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This is to certify that the

dissertation entitled

INVERTEBRATE TROPHIC RELATIONSHIPS
IN TEMPORARY WOODLAND PONDS IN MICHIGAN

presented by

Michael John Higgins

has been accepted towards fulfillment
of the requirements for

Ph.D. Entomology

degree in

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Majo rofessor

 

 

Date April 28, 2000

 

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INVERTEBRATE TROPHIC RELATIONSHIPS IN TEMPORARY
WOODLAND PONDS IN MICHIGAN

By

Michael John Higgins

A DISSERTATION
Submitted to
Michigan State University

in partial fulfillment of the requirements
for the degree of

DOCTOR OF PHILOSOPHY
Department of Entomology

2000

ABSTRACT

IN VERTEBRATE TROPHIC RELATIONSHIPS INT EMPORARY
WOODLAND PONDS IN MICHIGAN

By

Michael John Higgins

Temporary woodland ponds are small, fishless habitats that flood in the early spring
from snowmelt and rainfall. They may remain flooded for 8-50 weeks out of the year,
depending upon the size of the pond. While much of the energy flow within these
systems is detritus based, primary production is also very important in medium to large-
sized ponds. The invertebrate communities that inhabit these ponds are all
characterized by rapid development and possess either a drought-resistant stage or are
capable of dispersal to permanent water when the habitat dries. Mosquito larvae are the
most abundant insects within these habitats, and the feeding ecology of larval Aedes
stimulans mosquitoes was examined through field microcosm experiments. Larvae of
mosquitoes with little material on which to graze survived and grew as well as those
furnished with a biofllm on which they could feed. Analysis of gut contents indicated
that the non-grazing mosquitoes filtered substantially more high quality algae from the
water column than the grazing mosquito larvae, suggesting that the algae was an
important component of their diet. Other studies indicate that the invertebrate
communities in these temporary ponds are strongly influenced by sized-based
predation, and that phenology may be important for many prey species. Potential prey
organisms such as mosquitoes, fairy shrimp, and cladocerans may reduce their exposure

to predation by beginning their development early in the spring prior to the appearance

of most predators. In addition, by beginning development early they can reach a body
size that is beyond the handling capabilities of most later-appearing predators. Analysis
of the cladoceran community indicates seasonal shifts in species composition, body
size, and morphology that correspond to seasonal changes in the composition of the

predator community.

Copyright by
MICHAEL JOHN HIGGINS
2000

This dissertation is dedicated to the memory of Robert and Mary Ann,
beloved father and sister.

ACKNOWLEDGMENTS

A Ph.D. dissertation, being the culmination of one's academic training, is, in many
respects, the result of one's knowledge and experiences gained in life up to that point.
So many people and events throughout our lives have forged our way of thinking in
such subtle ways that we could never remember them all, much less acknowledge them.
And yet, looking back, we can see moments and places where paths diverged and one's
life turned to follow one over the other. More often than not, our choices were guided
by individuals who showed us ways of viewing life that we had not before considered;
individuals who—in retrospect—helped shape our lives. Science, like life itself, builds
on what has come before. The dissertation that follows is the direct result of my five
years of study at Michigan State University, but it is also the fruit of influences past and
present.

I would first like to thank my parents, Norma and Robert for their support over the
years. My undergraduate mentor in anthropology, Dr. Richard Flanders taught me how
to think critically. At Western Michigan University, special thanks go to Drs. William
Crernin and Betsy Garland of the Department of Anthropology, and Drs. Richard
Brewer and David Cowan of the Department of Biological Sciences. Dr. Brewer
provided me with a strong foundation in ecology, and Dr. Cowan was responsible for
instilling in me a passion for entomology and aquatic invertebrates. Through his
courses in evolutionary biology, Dr. Cowan also started me to think as a biologist.

At Michigan State University, I would like to acknowledge the assistance of several

individuals who helped out in many ways. Field and laboratory assistance was

vi

performed by Mike Chumley and Blair Richards. The support staff in the Department
of Entomology deserves special mention, particularly Jill Kolp, Barbara Stinnett, Linda
Gallagher, Jan Eschbach, Alice Kenady, and Heather Lenartson. The Merritt lab
graduate student crew was always a source of inspiration, support, and entertainment.
Special thanks go to Dr. John Wallace for his special insights into mosquito ecology
and Warner Brothers cartoons.

This dissertation would not have been possible without the careful and thoughtful
guidance of my committee. I owe a tremendous debt of gratitude to Drs. Donald Hall,
Department of Zoology, Frank D'Itri, Institute of Water Research, Mike Kaufman,
Kellogg Biological Station, Edward Walker, Department of Entomology, and, of
course, my advisor, Richard (Rich) Merritt of the Department of Entomology and the
Department of Fisheries and Wildlife. There is absolutely no way I could every repay
all that Rich has done for me over the years. Not having personally met him before
starting my Ph.D. program, I feel fortunate in getting an advisor who is as dedicated to
the role of mentoring as is Rich. As advisor, colleague, and friend to merely say "thank
you" seems wholly inadequate.

The initial funding for this research was provides by a USDA National Needs Water
Science Fellowship through Michigan State University (USDA Grant 93-38420-8798).
Additional support was provided by National Institutes of Health Grant A121884, the
College of Natural Science, and the Graduate School, and the Ray and Bernice Hutson

Endowment from the Department of Entomology at Michigan State University.

vii

TABLE OF CONTENTS

LIST OF TABLES .................................................... x
LIST OF FIGURES ................................................... xi
INTRODUCTION ..................................................... 1
CHAPTER 1
TEMPORARY WOODLAND PONDS IN MICHIGAN: INVERTEBRATE
SEASONAL PATTERNS AND TROPHIC RELATIONSHIPS ............... .9
Introduction .................................................. 10
Seasonal Pattems—Vemal Phase ................................. 12
Seasonal Patterns—Aestival Phase ................................ l9
Trophic Relationships .......................................... 21
Conclusions .................................................. 30
References ................................................... 31
CHAPTER 2
FEEDING ECOLOGY OF AEDES ST IM ULANS (WALKER) MOSQUITO
LARVAE IN TEMPORARY WOODLAND PONDS ....................... 35
Introduction .................................................. 36
Materials and Methods .......................................... 37
Study sites ............................................. 37
Microcosms ............................................ 39
Water and mosquito gut samples ............................ 42
Statistical analysis ....................................... 43
Results ...................................................... 43
Microcosm experiments ................................... 43
Water samples .......................................... 49
Mosquito gut samples .................................... 51
Discussion ................................................... 5 1
References ................................................... 55
CHAPTER 3
CLADOCERAN SUCCESSION IN A TEMPORARY WOODLAND POND
IN MICHIGAN: THE INFLUENCE OF PREDATION ...................... 57
Introduction .................................................. 58
Materials and Methods .......................................... 59
Study site .............................................. 59
Collecting methods ...................................... 61
Water samples .......................................... 62
Results and Discussion ......................................... 62
Seasonal succession ...................................... 62

viii

Seasonal changes in cladoceran body size ..................... 65

Predator succession ...................................... 67
Other invertebrates ....................................... 70
Seasonal changes in the microbial community ................. 72
Successional patterns and predation .......................... 75
Conclusions .................................................. 84
References ................................................... 86
CHAPTER 4
PHENOLOGY, BODY SIZE, AND PREDATION IN A TEMPORARY
WOODLAND POND ................................................ 91
Introduction .................................................. 91
Materials and Methods .......................................... 94
Study site .............................................. 94
Field studies ............................................ 95
Predator/size experiments ................................. 96
Results ...................................................... 97
Predator succession ...................................... 97
Predation and body size ................................. 100
Seasonal changes in body size relationships .................. 102
Discussion .................................................. 107
References ‘ ................................................. 113
APPENDICES ..................................................... 1 16
Appendix A. Record of Deposition of Voucher Specimens ........... 117
Appendix B. Voucher Specimen Data ............................ 118

ix

LIST OF TABLES

CHAPTER 1

Table 1. Summary of life history groups for invertebrates inhabiting

temporary woodland ponds ..................................

Table 2. Growth of first-instar Aedes stimulans mosquito larvae in field
microcosms supplied with no leaves or with 3g (initial dry wt.)
of conditioned or unconditioned leaves, Wild Ginger Pond,

Lansing, Michigan 1996 .....................................

CHAPTER 2

Table 1. Growth of first-instar Aedes stimulans mosquito larvae in field
microcosms supplied with no leaves or with 3g (initial dry wt.)
of conditioned or unconditioned leaves, Wild Ginger Pond #1,

Lansing, Michigan 1996 ....................................

Table 2. Growth of first-instar Aedes stimulans mosquito larvae in field
microcosms supplied with leaves (3g initial dry wt), no leaves, or
with no leaves and weekly replacement of microcosms, Wild

Ginger #1 Pond, Lansing, Michigan 1998 .......................

Table 3. Direct counts of suspended material in water column samples
using DAPI stain and epifluorescence microscopy. Values are

cells or particles ml'l (S.E.M.); n = 5 for each sampling date ........

Table 4. Direct counts of food particles from guts of fourth larval instars
of Aedes stimulans. Values are means (n = 5) of cells or particles

gut" and (S.E.M.) ..........................................

CHAPTER 3

Table 1. Major potential predators of cladocerans in WG-1 pond, 1999 .......

CHAPTER 4

Table 1. Predator feeding experiments using 4 larval Aedes stimulans
mosquitoes and l larval predator. Values are percentages of
mosquitoes eaten and mean number consumed per container in
parentheses; n= 10 for all except third instar Agabus (n=8). Mean

length of each instar is given in parentheses ......................

....14

...24

....45

...48

....50

...52

...68

. 101

LIST OF FIGURES

CHAPTER 1

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Temperature data for a small vernal pool in southern Michigan.
Each symbol represents a reading taken at approximately 1.5
hour intervals with a data logger ................................. 13

Functional feeding group composition (by genera) of invertebrates
in temporary woodland ponds ................................... 23

Predator composition by life history strategy in temporary
woodland ponds .............................................. 23

Functional feeding group composition for Wiggins et a1. (1980)
Group 4 life history strategy ..................................... 29

CHAPTER 2

Figure 1.

Figure 2.

Figure 3.

Water temperatures, Wild Ginger #1 Pond, 1996-1998 ................ 38

Diagram of floating microcosm used in field experiment. a) 4 1

plastic container, b) 250 pm N ytex mesh on sides and bottom,

c) Styrofoam floats, (1) nylon fishing line to anchor microcosm,

e) garden stake, f) water surface, g) substrate ....................... 40

1996 field microcosm results. a). survival, b). days to adult
emergence, c). adult weight. Values are means and S.E.M. ........... 44

Figure 4. 1998 field microcosm results. a). survival, b). days to adult

emergence, c). adult weight. Values are means and S.E.M. ........... 47
CHAPTER 3
Figure 1. Water temperatures, WG-l Pond, 1999 ............................ 60
Figure 2. Seasonal changes in cladoceran density, WG-l Pond, 1999 ............ 63
Figure 3. Seasonal changes in body lengths of parthenogenetic females of

the four most abundant cladoceran species. Values are means
and S.E.M ................................................... 66

xi

Figure 4.

Figure 5.

Figure 6.

Microbial and detritus counts for water column samples, WG-l
Pond, 1999. Values are means (S.E.M.), n=5. All numbers are
log transformed .............................................. 73

Seasonal changes in the algal community of the water column,
WG-l Pond, 1999. Values are means (S.E.M.), n=5 ................. 74

Tail spine length as a function of body length for parthenogenetic
Daphnia pulex during early (April) and late (June) season.
Slopes differ significantly at p < 0.0001 ........................... 82

CHAPTER 4

Figure 1.

Figure 2.

Relationship of seasonal changes in number of predatory taxa with
changes in water temperatures, Wild Ginger #1 Pond ................. 98

Seasonal trends in body size relationships between predators and
three prey taxa, Wild Ginger #1 Pond ............................ 103

Figure 3. Seasonal changes in body lengths of parthenogenetic females of

the four most abundant cladoceran species. Values are means
and S.E.M ................................................. 105

Figure 4. Tail spine length as a function of body length for parthenogenetic

Daphnia pulex during early (April) and late (June) season. Slopes
differ significantly at p < 0.0001 ............................... 106

Figure 5. Generalized relationships of predator/prey phenology and body

size in temporary woodland ponds .............................. 111

xii

INTRODUCTION

Temporary woodland ponds are small seasonal wetlands that may hold water from 2-
9 months out of the year. They may vary in size from less than 10 m2 to over 0.5 ha,
but most are probably less than 0.1 ha. These unique habitats have received relatively
little attention in the scientific literature and-—due their small size--practically no
protection from human impact. In southern Michigan forests and woodlots, the
remaining ponds are no doubt a tiny fraction of number that once dotted the
presettlement landscape.

Despite their diminutive size, temporary woodland ponds are exclusive breeding
sites for a number of vertebrate and invertebrate organisms. Although these ponds
generally do not support waterfowl, a number of amphibians use these seasonal habitats
as breeding sites. In particular, Wood Frogs, Rana sylvatica, Western Chorus Frogs,
Pseudacris triseriata trisen'ata, and several species of mole salamanders, Ambystoma
spp., use woodland pools for breeding and larval development in the spring (Harding
1997). In addition, Gray Treefrogs, Hyla versicolor, and Spring Peepers, Pseudacris
crucifer crucifer, may also use these small wetlands for breeding purposes (Harding
1997).

Several invertebrate species are unique to temporary ponds, and woodland ponds in
particular. Fairy shrimp (Family Chirocephalidae) occur only in temporary ponds, and
several species of Eubranchipus are common in woodland pools in the eastern United
States. The cladoceran, Daphnia ephemeralis, described as a species only in 1985

(Schwartz and Hebert 1985), is apparently only found in temporary woodland ponds in

eastern North America. Another cladoceran, Simocephalus exspinosus, may also favor
temporary habitats. Several species of insects are adapted to temporary ponds, and are
found exclusively in these seasonal habitats. The darnselfly, Lestes dryas, oviposits in
plant tissue along the margins of dry woodland pools, and Sympetrum dragonflies
(especially obtrusum and rubicundulum) also oviposit in the dry basins. These odonates
undergo obligate diapause as eggs and do not hatch until the following season (Wiggins
et a1. 1980). At least one species of beetle, the dytiscid Agabus erichsoni, is particularly
well adapted to temporary ponds, diapausing as eggs in pond basins during the dry
phase. Similarly, larvae of the phantom midge, Mochlonyx, are found exclusively in
temporary ponds.

In terms of abundance and impact on humans, mosquito larvae are perhaps the most
important organism to inhabit temporary ponds. Several species in the genus Aedes (in
particular, excucians, provocans, and stimulans) are very common in temporary
woodland ponds and, in many ways, epitomize an organism with the unique adaptations
required for survival and growth in these ephemeral habitats. Aedes mosquitoes have
drought and freeze-tolerant eggs that may remain viable in a suitable habitat for several
years(Horsfall 1956). Larvae can survive and feed at temperatures of 0° C during the
late winter and early spring (W estwood et a]. 1983; Walker 1995), and some species can
develop from egg to adult in as little as 5 days in summer rain pools (Horsfall 1955). In
addition to Aedes, several species of Psorophora mosquitoes are common in summer
rain pools in the eastern North America (Horsfall 1955; Wood et a1. 1979). Two
species in particular, P. ciliata and P. ferox, are common in woodland rain pools in

Michigan during the summer.

