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PB03-233395
EPA-600/3-83-047
June 1983
BIOLOGY OF
SUBMERGED AQUATIC MACROPHYTE COMMUNITIES
IN THE LOWER CHESAPEAKE BAY
Volume III
Interactions of Resident Consumers in a Temperate
Estuarine Seagrass Community: Vaucluse Shores,
Virginia, USA.
Region HI Librory
Environmental Protection Agency Robert j. orth
" ' and
Jacques van Montfvans
it *. Environmental Protection Agency
r;.r,;<;n III information Resource
*•-'''•'. ^ " . . ' Virginia Institute of Marine Science
rVi CheSJlUtMreei . , and School of Marine Science
• I: liviipfcia, PA WWI • ./ College of William and Mary
.Gloucester Point, VA 2.3062
Contract No. R805974
Project Officer
Dr. David Flemer
U.S. Environmental Protection Agency
Chesapeake Bay Program
2033 West Street
Annapolis, MD 21401
KPRODUCSO 8r
NATIONAL TECHNICAL
INFORMATION SERVICE I'.". !• ,;-'•' r-x ''n r ,-e-, -,
US DfP/UtKFH! Of COKMCRCf r ' ••--'!, ^<-.,~f
VA 22161 i'>•,-'.•>. ., ij.ii.uiion Resource
r.:-:M :•;:::/)
i.'i r.- • -,ii; Street
K-- - :-M, PA
EPA Report Collection
Regional Center for Environmental Information
US EPA Region III
Philadelphia, PA 19103
-------
Regional Center tot Environmental Information
US EPA Region III
1650 Arch St.
Philadelphia, PA 19103
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TECHNICAL REPORT DATA
(Please read Imtnit /:c'*n on the rri crsc hi jure c
1. REPORT NO.
EPA-600/3-83-047
4. TITLE AND SUBTITLE
BIOLOGY OF SUBMERGED AQUATIC MACROPHYTE COMMUNITIES IN
THE LOWER CHESAPEAKE BAY: Vol. III. Interactions of
Resident Consumers in a Temperate Estuarine Seagrass
Community; Vaucluse Shores, Virginia, USA
3 RECIPIENT'
PBS
5. REPORT DATE
June 1983
6. PERFORMING ORGANIZATION CODE
7. AUTHOR(S)
Robert J. Orth and Jacques van Montgrans
8. PERFORMING ORGANIZATION REPORT NO.
9. PERFORMING ORGANIZATION NAME AND ADDRESS
Virginia Institute of Marine Science
Glr-'cester Point, VA 23062
10. PROGRAM ELEMENT NO.
11. CONTRACT/GRANT NO.
Grant R805974
12. SPONSORING AGENCY NAME AND ADDRESS
Chesapeake Bay Program
U.S. Environmental Protection Agency
2083 West Street
Annapolis, MD 21401
13. TYPE OF REPORT AND PERIOD COVERED
14. SPONSORING AGENCY CODE
EPA/600/05
15. SUPPLEMENTARY NOTES
16. ABSTRACT
As a part of the Functional Ecology Program on Chesapeake Bay submerged aquatic
vegetation (SAV), this study investigated infaunal and epifaunal trophic dynamics.
The work was conducted in conjunction with other major aspects of the program (see
Volumes I, II, IV) and respresnts the culmination of four years of intensive field and
laboratory investigations.
The main study area established for investigating the functional ecology of
resident consumers in the lower Chesapeake Bay was a large grass bed located at
Vaucluse Shores on the bayside of Virginia's eastern shore. Vaucluse Shores was chosen
as the study site because: (1) the site had been previously studied and background
information was available; (2) the bed is well established and historically stable;
(3) the area is relatively remote and unperturbed; (4) the bed contained the two
dominant lower Bay macrophyte species, Zostera marina and Ruppia maritima; and (5) the
bed was large enough to simultaneously accommodate varied studies and sampling
regimes. This bed was intensively mapped in 1978 and 1979, and permanent transects
were established for sampling reference points.
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18. DISTRIBUTION STATEMENT
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19 SECURITY CLASS (Tins Report/
UNCLASSIFIED
21. NO. OF PAGES
24/
20. SECURITY CLASS fT/lls pus.'
UNCLASSIFIED
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EPA Form 2220-1 (Rev. 4-77) PREVIOUS EDITION is OBSOLE IE ^
-' -S. 12.?A Region III
\.;.'jit»nal Center for Environmental
fn formation
r'mia.-Jelphia, PA 19103
-------
NOTICE
This document has been reviewed in accordance with
U.S. Environmental Protection Agency policy and
approved for publication. Mention of trade names
or commercial products does not constitute endorse-
ment or recommendation for use.
11
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TABLE OF CONTENTS
Page
ACKNOWLEDGMENTS V
PREFACE VI
CHAPTER 1. Structural analysis of benthic communities associated with
vegetated and unvegetated habitats by J. van Montfrans and
R. J. Orth 1
Abstract 2
Introduction 3
Methods and Materials 5
Results 7
Discussion 31
References 35
CHAPTER 2. Predator exclusion experiments in a Chesapeake Bay grass
community by R. J. Orth and J. van Montfrans 39
Abstract 40
Introduction 41
Study Site, Materials and Methods 42
Results 47
Discussion 74
References 78
CHAPTER 3. Predator-prey interactions in an eelgiass ecosystem in the
lower Chesapeake Bay, Virginia by R. J. Orth and J. van
Montfrans 81
Abstract 82
Introduction 83
Materials and Methods 83
Results 86
Discussion 89
References 93
CHAPTER 4. Secondary production of some dominant macroinvertebrate
species inhabiting a bed of submerged vegetation in the
lower Chesapeake Bay by R. J. Diaz and T. Fredette 95
Abstract 96
Introduction 97
Methods 97
Life Histories of Production Species 99
Results and Discussion 114
References 122
-------
TABLE OF CONTENTS (continued)
Page
CHAPTER 5. Preliminary effects of grazing by Bittium varium on
eelgrass periphyton by J. van Montfrans, R. J. Orth and
S. Vay 124
Abstract 125
Introduction 126
Methods and Materials 128
Results 129
Discussion 137
References 159
CHAPTER 6. Aspects of waterfowl utilization in a mixed bed of
submerged vegetation of the lower Chesapeake Bay by
E. Wilkins 163
Acknowledgments 164
Abstract 165
Introduction 166
Methods 169
Results 175
Discussion 205
Summary 214
References 216
CHAPTER 7. Trophic relationships in a grass bed based on
values by J. van Montfrans and R. J. Orth 221
Abstract 222
Introduction 223
Methods and Materials 224
Results and Discussion 224
References 231
IV
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ACKNOWLEDGMENTS
The work for this volume depended upon the cooperation and coordination
of and could not have been achieved without the talents of the many
scientists, graduate students, technicians and summer aides at this Institute.
In particular, we want to thank Tom Fredette, Glenn Markwith, Page Mauck,
Cindy Miekly, Cliff Ryer, Linda Schaffner, Terry Stahl, Lee Stone, Tarn Vance,
Anna Vascott, Stephanie Vay and Elizabeth Wilkins. We are also indebted to
Dr. Don Boesch for his initial efforts in the organization of our program.
Carole Knox, Shirley Sterling and Nancy White are gratefully acknowledged
for their efforts in typing the many drafts of this report. Joe Gilley, Bill
Jenkins, Sylvia Motley, Kay Stubblefield and Ken Thornberry provided expert
assistance in areas of the art work, photographic work and reproduction
aspects.
Mr. William Cook, who was the former project officer of this program, was
a key figure for insuring the smooth operation of the administrative aspects
of the grant for which we are deeply thankful.
Our thanks also go to the many people in the Chesapeake Bay Program, both
at the state and federal levels and to the Citizens Program for allowing the
Submerged Aquatic Vegetation Program to become a reality as a major area of
research in the Chesapeake Bay.
The final copy of this report was prepared by the VIMS Report Center to
whom we owe gratitude.
Finally, a hearty thank you to those whose contributions we may have
overlooked.
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PREFACE
One of the most notable features about habitats with submerged aquatic
vegetation (SAV) is the characteristically high density of the associated
fauna. Included are epibiota and infauna which are represented by a diverse
and complex assemblage of micro- and macroalgae, protozoans, hydrozoans,
anthozoans, turb^ll^rians, gastropods, isopods, araphipods, polychaetes,
oligochaetes, bivalves, decapods and barnacles. Many of these groups exhibit
distinct seasonal pulses of abundance depending on their individual spawning
periods. The epibiotic community within grass beds is quite distinct from the
communities in adjacent unvegetated areas. Due to the lack of a suitable
substrate, there is usually very little epifauna in bare sand or mud areas.
The pibio a primarily use the blades as a substratum for attachment (i.e.
barnacles, algae, hydroids, etc.) or feeding platform in the case of micro
herbivores grazing on the microalgae that colonize the blades. Thus, grass
beds provide substiates, protection and food resources which allow for the
maintenance of high densities which in turn attract and trophically support
numerous migratory utilizers of SAV habitats, i.e. crabs, fishes and
waterfowl. These features are fundamental to the resource value of SAV beds
on a world wide basis.
The fact that numerous species of epibiota associated with SAV may not be
totally dependent for their survival on the presence of grass (since many can
exist on almost any biotic or abiotic substrate) does not detract from the
importance of SAV. Submerged vegetation is a renewable resource, unlike many
other substrates, and so persists through time.
The infaunal community also appears to benefit from the presence of SAV.
This community is quite distinct from that of adjacent unvegetated areas.
There is a tremendous increase in the numbers of species and individuals in
vegetated habitats which is in part related to increased sediment stability,
microhabitat complexity, greater food supply and decreased predation pressure.
The motile community consisting of larger macroinvertebrate species (e.g.
shrimp, crabs, and fish) is also diverse and distinct from surrounding
unvegetated areas.
Migratory waterfowl species such as Canada geese, redheads and widgeon
are closely associated with beds of submerged grasses because of the
importance of the grass as a food resource. Abundances of certain waterfowl
species which depend on submerged grasses for food have declined in the
Chesapeake Bay in conjunction with the decline of Bay grasses during the last
15-20 years.
The trophic function of SAV communities and the refuge factor that SAV
provides appear to be the key to understanding the role these habitats play in
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supporting living resources of direct importance to man. These two attributes
are so functionally interrelated that, although it may be necessary to
separate the two for the purpose of modelling the system, they must be
addressed with a unified research approach.
Our study on the functional ecology of resident consumers as a part of
the Functional Ecology Program on Chesapeake Bay SAV was concerned with an
investigation of infaunal and epifaunal trophic dynamics. This work was
conducted in conjunction with the other major aspects of the program (see
Volumes I, II, IV) and represents the culmination of four years of intensive
field and laboratory investigations involving many dedicated co-workers.
The main study area established for investigating the functional ecology
of resident consumers in the lower Chesapeake Bay was a large grass bed
located at Vaucluse Shores on the bayside of Virginia's eastern shore.
Vaucluse Shores was chosen as the study site because: 1) The site had baen
previously studied and background information was available; 2) the bed is
well established and historically stable; 3) the area is relatively remote and
unperturbed; 4) the bed contained the two dominant lower Bay macrophyte
species, Zostera marina and Ruppia maritima; and 5) the bed was large enough
to simultaneously accomodate varied studies and sampling regimes. This bed
was intensively mapped in 1978 and 1979, and permanent transects were
established for sampling reference points.
Our initial effort in examining the functional ecology of resident
consumers was to determine the structural aspects of the grassbed community
compared to unv^getated areas (Chapter 1). We subsequently conducted predator
exclusion experiments to determine the role of predation in structuring the
biotic community in grassbeds (Chapter 2) and examined in greater detail
predator-prey interactions in vegetated habitats (Chapter 3). Having
established which species were numerically dominant, we calculated the
secondary production of those species which were trophically or functionally
important (Chapter 4). We then focused our attention on one dominant species,
an herbivorous grazer, and examined its role in controlling epiphytic fouling
on Zostera marina (Chapter 5). Because waterfowl have been the least studied
trophic components of the grass bed systems in the lower Bay, we determined
the intensity of utilization by wintering waterfowl of the Vaucluse grass
system (Chapter 6). We also measured the impact of feeding by one species
(Buffleheads) on the density of macroinvertebrate population densities.
Finally, we tried to place into perspective major trophic links in the
Vaucluse Shores grassbed by examining natural carbon isotope ratios (•'••'C to
"C) in some of the dominant species (Chapter 7). Such an approach enabled us
to determine the sources of primary production utilized by the resident
consumers.
We have written each chapter as a unit to alljw for easier presentation
of the data ami to facilitate'the submission of discrete sections to peer
reviewed scientific journals. Chapter 5 has already been accepted for
publication in Aquatic Botany and other chapters are being redrafted for
publication at a later date. Although some chapters lack comprehensive
statistical analyses and data interpretation, our goals are to thoroughly
conduct such revisions prior to publishing our findings. These products will
be available in journals at a future date.
vii
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CHAPTER 1
STRUCTURAL ANALYSIS OF BENTHIC COMMUNITIES
ASSOCIATED WITH VEGETATED AND UNVEGETATED HABITATS
by
Jacques van Montfrans
and
Robert J. Orth
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ABSTRACT
Three distinct habitats in the lower eastern Chesapeake Bay (Vaucluse
Shores at the mouth of Hungars Creek) were compared based on a structural
analysis of the associated fauna. These habitats included a grassbed (Zostera
marina and Ruppia maritima), large sand patches within the grassbed, and an
offshore sand bar system. Within the vegetated habitat, comparisons were made
of the fauna associated with pure stands of "L_. marina, pure stands of
JR. maritima and mixed stands of both species.
Generally there was a trend towards a greater species diversity (Shannon
H1) and abundance of infaunal species and individuals in the vegetated
habitats than in the two sand habitats. Many species which occurred as one of
the top ten in each habitat persisted throughout the course of the study
(July, 1978 - Nov. 1979) and were characteristic of the habitat examined.
Although infaunal abundances were concentrated at the sediment surface in all
three habitats, the grassbed supported a larger number of individuals deeper
in the sediments than did the other two habitats.
The epifaunal component of the vegetated habitat comprised a unique and
diverse assemblage of species which was similar between each area investigated
(i.e. Zostera marina, Ruppia maritima, and mixed stands). Few seasonal
patterns in epifaunal abundance were evident in the data. Vegetated areas
provided greater habitat heterogeneity and were therefore capable of
supporting a greater overall diversity of species than nonvegetated habitats.
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INTRODUCTION
One of the most notable featuras of the shallower margins along the
Chesapeake Bay is the presence of submerged macrophytes in many ar°as. Over
8,400 hectares (20,750 acres) of the nearshore mesc- and polyhaline and
sublittoral zone is vegetated by Zostera marina and/or Ruppia maritima (Orth,
et al. 1979). This submerged aquatic vegetation (SAV) adds a third dimension
to an otherwise relatively flat saudy bottom and provides a food source,
substrate and refuge for numerous species allowing .for the maintenance of high
faunal densities. The large stock of organisms inhabiting grassbeds is
thought to be fundamental to the resource value of SAV.
Most invertebrates assimilate energy fixed by seagrasses via a detrital
pathway (Fenchel, 1977; Klug, 1980). These detritivores are in turn utilized
by resident and migratory consumers such as crabs, fishes and waterfowl,
thereby providing an important trophic link between primary producers and
species in higher trophic levels (Carr and Aosras, 1973: Brook, 1975, 1977;
Adams, 1976; Stontr, 1979; Stoner and Livingston, 1980; Zimmerman, 1979;
Nilsson, 196'JO . The transfer of energy from SAV to migratory waterfowl
species including swans, geese and some ducks, is more immediate through a
direct consumption of the macrophytes (Verhoeven, 1978; Bayley et al., 1978;
Cottarn and Munro, 1954).
The biotic community within grassbeds can be quite distinct from that of
unvegetated areas. The epifaunal and infaunal components are represented by a
diverse and complex assemblage which includes macto- and microalgae,
protozoans, nematodes and other meiofauna, hydrozoans;, bryozoans, polychaetes,
oligochaetes, mollusks, crustaceans and several other groups. Many species
exhibit distinct seasonal pulses of abundance depending on their individual
spawning periods (Stevenson and Confer, 1978).
Numerous epifaunal spe.cies are generally not found on sandy bottoms
unless a suitable substrate such as large shells are present. The fact that
the epifauna may not be totally dependent on the presence of grass but is able
to exist on a variety of non-living substrates does not diminish the
importance of seagrasses as a habitat for these species. Unlike many inert
substrates, marine grasses represent a renewable resource for colonization.
This quality accounts in part for the high faunal diversity and density found
in grassbeds from one year to the next.
The infaunal community of grassbeds is also quite distinct from that
found in adjacent unvegetated areas with substantially greater numbers of
species anu individuals found in vegetated areas. This increase may be
related to greater sediment stability, microhabitat complexity and/or food
supply (Orth, 1977; Thayer, Adams and La Croix, 1975). Orth (1977) found the
i
-------
infauna of a Chesapeake Bay "L_. marina bed to increase in density and diversity
from the edge of the bed to its center. A similar positive correlation
existed with species abundance, as well as divers-'ty, and the increasing size
of the bed. He related greater faunal abundances to the sediment stabilizing
function of eclgrass. Orth (1977) showed experimentally that through
decreasing the stability of sediments by clipping blades of grass near the
sediment surface and by simulating wave action, the density and diversity of
the infauna was decreased. Natural biological disturbances such as cownose
ray activity had similar affects (Orth, 1975). The vertical component
provided by seagrasses which is differentiated into leaves, stems, rhizomes
and roots increases microhabitat complexity and supports a greater faunal
diversity than is found in unvegetated bottoms (Kikuchi 1980). Furthermore,
numerous species of animals which do not feed directly on the seagrasses are
thereby able to exist in such vegetated habitats (Thayer et al. 1978).
The natant community associated with SAV is diverse and quite distinct
from that of surrounding unvegetated areas (Orth and Heck, 1980; Heck and
Orth, 1980; Kikuchi, 1974). Many species comprising this community rely on
the macrophytes during certain critical life history stages. Hardwick (1973)
found that the West Coast herring, Clupea harengus pallasi, used eelgrass
leaves for egg attachment. East coast species which use grassbeds in a
similar manner include the halfbeak, Hyporhampnus sp. and the rough
silverside, Meaibras martinica (John Olnsy, pers. comm.). The toadfish Opsanus
tau uses the rhizomes as attachment sites for its eggs as well (Orth, pers.
comm.). One of the more complete studieo of eelgrass fuh communities was
conducted by Adams (1976a,b,c) in North Carolina. He found the highest fish
biomass when temperature and eelgrass biomass were greatest. Further, food
produced within the grassbed could have accounted for approximately 56% by
weight of the diet of the fish in this community. The high fish production
was due to juveniles whic'.i had higher growth efficiencies than older fishes.
They accounted for 79-84% of the total annual fish production. In addition to
fish, natant invertebrates such as shrimp and blue crabs are found in
considerably greater abundance as both juveniles and adults in eelgrass beds
than in sandy habitats (Lippson, 1970; Heck and Orth, 1980). Changes in
eelgrass abundance are even thought to cause variations in the commercial
catch of blue crabs. Thus, it appears that grassbeds provide numerous
advantages to a variety of species and constitute a valuable natural•resource
in the Chesapeake Bay.
In addition tv> the biological benefits provided by submerged raacrophytes,
the plants serve other functional roles such as buffering erosion by trapping
sands and pumping nutrients from the sediments to the leaves and eventually to
the water column. These lunctions are generally not achieved by artificial
substrates which further emphasizes the importance of SAV in the marine
environment.
When studying the dynamics of a particular habitat, a knowledge of both
the structural complexity and functional aspects of the system are desirable.
Both serve as a means for evaluating the habitat for management purposes,
particularly if other habitats have been similarly studied so that comparative
data are available. The objective of this section is to compare the
macroinvertebrate assemblages associated with the different habitat types
-------
found at the Vaucluse Shores study site. These include the grassbed proper
(eelgrass, widgeongrass, and mixed vegetation), inshore unvegetated sand
patches within the grassbed, and an offshore series of sand bars and troughs
which separate the vegetated area from the deeper waters of the Chesapeake
Bay.
METHODS AND MATERIALS
Routine sampling was scheduled to coincide with major biological events
in the grassbed and adjacent areas. These events included the arrival of
major predators in the system (early spring), the partial defoliation of Z.
marina (mid-sunnier), and the predominant larval settling periods (spring and
fall). Such timing, rather than quarterly sampling, would yield the beet data
on the structural characterization of the grass bed and adjacent habitats.
Three habitats (Fig. 1) were sampled six times (July and October, 1978
and April, June and September and November, 1979) to determine quantitative
and qualitative differences in their associated fauna. The habitats included
an offshore sandbar system (outside sand or OS), sandy patches within the
grass bed (inside sand or IS) and the grass bed (G> proper (Fig. 1).
Vegttated areas included an inshore Ruppia maritima Lone, a Zostera marina
zone offshore and a mixed stand of vegetation in between. Samples were
considered to be from the mixed area if the least abundant plant species
comprised a minimum of 15% of the total vegetational dry weight biomass in the
sample .
Initially, 10 stations were established in each habitat. However, data
analysis from the first sampling indicated that 5 rather than 10 stations
adequately represented the infauna in each of the two sand habitats. One
sediment (3.8 cm^) and three macroinfaunal (0.007 m^ each) cores were taken at
each station. Prior to taking infaunal and sediment cores in the grass bed an
epifaunal sample was taken at each station by clipping and collecting grass
from the area to be sampled. Coring was then conducted within the clipped
area. Coring was chosen as the appropriate sampling method because the root
and rhizome mat in the grassbed made sampling with other devices difficult.
In order to maintain gear comparability, identical cores were used in
unvegetated habitats. All samples were taken while diving with SCUBA.
Vertical distribution of infauna was examined in July 1978. A 35 cm long
plexiglass core 9.4 cm in diameter (0.007 ra^) was used to collect infaunal
samples. One such core sample was taken at each station. The top 10 cm of
each sample was sectioned vertically into 2 cm intervals and the remaining
material was divided into 5 cm intervals. Based on these data, it was
determined that a sample depth of 15 cm adequately collected the infauna.
Before sieving and preservation samples were held for at least 30 min. in
labelled plastic bags containing isotonic MgCl2 as a relaxant. This kept many
of the .ET^sller polychaetes and oligochaetes from fragmenting and/or crawling
through the sieve. All infaunal samples were washed through 0.5 mm mesh
sieves and the retained material was preserved in 10% buffered seawater
formalin. A vital stain (Rose Bengal) was added to facilitate laboratory
sorting. All invertebrates in each sample were removed from the remaining
-------
R = RUPPIA
2 = ZOSTERA
S=SAND
/= MIXED
OS = OUTSIDE SAND
IS = INSIDE SAND
O = TRANSECTS
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500
Fig. 1. Study site showing vegetation zones, the inside sand station (IS)
and the outside sand station (OS).
-------
sediments and associated plant debris using forceps while microscopically
examining spoonfulls of each sample placed in a petri dish.
Epifaunal samples were collected by clipping plants to within 2-3 cm of
the sediment surface and easing the blades into a collecting bag with a 0.5 mm
mesh bottom (Marsh 1973). Samples were kept in water and processed live by
stripping all epifauna from the blades and preserving them in 102 buffered
seawater formalin containing the vital stain Rose Bengal. The remaining plant
material was sorted to species (Ruppia, Zostera and algae), oven-dried at 80°C
for at least 48 h and then weighed to the nearest 0.1 g.
Numerical abundance histograms were plotted by area for both species and
individuals found in the infaunal and epifaural (grassbed only) community.
Species diversity was calculated for each area using the index of Shannon
(Pielou, 1975). The index H1 is expressed as:
H1 =Z Pi Iog2 Pi
where s = number of species in the sample and Pi = proportion of the i-th
species in the sample. This index is commonly used for comparative purpo'^s
and includes both a species richness (the number of species in a community)
component and an evenness (how equitably the individuals are distributed
between the species) component.
RESl'LTS
Cumulative species curves for vertically sectioned cores taken in each
habitat approached a plateau after the number of species from the top 15 cm of
sediment had been plotted (Fig. 2). Although most species in each habitat
were found in the top 15 cm of sediment, the composition and numbers of
individuals of the dominant taxa differed from one area to the next (Table 1).
Infaunal abundances were concentrated at the sediment surface in all three
habitats, but the grassbed supported a larger number of individuals deeper in
the sediments than did the other two habitats (Table 1).
Generally infaunal species means per core were twice as great for
vegetated areas as those for unvegetated habitats (Fig. 3). Samples from the
sandy habitat had a mean of between 4 and 11 species per core whereas means
for vegetated areas ranged from 14 to 30 species per core. With the exception
of the September and November, 1979 sample dates, the number of infaunal
species of the inside sand habitats showed slightly higher abundance than the
more dynamic offshore sand habitat. Within the three vegetated areas (Ruppia,
Xostera, and mixed) fewer species were uaually associated with Ruppia than
were found in the Zostera or mixed zones.
Seasonal trends in species abundances were not readily apparent. Mean
numbers of species per core were depressed in all habitats during September,
1979. Otherwise, distinct seasonal pulses in species abundances were obscure.
-------
TO
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The .lean number of infaunal individuals per core generally followed the
trends seen for species, with those in the sandy area being lower than those
from the vegetated bottom (Fig. 4). One exception occurred in July, 1978,
when densities of individuals (x of about 300 per core) at the inside sand
stations exceeded that found in any other habitat. Typically, samples had
means of around 20 individuals per core and in all but the least two sample
periods, data from the inside sand habitat showed a greater mean abundance of
individuals than that from the more dynamic sand bar area. In general, the
range in numbers of individuals per core in the nonvegetated areas was greater
than that for the grassbed as evidenced by the wider scatter of individual
sample data points. This implies that the sand-associated fauna were more
patchily distributed than the grassbed fauna.
There was no consistent pattern for mean infaunal individual abundances
between the three vegetated areas (Fig. 4). On July and October, 1978 and
November 1979, the greatest number of individuals were found in the mixed
habitat whereas the Ruppia zone showed greatest abundances in April and
September 1979.
Seasonal trends in the number of individuals were clearly evident in the
vegetated area (Fig. 4). Mean abundances (between 500 to 1000) were
considerably increased during April 1979 with the lowest means evident the
following September (between 50 and 110). The months of October and September
showed the lowest mean abundances of individuals from 1978 and 1979 with
between 100-200 and 50-110 individuals, respectively.
Mean species diversities (Shannon H1) for the infauna varied widely over
the study period ranging from 1.6 to 2.2 in the outside sand area; 1.4 to 2.7
in the inside sand habitat; and 2.0 to 3.7 in the grassbed (Fig. 5). In
general diversities were higher in the grassbed than in the nonvegetated
areas. No consistent patterns in species diversity were seen between either
the two sandy habitats or between the three vegetated zones.
An examination of the top ten infaunal species in each habitat for the
six sample dates (Tables 2-7) shows that these species comprised between 77%
(Zostera 10/78) and 98% (IS 7/78) of the total community. Each habitat had
several species which persisted through time as one of the top ten species.
In many cases these species were locally common to each of the habitats
examined. For example, the small bivalve, Gemma gemma was consistently
abundant in both the sandy habitats and occurred sporadically in both the
Ruppia and mixed zones but was overshadowed by other numerically abundant
species in the Zostera area. The polychaete Scolelepis squamata generally
persisted as one of the top ten species in both unvegetated habitats although
it was more regularly found in the inside sand area. Heteromastis filiformis
(Polychaeta) and Oligochaeta spp. were consistently abundant ir. the IS habitat
as well as in all three vegetated sediments but not at the dynamic OS
stations. The inside sand (IS) -stations were characterized by the parasitic
gastropod Oaostomia spp. Acanthohaustorius millsi, a burrowing amphipod, was
found only in the OS samples. Species which characterized the vegetated
habitats included the errant polychaete Nereis succinea, the generally
epibenthic isopod, Edotea triloba, and several species which are common in the
11
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designations are as follows: OS = outside sand; IS = inside sand;
R = Ruppia maritima; Z = Zostera marina; M = mixed vegetation.
Closed circles indicate the diversity for each core. Boxes
represent the mean diversity for each area.
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epifaunal community such as Polydora ligni, Streblospio benedicti (Polychaeta)
•and the isopod, Erichsonella attenuata.
The epifaunal component of the vegetated habitat comprised a somewhat
unique assemblage of species. Only one epifaunal clip was made in the mixed
area on October 1978, and June, September and November, 1979. Therefore these
histograms represent single point data and do not indicate mean abundances as
indicated in other histograms. With this fact in mind, some comparisons
between epifaunal communities can be made.
The largest mean number of species per grass clip (25) vas found in the
Ruppia habitat during July, 1978, when mean species abundances in the Zostera
( 17) and mixed ( 18) habitats were also relatively high (Fig. 6).
Approximately ten or fewer species were present in September, 1979, epifaunal
samples. Zostera samples contained slightly higher species numbers on three
of the six sample dates (October 1978, June, November, 1979) than either
Ruppia or mixed samples. During April and September, 1979, mean species
abundances were almost equal between these habitats. No seasonal trends were
evident in the species abundance data.
A logarithmic plot of the mean abundance expressed as individuals per m^
of vegetated bottom indicates the presence of large numbers of individuals in
the epifaunal community (Fig. 7). Numbers ranged from approximately 2000 per
nr in the Ruppia area (November, 1979) to almost 60,000'in Zostera samples
(June, 1979). The variation within a jingle sample date was sometimes almost
as great (June, 1979) with no consistent patterns of individual abundances
from one habitat to the next appearing in the data.
The amount of vegetation expressed as grams dry weight/m* varied
temporally, yet patterns of relative mean individual abundances per gram cf
vegetation (Fig. 8) were similar to those plotted on an aerial basis alone
(Fig. 7). Only the July 1978 data showed a slight variation from the latter
pattern. Mean numbers of individuals varied from almost 30 per gram of grass
(Ruppia, November 1979) to a maximum of about 7,400 per gram (Ruppia, April,
1979). No clear seasonal pattern was seen. Between habitat patterns were
also difficult to ascertain although generally there was a decreasing trend in
the number of individuals per gram of Ruppia than for the other two vegetated
habitats. :
\
Shannon diversity (H1) calculated for epifaunal samples generally tended
to be higher for the Ruppia area than for the mixed or Zostera areas (Fig. 9).
Lowest diversities were seen during September and November, 1979, in all but
the Ruppia area which experienced its lowest diversity in April, 1979.
Seasonal patterns in species diversity were obscure but in general when
progressing from spring thrcugh summer to fall, the diversity of the epifauna
associated with both Zostera and mixed stands of vegetation decreased whereas
diversity in the Ruppia zone tended to increase.
An examination of the top ten epifaunal species associated with each
habitat (Tables 8-13) revealed that they were present as one of the top ten
species L. all habitats without regard to vegetation type. For example, the
isopod Erichsonella attenuata, barnacle Balanus itnprovisus, gastropods
20
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JUNE 1979
SEPT. 1979
NOV. 1979
R Z M
R Z M
AREA
R Z M
Fig. 9. Epifaunal species diversity (Shannon H ) for each vegetated zone
in the grassbed. Treatment designations are as follows: R =
Ruppia maritima; Z = Zostera marina; M = mixed vegetation. Closed
circles indicate the diversity for each core. Boxes represent
the mean diversity for each area.
24
-------
TABLE 8. EPIFAUNAL SPECIES RECORDED IN THE THREE DIFFERENT TYPES OF VEGETATED
AREAS (RUPPIA, ZOSTERA, MIXED) AT THE VAUCLUSE SHORES STUDY SITE,
JULY, 1978.
