G. Klein. 1981b. Mass trapping for suppression of Japanese beetles. Pp. 183-190. in: E. R. Mitchell ed., Management
of Insect Pests with Semiochemicals. Plenum, NY 514 pp.
M. G. Klein. 1982. Biological suppression of turf insects. Pp. 91-97 in: H. D. Niemczyk, and B. G. Joyner eds., Advances
in Turfgrass Entomology. ChemLawn Corp., Columbus, OH. 149 pp.
M. G. Klein. 1986. Bacillus popilliae: prospects and problems. Pp. 534-537 in: R. A. Samson, J. M. Vlak, and D. Peters,
eds., Fundamental and Applied Aspects of Invertebrate Pathology. 4th International Colloquium of Invertebrate
Pathology, Wageningen, The Netherlands, 711 pp.
M. G. Klein. 1988a. Pest management of soil-inhabiting insects with microorganisms. Agric. Ecosys. & Environ. In Press.
M. G. Klein. 1988b. Unpublished data.
M. G. Klein, J. H. Tumlinson, T. L Ladd, Jr., and R. E. Doolittle. 1981. Japanese beetle (Coleoptera: Scarabaeidae):
response to synthetic sex attractant plus phenethyl propionate: eugenol. J. Chem. Ecol. 7:1-7.
T. L. Ladd, and M. G. Klein. 1982. Controlling the Japanese Beetle. Home & Garden Bulletin No. 159. U.S. Department
of Agriculture. U. S. Government Printing Office, Washington, DC, 14 pp.
T. L. Ladd, M. G. Klein, and J. H. Tumlinson. 1981. Phenethyl propionate + eugenol + geraniol (3:7:3) and Japonilure: a
highly effective joint lure for Japanese beetles. J. Econ. Entomol. 74:665-667.
H. D. Niemczyk. 1980. The influence of application timing and posttreatment irrigation of the fate and effectiveness of
isofenphos for control of Japanese beetle (Coleoptera; Scarabaeidae) larvae in turfgrass. JL Econ. Entomol.
80:465-470.
H. D. Niemczyk, and R. A. Chapman. 1987. Evidence of enhanced degradation of isofenphos in turfgrass thatch and soil.
J. Econ. Entomol. 80: 880-882.
J. November. 1988. Runoff and ground water contamination. Amer. Lawn Appl. 9(7): 40-42.
F. Obenchain. 1989. Ringer, Eden Prarie, MN. Personal communication.
D. A. Potter. 1989. Flight activity and sex attraction of northern and southern masked chafers in Kentucky turfgrass. Ann.
Entomol. Soc. Amer. 73:414-417.
R. A. Samson, J. M. Vlak, and D. Peters. 1986. Fundamental and Applied Aspects of Invertebrate Pathology. 4th
International Colloquium of Invertebrate Pathology, Wageningen, The Netherlands, 711 pp.
H. Tashiro. 1987. Turfgrass Insects of the United States and Canada. Cornell Univ. Press, Ithaca, NY, 391 pp.
J. H. Tumlinson, M. G. Klein, R. E. Doolittle, T. L. Ladd, and A. T. Proveaux. 1977. Identification of the female Japanese
beetle sex pheromone: inhibition of male response by an enantiomer. Science. 789-792.
M. G. Villani, R. J. Wright, and P. B. Baker. 1988. Differential susceptibility of Japanese beetle, Oriental beetle, and
European chafer (Coleoptera: Scarabaeidae) larvae to five soil insecticides. J. Econ. Entomol. 81:785-788.
P. J. Vittum. 1988. Controlling Northern turf insects. AmSL Lawo AppJ. 9(7): 20-22.
P. J. Vittum. 1987. Home lawn IPM update. Amer. Lawn Appl. 8(10): 27-29.
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G. W. Warren, and D. A Potter. 1983. Pathogenicity of Bacillus popilliae (Cyclocephala strain) and other milky disease
bacteria in grubs of the southern masked chafer (Coleoptera: Scarabaeidae. J. Econ. Entomol. 76:69-73.
T. L. Watschke, G. Hamilton, and S. Harrison. 1988. Is pesticide runoff from turf increasing? AmsL Lawn AppJ. 9(7): 43-44.
G. W. West, H. D. Surges, R. J. White, and C. H. Wyborn. 1984. Persistence of Bacillus thuringiensis parasporal crystal
insecticidal activity in soil. J. Invert. Pathol. 44:128-133.
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FOOTNOTES
Mention of a proprietary product does not constitute endorsement by the USDA. In cooperation with
the Ohio Agricultural Research and Development Center, Ohio State University, Wooster and
approved for publication as Journal Article No. 268-88.
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ANNUAL BLUEGRASS TO BENTGRASS CONVERSION
WITH TURF GROWTH RETARDANTS (TGRs)
Dr. Milton E. Kageyama
and
Dr. Larry R. Widell
O. M. Scott and Sons Co.
Research Division
Marysville, OH 43041
INTRODUCTION
Another chapter has begun in the never-ending struggle between man and that baneful,
pernicious weed we collectively call annual bluegrass (Poa annua). Within the past several years,
an increasing number of golf course superintendent have chosen turf growth retardants (TGRs)
as an option to their existing, rather unsuccessful, control methods for reducing the spread of this
undesirable grass. This new dimension to Poa annua control is especially appealing to those who
desire a gradual transition to the more desirable grasses, such as bentgrass, without temporarily
taking greens and fairways out of play. However, we have observed that some turfgrass managers
are more adept than others at making turf growth retardants work for them. It cannot be
overemphasized that product knowledge and careful execution of the TGR program for Poa control
are the keys to greater success in the use of these products.
WHAT ARE TURF GROWTH RETARDANTS?
Turf growth retardants are a diverse group of plant growth regulators that act by blocking
gibberellic acid (GA) biosynthesis, a plant hormone influencing cell elongation, among other
functions. Retardant activity on turfgrasses results in shortened stem internodes and reduced leaf
and rhizome elongation. Diversion of photosynthate and altered hormone levels may be responsible
for increased tillering and subsequent greater turf density observed with TGR applications. These
effects are overcome by application of GA.
Examples of turf growth retardants currently being used on golf courses either commercially
or on an experimental basis include paclobutrazol (Fertilizer + TGR Poa annua control from O. M.
Scott & Sons Company) or flurprimidol (Gutless from Elanco Products). Both are gibberellin
antagonists but are not similar in chemical structure. Paclobutrazol is a triazole, a compound
containing a five-membered ring structure with three nitrogen atoms. Flurprimidol belongs to a class
of compounds possessing a six-membered ring containing two nitrogen atoms, the pyrimidines.
Despite their chemical dissimilarities, both compounds work in the same manner, selectively
controlling the growth of Poa annua and thereby resulting in a shift in competitive ability to favor the
more desirable, perennial grasses.
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HOW DO TGR's WORK?
The most important concept for the golf course superintendent to keep in mind when using
growth retardants for Poa annua control is that these compounds are mobile only in the xylem
(movement upward only) and therefore require root uptake to reach basal growing points. In
addition, differential species sensitivity is primarily attributed to greater uptake of the retardants by
the shallower-rooted annual bluegrass plants. Turfgrass managers can enhance TGR response
on Poa and maximize tolerance on desirable grasses by remembering this mode of action and
employing management techniques prior to application that are effective in spatially separating
actively-absorbing root zones of Poa annua from other grass roots.
Within one to two weeks following application of TGRs, growth control and discoloration of
annual bluegrass will become evident. During the period of growth regulation, the Poa annua plants
will remain alive but be very stunted in growth. Bentgrass will continue to grow but in a more prostrate
condition and may possibly appear "stringy" during this period of Poa growth regulation. Poa
seedhead suppression is attained by a reduction in the stalk, greatly reducing seedhead visibility.