In addition to being a major nuisance to humans engaged in outdoor activities, many
of the mosquitoes that breed in temporary woodland ponds are vectors of diseases that
afflict humans and animals. Several Aedes mosquitoes are competent vectors of the
California encephalitis group of viruses (LaCrosse and Jamestown Canyon), and a few--
most notably, A. vexans-- are capable of transmitting Eastern and/or Western Equine
encephalitis (Harwood and James 1979). Psorophora ciliata is a competent vector for
St. Louis encephalitis. Several species of Aedes mosquitoes are also potential vectors of
dog heartworm (Ludlam et a1. 1970).

Despite the unique organisms and the potential disease vectors that inhabit small
temporary ponds, these habitats have-—unti1 only recently--received relatively little
scientific scrutiny. Mozley (1928, 1932) published one of the first descriptive studies of
a temporary pond and its inhabitants, and Kenk ( 1949) compared temporary and
permanent pond communities in southern Michigan. In the 1950s and 19603, there
were studies that examined the ecology of some Aedes mosquito larvae (e.g., Horsfall
1956; Haufe and Burgess 1956; Haufe 1957; Horsfall and Fowler 1961; James 1966),
and potential predators of mosquito larvae in snowmelt pools (Baldwin et a1. 1955;
James 1961, 1969). There have been studies of the population ecology of temporary
pond Aedes mosquitoes (Iversen 1971; Enfield and Pritchard 1977) and a few studies
examining the feeding ecology of these mosquitoes (Hinman 1930; Howland 1930;
Ameen and Iversen 1978). Barlocher et a]. (1978) examined the importance of the dry
phase of temporary ponds in conditioning the leaf detritus. They determined that leaves
that were colonized by terrestrial fungi provided a more nutritive food source for

detritvorous insects than leaves that remained submerged for the same length of time.

More recently, there have been several syntheses regarding the ecology of temporary
ponds (Williams 1987, 1996) and wetlands in general, including temporary ponds
(Batzer and Wissinger 1996; Batzer et a1. 1999).

In a landmark paper, Wiggins et a1 (1980) examined the adaptive strategies of
animals inhabiting temporary ponds. Four strategies were recognized based on physical
adaptations to survive the dry phase and oviposition behavior. Group 1 inhabitants are
permanent residents possessing either a drought-resistant stage or the ability to burrow
into moist sediments. Dispersal is generally passive only. Group 2 inhabitants
overwinter in some drought-resistant stage, emerge as adults in the spring, and oviposit
in the pond before it dries. Group 3 is similar to Group 2 except that oviposition is
independent of the presence of water, so oviposition generally occurs in the dry basin.
Group 4 individuals possess no particular adaptation to the dry phase and must
recolonize the pond each spring. Larvae of Group 4 inhabitants must complete
development and emigrate to a permanent water source before the pond dries. The
description of these 4 strategies by Wiggins et a1. (1980) still provides a very useful
paradigm for viewing the adaptations of animals to life in ephemeral habitats.

Beyond the abiotic constraints placed on inhabitants of ephemeral ponds, biotic
interactions are also important in structuring communities. Recently, the role of
predation in shaping temporary pond communities has been examined (Wellbom et al.
1996; Schneider and Frost 1996; Schneider 1997, 1999), particularly with regard to
pond duration. Long-duration ponds support a much more diverse and, on average,
longer-lived predator community than do short duration ponds. Such predator

communities may exclude certain taxa from long-duration ponds, or limit population

sizes of other taxa (Schneider and Frost 1996). The mechanisms for such exclusion or
limitation may include behavioral tradeoffs (Wellbom et al. 1996). Animals in
temporary habitats need to grow quickly and thus forage actively. This foraging
activity, however, results in increased exposure to predation. In short-duration ponds
with limited predator communities, this may not present a problem. In long-duration
and permanent ponds, however, such active foraging may lead to extermination by
predators. Thus, animals that are well adapted to temporary ponds are often excluded
from permanent and semi-permanent ponds (W ellborn et a]. 1996). Such mechanisms
are viewed as accessory to life history constraints such as a prerequisite cold and dry
period to initiate egg hatching (e.g., most Aedes mosquitoes). That many permanent
and semi-permanent pond communities contain many temporary pond taxa and a
reduced predator community after a drought (Jeffries 1994; Schneider and Frost 1996)
supports the argument that such taxa are excluded by predation.

The research presented in the chapters that follow represents the results of a multi-
year study of the invertebrate communities in several temporary woodland ponds in the
Lansing, Michigan area. These ponds ranged in size from 5 m2-3700 m2, and from 10—
50 weeks in duration. Chapter 1 presents an overview of temporary woodland ponds in
Michigan and a summary of some of the research. Chapter 2 examines the feeding
ecology of Aedes stimulans larvae in these ponds. Chapter 3 describes the zooplankton
community and cladoceran succession through the wet phase of one woodland pond.
Chapter 4 examines predator-prey relationships and the role of both phenology and

body size.

REFERENCES

Ameen, M. and T. M. Iversen. 1978. Food of Aedes larvae (Diptera: Culicidae) in a
temporary forest pool. Archiv ftir Hydrobiologie 83: 552-564.

Baldwin, W. F., H. G. James, and H. E. Welch. 1955. A study of mosquito larvae and
pupae with a radio-active tracer. Canadian Entomologist 87: 350-356.

Barlocher, F., R. J. Mackay, and G. B. Wiggins. 1978. Detritus processing in a
temporary vernal pool in southern Ontario. Archiv ffir Hydrobiologie 81: 269-
295.

Batzer, D. P., Rader, R. B., and Wissinger, S. A. [eds] 1999. Invertebrates in
Freshwater Wetlands of North America: Ecology and Management. John Wiley
and Sons. New York.

Batzer, D. P. and S. A. Wissinger. 1996. Ecology of insect communities in nontidal
wetlands. Annual Review of Entomology 41: 75-100.

Enfield, M. A. and G. Pritchard. 1977. Estimates of population size and survival of

immature stages of four species of Aedes (Diptera: Culicidae) in a temporary
pond. Canadian Entomologist 109: 1425-1434.

Harding, J. H. 1997. Amphibians and Reptiles of the Great Lakes Region. University of
Michigan Press. Ann Arbor.

Harwood, R. F. and M. T. James. 1979. Entomology in Human and Animal Health, 7th.
ed. Macmillan. New York.

Haufe, W. O. 1957. Physical environment and behavior of immature stages of Aedes
communis (Deg.) in subarctic Canada. Canadian Entomologist 89: 120-139.

Haufe, W. O. and L. Burgess. 1956. Development of Aedes (Diptera: Culicidae) at Fort
Churchill, Manitoba, and prediction of dates of emergence. Ecology 37: 500-
5 19.

Hinman, E. H. 1930. A study of the food of mosquito larvae (Culicidae). American
Journal of Hygiene 12: 238-270.

Horsfall, W. R. 1955. Mosquitoes: Their Bionomics and Relation to Disease. Ronald
Press. New York.

Horsfall, W. R. 1956. Eggs of floodwater mosquitoes (Diptera: Culicidae). III.
Condition and hatching of Aedes vexans. Annals of the Entomological Society
of America 49: 66-71.

Horsfall, W. R. and H. W. Jr. Fowler. 1961. Eggs of floodwater mosquitoes VIII.
Effect of serial temperatures on conditioning of eggs of Aedes stimulans Walker
(Diptera: Culicidae). Annals of the Entomological Society of America 54: 664-
666.

Howland, L. J. 1930. Bionomical investigation of English mosquito larvae with special
reference to their algal food. Journal of Ecology 18: 81-125.

Iversen, T. M. 1971. The ecology of a mosquito population (Aedes communis) in a
temporary pool in a Danish beech wood. Archiv fiir Hydrobiologie 69: 309-332.

James, H. G. 1961. Some predators of Aedes stimulans (W alk.) and Aedes trichurus
(Dyar) (Diptera: Culicidae) in woodland pools. Canadian Journal of Zoology -
Journal Canadien de Zoologie 39: 533-540.

James, H. G. 1966. Location of univoltine Aedes eggs in woodland pool areas and
experimental exposure to predators. Mosquito News 26: 59-63.

James, H. G. 1969. Immature stages of five diving beetles (Coleoptera: Dytiscidae),
notes on their habits and life history, and a key to aquatic beetles of vernal
woodland pools in southern Ontario. Proceedings of the Entomological Society
of Ontario 100: 52-97.

Jeffries, M. 1994. Invertebrate communities and turnover in wetland ponds affected by
drought. Freshwater Biology 32: 603-612.

Kenk, R. The animal life of temporary and permanent ponds in southern Michigan.
(71). 1949. University of Michigan, Museum of Zoology. Miscellaneous
Publication.

Ref Type: Serial (Book,Monograph)

Ludlam, K. W., L. A. Jr. Jachowski, and G. F. Otto. 1970. Potential vectors of
Dirofilan'a immitis. Journal of the American Veterinary Medical Association
157: 1354-1359.

Mozley, A. 1928. Note on some fresh water mollusca inhabiting temporary ponds in
western Canada. Nautilus 42: 19-20.

Mozley, A. 1932. A biological study of a temporary pond in western Canada. American
Midland Naturalist 66: 235-249.

Schneider, D. W. 1997. Predation and food web structure along a habitat duration
gradient. Oecologia 110: 567-575.

Schneider, D. W. 1999. Snowmelt ponds in Wisconsin: Influence of hydroperiod on
invertebrate community structure, p. 299-318. In [eds], D.P.Batzer, R.B.Rader,
and S.A.Wissinger, Invertebrates in Freshwater Wetlands of North America:
Ecology and Management. John Wiley and Sons, New York.

Schneider, D. W. and T. M. Frost. 1996. Habitat duration and community structure in
temporary ponds. Journal of the North American Benthological Society 15: 64-
86.

Schwartz, S. S. and P. D. N. Hebert. 1985. Daphniopsis ephemeralis sp.n. (Cladocera,
Daphniidae): a new genus for North America. Canadian Journal of Zoology -
Journal Canadien de Zoologie 63: 2689-2693.

Walker, E. D. 1995. Effect of low temperature on feeding rate of Aedes stimulans larvae
and efficacy of Bacillus thuringiensis var. israelensis (H-l4). Journal of the
American Mosquito Control Association 11: 107-110.

Wellbom, G. A., D. K. Skelly, and E. E. Werner. 1996. Mechanisms creating
community structure across a freshwater habitat gradient. Annual Review of
Ecology and Systematics 27: 337-363.

Westwood, A. R., G. A. Surgeoner, and B. V. Helson. 1983. Survival of spring Aedes
spp mosquito (Diptera: Culicidae) larvae in ice-covered pools. Canadian
Entomologist 115: 195-197.

Wiggins, G. B., R. J. Mackay, and I. Smith. 1980. Evolutionary and ecological
strategies of animals in annual temporary pools. Archiv fiir Hydrobiologie,
Supplement 58: 97-206.

Williams, D. D. 1987. The Ecology of Temporary Waters. Croom Helm, Timber Press.
Portland, OR.

Williams, D. D. 1996. Environmental constraints in temporary fresh water and their
consequences for the insect fauna. Journal of the North American Benthological
Society 15: 634-650.

Wood, D. M., Dang, P. T., and Ellis, R. A. 1979. The mosquitoes of Canada (Diptera:
Culicidae). The Insects and Arachnids of Canada, Part 6. Publication 1686.
Ottawa, Ontario, Canada, Biosystematics Research Institute, Research Branch,
Agriculture Canada.

CHAPTER 1
TEMPORARY WOODLAND PONDS IN MICHIGAN:
INVERTEBRATE SEASONAL PATTERNS AND TROPHIC RELATIONSHIPS
ABSTRACT

Temporary woodland ponds are relatively small, shallow wetlands that retain water
for a few weeks to several months out of the year. Most of the energy flow within these
habitats stems from microbial degradation of leaf litter deposited by surrounding trees
and shrubs. The composition of the invertebrate community found within any particular
pond is related to its size and duration of flooding. The invertebrates that inhabit these
ponds show varying degrees of adaptation to ephemeral habitats, but nearly all are
characterized by rapid larval growth. Medium to large size ponds exhibit a predictable
seasonal succession of species, a pattern that has evolved in response to both physical
constraints and biotic interactions. The early-season inhabitants are particularly well-
adapted to both the ephemeral habitat as well as the cold temperatures characteristic of
early spring in Michigan. These animals feed primarily on the abundant microbial
community present on the the leaf litter and within the water column, and avoid heavy
predation pressure by beginning development before the appearance of most of the
predators. Most of the ponds' inhabitants that are not specifically adapted to ephemeral
habitats are predators. These are generally insects that overwinter in permanent water
and recolonize temporary ponds each spring. By consuming a hi gh-quality food source
such as animal protein, these migrants are able to develop rapidly and thus ensure

completion of the larval phase before the ponds dry.

INTRODUCTION

Prior to Euro-American settlement, the wooded landscape of southern Michigan was
dotted by innumerable ephemeral ponds formed millennia ago in vast glacial outwash
plains. Although only a small percentage of these temporary woodland ponds remain
today, they represent a fairly common, yet remarkably understudied aquatic habitat.
Woodland ponds can range in size from a few square meters to over a hectare, although
most are probably less than 0.4 ha. Maximum water depth is generally less than 1.5 m,
and the average depth is usually under 1 meter. These small woodland ponds are
generally unsuitable for waterfowl production compared to larger, more open habitats, a
factor which may explain the relative inattention these wetlands have received in the
scientific literature. Ponds may begin to flood in late autumn or winter, reaching
maximum size in the early spring as a result of snowmelt and spring rains. A distinction
has been made between vernal pools, which flood only in the spring, and autumnal
ponds, which flood in the autumn and remain wet until the following summer (Wiggins
et al. 1980). It should be pointed out that the flooding which occurs in autumn often
only covers the deepest parts of these ponds, and much of the pond area remains dry
until the following spring. While the flooded area of an autumnal pond may provide
important overwintering habitat for some aquatic invertebrates that lack specific
adaptations for drying and freezing (Batzer and Sion 1999), much of the well-adapted
temporary pond fauna remains unaffected by this flood event. Thus, while the presence
or absence of water during the autumn and winter will influence faunal composition

somewhat (Kenk 1949; Wiggins et al. 1980; Batzer and Sion 1999), we believe that the

10

size and duration of a particular pond during the vernal phase has an even more
pronounced influence on community composition.

The duration of flooding is directly related to area and depth. All of these water
bodies are closed depressions and dry from evaporation and groundwater outflow. Most
are dry by the middle of summer and some may undergo a second, somewhat
accelerated cycle of flooding and drying in the mid to late summer as a result of heavy
precipitation from thunderstorms. Flooding during this aestival (summer) phase is
generally smaller in areal extent compared with the vernal phase. Small vernal pools
flood only in the spring.