RUPPIA
Species
1. Caprella penantis
2. Erichsonella attenuata
3. Balanus improvisus
4. Idotea balthica
5. Bittium varium
6. Nereis succinea
7. Paracaprella tenuis
8. Ampithoe longimana
9. Cymadusa compta
10. Gastropoda
Total
Total Sample
ZOSTERA
Species
1. Crepidula convexa
2. Bittium vnrlum
3. Idotea balthica
4. Erichsonella attenuata
5. Polydora ligni
6. Balanus improvisus
7. Ampithoe jongimana
8. Paracaprella tenuis
9. Nereis succinea
10. Dorldella obscura
Total
Total Sample
MIXED
Species
1. Crepidula convexa
2. Bittium varium
3. Balanus i-provisus
4. Caprella penantis
5. Erichsonella attenuata
6. Ampithoe longimana
7. Idotea balthica
8. Gastropoda
9. Folydora ligni
10. Nereis succinea
Total Sample
o,
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28.26
17.26
10.74
8.18
7.03
6.27
3.58
3.45
3.07
1.92
89.76
100.00
81.19
8.03
3.11
1.35
1.07
0.88
0.80
0.61
0.44
0.44
97.92
100.00
40.77
15.68
10.57
6.08
5.55
4.93
3.74
2.64
2.20
". 2'. 03
94.19
100.00
///gram
34.05
20.80
12.94
9.86
8.47
7.55
4.31
4.16
3.70
2.31
56.38
62.81
///gram
89.95
8.90
3.44
1.49
1.19
0.98
0.88
0.67
0.49
0.49
103.89
111.20
///Rram
28.87
11.10
7.48
4.30
3.93
3.49
2.65
1.87
1.56
- 1.43
66.68
70.79
///m2
1106.70
676.04
420.65
320.49
275.42
245.38
140.22
135.21
120.18
75.12
3515.41
3916.46
///m2
5882.41
581.86
225.17
97.6'
77. 7i
63.77
57.79
43.84
31.88
31.88
7093.95
7244.64
3088.59
1187.41
800.50
460.29
420.26
373.57
283.51
200.12
166.77
153.43
7134.45
7574.53
25
-------
TABLE 9. EPIFAUNAL SPECIES RECORDED IN THE THREE DIFFERENT TYPES OF VEGETATED
AREAS (RUPPIA, ZOSTERA. MIXED) AT THE VAUCLL'SE SHORES STUDY SITE,
OCTOBER, 1978.
RUPPIA
Species
1. Crepidula convexa
2.
3.
4.
5.
6.
7.
8.
9.
10.
Bittium varium
Ampithoe longimana
Erichsonella attenuata
Paracaprella tenuis
Nereis succinea
Caprella penantis
Cymadusa compta
Astyris lunata
Balanus improvisus
Total
Total sample
ZOSTERA
Species
1 . Crepidula convexa
2.
3.
4.
5.
6.
7.
8.
9.
10.
Bittium varium
Atnphithoe longimana
Balanus improvisus
Erichsonella attenuata
Paracaprella tenuis
Astyris lunata
Caprella penantis
Anadara trans versa
Nereis succinea
Total
Total sample
40.58
18.85
9.98
9.09
4.88
3.10
3.10
2.66
1.77
1.77
95.78
100.00
"'.
81.89
6.79
2.80
2.08
1.59
1.38
1.06
0.95
0.30
0.15
98.99
100.00
f/gram
16.37
7.60
4.03
3.67
1.97
1.25
1.25
1.07
0.72
0.72
38.65
40.35
///gram
211.65
17.56
7.24
5.37
4.12
3.56
2.74
2.47
0.78
0.38
256.14
258.75
///m2
916.64
425.76
225.40
205.37
110.20
70.13
70.13
60.11
40.07
40.07
216.88
226.44
///m2
15177.7.6
1259.35
519.14
385.08
295.23
255.29
196.82
176.85
55.62
27.10
18348.24
38535.45
MIXED
Species
///gram
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
Crepidula convexa
Bittium varium
Balanus improvisus
Erichsonella attenuata
Ampithoe longimana
Paracaprella tenuis
Nereis succinea
Astyris lunata
Cymadusa compta
Anad a ra transversa
Total
Total sample
78.85
11.58
3.44
2.84
0.67
0.67
0.45
0.45
0.45
0.37
99.77
100.00
///in
10471.85
1538.52
456.59
377.19
89.33
89.33
5.9.56
59.56
59.56
49.63
13251.12
13281.67
26
-------
TABLE 10. EPIFAUNAL SPECIES RECORDED IN THE THREE DIFFERENT TYPES OF VEGETATED
AREAS (RUPPIA, ZOSTERA, MIXED) AT THE VAUCLUSE SHORES STUDY SITE,
APRIL, 1979.
RUPPIA
Species
1.
2.
3.
it.
5.
6.
7.
8.
9.
10.
Polydora llgnl
Crepldula convexa
Bittium varlum
Caprella penantis
Paracaprella tenuis
Gammarus mucronatus
Erichsonella attenuate
Balanus Iraprovisus
Astyris lunata
Cymadusa compta
Total
Total sample
X
93.55
1.42
1.32
1.11
0.75
0.71
0.63
0.16
0.12
0.12
99.89
100.00
#/grara
6103.23
92.90
85.16
72.26
49.03
46.45
41.29
10.32
7.74
7.74
6516.12
6523.30
tf/m2
30516.13
464.52
425.81
361.29
245.16
232.26
206.45
51.61
38.71
38.71
32580.65
32616.53
ZOSTERA
Species
1. Polydora 1igni
2. Crepldula convexa
3. Caprella penantis
4. Gammarus nmcronatus
5. Bittium varium
6- Paracaprella temiis
7. Microprotopus raneyl
8- Cerapis tubularis
9. Nereis succinea
10. Astyris lunata
Total
Total sample
///gram
423.48
54.78
15.20
14.65
5.82
3.28
1.64
1.00
0.45
0.45
520.75
521.64
///n.
11433,84
1478.98
410.28
395.54
157.23
88.44
44.22
27.02
12.28
12.28
14050.11
14074.04
MIXED
Species
///gram
t/m
1.
2.
3.
4.
5.
6.
7.
8.
9;
10.
?olyjora ligni
Crepidula convexa
Gammarus mucronatus
Caprella penantis
Bittium varium
Paracaprella tenuis
Astyris lunata
Microprotopus raneyi
Balanus iriprovisus
Erichsonella attenuate
Total
Total sample
80.16
7.93
2.74
2.19
1.92
1.64
0.96
0.96
0.68
0.41
99.59
100.00
371.47
36.77
12.68
10.14
8.87
7.61
4.44
4.44
3.17
1.90
461.49
463.39
11701.43
1158.16
389.37
319.49
279.56
239.62
139.78
139.78
99.84
59.90
14526.93
14586.74
27
-------
TABLE 11. EPIFAUNAL SPECIES RECORDED IN THE THREE DIFFERENT TYPES OF VEGETATED
AREAS (RUPPIA. ZOSTERA, MIXED) AT THE VAUCLUSE SHORES STUDY SITE,
JUNE, 1979.
RUPPIA
Species
1. Balanus improvisus
2. Polydora ligni
3. Caprella penantis
4. Erichsonella attenuata
5. Nereis succinea
6. Etylochus elliptieirs^
7. Bittium varium
8. Cymadusa compta
9. Astyris lunata
10. Paracaprella tenuis
Total
Total sample
///gram
55.44
59.1
3.01
2.84
0.83
0.35
0.24
0.18
0.12
0.12
69.04
70.16
tf/m
ZOS12RA
Species
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
Balanus improvisus
Polydora ligni
Gammarus mucronatus
Stylochus elliptic us
Crepidula convexa
Nereis succinea
Erichsonella attenuata
Bittium varium
Caprella penantis
Astyris lunata
Total
Total sample
91.28
2.68
1.62
1.24
1.11
0.68
0.21
0.19
0.19
0.16
99.36
100.00
/'/gram
397.80
11.67
.08
.39
.83
.95
0.90
0.83
0.83
0.71
432.99
435.78
*/m£
52907.24
1552.71
941.04
716.23
643.04
392.10
120.24
109.79
109.79
94.10
57586.26
57957.19
MIXED
Species /o
1. Balanus ipprovisus 86.61
2. Crepidula convexa 4.69
3. Gammarus mucronatus 2.23
4. Erichsonella attenuata 2.01
5. Polydora ligni ' 1.79
6. Stylochus elliptic us 0.78
7. Nereis succinea • 0.45
8. Astyris lunnra _ • ' 0.45
9. Ampithoe longimara 0.33
10. Nassarius pbsoletus 0.33
Total 99.67
Total sample 100.00
///gram
180.05
9.74
.64
,18
.71
.62
0.93
0.93
0.70
0.70
207.20
207.89
20165.20
1091.42
591.72
467.75
415.78
181.90
103.94
103.94
77.96
77.96
23205.57
23282.40
28
-------
TABLE 12. LPIFAUNAL SPECIES RECORDED IN THE THREE DIFFERENT TYPES OF VEGETATED
AREAS (RUPPIA, ZOSTERA, MIXED) AT THE VAUCLUSE SHORES STUDY SITE,
SEPTEMBER, 1979.
RUPPIA
Species
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
Erichsonella attenuata
Balanus improvisus
Crepidula convexa
Cymadusa compta
Gastropoda
Mollusca
Nereis succinea
Bittium varium
Paracaprella tenuis
Stylochus ellipticus
Total
Total sample
55.84
16.23
9.09
3.90
3.57
3.57
3.25
1.95
0.65
0.32
98.37
100.00
it
23.15
6.73
3.77
.62
.48
.48
.35
0.81
0.27
0.13
40.79
41.47
1620.46
471.06
263.80
113.06
103.63
103.63
94.21
56.53
18.84
9.42
2854.64
2901.94
ZOSTERA
Species
1. Crepidula convexa
2. Gastropoda
3. Balanus iraprovisus
4. Erichsonella attenuata
5. Idotea balthica
6. Bittium varium
7. Doridella obscura
8. Stylochus ellipticus
9. Astyris lunata
10. Ampithoe longimana
Total
Total sample
MIXED
Species
1. Crepidula convexa
2. Erichsonella attenuata
3. Balanus improvisus
4. Gastropoda
5. Nereis succinea
6. Idotea balthica
7. Paracaprella tenuis
8. Bittium varium
9. Ampithoe longimana
10. Anadara transve^sa
Total
Total sample
96.02
1.24
0.97
0.57
0.27
0.19
0.17
0.13
0.10
0.08
99.74
100.00
o
96.74
0.82
0.54
0.49
0.38
0.38
0.33
0.16
0.11
0.05
100.00
100.00
///gram
278.90
3.59
2.82
1.66
0.77
0.55
0.50
0.39
0.28
0.22
289.68
290.44
///gran
180.32
1.52
1.01
0.91
0.71
0.71
0.61
0.30
0.20
0.10
186.39
186.39
/'An
18685.96
240.61
188.78
111.05
51.82
37.02
33.31
25.91
18.51
14.81
19407.78
19458.37
///n.
15868.56
133.87
89.25
80.32
62.47
62.47
53.55
26.77
17.85
8.92
16404.03
16404.03
29
-------
TABLE 13. EPIFAUNAL SPECIES RECORDED IN THE THREE DIFFERENT TYPES OF VEGETATED
AREAS (RUPPIA, ZOSTERA. MIXED) AT THE VAUCLUSE SHORES STUDY SITE,
NOVEMBER, 1979.
RUPPIA
Species
I. Erlchsonella attenuata
2. Crepidula convexa
3. Cymadusa compta
4. Paracaprella tenuis
5. Nereis succlnea
6. Gastropoda
7. Balanus improvisus
8. Oxyurostylis smithi
9. Cammarus mucronatus
10. Caprella penantis
Total
38.11
28.11
84
14
59
89
89
1.89
1.35
1.35
92.16
tf/gram
9.26
Total sample 100.00
83
90
25
12
0.46
0.46
0.46
0.33
0.33
22.40
24.31
675.84
498.49
139.00
91.07
81.48
33.55
33.55
33.55
23.97
23.97
1634.47
1773.51
ZOSTERA
Species
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
Crepidula convexa
Balanus improvisus
Idotea balthica
Doridella obscura
Ampithoe longimana
Erichsonella attenuata
Polydora ligni
Caprella penantis
Gastropoda
Gammari's mucronatus
Total
Total sample
88.19
2.66
2.56
1.09
1.07
0.95
0.58
0.54
0.45
0.29
98.38
100.00
///gram
243.60
tf/rn
28013.67
844.34
811.61
346.90
340.35
301.08
183.27
170.18
144.00
91.63
31250.03
31764.62
MIXED
Species
///gram
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
Crepidula convexa
Erichs. 'uella attenuata
Balanus improvisus
Polydora ligni
Gastropoda
Doridella obscura
Idotea balthica
Nereis succinea
Bittium varium
Stylochus ellipticus
Total
Total sample
96.13
1.74
1.18
0.26
0.20
0.17
0.13
0.04
0.04
0.02
99.91
100.00
506.42
9.17
6.19
1.38
1.03
0.92
0.69
0.23
0.23
0.11
526.37
526. bn
51401.82
931.19
628.55
139.68
104.76
93.12
69.84
23.28
23.28
11.64
53427.16
53475.29
30
-------
Crepidula convexa and Bittium varium and the polychaete Nereis succinea were
all commonly ranked among the top ten species in all vegetated habitats.
Seasonal pulses of abundance for J5. inprovisus (June, 1979) and Polydora ligni
(April, 1979) were evident in the data with possibly similar evidence for
Crepidula convexa and Bittium varium.
The results presented here indicate that the grassbed and each of the
sandy habitats are distinct with respect to their associated fauna.
Differences between the vegetated habitats are less clear cut. The number of
species and individuals was greatly increased in the vegetated habitats
indicating their importance to the Chesapeake Bay fauna.
DISCUSSION
A primary understanding of the structural aspects of vegetated habitats
is necessary to further examine the functional roles of the organisms within
these habitats. Additionally, a comparison of grass bed community structure
with that of nonvegetated areas can provide greater insight into the
importance of the various habitats surveyed.
We have clearly demonstrated an increased abundance of infauna,
particularly oligochaetes, at depths of 6 to 15 cm below the sediment surface
in vegetated areas compared to exposed sandy bottoms. Infauna living in grass
beds apparently deri\2 some advantage from the root and rhizome system of the
plants. The redox potential discontinuity layer (RPD) in grass beds is
farther below the sedinent surface than in unvegetated habitats and probably
allows organisms to survive deeper in the sediments. Oxygenation of surficial
sediment by the rhizosphere increases the two dimensionality of the habitat in
which grass bed associated infauna live. Virtually no information exists on
the rhizofauna of marine grasses although related studies in salt marshes have
demonstrated the rhizosphere to be important in determining the vertical
distribution of associated infivna (Bell et al. 1978; Teal and Wieser, 1966).
Additional advantages provided by vegetation to the infaunal community
include increased sediment stability and protection from predation.
Seagrasses have been shown to stabilize seuiments by their current baffling
and wave damping action (Hartog, 1970; Taylor and Lewis, 1970; Zieman, 1972).
Orth (1977) experimentally demonstrated that such sediment stability caused
increased infaunal diversity and density. T.r> addition, observations made en
blue crab feeding prompted Orth (1977) to suggest that such activities were
hampered by the presence of the root and rhizome layer in Zostera beds. A
similar hypothesis suggesting the protection provided by the rhizosphere to
the infauna was made by Riese (1977). All three factors acting together
(increased oxygenation of the sediments, greater sediment stability and
protection from predation) probably account for the high infaunal densities
and species abundances observed in our study.
Besides the functional advantages provided by the root and rhizome system
of aquatic vegetation, decomposing leaf litter supplies a rich detrital food
source for the grass bed infauna (Thayer, et al. 1977; Fenchell, 1972). For
species living among the plants, this food source is readily accessible and
31
-------
probably enhances the structural magnitude and diversity of the grass bed
infaunal community to the degree observed in our study.
The only exception to increased individual abundances in the grass bed
infauna occurred during the July, 1978 sample date when the inside sand
habitat showed the greatest abundance of individuals. This high level was
caused by a Gemma gemma recruitment pulse bringing the total number of
individuals to just over 33,000 per meter squared. Similar increases in the
small gastropod Odostomia spp. were also observed. This species is parasitic
on Gemma gemma (Abbott, 1974) and showed a positive response to an increased
food source.
Population dynamics of species comprising the infaunal community are
evident in our data and emphasize the continually changing nature of the
dominance hierarchy over time. Also evident is persistence of certain
abundant species in the habitats studied imparting some degree of constancy to
the community associated with each habitat. The amphipoo Acanthohaustoris
millsi^ and polychaete Paraonis fulgens were numerous and almost exclusively
found in the dynamic offshore sand bar (OS) habitat. Both were always present
as one of the top ten in this habitat for the duration of our study.
Acanthohaustorius millsi, a burrowing amphipod, is a suspension feeder on
microscopic algae and detr:.':us and is commonly found at the low tide mark as
well as subtidally on sand/ beaches (Dexter, 19r-9), It is associated with
dynamic medium sar.ds such ar. those of the sand bar area. Similarly, Paraonis
fulgens, described as both a rio.i-selective burrowing deposit feeder and a
highly selective diatom grazer ^Fauchald and Jumars, 1979) was also found in
all OS samples. It constituted the most abundant species at all sample times
except during July 1978 when it was third in abundance. These species are
both adapted for living in shifting sediments and are apparently unable to
compete successfully in the more stable protected sandy bottom within the
grass bed .
The small bivalve, Gemm? gemma, is able to exist in both the more
turbulent offshore sandbar habitat and the sandy patches within the grass bed.
Species which more accurately distinguish the bare cand zones inside the
vegetated area include the opportunistic capitellid polychaete, Capitella
capitata, as well as the spionid polychaete, Scolelepis squamatus.
Surprisingly, neither of these species was among the ten most numerous ones in
grass bed infaunal samples although the latter species was occasionally found
on the offshore sandbar. Capitella capitata builds tubes at or near the
sediment surface and Scolelepis squamatus builds loosely constructed burrows
in sandy substrates (Fauchald and Jumars, 1979). Capitella capitata is known
to be an r- strategist (high fecundity and short life span) and, based on our
data is recruited in the late summer and early fall. Scolelepis squamatus
persisted throughout the study in the inside sand habitat.
The grass bed infaunal community contained a more varied group overall of
species comprising the top ten during the course of our study than that
exhibited for either of the sandy habitats. This fact reflects the diverse
and dynamic nature of the community with a variety of species recruiting and
subsequently decreasing in abundance through time. Those species which
occurred most abundantly and regularly included the polychaete Heteromastus
32
-------
filiformis, Polydora ligni, Nereis succinea and numerous unidentified
oligochaetes. Heteromastus filiformis is a deep burrowing opportunistic
capitellid that was abundant in the grass bed proper and in sand patches
within the vegetated zone as were unidentified oligochaetes. Both P_. ligni
(Spionidae) and _N. succinea (Nereidae) were numerous in the grass bed but were
rarely encountered in the two sandy habitats. The former species has been
described as the most, abundant species in estuarine waters of the Chesapeake
Bay (Wass, 1965) with peak abundances on Zostera marina occurring in April and
May (Marsh, 1970). Orth (1971) found peaks in larval abundance in the York
River to occur in April. Despite its distinct seasonal pulses, _P_. ligni was
the most abundant polychaete throughout the year on fouling panels in Hampton
Roads, Virginia (Calder, 1966). In our study, P^. ligni persisted as one of
the top ten species in all three types of vegetated areas during the entire
study. Nereis succinea likewise was constantly abundant. This highly
opportunistic species has been described as a surface deposit feeder as well
as an omnivore feeding on prey (i.e. other Nereis) and silt-clay to sand sized
particles and plant detritus (Dauer, 1980). Not only was 1^. succinea commonly
found infaunally, it also was an abundant epifaunal community member.
The isopods Edotea triloba and Erichsonella attenuata were also numerous
and routinely present in infaunal samples. Edotea is epibenthic and was
rarely found in the epifauna whereas Erichsonella was common in be
communities.
The infaunal community of eelgrass beds at Vaucluse Shores was similar to
those of Guinea Marsh grassbeds studied by Orth (1973). Polychaetes
(Heteromastus filiformis, Streblospio benedicti, Nereis succinea, Polydora
1igni and to a lesser extent Spiochaetopterus oculatus and Scoloplos robustus)
were among the most numerous species present in both studies. Oligochaetes
and the isopod Edotea triloba were similarly abundant. It appears that an
infaunal community occurs within grassbeds which distinguishes those areas
from non-vegetated sand bottoms and furthermore characterizes them in terms of
general dominance hierarchies and species abundances.
The epifaunal community was comprised of numerous species all of which
utilized the grass blades as a substrate and a feeding area. The barnacle,
Balanus improvisus, gastropods, Bittium varium and Crepidula convexa, isopod,
Erichsonella attenuata -and amphipod, Caprella penantis were all abundant in
grassbed epifaunal samples. They occurred consistently among the top ten
species in all vegetated habitats without regard to vegetation type. Some
species such as Bittium varium and Crepidula convexa were more abundant on
Zostera marina. Their prevalence on eelgrass is probably related to the
morphology of the plant, with the wide bladed species preferred to those such
as Ruppia maritima with narrow blades. Bittium varium feeds extensively on
eelgrass periphyton (see-grazing section, this report) and its great abundance
in the epifauna is probably related to the readily available food supply.
Although juvenile Crepidula, convexa .are thought to be microalgal grazers as
well, adults switch to a filter feeding mode (Hoagland, 1975) and therefore
use grassblades primarily as an attachment platform from which to feed.
Caprella penantis is the most common caprellid amphipod along the east coast
of the United States and occurs abundantly from Long Island to the Chesapeake
Bay. It is nonspecific in its habitat preference, occurring on a wide variety
33
-------
of substrates including algae, sponges, alcyonarians and particularly hydroids
(McCain, 1968). Erichsonella attenuata, an isopod, is characteristically
associated with eelgrass (Schultz, 1969) although in our study it was also
common on Ruppia maritima. Little is known about the biology of this species.
It is probably omnivorous and occurs in such great abundance in grassbeds
because of the large quantities of suitable food and habitat.
Not surprisingly, several of the dominant species found in the Vaucluse
Shores epifauna were also present in a York River epifaunal community studied
by Marsh (1973, 1976). Of the 5 most abundant species found by Marsh (1973),
four (Bittium varium, Crepidula convexa, Erichsonella attenuata and Ampithoe
longimana) were also dominants at: Vaucluse Shores. Paracerceis caudata an
epifaunal isopod was commonly found in the Chesapeake Bay during the time of
Marsh's study in 1967 and 1968 but declined drastically in abundance after the
devastating passage of hurricane Agnes in June of 1972 (Orth, 1976). Their
populations do not yet seem to have recovered which accounts for the absence
of P_. caudata during our study. Some species which were abundant for brief
periods during the year in Marsh's (1975) study were regularly abundant in the
Vaucluse Shores epifauna. These include the barnacle, Balar.us improvisus and
epifaunal polychaete, Polydora jigni. Both the ascidian, Molgula manhattensis
and saccoglossan, Ercolania fuscata were periodically abundant in the York
River but were uncommon in Vaucluse Shores samples. Reasons for this fact are
unclear.
We have demonstrated and confirmed the existence of a diverse and
abundant infaunal and epifaunal community associated with a vegetated habitat
in the lower Chesapeake Bay. Marine grasses create greater physical
complexity resulting in a more heterogeneous habitat that is capable of
supporting larger numbers of invertebrate species and individuals than
adjacent sandy areas. Fish are attracted to these meadows because of the
preponderence of invertebrates which are heavily preyed upon (Adams, 1976a,
b,c; Nelson, 1979; Young and Young 1978; Stoner, 1979; Orth and Heck, 1980).
Many of the fish (e.g. spot and speckled trout) which frequent grassbeds are
commercially harvested or are important recreational species. Grassbeds are
also an important refuge for both juvenile as veil as older blue crabs,
Callinectes sapidus, during the soft shell phase of their molt cycle. Thus
the demise of these habitats may have serious consequences to many species
although tne effects of such declines may take years to be felt.
\
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Reinnold Co. New York, N.Y.
Adams, S. M. 1976a. The ecology of eelgrass, Zostera marina (L.) fish
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Adam-;, S. M. I976b. The ecology of eelgrass, Zostera marina (L.) fish
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Adams, S. M. 1976c. Feeding ecology of eelgrass fish commuinities. Trans.
Aner. Fish. Soc. 105:514-519.
Bayley, S., V. D. Stotts, D. F. Springer, and L. Steenis. 1978. Changes in
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Bell, S. S., M. C. Watzin and B. C. Coull. 1978. Biogenic structure and its
effect on the spatial hererogeneity of meiofauna in a salt r^rsh. J.
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Brook, I. M. 1975. Some aspects of the trophic relationships among higher
consumers in a seagrass community (Thalassia testudinum Konig) in Card
Sound, Florida. Ph.D. Dissertation, Univ. of Miami, Coral Gables.
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Brook, I. M. 1977. Trophic relationships in a seagrass community (Thalassia)
testudinum), in Card Sound, Florida. Fish diets in relation to
macrobenthic and cry 'tic faunal abundance. Trans. Amer. Fish. Soc.
106:219-229.
Calder, D. R. 1966. Ecology of marine invertebrate fouling organisms in
Hampton Roads, Virginia. M.S. Thesis, College of William & Mary. 66 pp.
Carr, W. S. E. and C. A. Adams. 1973. Food habits of juvenile marine fishes
occupying seagrass beds in the estuarine zone near Crystal River,
Florida. Trans. Amer. Fish. Soc. 102:511-540.
Cottam, C. and D. A. Munro. 1954. Eelgrass status and environmental •
relations. J. Wildl. Mgmt. 18:449-460.
Dauer, D. M. 1980. Population dynamics of the polychaetous annelids of an
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Hydrobiol. 65:461-487.
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Dexter, D. M. 1969. Structure of an intertidal sandy-beach community
in North Carolina. Chesapeake Sci. 10:93-98.
Fauchald, K. and P. A. Jumars. 1979. The diet of worms: a study of
polychaete feeding guilds. Oceanogra. Mar. Biol. Ann. Rev. 17:193-284.
Fenchel, T. 1972. Aspects of decomposer food chains in marine benthos.
Verh. dt. Zool. Ges. Bd. 65:14-22.
Fenchel, T. 1977. Aspects of the decomposition of seagrasses. Pp. 123-145.
In: C. P. McRoy and C. Hellferech (eds.), Seagrass Ecosystems: A
scientific perspective. Marcel Dekker, Inc., New York, 1977.
Hardwick, J. E. 1973. Biomass estimates of spawning herring Clupea
harengus pallasi, herring eggs, and associated vegetation in Tomales Bay.
Calif. Fish and Game 59:36-61.
Hartog, G. den. 1970. The seagrass of the worl\d. Verh. Kon. ned. Ak.
Wetensch. afd. Natuurk. 59:1-275.
Heck, K. £., Jr. and R. J. Orth. 1980. Structural components of eelgrass
(Zostera marina) meadows in the lower Chesapeake Bay. Decapod Crustacea.
Estuaries 3:289-295.
Hoagland, E. K. 1975. Patterens of evolution and niche partitioning in North
American Crepidula (Gastropoda:Calyptraiidae). Bull. Amer. Malacological
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Kikuchi, T. 1974. Japanese contributions and consumer ecology in eelgrass
(Zostera marina L.) beds, with special reference to trophic relationships
and resources in inshore fisheries. Aquaculture 4:145-160.
Kikuchi, T. 1980. Fiunal relationships in temperate seagrass beds.
Pp. 153-172. In: R. C. Philips and C. P. McRoy (eds.). Handbook of
Seagrass Biology: An ecosystem perspective. Garland Publ. Inc., New
York, N.Y.
Klug, M. J. 1980. Detritus-decomposition relationships. Pp. 225-245. In:
R. C. Phillips and C. P. McRoy (eds.). Handbook of Seagrass Biology: an
ecosystem perspective. Garland STPM Press, N.Y. 1980.
Lippson, R. L. 1970. Blue crab study in Chesapeake Bay, Maryland. Final
Progress Report, NRI Ref. No. 71-9. Univ. Md.
Marsh, G. A. 1970. A seasonal study of Zostera epibiota in the York
River, Virginia. Ph.D. Dissertation, College of William and Mary,
156 pp.
Marsh, G. A. 1973. The Zostera epifaunal community in the York River,
Virginia. Chesapeake Sci. 14:87-97.
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Marsh, G. A. 1976. Ecology of the gastropod epifauna of eelgrass in a
Virginia estuary. Chesapeake Sci. 17:182-187.
McCain, J. C. 1968. The Caprellidae (Crustacea: Amphipoda) of the
Western North Atlantic. United States National Museum Bulletin 278.
Nelson, W. G. 1979. Experimental studies of selective predation on
amphipods: Consequences for araphipod distribution and abundance. J. exp.
mar. Biol. Ecol. 38:225-245.
Nilsson, L. 1969. Food consumption of diving ducks wintering at the coast
of South Sweden in relation to food resources. Oikos 20:128-136.
Orth, R. J. 1971. Observations on the planktonic larvae of Polydora
ligni Webster (Polychaeta: Spionidae) in the York River, Virginia.
Chesapeake Sci. 12:121-124.
Orth, R. J. 1973. Benthic infauna of eelgrass, Zostera marina, beds.
Chesapeake Sci. 14:258-269.
Orth, R. J. 1975. Destruction of eelgrass, Zostera marina, by the cowr.ose
ray, Rhinoptera bonasus, in the Chesapeake Bay. Chesapeake Sci.
16:205-208.
Orth, R. J. 1976. The demise and recovery of eelgrass, Zostera marina,
in the Chesapeake Bay, Virginia. Aquatic Bot. 2:141-159.
Orth, R. J. 1977. The importance of sediment stability in seagrass
communities. Pp. 281-300. In: 3. C. Coull (ed.). Ecology of Marine
Benthos. U. of South Carolina Press, Columbia, 1977.
Orth, R. J., K. A. Moore and H. H. Gordon. 1979. Distribution and abundance
of submerged aquatic vegetation in the lower Chesapeake Ba>, Va. E.P.A.
Rep. No. 600'8-79/029/SAV 1.
Orth, R. J. and K. L. Heck, Jr. 1980. Structural components of eelgrass
(Zostera marina) meadows in the lower Chesapeake Bay. Fishes. Estuaries
3:278-288.
\
Pielou, E. C. 1975. Ecological diversity. Wiley-Interscience, New York.
165 pp.
Reise, K. 1977. Predator exclusion experiments in an intertidal mudflat.
Helgolander wiss. Meeresunters 30:263-271.
Schultz, G. A. 1969. How to Know the Marine Isopod Crustaceans. Wm. C.
Brown Co. Publishers. Dubuque, Iowa.
Stevenson, J. C. and N. M. Confer. 1978. Summary of available information
on the Chesapeake Bay submerged vegetation. Md. Dept. Natural Resources,
U.S.E.P.A. & F.W.S. FWS/OBS-78/66. 335 pp.
37
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Stoner, A. W. 1979. Species-specific predation on amphipod Crustacea by
the pinfish Lagodon rhomboideb - mediation by raacrophyte standing crop.
Mar. Biol. 55:201-208.
Stoner, A. W. and R. J. Livingston. 1980. Distributional ecology and food
habits of the banded blenny Parachries fasciatus (Clinidae): a resident
in a mobile habitat. Mar. Biol. 56:239-246.
Taylor, J. D. and M. S. Lewis. 1970. The flora, fauna and sediments of
the marine grass beds of Mahe, Seychelles. J. Nat. Hist. 4:199-220.
Teal, J. M. and W. Wieser. 1966. The distribution and ecology of neraatodes
in a Georgia salt marsh. Limnol. Oceanogr, 11:217-222.
Thayer, G. W., P. L. Parker, M. W. La Croiz, and B. Fry. 1978. The stable
carbon isotope ratio of some components of an eelgrass, Zostera marina,
bed. Oecologia (Berl.) 35:1-12.
Thayer, G. W. and R. C. Phillips. 1977. Importance of eelgrass beds in
Puget Sound. Mar. Fish. Rev:.ew 1271:18-22.
Young, D. K. and M. W. Young. 1978. Regulation of species densities of sea
grass associated macrobenthos: evidence from field experiments in the
Indian River estuary, Florida. J. Mar. Res. 36:569-593.
38
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CHAPTER 2
PREDATOR EXCLUSION EXPERIMENTS IN A CHESAPEAKE BAY GRASS COMMUNITY
by
Robert J. Orth
and
Jacques van Montfrans
39
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ABSTRACT
The effects of predators on the density of eelgrass epifauna and
infauna and sand infauna was studied using predator exclusion
techniques. A large topless pen (20 nr) and smaller cages (0.25 m^)
within the pen as well as outside the pen were set up in a bare sand
and an adjacent grass habitat to test the hypothesis that predation
has a significant effect on the structure of associated faunal
communities.