The tremendous proliferation of spring seedheads causing poor playing surface conditions can be
avoided by making TGR applications in the spring just prior to the time seedheads begin emerging
on south-facing slopes or in warm soil areas. Applications at this time will greatly improve playing
conditions on fairways and greens for up to six weeks. Some seedheads will become visible in late
May/early June, but these will also be somewhat stunted and should not seriously impair payability.
Fall applications can also effectively reduce Poa seedhead visibility the following spring but for a
shorter duration (three to five weeks). Poa regreening should occur just prior to regrowth about five
to ten weeks after application . Inspection of the fairways and greens at this time should reveal
greatly improved coverage of bentgrass at the expense of annual bluegrass.
TURF RESPONSES TO TGR APPLICATION
• Severe reduction in growth of Poa annua 7 to 14 days after application, lasting from 4
to 10 weeks
• Shoot tissue discoloration (yellow-green to brown) of Poa annua for 3 to 8 weeks
• Aggressive growth of bentgrass for 4 to 8 weeks after an initial 14 to 20 day period of
reduced (50%) growth
• Spring seedhead stalk stunting for 5 to 6 weeks with spring or previous fall applications
• Regreening/regrowth of Poa annua 5 to 10 weeks after application
• Enhanced greening of bentgrass for 6 to 8 weeks
• Reduction in Poa annua coverage after application by 10 to 50%
• No reduction in bentgrass root growth
• No thinning of Poa annua under non-stress conditions
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PERFORMANCE VARIABILITY
It is not unusual for pesticides to perform variably. This is especially true for growth regulators
where the desired rate may be a fine line between tob much and too little activity. Delivery of effective
doses of TGRs into the Poa annua plant can be achieved by considering the physico-chemical
characteristics of TGRs. For instance, paclobutrazol displays rather low water solubility (30 ppm)
and readily adsorbs to organic matter and thatch. Therefore, its movement through the soil profile
is very limited except in sandy soils containing little organic matter. The insightful turf manager can
usually predict the nature of the growth regulation response of TGRs on Poa annua vs. bentgrass
by reflecting on the seasonal root growth dynamics of the two turf types and the soil type (texture).
The greatest differential response can be achieved with early summer applications on heavy soils
when uptake of nutrients and water occurs lower in the soil profile than paclobutrazol can move.
However, this response may not be desirable since it may result in aesthetically unpleasing color
on Poa annua for too long a time, especially on greens. The target regulation differential that is
most accepted by turfgrass managers occurs with mid-spring and late summer applications when
a moderate amount of activity is achieved on Poa annua. Less differential growth regulation will be
seen with fall applications when Poa annua roots begin to move deeper into the soil profile and
cooler, more moist weather conditions favor the growth of Poa.
Watering-in is essential for these systemic TGRs to work, whether they are formulated as a
granule or liquid. It is even more important to remove liquid TGRs from foliar surfaces to minimize
foliar uptake, volatilization, and photodecomposition. Recommendations state the need for 1/4" of
water within 48 hours to optimize activity, except in heavily-thatched areas where greater amounts
are needed. Aerating prior to application has proven to be very beneficial in these areas. Lack of
adequate rainfall or irrigation after application can greatly delay and/or reduce activity, especially
on heavy soils.
The degree of growth regulation can also be influenced by turf biotype. Conversion to
predominantly bentgrass greens where the initial amount of Poa annua is high has been
unsuccessful with the more upright colonial bentgrasses. Apparently these bentgrasses are not
aggressive enough to dominate while Poa annua is under regulation. Conversion on fairways also
appears to be less successful where the more perennial Poa annua biotypes proliferate.
PROGRAM SCHEDULING
It must be understood that Poa annua control with TGRs is a gradual process, requiring
sequential applications until the desired level of control is achieved. Applications must be made in
a constant, routine manner twice a year. Omitting applications before this time can lead to slower
long-term control. Once control has been achieved, routine annual treatments in late summer or
early fall should keep the Poa in check. Repeat applications over a two to three year period may
be required in some areas of high initial contamination. Programs using lower application rates with
greater application frequency do not provide any greater long-term benefits on fairways. However,
recent research on greens has shown promise when using lower rates every three to four weeks
in eradicating Poa annua without as much discoloration.
Proper time of application has already been considered with respect to root growth dynamics.
Timing must also be considered with respect to seeding, aerating and topdressing, and herbicide
application. The superintendent's primary consideration in the fall should be the sequence of events
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with respect to overseeding, a highly-recommended practice for high contamination areas. TGRs
offer greater flexibility than most preemergence controls since applications are not phytotoxic to
bentgrass seedlings. However, to avoid seedling growth regulation and slowed fill-in, wait at least
six weeks after overseeding before application; or in treated areas, wait at least two weeks after
application before overseeding.
AREAS OF USE
Retardants are effective in eradicating Poa annua on fairways, greens, and collars. Long-term
control of Poa on tees is more difficult because of the excessive wear on perennial turfgrasses and
the advantage annual bluegrass has reestablishing in divoted areas routinely irrigated. Overseeding
and filling divots with a sand/seed mix has proven to be a sound management practice in conjunction
with TGR use on especially those tees containing large amounts of Poa annua. The unevenness
of turf height on collars and greens caused by TGR use can result in undesirable lies and bumpy
putting conditions for a period of time. A light sand topdressing during the cooler periods of the
season can certainly improve ball roll on greens. Applications of retardants to nearby perennial
bluegrass collars should be avoided since the extent to discoloration in these highly visible areas
may not be acceptable.
THE NEED FOR NITROGEN
Best encroachment and stoloniferous action of bentgrass on fairways and greens are
accomplished when these areas are well-fertilized at the time of TGR application. Abiding by the
long-standing rule of encouraging the bentgrass by starving the predominantly annual bluegrass
turf through a very judicious fertilizer program does not necessarily apply when using TGRs.
Conversely, moderate-to-heavy fertilizations just before bentgrass starts growth in the spring
will actually provide greater Poa annua suppression. Spring applications of TGR and nitrogen
should be applied early enough to minimize the risk of lush growth when hot severe weather
develops and Pythium invasion is likely. In areas of recurrent disease problems, fungicide
applications should be used on a preventative basis and intervals tightened somewhat, since TGRs
can increase the turf's susceptibility to Pythium and snow mold. In addition to shifting the uptake
and assimilation of nitrogen to bentgrass, the use of TGRs with fertilizers also results in a very
dramatic greening of bentgrass, lasting longer than conventional fertilizers alone. Poa annua will
also benefit from this combination treatment after the growth retardation subsides, resulting in a
greener, healthier Poa annua/bentgrass turf throughout the ensuing stress periods.
OTHER BENEFITS
Not only will TGRs provide more consistent, higher quality bentgrass fairways and greens but
other benefits that the superintendent can enjoy include (1) significant labor savings in the spring
and fall due to fewer required mowings on fairways and less clippings to dispose of on greens, (2)
reduced water use due to the lower water requirements of bentgrass (a significant benefit in areas
faced with impending watering restrictions), (3) reduced fertilizer use, and (4) faster, more true ball
roll on greens containing primarily bentgrass.
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CONCLUSION
The science of growing turfgrass has taken a significant leap forward with the introduction of
growth retardant chemistry. Users of these sophisticated tools must be informed about their proper
application and the way they fit into existing turf management programs. It is essential to inform the
greens committee and membership of this course of action to explain the visual results. It is also a
good idea in some situations to begin a program on a limited basis to understand how these
chemicals are used and what to expect. The progress of this program can most easily be measured
by leaving a small portion of one fairway untreated by covering the area with a cloth or piece of
plywood.