Temporary woodland ponds occur in forested landscapes and are thus bordered on all
sides by trees (e.g., red maple, silver maple, elm, cottonwood) and shrubs (e. g.,
dogwoods, alder, spicebush). Trees frequently occur within the flooded portions of the
ponds as well as the borders. Because of the intense shading from trees and shrubs
along the margins of these ponds, there is often very little emergent vegetation present,
or the emergent plants may occur only in relatively small areas that receive sufficient
sunlight. In addition, submerged aquatic vegetation (including submerged macrophytes
and mats of filamentous algae) generally does not occur in these ponds. After the trees
leaf out in the spring, the ponds themselves may receive little direct sunlight, a factor
which may limit algal growth compared to more open types of wetlands (Kenk 1949).
The surrounding woodland vegetation is also important for the input of substantial

amounts of leaf litter into the dry basins in the fall. Barlocher et al. (1978) recorded an

average of 132.8 g/m2 of leaf litter (ash-free dry weight) falling into Ontario pond

basins in the autumn.

ll

In southern Michigan, water temperatures range from 3° C in the early spring when
ice is still present, to 27° C in the summer. Because of the shallow nature of these
bodies of water, daily water temperature fluctuations of 5° C are not uncommon in the
spring, particularly in the small ponds (Figure 1). In addition, a thin layer of ice
frequently covers the surface at night during the early spring. Early in the season, pH
generally ranges between 7-7.5, and gradually becomes more alkaline (7.5-8) as the
ponds shrink in size during the late spring and summer. Due to the large surface-to-
volume ratio, ice—free ponds do not often become anoxic, but anaerobic conditions exist
in the underlying sediments. Dissolved oxygen and pH also undergo diel fluctuations as
a result of increase algal respiration at night (Williams 1987).

SEASONAL PATTERNS—VERNAL PHASE

In a landmark paper on temporary pond ecology, Wiggins et al. (1980) divided
temporary pond breeding inhabitants into 4 groups (Table 1), based on their adaptations
(or lack thereof) to the dry phase of these habitats and also on their
oviposition/colonization habits. Animals that are particularly well-adapted to life in
these temporary environments (Groups 1-3) are basically year-round residents, spending
the dry phase in some drought-resistant stage (often the egg stage). Organisms which
lack drought-resistance (Group 4) must move to permanent water before the ponds dry
and then recolonize the temporary ponds the following spring. This latter category is
characterized by species with excellent colonizing abilities and rapid larval
development.

The composition of the invertebrate community present in any given pond is related
to its size and duration of flooding (Schneider and Frost 1996; Schneider 1999). Small

ponds of only a few weeks duration contain relatively few species, and are dominated

12

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14

by ostracods and mosquito larvae of the genus Aedes. In addition, there may be
gastropods, triclad turbellarians (planarians), cladocerans, and occasional predatory
beetle larvae (family Dytiscidae) present. Amphipods (Crangonyx) were surprisingly
abundant in several small vernal pools we have sampled. Amphipods are not thought to
be particularly well adapted to the dry and frozen conditions that characterize vernal
ponds during the autumn and winter (Wiggins et al. 1980; Batzer and Sion 1999), and
their presence in these short—duration (8-10) vernal pools remains an enigma. Isopods,
which are also poorly adapted to temporary ponds, were occasionally recovered from a
few vernal pools. Their presence may be explained, however, by the co-occurrence of
crayfish in these particular ponds. Crayfish burrows may provide a refuge in temporary
habitats for poorly adapted organisms such as isopods (Wiggins et al. 1980).

The relatively few number of species present in these small pools suggests relatively
simple trophic relationships (Schneider and Frost 1996). Medium- to large-sized ponds,
persisting for 4-6 months in the spring and summer, generally contain a large diversity
of invertebrate organisms and are characterized by a fairly predictible succession of
species. While there may be some invertebrates active during the winter in autumnal
ponds—generally small crustaceans such as copepods, ostracods and cladocerans--the
primary season of invertebrate activity begins when ice melts along the margins of the
ponds, usually in late February or early March in southern Michigan. If the ponds are
sufficiently flooded, Aedes mosquito eggs that were deposited in the dry basins by
females the previous season begin to hatch. Analyses of soil samples from temporary
ponds indicate that the vast majority of mosquito eggs are laid near the margins of

maximum flooding extent (James 1966) (Iversen 1971). Thus, if insufficient

15

precipitation occurs, resulting in lower than normal water levels, little hatching will take
place.

In addition to Aedes mosquito larvae, other early-season inhabitants of medium to
large—sized temporary woodland ponds include fairy shrimp (order Anostraca), small
crustaceans (copepods, cladocerans, ostracods), rnidge larvae (Chironomidae), phantom
rnidge larvae (genus Mochlonyx), caddisfly larvae (primarily Limnephilus), and
gastropods (e.g., Physella). Except for Mochlonyx, which preys upon small crustaceans
and perhaps some first-instar mosquito larvae, there are few predators during this early
part of the season. Conditions at this time are harsh, with cold water temperatures (<10°
C) and frequent ice formation on the surface, factors which do not appear to harm the
organisms listed above. Mosquito larvae have been shown to survive 10 days of ice
cover on a woodland pond in Ontario ((Westwood et al. 1983), and Walker ( 1995)
demonstrated that larvae continue to feed, albeit more slowly, at temperatures down to
0° C. Most of the predators in temporary woodland ponds do not appear until water
temperatures exceed 10° C on a regular basis. One of the few predators that appears to
have solved physiological problems associated with cold and ice is the dytiscid beetle
larva, Agabus erichsoni, the eggs of which hatch almost simultaneously with those of
mosquitoes. Cold early spring temperatures and short-term ice cover do not seem to
have a negative impact on this species, whose primary prey appears to be mosquito
larvae (James 1961).

As temperatures warm in mid to late April, more species--chiefly predators--make
their appearance within the ponds. Dragonflies and darnselflies (Sympetrum and Lestes)
present as eggs laid within the basin the previous summer, hatch out as very small

individuals and consume small crustaceans during their early instars. Eggs of a

16

predatory caddisfly, Polycentropis crassicorm's (Polycentropidae), hatch in late April,
and the larvae initially feed on small crustaceans that become trapped in the caddisflies'
silken retreats constructed within the leaf litter (Higgins, unpubl. data). Adult water
striders (Gerridae) and backswimmers (Notonectidae) that overwintered in permanent
water recolonize these temporary environments, and begin breeding at this time, as do
several species of beetles (e.g., Dytiscidae: Acilius, Colymbetes, Dytiscus, Rhantus;
Hydrophilidae: Hydrochara, Hydrochus, Tropistemus; Gyrinidae: Gyrinus). Eggs of
chorus frogs (Pseudacris triseriata) and salarnanders (Ambystoma) that were laid in the
ponds in late March or early April hatch by late April. Ambystoma larvae are the only
important vertebrate predators in temporary woodland ponds.

Adult mosquitoes begin to emerge from the ponds in early to mid-May of most years.
By this same time, fairy shrimp have completed development, deposited eggs, and died.
Limnephilid caddisflies, which have been feeding continuously on leaf detritus for two
months, reach their final instar by the middle of the month and begin pupating in late
May. With the emergence of mosquitoes, the pupation of caddisflies, and the
disappearance of fairy shrimp, the invertebrate fauna becomes dominated by predatory
species in late May. In addition to the species listed above, other migrants arrive,
including giant water bugs (Belostomatidae), broad-shouldered water striders
(Veliidae), water boatmen (Corixidae), water scorpions (Nepidae), and some additional
beetle species. In addition, migratory green damer dragonflies (Anaxjunius) oviposit in
large temporary ponds in April and May, and the voracious predatory larvae can become
quite abundant in some ponds by mid-May. Phantom rnidge larvae (Chaoborus) also

become abundant at this time. Many of these migrants are opportunistic and are not

17

particularly adapted for ephemeral habitats, except that they are all characterized by
rapid larval development.

There are few changes in the invertebrate fauna] composition in June. With the
advent of warm temperatures and less precipitation, the surface area and volume of
these ponds begin to shrink, with concomitant increases in organism densities and
nutrient concentrations. As the abundant predatory species increase their body sizes,
shifts in their preferred prey may drastically alter relative abundances within the fauna]
assemblages. The general paucity of non-predatory macroinvertebrates at this time of
the year means that predators are feeding on predators, and food webs may become very
complex.

Adult Sympetrum dragonflies and Lestes damselflies begin emerging from the ponds
by July 1, and Anax dragonflies emerge in mid- to late July from the larger ponds. By
mid— July, most of the medium-sized ponds have dried, and the larger ponds have
shrunk to only a small fraction of their maximum size. By this time, almost all insects
have completed larval development and emerged as adults, and cladocerans have
produced abundant ephippia, or drought-resistant eggs. The active invertebrate fauna at
this time is characterized by adult insects (primarily bugs and beetles) capable of flying
to permanent water, as well as other invertebrates that can burrow into the moist soil
and/or form a drought-resistant stage (e. g., gastropods, planarians, and ostracods).

Even the largest of the temporary woodland ponds usually lose all surface water by
early August. Undoubtedly, there are some insect larvae that do not complete
development by this time and perish. In drought years, even insects that are well
adapted to ephemeral habitats may become stranded. In most years, however, insects

that perish from dessication are either typical temporary pond migrants (i.e., Group 4 of

18

Wiggins et al. 1980) that failed to complete development, or they represent oviposition
mistakes by insects more typical of permanent water. An example of this latter category
is the presence of early-instar dragonfly larvae of the genera Libellula and Aeshna in
some of the larger temporary ponds during the summer. These insects are typical
residents of permanent ponds and most species require at least one year for larval
development. In years of high precipitation in which some of the usually temporary
ponds do not dry, these insects may survive and complete development the following
year. The usual consequence of such oviposition mistakes, however, is complete larval
mortality (Higgins, unpubl. data).
SEASONAL PATTERNS—AESTIVAL PHASE

In most years, heavy precipitation during the mid to late summer can cause dry (or
nearly dry) basins to flood again, triggering another cycle of invertebrate activity. The
surface area of flooding during this aestival phase is generally less than half that of the
much more extensive vernal phase. There are a few invertebrates that appear to be
specifically adapted to this later period of flooding. The floodwater mosquitoes, Aedes
vexans and Aedes trivittatus, as well as mosquitoes in the genus Psorophora are
particularly well-adapted to summer rain pools. Although some eggs may hatch in the
spring along with other species of Aedes, most A. vexans and A. trivittatus eggs, and all
those of Psorophora, hatch following reflooding in the summer (Carpenter and LaCasse
1955). Unlike spring species of Aedes that oviposit primarily near the margins of the
vernal extent of flooding, A. vexans also oviposits extensively in the interior portions of
pond basins (Enfield and Pritchard 1977), a strategy that ensures hatching during
summer flood events. Development is extremely rapid, with first-instars appearing

within a few hours of flooding and adults emerging in less than a week. Densities of A.

19

vexans larvae can reach several hundred per liter in these habitats (Dixon and Brust
1972), and the large number of biting adult females that emerge make this species a
serious pest of humans during the summer (Carpenter and LaCasse 1955; Wood et al.
1979). Another species of mosquito, Psorophora ciliata, that may have co-evolved
with A. vexans, is predatory in larval instars II-IV, feeding primarily on A. vexans larvae
(Breeland et al. 1961).

Other inhabitants of these aestival pools are either permanent residents (e. g., small
crustaceans, planarians, gastropods), or opportunistic migrants (e.g., Anopheles
mosquitoes, several species of beetles and bugs). This latter group includes adult
insects of species typical of more permanent water, some of which may oviposit and
attempt to complete an addtional generation in these summer rain pools. While some of
these migrants appear within 1 or 2 days of flooding (e.g., Anopheles mosquitoes),
predatory beetle larvae (e. g., Acilz'us), as well as most other predators, do not appear
until several days after inundation. This lag time between inundation and the
appearance of predators allows the rapidly-developing mosquito larvae to feed and grow
relatively unmolested. Drought-resistant eggs that were deposited by insects and other
arthropods that are well-adapted to temporary ponds do not hatch at this time because
they require a cold period followed by a warm-up in order to break their diapause
(Horsfall and Fowler 1961; Wiggins et al. 1980). In addition, most of these eggs are
deposited near the margins of the vernal extent of flooding and are not inundated by
summer flood events.

The aestival phase is usually very brief, with surface water persisting for only a
month or less. Animals that are specifically adapted to aestival pools, such as the

mosquito species listed above, must be capable of extremely rapid development for this

20

life history strategy to be successful. This strategy can be viewed as an evolutionary
tradeoff between risks and benefits. Although there is the risk of desiccation before
larval development is completed, the larvae occupy a warm, nutrient-rich, and relatively
predator-free environment in which development can occur rapidly.

TROPHIC RELATIONSHIPS

Temporary woodland ponds are detritus-based, heterotrophic habitats, with energy
flow stemming predominantly from the leaf litter that falls into the basins. Emergent,
submergent, and floating vascular plants are not common, and thus contribute little to
the overall energy budget. Although primary production in the form of algal
photosynthesis takes place, the intense shading by the surrounding woods in these ponds
reduces its input compared with more open bodies of water, particularly later in the
spring (Moore 1970). Algal production that occurs in the early spring prior to tree leaf-
out, however, may provide a significant food source for filter-feeding organisms (e.g.,
cladocerans).

Leaf litter that falls into the dry basins in the autumn is initially colonized by
terrestrial microbes (principally fungi) that begin the process of decomposition.
Barlocher et al. (1978) examined protein and fungal biomass levels in experimental leaf
packs placed in vernal pools in Ontario. Higher protein levels (corresponding to higher
levels of fungal biomass) were observed in leaf packs that were exposed to terrestrial
microbes and aerobic decomposition compared with leaf packs that were submerged in
water for the same period of time. All protein levels declined rapidly, however,
following submergence in the spring. The authors concluded that the protein-rich
detritus of temporary ponds supports the required rapid development of animals that

inhabit these ephemeral environments (Barlocher et al. 1978).

21

The rapid decline in leaf litter protein levels following submergence observed by
these researchers suggests, however, that there is more than just hi gh-protein detritus
supporting temporary pond fauna through larval development. The relative paucity of
shredding detritivores in these habitats (Figure 2), compared with many lotic situations,
also suggests that other trophic pathways may be more important than direct feeding on
leaf litter. Indeed, the early spring fauna is characterized by a diverse filter-feeding
guild comprised of cladocerans, ostracods, fairy shrimp, and—at least part time—
mosquito larvae. Larvae of Aedes mosquitoes, in addition to filtering micro-organisms
and detritus from the water column, are also known to graze biofilm from the surfaces
of leaf litter (Merritt et al. 1992). These larvae can apparently grow equally well
filtering pond water alone as they can when provided with detritus on which to graze. In
a field experiment conducted in 1996, we examined the growth of 30 first-instar
mosquito larvae (Aedes stimulans) in each of 15 microcosms provisioned with either
conditioned leaves, non-conditioned leaves, or no leaves. No difference in time to adult
emergence or adult weight was observed among the three treatments (Table 2). Walker
and Merritt (1988) reported similar results with the treehole mosquito, Aedes
triseriatus). These results suggest an abundance of planktonic food sources of at least
equal importance to the trophic hierarchy as the enriched leaf detritus. But are the two
related?