The grass habitat consistently had more infaunal species per core
than the sand habitat for all treatments. There were no distinct
differences among the grass treatments for species infaunal numbers
but in the sand, species numbers were higher in pen and cage
treatments compared with the control. Except for the sand cage
treatments, there was no difference between the pen and cage
treatments for number of species in both habitats.
Density of individuals in the grass habitat, treatments was
generally higher than the sand habitat treatments except for the June
cage treatments. In the sand area, infaunal densities were always
higher in the cage and pen treatments compared to the control while in
the grass habitat only the September cage and pen treatments were
higher than the control.
Epifaunal densities in the grass habitat were generally higher in
cage and pen treatments than the control. Species response to these
treatments were variable and controlled by the abundarce of grass in
the treatment.
The results of this work support recent evidence for the
importance of predation for the structuring of benthic communities
both in vegetated and non-vegetated habitats. j
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INTRODUCTION
The structure and organization of any biological community is
determined by a number of internal and external factors, both abiotic
and biotic. Most abiotic factors are usually external and cannot be
controlled by the community. Log damage in intertidal regions
(Dayton, 1971), wave stress and storm swells (Annala, 1974; Grigg and
Maragos, 1974), anchor ice (Dayton, et al. 1969, 1970) fire (Odum,
1971) and pollution stress (Wihlm, 1967; Wihlm and Dorris, 1966, 1968)
have all been shown to alter the structure of the affected community.
Predation and competition are the two most often cited biological
factors that control not only the structure but the function of the
community. Competition for a resource, e.g. space or food, can either
be through interference or exploitative competition (Peterson, 1980)
while predation can be size selective (Brooks and Dodson, 1965),
species selective (Dayton, 1971; Patrick, 1970) or non-selective with
respect to species or size of prey.
Predation in marine soft bottom benthic communities have recently
been shown to have dramatic effects on the density and diversity of
the infauna (Virnstein, 1977) and has bsen an implied factor for
structuring benthic communities associated with seagrass beds (Nelson,
1979; Heck and Orth, 1980a; Orth and Heck, 1980; Reise, 1978). Most
of the above studies have relied on manipulative tools, e.g. cages, to
examine the effects of predators. Though manipulative techniques have
piovided ecologists with some detailed insights into community
dynamics, they are not without their problems, e.g. separation of cage
effects from predator effects (Virnstein, 1978, 1980).
Eelgrass beds in the Chesapeake Bay have an associated infaunal
and epifaunal community that has a significantly higher density and
diversity than adjacent, unvegetated communities (Orth, 1975, 1977;-
see also Section 1 of this report). It is this dense assemblage of
invertebrates that undoubtedly serve as a food source for not only
invertebrate predators (e.g. blue crabs) but also vertebrate predators
(e.g. fish and waterfowl). The density of some of these predators i'l
these vegetated areas is sometimes extremely high (Orth and Heck,
1980) suggesting that their impact on epifaunal and infaunal density
may be important in reducing their density.
As part of the EPA Chesapeake Bay Program's Functional Ecology .of
Eelgrass Study in the Lower Chesapeake Bay, the objective of this
study was to determine what impact predation, excluding waterfowl, has
on the overall density and diversity of both epifauna and infauna.
41
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STUDY SITE, MATERIALS AND METHODS
All studies involving the predator exclusion experiments were
conducted in a large bed of submerged grasses located in the
Chesapeake Bay off Church Neck on the Delmax'va Peninsula, Virginia
(Fig. 1). This is the site of (he intensive functional ecology of
eelgrass program being used by Vi'iS .scientists in conjunction with the
Chesapeake Bay Program, Subnv: • t_a Aquatic Vegetation sub-program.
This site has been referred to as the Vaucluse Shores site and is
situated approximately 37'25'N latitude, 76°51'W longitude.
This site is characterized by five distinct habitat types: 1) a
large unvegetatcd intertidal sand flat adjacent to the shoreline; 2) a
Ruppia maritima dominated community ranging in depth from mean low
water (MLW) to approximately 0.3 m below MLW; 3) a mixed bed of R_.
mari tima and Z. .narina located from 0.3 to 0.6 m below MLW; 4) a T^.
marina dominated community located from 0.6 to 1.5 m below MLW; and 5)
a .second intertidal sandbar separating the grass bed from the main
Chesapeake Bay.
Sampling transects were set up during an initial intensive
mapping of SAV (Orth et al., 1979). Our experiments were conducted
along Transect C.
In order to assess the effects of predation on the epifauna and
infauna, we used two different types of exclosures. One exclosure
consisted of a large circular topless pen, 5 ;n in diameter (20 ra'' in
area). The other exclosure was a smalltr, square completely enclosed
cage (0.25 m^ in area).
Two pens were constructed, one in the mixed Ruppia-Zosterc bed
and another in the adjacent inshore sandy area (Fig. 1). The pens
were made of 4.3 ra long salt treated wooden pilings placed 1.5 m into
the bottom. Initially, thick-wall galvanized pipes (240 cm x 2 cm)
were placed between the equally spaced wooden pilings to provide shape
(Fig. 2). The pipes inadequately supported the weight of the netting
that was placed around the pipes and were later replaced with 10 cm x
10 cm x 360 cm wooden posts. Pens were encircled by a piece of black
plastic 0.63 cm r.iesh netting with a uv re.tardant (Conwed Corp Plastic
Netting f/OV3010). The netting, which was 324 cm wide, was attached to
the posts at a height of 240 cm above the bottom. Thus, the top of
the pen were always above the water. Excess netting was stapled aloru-
the bottom with 18 cm long wire staples to form a^i 84 cm wide skirf
which extended outward from each pen. The skirt prevented predators
from burrowing and gaining access into the pen. An entrance into each
pen was constructed by sewing a 5 cm wide x 324 cm long strip of
VELCRO to one end of the netting with the opposing piece attached to a
piling.
Smaller square cages measuring 50 cm on a side and 50 cm high
were constructed of reinforcing rod frames covered with the same
plastic netting as used on the pens. Each cage had 30 cm long legs
42
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R = RUPPIA
Z = 20STERA
S = SAND
/= MIXED
P=PENS
= TRANSECTS
CHESAPEAKE
BAY
Fig. 1. Location of study site for predator exclusion experiments.
43
-------
which were pushed into the bottom anchoring the cage. A top attached
with VELGRO strips on three sides allowed easy access into each cage.
Panels simulating only the sides of cages were similarly constructed
to simulate some of the cage effects but still allow predator access.
The use of a large topless pen and smaller cage in combination
was chosen for several reasons. Traditional caging experiments in
both soft and hard substrates have relied on small cages (less than
1 m^) with different size meshes. Cage effects such as current
reduction and sediment deposition are usually associated with the use
of a cage, and similarly would affect larval recruitment (Virnstein,
1978, 1980). The use of appropriate controls such as two-sided cages,
and topless cages have avoided some of these problems. However, for
motile predators, these controls are still not appropriate. We felt
that by building a large enough pen with no top, cage effects would be
considerably reduced from that of the smaller cage. The comparison
between the cages and cage controls inside and outside the pen would
allow us to further distinguish some of the complex cage effects.
Triads of experimental treatments were randomly arranged in
triplicate both within and outside of the pens in each of the two
habitats. A triad consisted of three experimental treatments: a
complete cage enclosing 0.25 m of bottom area, and open cage with no
top and paralle sides of 0.25 m^, and an uncaged control area (Fig.
2). One of the three triads per experimental condition (sand; sand
plus pen; grass, grass plus pen) was designed to be destructively
sampled after an appropriate time interval.
Pens were constructed in each of the two areas (grass and sand)
in late April, 1979. Prior to setting out the cages, infauna and
epifauna were sampled inside and outside the pen in both the sand and
grass (see below for sampling methodologies). After the faunal
sampling, the cages were placed randomly in the pen along each
experimental triad as discussed above. One of each of the three
triads were destructively sampled in June 12-14, September 11-13 and
November 13-16, 1979.
Two days prior to the first sampling period, a strong Northeast
storm destroyed the netting on the pens. Sampling for fauna was
conducted according to our design after which the pens were rebuilt.
In addition to the smaller mesh, a backing of heavier, large mesh
(13 mm) netting (Conwed Corp. Plastic Netting #OV1580) was added for
support.
Problems were also encountered with the cages in the sand area.
Despite the bottom edges of the cages being placed approximately 5 cm
below the sediment surface, large blue crabs burrowed under the edges
and had gained entrance to these cages. Because of this disturbance,
all sand cages were removed and replaced by new ones and positioned
over a portion of the bottom that had been uncaged. A 24 cm wide
skirt was also placed around each sand area cage. Cages in the grass
area were not disturbed by crabs. These cages were left in place to
-------
K.y
i i Complete tag*
Ii Op«n cog*
• No cog*
Fig. 2. Design of predator exclusion .experiments showing the construction
of the large pen and'the placement of experimental triads. One
triad consists of a complete cage, an open cage, and an area with
no cage; there are three triads per la^ge pen.
45
-------
follow the development of the community over time. In addition, new
cages were placed in the grass area to parallel those that were placed
in the sand area.
During each sampling period, both epifauna and infauna were
sampled similarly. Samples collected within the pen were done as
carefully as possible to minimize the disturbance to adjacent
vegetation. Prior to the sampling, one triad was randomly designated
to be sampled. Epifauna were collected first, by clipping the shoots
as close as possible to the sediment surface and gently placing these
blades into a collecting bag with 0.5 mm mesh bottom. If the
epifaunal sample was to be taken from a caged area, the cage was first
removed before sampling. All samples were taken from an area of
approximately 0.1 m^. After epifaunal samples were taken, additional
grass was clipped and removed to allow for adequate space to take the
infaunal samples.
After collection, epifaunal samples were kept in water and
processed live by stripping all epifauna from the blades and
preserving them in 10% buffered seawater with formalin containing the
vital stain Rose Bengal. The remaining plant material was sorted
according to species (Kuppia, Zostera, algae), oven dried at 80 C for
at least 48 hours and then weighed to the nearest 0.1 g.
Infaunal samples were collected at the same location as the
epifaunal samples. Initially, 10 cores for infauna were taken with a
plexiglas corer (0.007 m^) to a depth of 15 cm. Subsequently, it wao
found that seven rores were adequate to describe the density and
diversity of infauna. Infaunal cores were placed in labeled plastic
bags containing isotonic MgCl2 as a relaxant. This prevented smaller
polychaetes and oligochaetes from crawling through the sieve. All
infaunal samples were washed through a 0.5 mm mesh sieve and then
retained material was preserved in 10% buffered seawater and formalin.
Rose Bengal was also used to facilitate laboratory sorting.
All individuals were identified to species if possible using the
most recent keys for identifying marine invertebrates.
Three sediment cores were taken from each treatment each sampling
period and sediment grain size analysis conducted on each sample
according to Folk (1961).
Sediment traps, consisting of three small jars strapped to a
wooden top with funnels clamped to the wooden top to allow suspended
sediments to accumulate in the jar, were used to assess any
differences in sedimentation rates in the pens and cages in the sand
area only.
Dyed sediments were placed inside the pen and cages both in the
grass and sand area to monitor sediment mobility in each of these
treatments.
-------
Larval traps, made of one gallon jars attached to stakes inside
and outside pens, were also used to assess variations in larval
recruitment rates that may be due to cage effects.
Because of the excess fouling that can occur on exposed objects,
the pens and cages were cleaned regularly to prevent buildup of
excessive epiphytic algae by rubbing all sides with plastic cloth
brushes constructed of the same material the cages were made of.
Minnow traps and small crab pots were maintained inside each of
the pens to catch small fish and crabs that may have entered the pen
at small sizes and grown to sizes where they could not exit. Cages
were examined weekly to remove, fish or crabs that entered the cages.
Numerical abundance histograms were plotted by area for both
species and individuals found in the infaunal and epifaunal (grass bed
only) community. Species diversity was calculated for each area using
the index of Shannon (Pielou, 1975). The index H1 is expressed as:
H1 = £ Pi Iog2 Pi
where s = number of species on the sample and Pi = proportion of the
i-th species in the sample. This index is commonly used for
comparative pu-poses and includes both a species richness (the number
of species in a community) component and an evenness (how equitably
the individuals are distributed between the species) component.
Because the blue crab, Callinectes sapidus is such a dominant
predator in the grass bed, we examined the stomachs of blue crabs for
feeding analysis. Eighty-three blue crab stomachs were analyzed in
1978. Individuals were collected with a 4.87 m (16 ft) otter trawl
with 19 tarn (3/4 inch) wings and a 6.3 tarn (1/4 inch) cod end liner.
The trawl was pulled for a period of 2 min. at a speed of 2 to 3
knots. Collected crabs were subsampled and those selected were
immediately weighed, measured, sexed, and the molt stage noted.
Stomachs were removed in the field and preserved in 10% buffered
seawater formalin with" the vital stain, Rose Bengal. Each stomach was
carefully dissected in the laboratory and the contents enumerated and
identified when possible.
RESULTS
The pen and cagp experiments in the sand and grass areas affected
both the epifaunal and infaunal components during the course of this
study. Because of the large data set collected for both components,
the results for the infauna, and epifauna will be presented separately.
It must be stressed that this separation is artificial and done only
for simplification of the discussion. However, there are undoubtedly
important interactions that occur between both components and any
possible interaction will be analyzed in the discussion section.
47
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I. Infauna
Despite the cages and pens being present for only two months,
there were some dramatic differences in the response of the infauna to
several of the treatments.
In comparing the sand area to the grass area for the June data,
several effects were evident: 1. The mean number of species per core
for all the treatments in grass were higher than the comparable
treatments in sand (Fig. 3). Within the grass area, there were no
differences among the treatments whereas in the sand, the cage (C) and
pen + cage (PC) treatments had more species than the other treatments.
The pen (P) and pen + open cage (PO), in turn, had more species than
the control (S) and open cage (0). 2. The mean number of individuals
per core for the grass treatments were greater than the sand
treatments except for the cage (C) and pen + cage treatment (PC) (Fig.
4\ where similar numbers were recorded. There were no differences
among all of the grass treatments whereas the sand cage (C) and pen +
cage (PC) were greater than the other four sand treatments. 3.
Comparison of diversity between the two habitats (Fig. 5) was not as
distinct as with number of species or individuals since the H1 index
is sensitive to not only species number but the distribution of the
individuals among those species. Diversity was, in general, highest
in the grass areas as compared to the sand area, with the pen + (PC)
cage treatment having the highest diversity of the sand treatments.
Lowest diversity was found for the sand control (S) and open cage (0)
in the sand area. 4. The pattern of species dominance was very
different for the sand and grass habitats (Table 1, 2). This was
particularly evident for the soft shell c'ara, Mya arenaria, whose high
densities only in the sand cage (C) and sand cage + pen (P+C),
contributed to the high densities of individuals for the^c two
treatments. Gemma gemma was also found in increased abundance in
these two treatments as compared to the other sand treatments. Gemma
was the dominant species in the other sand treatments but densities
v:ere not as high in the cage treatments. The grass infauna was
dominated by large numbers of the capitellid polychaete, Heteromastus
filiformis, the spionid polychattes, Poiydora ligni and Streblospio
benedicti, and oligochaetes. The cirriped, Balanus improvisus, was
recorded in these samples. Though Balanus is epifaunal, many were
present on old leaf material that had settled on the bottom after the
barnacle covered leaves had sloughed off from tne plants. Mya \
arenaria was present in the grass treatments but their numbers were ',
low compared with the densities found in several of the cage
treatments. Many of the dominant grass infaunal species were present
in the sand area but in vary low densities and there were no species
that were restricted to either of the two habitats.
Data for the September sampling date revealed similar trends to
the June data: 1. Ihere were more species in the grass habitat than
the sand (Fig. 3). The numbers of species per core for the pen (P)
and cage (C1) treatments in the sand were not different from each
other but were higher than the control. The species per core in the
48
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Fig. 4. Number of individuals per core recorded from infaunal samples for
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pen + open cage; PC=.pen + cage; 0=open cage, 2 sides and no top;
C =new cage set in June; PC =new pen + cage set in June. Closed
circles (•) represent number of.individuals for the cores taken
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pci core.
50
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TABLE 1. LIST OF TOP TEN DOMINANT SPECIES RECORDED FROM INFAUNAL CAGING EXPERIMENT SAMPLES FOR THE SAND HABITAT FOR JUNE. NUMBERS
REPRESENT PER CENT COMPOSITION THAT EACH SPECIES COMPRISES OF THE TOTAL SAMPLE AND ITS DENSITY PER M2 . TOTALS FOR THE TOP
TEN AND FOR THE TOTAL SAMPLE ARE ALSO GIVEN.
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grass treatments were variable as evidenced by the distribution of
each of the cores for each treatment. Tha mean number of species per
core for the older cage (C) and pen + cage (PC) treatments were
greater than the other treatments while the grass control (G) had the
fewest but these are probably not significantly different. Species
number was reduced in the control as compared to the June data while
the new cage (C1) and pen + cage (PC1) treatments had less mean number
of species per core than the comparable older treatments. 2. Numbers
of individuals were again higher in the grass habitat than the sand
but the differences were not as large as in June. The density of
infauna for the- sand treatments were greater than the control as was
the case for the grass habitat. The density of infauna in the grass
control (G) was also similar to the sand treatments. Overall,
densities of infauna in the grass and sand were less than that
observed in June for all treatments. 3. Mean diversity (H1) was
higher in the grass habitat than in the sand habitat. There was no
difference among the grass treatments and control while in the sand,
H1 was higher in the treatments than the control though there was
considerable overlap of the H1 for the samples. 4. Dominance
patterns of species in each of the two habitats for the different
treatments varied from the previous sampling period (Tables 3. 4).
Because the caged areas in the sand were completely disturbed, after
the June sampling by blue crabs, the pattern represent trends recorded
for only two months. The grass cages, because they were not
disturbed, allowed for a comparison over a longer time scale. In
addition, the newer cages, also set up in June to compliment the sand
studies, allowed comparisons of recruitment on a shorter time scale.
In the sand area, the bivalve Gemma gemmr. was one of the dominant
species (Table 3) in the pen (Piand cage treatments (C1, FC1) but was
absent from the control area (S). Species present in the control area
were only small, tube dwelling polychaetes in very low abundances.
Another bivalve, Mulinia lateralis, was only abundant in the cage (C1)
and pen + cage (PC1)treatments. In the grass treatnents (Table 4)
Gemma was very abundant, whose densities were, in most cases, higher
than those densities recorded in June. The polychaete, Heteronastus
filiformis, was much less abundant in June, though it was still one of
the top 10 species. Balanus was no longer a dominant species (except
in the old cage (C), a result of the old leaves having either been
washed out of the area or dying as the leaves to which they were
attached decayed. Oligochaetes were also abundant as they were in \
June with approximately similar densities (one exception, they were \
not dominant in the cage treatment). j
One particularly interesting species found more abundantly in the
caged treatments, especially those initiated in April (C and PC) than
the pen (P) or control (G) was the oyster, Crassostrea virginica
(Table 5). Crassostrea is usually not found setting in grass beds but
was found to have actually set on pieces of eelgrass along tne bottom
of the cages.
Crepidula convexa, an epifaunal gastropod was abundant in all the
treatments. Its presence as an infaunal component is a reflection,
54
-------
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TABLE 5. DENSITIES (PER M2) OF THE OYSTER, CRASSpSTREA VIRGINICA. FOUND IN
THE GRASS HABITAT FOR EACH OF THE EXPERIMENTAL TREATMENTS AND CONTROL
FOR SEPTEMBER AND NOVEMBER.
Control (G)
Old cage (C)
New cage (C1)
Pen (P)
Pen + old cage (PC)
Pen + new cage (PC1)
September
21
3561
1760
642
10621
1491
November
41
4265
-
104
9317
1222
57
-------
probably, of its spillover from the epifauna where it was present in
very large numbers.
The patterns discussed above for the infauna collected in June
and September was evident in most cases through November. 1. The
number of species was again higher in the grass habit't compared with
the sand habitat (Fig. 3). Species number was higher in the sand
treatments compared with the control while in the grass, there were no
distinct differences among the treatments, although there was a lot of
variation between cores of similar treatments. Except for the old
cage treatment, the mean number of species for each of the grass
treatments and control was higher compared to September and in June.
2. The number of individuals per core was higher in all grass
treatments compared with the sand treatments (Fig. 4). Density in the
sand control was less than the three experimental treatments which
among themselves were not different. Densities in the grass
treatments were similar and were higher than densities found in the
grass habitat in September. 3. Diversity (H1) was also higher in the
grass habitats compared to the sand area. The sand treatments
incorporating the cages had a higher H' than the pen or control while
the mean diversity for each grass treatment was not different. 4.
The dominant species in the sand area in November was similar to that
found in September (Table 6). Gemma was the dominant species in the
pen + cage (PC1), pen (P), and new cage (C1) treatments and Capitella
(polychaete) was dominant in the control (S) with Gemma the second
most abundant species. The spionid polychaetes, Strebfospio and
Polydora, increased in abundances over the September densities.
Species dominance in the grass treatments for November (Table 7)
were, in most cases, not similar to each other. Gemma was the
dominant species in the new cage (C1) as it was in September and was
also abundant in the pen + new cage (PC1), pen (P) and grass control
(G). Densities of Crassostrea (Table 5) were similar to that recorded
in September for the new cage (C1) and was also very abundant in the
old cage (C) and pen + new cage (PC1) treatments. It was not recorded
in •'he new cage treatment (C1) where, in September, the new cage
contained 1760/m . Crepidula was still abundant in all treatments and
control. The oligochaetes increasad in density over September's
density in the new cage (C1), grass control, old cage + pen (PC) and
old cage (C). Densities of Polydora ligni and Streblospio benedicti
increased in all treatments compared with September as was the case
for the sand treatments discussed above.
II. Epifauna
Because of the experimental design, only one sample of eelgrass
could be taken at the time of sampling. All samples were roughly
estimated to be approximately 0.1 m^ in order to make sample size
equivalent.
In June, the penned treatments (P, PO and PC) had more species
per sample (Fig. 6) than the unpenned area while the caj-.t.d area (C)
58
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30-1
JUNE
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30-i
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NOVEMBER
G P C C PC PC
TREATMENT
Fig. 6. Number of epifaunal species per sample for each treatment and control
during the three sampling periods. Treatment designations are as
follows: G=grass control; P=*pen; C=cage; P0=pen + open cage; PC=
pen i cage; 0=open, topless cage; C*=new cage set; PC =new cage
•f pen set.
61
-------
had slightly more species than the open cage (0) and control (G). In
contrast to species number the open cage treatment had more
individuals/g of grass while the cage (C) and pen + cage (PC) had the
least number of individuals/g grass (Fig. 7). These differences are
primarily attributed to the differences in the density of the
barnacle, Balanus improvisus (Table 8) which was very abundant in the
open cage. Seven of the top ten dominant species were shared among
all treatments including the control while Balanus was the dominant
species and Crepidula the second or third most abundant species in
each treatment. The top three species in each treatment constituted
90% or greater of all individuals recorded for each sample. This
overwhelming dominance by a few species was the cause for the overall
low H' (diversity) for the treatments in June (Fig. 8). There were
also no major differences in H' among the treatments for June.
In September, all treatments had more species per sample than the
control (Fig. 6) with the cage (C) treatment having the greatest
number. Except for the cage treatment, the grass control, pen and pen
+ cage had fewer species than that recorded for June. The new cage
(C1) and new cage + pen (PC1) had slightly fewer species than the
comparable older treatments. This situation paralleled the response
of the infauna to the new cage sets also for the September sampling
data.
The density of epifaunal individuals per gram of -grass in
September was much greater in all treatments when compared to the
control (Fig. 7). The highest density was found in the new cage (C1)
and pen + new cage (PC1). These very high densities were caused by
the large numbers of Crepidula, which in five of the six treatments
made up 98% or greater of the total epifauna (Table 9). Balanus and
the isopod Erichsonella were either the second and third species in
all the treatments. Dense concentrations of Crepidula were observed
covering the blade from the tip to the base especially in the new cage
treatment, but were not evident anywhere outside the experimental area
in as dense concentrations. In addition, compared to June when seven
of the ten species were found in all treatments, only four of the top
ten were not found in all treatments.
The very low diversities of this sampling period, which were
lower than those calculated in June, were a result of the overwhelming
dominance by Crepidula. The slightly higher diversity value for the
cage (C) treatment was due to the fact that Crepidula comprised only
90% of the total sample compared with 98% or greater in the other
treatments.
By November, there appeared to be no difference in the total
number of species in each sample (Fig. 6). However, there were large
differences in the number of individuals among the different
treatments (Fig. 7). The lowest density was found in the cage (C) and
pen •*• cage (PC) treatments. This low density of individuals was due
primarily to the fact that the abundance of grass in these older cages
was very low. The oyster set that had occurred in these two
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0=open, topless cage; C =new cage set; PC =new cage + pen set.
66
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treatments probably caused some of this reduction as well as from the
overall reduction of light from the netting of the cages. The
reduction in -_he density of the grass in the newer cages was not as
dramatic since these cages were in the field for a shorter length of
time. The pen had the highest density of epifauna where the grass
density inside the pen was apparently not impacted by the presence of
the pen.
Crepidula maintained the dominant ranking in all treatments
through November (Table 10). The very large numbers in the pen (P)
treatment caused the large numerical density for this treatment
discussed above. In addition, Crepidula densities in all treatments
except the cage (C) made up greater than 96£ of the total sample. In
the cage treatment where grass density was low, Crepidula made up only
49% of the sample.
Also in the November samples, only three species were shared
dominants in all treatments compared with seven in June and four in
September.
The diversity (H1) of each treatment was very low again except in
the old cage (C) because of overwhelming dominance by Crepidula in
these treatments (Fig. 8). The decreased abundance of Crepidula in
the old cage (Table 10) allowed the other species to assume a greater
rank which resulted in a higher equilability component of H1 for the
cage treatment.
III. Blue Crab Stomach Analysis
The mastictory mode of feeding made the identification of gut
contents to the species level difficult. Percent frequency of
occurrence of food items indicated the blue crabs feed on both
epifaunal and infaunal species (Fig. 9). Zostera was found in 70% of
the stomachs analyzed. Generally, live, intact, and very uniformly
cut sections of leaf material were present, indicating that crabs may
ingest the blades but digest only the encrusting organisms. Epifaunal.
molluscs, isopods and Balanus improvisus were among the major food
items in crab stomachs. Callinectes also foraged among the rhizome
mat on infaunal molluscs. Feeding burrows and infaup.al feeding were
frequently observed in the field.
IV. Sediments
Table 11 presents the percent sand, silt and clay in the
sediments taken from the various treatments in the sand and grass
habitats in November, 1969. Within the sand habitat and grass
habitat, there appeared to be little difference among the treatments.
The percent sand in the grass control (G) and new cage (C1) was not
different from the sand. However the percent silt was higher in these
same grass treatments compared to the sand.
69
-------
100-r
75--
700
Fig. 9. Percent frequency of occurrence of food items in Callinectes
sapidus stomachs.
70
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TABLE 11. PERCENT SAND, SILT AND CLAY IN THE SEDIMENTS TAKEN FROM THE
DIFFERENT SAHD AND GRASS TREATMENTS IN NOVEMBER, 1979 (NUMBERS
REPRESENT MEANS OF THREE SAMPLES).
TREATMENT
SAND
CLAY
SILT
Sand (control)
Sand + Cage
Sand + Pen
Sand + Pen + Cage
94.2
93.6
Samples Lost
93.6
4.7
5.5
5.5
1.1
0.9
0.9
Grass (Control)
Grass + Cage (old)
Grass + Cage (new)
Grass + Pen
Grass + Pen + Cage (old)
Grass + Pen + Cage (new)
92.2
88 7
92.9
90.2
90.2
90.4
5.2
7.9
4.9
6.3
6.5
6.2
2.6
3.4
2.2
3.5
3.3
3.5
73
-------
The cage and pen treatments in the grass (except the new cage)
had less sand and more clay and silt than the control plot. The old
cage had the lowest percentage of sand and the highest percentage of
clay, a result of this cage being out the longest. These alterations
in the sediment fractions are not of a large magnitude. This may be
because the treatments we'e not in the field for a long enough time to
create sediment alterations and that the very dynamic nature of this
a^en prevents fine sands and silts and clays from accreting. It may
also indicate that the cages and pens did not have as significant
impact on the sediments as originally hypothesized.
DISCUSSION
Benthic environments colonized by submerged vegetation represent
a unique habitat with respect to their impact on the associated faunal
communities. The most notable characteristic of these beds are the
large densities of animals that are found associated with SAV compared
to the surrounding, unvegetated sediments (Thayer et al., 1975; Orth
1977; Reise, 1977b; Orth and Heck 1980; Heck and Orth 1980a). Recent
interest has centered on the factors that cause such high densities
(e.g. increased physical heterogeneity, decreased predation rates and
increased food) (Oi.th 1977; Reise 1977a; Peterson 1980; Nelson 1979;
Stoner 1980; Heck and Orth 1980b).
The advent of manipulative techniques in understanding function
as well as structure of the benthic communii-y has clearly identified
major factors that overwhelmingly influenced the makeup of the
community (Virnstein, 1977; Woodin 1974; Young et al. 1976; Reise 1977
a,b; Orth 1977; Peterson 1980). Though there are distinct problems in
field manipulation experiments, especially predator exclusion cages
(Virnstein 1978; Peterson 1980), these manipulative techniques have
been extremely useful in allowing a more thorough examination of
causative factors through experimentation, rather than previously
stressed correlative information.
Despite some of the difficulties encountered in the caging and
pen experiments (e.g. the breaching of the pen in June just prior to
our sampling and the crab disturbance of the sand cages), our results
suggest that exclusion of predators through cages and pens has an
impact on the macroinvertebrate fauna inhabiting the sand and grass
habitats.
Several trends were evident over the entire sampling period.
With respect to numbers of species, the grass habitat always had more
infaunal species per core than the sand habitat for all treatments.
There were apparently no distinct differences among the grass
treatments for species infaunal numbers but in the sand, species
numbers were higher in pen and cage treatments compared with the
control, with the cage treatments (C and PC) in June having the most
dramatic effect on increased numbers of species. However, once the
cages were disturbed and new ones set to replace the disturbed ones,
74
-------
the effects were not as dramatic though species numbers were stil
higher compared to the control.
In addition, except for the sand cage treatments (C and PC) in
June, there appeared to be no difference between the pen and cage
treatments for numbers of species in both habitats.
Infaunal species numbers were lower in September compared to June
and November. This could possibly be a result of natural mortality
due to high summer time water temperatures as well as predation
activity in Che uncaged and unpenned areas, and also possible
predatory activities of infaunal species on other infaunal species
that could not be detected through our study design. Similar summer
time depressions in infauna were observed by Virnstein (1977) for the
York River, Virginia.
Density of individuals in the grass habitat treatments was
generally higher than the sand habitat treatments except for the June
cage treatments. The differences in densities were not as pronounced
in the September period as in the other two periods. The September
density in the grass crntrol this month was very similar to the sand
treatments, but by November, the differences in densities had
increased between the sand and grass habitats.
In the sand area, densities were always higher in the cage and
pen treatments compared to the control in all months while in the
grass habitat only the September treatment densities were higher than
the control.
As with the species number, densities of infauna decreased in the
summer both in the sand and grass habitat. The large depressions in
the grass control suggests that predation in grass habitats can be
significant, especially in the summer when not only crabs are present
but also different benthic fish predators. The difference between the
highei numbers persisting in the treatments versus the control for
September's grass infauna possibly relates to that portion of the
infauna that escapes predation via the cages or pens.
The grass habitat acts as a refugia for infauna though many
individuals are still cropped by predatory effects during the period
when predation may be intense (e.g. summer periods). It is
interesting to note that the decrease in infaunal densities from June
to September was similar for both the sand (19%) and grass habitat
(17%). Those grass infauna surviving the high summer predation levels
do so primarily because of the presence of the grass.
Species numbers and density in the new cages in the grass area
were lower than comparable figures for-the older cages. This suggests
that timing of the placement'of cages has an effect on the settlement
densities as recruitment periods for different species may vary,
exposing the benthic environment to a different suite of recruits at
different periods.