The committed, informed superintendents are now making major strides in controlling the fate
of their golf courses. Growing and maintaining high quality bentgrass fairways and greens is not
an accident but the result of responsible blending of turfgrass art and science.
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Evaluation of the Site/Pest Complex:
A Starting Point for Development
of an Urban Pest Management
System for Turfgrass
SECTION VII
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DEVELOPMENT OF AN IPM PROGRAM FOR TURFGRASS
Anne R. Leslie
U.S. Environmental Protection Agency
401 M Street SW
Washington, DC 20460
A number of promising biological controls and cultural practices for turfgrass have been
presented in detail above. Although some of these are not yet available for general use, they are
expected to form an important part of the management tools needed to deal with pest problems.
However, the basic steps to design an IPM program for turfgrass can be presented so that turfgrass
managers can make best use of all control methods and realize economy in management with no
loss of turfgrass quality.
We start with our working definition: Integrated Pest Management is the coordinated use of
pest and environmental information with available pest control methods to prevent unacceptable
levels of pest damage by the most economical means, and with the least possible hazard to people,
property and the environment. The goal of the IPM approach is to manage pests and the
environment so as to balance costs, benefits, public health and environmental quality. IPM systems
use all available technical information on the pest and its interaction with the environment. Because
IPM programs apply a holistic approach to pest management decision-making, they take advantage
of all appropriate pest management options, including but not limited to pesticides. Thus, IPM is:
• A system utilizing multiple methods
• A decision-making process
• A risk reduction system
• Information intensive
• Cost effective
• Site specific.
COMPONENTS IN A GENERIC PEST MANAGEMENT SYSTEM
A generic pest management system includes the eight distinct steps that are outlined here:
1. Define the roles of all the people involved in the pest management system (i.e., occupant, pest
manager, decision-maker), assure understanding and establish communications between
them.
2. Determine the management objectives for each of the specific areas of the site as a basis for
deciding on possible control methods for the pest.
3. Set action thresholds-a point when pest populations or environmental conditions indicate that
some action must be taken; no action is taken until that point is reached.
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4. Monitor the site environment and pest population on a periodic, consistent basis to determine
when the action threshold is reached and to determine whether the action taken is effective.
5. Take action that modifies the pest habitat to reduce carrying capacity of the site, exclude the
pest, or otherwise make the site environment incompatible with the needs of the pest.
6. Take appropriate pesticidal action. A preferred pesticide would provide the longest dwell time
in contact with the pest while presenting the least possible hazard to the people, property and
the environment. It should be applied when the pest is in its most vulnerable stage.
7. Evaluate the results of the habitat modification and pesticidal treatment actions by periodically
monitoring the site environment and pest populations.
8. Keep written records of site pest management objectives, monitoring methods and data
collected, actions taken, and the results obtained by the pest management system methods.
All components of this system must be addressed and implemented in some form for the
system to be most effective. Omission of portions of the system, in our experience, has led to greater
unnecessary dependence on repeated pesticidal treatments.
Since IPM is site specific and information intensive, each site manager will need to develop a
plan that meets the management goals established in Step One. Some thought should be given to
identify all the people who fall into the categories of occupant, pest manager and decision-maker.
For instance, people who do not golf but who use the land neighboring a golf course must be
considered occupants if management practices on the course can potentially impact their
environment. Similarly, the golf course management, in setting management goals that include very
short, smooth greens for fast play, should consider the needs of the people using a water supply
that may be impacted by the pesticides required to attain the desired greens quality. That
consideration might involve choosing between a costly groundwater monitoring program and a
slightly altered mowing height that can result in a lower pest pressure. Other innovative solutions
to problems may be achieved if all the "actors"are willing to communicate their real concerns and
work productively toward their resolution.
An outstanding example of the progress that can be achieved is the cooperative effort in
Massachusetts between the Massachusetts Golf Course Superintendents Association and the state
regulatory agencies and universities. This effort has led to implementation of IPM programs at golf
courses across the state.
With the above components in mind, we can define the strategies that would be important for
turf areas with different management goals. A number of strategies will be listed for three kinds of
sites. A good monitoring plan, with action thresholds and proper record keeping, will be used to
evaluate the effectiveness of these strategies.
Site A: High Management Turf.
Example: Golf Course Greens and Tees
1. Establish pest-resistant varieties of grass suitable to the site, climate, and expected use.
2. Use bacterial or biochemical control, such as plant growth regulators, for poa annua on tees
and greens.
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3. Use biological controls, such as nematodes for control of white grubs, and endophytic grasses
for surface feeding insects.
4. Raise mowing height and reduce watering frequency to reduce weed populations and
expression of fungus disease; evaluate problem areas and the need for drainage control and/or
irrigation system improvements; use slow release fertilizers along with soil amendments.
5. Use caning and syringing as methods of stress reduction to reduce threat of fungus damage
in summer months.
6. Put fungicide use on a strict degree/moisture threshold schedule by use of computerized
monitoring and diagnostic tests to determine disease potential; select least invasive effective
fungicidal treatment; consider rotation or tank mixes of fungicides to reduce resistance buildup.
7. Monitor for changes in populations of flora and fauna, beneficial as well as destructive.
8. Educate the public and the course management on the strategies being used at the site.
Site B: Medium Management Turf.
Example: Home lawn or public lawn other than golf course
1. Evaluate the soil for pH, texture and type; use soil amendments and consider renovation rather
than heavy use of pesticides to solve problems.
2. Overseed or plant a variety that suits the use pattern and site.
3. Set up action thresholds and monitoring methods for weeds and insects. Note that disease
problems in home lawns are almost always due to over fertilization and over watering. Note
also that there should be greater tolerance for pest populations and the use stress on the grass
will probably be less than on site A.
4. Establish proper cultural practices; for example, water deeply when the wilt point is reached
rather than on a calendar schedule, use slow release fertilizer, increase mowing height and
frequency, leave clippings on the lawn and include periodic aeration by vertical mowing or
dethatching.
Site C: Low Maintenance (or "NoPesticide")Turf.
Example: Some Park Sites, Homeowners Interested In Alternatives to Tlirf
1. Use mowing to control woody plants, and encourage growth of native species, rather than
adhere to a monoculture of grass.
2. Use grass varieties suitable to the use pattern; have paving where heavy traffic is expected.
3. Convert some areas to meadow by planting wildflower cover, minimizing long term
maintenance, especially in areas where it is difficult to maintain grass.
4. Use monitoring to help with decisions on aggressive plant control. Not much is known of the life
cycle of many such plants, and if this is studied carefully, the manager will be better able to
choose the least invasive method of control.
5. Use biological controls on pests wherever feasible.
6. Use good cultural practices as in Site B.
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To continue to improve IPM programs, there should be continuing research on a number of
questions, such as:
1. What are the effects of pesticides on beneficials in greens and tees?
2. Is there a pest population difference between greens, tees, fairways and roughs that is the
result of pesticide use, and are pesticides perpetuating problems?
3. What natural predator biocontrols can be found to decrease high populations of pests on
monoculture areas?
4. Does healthy turfgrass act as a barrier to surface water and groundwater pesticide
contamination in golf course watersheds? What kinds of irrigation systems and soil
amendments will minimize problems?