It has been demonstrated that the degree of microbial colonization of leaf litter plays
an important role in subsequent growth rates of invertebrate detritivores in both
terrestrial and aquatic habitats (e.g., Barlocher et al. 1978; Suberkropp et al. 1983;
Lawson et al. 1984; Merritt et al. 1984; Arsuffi and Suberkropp 1989; Walker et al.

1997). The dry phase of temporary ponds appears to be the most important period of

22

 

Scrapers
em Shredders
|:l Filterers

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Figure 2. Functional feeding group composition (by genera) of invertebrates in
temporary woodland ponds.

16.7%
Group1
21.7% - Group2
C Group 3

 

Figure 3. Predator composition by life history strategy in temporary woodland ponds.

23

 

 

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microbial colonization of leaf litter, due to the prevalence of terrestrial fungi as the
major decomposers (Barlocher et al. 1978). This microbial colonization process begins
as soon as water levels begin to decline in the late spring or summer. As a pond loses
surface water and shrinks in size, the leached-out and highly-recalcitrant leaf detritus
from the previous year becomes exposed and the moist surfaces are rapidly colonized by
a host of fungi, bacteria, and protozoa. The celluloses and hemicelluloses contained in
the leaves are principally exploited by terrestrial fungi, which depolymerize these
complex compounds via cellulolytic enzymes into simpler carbohydrates (Ljungdahl
and Eriksson 1985). Terrestrial fungi, principally white-rot fungi, are also important in
breaking down lignin, which binds to the celluloses and hemicelluloses in leaves
(Ljungdahl and Eriksson 1985). Although some lignin degradation occurs during the
aquatic phase (Chamier 1985), the process is slow compared to that which occurs during
the terrestrial phase, and much of the celluloses and hemicelluloses remain bound and
unavailable for enzymatic degradation (Webster and Benfield 1986). The leaf surfaces
are also colonized during this terrestrial phase by bacteria and their protozoan predators
(Bamforth 1977), many of which secrete extracellular compounds (Nalewajko 1977). A
similar colonization occurs on leaves that fall into the dry basins in the autumn. In this
way, the complex structure of the leaves is slowly converted into microbial biomass.

It is suggested here that when the ponds reflood in the spring to their maximum size
(and when they partially reflood in the summer to form aestival ponds), the heavily-
enriched surfaces of the leaf detritus provide a nutrient broth in the form of dissolved
and fine particulate organic matter stemming from the inundated fungal biomass, by-
products of lignin degradation (Kirk 1984), partially degraded celluloses, and the

biomass and extracellular compounds of bacteria and protozoa. These dissolved

25

substances, principally dissolved organic carbons and nitrogens (DOC and DON), are
used by planktonic and attached heterotrophic bacteria, and a microbial bloom ensues.
At this same time, algal growth may also be stimulated from DON and the sunlight
available before trees leaf out in the spring. The resulting growth in the microbial
community, in turn, supports the vast filter-feeding guild characteristic of the early
spring fauna of temporary woodland ponds. In addition, following inundation, aquatic
hyphomycetes readily colonize and degrade the dead terrestrial fungal cells (which
contain little or no lignin), resulting in a substantially higher biomass of hyphomycetes
and associated micro-organisms than would be possible with the recalcitrant leaf
detritus alone (Chamier 1985). This helps support invertebrate scrapers and gathering
collectors, as well as shredding detritivores.

Trophic relationships within temporary woodland ponds are closely tied to the
seasonal succession and adaptational strategies (Table 1) of the associated fauna.
Animals with drought-resistant stages may begin/resume development soon after the
ponds reflood, triggered by physio-chemical cues within the water(Horsfall 1956;
Horsfall and Fowler 1961). The organisms that initially appear early in the spring are
generally those that take advantage of the microbially-enriched water and detritus, i.e.,
filter-feeders, gathering collectors (e.g., certain chironomid midge larvae), and
detritivorous shredders (primarily limnephilid caddisflies). These species can
apparently tolerate the low temperatures and frequent ice cover characteristic of this
time of the year. Even though growth is slower in this cold environment (Atkinson
1994), development occurs in a relatively nutrient-rich and predator-free environment.
This strategy of beginning development early in the spring may have initially evolved as

an adaptation for survival in small, ephemeral habitats. A reinforcing factor may have

26

been predator avoidance in time. By hatching early, organisms such as mosquito larvae
and fairy shrimp--animals with few defensive mechanisms--feed and grow relatively
unmolested by predators. The majority of predators do not appear until weeks later. By
the time most of the predatory larvae of the odonates and beetles make their appearance,
these potential prey species are generally too large for the small, early-instar predators to
effectively catch. Insects that develop in cold temperatures reach larger body size than
those reared at higher temperatures (Brust 1967; Atkinson 1994), and the larvae of
spring species of Aedes are some of the largest in this genus (Wood et al. 1979). Thus,
the early spring inhabitants of temporary ponds may escape predation in time by
beginning development early, and by achieving larger body sizes than their potential
predators. As previously stated, only some dytiscid beetles in the genus Agabus that
overwinter in the egg stage have apparently evolved to take advantage of the abundant
prey available early in the spring. By beginning development early in the spring, larvae
of these beetles are able to exploit even small ponds of only a few weeks duration,
habitats unavailable for other beetle species that appear later in the season.

Although there are relatively few predators early in the spring, the number of
predatory species increases substantially as the water temperature rises. Predator
diversity reaches its peak in mid-May, with predators often becoming the dominant
functional group within the ponds at this time. Most predators in temporary woodland
ponds can be classified as either opportunistic migrants (Group 4 of Wiggins et al.
1980) or cyclic colonizers (Batzer and Wissinger 1996; Wissinger 1997), i.e., they
generally lack specific adaptations to survive drought and overwinter in permanent-

water habitats. Figure 3 illustrates that over half the predatory genera found in these

27

ponds belong to this life history category. More striking perhaps is the very high
proportion of predators within the Group 4 category itself (Figure 4). The dominance of
predators in this category is not terribly surprising given that animals in this group must
recolonize ponds every year, breed, and complete larval development before the ponds
dry. The consumption of animal protein allows the larvae of these relatively late-
arrivals to develop very quickly, the assimilation efficiency of predators being highest
among trophic groups (Wotton 1994). Relatively rapid development is a characteristic
of most animals breeding in ephemeral habitats, particularly those organisms that lack
adaptations for coping with the dry phase.

Conversely, this probably explains the total lack of shredding detritivores exhibiting
a Group 4 strategy (Figure 4). Although the leaf litter of temporary ponds may be
enriched by the microbial processes described above, it is still a relatively poor food
source, and detritivorous animals must consume large quantities to maintain growth.
One of the few shredding insects, the caddisfly Limnephilus indivisus, begins
development early in the spring-sometimes hatching the previous fall in autumnal
ponds (Wiggins l973)--a strategy which helps to ensure that the 8-10 week development
will be completed before the pond dries. For a migrant species that arrives at a pond
later in the spring, a feeding strategy based on consuming leaf detritus would be risky;
growth would be slow and there would often be insufficient time to complete
development. Interestingly, limnephilid caddisfly larvae in temporary ponds are known
to be occasionally cannibalistic (W issinger et al. 1996), and have been reported to be
infrequent predators of mosquito larvae (Downe and West 1954; Baldwin et al. 1955).
Cargill et al. (1985) demonstrated the importance of lipids in the diet of final-instar

shredding caddisflies. The accumulation of triglyceride reserves during the last larval

28

 

E Filterers
Gatherers

Predators

n= 39

 

Figure 4. Functional feeding group composition for Wiggins et al. (1980) Group 4 life
history strategy.

29

instar is apparently essential for completion of the larval stage and for subsequent adult
reproduction (Cargill et al. 1985). Although lipids are available in aquatic hyphomycete
fungi (Cargill et al. 1985), incidences of cannibalism and predation in otherwise
detritivorous insects may be a means of quickly acquiring lipids as well as protein. This
diet supplementation of protein and essential lipids may provide a boost in growth rates
and ensure survival through the larval period (Wissinger et al. 1996).
CONCLUSIONS

In summary, temporary woodland ponds are small, microbially-driven wetlands that
may be flooded from a few weeks to several months out of the year. What may initially
appear as a harsh and uncertain habitat actually exhibits a reasonably predictable cycle
of flooding and drying, as well as a fairly predictable seasonal succession of species.
Invertebrates that are well adapted to this ephemeral habitat have evolved within the
constraints of the physical environment and in response to community interactions
(Schneider and Frost 1996; Williams 1996). Both abiotic and biotic factors appear to
have shaped the observed succession of species, with early-season, cold-adapted
inhabitants simultaneously taking advantage of the microbially-enriched environment
and minimizing predation pressure by beginning development before most of the
predators appear. Many of the insects that arrive later in the spring are migrants with no
special adaptations to the dry phase of these ponds. The vast majority of these species
are predatory in at least the larval stage, employing a trophic strategy that permits rapid

growth in a shrinking environment.

30

REFERENCES

Arsuffi, T. L. and K. Suberkropp. 1989. Selective feeding by shredders on leaf-
colonizing fungi: Comparison of macroinvertebrate taxa. Oecologia 79: 30-37.

Atkinson, D. 1994. Temperature and organism size--a biological law for ectotherrns?
Advances in Ecological research 25: 1-57.

Baldwin, W. F., H. G. James, and H. E. Welch. 1955. A study of mosquito larvae and
pupae with a radio-active tracer. Canadian Entomologist 87: 350—356.

Bamforth, S. S. 1977. Litter and soils as freshwater ecosystems, p. 243-256. In [ed.],
J .Jr.Caims, Aquatic Microbial Communities. Garland. New York.

Barlocher, F., R. J. Mackay, and G. B. Wiggins. 1978. Detritus processing in a
temporary vernal pool in southern Ontario. Archiv fiir Hydrobiologie 81: 269-
295.

Batzer, D. P. and K. A. Sion 1999. Autumnal woodland ponds of western New York:
Temporary habitats that support permanent water invertebrates, p. 319-332. In
[eds.], D.P.Batzer, R.B.Rader, and S.A.Wissinger, Invertebrates in Freshwater
Wetlands of North America: Ecology and Management. John Wiley and Sons.
New York.

Batzer, D. P. and S. A. Wissinger. 1996. Ecology of insect communities in nontidal
wetlands. Annual Review of Entomology 41: 75-100.

Breeland, S. G., W. E. Snow, and E. Pickard. 1961. Mosquitoes of the Tennessee valley.
Journal of the Tennessee Academy of Science 36: 249-319.

Brust, R. A. 1967. Weight and development time of different stadia of mosquitoes
reared at various constant temperatures. Canadian Entomologist 99: 986-993.

Cargill, A. S., K. W. Cummins, B. J. Hanson, and R. R. Lowry. 1985. The role of lipids
as feeding stimulants for shredding aquatic insects. Freshwater Biology 15: 455-
464.

Carpenter, S. J. and W. J. LaCasse. 1955. Mosquitoes of North America. University of
California Press. Berkeley, CA.

Chamier, A. C. 1985. Cell-wall degrading enzymes of aquatic hyphomycetes: A review.
Botanical Journal of the Linnean Society 91: 67-81.

Dixon, R. D. and R. A. Brust. 1972. Mosquitoes of Manitoba III: Ecology of larvae in
the Winnipeg area. Canadian Entomologist 104: 961-968.

31

Downe, A. E. R. and A. S. West. 1954. Progress in the use of the precipitin test in
entomological studies. Canadian Entomologist 86: 181-184.

Enfield, M. A. and G. Pritchard. 1977. Estimates of population size and survival of
immature stages of four species of Aedes (Diptera: Culicidae) in a temporary
pond. Canadian Entomologist 109: 1425-1434.

Horsfall, W. R. 1956. Eggs of floodwater mosquitoes (Diptera: Culicidae). III.
Condition and hatching of Aedes vexans. Annals of the Entomological Society of
America 49: 66-71.

Horsfall, W. R. and H. W. Jr. Fowler. 1961. Eggs of floodwater mosquitoes VIII. Effect
of serial temperatures on conditioning of eggs of Aedes stimulans Walker
(Diptera: Culicidae). Annals of the Entomological Society of America 54: 664-
666.

Iversen, T. M. 1971. The ecology of a mosquito population (Aedes communis) in a
temporary pool in a Danish beech wood. Archiv fur Hydrobiologie 69: 309-332.

James, H. G. 1961. Some predators of Aedes stimulans (Walk.) and Aedes trichurus
(Dyar) (Diptera: Culicidae) in woodland pools. Canadian Journal of Zoology -
Journal Canadien de Zoologie 39: 533-540.

James, H. G. 1966. Location of univoltine Aedes eggs in woodland pool areas and
experimental exposure to predators. Mosquito News 26: 59-63.

Kenk, R. The animal life of temporary and permanent ponds in southern Michigan. (71).
1949. University of Michigan, Museum of Zoology. Miscellaneous Publication.

Kirk, T. K. 1984. Degradation of lignin, p. 399—437. In [ed.], D.T.Gibson, Microbial
Degradation of Organic Compounds. Marcel Dekker. New York.

Lawson, D. L., M. J. Klug, and R. W. Merritt. 1984. The influence of the physical,
chemical, and microbiological characteristics of decomposing leaves on the
growth of the detritivore Tipula abdominalis (Diptera: Tipulidae). Canadian
Journal of Zoology - Journal Canadien de Zoologie 62: 2339-2343.

Ljungdahl, L. G. and K.-E. Eriksson. Ecology of microbial cellulose degradation.
Marshall, K. C. (8), 237-299. 1985. New York, Plenum. Advances in Microbial
Ecology.

Ref Type: Serial (Book,Monograph)

Merritt, R. W., R. H. Dadd, and E. D. Walker. 1992. Feeding behavior, natural food,
and nutritional relationships of larval mosquitoes. Annual Review of
Entomology 37: 349-376.

32

Merritt, R. W., W. Wuerthele, and D. L. Lawson. 1984. The effect of leaf conditioning
on the timing of litter processing on a Michigan woodland floodplain. Canadian
Journal of Zoology - Journal Canadien de Zoologie 62: 179-182.

Moore, W. G. 1970. Limnological studies of temporary ponds in south-eastern
Louisiana. Southwestern Naturalist 15: 83-110.

Nalewajko, C. 1977 . Extracellular release in freshwater algae and bacteria: Extracellular
products of algae as a source of carbon for heterotrophs, p. 589-624. In [ed.],
J .Jr.Cairns, Aquatic Microbial Communities. Garland. New York.

Schneider, D. W. 1999. Snowmelt ponds in Wisconsin: Influence of hydroperiod on
invertebrate community structure, p. 299-318. In [eds.], D.P.Batzer, R.B.Rader,
and S.A.Wissinger, Invertebrates in Freshwater Wetlands of North America:
Ecology and Management. John Wiley and Sons. New York.

Schneider, D. W. and T. M. Frost. 1996. Habitat duration and community structure in
temporary ponds. Journal of the North American Benthological Society 15: 64-
86.