75
-------
Species response to the cages and pens in the sand and grass
habitats was variable. Gemma gemma, a sand dominant, persisted in the
cage and pen areas, but was almost entirely eliminated from the sand
control area by predation, either by blue crabs or rays which
frequented this habitat all summer. The large increase in Mya in the
June cage areas in the sand only suggests a cage effect in that the
reduction in current velocity inside the cages may have allowed high
densities of Mya to settle preferentially. It is also possible that
the planktonic larvae of Mya, when contacting the cage surface,
initially attached to the cage via byssal threads and then fell into
the cage as they got older, which could explain why they were not as
dense in the pen treatment (P). The absence of Mya in the grass
habitat cages cannot be explained except by vagaries of planktonic
recruitment or the grass bed acting as a filter and allowing a more
even settlement of Mya throughout the grass area.
Crassostrea, the American oyster, appeared to be affected by the
older grass cages. Like Mya it has planktonic larvae and the
conditions that favored Mya settlement may have been the same for the
oyster. Crassostrea attached to the blades of grass and subsequently
grew on the bottom. The lack of a hard substrate in the sand cages
(oysters do not produce byssal threads) may be the reason for lack of
oyster settlement in the bare sand area.
The results of our caging work present both similarities and
dissimilarities to recent work done in other comparable grass
habitats. Reise's (1978) data paralleled our results where predator
exclusion experiments he conducted had greater impact in unvegatated
habitats than vegetated habitats, which was similar to what we found
in our experiments. Reise concluded that predation was mitigated by
the spatial resistance of the grass and limited accessibility. Orth
(1977) showed densities in caged treatments significantly increasing
over short periods of time in similar vegetated habitats in the
Chesapeake Bay. The cause for this difference may be timing at which
cages were initialized, i.e. August in Orth's study and April and June
in this study. This suggests that the timing of the csge placement
relative to predatory activities may be critical in understanding the
role of predation in these habitat. !
Epifauna densities were impacted by the cage's effect on the \
growth of grass inside the cage. This was particularly evident in the
older cages where, compounded with the dense set of oysters and
fouling on the cages, the density of grass was reduced inside the
cages compared to outside the cages. In discounting the cages and
their effect on the grass density, the pens alone, where grass density
was not affected, had a large effect on epifaunal densities. In June,
densities of BaIanus were higher in the pen treatment and in September
and November, the very high densities of Crepidula inside the pen were
responsible for the large differences inside and outside the pen. In
September the new cages (C1 and PC1), which had not drastically
affected the growth of grass, also had very high densities of
Crepidula. Some stomachs of blue crabs examined during this period
76
-------
(1979) which had different contents than those examined in 1978,
suggest that blue crabs were feeding on Crepidula and that their
exclusion from the penned area and newer cages caused the high
densities of Crepidula to persist. Blue crabs do ingest grass and
most likely whatever is on the blades. Being very opportunistic they
will feed on anything that is available. The large abundance of food,
both in the sediment and on the blades, allow the blue crab an ample
food supply.
It appears that during the course of this experiment, predators
(including fish) consumed large quantities of food items from the
sediments and grass. The large secondary production estimates
observed from additional work done in this area (see Section IV on
Secondary Production) suggest an enormous food supply available for
consumption by many pred;.tor species, both fish and invertebrates.
Our data show large reductions of both epifauna and infauna between
June and September in open, uncaged or unpenned areas and that the
presence of the pens or cages had a significant impact on the
survivalship of prey species. The results here support many of the
recent works cited above on tne importance of predation in structuring
the benthic fauna and that this fauna provides a significant supply of
food to those predators.
77
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REFERENCES
Annala, J. H. 1974. Foraging strategies and predation effects of
Asterias rubens and Nucella lapillus. Ph.D. Thesis. Univ. of
New Hampshire. 233 pp.
Brooks, J. L. and S. I. Dodson. 1965. Predation, body size and
composition of plankton. Science 150:28-35.
Dayton, P. K. 1971. Competition, disturbance, and community
organization: The provision and subsequent utilization of space
in a rocky intertidal community. Ecol. Monogr. 41:351-389.
Dayton, P. K., G. A. Robilliard and A. L. DeVries. 1969. Anchor ice
formation in McMurdo Sound, Antarctica, and its biological
effects. Science 163:273-275.
Dayton, P. K., G. A. Robilliard, A. L. DeVries and R. T. Paine. 1970.
Bcnthic faunal zonation as a result of anchor ice formation at
McMurdo Sound, Antarctica. p. 244-258. Vol. 1 Antarctica
Ecology. Academic Press, London.
Folk, R. L. 1961. Petrology of sedimentary rocks. Hemphill's,
Austin, Texas. 154 pp.
Grigg, R. W. and J. E. Maragos. 1974. Recolonization of herciatypic
corals on submerged lava flows in Hawaii. Ecology 55:387-395.
Heck, K. L., Jr. and R. J. Orth. 1980a. Seagrass habitats: The
roles of habitat complexity, competition and predation in
structuring associated fish and motile raacroinvertebrate
assemblages. p. 449-464. In: V. S. Kennedy (ed.). Estuarine
Perspectives. Academic Press, New York.
Heck, K. L., Jr. and R. J. Orth. 1980b. Structural components of
eelgrass Zostera marina meadows in the Lower Chesapeake
Bay-Decapod Crustacea. Estuaries 3:289-295.
Nelson, W. G. 1979. Experimental studies of selective predation on
amphipods: Consequences for amphipod distribution and abundance.
J. exp. mar. Biol. Ecol. 38:225-245.
Odum, E. P- '971, Fundamentals of ecology. W. B. Saunders Co.
574 pp.
78
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Orth, R. J. 1975. The role of disturbance in an eelgrass,
Zostera marina, community. Ph.D. Dissertation. Univ. of
Maryland. College Park. 115 pp.
Orth, R. J. 1977. The importance of sediment stability in seagrass
communities, pp. 281-300. In: B. C. Coull (ed.) Ecology of
Marine Benthos. Univ. South Carolina Press, Columbia.
Ortu, R. J. and K. L. Heck, Jr. 1980. Structural components of
eelgrass Zostera marina meadows in the Lower Chesapeake
Bay-Fishes. Estuaries 3:278-288.
Orth, R. J., K. A. Moore and H. H. Gordon. 1979. Distribution and
abundance of submerged aquatic vegetation in the lower Chesapeake
Bay. U.S.E.P.A. Final Report. 600/8-79-029/SAVI. 199 pp.
Patrick, R. 1970. Benthic stream communities. American Sci.
58:456-459.
Peterson, C. H. 1980. Predation, competitive exclusion, and
diversity in the soft sediment benthic communities of estuaries
and lagoons. In: R. J. Livingston (ed.). Ecological Processes in
Coastal and Marine Systems. Plenum Press, N. Y. pp. 233-264.
Pielou, E. C. 1975. Ecological Diversity, Wiley Interscience, N. Y.
165 p.
Reise, K. 1977a, Predation pressure and community structure of an
intertidal soft-bottom fauna. In: B. F. Keegan, P. 0. Ceidigh,
and P. J. S. Boaden (eds.), Biology of Benthic Organisms.
Pergamon Press, N. Y. 513-519 pp.
Reise, K. 1977b. Predator exclusion experiments in an intertidal
mudflat. Helg. wiss. heersunters. 30:263-271.
Reise, K. 1978. Experiments on eoibenthic predation in the Wadden
Sea. Helg. wiss. Meersunters. 31:55-101.
Thayer, G. U., S. M. Adams, and M. W. LaCroix. 1975. Structural and
functional aspects of a recently established Zostera marina \
community. In: Estuarine Research, Academic Pr«ss N. Y. \
1:518-540. ',
Stoner, A. W. 1980. The role of seagrass biomass in the organi-
sation of benthic macrofaunal assemblages. Bull. Mar. Sci.
30:537-551.
Virnstein, R. W. 1977. The importance of predation by crabs and
fishes on benthic infauna in the Chesapeake Bay. Ecology
58:1199-1217.
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Virnstein, R. W. 1978. Predator caging experiments in soft
sediments: caution advised. Pp. 261-273. In: M. L. Wiley (ed.)
Estuarine Interactions. Academic Press, N. Y. 261-273 pp.
Virnstein, R. W. 1980. Measuring effects of predation on
benthic communities in soft sediments. In: V. S. Kennedy (ed.).
Estuarine Perspective. Academic Press, N. Y. 281-290 pp.
Wihlm, J. L. 1967. Comparison of some diversity indices applied to
populations of benthic macroinvertebrates in a stream receiving
organic wastes. J. Water Poll. Control 39:1673-1683.
Wihlm, J. L. and T. C. Davis. 1966. Species diversity of benthic
macroinvertebrates in a stream receiving domestic and oil
refinery effluents. Araer. Midland Naturalist 76:427-449.
Wihlm, J. L. and T. C. Dorris. 1968. Biological parameters for
water quality criteria. Bioscience 18:447-481.
Woodin, S. A. 1974. Polychaete abundance patterns in a marine soft
sediment environment: The importance of biological interactions.
Ecol. Monogr. 44:171-187.
Young, D. K., M. A. Buzas and M. W. Young. 1976. Species
densities of macrobenthos associated with seagrasses: a field
experiment study of predation. J. Mar. Res. 34:577-592.
80
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CHAPTER 3 /
PREDATOR-PREY INTERACTIONS IN A ZOSTERA MARINA (EELGRASS)
ECOSYSTEM IN THE LOWER CHESAPEAKE BAY, VIRGINIA
by
Robert J. Orth
and
Jacques van Montfrans
81
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ABSTRACT
Experiments were conducted with artificial seagrass in small wading pools
to assess the ability of prey to survive predation at different densities of
grass. Experiments using Mulinia laterialis, a bivalve, as prey, and adult
Callinectes sapidus, a crab, as predator, showed that almost no >1. lateralis
survived at 3 different densities of grass. Experiments with juvenile £.
sapidus as prey and adult C_. sapidus as predator showed greatest survival at
highest densities of grass. The behavior of the juvenile crabs in relation to
its predator was different in the presence of the grass than in its absence.
It was believed that the survival of a particular prey species in a vegetated
habitat will depend upon tne life style and life cycle of both prey and
predator and the density and morphology of the vegetation.
82
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INTRODUCTION
A species presence or absence and its abundance in any particular habitat
is regulated by its physiological tolerances, morphological constraints,
habitat preferences, and biological interactions such as competition and
predation with other animals (Dayton, 1971; Connell, 1972; Virnstein, 1977;
Nelson, 1979a, b; Stoner, 1980a, b, c). Predation is a significant biological
interaction in aquatic systems and has been shown to be the primary
structuring agent in many recent ecological studies in terrestrial, freshwater
and marine systems (Pai.ne, 1966; Dayton, 1971; Brooks and Dodson, 1965;
Connell, 1975). The ability of a prey species to avoid a predator will depend
on the morphological and behavioral modifications that the prey has evolved
over time in response to predation. In addition, the ability of the habitat
to mediate the effect of predation can play a significant role in the survival
of the prey (Stoner, 1980c).
Seagrass systems contain a very dense and diverse raacroinvertebrate
assemblage (Orth, 1973; Kikuchi and Peres, 1977) in which predation plays an
important if not key role in structuring the associated faunal community
(Nelson, 1979a, b; Heck aivi Orth, 1980a). Several studies have also alluded
to the idea that vegetations 1 density can have a significant affect on the
survival of the prey (Weinst-.'in and Heck, 1979; Heck and Orth, 1980a, b; Orth
and Heck, 1980; Stoner, 198Ub; Heck anf4 Thoman, 1981). Our objectives in this
study were to examine predator-prey interactions in a Zostera marina dominated
system and to assess the prey's ability to survive predation at different
vegetational densities.
MATERIALS AND METHODS
Two prey species with very different life styles were chosen for
predation experiments. We used a sedentary infaunal bivalve, Mulinia
lateral is, in one series of experiments. Mulinia is ubiquitous throughout the
Bay and inhabits a variety of sediment types where it burrows to a depth of
2-3 cm. This species grows to a length of approximately 2.5 cm and undergoes
periodic population eruptions, particularly in the spring (Boesch, 1973,
1974). However, the dense Mulinia populations experience high mortalities in
the summer, most likely due to predation (Virnstein, 1977).
Juvenile blue crabs, Callinectes sapidus, were used as prey in the second
set of experiments. Callinectes is highly motile and juveniles are
characteristically abundant in vegetated habitats of the lower Bay (Heck,
1981). This species is very important comnercially, being second only to
oysters (Crassostrea virginica) in terms of dollars contributed to Virginia's
seafood economy.
83
-------
Large, adult male C^. sapidus were used as predators in both sets of
experiments. Blue crabs are voracious predators and can be considered a
keystone species (sensu Paine, 1966) in structuring Chesapeake Bay benthic
communities (Virnstein, 1977).
Prey refuge experiments were conducted in three wading pools (2.43 m
diameter x 0.45 m high). Each pool had 10-13 cm of sand placed on the bottom
and was filled with estuarine water from the York River. Predation
experiments on Mulini •» were conducted outdoors using a flow-through water
system whereas those on Callinectes were set up indoors. Water from each
indoor pool was continually pumped through a large header tank which contained
crushed oyster shell to insure adequate oxygenation and removal of any
suspended material (Fig. 1). Each pool in both sets of experiments received
additional aeration from two piston air pumps.
Artificial Zostera marina rhizomes and leaves were used to simulate the
live system. Three densities of rigid plastic netting (1 incn diameter)
measuring 1 ra x 1 m (Conwed Corp. Vexar) were used to simulate the rhizomes.
High density mats were arbitrarily set at the normal plastic mesh density.
Medium and low density mats were reduced proportionately by cutting out cross
mesh strands.
Extruded polypropylene ribbon 5 mm wide and tinted green was used to
simulate the leaves. Three densities of grass were chosen for the
experimental treatments: a high density count consisting of 1600 blades/m , a
medium density count consisting of 800 blades/m^; and a low density count
consisting of 400 blades/m . The high values were Approximated from maximum
stem density counts of eelgrass frr-m a Zostera marina bed at the mouth of the
York River, Virginia. Artificial grass was attached to the artificial
rhizomes for those treatments testing both rhizome and leaf effects. This was
done by taking a single strand 30 cm long and tying it in half around the
plastic rhizome nat yielding 2 strands, each approximately 15 cm long. Low
densities of grass blades were attached to low rhizome density mats, medium
density blades to medium density rhizomes and high density blades to high
density rhizomes based on the assumption that in 2_. marina beds, there is a
positive correlation between blade and rhizome densities. Biomass
measurements from different j£. marina beds support this assumption (Orth and
Moore, 1982). All rhizome mats (with or without leaves) were placed 1 to 2 cm
beneath the sediment surface in each pool.
Adult male Callinectes were collected from a large Zostera marina bed at
the mouth of the York River using an otter trawl and maintained in holding
tanks. Prior to being used in experiments, all predators were starved for
48 hours by placing them in wire mesh cages, which prevented them from
effectively foraging in the hol'ding tank. Care was taken to handle the crabs
as gently as possible to prevent damage to the crab. Only males ranging in
size from 10 to 15 cm (carapace width), that had all appendages and no
visible, external breaks in the exoskeleton were used. Any male that was near
the shedding phase was not used.
The Mulinia-Callinectes experiments initially tested the eftects of high
density rhizome mats and also the high density rhizome and leaf combination on
84
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the survival of Mulinia. This was done because we assumed that if the bivalves
received little or no protection from the high density treatments, there would
be no refuge at lower rhizome and grass densities. One pool with no
artificial vegetation was also established and each treatment was randomly
assigned to each pool. Hulinia were provided from laboratory cultured stocks
grown at the VIMS Eastern Shore Laboratory. One hundred Mulinia ranging in
size from 1.5 to 2.5 cm were placed within the boundaries of each mat or
within a 1 m^ area at the center of the pool with no artificial vegetation.
Prior to introducing the predators the Mulinia were left undisturbed from 24
to 48 hrs until all individuals had burrowed into the sediment. Two predators
per pool were then introduced between 0800 and 1000 hrs and experiments were
terminated 24 hrs later. The crabs were removed from each pool and the
remaining Mulinia were enumerated after raking and sieving the sediment.
The initial Callinectes-Callinectes experiment tested the condition
thought to provide the greatest and least protection, respectively, to
juvenile crabs: high density leaves/rhizomes in one pool and no
leaves/rhizomes in a second pool. It was again assumed that if no refuge
existed for juvenile Callinectes at high density leaves/rhizomes, there would
be no refuge at lower densities. Since the prey appeared to derive some
protection from the high density treatment (see results), medium and low
density treatments were also tested. Experiments were conducted
simultaneously in pools with sand but without artificial grass mats.
Treatments were randomly selected and assigned to each of the 3 pools. Only
combinations of rhizome mats and grass were used because it was assumed that
juvenile crabs, being motile prey, would not remain buried when approached by
a crawling predator, and therefore the rhizome mat alone would provide little
or no protection. Leaves provide the greatest protection for juvenile crabs
by restricting the visual cues initiating predator attack and by presenting a
physical barrier to successful predation encounters.
Juvenile male and female blue crabs ranging in size from 4 to 6 cm in
carapace width were separated from otter trawl collections taken in a York
River Zostera marina bed and held in e flow-through tank for use as prey.
Only intact crabs showing no signs of molting were used. Ten prey were placed
in each of three pools and left to acclimate for 24 hrs. Four predators were
then introduced into each pool. Experiments were terminated 48 hrs later and
all remaining crabs were removed, measured and examined for any physical
damage.
Salinity and both sediment and water temperature were monitored twice
during each experiment. Frequent visual observations were made of predator
and prey behavior in each pool from a vantage point that caused minimal
disturbance to che experimental animals. All experiments were conducted under
ambient light conditions.
RESULTS
Muliria-Callinectes Experiments
Data from two complete experimental series (Table 1) indi^afe that
Mulinia received virtually no protection from either the high density rhizome
86
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TABLE 1. NUMBER OF MULINIA SURVIVING IN 24 HOUR EXPOSURES TO CALLINECTES AT
HIGH RHIZOME DENSITY, HIGH LEAF/RHIZOMES DENSITY AND BARE SAND (EACH
TREATMENT UTILIZED 100 M '.INIA and 2 CALLINECTE3).
Percent Mulinia Surviving
Treatment Test 1 Test 2
High Leaf/Rhizome 2 1
High Rhizome 2 1
Bare Sand 2 3
TABLE 2. NUMBER OF JUVENILE CALLINECTES SURVIVING IN 48 HOUR EXPOSURES TO
ADULT CALLINECTES AT THE DIFFERENT LEAF/RHIZOME DENSITIES.
Treatment Percent of juvenile Callinectes surviving - Test No.
JL _?. _! JL _JL _A _! _§. _i *
High 70 70 80 70 60 100 77
Medium 80 100 100 93
Low 50 20 60 60 40 90 . 70 80 59
None 30 20 30 50 30 0 30 0 40 26
87
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component or a combination of high density leaves and rhizomes.
Our observations indicated that Callinectes began feeding on Mulinia soon
after they were introduced into the pools regardless of the experimental
treatment being tested.
Callinectes-Callinectes Experiments
The initial test conducted with three adult predators and 10 juvenile
prey in each pool yielded 90% survival in t.ie pool with high density rhizomes
and leaves and only 20% surviving in sand. This suggested a protective value
of grass for juvenile Callinectes. We then proceeded to test the effects of
other vegetational densities on prey survival.
Nine experiments were conducted at four different levels of leaf density
(high, medium, low and none) (Table 2). Only three tests were run with the
medium grass density because of inadequate time and the reduced availability
of suitably sized crabs. Declining water temperatures caused the adult male
crabs to move into deeper water while most individuals of the year class that
provided the prey had grown too large. Lower water temperatures also caused
crabs in several later experiments to be lethargic thus confusing
interpretations of vegetational refuge effects. These data were not included
here.
Several earlier tests were aborted because the water flow was interrupted
due to pump breakdowns causing conditions in the pools to change. Crabs
behaved differently in these situations, being more lethargic. Thus the
number of replicate experiments was lower than that originally planned.
Experimental data were statistically treated using a one way analysis of
variance and the Studeiit-Newraan-Keuls multiple comparison test for unequal
sample size was used for testing differences among the means (Table 2).
Because of the nature of the data (counts), they were square root transformed
/ (x +.5) and then the calculations were performed. There was a significant
difference (p<.01) between the vegetated and the unvegetated treatments.
However, there was no significant difference among the three densities of
vegetation though the trend in the means indicated that low density vegetation
had less of a refuge value than the high and medium dense vegetation. We feel
that increased replicability could have reduced the variability but
environmental considerations (low temperatures) did not allow for further
effective experimentation.
Observations on both juvenile and adult Callinectes during the course of
the experiments provided some insight into predator-prey behavior as affected
by the presence or absence of vegetation. When first placed in the pools with
no vegetation, juvenile (3. sapidus initially moved around the entire pool and
eventually burrowed randomly throughout the pool. However, when placed in the
pools with vegetation, juveniles initially exhibited the same random movement
but then virtually all individuals gravitated towards the grass mat and
burrowed within its boundaries.
88
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When predators were introduced after the juveniles had acclimated tc the
pools for 24 hours, different responses were again elicited by the juveniles
dependirg upon the presence or absence of the artificial vegetation. The
introduction of predators into the unvegetated pools caused the juveniles to
immediately emerge from the sand and move actively around the pool in an
attempt to avoid predation. In several experimental replicates without
vegetation, a juvenile would be caught and either be eaten or lose several
limbs soon after the introduction of the predators. The restless disposition
of the prey in these treatments was evident during the entire experiment. In
contrast, when the adult crabs were introduced into the vegetated pools,
juveniles remained buried or hidden in the grass plot for the duration of the
experiment. Phis was particularly true in treatments with highest density
vegetation.
The adult crabs behaved in a dissimilar manner at the three different
densities of vegetation. At the high density vegetation, they were rarely
seen foraging inside the vegetation zone although some were occasionally
observed resting on the artificial blades. It appeared that the dense area of
blades imped€-d their ability to forage effectively. Adult crabs were
frequently observed in the low density vegetated area and their movements did
not appear to be as significantly impeded by the grass as they were in the
densely vegetated plot. Remains of juvenile crabs were seen in the sparse
vegetation but where these prey were actually caught was not witnessed.
DISCUSSION
Beds of submerged aquatic vegetation serve as both a refuge from
predation and a feeding area. Though a species might utilize a grassbed for
multiple reasons (e.g. both feeding and protection), it is important to
separate the relative ecological role of each. Furthermore, a species
utilization of a grassbed may vary depending on its life cycle stage. For
example the habitat may be more important ac a refuge to a juvenile individual
of a species but may shift towards importance as a feeding area in the adult
stage. Or efforts concentrated on examining the refuge function of eelgrass.
The results of our experiments suggest that beds of submerged vegetation
do not have the same refuge 'value for all species. Mulinia received little
protection from the presence of the vegetation. Its only escape responses is
to retract into its thin shell. Even in very dense vegetation, a predator,
such as the blue crab, has easy access to Mulinia which helps to explain why
this species is never very abundant in vegetated habitats. Mulinia undergoes
population eruptions but numbers are rapidly reduced by predators. Only in
those situations where they have been completely protected from predators
(e.g. inside predator exclusion cages) do large numbers of Mulinia survive for
a significant length of time (Virnstein 1977; our unpublished data from the
pen experiments for this project).
Juvenile Callinectes, on the other hand, were significantly protected by
the vegetation and the degree of protection appeared to be related to
vegetational density. Submerged plants visually and physically impede a
predator thereby interfering with its search attack strategy. It was probably
89
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for this reason that the juveniles we observed remained within the artificial
grass mat when a predator approached.
Our experiments involved only one predator and two prey species.
However, when our results are considered with both those of Ken Heck of the
Philadelphia Academy of Natural Sciences (unpublished) who conducted similar
experiments and with other previously published accounts of predator-prey
interactions (Heck, 1981; Heck and Thoman, 1981) a more generalized scheme of
such relationships in grassbeds can be conceptualized. The following scheme
incorporates the importance of predator and prey life styles, life cycle
stages, and the density and morphology of the vegetation.
1. In general, vegetated habitats provide a greater refuge for mobile prey
than for more sedentary prey. Among the mobile epifaunal species, those that
are highly motile (e.g. juvenile fish, shrimps, and crabs) will be less
susceptible to predation than those which are slower moving (i.e. isopods and
amphipods) in a three dimensional habitat (grassbed) than in a two dimensional
habitat (bare sand). This is particularly true if the predator has a search
and destroy type strategy rather than an ambush type approach. Among the
sedentary infaunal prey species, the refuge value of the grassbed will not
differ greatly from that of a bare sand habitat. Instead it will depend on
the lifestyle and biology of the prey rather than as much on the presence of
the grass. The degree of protection for such species will depend on whether
or not it is a tube dweller, if it has some external means of protection such
as a shell and if so, the nature and quality of the shell, and lastly, the
vertical extent to which the species can burrow. Sedentary infaunal species
that build tubes will recieve greater protection than non-tube builders in
both kinds of habitats. However, species which are able to burrow beneath the
rhizome layer will derive more protection than those which burrow equally as
deep in unvegetaced areas. In addition, species that live in tubes that
extend well below the sediment surface receive adequate protection from the
rhizome mat so that their abundances are not greatly affected by additional
protection from predators (e.g. via predator exclusion cages). These facts
have been demonstrated for the deep burrowing polychaetes such as Heteromastus
filiformis and Spiochaetopterus oculatus (Orth 1975, 1977; Virnstein, 1977)
which were more abundant in vegetated areas than adajcent non-vegetated areas
and also which were equally abundant inside and outside predator exclusion
cages in the two respective areas. The refuge value for tubeless sedentary
forms will also depend on their position in the sediment horizon with those
species living closer to the sediment surface being more susceptible to
predation. Our data show this to be true for Mulinia which lives just below
the sediment surface and which derives virtually no protection from its thin
shell against blue crab predation. Within a grassbed, epifaunal tube builders
would be less protected than those which are infaunal since the latter could
be protected by rhizome layer. Yet we hypothesize that epifaunal tube
builders have a greater chance of survival than epifaunal non-tube builders.
2. The refuge value of the vegetation will invariably be a function of the •
different stages of the life cycle of a species. For example, a juvenile blue
crab is highly protected by the vegetation. However, once the crab reaches a
certain minimum size natural predation becomes less of a factor in its
survival. Therefore the grassbed is diminished in importance as a refuge for
90
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the larger crab, with the one important exception being the very vulnerable
soft crab stages during the molting cycle. The reverse case would be that
juveniles of a species are not protected by the vegetation but older
individuals are. For example, the soft shell clam, Mya arenaria, lives near
the sediment surface when their planktonic stages first set and the juveniles
start to grow. With age, this species burrows deeper in the sediment.
Because adult Mya are also found outside vegetated areas, we suggest that the
minimum depth at which older Mya escape predation is less in vegetated areas
than in non-vegetated areas because the rhizome mat would provide a physical
barrier to the digging activities of predators such as the blue crab.
3. The refuge value of vegetation will be directly correlated with the
density or biomass of the leaves (Heck and Orth, 1980a, b; Stoner, 1980a, b)
for mobile species and for deeply burrowing ones it will be correlated with
the density of the rhizome mat. The inceasing coverage offered by vegetation
makes it more difficult for predators to effectively seek out and consume prey
items, possibly interfering with potential behavioral patterns in these search
strategies (Stoner, 1980b).
4. The refuge value of vegetation for a prey item will vary depending upon
the foraging strategy of a particular predator. For example the refuge value
for the prey of an ambush predator (i.e. one which sits and waits for prey
items to pass by) may be different than that for a prey species fed upon by
search predator (i.e. one which actively forages over a given area for prey
items).
5. Different species of vegetation may have different refuge val;.es depending
on theii morphology. We are suggesting that at the same density of plants per
unit area of bottom, the more foliose species (i.e. those which are more
highly branched or having a high ratio of surface area to biomass) have a
greater reguge value than less foliose species. The degree of branching is
directly related to amount of cover which allows prey species to effectively
escape predation. Data from Heck's (1981) experiments showed grass shrimp,
Palaemonetes spp., to have significantly higher survival rates in Ruppia
vegetated areas than Zostera vegetated areas. According to Heck, Ruppia is
more foliose than Zostera which would account for tl>e increased survival of
grass shrimp that he observed. In addition, field samples collected in. a
dense Ruppia bed by Heck yielded densities of grass shrimp higher than any
samples collected from Zostera beds (Heck and Orth, 1980b; Heck, 1981).
Since the amount of branching and plant density are both critical factors
in the survival of prey in grassbeds and different species of vegetation have
different surface areas based on their morphology, we can hypothesize that a
low density of a highly foliose species would have the same refuge value as a
high density of a less foliose species. Stoner's data (1980c) is particularly
relevant in that he concluded that blade surface area of macrophytes provides
the best estimate of habitat complexity in seagrasses. This particular factor
would be a critical one in management's option to replant vegetation. Because
of the increased coverage afforded by more foliose species, the most viable
option for replanting would be to use these species where possible.
91
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In conclusion, beds of submerged aquatic vegetation play a distinct role
in regulating the distribution and abundance of associated animals by their
ability to mediate both predator-prey and competitive interactions. The
degree of mediation will depend on the animal species in question and the
density and morphology of the vegetation. This degree of interaction of the
plant with its environment make submerged aquatic vegetation areas one of the
most interesting and ecologically important systems in the marine environment.
92
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LITERATURE CITED
Boesch, D. F. 1973. Classification and community structure of macrobenthos
in the Hampton Roads area, Virginia. Mar. Biol. 21:226-244.
Boesch, D. F. 1974. Diversity, stability and response to human disturbance
in estuarine ecosystems. Proc. 1st Intern. Cong. Ecol., The Hague,
Netherlands, p. 109-114.
Brocks, J. L. and S. I. Dodson. 1965. Predation, body size and composition
of plankton. Science 150:28-35.
Connell, J. H. 1972. Community interactions on marine rocky intertidal
shores. Ann. Rev. Ecol. Syst. 3:169-192.
Connell, J. H. 1975. Some mechanisms producing structure in natural
communities. Pp. 460-490. In: M. L. Cody and J. M. Diamond (eds.),
Ecology and Evolution of Communities. Harvard Univ. Press, Cambridge.
Dayton, P. K. 1971. Competition, disturbance and community organization: the
provision and subsequent utilization of space in a rocky intertidal
community. Ecol. Monogr. 41:351-389.
Heck, K. L., Jr. 1981. Value of vegetated habitrats and their roles as
nursery areas and shelter from predation. EPA Chesapeake Bay Program.
Final Report. Grant No. 806151.
Heck, K. L., Jr. and R. J. Orth. 1980a. Seagrass habitats: The role of
habitat complexity, competition and predation in structuring associated
fish and motile macroinvertebrate assemblages. Pp. 449-464. In: V. S.
Kennedy (ed.), Estuarine Perspectives. Academic Press, New York.
iieck, K. L., Jr. and R. J. Orth. 1980b. Structural components of eelgrass
(Zostfra mnrina) meadows in the lower Chesapeake Bay - Decapod Crustacea.
Estuaries"3:289-295. \
I
Heck, K. L., Jr. and T. A. Thoman. 1981. Experiments on predator-prey
interactions in vegetated aquatic habitats. J. exp. mar. Biol. Ecol.
53:125-134.
Kikuchi, T. and J. M. Peres. 1977. Consumer ecology of seagrass beds. Pp.
147-193. In: C. P. McRoy and C. Helfferich (eds.), Seagrass Ecosystems.
Marcel Dekker, Inc., New York.
93
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Nelson, W. G. 1979a. An analysis of structural pattern in an eelgrass
(Zostera marina) amphipod community. J. exp. mar. Biol. Ecol.
39:231-264.
Nelson, W. G. 1979b. Experimental studies of selective predation on
amphipods: Consequences for amphipod distribution and abundance. J. exp.
mar. Biol. Ecol. 38:225-245.
Orth, R. J. 1973. Benthic infauna of eelgrass (Zostera marina) beds.
Chesapeake Science 14:258-269.
Orth, R. J. 1975. The role of disturbance in an eelgrass (Zostera marina)
community. Ph.D. Dissertation. Univ. of Maryland, College Park.
115 pp.
Orth, R. J. 1977. The importance of sediment stability in seagrass
communities. Pp. 281-300. In: B. C. Coull (ed,), Ecology of Marine
Benthos. U. Scouth Carolina Press, Columbia.
Orth, R. J. and K. L. Heck, Jr. 1980. Structural components of eelgrass
(Zostera marina) meadows i the lower Chesapeake Bay-Fishes. Estuaries
3:278-288.
Orth, R. J. and K. A. Moore. 1982. The biology and propagation of Zostera
marina, eelgrass, in the Chesapeake Bay, Virginia. Final Report. U.S.