5. What are the real economic benefits of an IPM program for turfgrass?
EPA is planning projects at several of the sites discussed. A Memorandum of Agreement is
being processed between EPA and the Military District of Washington to establish cooperation
on a survey of IPM practices at military establishments in the D.C. area. This agreement
addresses the presidential order of September 2,1979, which requests all agencies to "support
and adopt IPM strategies whenever practicable" and to "assess the potential for increased
emphasis on integrated pest management." The military establishments offer managed
turfgrass at all levels listed, including parade grounds, home lawns, parks and golf courses.
In addition, because golf courses involve high level management and are highly visible
targets for environmental concern, EPA has proposed to develop an IPM demonstration project
at several golf courses in the northeast. We believe that such projects will greatly contribute to
the establishment of safe, sound pest management of the growing recreational land use
demanded by the American public. Such land use should be compatible with the surrounding
environment and the plans should address the reasonable concerns of the neighboring
residents. By cooperative efforts landowners should be able to develop their holdings as they
wish and still contribute something of value to the entire community.
Only continued, careful investigation and a commitment to meaningful use of IPM
techniques in urban turfgrass management will enable managers to achieve reduction of
dependence on chemical controls. It is hoped that expert systems will be developed that will
assist the professional turfgrass manager. The final chapter addresses this technology and
what such a system can and cannot do.
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KNOWLEDGE BASED SYSTEMS FOR USE IN
INTEGRATED PEST MANAGEMENT:
REQUIREMENTS, PITFALLS, AND OPPORTUNITIES
Jan P. Nyrop
Department of Entomology
New York State Agricultural Experiment Station
Cornell University
Geneva, NY 14456
Bernie Huber
IPM Program
New York State Agricultural Experiment Station
Cornell University
Geneva, NY 14456
Walter Wolf
Department of Computer Science
Rochester Institute of Technology
Rochester, NY
Naive, prophylactic application of pesticides continues to be a frequently used pest control
tactic. This approach to pest control results in needless expense by crop managers, unjustified
exposure of the environment to chemical toxicants, and hastened resistance by pests to chemical
pesticides. To counter the myriad costs of excessive chemical pesticide use, a more economic and
ecologically rational pest control paradigm has been advocated; integrated pest management
(IPM). Ideally, IPM entails a multi-faceted pest control effort through the use of cultural practices,
the conservation and possible augmentation of biological control agents, and the judicious use of
chemical pesticides. Even in its most simplified form of using monitoring and action thresholds to
schedule pesticide applications, IPM can greatly reduce the use of chemical pesticides. In many
cropping systems a library of IPM technologies has been developed through research. However the
adoption and use of IPM has been frustratingly slow.
Wearing (1988) groups causes for this slow acceptance into five classes. First, requisite tools
for IPM such as simple monitoring methods and selective control strategies may be lacking. Second,
the actual and/or perceived costs of practicing IPM may not be conducive to its adoption. Third,
deficiency in knowledge required by growers to use IPM methods may hinder adoption. Fourth,
crop managers are generally satisfied with chemical control and often lack confidence in IPM
methods. Finally, the lack of trained experts needed to educate and provide consultation to growers
about IPM may limit its adoption. This paper will focus on a relatively new computer technology
that offers a means of overcoming this last impediment to the adoption of IPM.
Use of IPM necessitates a considerable degree of expertise in applying and integrating many
sources and types of information and often requires the simultaneous consideration of multiple crop
protection goals. In addition crop managers often do not have the skill or background to effectively
use many IPM tools. A recently proposed solution to the problem of insufficient availability of
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expertise in IPM is the development of expert or knowledge based systems (Coulson and Saunders
1987, Naegle et al 1986, Stone et al 1986). Unfortunately, the term "expertsystem" has been badly
misused and misunderstood. Thus we will employ the more generic name"knowledge-based
systems" (KBS). In this paper we present our views on the requirements, pitfalls and opportunities
associated with developing KBS's for use in pest management. These views have developed as a
result of our work on a KBS for use in apple pest management (EASY-MACS; Expert Advisory
SYstem for Managing Apple Cropping Systems) and through study of the literature dealing with
KBS's. While EASY-MACS deals specifically with apple cropping systems, the discussion presented
here is germane to all pest management systems including those in the urban environment. The
paper is composed of three sections. First, we provide a brief overview of what knowledge based
systems are and present some details about the EASY-MACS system in order to illustrate an actual
system. Our intent here is to provide a setting for the remainder of the paper and not to provide a
full explanation of how knowledge based systems work. There are a number of accessible reviews
detailing the nature of KBS's (e.g. Waterman 1986, Davis 1986). In the second section, we discuss
requirements for building a KBS for use in pest management and present pitfalls that we and others
have encountered in developing knowledge based systems. An understanding of these
requirements and pitfalls is important because they are frequently masked by the hyperbole that
ensconces a new technology. Finally we discuss the opportunities for use of KBS's in IPM.
WHAT ARE KNOWLEDGE BASED SYSTEMS?
A knowledge based system is a computer program specially designed to represent human
expertise in a particular domain of knowledge. It attempts to mimic a human being's ability to make
complicated decisions and is designed to assist a user to make similar decisions. For this reason,
knowledge based systems may also be called decision support systems. These systems act as
intelligent assistants to human experts, and also assist people who might not otherwise have access
to expertise. They have been developed and used extensively in medicine and industry, and are
now finding application in agriculture.
The techniques used to develop KBS's are products of investigations that have delved into the
possibility that computers could behave in a way that would be perceived as intelligent. This line of
research, known as artificial intelligence (Al) had its roots in a conference that took place in 1956
at Dartmouth College. Early work in Al emphasized development of computer systems that could
solve very general problems. Repeated failures at this endeavor led to the realization that much of
the power in problem solving lies in possessing a great deal of specific knowledge about the problem
and its likely solution. This led to research that examined how to represent such knowledge on a
computer and how to manipulate it. The end products of this work are the tools for developing
knowledge based systems.
The principal parts of an expert system are a knowledge base coupled with an inference
engine, and a user interface. The knowledge base is a collection of facts, expert opinions,
'rules-of-thumb' or heuristic knowledge, and procedural knowledge including relationships amongst
these facts, etc. The knowledge is that which an expert would employ to solve a particular problem.
The inference engine drives the system during a consultation by a user. It controls what portion of
the knowledge base should be used to solve a particular problem.
One of the most frequently used methods of representing knowledge is through a construct
known as if - then rules. If the antecedent of such a rule (the if part) is true, then the consequent
portion (the then part) is also true. An example of an if - then rule in pest management might be; if
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the density of pest A is greater than Y and if the median development of pest A is at least Z then it
is appropriate to treat for pest A. The inference engine controls the linking of the if - then rules in
order to reach a conclusion. Other rules would likely have to be used to determine the density of
pest A and if the median development exceeded Z. The inference engine would control the execution
of these rules. One can also envision a group of rules being used to determine the best pesticide
to use once it is established that a treatment should be made.
The user interface elicits needed information from the user, presents the results of a
consultation (i.e. a diagnosis or recommendation) to the user, and offers explanations supporting
those results. In addition to these major components, a KBS may also access databases and
simulation models to obtain needed information.
One way to picture a KBS is by way of analogy to a system of logic (Denning 1986). A system
of logic consists of axioms that are self-evident or universally recognized truths and rules of
inference. New knowledge, usually in the form of proofs, are derived from this system by sequencing
strings of axioms or prior proofs using the rules of inference. A KBS is analogous with some notable
differences. A KBS may contain axioms but it also contains other statements of fact (e.g., expert
opinion) that are used as axioms but clearly do not meet the definition of an axiom. In addition, the
rules of inference used by a KBS will often not be universally agreed upon.