Suberkropp, K., T. L. Arsuffi, and J. P. Anderson. 1983. Comparison of degradative
ability, enzymatic activity, and palatability of aquatic hyphomycetes grown on
leaf litter. Applied and Environmental Microbiology 46: 237-244.

Walker, E. D. 1995. Effect of low temperature on feeding rate of Aedes stimulans larvae
and efficacy of Bacillus thuringiensis var. israelensis (H-14). Journal of the
American Mosquito Control Association 11: 107-110.

Walker, E. D., M. G. Kaufman, M. P. Ayres, M. H. Riedel, and R. W. Merritt. 1997.
Effects of variation in quality of leaf detritus on growth of the eastern tree-hole
mosquito, Aedes triseriatus (Diptera: Culicidae). Canadian Journal of Zoology -
Journal Canadien de Zoologie 75: 706-718.

Walker, E. D. and R. W. Merritt. 1988. The significance of leaf detritus to mosquito
(Diptera: Culicidae) productivity from treeholes. Environmental Entomology 17:
200-206. -

Webster, J. R. and E. F. Benfield. 1986. Vascular plant breakdown in freshwater
ecosystems. Annual Review of Ecology and Systematics 17: 567-594.

Westwood, A. R., G. A. Surgeoner, and B. V. Helson. 1983. Survival of spring Aedes
spp mosquito (Diptera: Culicidae) larvae in ice-covered pools. Canadian
Entomologist 115: 195-197.

Wiggins, G. B. 1973. A contribution to the biology of caddisflies. Life Science
Contributions of the Royal Ontario Museum 88: 1-28.

33

Wiggins, G. B., R. J. Mackay, and I. Smith. 1980. Evolutionary and ecological strategies
of animals in annual temporary pools. Archiv fur Hydrobiologie, Supplement 58:
97-206.

Williams, D. D. 1987. The Ecology of Temporary Waters. Croom Helm, Timber Press.
Portland, OR.

Williams, D. D. 1996. Environmental constraints in temporary fresh water and their
consequences for the insect fauna. Journal of the North American Benthological
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Wissinger, S. A. 1997. Cyclic colonization in predictably ephemeral habitats: A
template for biological control in annual crop systems. Bilogical Control 10: 4-
15.

Wissinger, S. A., G. B. Sparks, G. L. Rouse, W. S. Brown, and H. Steltzer. 1996.
Intraguild predation and cannibalism among larvae of detritivorous caddisflies in
subalpine wetlands. Ecology 77: 2421-2430.

Wood, D. M., Dang, P. T., and Ellis, R. A. 1979. The mosquitoes of Canada (Diptera:
Culicidae). The Insects and Arachnids of Canada, Part 6. Publication 1686.
Ottawa, Ontario, Canada, Biosystematics Research Institute, Research Branch,
Agriculture Canada.

Wotton, R. S. 1994. Particulate and dissolved organic matter as food, p. 235-288. In
[ed.], R.S. Wotton, The Biology of Particles in Aquatic Systems. Lewis. Boca
Raton, FL.

34

CHAPTER 2
FEEDING ECOLOGY OF AEDES STIMULANS (WALKER) MOSQUITO LARVAE

IN TEMPORARY WOODLAND PONDS

ABSTRACT

The larval feeding ecology of a common vernal pool mosquito, Aedes stimulans
(Walker) was studied using field microcosms and through quantitative analysis of larval
gut samples. In addition, a comparison was made of the food of larvae from two very
different vernal habitats, a small woodland vernal pool and a larger woodland pond.
The microcosm experiments took place in the larger pond and were designed to
examine the importance of grazing versus filtering for larval A. stimulans through the
presence or absence of a grazeable substrate, testing for effects on survival, days to
eclosion, and adult weight. No differences were observed, indicating that A. stimulans
larvae in the larger pond were capable of obtaining adequate food from filtering the
water column alone. Analysis of guts from the microcosm treatments indicated that
larvae in the treatment with little grazeable substrate were consuming high quality
flagellate phytoplankton from the water column. The ingestion of these algae was
probably responsible for the sustained growth and survival of the mosquitoes. Analysis
of both water and larval gut samples from the small vernal pool indicated that primary
production is minimal in this habitat. Grazing microbially-colonized surfaces in this
smaller, less-productive environment may be necessary due to the paucity of algae.

Small vernal pools are probably more abundant on the landscape than larger ponds, and

35

grazing by A. stimulans larvae may be an adaptation for growth and survival in these
less-productive and very ephemeral habitats.
INTRODUCTION

Temporary vernal pools are the larval habitats for many species of spring Aedes
mosquitoes. In addition to being a nuisance to humans, the biting adults that emerge
from these small pools and ponds are also potential vectors of disease, primarily
LaCrosse and Jamestown Canyon encephalitis (Harwood and James 1979). The large
numbers of mosquitoes produced by these small, ephemeral habitats (Enfield and
Pritchard 1977) indicate that these ponds contain abundant larval food resources.
Larvae of Aedes mosquitoes filter suspended material from the water column, but also
spend considerable time grazing the biofilm from substrates (Horsfall 1955; Ameen and
Iversen 1978; Merritt et al. 1992; Clements 1992). It has been generally assumed that
larval grazing is a necessary component of mosquito feeding and growth (Fish and
Carpenter 1982). Temporary woodland ponds contain abundant leaf detritus, and the
microbial degradation of this leaf litter is believed to drive much of the energy flow
within these systems (Barlocher et al. 1978). The role of leaf litter in the growth and
survival of larval mosquitoes has been examined in detail for small container habitats
such as treeholes (Fish and Carpenter 1982; Carpenter 1983; Walker and Merritt 1988;
Walker et al. 1991; Merritt et al. 1992; Leonard and Juliano 1995; Walker et al. 1997;
Aspbury and Juliano 1998), but has received relatively little attention with regard to
other larval mosquito habitats (however, see Hinman 1930, Howland 1930). The role of
leaf detritus in treehole ecosystems has proven to be complex. Leaves are colonized by

microbes, which may then be grazed by mosquito larvae (Fish and Carpenter 1982), but

36

leaves may also provide dissolved nutrients important for the growth of bacteria within
the water column, which could be filtered by larvae (Walker and Merritt 1988; Walker
et al. 1991; Merritt et al. 1992; Kaufman et al. 1999).

The objective of this research was to study the larval feeding ecology of a common
vernal pool mosquito, Aedes stimulans (Walker), and examine the role of leaf detritus in
survival, growth, and subsequent adult fitness. I hypothesized that larvae furnished
with leaves on which to graze will exhibit increased survivorship, growth, and adult
fitness compared to larvae without a suitable substrate on which to graze. I also
compared the food of larvae from 2 very different vernal ponds.

MATERIALS AND METHODS
Study Sites

Feeding experiments were conducted at Wild Ginger #1 Pond (WG-l), which is a
temporary woodland pond near Haslett, Michigan, USA (42° 45' 30" N, 84° 23' 50" W).
This pond is approximately 600 m2 when completely flooded, with a maximum depth of
0.8 m. In an average year, the pond begins to fill with water during the late autumn, and
reaches its maximum size and depth in March from snowmelt and rainfall. The pond
loses all surface water by mid July or early August. Water temperatures for 1996-1998
ranged from 4° C in late March to 255° C in mid June (Figure 1). The basin is situated
within a 60-70 year-old deciduous woodlot of 70 ha and is surrounded by trees and
shrubs, primarily red maple (Acer rubrum), American elm (Ulmus americana), black
ash (F raxinus nigra), swamp white oak (Quercus bicolor), and northern swamp
dogwood (Camus racemosa). The canopy does not completely close over the pond, but

after the trees leaf out, most sunlight reaching the surface is indirect. Leaves from trees

37

NM
001

Temperature (°C)
3 61‘

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Temperature (°C
8 5?

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2-Mar

[01003
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Temperature (°C)
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001

25-Feb

1996

 

 

 

 

 

 

 

 

 

 

 

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1 4-May

1997

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13-Jun

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1

30-Jun

30-Jul

 

 

 

 

 

, $11.

 

(
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l

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26-Apr

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Figure 1. Water temperatures, Wild Ginger #1 Pond, 1996-1998.

38

I

25-Jul

near the basin and the surrounding upland (predominantly sugar maple and white oak)
contribute to the extensive detritus that provides the energy source for the temporary
pond community in the spring (Higgins and Merritt 1999). Wild Ginger #1 Pond
supports a diverse invertebrate community, including large numbers of mosquito larvae
in the early spring, with Aedes stimulans being the most abundant species.

Research was also conducted at a much smaller vernal pool, Hudson #1 Pond (HU-
1), on the campus of Michigan State University, East Lansing, Michigan, USA. This
pond covers an area of only 5 m2 when flooded in the early spring, with a maximum
depth of 0.5 m. From 1996-1999, the average duration of flooding was approximately 9
weeks, usually from late March through May. This small pool is situated in a mature
beech-maple woodlot and, like WG-l, receives abundant leaf litter. The pond is
completely shaded by the tree canopy when the trees leaf out in early May. In addition,
leaf litter nearly fills the pond from top to bottom, further hindering light penetration.
The invertebrate community of HU-l is depauperate in comparison to WG-l,
dominated by Aedes stimulans mosquito larvae and ostracods.
Microcosms

A field microcosm experiment to study the role of leaf litter in larval mosquito diets
was conducted in WG-l in 1996-1998. Microcosms were constructed from 4 1 food-
grade plastic containers measuring 17 cm in diameter at the top and tapering to 15 cm at
the base (Figure 2). A hole 10 cm in diameter was cut in the base and two holes 10 x 10
cm were cut in the sides near the top. These holes were then covered with 250 um
N ytex nylon mesh. Curved Styrofoam pieces were glued between the upper holes and

the top of the containers to keep the microcosms afloat (Figure 2). When placed in the

39

 

 

 

 

 

 

 

 

 

 

 

 

Figure 2. Diagram of floating microcosm used in field experiment. a) 4 1 plastic

container, b) 250 um Nytex mesh on sides and bottom, c) Styrofoam floats,

d) nylon fishing line to anchor microcosm, e) garden stake, f) water surface,
g) substrate.

40

water the holes at the bottom and sides permitted pond water and most microbes to
enter the microcosm, but excluded most invertebrates and kept mosquito larvae inside.
Fifteen microcosms were placed into 60-70 cm deep water within WG-l and anchored
in place with garden stakes and fishing line. The microcosms were placed in groups of
3, representing the 3 treatments, to insure that each treatment within a group was
exposed to similar micro-environmental conditions. In 1996, the treatments were 1) 3g
of dried senescent sugar maple (Acer saccharum) leaves; 2) 3g of sugar maple leaves
conditioned for 5 days in filtered (125 um) pond water, and 3) no leaves. In 1997 and
1998, I wished to control for the potential build-up of biofilm inside the microcosms so
the three treatments were: 1) 3g of dried leaves, 2) no leaves, with weekly replacement
of the microcosm with a clean, dry one, and 3) no leaves and no microcosm
replacement.

First instar (< 1 (1 old) Aedes mosquito larvae were collected from WG-l, and 30
were placed into each microcosm. It was not possible to make field identifications of
mosquito larvae at that time, but all were subsequently identified (as adults or larvae) as
Aedes stimulans. A plastic cover with 250 um nylon mesh was placed over each
microcosm to minimize the input of other detritus falling from the canopy above and to
prevent predators from flying/crawling into the microcosms. When the microcosms
were replaced each week in 1997 and 1998, larvae within the other treatments were also
transferred briefly to another container and then returned to their original microcosm.
This was done to minimize any effect of handling. When the larvae pupated, they were
placed into small 0.5 l microcosms attached to the larger microcosms. These pupal

containers were checked daily and adult mosquitoes, when present, were collected by

41

microcosm and separated by date of emergence. Adults were immediately chilled in ice
to minimize damage, and killed by freezing at -4° C. Each adult was subsequently
identified to the species level, dried at 50° C for 48 h, and weighed to the nearest
0ng with a Cahn micro-balance.
Water and mosquito gut samples

Water column samples from WG-l and HU-l were collected on a monthly basis
(early April and early May) for analysis of the microbial community. Water (2.5 ml)
was collected with sterile pipettes, preserved immediately in 37% formaldehyde
solution (final concentration 4%), and stored at 4° C. Five samples were collected each
month. Samples were diluted 1:1 with deionized water and stained with the fluorescent
dye 4'6-diamidino-2-phenylindole (DAPI) at a concentration of 30 rig/ml. In 1998, 5
fourth-instar larvae were collected from each treatment from one group of microcosms
(designated a priori for such use), and 5 fourth instars were collected from HU-l.
Following procedures outlined in Walker et al. (1988), the larvae were killed in hot
water and preserved in 4% formaldehyde solution at 4° C. For each mosquito larva, the
entire gut, with the perithrophic membrane intact, was removed with forceps and
washed with deionized water. The contents of the gut was teased from the membrane
with minuten pins in a drop of deionized water on a sterile microslide. The entire
contents were pipetted into 2 ml of deionized water and shaken to dislodge particles.
Because of the relatively large amount of material in the gut samples, only 1 ml of each
sample (representing one-half gut) was processed, and subsequent counts were doubled.
Using the procedures described by Hobbie et al. (1977) and Porter and Fei g (1980),

after staining with DAPI, gut and water samples were processed through a 0.22 pm

42

black filter (backed by a 0.45 pm HA Millipore filter) using low vacuum pressure. The
black filter was placed on a microslide that had been smeared with a thin layer of
immersion oil. A drop of immersion oil was placed on the filter and a glass cover slip
placed on top. All samples were stored in darkness at 4° C until counted. Algae were
counted with an ocular grid at 250X using a Jenaluma microscope fitted for
epifluorescence, a mercury lamp, and UV filter set. Bacteria were counted in a similar
manner at 1000X, and identified as rods or cocci. Detritus particles < 10 um were also
counted at 1000X.
Statistical Analysis

Each microcosm was treated as the experimental unit. I tested for treatment effects
on survival, days to adult emergence, and adult weight using a one-way analysis of
variance (ANOVA) with the general linear models (GLM) procedure in SAS (SAS
Institute 1990). Due to inherent differences between male and female mosquitoes in
emergence and adult weight, sexes were analyzed separately. For survival analysis,
sexes were combined, and proportions were analyzed using an arcsine transformation of
the square root.

RESULTS

Microcosm Experiments

The results of the 1996 field experiment are shown in Figure 3. There were no
differences in survivorship, days to adult emergence, or adult weight (Table 1). At the
conclusion of this experiment, a thin biofilm was noted on the inside surfaces of the
microcosms, including those with no leaves. Mosquito larvae certainly could have

grazed on this biofilm, which could have been an adequate substitute for the biofilm on

43

50%

40%

30%

20%

Percent Survival

10%

 

0%
Conditioned Non-conditioned No Leaves

 

01
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.h
0

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0.8

0.7
A 0.6
v 0.5
S 0.4
0.3
0.2
0.1

mg

Adult

 

Conditioned Non-conditioned No Leaves

Figure 3. 1996 field microcosm results. a). survival, b). days to emergence, c).
adult weight. Values are means and S.E.M.