E.P.A, Chesapeake Bay Program. Grant No. R805953. SRAMSOE No. 265,
Virginia Institute of Marine Science, Gloucester Point. 187 pp.
Paine, R. T. 1966. Food web complexity and species diversity. Amer.
Natural. 100:65-75.
Stoner, A. W. 1980a. The role of seagrass biomass in the organization of
benthic macrofaunal assemblages. Bull. Mar. Sci. 30:537-551.
Stoner, A. W. 1980b. Abundance, reproductive seasonality and habitat
preferences of amphipod crustaceans in seagrass meadows of Apalachee Bay,
Florida. Cont. Mar. Sci. 23:63-77.
Stoner, A. W. 1980c. Perception and choice of substratum by epifaunal
amphipods associated with seagrasses. Mar. Ecol. 3:105-111.
Virnstein, R.. W. 1977. The importance of predation by crabs and fishes on
benthic infauna in Chesapeake Bay. Ecology 58:1199-1217.
Weinstein, M. P. and K. L. Heck, Jr. 1979. Ichthyofauna of seagrass meadows
along the Caribbean coast of Panama and in the Gulf of Mexico:
Competition, structure ~nd community ecology. Mar. Biol. 50:97-107.
94
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CHAPTER 4
SECONDARY PRODUCTION OF SOME DOMINANT MACROINVERTEBRATE SPECIES
INHABITING A BED OF SUBMERGED VEGETATION IN THE LOWER CHESAPEAKE CAY
by
Robert Diaz
and
Tom Fredette
95
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ABSTRACT
The production of the top 9 trophically important species to the higher
level consumers at the Vaucluse Shores grassbed was 40.7 g-nf^-yr"*. This is
a higher productivity than reported for most community production studies. If
this rate of production is projected over the entire 140 hectare grassbed a
total of 53 metric tons of dry tissue was produced and potentially available
for consumption by other trophic levels. This also represents 6 x 10^
individuals which are born, grow, and die in a year. The average standing
stock over the year was 4.6 metric tons leaving 48.4 metric i_ons to be
accounted for.
The isopod E_. attenuata accounted for 43% of the total production for the
9 species. The next two high ranking producers were C_. sapidus and (3.
mucronatus, when combined with E. attenuata accounted for 84.8% of biomass
produced by the 9 species. Turnover ratios were highest for G_. mucronatus
(24.5) and lowest for the snail B. varium (3.2).
96
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INTRODUCTION
In addition to the spatial heterogeneity provided by the presence of
bu merged aquatic vegetation the most notable feature of these habitats is the
high density of animals residing in the grass bed. This large standing crop
jf animals is thought to be fundamental to the resource value of submerged
aquatic vegetation beds to migratory predators (crabs, fish, waterfowl) that
utilize the beds for protection and as a feeding ground. However, one does
not get an appreciation for the flow of energy needed to support the large
populations of prey and predatory species by simply looking at the structural
complexity of the populations at any given time. The amount of energy or
biomass produced within the grass bed system can only be estimated by a
detailed look at the secondary production of the individual species in the
beds.
From our analysis of the feeding habits of the higher level consumers
(fish and crabs) it is obvious that benthic invertebrates play a major role in
the flux of energy through the seagrass system. The benthos then represent
the major link between primary production, detritus, and higher trophic
levels. Secondary production estimation is a very labor intensive process so
we chose to focus on nine top tophically important benthic species to higher
level consumers.
METHODS
Twelve consecutive monthly samples were taken for secondary production
using a suction dredge (Fig. 1). Quantitative samples were collected from
within a weighted plexiglass cylinder with a diameter of 28.6 cm (0.065 m^)
and a height of 65 cm. The cylinder was carefully placed over the grass
blades and the sample was taken from within by filtering water through a
plastic bag with a removable 0.5 mm uesh sieve bottom. Samples of larger,
more motile, or widely spaced species were collected from within a weighted
fiberglass cylinder 110 era in diameter (0.95 m ) and 30 cm high equipped with
a 0.5 mm mesh screened top (Fig. 1). All samples from the larger fiberglass
frame were filtered through a 1 mm x 1.5 mm mesh bag. The sampling frame was
dropped from a boat over dense vegetation. Only drops over 100% vegetation
cover were sampled. The majority of samples were taken from mixed
Zostera-Ruppia areas. All samples were preserved in 10% buffered formalin.
Samples were sorted in the laboratory and up to 200 complete individuals for
each species per sample date were measured, dried and weighed. Based on their
trophic importance to higher level consumers nine species were selected for
production estimates:
97
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98
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DECAPODS ISOPODS
Callinectes sapidus Erichponella attenuata
Crangon septemspinosa Edotea criloba
Palaemonetes vulgaris Idotea balthica
MOLLUSCS AMPHIPODS
Bittium varium Gammarus mucronatus
Gemma gemma
Length-weight equations calculated for each species were based on dry
weights (Table 1). Ash free dry weights (AFDW) were obtained by ashing known
quantities of each organism in a muffle furnace at 500°F for 3 hours.
Production for each species was determined with the size-frequency method
(Hamilton 1969, Waters and Hokenstrom 1980, Hynes 1980) Multiplied by the
factor 365/CPI, where CPI is the cohort production interval or maturation
period (Benke 1979). The instantaneous growth method (Waters 1977) was also
used to calculate production of Callinectes sapidus and Bittium varium, for
which cohorts were distinct.
Measurement data were partitioned into 6-12 size classes for each species
and densities converted to individuals/in^-. With these data and. length-weight
equations (Table 1), mean size and weight were determined for each month and
size class (Tables 2-10 and Fig. 2-4).
Species abundance data were analyzed graphically to determine population
trends and sample variation. Population size-frequency distributions of
replicate samples were tested with the non-parametric G-test (Sokal and Rholf
1969).
LIFE HISTORIES OF PRODUCTION SPECIES
Marine isopods are generally considered to be oraniverous, scavenging a
variety of plant and animal matter (Shultz 1969). Reproduction is by direct
development of young within the marsupium of the female. The three isopods
discussed here all occur within the grass bed as epifauna or epibenthos.
Edotea triloba, common in eelgrass, is also associated with mud substrates, i
It is distributed from Virginia to Maine. j£. triloba life spans seems to be;
about six months with peak recruitment from June to October. After spawning
in the spring and early summer larger individuals disappear from the
population (Fig. 2). Erichsonella attenuata has been reported from coral
habitats as well as eelgrass. Its range extends from Connecticut to /Jorth
Carolina (Shultz 1969). Ovigerous E_. attenuata were present in the grassbed
from May through January, peaking in July through September. Juvenile
recruitment occurred from June to March. Idotea balthica has an
amphi-Atlantic distribution occurring in the western Atlantic from the Gulf of
St. Lawrence to South America. Strong and Daborn (1979) indicate that life
span is slightly longer than one year in Canadian populations with juvenile
recruiLment in July. Ovigerous females were collected i.n the grassbed from
May to November with juvenile recruitment occurring throughout this period and
into December (Fig. 2).
99
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TABLE 1. LENGTH-WEIGHT REGRESSIONS WHERE W IS THE PREDICTED DRY WEIGHT OF
AN INDIVIDUAL WHOSE LENGTH MEASUREMENT IS L.
Species
Equation
Length
measurement
L
P. vulgaris
C^. septemspinosa
£. sapidus
J±- trilqba
E. attenuata
I. balthica
G. mucronatus
B. varium
G. gemma
w = 0.5880 1
2.53
w = 0.5999 1
2.41
w = 0.0643 1
2.74
w = 0.0070 1
2.87
w = 0.0066 1
2.41
w = 0.0137 1
2.17
w = 0.1272 1
3.00
w = 0.0372 1
1.78
w = 0.1039 1
1.56
43 0.92 carapace length
42 0.89 carapace length
71 0.96 carapace width
52 0.84 head to telscn
91 0.90 head to telson
42 0.94 head to telson
72 0.96 head plus 1st abdominal
3 segments
35 0.90 shell length
13 0.91 shell height
100
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40 80 120 160
LENGTH MEASURE (mm)
Fig. 2. Monthly size-frequency data for Edotea triloba, Idotea balthica
and Erichsonella attenuata.
110
-------
Gammarus mucronatus is a shallow water amphipod distributed froip the Gulf
of St. Lawrence to the Gulf of Mexico (Bousfield 1972). It is eurytopic and
can be found associated with algae, fouling communities, Spartina marshes (Van
Maren 1978, Borowsky 1980), and eelgrass (Marsh 1973). It has a generalized
diet consisting of both macro- and microphytes (Zimmerman et al. 1979).
Development of juveniles is diract and occurs within the marsupium of the
female. Ovigerous females were collected and juvenile recruitment occurred
throughout the year. From June to October greater than 10% of the total
population was ovigercus (range 11-232) with less than 10% of the population
ovigerous in all other months (range 3-8%). Based on laboratory study life
span is estimated to be approximately four months.
The filter feeding bivalve, Gemma gemma is generally found in well sorted
fine sand. It is distributed from Nova Scotia to Texas (Abbott 1974).
Maximum lifespan is approximately two years. Reproduction is ovoviviparous
(young are brooded). Sellmer (1967) determined the mean size of juvenile
length at release to be 410 u. New England and mid-Atlantic populations
release juveniles from June to August (Sellmer 1967, Green and Hobson 1970).
However, the growth rates for the two areas are quite different. One year old
individuals from New England were estimated to be 1.6 mm (Green and Hobson
1970) and 4.1 mm long along the mid-Atlantic coast (Sellmer 1967). Continuous
reproduction and rapid growth of G_. gemma at the Vaucluse Shores site clouded
cohort separation (Fig. 3). The actual growth rate or life span of (». gemma
would not be determined. The model size throughout the year was 1.25 to
1.75 mm with no individual ever being larger than 3.25 mm.
The prosobranch gastropod Bittium varium inhabits eelgrass beds from
Chesapeake Bay south to Florida. Texas, and the West Indies (Wulff 1970). It
is thought to be primarily a detritivore or algivore. Marsh (1976) observed
egg masses present on grass blades in May and June with recruitment beginning
in late June and lasting into the fall. Lifespan is approximately one year,
the newly recruited population overwintering close to the bases of Zostera
marina turions or within the sediment (Wulff 1970, Marsh 1976). Recruitment
was observed in the fall, from October to December (Fig. 3).
The grass shrimp Palaemonetes yulgaris is distributed in shallow coastal
and estuarine waters from Massachusetts to Texas (Williams 1965). Population
migration from Zostera marina beds to sandy-shell bottoms has been reported
(Thorp 1976). Palaemonetes vulgaris is an opportunistic omnivore often
consuming large quantities of detritus, digesting the associated bacteria,
fungi and protozoans (Adams and Angelovic 1970).
Knowlton and Williams (1970) reported ovigerous females occurring from
February to October in North Carolina populations with recruitment of
juveniles beginning in June. These new recruits grow quickly and may spawn in
the late summer. The Vaucluse Shore populations have a slightly less
extensive breeding season from June to September with recruitment occurring
from July to September (Fig. 4).
The decapod Crangon septemspinosa has a shallow water (0-35 m)
subarctic-boreal distribution. It occurs on the North American Atlantic Coast
from Baffin Bay to eastern Florida (Williams 1965). C_. septemspinosa is
111
-------
Fig. .3. Monthly si^e-frequency data for Gammarus mucronatus, Getama gemma
and jittium varium.
112
-------
I
P vulgartt
19 29 J9 49
C. tapidut
19 29 35 49 59 «9 79 69 99 109
LENGTH MEASURE Imm)
Fig. 4. Monthly size-frequency data for Palaemonetes vulgaris, Crangon
septemspinosa and Callinectes sapidus.
113
-------
eurytopic inhabiting a general salinity range of 10-31%. It undergoes
migrations to deeper water in response to low temperatures (Haefner 1979). C_.
septemspinosa is a nocturnal feeder with an opportunistic feeding strategy.
It can be a detritivore scavenger or predator. Predation on mysids accounts
for large portions of the diet for some populations (Welsh 1970).
Regionally, £. septemspinosa seems to have a single extended breeding
period from October to June with a March-April peak (Haefner 1979). Eggs are
brooded by the females for a short period after which development of
planktonic larvae occurs. Larvae are present in the plankton throughout the
year with a mid winter to early spring maximum. Lifespan has been estimated
at 2.5 years from studies of more northerly populations (Haefner 1979). In
the grassbed ovigerous females were observed only from March to June followed
by recruitment in June through August. Much of the winter population decline
may be due to migration to deeper channel areas (Fig. 4).
Callinectes sapidus is distributed in shallow coastal and estuarine
waters (0-35 m) from Nova Scotia south to northern Argentina (Williams 1974).
The species is euryhaline occurring in fresh water to hyperhaline lagoons.
Trophically, £. sapidus can best be described as an opportunistic omnivore.
Life span is up to 3.5 years. Recruitment of juveniles begins in August and
continues into the fall months. Mating occurs froji May to October with
spawning delayed two to nine months and occurring from May to September of the
following year (Van Engel 1958). Spawning activity is concentrated near the
mouths of estuarine and shallow coastal waters (Williams 1974). Recruitment
at the grassbed occurred in September and continued through November (Fig. 4).
RESULTS AND DISCUSSION
Abundance data were analyzed by determining median and semi-interquartile
range for replicate samples (Fig. 5). The distribution of most species was
typically patchy. Most of the species exhibited one major annual population
maximum. £. vulgaris, C^. septemspinosa, £. mucronatus and _I. balthica showed
the least month to month variability. The other 5 species fluctuated widely
from month to month. This type of variation is indicative of spatial
heterogeneity that may be related to patchiness of populations or migration.
Analysis of size-frequency distributions of replicate samples was done
for _E_. triloba and (5. mucronatus. These two species were chosen because it
was thought that microhabitat parameters could have greater influence on the
population structure of species with relatively short maturation times and
extended breeding periods. Significant differences existed in four of eight
months for E^. triloba and in two of seven months for (5. mucronatus (Table 11).
To further identify where variation in size frequency distributions was
occurring samples from pure stands of Zostera and Ruppia were eliminated
leaving only samples from the mixed grassbed habitat. Results indicated that
much of the variation in size'frequency distribution was related to vegetation
type. All months that were different when all habitats were combined were now
not different. However, there were still two months for each species where
the replicates from the mixed grassbed were different. These differences were
due mainly to variation in the number of smaller size class individuals
between replicates.
114
-------
-------
TABLE 11. RESULTS OF G-TEST COMPARISONS. *p^.0.05, *p<..01
All Replicates includes Zostera, Ruppia, and mixed grassbed samples
G. mucronatus
E. triloba
G. mucronatus
E. triloba
— — — —
Apr
May
Jun
Jul
Aug
Sep
*
**
*
*
n.s.
n.s.
n.s.
n.s.
n.s.
*
—
**
Oct
Nov
Dec
Jan
Feb
Mar
n.s.
n.s.
—
—
—
~~
^_
—
—
—
—
"•—•
Only mixed grassbed samples
G. mucronatus
E. triloba
G. mucronatus
E. triloba
Apr
May
Jun
Jul
Aug
Sep
N.S.
*
**
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
- Not significant
- pj<0.05
- n<0.m
n.s.
n.s.
n.s.
n.s.
**
n.s.
Oct
Nov
Dec
Jan
Feb
Mar
n.s.
n.s.
n.s.
*
**
n.s.
n.s.
**
n.s.
n.s.
n.s.
n.s.
- Only samples from mixed grassbed habitat were collected.
116
-------
Production estimates using the size-frequency method for the nine species
are based on combined data from all three habitats (Table 12). Secondary
production by E^. attenuata was found to be greatest, amounting to 43% of the
total production for the nine species. The next two high ranking producers,
C. sapidus and G. mucronatus, when combined with E. attenuata accounted for
84.8% of the biomass produced by these nine species. The contributions by j^.
attenuata and (5. mucronatus can be attributed to their relatively high
turnover rates (P/B), 18.9 and 24.5 respectively. While £. sapiuus P/B ratio
was low its standing stock was high (Table 12).
Since C_, sapidus could be traced as a single cohort production was also
estimated by the instantaneous growth method, which yields 15.8 g-.m~^-yr~^.
C. sapidus would then account for 33% of the production, as opposed to 22%
based on the size-frequency method, and the top three species would account
for 87%. The difference between these two estimates illustrates the
difference that can occur by the application of different methods. The
results for B. varium show that the instantaneous growth method (0.2
g-m~~^ •yr*) does not necessarily produce larger estimates than the
size-frequency method, as in this case there is close agreement. In the case
of C_. sapidus only production for a small portion of its life span was
calculated, which lead to the discrepancy in values.
Four species that were moderately abundant in the community but were not
used for secondary production estimates are the amphipods Aiapithoe longimana,
Cymadusa c ompta, Microprotopus raneyi and the gastropod Astyris lunata., For
these species and the nine production species wet weight bioraass was
determined from the routine baseline epifaunal and infaunal samples. Wet
weight biomass was converted to dry weight biomass using a conversion factor
of 0.17 (Waters 1977) (Table 13). It can be noted that for the secondary
production species there is at times disagreement between the mean dry weights
obtained from ire secjniary production data and that from the routine data.
This can probably be attributed to the patchiness of distributions and the
different amounts of information contained in each mean. Tha routine baseline
biomass data were next converted to production values by multiplying the P/B
ratios determined from this study. For the amphipods the P/B ratio of <3.
mucronatus was us'ed and for A^. lunata the ratio from JJ. varium (Table 10).
The total production based on routine sampling was 18 g-m~2.yr-l
estimated from the monthly samples excluding the decapods. The difference is
due to the quarterly sampling not being able to discern turnover shorter than
3 months. All the amphipods and isopods turnover at much shorter intervals,
on the order of weeks in the summer. Quarterly sampling does not accurately
estimate biomass and tends to yield conservative production values (compare
tables 12 and 13). For Z_. varium which has a lower turnover rate quarterly
samples do accurately estimate production. For (J. gemma mean biomass was
twice as high in the quarterly samples yielding twice the production of
monthly samples. G_. gemma was. simply much more abundant in the quarterly
samples. Its higher turnover rate (Table 12) and irruptive populations would
tend to indicate that both the quarterly and monthly samples underestimated
its population.
117
-------
TABLE 12. PRODUCTION ESTIMATES BASED ON THE SIZE FREQUENCY METHOD (HYNES
1980). P = PRODUCTION IN GRAMS DRY WT; AFDW P = PRODUCTION IN
ASH FREE DRY WEIGHT; P/B = TURNOVER RATIO; B = MEAN BIOMASS;
CPI = COHORT PRODUCTION INTERVAL.
P.
c.
c.
E.
E.
I.
G.
B.
G.
Species
vulgaris
septemspinosa
sapidus
triloba
attenuata
balthica
raucronatus
varium
gemma
P
g.m~?yr-l
1
0
8
2
17
1
8
0
0
.8
.5
.9
.0
.6
.0
.0
.2
.7
% Total
P
4.
1.
21.
4.
43.
2.
19.
0.
1.
4
2
9
9
2
4
7
5
7
AFDW P
g.m~2yr-l
1.
0.
5.
1.
14.
0.
6.
-
54
43
11
31
86
80
89
g
0
0
1
0
0
0
"0
.0
0
B
.m-2
.520
.119
.908
.175
.938
.116
.327
.062
.125
N
P/B
3.4
4.4
4.7
11.3
18.9
8.5
24.5
3.2
5.9
CPI
days
365
365
365
182
91
203
91
365
182
40.7 g.nT2yr
118
-------
TABLE 13. DRY WEIGHT BIOMASS DETERMINATIONS (G.M~2) FROM THE BASELINE
PORTION OF THE SAV STUDY. THE PRODUCTION WAS DETERMINED FROM
P/B RATIOS.
Species
E. triloba
I. balthica
E. attenuata
G. mucronatus
A. longimana
C. compta
M. raneyi
B. varium
A. lunata
G. gemma
4/79
0
0
0
0
0
0
0
0
0
0
.18
.02
.23
.37
.01
.01
.04
.09
.05
.15
6/79
0.14
0.05
0.28
0.15
0.00
0.03
0.04
0.15
0.13
0.51
9/79
0
0
0
0
0
0
0
0
0
0
.11
.08
.48
.05
.01
.12
.02
.02
.01
.26
11/79
0
0
0
0
0
0
0
0
0
0
.13
.12
.74
.05
.02
.13
.03
.03
.06
.16
Mean
0
0
0
0
0
0
0
0
0
0
.13
.07
.42
.15
.01
.05
.03
.07
.09
.26
Total
Production
1.
0.
7.
3.
0.
1.
0.
0.
0.
1.
18.
5
6
9
7
2
2
7
2
5
5
0
119
-------
— *? — 1
The nine species examined produced a total of 40.7 g dry wfm~'iyr-
which is a high production value. While there are no other grass bed studies
for comparison these nine species were found to be more productive then most
community production studies from both freshwater and marine systems (Waters
1979). To put this high rate of production into perspective we project the
40.7 g-~2.yr-l to the entire 140 hectare grass bed., making the basic
assumption that production of the nine species would be uniform over the
entire bed. A total of 53 metric tons of dry tissue was then produced and
potentially available for consumption by other trophic levels, which could be
either higher level consumers or lower level decomposers. This represents
approximately 60,000,000,000 individuals which are born, grow, and die in the
grass bed each year (Table 14). Our estimates are most likely conservative
since they represent only 9 of well over 75 trophically or numerically
dominant species in the grass bed system. Also our monthly sampling program
tended to underestimate production of those species (amphipods and isopods in
particular) which turned over in less than a month. Gammarus mucronatus, as
an example, in the lab grew to reproductive size in less than two weeks from
marsupial release at 17°C. In the field under more optimal growing conditions
growth may be even faster and turnover higher.
The importance of this high secondary productivity to fish and crab
predators is intuitive, but the portion of the production which goes to
predators is unknown. On average there are 4.6 metric tons of standing stock
over the year in the grass bed. This leaves 48.4 metric ^ns to be accounted
for.
120
-------
Table 14. PRODUCTION ESTIMATES PROJECTED FOR THE ENTIRE VAUCLUSE SHORES
GRASS BED (AREA = 140 HECTARES).
Biomass
Produced/Year
G.
G.
E.
I.
P.
C.
£•
B.
G.
mucronatus
triloba
attenuate
balthica
vulgaris
septemspinosa
sapldus
varium
gemma
11
2
24
1
2
0
12
0
0
.2
.8
.6
.4
.5
.74
.5
.28
.98
x 103 Kg
x 103
x 103
x 103
x 103
x 103
x 103
x 103
x 10 3
# of Individuals
Produced/Year
2
1
2
1
8
2
1
9
4
.0
.1
.7
.1
.1
.3
.5
.5
.5
xlO10
xlO10
xlO10
x 109
x 107
x 108
x 107
x 108
x 109
Total 53.0 x 103 Kg 6.1 x
121
-------
REFERENCES
Abbott, R. T. 1974. American Seashells. Van Nostrand Reinhold Co., N. Y.
663 p.
Adams, S. M. and J. W. Angelovic. 1970. Assimilation of detritus and its
associated bacteria by three species of estuarine animaJ". Ches. Sci.
11:249-254.
Benke, A. C. 1979. A modification of the Hynes method for estimating
secondary production with particular significance for raultivoltine
populations. Limnol. Oceanogr. 24:168-171.
Borowsky, B. 1980, Reproductive patterns of three intertidal salt-marsh
gammaridean amphipods. Mar. Biol. 55:327-334.
Bousfield, E. L. 1972. Shallow-Water Gammaridean Amphipoda of New England.
Vail-Ballou Press, Inc. 312 p.
Green, R. H. and K. D. Hobson. 1970. Spatial and temporal structure in a
temperate intsrtidal community, with special emphasis on Gemma gemma
(Pelecypoda: Mollusca). Ecology 51:999-1011.
Haefner, P. A. 1979. Comprehensive review of the biology of North American
caridean shrimps with empuasis on Crangon septemspionosa. Bull. Biol.
Soc. Wash. 3:1-40.
Hamilton, A. L. 1969. On estimating annual production. Limnol. Oceanogr.
14:771-782.
Hynes, H. B. N. 1980. A name change in the secondary production business.
Limnol. Oceanogr. 25:778.
Knowlton, R. E. and A. B. Williams. 1970. The life history of Palaemonetes
vulgaris (Say) and P. pugio Holthuis in coastal North Carolina. J.
Elisha Mitchell Scient. Soc. 86:185.
Marsh, G. A. 1973. The Zostera epifaunal community in the York River,
Virginia. Ches. Sci. 14:87-97.
Marsh, G. A. 1976. Ecology of the gastropod epifauna of eelgrass in a
Virginia estuary. Ches. Sci. 17:182-187.
Shults, G. A. 1969. How to Know the Marine Isopod Crustceans. Wm. C. Brown
Co., Dubuque, Iowa. 369 p.
122
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Selimer, G. P. 1967. functional morphology and ecological life history of
the gem clam, Gemma gemma (Eulamellibranchia: Veneridae). Malacologia
5:137-223.
Sokal, R. R. and F. J. Rohlf. 1969. Biometry. W. H. Freeman and Co., San
Francisco. 776 p.
Strong, K. W. and G. R. Daborn. 1979. Growth and energy utilisation of the
intertidal isopod Idotea baltica (Pallas) (Crustacea: Isopoda). J. exp.
mr. Biol. Ecol. 41:101-123^
Thorp, J. H. 1976. Interference competition as a mechanism of coexistence
between two sympatric species of the grass shrimp Palaemonetes (Decapoda:
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Van Engel, W. A. 1958. The blue crab and its fishery in Chesapeake Bay.
Part 1 - Reproduction, early development, growth and migration. Comm.
Fish. Rev. 20:6-17.
Van Maren, M. J. 1978. Distribution and ecology of Gatnmarus tigrinus Sexton.
1939 and some other amphipod Crustacea near Beaufort (North Carolina,
U.S.A.). Bijdragen Tot de Dierkunde 48:45-58.
Waters, T. F. 1977. Secondary production in inland waters. Adv. Ecol. Res.
10:91-164.
Waters, T. F. 1979. Influence of benthos life history upon the estimation of
secondary production. J. Fish. Res. Board Can. 36:1425-1430.
Waters, T. F. and J. C. Hokenstrom. 1980. Annual production and drift of the
stream amphipod Gammaras pseudolimnaeus in Valley Creek, Minnesota.
Liranol. Oceanogr. 25:7W-710.
Welsh, B. L. 1970. Some aspects of the. vertical migration and predatory
behavior of the sand shrimp, Crangon septemspinosa. M.S. Thesis, Univ.
of Maryland. 66 p.
Williams, A. B. 1965. Marine decapod crustaceans of the Carolinas. Fish.
Bull. 65:1-298.
Williams, A. B. 1974. The swimming crabs of the genus Callinectes (Decapoda:
Portunidae). Fish. Bull. 72:685-798.
Wulff, E. M. T. 1970. Taxonomy and distribution of westrn Atlantic Bittium
(Gastropoda: Mesogastropoda). M.S. Thesis, The College of William and
Mary, Va. 58 p.
Zimmerman, R., R. Gibson and J. Harrington. 1979. Herbivory and detritivory
among gammaridean amphipods from a Florida seagrass community. Mar.
Biol. 54:41-47.
123
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CHAPTER 5
PRELIMINARY STUDIES OF
GRAZING BY BITTIUM VARIUM ON EELGRASS PERIPHYTON1
by
Jacques van Montfrans
Robert J. Orth
and
Stephanie A. Vay
Accepted for publication in Aquatic Botany, Contribution No. 1036 from the
Virgini : Institute of Marine Science.
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ABSTRACT ]
The grazing activities of Bittium varium Pfeiffer on periphyton >
colonizing live eelgrass (Zostera marina L.) and artificial eelgrass ' \
(polypropylene ribbon) were investigated. Quantitative measurements of <;
grazing impact on artificial substrates were determined by periphyton pigment !.
extraction and dry weight differences between grazed and ungrazed blades. ,'
Significant differences occurred in phaeophytin and dry weight calculations
but chlorophyll _a measurements were not significantly different. This
suggests that senescent diatoms constituted the bulk of the periphyton weight :
and were selectively removed over more actively photosynthesizing diatoms. j i-'
; \
An examinacion of scanning electron micrographs further elucidated the . ;
impact of grazing by Bittium varium. Some micrographs revealed that B_. varium ;
removed primarily the upper layer of the periphyton crust on both artificial
substrates and living Zostera marina. The diatom Cocconeis scutellum Ehrenb. • '
which attaches firmly to living Z_. marina blades was less commonly removed
than Nitzschia or Amphora. Through its grazing activities, _B. varium may
maintain community dominance by tightly adhering diatoms such as C. scutellum.
Evidence of the complete removal of periphyton exposing the Z_. marina
epithelium, was revealed in other micrographs.
The grazing activities of Bittium varium which removes periphyton from
seagrass blades, could have important implications for the distribution and
abundance of Zostera marina in tho Chesapeake Bay.
125
I!
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INTRODUCTION
The term grazing is generally used in terrestrial and aquatic ecological
studies to indicate herbivory. Grazing food webs in terrestrial ecosystems
are more easily studied and have historically received greater attention than
those in the aquatic realm (Crisp, 1964). However, in recent years, an
emphasis has been placed on understanding buch relationships in both
freshwater and marine habitats.
Primary producers in aquatic systems include planktonic and benthic
microalgae (e.g. diatoms), macroscopic algae, and both submerged as well as
emergent macrophytes. The majority of energy fixed by the latter two groups
is generally not directly utilized by invertebrate herbivores and enters the
food chain via a detrital pathway (Teal, 1962; Harrison and Mann, 1975;
Tenore, 1975; Tenore et al., 1977). Phytoplankton and benthic raicroalgae
constitute the major sources of energy fixed by primary producers that is
available for direct transfer to higher trophic levels (Steele, 1974).
Many of the original investigations on aquatic grazing dealt with
microplanktonic crustaceans and their influence on phytoplankton populations
(Marshall and Orr, 1955; Porter, 1977). Similar studies on the effects of
benthic grazers have received more recent attention.
Grazing studies of benthic aquatic herbivores emphasize their impact on
both macro- and microscopic plant communities. Herbivorous fishes (Stephenson
and Searles, 1960; Randall, 1965; Earle, 1972; John and Pope, 1973), sea
urchins (Margalef and Rivero, 1958; Leighton et al., 1965; Jones and Kain,
1967; Paine and Vadas, 1969; Breen and Mann, 1976) and gastropod mollusks
(Randall, 1964; Southward, 1964; Kain and Svedsen, 1969; Dayton, 1971; Lein,
1980) have a dramatic effect on biomass and species composition of macroalgae
or marine vascular plants.
Herbivore-plant interactions involving microalgal communities are
somewhat less well studied (Nicotri, 1977). The nutritional importance of
benthic marine diatoms in the diet of the marsh snail, Ilyanassa obsoleta, has
only recently been established (Wetzel, 1977). Castenholz (1961) demonstrated
the drastic reduction in biomass of intertidal epilithic diatoms in the
presence of the grazing mollusks, Littorina scultata and Acmaea spp. A
similar result was demonstrated and selective removal of both the outermost
portion of the diatom mat and'the more loosely adhering species was shown to
occur when four intertidal gastropod species grazed on diatom colonized
artificial substrates (Nicotri, 1977).. In contrast, studies by Kitting (1980)
showed that-eve;', under high experimental grazer (Acmaea scutum, a gastropod)
densities, the principal algal species preyed upon did not detectably
decrease. Algal declines were instead attributed to physical factors.
126
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METHODS AND MATERIALS
Field Work
Both live Zostera marina and diatom colonized polypropylene ribbon which
resembled the living plants in size but was slightly paler in color were used
in the grazing experiments. Living blades, collected from a Guinea Marsh Z_.
marina bed at the mouth of tho York River on the southwestern shore of the
Chesapeake Bay, were held for not more than two days in large wooden
flow-through tanks before being used. The polypropylene strips were suspended
for 30 days from a pier at the mouth of the York River to condition the blades
before use. The artificial plants consisting of six 45 cm strips of ribbon
tied to a wire staple were then wiped clean and anchored to the sediment in
the Guinea Marsh seagrass bed to be colonized. Thirty days later the
artificial grass was collected for immediate use in grazing experiments and
scanning electron microscopy (SEM).
Bittium varium were collected from a Zostera marina bed at Vaucluse
Shores on the southeastern side of the Bay. Snails were acclimated for two
days in aquaria with York River water (23 °/oo salinity; 22°C) and live
periphyton covered Z_. marina prior to experimental use.