We will now provide a description of the EASY-MACS system in order to more specifically
illustrate some of the points made above. EASY-MACS is designed to be a coach for implementing
integrated management of arthropod pests of apples. It runs on an Apple Macintosh computer and
is being developed using NEXPERT (Neuron Data, Palo Alto, CA). Like a human consultant, the
system asks the client for detailed information about the current condition of his orchard block. It
then makes a recommendation for action based upon that information, the history of that orchard
block, and the system's own knowledge of pest dynamics. EASY-MACS may also warn the user
of upcoming events and make tentative predictions about the future.
In the process of arriving at a recommendation, EASY-MACS takes into accountstate-of-the-
world considerations, such as the physical makeup and the phenological stage of the apple trees,
and the current pest infestation level. These external conditions are then combined with internal
considerations, such as the interactions that occur when more than one pest is present, or that the
presence of a biological control agent is important, or user preference requests an alternate
recommendation.
The system is made up of three components: 1) A Rule Base and Inference Engine. The rule
base encodes knowledge needed to make decisions about apple pest control. The inference engine
links relevant portions of the knowledge base in order to obtain needed data from a user and to
arrive at a recommended course of action. The following is a fairly complex example of the kind of
considerations that compose a rule and allow the system to arrive at a recommendation. The first
block of statements (the MIF"part) are conditions which may or may not be true. If all the conditions
listed in a rule are true, then the hypothesis (the 'THEN"part) is true and the actions (the last block
of statements) associated with that rule are carried out. These actions may in turn affect the
evaluation of further conditions composing other hypotheses.
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IF the phenological stage of the block is Pink,
AND Spotted Tentiform Leaf miner infestation is a problem,
AND Rosy Apple Aphid infestation is not a problem,
AND the block has a history of Oblique Banded Leaf roller damage,
AND Recommend applying Lannate at Petal Fall to control Spotted Tentiform Leaf miner
and Oblique Banded Leaf roller (TRUE),
AND you choose not to follow this recommendation,
AND the pesticide Dimilin is not currently available,
AND Recommend applying Vydate at Pink to control Spotted Tentiform Leafminer
(TRUE),
THEN a recommendation for pest control has been made,
AND record that Vydate has been recommended at Pink to control Spotted Tentiform
Leafminer,
AND record that Rosy Apple Aphid was not a problem at Pink, ^ ,
AND inform the user that he should sample for Oblique Banded Leafroller at Bloom.
In this example the conditions end with a recommendation of Vydate because the best expert
opinion does not have a good alternate recommendation to make. The dynamic features of the
system, however, allow that the user may actually use a different treatment, and so, any rule which
considers a spray material that has already been applied will explicitly ask the user what, if any,
material he used.
An interesting feature of the system is that recommendations are treated as conditions which
are always true. This allows that other conditions may follow before a given hypothesis is determined
to be true. In the above example, an additional condition is that the user accept the recommendation.
Here he rejects the recommendation, and an alternate recommendation is made after checking a
further condition (the availability for use of Dimilin).
The example rule belongs to a set of similar rules; each rule in that set leads to the same
hypothesis. In the course of a consultation, this particular hypothesis will always be proven true,
and one and only one rule in its rule set will have all of its conditions be true. An individual
knowledge-base may contain many such hypotheses, each with its own rule set. This kind of rule
organization allows for maximum flexibility in dealing with pest interactions, user preferences, and
conditions which may vary over time (such as the availability of a particular pesticide). This flexibility
is most evident in that the rules that belong to a particular set do not have to be composed of a
uniform set of conditions. For instance, if both Spotted Tentiform Leafminer and Rosy Apple Aphid
were a problem in a particular orchard block, then a single pesticide recommendation would be
made to control both of these pests, and a history of Oblique Banded Leafroller damage would not
be a condition in that particular rule since it would not affect the recommendation.
A condition may itself represent a set of rules. In the example given, those conditions that
deal with pest infestation levels are in turn dependent upon other condition sets, ones that are
made up of block characteristics, past pesticide use, and results of samples taken to determine the
density of the pest in question. Just how that information is gathered will be described in the next
section.
It should be noted that this example is a logical rendering of the state of the system after its
hypothesis has been proven. Actual implementation details are different in some small respects,
and will not be discussed here since they would unnecessarily complicate the description and might
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obscure our view of the logical situation. Procedural details (that is, the operation of the inference
engine) are best summed up by saying that the system considers the conditions in the order in which
they appear, and that alternate rules contain the alternate evaluations of those conditions which are
necessary to arrive at a recommendation. The overall operation of the inference engine as it works
its way through the whole system (a collection of hypotheses and associated rule sets) will not be
described here.
2) A User Interface. The user of this system sees a series of pre-designed screens. These
screens are displayed on the computer and consist of text and graphic images. The only data
actually typed into the system is a block name that is used to index data written to a database and
can be used by the system at a later time. All other information is supplied by selecting labeled
boxes on the screens. The screens are of three types: data entry; instruction and illustration; and
recommendation and explanation.
Whenever the system needs information that it can not deduce or that has not been previously
entered, it displays a screen that will be used to obtain the data from a user. The screen will ask the
user to supply the necessary information, and it will display all the alternatives that the system
recognizes. The user's only choice is to choose one of those alternatives via the "point and click"
operation of a mouse system. Care has been taken to include all reasonable alternatives, and to
include such options as "unknown"and "other"to take care of those cases where the user does not
know the information, or knows a different alternative than those that were considered by the
system's designers. The system can accept such catchall alternatives by converting them into
default values, ones that usually represent the most conservative interpretation of the condition.
The advantage of such a closed system for eliciting information from the user is that the chance for
minor errors such as spelling inconsistencies or typing errors are eliminated. While such minor
errors might pass unnoticed between human beings, they would of course be catastrophic to the
system, which believes that "lannate"is always "lannate"and never "lanate".
While eliminating mechanical errors is important to the smooth operation of the system, it is
even more important to insure that the alternative chosen by the user does indeed reflect the state
of the orchard block. In order to assist the user in choosing the correct alternative, instruction and
illustration screens are provided. In some cases this is as simple as providing a picture to show
what an insect looks like at a particular stage in its life cycle. In some cases, however, the kind of
information required of the user goes beyond mere identification, and involves quantitative analysis
(how many Rosy Apple Aphids have to be present to justify applying a pesticide, for instance). In
these cases, much more detailed instructions are given to the user. These instructions may involve
many screens giving the user detailed instructions on how to determine the density of a pest
population. These more complicated instructions involve extensive use of hypercard and hypertext
facilities provided by the Macintosh computer and the capabilities of the development tool. The
user is free to move back and forth through these screens; he may browse the instructions provided,
and he may choose to read more detailed presentations of what he does not understand. All of
these instruction and illustration screens have been implemented in the same "point and click"
fashion as previously mentioned.
The third kind of screen belongs to the area of recommendation and explanation. When the
system has enough information, it makes a recommendation for treatment (two such recommendations
occur in the example rule above). Attached to these recommendation screens are screens which
give detailed explanations of why a particular action is being recommended to control a particular
pest. These screens may also partially justify the recommendation by reminding the user of some
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of the information he has previously entered in response to the system's queries. However, the
major focus of the explanation screens is not to justify, but rather is to explain the expert's reasons
for recommending a particular treatment, or perhaps, a lack of treatment. The explanation screens
attempt to address the user's concerns, and to deal with subtleties that could not be addressed in
the rules. They may, for instance, give information about the effects of the recommended pesticide
on other pests, or on certain cultivars or strains of apples. These explanation screens attempt to
mimic a human expert by giving all those details that are not expected from a computerized system.
While the rule system itself will only remember what value went into what slot, the user will have
access to a great deal of additional information.