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45

leaves in the other treatments. For this reason, the experimental design was altered the
second and third years to include the weekly replacement of microcosms in one of the
treatments with no leaves. While this did not totally eliminate microbial colonization of
the microcosm surfaces, it did minimize it. It was believed that more frequent
replacement would have subjected the larvae to increased handling stress. Also,
because the dried leaves quickly became conditioned inside the microcosms, the
conditioned-leaves treatment was dropped, keeping the number of treatments at 3.

The redesigned experiment was run in the spring of 1997. Unfortunately, a
prolonged cold period during the first half of May (Figure 1) resulted in very heavy
mortality of pupae in the microcosms. There was 100% mortality in 4 of 15
microcosms, and only 26 individuals survived to emerge as adults, with no microcosm
yielding more than 4 adult mosquitoes. Mortality appeared to have been heaviest on
females, perhaps due to their later pupation, with only 5 adult females emerging from
the 15 microcosms. Six microcosms yielded only males and one treatment (no leaves-
no microcosm replacement) yielded only 1 female. No analysis could be performed on
adult weight or development time due to the small numbers of surviving adults.
Analysis of survival data indicated that there were no differences in survival (p =
0.8995) among the 3 treatments.

In 1998, the experiment was repeated, again with weekly replacement of the
microcosms in one of the treatments. Although mosquitoes in the replacement
treatment were, on average, slightly smaller and took longer to emerge (Figure 4),
these differences were not statistically significant (Table 2). Survival also was not

significantly different among the 3 treatments.

46

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.3;

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Leaves No Ivs., no replac. No Ivs., replac.

Figure 4. 1998 field microcosm results. a). survival, b). days to emergence, c).
adult weight. Values are means and S.E.M.

47

 

 

 

 

 

 

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Water samples

Direct counts of algae, bacteria, and detritus for water samples from WG-l and HU-
1 are presented in Table 3. Protozoan numbers are not presented in this table as their
numbers were surprisingly very low (< 5 ml’l) in all samples. In addition, samples were
not collected from HU-l in 1996. While both ponds showed an increase and similar
numbers of bacteria from April to May, the paucity of planktonic algae in HU-l is
notable. As previously stated, this pond contains water for only 8-10 weeks out of the
year, and is heavily shaded by the forest canopy in May, conditions which may not be
conducive for algal survival and growth. In addition, a large amount of leaf litter nearly
fills the pond from top to bottom, further hindering light penetration. The dramatic
increase in bacteria numbers from April to May in HU-l may be attributed to the
shrinking volume of the pond. The amount of algae in WG-l remained fairly consistent
from season to season, and in each year showed an increase in numbers from April to
May.

One problem with comparing water samples by calendrical date among different
seasons is that the phenology of these small bodies of water is largely dependent on
hydrology (i.e., water volume) and temperature, which vary from year to year. For
example, in 1996, WG-l did not reach its maximum volume until the first week in
April, and HU-l was dry until that time. In 1998, both WG-l and HU-l reached their
maximum extent of flooding the first week in March. In addition, there were

differences in temperature between these two years (Figure 1).

49

Table 3. Direct counts of suspended material in water column samples using DAPI
stain and epifluorescence microscopy. Values are cells or particles ml'l (S.E.M.);
n = 5 for each sampling date.

 

Bacteria Detritus Algae
Rods Cocci
Wild Ginger #1
1996 April 1.83 x 106 3.56 x 105 1.08 x 106 1.04 x 105
(1.02 x 105) (2.32 x 104) (1.11 x 105) (2.08 x 104)
May 3.56 x 106 9.20 x 105 1.36 x 106 3.78 x 105
(1.65 x 105) (3.73 x 10“) (1.48 x 105) (1.89 x 10‘)
1997 April 2.37 x 106 2.51 x 105 9.23 x 105 1.29 x 105
(1.11 x 105) (1.39 x 104) (2.24 x 104) (1.62 x 104)
May 3.06 x 106 7.47 x 105 1.19 x 10‘5 3.11 x 105
(2.18 x 105) (3.76 x 104) (1.26 x 105) (2.36 x 104)
1998 April 2.79 x 106 4.49 x 105 1.25 x 106 1.71 x 105
(2.12 x 105) (3.22 x 10“) (2.03 x 105) (2.17 x 104)
May 4.51 x 106 1.02 x 106 1.94 x 106 4.19 x 105
(2.73 x 105) (8.44 x 10“) (1.81 x 105) (2.97 x 10‘)
Hudson #1
1997 April 3.42 x 106 4.12 x 105 2.24 x 106 82
(2.63 x 105) (3.69 x 104) (2.08 x 105) (21)
May 8.24 x 106 1.83 x 106 2.32 x 106 124
(5.12 x 105) (8.47 x 104) (1.19 x 105) (37)
1998 April 2.89 x 106 5.74 x 105 1.97 x 106 108
(1.32 x 105) (2.33 x 10“) (1.48 x 105) (19)
May 9.16 x 106 1.69 x 106 2.78 x 106 132
(4.05 x 105) (7.15 x 10“) (1.76 x 105) (29)

50

Mosquito gut samples

Direct counts of food particles from larval gut samples are presented in Table 4. Of
the larvae from the microcosms in WG-l, those from the treatment in which the
microcosms were replaced showed distinct differences in the number and types of algae
present in their guts. There were significantly fewer diatoms in these larvae compared
to the other two treatments (p < .001), and more flagellate algae (p < .05). All larvae
from each treatment contained abundant bacteria and detritus. The guts of larvae from
HU-l contained abundant detritus and bacteria, and, as expected, almost no algae
(Table 4).

DISCUSSION

The hypothesis that grazing leaf litter is necessary for growth and survival of Aedes
stimulans larvae, at least in WG-l pond, can be rejected. That there were no differences
in survivorship, days to eclosion, and adult weight among the 3 microcosm treatments
in 1998 indicates that A. stimulans larvae are capable of growth by filter feeding alone.
Larvae in the microcosm replacement treatment had very little material on which they
could graze, yet performed equally well as those in the other 2 treatments. Water
column samples from WG-l indicate abundant bacteria, detritus, and algae (Table 3),
and the gut contents of the microcosm-replacement larvae show that they were
consuming large quantities of all of these (Table 4). In addition, the predominance of
flagellate forms of algae in the guts of larvae in the replacement treatment suggests that
these were obtained by filter feeding. Chlamydomonas and Cryptophyceae
nannoplankton dominate the early season phytoplankton community in WG-l, and are

important food sources for the zooplankton community (see Chapter 3). These are

51

Table 4. Direct counts of food particles from guts of fourth larval instars of Aedes
stimulans. Values are means (11 = 5) of cells or particles gut'1 and (S.E.M.).

 

Bacteria
Rods

Cocci
Detritus
Algae

Diatoms

Flagellatesa

Other

 

Wild Ginger #1 Microcosms Hudson #1
Leaves N 0 Leaves, No No Leaves,
Replacement Replacement

2.62 x 106 2.19 x 106 2.45 x 106 3.11 x 106
(1.22 x 105) (1.67 x 105) (1.32 x 105) (1.77 x 105)
4.71 x 105 3.92 x 105 4.41 x 105 6.27 x 105
(2.29 x 10“) (3.01 x 10“) (2.78 x 10“) (4.23 x 10“)
2.37 x 106 2.55 x 106 1.69 x 10‘5 2.87 x 106
(1.17 x 105) (2.33 x 105) (1.52 x 105) (2.02 x 105)
430 314 26 0
(96) (81) (11)
138 188 396 2.4
(31) (34) (103) (0.75)

20 32 152 0

(7) (8) (19)

a Flagellates primarily include Chlamydomonas and Cryptophyceae nannoplankton.

52

considered highly edible and nutritious forms of algae, even more so than diatoms
(Schindler 1970; Porter 1973). The relatively large numbers of these flagellates in the
guts of the replacement-treatment larvae may be the key to their survival and growth.

These data are similar to those found by Ameen and Iversen (1978), who examined
gut contents and growth rates of Aedes communis and A. cantans from a temporary
woodland pond in Denmark. Although only relative proportions are presented, and
bacteria were not quantified in this study, gut contents of larvae were found to contain
abundant Chlamydomonas. In laboratory growth experiments, larvae consuming only
pond water grew at a somewhat slower rate than those provided with pond water and
"bottom substrate" (Ameen and Iversen 1978). In the pond water only treatment,
however, the water was changed only every second day, and the mosquito larvae
removed 57% of the algal biomass during that time period (Ameen and Iversen 1978).
Those short-term fluctuations in the food (algal) supply could have been responsible for
the observed differences between the two treatments. In the present study, the screened
openings in the microcosms allowed for a continuous influx of suspended material,
including algae, which was representative of that found in the pond as a whole.

If larval A. stimulans mosquitoes are capable of obtaining sufficient food by filter
feeding, why then do they graze? A clue may be provided by the data from HU-l. This
very ephemeral and heavily shaded pond contained very little algae (Table 3), and gut
samples of mosquito larvae from here are dominated by bacteria and detritus. In the
microcosm experiments in WG-l, larvae with little material on which to graze were
apparently able to receive adequate nutrition by ingesting suspended material,

particularly hi gh-quality algae. In HU-l, larvae did not have algae as a food source.

53

While they may be able to grow in such an environment by filter feeding bacteria and
detritus from the water column, grazing the biofilm on leaf surfaces probably provides
for faster growth in this very temporary habitat. The other invertebrate inhabitants of
HU-l include ostracods and a small population of amphipods, both essentially grazers.
Small, shallow vernal pools like HU-l are probably more abundant in the landscape
than larger ponds like WG-l. Aedes stimulans is common to all of these vernal habitats,
and grazing may be an adaptation for survival in the more common, but less productive
shallow pools. Ideally, the microcosm experiment should be repeated in small ponds
like HU-l, although the small, shallow nature of these pools would make such an
experiment difficult.

The role of leaf detritus in temporary woodland ponds systems is complex. While
there are a few detritivores that feed directly on leaves, the more indirect microbial
route appears to be more important (Barlocher et al. 1978; Higgins and Merritt 1999).
The release of dissolved organic carbon and nitrogen compounds from detritus drives
benthic and planktonic microbial growth, which, in turn, provides the foundation for
filtering and grazing guilds of invertebrates. In small ponds like HU-l with little
primary production, microbial colonization of leaves forms a biofilm that can be
exploited by a relatively small group of grazing invertebrates. In larger ponds that
receive sufficient light, the benthic grazing guild is accompanied by an extensive filter
feeding guild, with mosquito larvae exploiting both benthic and planktonic

environments.

54

REFERENCES

Ameen, M. and T. M. Iversen. 1978. Food of Aedes larvae (Diptera: Culicidae) in a
temporary forest pool. Archiv fiir Hydrobiologie 83: 552-564.

Aspbury, A. S. and S. A. Juliano. 1998. Negative effects of habitat drying and prior
exploitation on the detritus resource in an ephemeral aquatic habitat. Oecologia
115: 137-148.

Barlocher, F., R. J. Mackay, and G. B. Wiggins. 1978. Detritus processing in a
temporary vernal pool in southern Ontario. Archiv fiir Hydrobiologie 81: 269-
295.

Carpenter, S. R. 1983. Resource limitation of larval treehole mosquitoes subsisting on
beech detritus. Ecology 64: 219-223.

Clements, A. N. 1992. The Biology of Mosquitoes. Chapman and Hall. London.

Enfield, M. A. and G. Pritchard. 1977. Estimates of population size and survival of
immature stages of four species of Aedes (Diptera: Culicidae) in a temporary
pond. Canadian Entomologist 109: 1425-1434.

Fish, D. and S. R. Carpenter. 1982. Leaf litter and larval mosquito dynamics in tree-hole
ecosystems. Ecology 63: 283-288.

Harwood, R. F. and M. T. James. 1979. Entomology in Human and Animal Health, 7th.
ed. Macmillan. New York.

Higgins, M. J. and R. W. Merritt 1999. Temporary woodland ponds in Michigan:
Invertebrate seasonal patterns and trophic relationships, p. 279-297. In [eds.],
D.P.Batzer, R.B.Rader, and S.A.Wissinger, Invertebrates in Freshwater
Wetlands of North America: Ecology and Management. John Wiley and Sons.
New York.

Hinman, E. H. 1930. A study of the food of mosquito larvae (Culicidae). American
Journal of Hygiene 12: 238-270.

Hobbie, J. B., R. J. Daley, and S. Jasper. 1977. Use of Nuclepore filters for counting
bacteria by fluorescence microscopy. Applied and Environmental Microbiology
33: 1225-1228.

Horsfall, W. R. 1955 . Mosquitoes: Their Bionomics and Relation to Disease. Ronald
Press. New York.

Howland, L. J. 1930. Bionomical investigation of English mosquito larvae with special
reference to their algal food. Journal of Ecology 18: 81-125.

55

Kaufman, M. G., E. D. Walker, T. W. Smith, R. W. Merritt, and M. J. Klug. 1999.
Effects of larval mosquitoes (Aedes triseriatus) and stemflow on microbial
community dynamics in container habitats. Applied and Environmental

Microbiology [Appl.Environ.Microbiol.] 65: 2661-2673.

Leonard, P. M. and S. A. Juliano. 1995. Effect of leaf litter and density on fitness and
population performance of the hole mosquito Aedes triseriatus. Ecological
Entomology 20: 125-136.

Merritt, R. W., R. H. Dadd, and E. D. Walker. 1992. Feeding behavior, natural food,
and nutritional relationships of larval mosquitoes. Annual Review of
Entomology 37: 349-376.

Porter, K. G. 1973. Selective grazing and differential digestion of algae by zooplankton.
Science 244: 179-180.

Porter, K. G. and Y. S. Feig. 1980. The use of DAPI for identifying and counting
aquatic rnicroflora. Limnology and Oceanography 25: 943-948.

SAS Institute, Inc. 1990. SAS/STAT User's Guide, Version 6, 4th ed. Cary, N .C.

Schindler, J. E. 1970. Food quality and zooplankton nutrition. Journal of Animal
Ecology 40: 589-595.

Walker, E. D., M. G. Kaufman, M. P. Ayres, M. H. Riedel, and R. W. Merritt. 1997.
Effects of variation in quality of leaf detritus on growth of the eastern tree-hole
mosquito, Aedes triseriatus (Diptera: Culicidae). Canadian Journal of Zoology -
Journal Canadien de Zoologie 75: 706-718.

Walker, E. D., D. L. Lawson, R. W. Merritt, W. T. Morgan, and M. J. Klug. 1991.
Nutrient dynamics, bacterial populations, and mosquito productivity in tree hole
ecosystems and microcosms. Ecology 72: 1529-1546.

Walker, E. D. and R. W. Merritt. 1988. The significance of leaf detritus to mosquito
(Diptera: Culicidae) productivity from treeholes. Environmental Entomology 17:
ZOO-206.

Walker, E. D., E. J. Olds, and R. W. Merritt. 1988. Gut content analysis of mosquito
larvae (Diptera: Culicidae) using DAPI stain and epifluorescence microscopy.
Journal of Medical Entomology 25: 551-554.