Laboratory Experiments
Periphyton-colonized artificial grass blades were used ro quantitatively
assess the effects of grazing. The blades that were used were initially
selected based on the extent of periphyton coverage. Twenty-six blades with
the densest growth were cut into 12 cm lengths. One end of each blade was
then wedged against the inside of a 1/2 dram glass vial using a cheesecloth
plug while the other end was tied to a piece of monofilament thread. Care was
taken to keep blades moist at all times and not to disrupt the periphyton
layer. The blades with vials were then suspended in two 40 liter aquaria
filled with millipore filtered seawater (23 °/oo salinity). Aquaria were
situated in a laboratory window with an eastern exposure and experiments were
conducted under ambient light conditions. Temperatures in the laboratory
fluctuated between 23° and 25°C. Each aquarium was equipped with a corner
charcoal filter housing an airstone. Thirteen blades were randomly designated
as experimental blades using a random numbers table and forty Bittium varium
(x length = 2.1 mm) were placed in the vials of each. Periodic counts of the
snails which crawled onto the blades were used as an Indication of grazing
pressure. When the experiment was terminated after 96 hours, the middle 8 cm
portion of each blade (3.2 cm^ total surface area per blade) was removed for
analysis. Twelve experimental and twelve control blades were used for pigment
analyses and gravimetric calculations of periphyton biomass while the
remaining two blades (one experimental and o:.e control) were prepared for SEM
examination. Results of the pigment extraction and cry weight calculations
were statistically analyzed using a Wilcoxin two-sample test (Sokal and Rohlf,
1969).
Chlorophyll a_ and chlorophyll degradation products (phaeopigments) were
extracted from each blade and analyzed by a phase partition technique (Whitney
and Darley, 1979). Three unused 8 cm long pieces of artificial grass were
128
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similarly tre-.'ted and the mean absorbance values used as correction factors
for solubles present in the polypropylene ribbon. Absorbance readings were
measured using a Bausch and Lomb Model 21 spectrophotometer. After pigment
extraction the periphyton adhering to each blade was removed by scraping with
forceps, dried to a constant weight, and weighed to the nearest 0.01 mg on a
Mettler balance (model H-51).
A scanning electron microscope (AMR-1000) was used to examine Bittium
varium fecal pellets, grazing trails, and food selectivity on periphyton
colonizing both living Zostera marina and artificial grass blades.
Micrographs were also used to assess the quality and composition of the
periphytic communities colonizing these substrates. When experiments were
terminated, blades and fecal pellets were immediately fixed in a 3%
gluteraldehyde, 0.1 M sodium cacodylate buffer (pH 7.2) and 0.25 M_ sucrose
solution. After two hours, samples were rinsed three times for up to 30 min
each in a 0.1 M_ buffer solution containing 0.25 M_, 0.1 M_ and 0.0 M_ sucrose
solutions, respectively. They were then fixed in a 1% osmium tetroxide and
0.1 M_ sodium cacodylate buffer (pH 7.2) for 2 to 24 hours, rinsed twice
thereafter in distilled water, and dehydrated in a graded series (25, 50, 75,
90, 95 and 100%) of ethanol solutions. After dehydration, samples were
critical point dried (Polaron Critical Point Drying System) with liquid CC>2,
mounted on stubs and coated with gold/palladium (40:60) in a high vacuum
evaporator. They were then examined and photographed under the SEM.
RESULTS
Periphyton pigment analyses of grazed and ungrazed artificial grass
blades (Table 1) showed no significant differences .(p>0.05) in chlorophyll a
concentrations whereas experimental blades exhibited significantly (p<0.001)
lower phaeophytin a_ concentrations than control blades. Mean chlorophyll &_
concentrations of 0.1882 and 0.1287 mg/1 for grazed and ungrazed blades,
respectively, were lower than the corresponding phaeophytin a values of 0.8607
and 1.8436 mg/1. Gravimetric differences of attached periphyton existed
between grazed and ungrazed blades (significant at p<0.001) indicating a mean
overall removal of 62.7% of the periphyton from artificial blade surfaces
(Table 2).
Scanning electron micrographs (plates 1 to 24) enhanced the understanding
of feeding activities by Bittium varium. Natural Zostera marina used in this
study was coated with a thick layer of periphyton which spanned the width of
the older blades (plate 1). At magnifications of 2200 and 4400X (plates 2 and
3) the complex nature of this crust is revealed. It consists of at least
three genera of diatoms (Cocconeis scutellum, Nitzschia sp., Amphora sp.),
blue-green algae, bacteria and organic debris, some of which might be
degrading fecal pellets. The crust i <= up to 15 pm thick with as many as 3-4
layers of diatoms (plate 4).
Bittium varium ingests the periphyton crust using a taenioglossate radula
consisting of seven teeth in each transverse row. The central tooth is
flanked on each side by one lateral and two similar slender marginal teeth
(plate 5). With the marginals laterally compressed, the radular band of an
adult j^. varium is approximatly 30 pm wide.
129
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TABLE 1. PERIPHYTON PIGMENT ANALYSIS OF GRAZED AND UNGRAZED ARTIFICIAL Z_.
MARINA BLADES. SIGNIFICANT DIFFERENCES WERE DETERMINED BY THE
WILCOXON TWO-SAMPLE RANK TEST^ (a= 0.05).
Functional Chlorophyll A
Grazed
Overall 1
Rank 3
8.5
8.5
8.5
12.5
16.5
16.5
16.5
21.5
23
24
n =
X =
s .d. =
Cy(b) =
jj(c) =
-0.2514
0.0000
0.0965
0.0965
0.0965
0.1609
0.1931
0.1931
0.1931
0.2574
0.2896
0.9332
12
0.1882
0.2738
145%
(mg/1/blade) Phaeophyutin a (mg/1/blade)
Ungrazed
3
3
5
6
8.5
11
12.5
16.5
16.5
16.5
20
21.5
82 ns
0.0000
0.0000
0.0322
0.0o44
0.0965
0.1287
0.1609
0.1931
0.1931
0.1931
0.2252
0.2574
12
0.1287
0.0889
69%
Grazed
Overall 1
Rank 2
3
4
5
6
7
8
10
11
16
24
0.0840
0.0988
0.1355
0.1583
0.4180
0.4402
0.8186
0.8756
1.1848
1.4026
1.7637
2.9488
12
0.8607
0.8609
100%
125
Ungrazed
9
12
13
14
15
17
18
19
20
21
22
23
***
1.1600
1.5014
1.6053
1.6127
1.6423
1.8254
1.9072
2.0333
2.0977
2.1025
2.1816
2.4539
12
1.8436
0.3560
19*
(a) ns = not significant at P = 0.05
*** = significant at P<0.001
(b) CV = coefficient of variation
(c) U = Mann-Whitney U test statistic
130
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Reproduced from
best available copy. %,s
Plate 1. Live Zostera marina showing complete coverage by the periphyton
crust (260X; size bar = 100 pm).
132
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Plate 2. Detail of plate 1 showing organic debris and at least three
species of diatoms including Cocconeis jscutellum, Amphora,sp.
and possibly Nitzschia sp. (2200X; size bar = 10 inn).
133
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Reproduced (rom
best available copy.
Plate 3. Part of a live Zostera.marina blade that was completely covered
with pcriphyton reveaTing the complex nature of the crust. The
periphyton community included blue-green algae, diatoms, bacteria
and organic debris, embedded in a mucous matrix (4AOOX; size bar =
10 urn).
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Reproduced from
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Plate 5. The radula of BiEtium varium showing its taenioglossate
configuration with one central tooth flanked by a lateral
and two marginal teeth on each side. Note that the central
teeth are badly worn in some cases. The width of the radula
is approximately 30pm with the marginal teeth laterally
compressed (2200X; size bar = 10 ym).
136
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Grazing by Bittium variant on periphyton of live Zostera marina results in
various effects (plates 6 to 8). Some feeding activities remove the upper
layer of periphyton crust, with little damage to the underlying diatoms
(plates 6 to 9). In most cases, grazed patches occur in which the total
periphyton matrix is removed, leaving only a few bacteria attached to the Z_.
marina epithelium (plates 10 to 12). Distinct grazing trails are evident in
other micrographs (plates 13 to 15). Individual straight-run trails vary in
width from approximately 19 to 29 urn (plates 13 and 14). Impressions of
Cocconeis scute Hum in the T^. marina epithelium indicate that this tightly
adhering species is sometimes removed by J3. variuu (plates 14 and 15).
However, examinations of fecal pellets (plate 16) reveal that pennate diatOu.s
such as Nitzschia and Amphora are commonly ingested, suggesting that these
species are less tightly adhered to the grass blades. Closer examination of
the diatom frustules observed in this fecal pellet revealed the absence of
protoplasm that fills the pores in live diatoms which is evidence that they
are digested as well (plates 17 and 18).
The periphyton assemblage found on polypropylene ribbon (plates 19 to 21)
is very different from that of living Zostera marina. A hair-like mat of
unidentified tubular material (possibly diatom sheaths and bacterial
filaments) and organic debris covers the entire blade. The virtually complete
removal of the hair-like mat after grazing (plate 22) revealed patches of
pennate diatoms that were evident under higher magnification (plates 23 and
24). The considerable reduction in periphyton biomass as a result of grazing
by Bittium variura, evidenced in the gravimetric data (Table 2), is readily
apparent in micrographs of grazed artificial blades.
DISCUSSION
Grazing on periphyton of marine macrophytes nay have important
implications for the productivity, distribution and abundance of the colonized
plants. Zostera marina has experienced widespread declines primarily on the
western shore and, to a lesser extent, the eastern boundary of the Chesapeake
Bay (Orth et al., 1979). Reasons for the observed declines are as yet unclear
but factors such as climatological changes, herbicides, increased turbidity
and increased nutrient loading have been hypothesized. Epiphytic growth has
been cited as the major causative factor in similar historical declines of
freshwater macrophytes of eutrophic lakes (Phillips et al., 1978; Moss, 1979).
The macrophyte host is adversely affected by epiphytes since the latter absorb
much of the light that normally reaches the plant surface and also act as a
barrier to carbon uptake (Sand-Jensen, 1977). Epiphytic fouling, if rapid and
severe enough, can eventually kill the host plant.
Two mechanisms to control colonization on marine plants by epiphytes have
evolved. Many plants produce mucous or periphyton inhibiting substances
(Cariello and Zanetti, 1979; Zapata and McMillan, 1979) while others, such as
Zostera marina, vegetatively generate c-lean, actively photosynthetic tissue at
a rapid rate while sloughing off fouled blades (Sand-Jensen, 1977). If
conditions such as nutrient enrichment (abiotic) and/or the reduction or
elimination of grazers (biotic) enhance periphytoa growth, the formation of
new photosynthetic tissue may be too slow for the continued health and
survival of the macrophyte. Thus, the micrograzer component of seagrass
137
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habitats may be essential in maintaining viability of the seagrasses,
especially under nutrient-rich conditions.
We utilized artificial substrates to quantify the impact of Bittium
varium grazing on periphyton. However, the use of inert substrates in
assessing the quantity and quality of periphyton found on natural macrophytes
is a subject of much debate. The importance of nutrient transfer and other
metabolic interactions between macrophytes and their epiphytic colonizers (see
Moss, 1981; Eminson and Moss, 1980 for review) has been recognized for
freshwater systems. External environmental factors determine periphyton
community composition in marine systems (see Harlin, 1980 for review).
However, a recent study (Eminson and Moss, 1980) demonstrated that greater
macrophyte host specificity by microalgae occurred in oligotrophic lakes than
in lakes with moderate to high nutrient loading. Under eutrophic conditions
host specificity was progressively less apparent and peiiphyton communities
became similar between all submerged vascular plant species, despite
differences in macrophyte surface texture and metabolic activity. It is
possible that the distinct differences we observed in periphyton species
composition between polypropylene ribbon and live eelgrass was caused by the
actively metabolizing, cobblestone textured leaves of the living plants.
We have demonstrated that grazing resulted in a significant reduction of
periphyton biomass on polypropylene ribbon. Since an analysis of
phaeopigments (and not chlorophyll a) showed differences paralleling the
gravimetric analyses, implications are that the periphytic crust utilized by
Bittium varium in these experiments was predominantly senescent. Scanning
electron micrographs of the artificial blades revealed that the epiphytic
complement differed considerably from that found on live Zostera marina.
Grazing impacts of _B_. varium on periphyton of both substrates, however, are
comparable. SEM photographic evidence of short term feeding activities
supports the fact that B. varium grazing reduces or removes the periphytic
community on natural blades.
Bittium varium grazing sometimes affects the structure of the diatom
population. This is accomplished by the mechanically selective removal of all
loosely adhering species such as Amphora sp. and Nitzschia sp. which inhabit
the upper portion of the periphyton crust. Cocconeis scutellum is able to
firmly attach to the Zostera marina epithelium by a mucilagenous secretion
thereby avoiding extensive grazing by J3. varium. Thus, the grazing activity
of J3. varium may facilitate community dominance by C^. scutellum, a species
which has been previously identified as the most ecologically and numerically
important diatom on Z_. marina (Sieburth and Thomas, 1973; Jacobs and Noten,
1980).
The shading imposed by epiphytes on their seagrass host can be severe
enough to either restrict their vertical distribution (Caine, 1980) or cause
the complete disappearance of the macrophytes (Sand-Jensen, 1977; Moss, 1981;
Eminson and Moss, 1980). The removal of most periphyton from artificial
blades by grazing and evidence of similar removal from live Zostera marina
suggests that Bittium varium plays an important role in mediating the
proliferation of epiphytic diatoms on these substrates. The disruption of the
periphyton grazer component (as is the case with the elimination of JK varium
157
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from seagrass habitats along the western shore of the Chesapeake Bay) could
seriously alter the steady state of periphyton abundance to the detriment of
the host plant. The preliminary results of our work indicate that a more
detailed and quantitative study of the macrophyte-periphyton-raicrograzer
relationship is necessary to substantiate this hypothesis as a partial
explanation for demise of Z_. marina in certain areas of the Bay.
158
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phytoplankton populations and periphyton populations in a shallow lake
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Orth, R. J. 1977. The effect of Hurricane Agnes on the benthic fauna of
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and detritivory among gammaridean amphipods from a Florida, USA, seagrass
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162
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CHAPTER 6
WATERFOWL UTILIZATION OF A SUBMERGED VEGETATION
CZOSTERA MARINA AND RUPPIA MARITIMA) BED
IN THE LOWER CHESAPEAKE BAY*
by
Elizabeth W. Wilkins
A thesis presented to the Faculty of the School of Marine Science,
The College of William and Mary, Williamsburg, Virginia
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ACKNOWLEDGMENTS
Special contributions of field assistance, moral support and
technical advice were made by Cary Peet, Deborah Penry, Tom Fredette,
and Anna Vascott. Brian Meehan, Linda Schaffner, Marcia Bowen, Karl
Nilsen and Priscilla Hinde offered vital assistance and companionship
during waterfowl censuses. Jacques van Montfrans was a supportive and
invaluable friend and consultant through all phases of the study.
Waterfowl specimens were collected by Vernon Leitch, Buck Wright
and Curtis Jones of Northampton County, and Louise and Bart Theberge
of the Virginia Institute of Marine Science. Rich DiGiulio, of
Virginia Polytechnic Institute, provided a number of specimens, as
well as valuable discussion and good company, while collecting in the
area for his own research.
Martha and Vernon Leitch, Vaucluse Pt. residents, deserve special
thanks for their warmth and hospitality during the bitter cold months.
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ABSTRACT
A study of waterfowl use of a bed of submerged aquatic vegetation
was conducted over two winters in the Lower Chesapeake Bay (Virginia).
In the season of 1978-1979, Canada geese (Branta canadensis) were the
dominant waterfowl in the study area. Goose foraging activity was
correlated with tide stage, and was greatest at low tide. Consumption
by grazing waterfowl was calculated from bird densities, and was
approximately 25% of the standing crop of vegetation in the shallow
portion of the habitat. In 1979-1980 diving ducks, primarily
buffleheads (Bucephala albeola), were dominant. Abundance of
waterfowl was influenced by wind parameters, but tide, temperature and
time of day hlad little or no influence on bird numbers.
Within-habitat variation in abundance was examined, and highest
densities were associated with the deeper Zostera marina zone.
Gizzard samples and 6*-*C analysis revealed that buffleheads fed
primarily on small gastropods and nereid worms characteristic of the
grassbed epifauna. Consumption of important invertebrate prey items,
calculated from exclosure experiments and waterfowl densities,
amounted to nearly 502 of the fall standing crop of these species in
Zostera marina.
165
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INTRODUCTION
Submerged aquatic vegetation (SAV) is widely recognized as a
valuable food resource for wintering waterfowl populations (Bent 1923,
Cottam 1939, Stewart 1962, Bellrose 1976, Munro and Perry 1981). The
demise of Zostera marina during the 1930"s was thought to cause the
precipitous decline of the Atlantic brant (Branta bernicla hrota)
(Cottam 1934, Addy and Aylward 1944, Cottam and Munro 1954), although \
coincidence of poor reproductive success may also have been important •
in reducing populations (Palmer 1976). Numbers of waterfowl utilizing ]
the traditionally important Susquehanna Flats as a winter feeding \
ground in the Chesapeake Bay plummeted during the height of the j
eurasian water milfoil epidemic in the 1960s, but returned to former S
levels after native aquatics became re-established (Bayley et al. ;
1978). j
|
Recent surveys indicate that submerged vegetation has declined in !
most areas of the Chesapeake Bay in the last 15 years (Bayley et al. '
1978, Anderson and Macoraber 1980, Orth and Moore 1981). The response .;
by several waterfowl species has been to alter feeding habits or 1
distribution patterns rather than sustain population losses (Munro and j
Perry 1981). Canvasbacks (Aythya valisineria) once fed primarily on j
wild celery (Vallisneria americana), but since the early 1970's have !
fed mostly on bivalves (primarily Macoma balthica; Perry and Uhler i
1976). Canada geese (Branta canadensis) and to a lesser extent 3
whistling swans (Cygnus columbianus columbianus), now rely on <
agricultural grain as a major dietary component on the wintering I
grounds (Bellrose 1976). Other species such as redheads (Aythya i
americana), wigeon (Anas americana) and pintails (An as a c u t a ), wh i c h j
indicate a continued preference for SAV, have declined in the Bay in j
recent years, and it is likely that their winter distribution now ;
coincides with areas of greater SAV abundance (Munro and Perry 1981). , j
\ '
Past or current preference for submerged vegetation in the diet ' >
is well documented for the above species (Martin and Uhler 1951, l j
Stewart 1962, Munro and Perry 1981). With the exception of j
canvasbacks and redheads, all are non-divers, or dabblers, which feed j
in shallow water by tipping up rather than diving to obtain food. :
Many diving species also feed in SAV habitats on benthic j
invertebrates. Animal communities associated with grassbeds differ i
markedly from those in unvegetated areas, both in structural and !
functional aspects. Submerged aquatic vegetation supports a dense and • •
diverse epifaunal assemblage not found on bare substrates (Marsh ,
1970), and organisms living on or within sediments are also more ,]
abundant due to greater sediment stability and microhabitat complexity }
(Thayer et al. 1975, Orth 1977). Grassbeds should therefore attract ;
waterfowl which feed on invertebrates as well as those which rely on i
vegetation, although there is scant evidence to this effect. Nilsson '
(1969) reported that in shallow water in the Oresund, Sweden, two ;
166
J
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diving duck species studied fed preferentially over Zostera marina and
one fed over patchy Ruppia sp. and 2^. marina, whereas an intervening
belt of vegetation-free sand contained no fauna of trophic importance
for these species.
In spite of the food resources available to waterfowl in SAV
habitats, Munro and Perry (1981) found few significant relationships
between the distribution and abundance of submerged vegetation and
waterfowl populations in the upper Chesapeake Bay. Several species,
such as whistling swans, black ducks (Anas rubripes), mallards (Anas
platyrhynchos) and buffleheads (Bucephala albeola), showed positive
associations with SAV in certain areas, but results were not
consistent over all survey zones. In the Lower Bay, tha current
relationship between waterfowl and SAV is largely unknown. The
purpose of this research was to provide detailed information regarding
waterfowl use of a particular bed of submerged vegetation in the Lowar ' s
Bay. Specific objectives were to examine short term patterns of
utilization, and to identify and estimate consumption of important
waterfowl foods within the study area.
Waterfowl foraging studies have traditionally emphasized gizzard
analysis, but more recent research has sought to quat.cify consumption
in addition to describing food habits. A common approach employs
average population estimates, theoretical daily ration based on body
weight, and knowledge of trophically important foods to arrive at
values for annual consumption. These values may then be compared with
either standing crop or production of food items to determine grazing
or predation pressure. In the saline Lake Grevelingen, The
Netherlands, Wolff et al. (1975) and Neinhuis and van lerland (1978)
reported that waterfowl consumed less than 1% of the annual production
of Zostera marina, whereas Jacobs et al. (1981) calculated that
consumption by waterfowl amounted to 50% of the standing crop of
Zostera noltii near Terschelling, The Netherlands. Intermediate
values for grazing pressure have been obtained by other investigators
using similar methods (Sincock 1962, Steiglitz 1966, Cornelius 1977).
Another technique compares biomass samples taken before arrival and
aft^r the departure of seasonally-resident birds (Ranwell and Downing
1959, Burton 1961). Values obtained in this way tend to overestimate
consumption during the non-growing season, as seasonal declines
related to physical factors are also included in these estimates
(Charman 1977).
Exclosure experiments have provided additional estimates of
consumption, using differences in biomass between grazed and ungrazed
(caged) plots to quantify waterfowl feeding. Verhoeven (1978) used
exclosures to estimate the impact of foraging by European coots
(Fulica atra) -and found a marked reduction in the biomass of Ruppia
cirrhosa outside exposures. Jupp and Spence (1977) protected plots
of Potamogeton spp. in Loch Leven, Scotland, and reported a similar
decline in plant biomass due to waterfowl grazing. Charman (1977) did
not estimate grazing pressure, but attributed early seasonal depletion
167
!J
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.-J
of Zostera to the foraging activities of brent geese based on the j
results of his previous exclosure experiments. ]
Similar information for non-grazing waterfowl is almost entirely
lacking. Nilsson (1969) calculated that diving ducks consumed less
than 102 of the standing crop of invertebrates in a Zostera and Ruppia
bed. Sincock (1962) estimated consumption by a number of non-grazing
waterfowl but did not relate these values to standing crop. The
diversity and patchy distribution of potential food organisms, and the
difficulties associated with gizzard analysis may account for the lack
of quantitative data.
A technique recently employed to characterize trophic
relationships in seagrass communities involves analysis of stable
carbon isotope ratios in tissues of herbivores or higher-level
1TO1O1O
consumers. Based on differential upcake of iJC by plants, 1JC: C
ratios (expressed in <$^C units) have been used to identify primary
sources and fluxes of organic carbon in grassbeds and other habitats.
Comparisons of animal 6 C values with known or estimated dietary
values indicate that isotope ratios are conserved through the food
chain (Haines 1976, Fry et al. 1978, Haines and Montague 1979), with
only slight variation due to effects of metabolic fractionation (De
Niro and Epstein 1978). Seagrasses exhibit 6 ^C values of -3 to
-13°/oo which are readily distinguished froni those of phytoplankton
(-18 to -24.5 °/oo), with benthic diatoms having intermediate values
(Fry and Parker 1979). Resolution of dietary components is thus
limited to fairly broad taxonomic or functional groups, but the
technique is much less tedious than examination of gut contents.
Application of 6 C analysis to waterfowl trophic studies has
thus far been limited, but suggests a similar strong relationship
between isotope ratios of bird tissue and dietary values. Patrick
Parker and James Winters (pers. comm.) have used 5^-^C values from
liver and other tissues to study redheads foraging in shoalgrass
(Halodule wrightii). Bird 6 ^C values exhibited a positive seasonal
shift of about 8 °/oo soon after arrival of birds from the breeding
grounds, indicating rapid carbon turnover in bird tissue associated
with the new winter diet. McConnaughey and McRoy (1979) reported a
similar seasonal shift in values for waterfowl species in the Izembek
Lagoon, Alaska. Although turnover may be very rapid, dietary
information is time-integrated in the short term, whereas gizzard
samples represent single foraging episodes.
Details of diet and reliable consumption estimates are needed to
assess the functional role of waterfowl in SAV habitats and to
evaluate the importance of this resource for wintering waterfowl. In
this study, several of the above methods wera combined, as it was felt
that an integrative approach. would provide more information than the
use of z cinglc technique, and would allow for comparison of results
obtained by different methods.
, !
f
168 ;
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METHODS
The Study Area
Vaucluse Shores is located on the Delmar/a Peninsula in the lower
Chesapeake Bay, just north of Hangar's Creek in Northampton County,
Virginia (37*25'N latitude, 75°39'W. longitude) (Figure 1). The site
consists of approximately 150 hectares vegetated subtidally by Ruppia
maritima and Zostera marina (hereafter Ruppia and Zostera) which
dominate beds of submerged vegetation in meso- and polyhaline regions
of the Bay. These opecies are distributed according to depth, with
Ruppia dominant in shallow water [less than 0.5 m at mean low water
(MLW)], Zostera dominant in deeper water (greater than 1.0 m) and a
mixed vegetation zone present at intermediate depths. Areal extent of
the grassbed is delimited bayward by a series of parallel offshore
sandbars oriented obliquely to the shoreline. Six transects (A-F)
were established in the study area in 1978 for use in mapping
vegetation at the site (Orth et al. 1979) and these provided
convenient boundaries for waterfowl censuses.
Biomass data for Zostera at Vaucluse Shores indicate a seasonal
maximum coinciding with seed production in June and July, averaging 85
g m~2 in 1978 (Orth et al. 1979). A second smaller peak in biomass
takes place in the fall, followed by winter values of less than 50 g
ra~ . Ruppia has a slightly different growth cycle, with one major
biomass peak occurring in August and September. Both species may
exhibit different patterns of growth at mixed vegetation sites (P. A.
Penhale, pers. coiam.).
Salinity at the site varies from 14 °/oo to 24 °/oo and water
temperatures range from -2C to 28C. In winter months, extreme lot*
temperatures may cause ice formation in the shallow areas.
The same site was the focus of a broad scale interdisciplinary
study (EPA-CBP contract #R80-59-74) designed to describe the principal
components of seagrass communities in the lower Chesapeake Bay, and to
elaborate important aspects of the functional ecology of these
systems. This integrated program included the following investigation
of waterfowl use of the habitat. !
Waterfowl Abundance Estimates \
1978-79: A preliminary census effort was undertaken in 1978-79
consisting of 13 census days between 6 December and 22 March, with a
variable number of censuses per day. Waterfowl observed between
previously established transectr. A through F were identified and
counted with the aid of a spr-tcing telescope and located oy transect
interval. The duration el each census was 15 minutes, and all birds
present during trhac time were counted. Feeding activity of Canada
geese was noted, and the relationship between percent feeding and tide
level was tested using the Spearman rank-correlation coefficient rs,
computed as
169
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- R2)2
where R is the variable rank, and n is the sample size (Sokal and
Rohlf 1981). Census times were used to obtain approximate tide level
data from NOAA tide prediction tables.
1979-80: All observations were made between transects B and C
(Figure 1) in 1979-80, allowing a more intense effort in a smaller
area (approximately 26.5 ha) which had been consistently utilized by
waterfowl the previous year. Waterfowl were censused at intervals
averaging 11 days from 8 November to 3 April and on each cencus date
birds were counted at approximately 2-hourly intervals during
daylight.
At the outset of the study, four zones were marked in the census
area from shore to the offshore sandbar which encloses the grass bed:
bare sand, patchy Ruppia maritime, mixed Ruppia and Zostera, and pure
Zostera marina. Although the zones are not highly discrete,
fluorescent stakes were placed at transitions along transects B and C
such that major vegetation type was indicated between pairs of stakes.
The position of each bird was recorded in reference Lo these stakes.
In order to express waterfowl numbers in terms of vegetation type,
areal extent of each zone was estimated from the results of
vegetational transect analysis reported by Wetzel et al. (1979) and
from personal observation of transition zones. Density of waterfowl
within these zones was then calculated, and differential utilization
was tested between each pair by the Wilcoxon nonparametric two-sample
rank test. The Wilcoxon statistic is calculated for samples of equal
size as follows:
- n
C = n2 + n(n + 1) - jR
where n is sample size and R is the variable rank. This statistic is
then compared with (n - C) and the greater of the two quantities is
the test statistic Us (Sokal and Rohlf 1981). The bare sand zone was
excluded from analyses, as waterfowl rarely utilized that area.
A tide gauge consisting of a stake graduated in 5 cm increments
was placed in subtidal shallow water and water level was recorded at
the time of each census. The stake was destroyed by ice floes and
replaced twice, but after 1 February tide data were obtained from NOAA
tables as in 1978-79. Time and air temperature were also recorded,
and wind speed and direction were obtained from the National Weather
Service station in Norfolk, Virginia. The above parameters were
related to waterfowl abundance using nonparametric correlation
statistics as described above. In th
-------
R = RUPPIA
Z = ZOSTERA
S SAND
M : MIXED
D: WATERFOWL EXCLOSURES
= TRANSECTS
Fig. 1. The Vaucluse Shores study area, showing previously established
transects A-F, and the location of waterfowl exclosures within
transect interval B-C.
171
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presence of a single large flock of redheads which would have obscured
major trends.
Food Habits
Waterfowl gizzards and livers were obtained from birds collected
by local hunters and scientific personnel in the study area and in the
mouth of Hungar's Creek between October 1979 and March 1980. Because
buffleheads were predominant in the second year of study, the diet of
this species was the focus of food habits studies. Bufflehead
gizzards were analyzed for food items, and livers of all species were
analyzed for stable carbon isotope ratios (6^C). Gizzards were kept
frozen before laboratory processing, and contents were then sieved
into two fractions for ease of examination. The coarse and fine
fractions were retained on 0.5 mm and 62y sieves, respectively.
Material which passed through the 62p sieve was negligible and
therefore was discarded. Both fractions were preserved in 10%
formalin. Contents of intact esophagi were examined, but were sieved
on 62y mesh only.
Identifiable species were enumerated under a dissecting
microscope and noted as present or absent in the case of fragmented
remains. Total contents of individual gizzards were not weighed, as
it was felt that differential digestion would bias these quantities to
a great extent. Instead, a representative sample of entire specimens
of each prey species was obtained and dried to constant weight.
Ash-free dry weights were estimated using conversion factors in
Cummins and Wuycheck (1971) and values provided by J. Lunz and D.
Weston (pers. comm.) for two mollusc species, as follows:
Peracarida 0.82 x Dry weight
Annelida 0.82
Decapoda 0.74
Mollusca 0.10 (For Bittium varium and Crepidula convexa)
These weights were multiplied by abundance per gizzard in order to
calculate percent composition by dry weight and ash-free dry weight.
The aggregate percent method was used to calculate mean composition,
where the proportion of a species in each gizzard is averaged over all
gizzards (Swanson et al. 1974). By this method, each gizzard has
equal importance despite differences in volume of contents. Dietary
importance was determined using the 'index of relative importance'
(IRI) (Pinkas et al. 1971):
IRI = (% N -f- % W) x % F
where N is numerical abundance, W is weight, (substituted here for
volume) and F is frequency of occurrence.
Bufflehead dietary electivity was calculated within mollusc prey
species only, as the numerical importance of softer-bodied forms may
not be as accurately reflected in gizzard samples. The Jacobs index
172
-------
(L) was used to measure electivity because the degree of departure
from zero (non-selectivity) can be statistically tested (Gabriel
1978). L is calculated as follows:
L = In (0) where 0
and pi - proportion of diet comprised by a given prey taxon
qj =• proportion of diet comprised by all other prey taxa
P2 = proportion of food complex in environment comprised by given
taxon
q2 = proportion of food complex in environment comprised by all
other taxa
Estimates of environmental abundance of prey items were obtained from
cores collected in January, and only gizzard samples which were
collected within two weeks of benthic sampling were used to obtain
dietary values.