3) Data Bases. EASY-MACS has been designed to be consulted at certain key times
throughout the course of a growing season. These key times correspond to various phenological
stages in the growth of apples. In addition, only a predetermined set of conditions are considered
at each growth stage. This situation has been reflected in the design of the knowledge base which
is broken up into a number of smaller knowledge bases. Each of these modules is designed to be
consulted at a particular phenological stage. Several data bases retain information generated by
consultations at successive growth stages. These databases serve as a history of the block for the
current season. They also serve as communication among the various knowledge bases, so that
information gained at one session is available for use at a later session. For instance, the system
would like to know at the summer sessions what pesticides have been previously applied to the
block. Such information can be useful in determining whether there is a possibility of the block
containing predators that feed on phytophagous mites. The presence of mite predators may in turn
obviate the need for an early summer application of a miticide. Besides serving as a communication
between the knowledge bases, the data bases also serve as record keepers, allowing us to see
what kind of pest pressure has been encountered throughout the growing season, and how often
the system users have chosen treatments other than those recommended by EASY-MACS. Such
information can then be considered when making changes to future versions of the system.
In the previous example information would be written to the database that would record the
recommendation of Vydate as a treatment for Spotted Tentiform Leafminer at Pink, and that would
record that Rosy Apple Aphid was not a problem at Pink. In addition, the data base would record
the fact that the user should sample for Oblique Banded Leafroller infestation at Bloom. The user
will be reminded of this when he consults the system at Bloom; in the course of the same
consultation, he will be asked what spray he actually applied at Pink.
REQUIREMENTS FOR BUILDING A KBS FOR USE IN IPM
There are many requirements that must be met prior to and during development of a KBS.
Before embarking on a KBS project, the effort should be deemed justified and feasible. During
development of the system it is important that an appropriate methodology be used to codify the
knowledge and that management and evaluation of the system be considered from the start. We
will now discuss these requirements in more detail and relate them to our work on the EASY-MACS
system.
Developing an expert system is an expensive and time-consuming endeavor. A prototype
system based on a few hundred rules can often be built in a couple of months. However, it is not
unusual that a KBS requires several thousand rules and several years to build. In addition, once a
complete KBS is developed, a final deliverable product must be produced. This will usually involve
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significant product enhancement where factors such as performance, usability, documentation and
reliability come into play. This stage of the KBS effort may require two to three times the effort
required to develop the basic system (Cupello and Mishelevich 1988). As a result of development
costs, prudence dictates that a careful evaluation be made of both the justification and feasibility
of a proposed project. Waterman (1986) provides a list of criteria which should be satisfied in order
to justify the development of a KBS and another set of criteria that can be used to assess the
feasibility of a KBS project. Prerau (1985) also discusses criteria appropriate for determining the
feasibility of a KBS project. We used these criteria to evaluate whether a KBS for apple pest
management was justified and feasible. Justification for development of a KBS rests on two principal
criteria; 1) solution of the problem to be dealt with by the KBS should have a high payoff and 2)
expertise required to solve the problem dealt with by the KBS should be a scarce resource. The
goal of the EASY-MACS system is to provide expertise necessary to realize integrated control of
apple pests at the farm level. The desirability of IPM and potential benefits accruing from its adoption
justify the cost of developing a KBS in this domain. It is also clear to us that in this problem domain
human expertise is scarce. That is, there are few experts who can provide expertise required to
realize apple IPM. In addition, the cost of providing human expertise for this purpose is high.
Concluding that human expertise is scarce does not however guarantee that the expertise
necessary to develop a KBS exists. This is a particularly dangerous trap to fall in, especially from
the standpoint of developing KBSs for use in agriculture. Many of the experts to be relied on for
contributing knowledge to a KBS are principally involved in research rather than applications or are
experts in only a portion of the complete problem domain. Therefore, the potential exists to
overestimate the availability of the knowledge necessary to develop the system.
There are two principal criteria which must be met in order to conclude that expert system
development is possible. First, it must be determined that the problem to be solved is sufficiently
well understood that a solution can be found. As a corollary, genuine experts must exist and they
must be able to articulate the methods they use to arrive at a solution. Also, if multiple experts are
used, the experts must agree on solutions. We feel that the best way to determine that the expertise
necessary to render a solution to a problem exists is to observe this expertise in action under a
real world setting. Thus, one year prior to beginning development of EASY-MACS, part of the
knowledge to be encoded in the system was put into practice under the guidance of some of the
experts to be used in system development. Essentially we were asking whether an expert's
performance on this problem was measurably better than that of an inexperienced individual. While
this did not ensure that all the expertise required would be available, it did provide us with some
assurance that a reasonable knowledge base existed.
The second criteria that must be met in order to conclude that KBS development is possible
is that the task to be addressed should not be too difficult nor should it be too simple. Whether a
task is so simple that a KBS is unnecessary can usually be ascertained. If a task is simple it should
be possible to write down instructions that are to be carried out in order to complete it. If this can
be done, then a KBS is not necessary. Whether a task is too difficult for a KBS solution is more
difficult to determine. Some insight in this regard can by obtained by determining whether the
problem domain is reasonably bounded. In other words, can the extent of the knowledge required
to solve the problem be delimited or is a vast array of knowledge required that resides outside of
the boundaries of the problem. Another strategy is to develop a prototype system to test the concept
of building a more complete system.
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KBS's are unlike many other computer programs in that the gathering of knowledge for
inclusion in them tends to be harder and more important than the actual coding of the system.
Typically, KBS's are constructed by a team consisting of an expert, a knowledge engineer and a
programmer (the same person may serve the latter two functions). The role of the knowledge
engineer is to elicit the knowledge of the expert through a series of interviews and state it in a form
amenable to computer codification. Furthermore, a rapid prototyping methodology is frequently
advocated (Waterman 1986). This approach places an emphasis on rapidly achieving a working
system, even if only a simplified one, rather than on design and specification. A system may have
to be discarded and rewritten many times before the final program is arrived at. The main advantage
of this method is that it is often difficult to specify a KBS in advance; the process itself assists in
arriving at the specification. However, this reasoning has probably been taken too far. For example,
McKinion and Lemmon (1985) state that through the use of a rapid prototyping methodology, system
developers can explore ill-specified, ill-understood, and changeable requirements and that a
problem does not necessarily have to be well understood in order to be amenable to a KBS solution.
We strongly feel that this is not true. Taken to this extreme, the rapid prototyping approach is likely
to produce an inconsistent and incomplete knowledge base. In short a system produced using this
methodology is not likely to be reliable (Denning 1986).
There are at least two good reasons not to follow this paradigm for KBS development explicitly.
In the EASY-MACS project we departed from this paradigm by using a team of experts that included
an individual who was knowledgeable about KBS technology and apple IPM and by employing
some more conventional software engineering methods.
The first reason for not using the frequently cited development model centers on codifying the
knowledge to be placed in the system. IPM knowledge is rather diffuse, that is experts are usually
knowledgeable in rather limited sub-fields and in the areas where experts overlap they often don't
agree. Thus, to develop EASY-MACS a team of experts was used that met as a group and were
required to come to consensus concerning the knowledge to be incorporated into the KBS. The
process of consensus was difficult and only worked because a project coordinator was available
who could serve as an intermediary. This individual was a expert in the field, but also was familiar
with computers and their requirements for knowledge representation and manipulation. The second
reason for using the team of experts centers around articulating the knowledge to be placed in the
KBS. Parnas (1985) has argued that a trial and error approach to eliciting knowledge for use in a
KBS is likely to produce an incomplete and inconsistent knowledge base and that instead of
examining how people (experts) solve problems, attention should be devoted to studying the
problem itself. An expert may not know why a particular method works and a knowledge engineer
may not ask the right questions which will allow an expert to articulate his methods. We found that
by using a team of experts considerable attention was devoted towards studying the problem itself
and as a result, a more consistent and complete knowledge base was developed.