56

CHAPTER 3
CLADOCERAN SUCCESSION IN A TEMPORARY WOODLAND POND IN

MICHIGAN: THE INFLUENCE OF PREDATION

ABSTRACT

Zooplankton and predator communities in a temporary woodland pond in southern
Michigan, USA were sampled on a weekly basis from March through mid-July, 1999.
Five species of cladocerans were recovered during this period. Early in the season, the
only cladoceran present was Daphnia ephemeralis. This species underwent sexual
reproduction and produced ephippial eggs in April, completing its life cycle for the
season. Two forms of Daphnia pulex were evident at different times. Beginning in
April, parthenogenetic D. pulex reached body sizes of 2.5-3.0 mm. This large early
form underwent sexual reproduction in May, producing ephippial eggs, and thereafter
parthenogenetic females of D. pulex rarely exceeded 1.6 mm in length. The later form
also exhibited significantly longer tail spines relative to body size than the early form.
Two other relatively abundant species, Ceriodaphnia reticulata and Simocephalus
exspinosus, were found almost exclusively in the shallow portions of the pond, and
exhibited relatively little season change in body sizes. Both seasonal succession and
shifts in body size appear to be closely linked with shifts in the predator community.
Early in the season, only small predators such as cyclopoid copepods and early-instar
phantom midge (Mochlonyx) larvae are present. These predators would necessarily
prefer smaller prey, such as juvenile cladocerans. The large adults of both D.

ephemeralis and the early form of D. pulex were effectively immune to heavy predation

57

due to their body size. In May, larger predators such as larvae of the dytiscid beetle,
Acilius semisulcatus, and larvae of Ambystoma salamanders appeared, preferring larger
prey. Large body size for cladocerans then became disadvantageous. Daphnia
ephemeralis had completed its life cycle by the end of April, and D. pulex began
producing ephippia through sexual reproduction in early May. The smaller form of D.
pulex that remained was apparently less susceptible to these larger predators due to a
smaller body size, smaller size at first reproduction, and longer tail spine. Simocephalus
exspinosus apparently reduced its exposure to predators by being more benthic than
planktonic, attaching itself to detritus. Ceriodaphm'a reticulata, which first appeared in
the pond in early May, was probably too small to attract the larger predators present
later in the season.
INTRODUCTION

Cladoceran community succession within lakes and permanent ponds has been
examined extensively with regard to food resources and predation pressures. In
contrast, the ecology of temporary pond zooplankton has received much less attention,
particularly from a community perspective. Models of cladoceran succession based on
data from permanent waters may be of limited utility in temporary habitats. Temporary
ponds and pools are not small versions of their permanent counterparts, but have a
hydrology, nutrient input, and fauna that are unique to this habitat (Wiggins et al. 1980;
Williams 1987). Temporary ponds, for example, are not thermally stratified, and the
shallow nature of these habitats precludes the existence of any aphotic zone. Small
seasonal ponds located in woodlands generally receive much less direct sunlight than

more open wetlands, and usually do not support emergent or floating macrophytes.

58

Invertebrate predators are numerically abundant, but salamander larvae (Ambystoma
spp.) are often important predators of zooplankton. There are no fish in these seasonal
ponds. The dry phase of temporary ponds is critical to the cycling of nutrients by
increasing the rate of cellulose and lignin degradation in the leaf detritus compared to
non-flooded or permanently-flooded habitats (Lockaby et al. 1996a; Lockaby et al.
1996b). The detrital pathways in these temporary habitats are very important, with
microbial processes driving much of the nutrient cycling and energy flow within the
system in both dry and aquatic phases of ponds (Higgins and Merritt 1999). The dry
phase of these ponds also "resets" the system each year, making temporary woodland
ponds ideal habitats for research.
MATERIALS AND METHODS

Study site

Research was conducted at a small woodland pool, Wild Ginger #1 (WG-l), near
Haslett, Michigan, USA (42° 45' 30"N, 84° 23' 50"W). This pond is approximately 600
m2 when completely flooded, with a maximum depth of 0.8 m. In an average year, the
pond begins to fill with water during the late autumn, and reaches its maximum size and
depth in March from snowmelt and rainfall. In 1999, the pond lost all surface water in
mid July.

Water temperature in 1999 ranged from 55° C in late March to 255° C in mid June
(Figure l). The basin is situated within a 60-70 year-old deciduous woodlot of 70 ha
and is surrounded by trees and shrubs, primarily red maple (Acer rubrum), American
elm (Ulmus americana), black ash (F raxinus nigra), swamp white oak (Quercus

bicolor), and northern swamp dogwood (Camus racemosa). The canopy does not

59

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completely close over the pond, but after the trees leaf out, most sunlight reaching the
surface is indirect. Leaves from trees near the basin and the surrounding upland
(predominantly sugar maple and white oak) contribute to the extensive detritus that
provides the energy source for the temporary pond community in the spring (Higgins
and Merritt 1999).
Collecting Methods

The zooplankton community was sampled on a weekly basis beginning when ice
melted along the margins of the pond on March 15, 1999. Samples were collected by
two different methods. A plankton net (mesh size 80 um) was towed 3 times on each
sampling date just below surface of the pond for a distance of 1.5 m. In the early
spring, the net could not be towed due to ice cover. To sample near shore and during
ice cover, a standard 500 ml mosquito dipper was used to collect water, which was then
poured through the plankton net. This procedure was repeated 4 times for a total
volume of 2 l at each of 3 sampling locations on each date. All samples were preserved
in 70% ethanol and specimens were identified using keys in Pennak (Pennak 1989) and
Wilson and Yeatman (1959). Cladoceran body lengths were measured to the nearest
0.03 m using an ocular micrometer on a dissecting microscope. Body lengths for
cladocerans do not include tail spines.

Larger invertebrates were collected in plankton tows at the same time the
zooplankton was sampled. In addition to the invertebrates captured with the plankton
net, the pond margins and interior were sampled with a D-frame aquatic net (mesh size

0.5 mm). The net was dragged for a distance of 1 m (total area 0.3 m2) through the

61

detritus near the shore, but only through the surface (0-20 cm) in the deeper part of the
pond (in order to sample Acilius beetle larvae).
Water Samples

Water column samples from the pond were taken monthly for bacteria and algae
counts. Water was collected with sterile pipettes, preserved immediately in 37%
formaldehyde solution (final concentration 4%), and stored at 4° C. Five samples were
collected each month. Samples were diluted 1:1 with deionized water and stained with
the fluorescent dye 4'6-diamidino-Z-phenylindole (DAPI) at a concentration of 30
rig/ml. Using the procedures described by Hobbie et al. (1977) and Porter and Fei g
(1980), each sample was processed through a 0.22 pm black filter (backed by a 0.45 pm
HA Millipore filter) using low vacuum pressure. The black filter was placed on a
microslide that had been smeared with a thin layer of immersion oil. A drop of
immersion oil was placed on the filter and a glass cover slip placed on top. All samples
were stored in darkness at 4° C until counted. Algae were counted at 250X using a
J enaluma microscope fitted for epifluorescence, a mercury lamp, and UV filter set.
Algae was identified using reference keys (Prescott 1962; Prescott 1978; Cox 1996).
Bacteria were counted in a similar manner at 1000X, and identified as rods, cocci, or
spirilla. Detritus particles < 10 um were also counted at 1000X.

RESULTS AND DISCUSSION

Seasonal Succession

Seasonal changes in species composition and density for the cladoceran community
are shown in Figure 2. Increasing densities from late May through June probably

reflect the decreasing size of the pond more than any increases in population sizes.

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Only 5 species were identified during the spring, and only 4 of these were abundant.
Early in the spring, the only cladoceran present was Daphnia ephemeralis (Schwartz
and Hebert). This species apparently is found only in temporary woodland ponds in the
eastern United States (Schwartz and Hebert 1985). Adult parthenogenetic females were
collected from beneath the ice in February, and were recovered along the margins of the
pond as the ice melted in March. At that time the population was comprised primarily
of parthenogenetic females, juvenile females, and a few males. By April 1, both males
and sexually reproducing females became abundant, with ephippia being produced
beginning shortly thereafter. No parthenogenetic females were collected after April 7,
only males, unmated females, and ephippial females. Daphnia ephemeralis completed
its life cycle by the end of April and no individuals were collected after April 24.

Daphnia pulex (Leydig) was first collected on April 3, shortly after D. ephemeralis
began sexual reproduction, and about the same time that Simocephalus exspinosus
(Koch) appeared in the pond. D. pulex became the numerically dominant cladoceran
through the remainder of April and into May. Collections made May 7 through May 22
recovered numerous sexually reproducing females, males, and ephippial females of D.
pulex. During this period, smaller parthenogenetic females of D. pulex appeared in the
collections, exhibiting smaller body size and a longer tail spine than those recovered in
April. This smaller form apparently replaced the earlier, larger form and was present
until late June, shortly before the pond dried.

Ceriodaphnia reticulum (J urine) was present in the pond from May 7 until the pond
dried, and was the numerically dominant cladoceran after mid May. C. reticulata was

primarily recovered in aggregations from the shallow margins of the pond, in

association with Scapholeberis mucronata (O. F. Miiller) and Simocephalus exspinosus.
Scapholeberis mucronata was collected in very small numbers until late June (Figure
2). Simocephalus exspinosus was ubiquitous but never abundant, and was always found
in association with detritus near the pond margins. The population of this species
declined drastically during June as the pond shrank in size.
Seasonal Changes in Cladoceran Body Size

Body size measurements of parthenogenetic females for the four most abundant
species in WG-l are shown in Figure 3. Early in the spring, Daphnia ephemeralis
females reached body lengths over 3m. After the ice melted from the pond, these
large individuals were only recovered from the interior portion of the pond, away from
the margins. This distributional pattern probably reflects the warmer water temperature
near shore (up to 7° C warmer) and the stenothermic cladoceran's avoidance of this
warmer area. Body sizes of D. ephemeralis remained relatively large until the
parthenogenetic individuals were replaced by smaller, sexually reproducing forms in
early April. In April, Daphnia pulex females reached maximum sizes of 2.5-3.0mm,
and showed a distribution pattern similar to the large D. ephemeralis individuals (i.e.,
occurring away from the margins of the pond). By May 7, however, the number of
these large parthenogenetic females began to decline drastically, while the number of
males and sexually-reproducing females rose even more drastically. During and after a
period of intense ephippia production in May, parthenogenetic females of D. pulex
collected from the pond were much smaller in size, rarely reaching body lengths over
1.6 mm. Only small parthenogenetic females of D. pulex were recovered through the

remainder of the season. These smaller individuals also possessed significantly longer

65

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tail spines relative to body length than the D. pulex individuals collected in April. Body
lengths of the other two abundant species, Simocephalus exspinosus and Ceriodaphnia
reticulata showed less seasonal change than was exhibited by D. pulex, but S.
exspinosus size decreased slightly as their numbers declined through June (Figure 3).
Predator Succession

Potential predators of cladocerans in WG-l are listed in Table 1. Very early in the
season few predators were present. In early March, the only predators collected were
the cyclopoid copepods, Diacyclops bicuspidatus thomasi (Forbes) and the ubiquitous
Acanthocyclops vemalis (Fischer). By mid-March, these were joined by the larger
cyclopoid, Macrocyclops albidus (J urine), and first and second instars of the phantom
midge, Mochlonyx cinctipes (Coquillett). The 3 cyclopoid copepod species were not
collected beyond April 24, but another, smaller cyclopoid, Diacyclops navus (Herrick)
was present in May and June. Mochlonyx larvae were present through April. When
Aedes mosquito larvae began hatching in substantial numbers in late March and early
April, first instar larvae of the dytiscid beetle, Agabus erichsoni (Gemminger and
Harold) also appeared in collections. Although this beetle apparently prefers mosquito
larvae, it has been observed attacking cladocerans in a laboratory setting (Higgins,
unpublished data). This species was most often found clinging to detritus near the
pond's margins.

Odonate larvae of Lestes (primarily dryas Kirby) and Sympetrum (mostly obtrusum
Hagen) began appearing in collections April 3. Teneral Lestes and Sympetrum adults
were observed along the margins of the pond beginning June 15. First instar Chaoborus

amen’canus (J ohannsen) were collected on April 24, and third and fourth instars

67

Table 1. Major potential predators of cladocerans in WG-l pond, 1999.

 

PERIOD
PREDATOR PRESENT DENSITY*
COPEPODA: CYCLOPOIDA
Diacyclops bicuspidatus thomasi (Forbes) March-April 1.3-2.4 l'l
Acanthocyclops vemalis (Fischer) March-April 0.6-1.8 l'l
Macrocyclops albidis (Jurine) March-April 0090.12 1'1
Diacyclops navus (Herrick) May-June 1.1-1.8 l"
INSECT A: ODONATA
Lestes dryas Kirby April-mid June 0.7-2.6 m'2
Sympetrum obtrusum Hagen April-mid June 1.2-2.5 m’2
IN SECTA: COLEOPTERA
Agabus erichsoni (Gemminger and Harold) March-April 0.4-1.7 rn'2
Acilius semisulcatus Aubé May 2.1 In2
INSECT A: DIPTERA
Mochlonyx cinctipes (Coquillett) March-April 0.9—2.7 l"
Chaoborus americanus (J ohannsen) late April-June 06-08 I1
AMPI-IIBIA: AMBYSTOMATIDAE
May-June 0.07 m'2

Ambystoma sp.

 

*Densities listed as no. 1'1 were determined using plankton tows. Densities listed as no.

rn'2 were determined using a D-frame net.

68

collected May 15. Chaoborus larvae, representing multiple generations, were present in
the pond for the remainder of the season. A surprisingly significant predator of
cladocerans in temporary woodland ponds is the dytiscid beetle larva, Acilius
semisulcatus Aubé, which was first recovered on May 1 and was abundant through the
entire month of May. Unlike many other dytiscid larvae that are found clinging to
debris near the margins of ponds, first and second instars of A. semisulcatus were most
often found near the surface in the deeper areas of the ponds. The larvae suspend
themselves within the water column with their respiratory spiracles in contact with the
surface and capture prey with their mandibles. Laboratory-reared first and second
larval instars readily captured and consumed Daphnia pulex >2mm in length. Densities
of A. semisulcatus first and second instar larvae within the interior portion of the pond
(approximately 400m2) on May 7 averaged 2.1 m'2 (range: 0-8 m'z). Acilius larvae were
found to be important predators of Daphnia pulex in a small pond near Montreal (Arts
et al. 1981).

Larvae of salamanders (Ambystoma spp.) were present in relatively small numbers in
WG-l in 1999, although they were abundant in 1996 and 1997. Another temporary
woodland pond 200 m to the west of WG-l contained abundant salamander larvae in
1999, so the reason for their low numbers in WG-l is unknown. Adult salamanders
enter small woodland pools in late March or early April to breed and lay eggs, and the
eggs hatch in 3-5 weeks, depending on temperature (Harding 1997). Larvae of
Ambystoma are the only important vertebrate predators in small, temporary woodland
ponds like WG-l, and they can have a significant impact on a zooplankton community

as size-selective predators (Taylor et al. 1988).