Stable Carbon Isotope Analysis
Waterfowl livers were rinsed in distilled water, dried at 65°C
for 96 hr and ground in a Wiley Mill to a fine powder. These samples
were analyzed by Dr. Evelyn Haines at the University of Georgia Marine
Science Institute and Ors. Patrick Parker and James Winters of Coastal
Science Laboratories, Inc., at Port Aransas, Texas. Details of
further sample preparation and analyses by these labs are described in
Haines (1976) and Parker et al . (1972), respectively. In general
samples are first combusted to convert organic carbon into CC>2, which
is then isolated from other evolved gases. Isotopic analysis of C(>2
is carried out on a marfs spectrometer, and isotope ratios are reported
relative to a carbonate standard, in <$ ^C units (parts per mil):
/13C/12C sample \
— __ - _H X 103
WC/^C standard /
Tissues of important waterfowl foods (invertebrates from the
study area) were prepared and analyzed in the same manner, except
that in many cases specimens were pooled to obtain sufficient tissue
(=60 rag). For comparison with observed biifflehead 6* C values, an
expected value was calculated by multiplying the mean percent
contribution of each prey species to the diet (ash-free dry weight) by
its 6^- C value, and summing these values over all gizzards (Fry et al.
1978).
Waterfowl Exclosure Experiments
To investigate the impact of grazing waterfowl (primarily Canada
geese and redheads) on vegetation density at the study site, two areas
between transects B and C were chosen to locate exclosures: a shallow
mixed Ruppia and Zostera zone and a deeper pure Zostera zone (Figure
173
\ ' -
-------
1). Between 14 and 18 October 1979, two caged plots were established
in each of these zones at depths of approximately 0.5 m and 1.2 m at
MLW, respectively. Cage pairs included one cage (cage I) to be
sampled at two intervals during waterfowl residence and another (cage
II) to be sampled only if cage I was damaged.
Exclosures measured 2m x 2m x 0.5m and were constructed with 2.5
cm mesh vinyl-coated wire sides and crab pot wire tops (2.5 cm
hexagonal mesh), hinged on two sides to open from the center during
sampling. A frame consisting of a length of shaped concrete
reinforcing rod supported the top and penetrated the sediment to 50
cm. In addition, aim length of reinforcing rod was attached to each
corner and buried to 50 cm.
Benthic samples were taken with a 0.031 m^ plexiglass corer to a
depth of approximately 15 cm during three sampling periods: 18 October
1979, 16-19 January 1980, and 19 March 1980. On 18 October, six
replicate cores were taken in the vicinity of cages located in the
Zostera and mixed vegetation zones. Sample size was chosen based on
previous estimates of variability in plant biomass in the study area
(Orth et al. 1979). These samples were processed for vegetation only,
which was separated into above and below ground fractions, then dried
in an oven at 55°C for 48 hours and weighed.
During the second sampling period methodolgy was modified based
on the near-absence of Canada geese from the grassbed (see results).
As the dominant species was the bufflehead, which feeds primarily on
invertebrates (Stewart 1962), samples were processed for- animal
abundance as well as quantity of vegetation. Sample size was
increased to ten cores each from caged and uncaged sites to account
for greater patchiness of the invertebrate species.
Cores from uncaged areas were taken in a pattern radiating from
the center of the cage using random compass headings and distances
between 6 m and 12 m from the cage. Within exclosures, cores were
taken randomly from a 2m x 2m grid. Care was taken to position and
remove the corer with the least possible disturbance to adjacent
bottom. Samples were placed in muslin bags, refrigerated and washed
the following day on a 0.5 mm sieve. Cores collected in January were
frozen after sieving, but this resulted in damage to soft-bodied ,
invertebrates and thus samples collected in March were stored in 10% \
formalin. 1
In the lab, samples were rinsed and elutriated repeatedly to
separate vegetation from the animal and sediment component, which was
then sieved into two fractions. The coarse fraction (>2 mm) was
sorted and identified in its entirety, and the fine fraction
(<2 mm >0.5 mm) was distributed evenly on the sieve by flotation and
then split into quarters. Two quarters were chosen randomly for
sorting and the counts obtained were then doubled. Split counts were
compared to total counts for two samples. Total number of individuals
was 3.0% in erior for one comparison and 3.1% for the other. Error by
174
-------
species varied, with the rarest species most affected by the
technique. All organisms were identified to lowest taxa, with some
exceptions. In the January samples polychaetes, oligochaetes, and
nemertea were eliminated from analysis because damage from freezing
rendered numbers unreliable. Only two dominant epifaunal polychaetes,
Nereis succinea and Polydora lignjL, were identified to species in the
March samples.
Sediment cores were taken Lo determine effects of exclosures on
sedimentation processes. Three cores were taken from each treatment j
in January and five were taken from each treatment in March. Percent i
sand and silt-clay were determined by sieving and pipette anax/sis
outlined by Folk (1961). |
Differences between treatment means were tested using ti.e
Wilcoxon statistic, with the exception of sediment data, which were
arcsin transformed (Sokal and Rohlf 1981) and compared between
treatments using a standard t-test.
Estimates of Consumption from Waterfowl Density
Mean waterfowl abundances, theoretical daily intake, and days in
residence were used to estimate total consumption of biomass by birds
utilizing the study area. Methods for determining daily intake are
from Wolff et al. (1975) where standard metabolism M is multiplied by
5 to obtain consumption in kcal/day. M is determined by the formula:
Log M = Log 78.3 + 0.723 logW
where W is body weight in kg. Kcal were converted to grams ash-free
dry weight (AFDW) by multiplying by a factor of 0.2. These values
were then used in the following formula for consumption:
C = I-A-R
where I =* daily intake in grams AFDW
A = mean abundance
R = residence (estimated as 150 days)
Consumption was calculated over the total habitat as well zs more
restricted areas, based on patterns of utilization within the habitat.
Estimates were partitioned according to predominant feeding type
(animal vs vegetation) according to Stewart (1962) and Munro and Perry
(1981).
RESULTS
Waterfowl Abundance
1978-79: The Canada goose was the most important waterfowl
species in the study area in 1978-79, and averaged 526 individuals per
100 hectares (Table 1). The overwhelming dominance demonstrated by
175
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the species is obvious when plots of total waterfowl and Canada goose
abundance are compared (Figure 2). Second in importance was the
bufflehead, which averaged 46 birds per 100 ha and was the only
species present on every census date. Large flocks of redheads
utilized the study area, but occurred on only 5 of the 13 census days.
It is uncertain whether this species was adequately censused, as
foraging may have been primarily nocturnal. Redheads were most often
observed at dawn and dusk, and did not generally remain in the area
throughout the day.
Brant occurred on only two census dates, but one flock of
approximately 1300 birds inflated the relative importance of the
species. Whistling swans and wigeon were present regularly (in more
than 60% of censuses) but in low numbers. Red-breasted mergansers
(Mergus serrator) occurred less frequently but in flocks with an
average density of 19 birds per 100 ha. Although non-divers
(primarily Canada geese) were more abundant than diving ducks, both
groups were represented by nearly equal numbers of species throughout
the season.
Abundances of most species fluctuated without respect to
seasonality in 1978-79. However, Canada geese were most abundant in
the first few censuses, and this trend would probably have been more
pronounced had the earliest part of the season (November to early
December) been included.
Utilization of the study area by foraging Canada geese was
influenced by tide level (Figure 3). At the lowest water levels (2
hr. before and after low tide) the majority of geese present were
feeding, whereas geese almost never attempted to feed at higher tide
levels, and instead remained on the offshore sandbar. A negative rank
correlation between percent feeding and departure from low tide in
hours was significant at p < 0.001.
1979-80: Patterns of waterfowl abundance changed dramatically in
the second year of observations. Fewer species utilized the area
consistently (four per day average) and the proportion of non-diving
to diving species decreased to less than 0.2 per day (Figure 4).
Although large numbers of Canada geese were noted in the vicinity of
Hungar's Creek, no large flocks were censused within the study area
(Table 2). During a number of censuses, rafts of several hundred
geese were observed directly offshore at a distance of approximately
500 m beyond the sandbar (numbers in parentheses in Table 2), but they
did not come into the grassbed.
The bufflehead was the dominant species in 1979-80, and total
waterfowl numbers closely tracked the abundance of this diving duck
(Figure 5). Again, they occurred on every census date, and mean
density of this species (96 birds per 100 ha) was approximately twice
as great as in 1978-79. Redheads were also important though
infrequent the second year, primarily due to a flock of approximately
500 birds which fed in shallow Ruppia on 6 March. In contrast to the
177
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i
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/\ Totol Waterfowl Abundance
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DECEMBER JANUARY FEBRUARY MARCH
Fig. 2. Abundances of total waterfowl and Canada geese at Vaucluse Shores,
1978-1979. Points represent means and bars are standard errors of
the mean.
178
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Fig. 3. Relationship between tide stage and foraging activity in Canada
geese at Vaucluse Shores,- 1978.-1979. Curve fit by eye.
179
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^' '.] DIVERS V///\> NON-DIVERS
% SPECIES
50%-
NOVEMBER DECEMBER JANUARY FEBRUARY MARCH APRIL
% INDIVIDUALS
50%- 1978- 1979
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NOVEMBER ' DECEMBER JANUARY FEBRUARY MARCH
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NOVEMBER DECEMBER JANUARY FEBRUARY MARCH APRIL
% INDIVIDUALS
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1979-
1980
NOVEMBER DECEMBER JANUARY FEBRUARY MARCH APRIL
Fig. 4. Numbers of diving vs. non-diving waterfowl, as a percentage of
total waterfowl during 1978-1979, compared to 1979-1980.
180
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previous year, scaup (Aythya spp.) were important and were present in
greatest numbers (45-60 per 100 ha) in February and early March.
In 1979-80 waterfowl abundance was independent of tide level,
except in the shallow Ruppia zone, where numbers oZ birdi. were
generally low but increased with higher tide levels (Figure 6). Rank
correlation coefficients for the mixed and Zostera zones and the total
study area were not significantly different from zero (Table 3).
Temperatures ranged from -6C to 22C but did not influence
waterfowl abundance in the study area. Winds were predominately NNW,
but direction had some effect on waterfowl numbers.- A positive
correlation was found between abundance and direction (from 10-360°),
and higher numbers were associated with winds from the NNW (p < 0.05).
Wind speed alone did not have a significant effect, but when wind
direction was held constant, wind speed had a positive influence on
bird numbers in the case of NNW winds (p < 0.05). When wind speed was
held constant (in 5 knot increments) direction had a positive effect
only at 21-25k (p < 0.05). No correlation was found between waterfowl
abundance and time of day during daylight hours.
Within the grassbed, vegetation zone had a pronounced effect on
waterfowl use (Figure 7). Mean densities of birds within these zones
indicated an increasing inshore to offshore trend, with ^axiirura
densities in the Zostera zone. Numbers of birds were very low in bare
sand and Ruppia, rarely exceeding one individual per hectare.
Multiple comparisons indicated that these differences were highly
significant ror each pair considered (Table 4).
Again, few seasonal trends were evident in waterfowl abundance.
A gradual increase in total numbers from January through March 1980
reflects primarily the occurrence of greater numbers of scaup and
redheads, while bufflehead numbers fluctuated around the overall mean
wich no sustained increases or decreases.
Food Habits: Gizzard Analysis
Gizzards from 32 buffleheadc were examined. Due to the
difficulties of collecting waterfowl during active feeding, most
gullets and a number of gizzards contained very little or no food. Of
25 esophagi collected, 22 were empty. Therefore, results are
presented for gizzards only, two of which were completely empty and \
were also omitted from analysis. All other gizzards were analyzed
regardless of fullness, in order to obtain an adequate sample size.
A total of 27 taxa were identified in bufflehead gizzards,
including 23 invertebrate species, three plant species and fish
vertebrae (Table 5). Molluscs and peracaridan crustaceans accounted
for 18 of the 23 invertebrate species and the remainder included
polychaetes, decapods, br-ozoans and barnacles. Plant material in the
183
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Fig. 6. Relationships between numbers of waterfowl and tide levels in three
vegetation zones, 1979-1980. Numbers in parentheses refer to a
single flock of redheads which were not included in analyses.
"cans are indicated by the height of blocks, and points are
individual observations.
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185
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ID-
S'
6-
4-
2-
UJ
£ 0^
Zostero
4,
o
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x 6-
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£ 4-
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Q 21
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Zostera
1
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A A I
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Bare Sand
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A .*. __
NOVEMBER 1 DECEMBER
1979
JANUARY
FEBRUARY | MARCH
1980
APRIL
Fig. 7. Within-habitat variation in waterfowl density at Vaucluse
Shores, 1979-1980. Means and standard errors are indicated.
186
-------
TABLE 4. EFFECT OF VEGETATION ZONE ON WATERFOWL DENSITY IN THE STJDY
AREA. COMPARISONS TESTED BY THE WILCOXON STATISTIC UK.
Mixed Zostera Ug
Mean density
(Birds/ha)
± Std. Error
N=76
0.43
±0.110
1.71
+0.263
~—
4.92
±0.697
Mean Ranks R/M
M/Z
Z/R
60.62
55.72
92.38
66.30
86.70
97.28
7021.0***
5038.5**
7393.5***
** p < 0.01
187
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diet consisted primarily of Ruppia maritima and Zostera marina, with \
corn (Zea mays) present in a single gizzard.
Crepidula convexa was the dominant ~e- y item by numerical ]
abundance and dry weight, with a mean abundance of 49 individuals and i;
mean dry weight of 43 mg per gizzard. In terms of ash-free dry '•
weight, C^. convexa was less important than the polychaete, Nereis i
succinea, which averaged 30% of gizzard contents by ash-free weight. j'
However, abundance of _N. succinea was relatively low (nine individuals j
per gizzard). Only chitinous jaws and setae of this polychaete were :
evident in gizzards due to rapid digestion of softer tissue, but j,
numbers of individuals (and thus reconstructed weights) were obtained i
by counting pairs of jaws. [
By taxonomic group, gastropods dominated gizzard contents (Figure |
8). Of the five most important prey species by the index of relative t
importance (IRI) four were gastropods: Crepidula convexa,
Pyramidellidae sp., Bittium varium and Astyris lunata. These four r
species accounted for nearly 60% of gut contents by dry weight (36% by [
AFDW) and 64% by abundance, and occurred with an average frequency of !
70%. i
\
Polychaetes were represented in gizzards only by Nereis succinea, j
although the contribution to the diet by this group may be j
underestimated. Bivalves (primarily Anadara transversa) and isopods t
(dominated by Erichsonella attenuata) were of roughly equal importance ;
averaging from 5-12% of gizzard contents by dry and ash-free dry |
weight. Mysids (Neomysis americana) were abundant in several samples,
but dry weight contribution was minor. Identifiable amphipods and ,
decapods were encountered rarely and in low numbers. !
j
The barnacle Balanus improvisus was a consistent prey species, 1
with shell fragments found in 25 gizzards. Exoskeletal fragments of j
bryozoans were also found frequently (70% occurrence). Because }
numbers could not be determined for either of these groups, dietary
importance was not assigned. Importance was not determined for plant
material as no quantitative measure of percent composition was made.
However, it appeared by visual estimate that vegetation was a minor
dietary component, taken with invertebrate prey items found among
vegetation.
Results of electivity calculations among mollusc prey species
indicate that buffleheads may be at least partially selective (Table
6). Crepidula convexa was eaten in proportionally low numbers
relative tu its abundance in the grassbed, resulting in a
significantly negative L value (p < 0.001) although it was still the
dominant prey item. The gastropods Bittium varium, Pyramidellidae
spp., Astyris lunata, and the bivalves Gemma gemma and Anadara
transversa are apparently preferred (i.e. had significantly positive L
values), Tmt are found in much lower abundances in the environment
than is C. convexa. The gastropods Triphora nigrocincta, Acteon
189
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punctostriatus and Acteocina canaliculata contributed to the diet in
close proportion to their environmental abundances.
Food Habits: Stable Carbon Isotope Ratios
Bufflehead livers were fairly consistent in carbon isotope
composition, with an average 613C of -17.2 _+ 0.81 °/oo (Table 7).
fil-^C values were obtained directly for 11 prey species (van Montfrans
1981) and were estimated by taxonoraic group or feeding category for
the remaining species (Table 8). In general, values were slightly
less negative than bufflehead liver tissue and varied widely among
taxa. The polychaete Nereis succinea (-13.3 °/oo), the gastropod
Bittium varium (-13.4 °/oo) and the isopod Erichsonella attenuate
(-13.4 °/oo) had the highest fi^C values, while the gastropods
Crepidula convexa (-20.2 °/oo), Astyris lunata (-16.4 °/oo) and the
amphipod Cymadusa compta (-16.8 °/oo) were less 6l3c-enri.ched. The
suspension feeding bivalves Anadara transversa and Gemma gemma were
assigned a value of -17.5 °/oo based on measured ^C: "C ratios for
the clams Mya arenaria and Mercenaria mercenaria. Values for other
prey species ranged from -14.0 to -15.9 °/oo.
From these values for prey items and the percent contribution of
each species (by ash-free dry weight) to the diet, the resulting value
for bufflehead tissue should approximate -15.4 °/oo, if all prey items
are accounted for in correct porportions. Although this assumption
was not strictly met, the observed mean was within 1.8 °/oo of the
predicted value.
6 C values for other waterfowl species were also lower than most
potential prey species (Table 9). With the exception of a single
wigeon liver (-12.7 °/oo), values were even further removed from those
obtained for submerged vegetation. Ruppia and Zostera ranged in 6 C
values from -7.5 to -10.6 °/oo, and the value for associated
periphyton was -11.2 °/oo.
Waterfowl Exclosures
By 23 January, the inshore exclosures had been removed by ice,
and results are presented for cages in pure Zostera only. Cage I in
Zostera was sampled in January but not in March, as the top had been
forced open for an unknown length of time. Instead, Cage II was
sampled, and therefore the results from the two dates are not strictly
comparable.
Samples from both cages (i.e. both sample dates) yielded
significantly greater numbers of individuals and species than samples
from uncaged areas (Table 10). Species abundances were significantly
greater inside cages in approximately half of the comparisons (p<0.05)
(Figures 9 and 10). Eight species were found in significantly higher
numbers in both sets of caged samples; the gastropods Doridella
obscura, Crepidula convexa, Astyris lunata, and Bittium varium, a
bivalve Anadara transversa, the isopods Erichsonella attenuata and
192
-------
TABLE 7. CARBON ISOTOPE COMPOSITION OF BUFFLFHEADS
COLLECTED NEAR VAUCLUSE SHORES, 1979-1980.
613c Values
Bufflehead
Livers
°/oo
-15.8
-17.1
-16.4
-18.0
-17.2
-17.4
-18.0
-18.0
-17.8
-15.5
-16.8
-17.8
-17.0
-17.3
-16.5
-17.5
-18.4
-17.7
-17.6
-17.9
-16.4
-16.7
-17.0
-18.3
-15.3
-18.1
-15.3
-18.1
-18.5
-16.9
-18.0
- ' -16.5
-17.3
-16.8
X = -17.2 o/oo
S.D. ± 0.81
Date
Collected
12/18/79
12/18/79
12/18/79
12/18/79
12/18/79
12/19/79
12/19/79
12/19/79
12/19/79
12/24/79
12/26/79
01/02/80
01/14/80
01/14/80
01/15/80
01/16/80
01/16/80
01/16/80
01/16/80
01/16/80
01/23/80
01/23/80
01/23/80
01/23/80
01/23/80
01/23/80
01/23/80
01/23/80
01/23/80
01/23/80
02/22/80
02/22/80
02/22/80
02/23/80
I
i 1
!J
193
-------
TABLE 8. ISOTOPIC COMPOSITION OF BUFFLEHEAD INVERTEBRATE PREY
SPECIES.
PREY SPECIES
Crepidula convexa
Nereis succinea
Pyrainidellidae sp.
Bittium varium
Astyris lunata
Erichsonella attenuata
Anaoara transversa
Cra igon septemspinosa
Neoniysis americana
Nassarius vibex
Triphora nigrocincta
Edotea triloba
Gemma gemma
Acteocina canaliculata
Gamrcarus mucronatus
Idotea balthica
Cymadusa compta
Epitonium rupicola
Acteon punctoscriatus
Xanthidae sp.
Paracerceis caudata
,13C
&/00
-20.2
-13.3
-14. 5a
-13.4
-16.4
-13.4
-17. 5b
-14.2
-17. 5b
-14.2
-14. 7C
-15.5
-17.5b
-14. 7C
-15,9
-14.0
-16.8
-14. 7C
-14. 7C
-14. 5a
-14.3d
PROPORTION
OF DIET
BY AFDW
0.164
0.296
0.060
0.041
O.C90
0.098
0.061
0.050
0.029
0.040
0.007
0.009
0.008
0.008
0.006
0.017
0.004
0.002
0.001
0.004
0.002
CONTRIBUTION
TO TOTAL
6l3C
-3.31
-3.94
-0.88
-0.55
-1.48
-1.31
-1.07
-0.71
-0.51
-0.57
-0.10
-0.14
-0.14
-0.12
-0.10
-0.24
-0.07
-0.03
-0.001
-0.06
-0.03
Total = Expected 13g = -15.35 °/oo
aMean value for:
b « .
c » .
d 11
predator/omnivores
suspension feeders
gastropods
isopods
194
-------
TABLE 9. CARBON ISOTOPE COMPOSITION OF WATERFOWL OTHER
THAN BUFFLEHEADS COLLECTED NEAR VAUCLUSE SHORES,
1979-1980.
Species
Canada goose
American wigeon
Black duck
Pintail
Lesser scaup
Greater scaup
Oldsquaw
Surf scoter
Red-breasted merganser
613c Values °/oo
(Livers)
-19.6
-21.6
-19.6
-19.1
-17.6
-16.2
-16.3
-15.0
-16.2
-12.7
-18.8
-17.8
-16.9
-18.9
-19.1
-16.5
-17.7
-17.1
-18.3
-20.8
Date
Collected
12/31/79
01/05/80
01/11/80
12/17/80
12/17/79
12/17/79
01/01/80
03/14/80
03/14/80
03/14/80
01/01/80
01/02/80
01/11/80
01/23/80
12/31/79
01/16/80
01/23/80
01/01/80
01/01/80
02/23/80
195
-------
TABLE 10. NUMBER OF SEPCIES AND INDIVIDUALS FROM
CORES TAKEN IK CAGED AND INCAGED
ZOSTERA IN JANUARY AND MARCH 1980.
DIFFERENCES WERE
STATISTIC Us.
O
TESTED BY THE WILCOXON
January
N=10
March
N=10
No. Species
Caged Uncaged
33 29
34 29
30 29
31 ?.9
32 29
31 28
29 26
33 25
29 26
29 25
X 31.1 27.5
S 1.85 1.78
Us 92.5***
45 41
38 35
34 32
38 34
39 31
33 29
41 29
31 29
43 33
42 32
X 38.4 32.5
S 4.58 3.66
Us 84 . 0**
No; Individuals
Caged Uncaged
1257 854
1615 937
1264 1000
978 1335
1343 1027
1002 941
1360 930
1153 694
1089 620
997 740
1025.8 907.8
202.62 202.00
88.0**
1179 1161
1504 1202
1987 1522
2154 1559
2015 1741
2013 1681
2098 1444
2316 1259
2218 1079
2607 1556
2069.1 1420.4
297.55 230.16
95.0***
** p <
*** p <
0.01
0.001
196
-------
MEAN RANK SCORE
Acteocma canofrculota +
Acleon puncfostr/atus +
Astyns lunjfa +
Crepidvlo con veto -f
Tlyonosso obsoteta -f
Pyrom.delhda* spp +
Tftphoro nigrocmcta +
Dortdella ebscura —
x3 /7 p >OOI
** 001 > p > 0001
*K* p
-------
MEAN RANK SCORE
15
Nemerleo sp —
Acfeocma cano/'Cutafa +
Acteot punctostriotus -*•
Astyns lunota +
Crtptdulo COnvexa +
Biffium vQrtum +
Hyonossa obsolete — #*|
Pyramideliidae spp +
TttphorQ ntgroctnctQ +
Do ride ila obsc wo ~~
Anodofo tronivcrsa +
Gemma gemma +
Lyonsio ftyglino -
Mytihdoe sp —
Poiychoeio spp +
Polydo ra iignt ~
Nereis sue c me a +
Oi-gochoefa spp —
Osiracodo spp —
Bo/anus- impfOviSuS -+•
Cydaspis if ortats —
LeptQcfieim rapa* —
Idotey botlhtca +
Cymodasa compto +
flasmopvs taevts —
GamrrtQrus muc'Ofiotvs +
Me/i to ritttcta -f-
Microp 'otopus raneyi —
Cap re HQ p e nanti $ —
Porocapreifo fenuis —
NO CAGE
(0
CAGE H
10
I **
• * **
• ***«•
| **•
*
HBHH Higher score, significant
r.Tm Not significantly different
— Abser.t from gut sompfes
* 005 > p) 0 0(
** 001 >p>000>
***** P< °°°l
Fig. 10. Rank scores for species abundances in caged vs. uncaged samples
taken in March 1980, as designated by the Wilcoxon 2-sample test.
Expected score under Ho (that treatment means are equal) = 10.5.
Significance level of the U statistic is indicated.
198
-------
Edotea triloba, and an amphipod Paracaprella tenuis. With the
exception of P_. tenuis and D^. obscura, all of these species were found
in bufflehead gizzard samples, and most were important components of
the diet. Other species with significantly higher abundances inside
cages which were not present in gizzard or gullet samples included a
number of peracarid crustaceans and juvenile blue mussels (Mytilus
edulis). Only one species, the gastropod Ilyanassa obsoleta, was
found in significantly higher numbers outside cages.
For most bufflehead prey species, the magnitude of the observed
differences between treatments did not increase with the duration of
the experiment, as indicated by a Wilcoxon test comparing these trends
between January and March samples (Table 11). However, abundances of
five prey species were significantly greater inside cages in March but
not in January, and the reverse was true for two prey species.
Determinations of plant biomass indicated that the cage structure
may have had a negative impact on plant survival and/or growth (Table
12). Orth et al. (1979) reported lower biomass values for Zostera in
winter months, and a similar decline was observed from October to
January in uncaged cores. However, biomass of vegetation inside cages
was reduced to a greater degree, and the difference was significant
(p<0.001) in March. Cages were observed to be badly fouled with
macroalgae and hydrozoans at that time.
Differences in percent sand and silt-clay were not apparent
between treatments in January or March (Table 13). Sediments were
fine sands, with less than 15% silt-cl?y.
Consumption Rates
Total consumption estimated from waterfowl density in 1978-79 and
1979-80 amounted to 11.67 and 1.70 g AFDW nT? respectively, over the
entire area censused (Tables 14 and 15). In 1978-79 vegetation i*as
the predominant waterfowl food, according to the general food
preferences of abundant species. Foraging Canada geese removed
approximately 8.26 g AFDW m~2, or 74% of the total for vegetation.
Brant, redheads, and whistling swans consumed 2.72 g, while the
remaining grazers ate an estimated 0.18 g AFDW m~2. If only the
vegetated shallows are considered (approximately half the total area)
the adjusted estimate for consumption of vegetation becomes 21.44 g '
m~2. Of the total for animal material consumed by waterfowl in 1979;
buffleheads and red-breasted mergansers consumed 92%, or 0.28 and 0.21
g AFDW m~2, respectively.
In 1979-80, plant and animal foods were consumed in roughly equal
proportions, although total consumption was an order of magnitude
lower than in the previous year, reflecting primarily the absence of
Canada geese. Redheads were the only important grazing species,
removing 0.76 of the 0.88 g AFDW m~^ vegetation consumed over the
entire area. Buffleheads and scaup were the only other abundant
waterfowl, and together consumed 0.76 g of animal material per m .
199
-------
"1
TABLE 11. ABUNDANCES OF PREY SPECIES WHICH SHOWED SIGNIFICANT
DIFFERENCES BETWEEN TREATMENTS IN JANUARY OR MARCH 1980
(INDICATED BY *). Ug COMPARES THE MAGNITUDE OF THESE
DIFFERENCES OVER ALL SPECIES ACROSS SAMPLE DATES.
MEANS AND STANDARD ERRORS OF THE MEAN.
VALUES ARE
JANUARY
NO CAGE CAGE
Crepidula convexa
Pyranidellidae
Bittium varium
Astyris lunata
Erichsonella attenuata
Anadara transverse
Edotea triloba
Acteocina canaliculate
Gammarus mucronatus
Idotea balthica
Acteon punctostriatus
Balanus improvisus
Paracerceis caudata
22690
±1937.7
200
±81.0
255
±47.9
92
±21.5
370
±31.9
169
±33.9
427
±99.3
57
±27.6
866
±266.8
373
±30.0
70
±19.5
99
±28.3
204
±19.1
28254*
±1643.7
825*
±254.1
519**
±70.6
631***
±166.7
796**
t!74.1
306**
±30.5
936**
±113.7
121 n.s.
±51.5
573 n.s.
±70.3
675**
±82.6
102 n.s.
±22.2
213 n.s.
±52.2
201 n.s.
±35.2
Uq = 88. C
MARCH
NO CAGE CAGE
12230
±1171.6
328
±88.3
150
±60.5
51
±20.3
382
±71.7
80
±15.2
946
±83.9
22
±13.5
940
±101.4
248
±46.9
54
±25.1
48
±13.6
89
±20.6
n.s.
21540***
±1761.0
468 n.s.
±88.4
271*
±48.5
541***
±147.2
573*
±87.8
188
±36.6
1306*
±179.2
121
±34.5 '
1436*
±175.6
338 n.s.
±53.3
194**
±34.4 '
140*
±36.8
201*
±44.3
200
-------
w
%
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201
-------
TABLE 13. COhPOSITION OF SEDIMENTS SAMPLED IN JANUARY AND
MARCH 1980, FROM CAGED AND UNCAGED ZOSTERA.
DIFFERENCES WERE TESTED BY A T-TEST, ON ARCSIN
TRANSFORMED PERCENTAGES.
Sand
Uncaged
% Silt and Clay
Uncaged Cagec
January
N=3
X
S
t
91.36
91.64
89.24
90.75
1.315
1.76
92.09
92.68
92.31
92.36
0.297
n.s.
8.64
8.35
10.76
9.25
2.329
7.91
7.32
7.69
7.64
0.638
n
March
N=5
X
S
t
93.68
89.76
88.83
89.33
92.45
90.81
2.129
2.00
89.81
88.23
86.04
89.25
90.03
88.67
1.630
n.s.
6.32
10.24
11.17
10.67
7.55
9.19
2.259
10.19
11.77
13.96
10.75
9.97
11.32
2.981
202
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TABLE 14. ESTIMATES OF CONSUMPTION BY WATERFOWL AT VAUCLUSE SHORES,
1978-1979, BY PREDOMINANT FOOD TYPE.
Canada goose
Brant
Redhead
Whistling swan
American wigeon
Pintail
Black duck
Mallard
Daily
Consumption
g AFDW ind"1
193.6
120.6
83.3
308.1
62.1
73.0
85.8
85.8
Vegetation (over
Mean
Abundance
100 ha"1
(total habitat)
284.3*
46.1
44.2
29.9
12.0
2.7
2.2
0.3
total habitat)
(over vegetated shallows)
Bufflehead
Red-breasted merganser
Common goldeneye
Scaup spp.
Surf scoter
40.6
73.0
73.0
73.0
46.1
18.9
2.2
0.9
75.6 0.4
Invertebrates/Fish (over total
habitat)
Annual
Consumption
g AFDW m~2
8.26
0.83
0.55
1.34
0.11
0.03
0.03
<0.01
11.15 g
21.44 g
0.28
0.21
0.02
0.01
<0.01
0.52 g
* Foraging geese only.
203
I ,
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TABLE 15. ESTIMATES OF CONSUMPTION BY WATERFOWL AT VAUCLUSE SHORES,
1979-1980, BY
PREDOMINANT FOOD TYPE.