EASY-MACS is not a typical system in that it deals with a series of consultations over time
rather than a single session. This immediately suggested using a modular design and incorporating
a system 'memory' (data base). Each of the smaller knowledge bases could have sub-goals of their
own, which would contribute to the problem solution. Also, their organization could differ (inasmuch
as the development tool would allow) to reflect their particular purpose. The memory would allow
the system to refer to what treatments and infestations had occurred previously, as a real expert
would.
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Thus because of the nature of the problem being tackled and because of misgivings about the
rapid prototyping methodology, a rapid prototyping philosophy was used, but imposed on it was a
modular organization, so only small parts of the system were under development at any one time.
This modular approach allowed us to keep the individual knowledge-bases small, which makes
them more comprehensible and easier to maintain. It also allowed us to use a more conventional
software development strategy wherein specifications about the modules were determined prior to
actual coding.
The final point to be considered in this section is that of evaluation of the system. Excellent
reviews of this topic are presented by Cupello and Mishelevich (1988) and O'Keefe et al (1987).
Therefore, we will focus only on one important point and relate them to our work on EASY-MACS.
We feel it is very important to evaluate a KBS both for correctness and usability early in the
developmental cycle. Although EASY-MACS is still in an early phase of development, we feel it is
important to allow potential users access to it. Thus we have provided copies (and computers) to
several apple growers. The information gained from them will be incorporated into the next test
system to be distributed.
We have already obtained some useful advice from our trial users. One point that has become
obvious is that dynamically constructed screens need to be added to the interface. This is necessary
in order to provide a more useful explanation of the reasoning process employed by the system
when arriving at a recommendation. Since this is beyond the capabilities of our development tool,
we are required to code these ourselves. Another, unexpected, problem involves the knowledge
itself. Users desired access to the expertise in the system at other times and in other ways than
during consultations designed to provide a management recommendation. For example, a user
might be interested in querying the system to determine the toxicities of various insecticides to mite
predators. The current system does not allow this, nor could it without a major redesign, such as
going to an object-oriented programming environment, rather than a rule-based one. This last point
is not trivial because a major difficulty in developing KBS's is to express knowledge about a problem
without committing to a particular way of using it.
We also watched fruit growers use the system, which was, in effect, an evaluation of our
presentation method. Their choice of which screens to read and which to skip showed us that the
examples chosen were not always the most relevant ones, and that certain facts must be included
in every possible path through the system, including highly unlikely ones. This will insure that certain
information is presented, but can not guarantee that it will be read, understood or acted upon.
PITFALLS TO AVOID
When a nascent technology is embraced by a new discipline it is often surrounded by
misunderstanding and overly ambitious claims about its potential. This is certainly true with respect
to KBS's and IPM. The danger here is that when the technology fails to meet its advertised potential,
it is prematurely judged ineffective and inappropriate. To guard against this it is important that those
who may use the technology or who evaluate tools produced by it be aware of pitfalls that may
befall them. Towards this end we have constructed the following list.
1) KBS's, especially those with sophisticated graphical interfaces, are inherently high-tech and
impressive. However, like any computer program, they only function as well as their design and
content allow. The temptation to present in this format ideas we are not certain of is great, for they
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are likely to be accepted solely due to the manner of presentation. We must be sure to produce
only systems that incorporate what we know, not ones that present what we would like to know.
2) The amount of work involved in EASY-MACS, a relatively small system, is immense and
inherently long-term. It is essential that other projects of this type not be undertaken unless
adequate, long-term resource commitment (personnel and equipment) is insured. Coordinate with
this is recognition of the value of this type of activity for the participants, something which may be
difficult at a traditional, research-oriented institution.
3) Are our expectations about KBS realistic? These systems do not think and only seem to display
any type of intelligence. In reality, KBS use programmed rules of inference to reach a conclusion.
They manipulate symbols, but in a context free situation and without any understanding of what the
symbols mean. A KBS is constrained by the knowledge it contains and can not reach conclusions
that are not implicit in that knowledge. Most KBS can not detect faulty data or if they are being
employed for a problem not in their domain. In either case, answers will be provided, but almost
certainly they will be incorrect, and the user is more apt to blame the system then themselves.
4) Is thought being given to ensure that a KBS is consistent and complete? A trial and error or
case study approach to eliciting knowledge may produce an incomplete and inconsistent knowledge
base. This type of software is likely not to be as reliable as that developed from precise
specifications. The system may well reproduce any errors the expert would make. The designer
and user may well disagree at to whether this is a feature or a fault of the system.
5) Are we using the elicited knowledge effectively? Knowledge encoded in rules, by far the most
common representation in KBS's, can only be accessed in a manor consistent with the way the
inference engine manipulates the rules. That is, certain questions may be answered, but others can
not be, even though the knowledge to answer them is in the system. This is because the form of
the system itself limits the ways the knowledge can be accessed. If knowledge was encoded as
facts, multiple access paths would be possible, but coding would become much more difficult. Until
tools are developed to assist the KBS developer in this form of knowledge representation, we will
continue to waste the very resource we are trying to conserve, expert knowledge.
OPPORTUNITIES FOR USE OF KBS's IN IPM
In this final section of the paper we list five conventional opportunities and benefits of KBS's
and then discuss what we feel is the most fundamental opportunity for use of KBS in IPM. There
are a number of important advantages of KBS's compared to conventional text-based or
computer-based decision aids that are often cited. First, the information base not only consists of
objective information (published technical data) but also includes expert opinions on issues and
problems not necessarily addressed by such information. Second, KBS's provide a format for
dealing with imprecise or incomplete data, precisely that with which a real expert must often contend.
Third, because a KBS can record its logical chain of reasoning, it has explanatory power, although
it should be noted that providing such explanations in a form a user can comprehend is not a trivial
task. Fourth, little technical expertise is required to use the system. Finally, interactive graphics can
provide a visual display of information for diagnostic and educational purposes, thereby improving
the usefulness of the system and increasing the user's confidence in the system's recommendations.
The fundamental opportunity in the use of KBS's is to deliver IPM related knowledge in a form
that will facilitate its use. It is important though to address this opportunity in the proper framework.
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We do not think it is appropriate to ask "how can we build a system that will behave like an expert
solving a pest management problem". The reason for this is that KBS's use rationalistic problem
solving; given a precise statement of a situation they enumerate alternatives for solution and find
the best solution based on some objective criteria. However, this type of problem is only a partial
description of how people solve problems. A person processes data within a framework of
interpretation whereas a KBS does not. As a result, it is more appropriate to ask "how can KBS's
be designed to help people do things more effectively". If this is kept in mind KBS's will likely make
a significant contribution to the adoption of IPM practices.
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REFERENCES CITED
Coulson, R. N., and M. C. Saunders. 1987. Computer assisted decision making as applied to entomology. Ann. Rev.
Entomol. 32:415-438.
Cupello, J. M. and D. J. Mishelevich. 1988. Managing prototype knowledge/expert systems projects. Commun. ACM.
31:534-550.
Davis, R. 1986. Knowledge-based systems. Science. 231:957-963.
Denning, P. J. 1986. The science of computing - expert systems. Am. Sci. 74:18-20.
McKinion, J. M. and H. E. Lemmon. 1985. Expert systems for agriculture. Comput. Electron. Agric. 1:31-40.