Redhead
Brant
American wigeon
Whistling swan
Canada goose
Pintail
Black duck
Bufflehead
Scaup
Red-breasted merganser
Surf scoter
Horned grebe
Oldsquaw
Common goldeneye
Common loon
Mean
Daily Abundance
Consumption 100 ha"-*-
(g AFDW ind"1) (total habitat)
83.3 60.1
120.6 1.8
62.1 1.6
308.1 1.5
195.6 0.4
73.0 0.3
85.8 0.1
Vegetation (over total habitat)
(over vegetated habitat)
40.6 96.1
73.0 15.0
73.0 3.1
75.6 2.2
0.9
59.3 0.3
73.0 0.3
<0.1
Invertebrates/Fish (over total
habitat)
(over vegetated habitat)
(over Zostera only)
Annual
Consumption
(g AFDW nT2)
0.76
0.03
0.01
0.07
0.01
<0.01
<0.01
0.88 g
1.19 g
0.59
0.17
0.03
0,03
<0.01
<0.01
<0.01
<0.01
0.82 g
1.09 g
3.32 g
204
-------
Consumption by all other species totalled only 0.18 g AFDW a"* over
all habitat zones. Because the distribution of birds within these
zones was recorded consumption of plant and animal foods was also
calculated over the vegetated area (for all species) and the Zostera
zone (for non-grazers). Utilization of the bare sand area was
negligible and thus consumption rates are higher per -or of vegetation
than when averaged over the entire habitat. Consumption of animal
foods in the Zostera zone was approximately three times the rate
averaged over all zones, reflecting higher bird densities associated
with Zostera.
The results of the two methods used to estimate consumption of
invertebrates in Zostera marina in 1980 are compared in Table 16. The
disparity between measures was greatest in January, whereas in March
the difference was negligible. Total consumption of six important
prey species amounted to approximately 1.46 g and 1.43 g AFDW m~^ in
January and March respectively by the exclosure method. Based on
calculations from bird density, buffleheads, scaup and surf scoters
removed 0.59 and 1.42 g of these prey species in January and March
respectively, assuming a similar diet within this habitat for all
three waterfowl species. Degree of agreement varied for individual
prey speceis, and was generally poorer than between combined values.
Consumption estimates calculated for March are cumulative, and
should approximate total annual consumption per unit area, for
comparison with the fall standing crop of the same species (Table 16).
Combined ash-free dry weight biomass was approximately 3.1 g in
Zostera in October/November 1979 (data from van Montfrans 1981), or
about twice the amount consumed by waterfowl.
DISCUSSION
Patterns of Waterfowl Abundance
Short term fluctuations in waterfowl abundance are difficult to
interpret, and may relate to changes in conditions on the breeding or
wintering grounds. Absence of Canada geese from the grassbed in the
second year of this study, following high abundances in 1978-79, did
not simply reflect local changes in wintering populations, as aerial
surveys conducted by U.S. Fish and Wildlife Service and the Virginia
Commission of Game and Inland Fisheries indicated similar abundances
of this species in the Eastern Shore survey zone in both years (F.
Settle, pers. comm.). Large flocks of geet'e rafting directly offshore
from the study area in 1979-80 also indicaced the presence of a
comparable wintering population.
The intense foraging activity exhibited by Canada geese at
Vaucluse Shores in 1978-79 is presumably atypical, as the species is
primarily field feeding in the Chesapeake Bay (Stewart 1962, Munro and
Perry 1981). Factors which influence such short term use of submerged
vegetation are not clear, but possibly reflect the availability and
accessibility of SAV in a given year. It is likely that when aquatic
205
-------
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1
vegetation is abundant in a localized area, geese may switch from or
supplement field feeding. Grain fields on the Eastern Shore of
Virginia are often adjacent or very close to beds of submerged
vegetation, and thus a temporary transition would not involve a
redistribution of the population. This is especially important for
Canada geese, as wintering flocks are highly organized socially, and
members remain strongly attached to specific feeding and resting
sites (Raveling 1979). i
Goose foraging may have had a negative impact on SAV in the
shallows in 1978-79, discouraging utilization the following year.
However, several authors report comparable or more extensive depletion
of SAV by waterfowl, yet do not infer a significant impact on
vegetation (Ki^rboe 1980, Jacobs et al. 1981). Alternatively, Ruppia
may have been less abundant in 1980 for reasons unrelated to waterfowl
grazing. Comparable biomass data are not available for both years,
but researchers in the area noted a visible decline in cover of Ruppia
in the shallows, and low abundance of this species was also reported
in other areas of the Bay in 1980 (R. J. Orth, pers. comm.). The
decrease in numbers and species of non-diving waterfowl as a group in
1979-80 may also reflect depleted SAV resources in the area, as
non-divers are restricted to very shallow water for feeding and as a
general rule, vegetation is the principle dietary component.
The importance of the bufflehead at Vaucluse Shores in both years <
of this study is consistent with the findings of Perry et al. (1981) j
that populations of this diving duck wintering in the Chesapeake Bay -t
appear to be stable over the short term, and have shown a long term ;
increase in proportion to increases in the flyway as a whole. "j
Vegetation comprises a minor portion of the diet of buffleheads, and 1
declines in SAV have not greatly affected its abundance or , |
distribution (Perry et al. 1981). An invertebrate diet increases the j
range of suitable foraging habitats available to buffleheads, and this |
flexibility may partially account for the relative stability of \ j
wintering populations. ; j
! 1
Species historically more dependent on submerged vegetation, such > >
as brant and redheads, were infrequently observed at Vaucluse Shores : j
but were occasionally very abundant. Brant.are more typically found , ' \
in coastal bays rather than estuaries, and now feed primarily on sea f
lettuce (Ulva latuca). Within the Chesapeake Bay, brant are abundant j
only where large areas of Zostera still exist (Stewart 1962). I
Redheads still rely on submerged vegetation, and therefore have j
declined in the Bay in response to declines in SAV. As with brant, |
they are concentrated only in areas with considerable coverage of SAV, j
such as Tangier Sound (Perry et al. 1981). Sporadic use of the study j
area exhibited by these two species thus reflects a currently patchy i
distribution throughout the Bay.- Whistling swans and wigeon were i \
relatively important in 1978-79 but the following year were nearly ' j
absent. Both species are primarily herbivorous, but whistling swans i I
have recently begun field-feeding and include some animal material in ' j
207
-------
the diet, whereas wigeon have not greatly altered food habits (Munro
and Perry 1981).
In 1978-79 water depth was found to be important in determining
the periodicity (via tide stage) of foraging by Canada geese. This
relationship undoubtedly results from the behavior of up-ending rather
than diving to obtain food, whereby foraging is restricted to very
shallow water. Palmer (1976) states that timing of feeding in brant
is governed by tide stage, food being more accessible at low tide.
Jacobs et al. (1981) also found a relationship between low tide and
numbers of waterfowl foraging in a Zostera noltii bed in the Dutch
Wadden Sea. The area available to non-diving waterfowl for feeding is
greatly increased at low tide, especially where the depth gradient is
gradual, as is characteristic of seagrass meadows.
Tide level had little effect on foraging by waterfowl in the
second season of study, as the most abundant species were diving
ducks, notably buffleheads, redheads and scaup. Buffleheads will feed
at all stages of the tide in areas where the preferred feeding depth
of 2 to 3 m is not greatly exceeded at high tide (Erskine 1971).
Redheads usually feed at depths less than 2 m, including extremely
shallow water where they will feed as dabbling ducks if they cannot
dive (Palmer 1976). Scaup forage at comparable depths, and are
affected by tide level only when feeding grounds are completely
exposed at low tide, in which case they cannot feed (Cronan 1957). In
the present study the only significant effect of tide on-waterfowl
numbers in 1979-80 occurred in the inshore Ruppia zone, due to the
fact that the area was often exposed at low tide or covered by only a
few cm of water, which effectively excluded all waterfowl. The
maximum depth in the study area at high tide was approximately 2 m,
which is well within the preferred range of the above species.
The range of temperatures observed had no effect on waterfowl
abundance, as ice formed rarely at the study site. Open water always
remained in deeper areas and therefore birds could feed throughout
freezing conditions. Time of day was not an important factor
influencing numbers of birds present in the study area.. Buffleheads
moved in and out of the study area in small groups throughout the day,
and did not exhibit obvious morning flights to the feeding area
typical of many waterfowl species. Johnsgard (1975) notes that, while
data are few, local movements of buffleheads on the wintering grounds \
are probably limited. \
\
Waterfowl generally seek shelter from severe winds, which may
account for the observed correlations between wind parameters and
waterfowl numbers. At most stages of the tide, the sandbar which
encloses the grassbed acts as a buffer to wave action, especially when
winds fetch across or down the bay. Shoaling is more extensive at the
extensive at the northern end and thus the sandbar offers more
protection from NNW winds than from winds with a more westerly
component. When winds are from the east or northeast, the entire
western shore of the peninsula is equally protected and the study area
208
-------
offers no additional shelter. The presence of greater numbers of
birds during strong NNW winds therefore reflects the orientation of
the study area and the configuration of the protective sandbar.
Variation in bird density within the habitat in 1979-80 may be
related to several factors. Densities were greatest in the Zostera
zone, which approximates the preferred feeding depth of buffleheads
(Erskine 1971) and is also the vegetated area farthest from shore.
Avoidance of the irr,hore sand and Rupfia zones can be partially
explained in similar terms in that these areas are very shallow and
close to shore. Availability of food may be a more important factor.
Abundances of epifaunal invertebrates were much lower in Ruppia than
in the mixed and Zostera zones (van Mont trans 1981), possibly due to
the shorter growth form and narrower blade width of Ruppia, and also
its patchy distribution within the grassbed. The bare sand zone
contained even lower numbers of invertebrates, with very few species
of importance to foraging waterfowl. Nilsson (1969) also found that
diving ducks in the Oresund fed over dense Zostera marina in
preference to mixed areas with patchy cover, and that food resources
were less abundant in the latter zones.
Bufflehead Food Habits
The importance of invertebrates in the diet of buffleheads is
well documented, and small molluscs and crustaceans are tne dominant
prey in salt water habitats. Weimeyer (1967) found that buffleheads
in the Humboldt Biy region fed primarily on bivalves, crustaceans,
fish and gastropods and that the relative contribution of these groups
varied between habitats. Erskine (1971) also emphasized the
importance of crustaceans (mostly decapods and isopods) and molluscs
as bufflehead foods on the wintering grounds. Nereid worms and
bryozoans were cited as minor components of the diet. In these and
other general accounts of bufflehead food habits (Cottam 1939, Stewart
1962, Munro and Perry 1981), diversity of food items is high, whereas
Stott and Olson (1973) found that on the New Hampshire coast, sand
shrimp (Crangon septemspinosa) comprised 75% of the diet of
buffleheads,
Bufflehead gizzard contents analyzed in this study were dominated
by species which are also abundant members of the epifaunal
communities associated with Ruppia and Zostera, such as Crepidula
convexa and Nereis succinia, suggesting that buffleheads rely heavily
on commonly encountered animals. This agrees with the findings of
Madsen (1954), who maintained that the diet of most diving duck
species reflects the availability of prey. Stott and Olson (1973)
also reported a close relationship between foods utilized by sea ducks
and the abundance of these foods in preferred habitats. However,
buffleheads in this study exhibited a degree of apparent electivity,
with several species eaten in numbers disproportionate to their
relative environmental abundances. Foraging behavior in buffleheads
is probably similar to the closely related goldeneye (Bucephala
clangula), which takes food items singly with a forceps action of the
209
-------
bill (Pehrsson 1976). Prey selection is enhanced by such a strategy
and is limited only by bill morphology, visual acuity, and energy
.cost. A major difficulty in demonstrating electivity is that the
relationship between numerical abundance and ecological availability
is often unknown. Madsen (1954) stated further that among available
(i.e. abundant) food items, the most easily obtainable within size
limits are preferred. Thus positive selection may indicate real
preference or degrees of availability, and for this reason tha term
apparent electivity is used.
Crepidula convexa was the only species which was apparently
selected against by foraging buffleheads, although it was still the
dominant prey item. This Hirk-shelled species lives attached to
vegetation or hard substrates which, combined with the extremely small
size of overwintering individuals (less than 2 mm average), may make
it difficult to collect. Alternatively, some gastropods may move into
the rhizome layer in th~ winter when above-ground vegetation is
reduced (Marsh 1976), and may be encountered infrequently rather than
avoided by diving ducks.
The gastropod Bittium varium is also dark in color, but is not
firmly attached to vegetation and is conical in shape. It should
therefore be more easily removed from blades by predators, although
size in winter is comparable to Crepidula convexa individuals. The
dove shell Astyris lunata and the bivalve Anadara transv'ersa arc
larger (3-5 mm) and therefore more visible, which could explain the
greater importance of these soecies in the diet relative to
environmental abundances. Selection of pyramidellid gastropods is
difficult to reconcile with the minute size of individuals (1.6 mm
average) and the translucent nature of che shell. However, species of
the genus Odostomia are reported to b^ ectoparasitic on other
invertebrates, notably^, varium (Hyraan 1967), and this association
should increase availability.
Electivity studies inherently assume that the predator has fed in
the same area where samples of prey abundance are taken. Because
waterfowl are highly mobile, this may not always be true. In the
present study, the presence of Ruppia and Zostera fragments in gizzard
samples, as well as epifauna characteristic of the habitat, suggest (
that birds had fed either in the study area or in similar vegetated \
habitats. !
Carbon isotope analysis also indicated the importance of
SAV-associated invertebrates in the bufflehead diet. The difference
between the mean 6^c value for bufflehead liver tissue and that
predicted from mean composition of gizzard contents and prey 6^C
values was within the 1-2 °/oo variation typically reported for such
comparisons. However, the departure was in the negative direction
whereas the shift is usually positive, resulting from metabolic
processes which conserve '^C (De Niro and Epstein 1978). It is likely
that gizzard data used in this study to predict g^C values did not
accurately reflect the diet, due to inadequate sample size or
210
-------
differential digestion of prey items. Gizzard analyses appear to have
underestimated the nutritional contribution of species with more
negative 6^^C values (primarily suspension feeders) rather than the
softer-bodied polychaetes and crustaceans which had higher 6*-'C
values. Barnacles and bryozoans may account for most of the
discrepancy, as these filter feeders were frequently eaten, but
because only shell fragments remained in the gizzard, proportional
contribution to total 6^C could not be calculated.
Intraspecific variability in bufflehead 6C values (3.2 °/oo
range) exceeded that suggested by Fry et al. (1978) for animals having
the same diet «1.6 °/oo). However, the low standard deviation
obtained suggests that individuals did not vary widely in food habits,
at least with respect to broad trophic groups. The greater
variability in S^-^C values of food items and species composition of
gizzard contents emphasizes the value of time-integrated data when
describing food habits of species with highly mixed diets.
analysis confirmed the minor role of submerged vegetation in
the diet of buffleheads and most other waterfowl sampled. With few
exceptions, waterfowl values were several paits per mil lower than
those for Zostera and Ruppia, with considerable overlap between
species having known preferences for vegetation (Canada geese, wigeon,
pintails, black ducks) and the remaining species which rely more on
animal foods. It is likely that terrestrial sources (especially
agricultural grains such as corn and wheat) provide a large portion of
vegetation eaten by Canada geese and possibly black ducks, as these
plants are highly negative in £13C values (De Niro and Epstein 1978).
Slightly more positive values exhibited by wigeon and pintails suggest
a more substantial contribution by aquatic vegetation. Values for
species with predominately animal diets were generally more negative
than those for buffleheads, implying greater importance of suspension
feeders or planktivorous fish.
Waterfowl Consumption Estimates
Submerged vegetation was an important resource for wintering
waterfowl (primarily Canada geese) at Vaucluse Shores in 1978-79. If
80 g AFDW m~2 is considered a maximum early winter biomass value for
Ruppia and stands of mixed Rupfja and Zostera, (R. J. Orth, unpubl.
data) then waterfowl removed 2i>% of the standing crop in shallow water
at the study site. A comparison of this estimate with those from
other studies is attempted in Table 17, by standardizing all reported
values to percentages of standing crop biomass, and restricting
examples to studies conducted in the non-growing season. From these
data, it is evident that the impact of waterfowl grazing varies widely
among habitats and with waterfowl species composition and density. At
Vaucluse Shores, grazing pressure was moderate in 1978-79 and minimal
the following year, relative to previous estimates.
Apart from variable research conditions, a major difficulty with
such comparisons is that consumption is often averaged over a large
211
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TABLE 17. REPORTED OR CALCULATED ESTIMATES OF WATERFOWL GRAZING PRESSURE
(% OF STANDING CROP CONSUMED) IN SAV HABITATS.
References
Habitat and Location
Estimated
Grazing Pressure
Ranwell and Downing (1959) Zostera nana
Sincock (1962)
Steiglitz (1966)
Zostera hornemanniana 30-75%
Scolt Head Is., England
Submerged Aquatics 20%
Back Bay, VA and Currituck
Sound, NC
Halodule wrightii 32%
Cornelius (1977)
Jupp and Spence (1977)
Verhoeven (1978)
Ki«*rboe (1980)
Jacobs et al. (1981)
Wilkins (1982)
(This study)
Ruppia maritima
Apalachee Bay, FL
Halodule beaudettei
Laguna Madre, TX
Potamogeton spp.
Loch Leven, Scotland
Ruppia cirrhosa
Texel, Netherlands
Submerged Aquatics
Ringkfibing Fjord, Denmark
Zostera noltii
Dutch Wadden Sea
Ruppia maritima
Zostera marina
Chesapeake Bay, VA
4%
13%
21%
50%
50%
25%
212
-------
area, ignoring within-habitat variations in resource use. Jacobs ct
al. (1981) found that grazing pressure by geese and wigeon was not
uniform in Zostera noltii, and was directly proportional to initial
percent cover of vegetation. In the present study, bird densities,
and therefore consumption rates, were much higner in the vegetated
area than in the total habitat. Foraging by Canada geese was
restricted to the shallows, further increasing consumption estimates
in those areas. Variable consumption rates within a given habitat
have also been reported for wading birds (Wolff et al. 1975) and
diving durks (Nilsson 1969), emphasizing the need to partition
consumption within a habitat before attempting to estimate impact on
benthic communities.
The results of exclosure experiments carried out in 1979-80
suggest that waterfowl had a significant effect on the abundances of a
number of invertebrate species in the Zostera zone. By 19 March, when
exclosures were removed; both estimates indicated a consumption of
nearly 50% of the combined ash-free dry weight standing crop of six
important bufflehead prey species. Qualitative agreement was obtained
between the results of caging experiments and bufflehead gizzard
analyses, in that species most affected were also important prey
items. However, caging results obtained in January are diffcult to
interpret on the basis of waterfowl foraging alone, with respect to
these dominant prey species. Consumption calculated from exclosure
samples was much higher than that based on bird density, and was
within 0.03 g of the estimate for March. Waterfowl densities were
comparable over the two intervals, and one would expect an increased
difference between treatments in proportion to the number of days
between sampling periods.
In studies where cages are used to exclude predators, the
possibility of an artificial cage effect must always be considered.
Larval settlement is enhanced by the current-baffling effect of the
cage structure, and has been a major problem in previous caging
experiments in soft-bottom habitats (Virnstein 1981). This effect was
not demonstrated by sediment analyses in this study, although pipette
analysis may not have detected slight changes in the silt and clay
fractions. Increased sedimentation would have been expected from the
degree of fouling that reduced the effective mesh size of the cages.1
In this habitat, however, few invertebrates which were significantly :
more abundant inside exclosures have free-swimming larval stages, and1
recruitment should not be affected by current velocity. Crepidula
convexa exhibits direct development of larvae, with individuals
hatched as juvenile snails (Ament 1979). The same is probably true
for the gastropod Astyris lunata, and peracarid crustaceans are known
brooders (Barnes 1980).
• The prosobranch gastropod Bittium varium has a planktonic veliger
larva, as does the bivalve Anadara transversa, but it is unclear
whether reproduction continues into the fall. Marsh (1970) reported
egg masses of j^. varium in May and June in a Zostera bed in the lower
York River, with juveniles predominant through the late summer and
213
-------
fall. Newly set individuals (0.5-0.7 mm) were not found in field
collections at Vaucluse Shores in September 1979 (J. Lunz, pers.
comm.) although bufflehead gizzard samples contained some individuals
less than 1.0 mm. Information on the reproductive cycle of A^
transversa was not available, but Marsh (1970) reported peak densities
in August poss;bly indicating larval settlement. High densities of
these two species may be related to the effect of the cage structure,
but only if recruitment occurred after mid-October when exclosure
experiments began. The high abundances of Mytilus juveniles in caged
samples in March was almost certainly induced by the cage structure,
as planktonic larvae are produced in early spring in the Chesapeake
Bay, and Mytilus was not recorded in gizzard contents. The reverse
trend for Ilyanassa obsoleta (higher numbers outside cages) may also
be an artifact of the experiment, as I_. obsoleta are attracted to
artificial structures in order to deposit egg capsules and would
therefore be found at the edges of the cages rather than in the i
sampled area (R. Orth pers. comm.). S
The above comparisons between estimates of waterfowl consumption ;
are made with caution, as confidence intervals on each estimate are )
very broad and many assumptions are involved in calculations. j
However, 1979-80 data suggest a range of values for annual consumption
of invertebrates of approximately 2-3 g ash-free dry weight m in
Zostera marina, with lower values for the total habitat.
Few previous studies provide comparable estimates of the impact
of waterfowl on invertebrates. Nilsson (1969) calculated that diving
ducks consumed 9% of the total standing crop of invertebrates, or 22 g
fresh weight m~^j in the most heavily utilized part of the habitat.
If this quantity is converted to ash-free dry weight and only the
standing crop of prey species considered, the resulting values would
probably be within the range obtained in this study.
Consumption by waterfowl at Vaucluse Shores was undoubtedly low
relative to total standing crop biomass and annual production of
invertebrates, but it was shown that significant cropping of dominant
prey species occurred. Given the predominance of very small food
items in the diet of buffleheads, this habitat represents an optimal
feeding ground for the species, as the density and diversity of
invertebrates are higher than in unvegetated areas. This research
suggests that the interaction between waterfowl and the benthic fauna
of SAV ecosystems is of greater trophic importance than has been
previously recognized. Further long-term studies are required to more
clearly define the role of non-grazing waterfowl in SAV habitats, and
to determine and interpret patterns of direct utilization of submerged
vegetation by grazing species.
SUMMARY
1. Canada geese were the dominant waterfowl at Vaucluse Shores in
1978-79, averaging 526 birds per 100 ha. Foraging by this species
was influenced by tide level, with greatest activity around low
214
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tide. An estimated 21.4 g AFDW ra~^ of vegetation was removed by
grazing waterfowl during the season, if bird density calculations
are based on shallow vegetated areas. This represents
approximately 25% of the estimated fall standing crop of
vegetation.
2. The following year (1979-80), the waterfowl community in the study
area was dominated by diving ducks, primarily buffleheads. Canada
geese and other non-diving species were nearly absent, although
local wintering populations were much the same size as in the
previous year. Reasons for this marked contrast are unclear, but
intense grazing in 1978-79 may have reduced the availability of
vegetation in the shallows, or a decline in Ruppia biomass
unrelated to waterfowl activity may have discouraged foraging in
the study area in 1979-80.
3. In 1979-80, daily patterns of waterfowl abundance were influenced
by wind parameters, whereas tide level, temperature, and tine of
day had little or no effect.
4. Differential waterfowl use of areas within the SAV habitat vas
found to occur in the 1979-80. Bird densities were greatest in
the Zostera and mixed vegetation zones, and minimal in RujpLf. and
bare sand areas. The latter areas are very shallow and contain
lower densities of invertebrates, and would therefore be less
attractive to foraging buffleheads.
5. Bufflehead gizzard analyses indicated the importance of small
gastropods such as Crepidula convex';, peracaridan crustaceans such
as Erichsonella attenuata and the polychaete Nereis succinea in
the diet of this diving duck. Predominant food items were also
abundant members of the grassbed epifauna, although some evidence
for selectivity was found. Carbon isotope analysis generally
supported conclusions regarding bufflehead diet. Variability in
bufflehead S C values was low compared to the range obtained for
food items, indicating a similar diet among individuals. These
analyses confirmed the minor role of submerged vegetation as a
direct food source for buffleheads and other waterfowl in the area
in 1979-80.
6. Exclosure experiments yielded estimates of consumption of
invertebrates which compared well with calculations based on bird
density in March, and annual consumption in Zostera was estimated
at 2-3 g AFDW m~ . Approximately 50% of the fall standing crop cf
six important prey species was removed by foraging waterfowl in
1979-80.
7. These data suggest that waterfowl foraging may be an important, if
unpredictable, component'of energy flow in SAV habitats in winter
months, both from direct consumption of vegetation and predation
on associated epifaunal invertebrates.
215
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21P
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219
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220
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CHAPTER 7
TROPHIC RELATIONSHIPS IN A SUBMERGED MACROPHYTE BED
BASED ON 6l3c VALUES
by
Jacques van Montfrans
and
Robert J. Orth
j
M
;f
221 ! i
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ABSTRACT
Trophic relationships in a lower eastern shore Chesapeake Bay (Vaucluse
Shores at the mouth of Hungars Creek) seagrass bed were investigated by
examining time integrated stable carbon isotope ratios C^C/^c) in primary
producer and consumer populations. The periphyton grazing snail, Bittium
varium exhibited close ties to the microalgae found on Zostera marina leaves.
Dominant isopods (Erichsonella attenuata and Idotea baitica) were more closely
linked to the seagrasses themselves. In several other invertebrate and
vertebrate species trophic relationships were more obscure although these will
be more closely examined in a forthcoming publication. Overall, carbon
isotope analysis appears promising as a method for elucidating general trophic
relationships in seagrass communities.
222
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INTRODUCTION
The natural proportions of two stable carbon isotopes, ^C (1.1 °/o) and
*-*G (98.9 °/o) are fractionated differentially by the various functional
groups of primary producers depending in pav t on their photosynthetic pathway
(Thayer et al., 1978). Vascular plants with the C^ metabolic pathway tend to
incorporate the *3C isotope t.o a greater degree than those having a €3 pathway
(Hatch and Slack, 1970; Black, 1971; Welkie and Caldwell, 1970). For the
purposes of comparing carbon isotope ratios in plant and animal tissues and
those of inorganic substances, the 5 (delta) 13C index is used and is defined
as:
.„ / (13C/12C) in sample \
61JC(°/oo) « {-rr:—— -1 X 1000
\UJC/12C) £n standard (Chicago PDB) /
Carbon isotope ratios fixed by plants remain relatively constant in both
living and decomposing plant tissue (De Niro and Epstein, 1978; Haines and
Montague, 1979). This ratio (i.e. 8^ C value) is maintained in a near
one-to-one correspondence when transferred to herbivores specialized for
feeding on a particular plant source and subsequently to higher trophic levels
through carnivory or omnivory (Fry et al., 1978; De Niro and Epstein, 1978).
Because 6 C values can remain relatively unchanged throughout various trophic
levels, consumer tissue S C values reflect the organisms time-integrated
dietary history. Thus, herbivores and their predators should reflect a narrow
range of 6 C values characteristic of the original plant substrate fed upon
whereas species with a general feeding habit will have a broader range of
values.
The primary producers which supply organic carbon for utilization by
marine organisms such as those found in Chesapeake Bay grass beds include:
seagrasses and fringing C^ marsh plants such as Spartina alterniflora
with 613C values from -9 to -13 °/oo (Thayer et al., 1978; Haines, 1976);
benthic microalgae, mostly diatoms, with values from -16 to -18 °/oo (Haines,
1976); phytoplankton with ratios of -20 to -26 J/oo (McConnaughey and McRoy,
1979; Haines and Montague, 1979); C$ photosynthetic plants showing values of
-24 to -29 °/oo (Haines and Montague, 1979); and algae (no distinction between
macro- and microalgae) with ratios ranging from -12 to -23 °/oo (Haines,
1976). Clues to the origin of those organic carbon sources should appear in
tissue 6*3C values of the major grass bed utilizers and therefore shed light
on the trophic structure of the grass bed community. The purpose of this
section is to report on the preliminary results of trophic interactions based
on 5*3C values found in primary producers as well as secondary resident and
migratory consumers of the Vaucluse Shore grass bed. A more complete analysis
and presentation of these data will be forthcoming.
223
.—J
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METHODS AND MATERIALS
Tissue samples for C/C carbon ratio (6C) analyses were collected
throughout the summer of 1978 and 1979. Additional samples of waterfowl were
collected during the winter of 1979-80. Plant material was carefully checked
for epiphytes or epifauna which were removed by scraping or brushing prior to
drying. Both the macrophyte and attached material were saved for analysis.
Benthos and fish had their guts removed or were held in screened containers in
aquaria for 24 hr to permit the voiding of gut contents. Specimens of resident
consumers and predators were grouped by size. A special effort was made to
examine changes in 6 C values with growth. Shelled animals were treated with
10 °/o HC1 prior to analysis to remove carbonate shell fragments. Waterfowl
liver tissue was collected from freshly killed birds in the grass bed. All
tissues collected were then dried, ground to a fine powder with a mortar and
pestel or Wiley mill and distributed to consultants for further analyses.
Some tissue samples were analyzed for S^C values by Dr. Evelyn Hair.es of the
University of Georgia Institute of Ecology, Athens, Ga. The majority were
analyzed by Drs . James Winters and Patrick Parker of Coastal Science
Laboratories, Inc., Port Aransas, Texas.
RESULTS AND DISCUSSION
A wide variety of grass bed associated species representing different
trophic levels and several feeding modes were analysed for <5^C values (Table
1). The primary producers in the system had a wide range of values.
Macroalgae exhibited 6^C values between -16 and -19 °/oo, epiphytic
microalgae around -11.2 °/oo and submerged macrophytes had higher 6 C values
of between -7 and -10.6 °/oo. Additional food sources sampled in the system
which include or originate from primary producers are periphyton (i.e.
microalgae and associated microfauna and detritus) found growing on the plants
with 6l-*c values of -18.3 and particulate detritus having 6"c values of -16.3
°/oo . Three sources of primary production with potential carbon input that
were not sampled in this study bu1: for which literature values exist include
benthic algae, (mostly diatoms, with carbon isotope ratios between -16 and -18
°/oo, Raines, 1976), phytoplankton (-20 to -26 °/oo, McConnaughey and McRoy,
1979) and the fringing marsh vegetation consisting of Spartina alternif lora
(-9 to -13 °/oo, Haines, 1976). Some of these carbon sources can be detected
in the invertebrates and vertebrates which inhabit or feed in the grass bed.
For example a hydrozoan feeding on zooplankton had a value (-20.5 °/oo) very
near that reported for phytoplankton based food webs (-20 to -26 °/oo, i
McConnaughey and McRoy, 1979). Similar plankton based food sources were
indicated for other filter feeders such as adult epifaunal Crepidula convexa
(-20.2 °/oo) and My a arenaria from the York River (-20.2 °/oo) as well as
red-breasted mergansers (-20.8 °/oo) which consume primarily planktivorous
fishes. Interestingly, several infaunal bivalve filter feeders showed
somewhat higher than expected 6^C values ( -15.5 °/oo) indicating perhaps the
incorporation of some SAV detrital carbon.
The grazing gastropod, Bittium varium had 6^-^C values (-13.4 °/oo)
approximating those of microepiphytes (-11.2 °/oo) which confirm the
utilization of eelgrass associated diatoms by 15. varium. Species which show
close trophic ties with SAV (S^C of -7.1 to -10.6 °/oo) include the isopods
224
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Erichsone 11 a attenuate-; (-7.9 to -12.2 °/oo) and Icotea baltica (-8.7 to
-14.0 °/oo).
Many of the remaining invertebrates showed intermedite ^/C values
ranging from between -11 to -17 °/oo. A complete interpretation of trophic
relationships among these species must await a more detailed analysis of the
data although at first glance these values imply considerable utilization of
submerged macrophyte derived carbon.
Trophically important fishes in the grass bed included pipefish
(Syngnathus fuscus), silver perch (Bairdiella chrysura) and spot (Leiostomus
xanth'Tus) with 6 C values from -13.1 to -17.0 °/oo. Other migratory
consumers utilizing the grass bed included numerous species of waterfowl with
a wide range of 6*->C values between species. Lowest 6^C ratios were seen in
the American coot (-25.0 °/oo), Canada goose (-21.6 °/oo in one individual)
and red-breasted merganser (-20.8 °/oo). The low values observed for the
former two species can possibly be explained by feeding on agricultural
grains, primarily corn, which is readily available in nearby fields. The
latter species, as already explained, feeds on planktivorous fish reflecting a
plankton based food source. Buffleheads, for which a large number of liver
saftples were obtained, exhibited a fairly narrow range of vaiaes (-15.8 to
-18.5 °/oo). These values closely correspond with those for the invertebrates
which were important food items in bufflehead gizzards.
Although there was inadequate time to fully discuss the implications of
our observed values, we expect to publish these results foil-owing a more
complete evaluation and detailed comparison with other pertinent studies on
this topic .
230
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