Naegle, J. A., R. N. Coulson, N. D. Stone, and R. E. Frisbie. 1986. The use of expert systems to integrate and deliver IPM
technology. In Integrated Pest Management on Major Agricultural Systems. R. E. Frisbie and P. L. Adkisson
eds. Texas A & M University.
O'Keefe, R. M., O. Balci, and E. P. Smith. 1987. Validating expert system performance. IEEE Expert. Winter 1987:81-89.
Parnas, D. L 1985. Software aspects of strategic defense systems. Am. Sci. 73:432-440
Prerau, D. S. 1985. Selection of an appropriate domain for an expert system. Al Magazine. 7,2:31-40.
Waterman, D. A. 1986. A Guide to Expert Systems. Addison-Wesley, Reading, MA.
Wearing, C. H. 1988. Evaluating the IPM implementation process. Ann. Rev. Entomol. 33:17-38.
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LIST OF
CONTRIBUTORS
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LIST OF CONTRIBUTORS
ANGLE, J. S.
Department of Agronomy
University of Maryland
College Park, MD 20742
BACON, C. W.
Toxicology and Mycotoxins Research Unit
USDA/ARS
Richard B. Russell Agricultural Research Center
P.O. Box 5677
Athens, GA 30613
BROWN, W. M., JR.
Department of Plant Pathology and Weed Science
Colorado State University
Fort Collins, CO 80523
BUSH, L P.
Department of Plant Pathology, Entomology and Agronomy
University of Kentucky
Lexington, KY 40546-0091
CLARKE, B. B.
New Jersey Agricultural Experiment Station
Rutgers University
New Brunswick, NJ 08903
CRANSHAW, W.
Department of Entomology
Colorado State University
Fort Collins, CO 80523
COCKFIELD, S. D.
Department of Entomology
University of Kentucky
Lexington, KY 40546
DAHLMAN, D. L
Departments of Plant Pathology, Entomology and Agronomy
University of Kentucky
Lexington, KY 40546-0091
DANNEBERGER, T. K.
Departments of Botany and Plant Pathology, and the Pesticide Research Center
Michigan State University
East Lansing, Ml 48824
DAVIDSON, J. A.
Department of Entomology
University of Maryland
College Park, MD 20742
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DERNOEDEN, P. H.
Department of Agronomy
University of Maryland
College Park, MD 20742
DETWEILER, R.
Departments of Botany and Plant Pathology, and the Pesticide Research Center
Michigan State University
East Lansing, Ml 48824
FUNK, C. R.
New Jersey Agricultural Experiment Station
Rutgers University
New Brunswick, NJ 08903
FUNK, R. C.
The Davey Tree Expert Company
1500 North Mantua Street
Kent, OH 44240
GEORGIS, R.
Biosys
1057 East Meadow Circle
Palo Alto, CA 94303
GOLD, A. J.
Departments of Natural Resources Sciences and Plant Sciences
Rhode Island Agricultural Experiment Station
University of Rhode Island
Kingston, Rl 02881
GRANT, Z.
Board of Supervisors
70 W. Hedding St.
San Jose, CA 9510
GROSS, C. M.
Department of Agronomy
University of Maryland
College Park, MD 20742
GROTHAUS, G. D.
Agri-Diagnostics Associates
2611 Branch Pike
Cinnaminson, NJ 08077
HILL, R. L.
Department of Agronomy
University of Maryland
College Park, MD 20742
HUBER, B.
IPM Program
New York State Agricultural Experiment Station
Cornell University
Geneva, NY 14456
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HULL, R. j.
Departments of Natural Resources Sciences and Plant Sciences
Rhode Island Agricultural Experiment Station
University of Rhode Island
Kingston, Rl 02881
JOHNSON-CICALESE, J. M.
New Jersey Agricultural Experiment Station
Rutgers University
New Brunswick, NJ 08903
KAGEYAMA, M. E.
O. M. Scon and Sons Co.
Research Division
Marysville, OH 43041
KLEIN, M. G.
Horticultural Insects Research Laboratory
Application Technology Research Unit
ARS/USDA
Ohio Agricultural Research and Development Center
Wooster, OH 44691
KNOOP, W.
Texas A&M University
Research and Extension Center
17360 Co it Road
Dallas, TX 75252
LARSON, L
R & D Dept.
Soil Technologies Corp.
600 North 12th Street
Fairfield, IA 52556
LANKOW, R. K.
Agri-Diagnostics Associates
2611 Branch Pike
Cinnaminson, NJ 08077
LESLIE, A. R.
U. S. Environmental Protection Agency
Office of Pesticide Programs
Field Operations Division (H7506C)
401 M Street, S.W.
Washington, DC 20460
METCALF, R. L.
Department of Entomology
University of Illinois
Urbana, IL61801
MILLER, S. A.
Agri-Diagnostics Associates
2611 Branch Pike
Cinnaminson, NJ 08077
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MORRIS, T. A.
Department of Entomology
University of Kentucky
Lexington, KY 40546
NYROP, J. P.
Department of Entomology
New York State Agricultural Experiment Station
Cornell University
Geneva, NY 14456
OTTO, M.
Departments of Botany and Plant Pathology, and the Pesticide Research Center
Michigan State University
East Lansing, Ml 48824
PETERSEN, F. P.
Agri-Diagnostics Associates
2611 Branch Pike
Cinnaminson, NJ 08077
PLUMLEY, K. A.
Agri-Diagnostics Associates
2611 Branch Pike
Cinnaminson, NJ 08077
POINAR, G. O., JR.
Department of Entomological Sciences
University of California
Berkeley, CA 94720
POTTER, D. A.
Department of Entomology
University of Kentucky
Lexington, KY 40546
RASMUSSEN-DYKES, C.
Jefferson County Cooperative Extension
Golden, CO 80401
RAUPP, M. J.
Department of Entomology
University of Maryland
College Park, MD 20742
RITTENBURG, J. H.
Agri-Diagnostics Associates
2611 Branch Pike
Cinnaminson, NJ 08077
ROBERTS, D.
Departments of Botany and Plant Pathology, and the Pesticide Research Center
Michigan State University
East Lansing, Ml 48824
SCHAEFER, J.
R & D Dept.
Soil Technologies Corp.
600 North 12th Street
Fairfield, IA 52556
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SHETLAR, D. J.
ChemLawn Services Corporation
Research and Development
P.O. Box 85-816
Columbus, OH 43085
SIEGEL, M. R.
Departments of Plant Pathology, Entomology and Agronomy
University of Kentucky
Lexington, KY 40546-0091
SMITH, M. F.
Department of Entomology
University of Maryland
College Park, MD 20742
SULLIVAN, W. M.
Departments of Natural Resources Sciences and Plant Sciences
Rhode Island Agricultural Experiment Station
University of Rhode Island
Kingston, Rl 02881
VARGAS, J. M., JR.
Departments of Botany and Plant Pathology, and the Pesticide Research Center
Michigan State University
East Lansing, Ml 48824
VILLANI, M. G.
Department of Entomology
New York State Agricultural Experiment Station
Cornell University
Geneva, NY 14456
WELTERLEN, M. S.
Grounds Maintenance Magazine
P.O. Box 12901
Overland Park, KS 66212;
formerly, Department of Agronomy,
University of Maryland
College Park, MD 20742
WIDELL, L R.
O. M. Scott and Sons Co.
Research Division
Marysville, OH 43041
WILKINSON, J. F.
Professional Lawn Care Association of America
101 Buena Vista Drive
North Kingston, Rl 02852
WOLF, W.
Department of Computer Science
Rochester Institute of Technology
Rochester, NY 14623
WRIGHT R. J.
Department of Entomology
University of Nebraska
Lincoln, NE 68583
007
•k U.S. GPO: 1989—625-030 °°'
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