69

Other Invertebrates

No discussion of the zooplankton community within a temporary pond would be
complete without considering the impact of other filter—feeding organisms inhabiting the
pond, principally Aedes mosquito larvae and the fairy shrimp, Eubranchipus. In 1999,
the larvae of Aedes (primarily stimulans and provocans) began to hatch from eggs in
late March (somewhat later than usual due to a dry winter), and reached their peak
abundance after heavy rains in mid April. A larval density survey of the pond
conducted on April 16 resulted in an estimate of 230,000-300,000 first and second
instar mosquito larvae in the pond. Adult mosquitoes began to emerge in early May,
and no larvae or pupae were observed later than May 15. Although Aedes larvae spend
considerable time grazing the biofilm of leaf litter, they also filter feed with remarkable
efficiency. Fourth instar Aedes aegypti larvae have been shown to clear water of yeast
cells at the rate of 0.59-0.69 ml larva" h" (Aly 1988). Ameen and Iversen ( 1978)
found that 9 third-instar Aedes communis larvae removed 57% of the algal biomass
from 200 ml of pond water in 2 days. Gut contents of fourth-instar, filter-feeding A.
stimulans larvae indicate an ability to filter particles ranging in size from bacteria (<1
pm) to large protozoa (> 100nm) (see Chapter 2).

Immature fairy shrimp (Eubranchipus bundyi Forbes) were already present in the
pond when the ice began to melt in mid March. Growth was relatively fast; females
carrying egg sacs were observed April 5, 10, and 16. By April 24 the population had
declined drastically, and none were observed after that date. Density estimates for E.
bundyi based on D-frame net samples were 15-20 individuals In2 (9000-12,000 total

individuals in the pond). Eubranchipus bundyi is a filter feeder, swimming ventral side-

70

up as the legs move in a wave-like fashion, the legs serving as both means of
locomotion and food-gatherin g device. Food particles are gathered through the beating
motion of the legs into a ventral medial groove leading to the head. Food is reported to
consist of algae, bacteria, protozoans, rotifers, and small detritus (Modlin 1982a;
Pennak 1989).

Both Aedes mosquito larvae and fairy shrimp are common and usually very abundant
members of the early spring fauna of temporary woodland ponds. Both are capable of
filtering a wide range of particle sizes from the water column, and are potentially
important competitors with the smaller zooplankton for algal resources. However, they
may also play an important role in recycling nutrients. Crustacean zooplankton have
been shown to be important in recycling nitrogen and phosphorus back into the water
column where the nutrients can be reabsorbed by phytoplankton (Lehman 1980).
Mosquito larvae in particular, through their grazing of leaf litter and production of
feces, may provide an important link from benthic to planktonic food webs. Also, due
to the mosquitoes' ability to filter and assimilate bacteria, an inadequate food source for
cladocerans (Porter 1984), they may provide a link between planktonic bacteria and
algae. Nitrogen and phosphorus contained within the feces could stimulate algal growth
when released into the water, which would increase food availability to the zooplankton
community. Clearly, additional research needs to be conducted regarding the
competitive versus recycling relationship of large filter-feeding invertebrates with
zooplankton in aquatic habitats.

In addition to these relatively large filtering-gatherers, the herbivorous calanoid

copepod, Aglaodiaptomus leptopus (Forbes) was very abundant from mid-May through

71

June. By late May, the density of all life stages of this copepod reached 23 1". The
planktonic rotifer, Hexarthra, was common in May through June. This herbivorous,
soft-bodied rotifer is relatively large at approximately 250 pm in length. By mid June,
when most females were carrying resting eggs, the density of rotifers reached 37 1'].
Other common filter-feeding organisms include the benthic fingernail clam, Musculium.
Seasonal Changes in the Microbial Community

Densities of bacteria, algae, and detritus are presented in Figure 4. Both bacteria and
algae numbers increased from March through May, and then leveled off in June. Of
particular interest to this study is the algal community, and a more detailed analysis of
seasonal changes is presented in Figure 5. In March and April, the flagellates,
Chlamydomonas and species of Cryptophyceae dominated the planktonic algae. By
May, other green algae, particularly Ankistrodesmusfalcatus and Scenedesmus
(quadricauda and opoliensis) increased in number, while Chlamydomonas numbers
remained relatively constant. As the pond began to shrink rapidly during J une--with a
concomitant rise in temperature--blue-green algae (principally filamentous forms such
as Oscillatoria, Anabaena, and Spirulina) increased drastically and Chlamydomonas
numbers dropped. The increase in the numbers of desmids and dinoflagellates late in
the season may be attributable to grazing effects. Diatom numbers remained relatively
constant through May, but were never abundant in the phytoplankton. Diatoms were
much more abundant on the leaf litter in the pond (Higgins, unpubl. data). The most
common diatom genera recovered from the water column were Nitzchia, Navicula, and

Gomphonema.

72

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Both Chlamydomonas and the Cryptophyceae are considered highly edible forms of
algae, and their predominance in the early spring indicates a hi gh-quality food source
for cladocerans. The two common green algae, Ankistrodesmus and Scenedesmus are
also edible (Schindler 1970; Lynch and Shapiro 1981; Bergquist et al. 1985). The
predominance of filamentous Cyanophyta late in the season may be attributable to
increases in temperature as the pond shrank drastically in size. Blue-green algae tend to
predominate over other a] gal forms at temperatures above 20° C (T ilman et al. 1986).
Blue-green algae, especially filaments, are considered poor food sources for cladocerans
(Porter and Orcutt, Jr. 1980). Mats of filamentous algae never appeared, probably
because of the limited amount of sunlight reaching the pond.

Successional Patterns and Predation

Successional and body size changes in cladoceran communities have been linked to
both shifts in available food (algal) resources and predation pressure (Brooks and
Dodson 1965; Hall et al. 1976; Zaret 1980; Romanovsky and Feniova 1985; Sommer et
a1. 1986; Gliwicz and Pijanowska 1989). Both food limitation and predation pressure
can produce similar effects on the zooplankton community and it is often difficult to
separate these two not necessarily mutually exclusive processes. In general, smaller-
bodied cladocerans are better competitors in an environment with a fluctuating food
supply (Gliwicz 1990). Although qualitative seasonal changes in the microbial
community occurred, there is no indication that edible forms of algae declined until
June, when blue-green algae began to predominate (Figure 5). Figure 4 shows that the
quantity of algae and bacteria actually increased through the spring. In addition, by

early May, the large filter-feeding organisms such as fairy shrimp and mosquito larvae

75

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had completed their life cycle or exited the pond as adults. If food was the driving
factor behind the observed changes in the cladoceran community, the departure of these
larger competitors would be expected to lead to an increase in larger-sized cladocerans,
rather than a decline (keeping in mind, however, that these larger invertebrates may be
important in nutrient recycling). Finally, all cladoceran species did not exhibit shifts in
body size at the same time. Simocephalus exspinosus body size, for example, remained
relatively constant until June (Figure 3).

Much of the seasonal changes may be explained by shifts in predation pressure.
Early in the spring, the predator community was comprised of copepods and early-instar
Mochlonyx larvae. These early season predators are all selective toward small-sized
prey. Brambilla (1982) found that 95% of Daphnia pulex consumed by third and fourth
instar Mochlonyx larvae were < 0.80 mm long, so first and second instar Mochlonyx
could be expected to prefer even smaller prey. Brand] and Fernando (1974) reported
that Acanthocyclops vemalis preferred Ceriodaphnia prey < 0.32 mm long over those
0.40-0.54 m in length. Macrocyclops albidus, being somewhat larger (up to 2.5 mm
long), is capable of capturing larger prey (including first instar mosquito larvae), but
appears to prefer prey < 1 mm long (Fryer 1957). Given the preference for small prey
for these early predators, predation pressure on the only cladoceran present at that time,
Daphnia ephemeralis, would have been heaviest on juveniles and smaller adults. After
individuals reached a certain size, they were effectively immune to predation because
virtually no large predators were present. The only early-season large predator was the
dytiscid larva, Agabus en'chsoni, which is capable of capturing large cladocerans.

However, this beetle appears to prefer mosquito larvae and was recovered exclusively

76

from debris near the margins of the pond, an area where large D. ephemeralis rarely
occurred, probably due to the warmer water temperature.

The influence of predation on the seasonal patterns of D. ephemeralis also can be
inferred by examining the defensive morphologies exhibited by this cladoceran.
Neonates exhibit both a tail spine and a neck spine (Schwartz and Hebert 1985),
morphological traits that reduce susceptibility to invertebrate predation (Pijanowska
1990; Repka et al. 1995b; Repka and Pihlajamaa 1996). Males and ephippial females,
which are much smaller than parthenogenetic females (l.0—l.4mm), also possess a
distinct tail spine (Schwartz and Hebert 1985). Adult parthenogenetic females of D.
ephemeralis, however, show little in the way of defensive morphology; they even lack
the tail spine that is characteristic of other members of the genus Daphnia. In their
environment of small predators, D. ephemeralis clearly concentrates defensive
strategies in smaller individuals.

One apparent drawback to large body size in cladocerans is an increase in
vulnerability to egg predation by the copepodite stage of cyclopoid and calanoid
copepods. These immature copepods are capable of entering the brood chambers of
large (> 2.5 mm) cladocerans and feeding on the developing eggs (Gliwicz and Stibor
1993). Vulnerability to egg predation is apparently reduced by the presence of a large
second abdominal process (Hanazato and Dodson 1995). Although egg predation in D.
ephemeralis was not examined in this study, adult parthenogenetic females do possess a
well-developed second abdominal process (see Schwartz and Hebert 1985), possibly a

defense against egg predation by immature copepods.

77

What, then, is the reason for the relatively early departure of D. ephemeralis from
the pond? Food limitations seem unlikely given that algal biomass is increasing during
April (Figure 4). Food quality does not appear to have decreased (Figure 5), and the
similarly—sized Daphnia pulex that replaced this species was able to grow and reproduce
well on the available resources. Direct competition with D. pulex also seems unlikely
given that sexual reproduction began before D. pulex appeared in the pond. The
relatively early production of ephippia and the completion of the life cycle of D.
ephemeralis in April may be viewed as an adaptive strategy to avoid heavy predation
later in the spring. Ephippia production is completed prior to the appearance of such
large predators as Acilius and Ambystoma larvae. With little in the way of defensive
morphology to protect them, adult D. ephemeralis would certainly be vulnerable to
heavy predation pressure. Although early-season ephippia production may have
evolved as a consequence of the stenothermic nature of this species, as well as the
ephemeral nature of the habitat, the advantage of predator avoidance has probably
contributed to the maintenance of such a strategy. In this situation, the evolution of any
trait extending the life cycle of this species would be selected against. Individuals with
a higher temperature threshold, for example, would persist in the pond further into the
season and be more likely to fall prey to the larger predators present at that time, thus
reducing their fitness. In addition to avoiding predation, the early ephippia production
by D. ephemeralis avoided any possible competition with the similarly-sized D. pulex
that followed.

In terms of body size and cyclomorphosis, Daphnia pulex exhibited the most

seasonal variation of any cladoceran species present in the pond. The pattern of large-

78

sized individuals early, and then replacement by smaller individuals later in the spring
has been described previously for temporary ponds (Brambilla 1980; Modlin 1982b)
(Dodson 1974; Crosetti and Margaritora 1987) and permanent bodies of water (Hall
1964; Lynch 1978; Threlkeld 1979). Larger bodied cladocerans are able to feed more
efficiently at lower food levels than smaller cladocerans (Gliwicz 1990), but are more
vulnerable to size-selective predators (Brooks and Dodson 1965). The two forms from
WG-l differ in more ways than body size. Of particular interest are the presence of
neck teeth in first instars of the large clone (absent in the small clone) and the longer tail
spine on adults of the smaller form. Although cyclomorphosis in D. pulex is less
pronounced than in some other Daphnia species, there can be considerable variation in
the development of neck and tail spines (Black and Dodson 1990; Repka and
Pihlajamaa 1996). In addition to these morphological differences, the late form begins
reproduction at a smaller body size than the earlier form (0.9 mm versus 1.4 mm,
respectively).

The larger-sized D. pulex compares favorably with D. ephemeralis in terms of
defensive morphology. The presence of a neck tooth and a relatively long tail spine on
first and second instars of D. pulex, and the short tail spines of large adults indicate
that—as is the case with D. ephemeralis—predator defense is concentrated in smaller
individuals. Through April, D. pulex shared the same predator species as D.
ephemeralis, primarily cyclopoid copepods and Mochlonyx larvae (third and fourth
instars during April). These predators would select smaller prey, and for D. pulex, this
means early instars would be most vulnerable. With only these predators as the primary

threat, larger individuals were at an advantage and could essentially escape predation.

79

This situation changed rather abruptly in early May, however. Predators like Acilius
and Ambystoma larvae appeared. Unlike the early-season predators that selected for
small individuals, these larger predators preferred larger prey. Ambystoma larvae
apparently prefer prey 2 1.3 mm in length (Brambilla 1980). While no prey size
preference has been determined for first and second instar Acilius larvae, individuals in
a preliminary laboratory experiment captured and consumed D. pulex 1.8-2.5 mm long.
For the early-season D. pulex, large size quickly became a disadvantage. At the same
time these predators began to appear in the pond, D. pulex began to produce males,
sexually-reproducing females, and—soon after—abundant ephippia. Thereafter, only
smaller parthenogenetic females were recovered from the pond.

If the two forms of D. pulex in WG-l represent different genotypes (which has yet to
be determined), the production of ephippia by the larger clone in May appears to be a
strategy to avoid predation. Predator avoidance through diapause is not unprecedented.
Slusarczyk (1995) found that the exudates of predatory fish triggered ephippia
production in Daphnia magna. The production of diapausing eggs in the copepod,
Diaptomus sanguineus (Forbes) has been shown to be heavily influenced by increased
predation levels (Hairston and Munns 1984; Hairston 1987). At present, it is unknown
whether the cues that triggered sexual reproduction in D. pulex in May came directly
from the presence of predators or were based on an indirect environmental cue such as
temperature or photoperiod. If temperature or photoperiod is found to be the proximate
cause for ephippia production, this does not necessarily diminish the adaptive
significance of entering diapause at a time in the season when predation pressure

becomes severe. Predator-induced ephippia production can be viewed as a "bet-

80

hedging" strategy (Schaffer 1974). Predation pressure may become severe enough to
eliminate a population, and the production of resting eggs insures survival of the
population into the following season. A pond 200 m west of WG-l contained abundant
Ambystoma larvae, and no D. pulex were recovered after May 22, suggesting that the
salamanders eliminated this population.

The smaller, late season D. pulex exhibited different defensive morphology than the
early season form. Neonates did not have neck a neck tooth, which was somewhat
surprising given the presence of Chaoborus and copepod predators that would favor
smaller prey. The presence of Chaoborus is known to induce the development of neck
teeth in D. pulex (Schwartz 1991; Parejko 1991; Repka et al. 1994; Luning 1995), but
the density of this predator in WG-l may have been too low (< 1 liter") to trigger this
response. Another indication that predation pressure had shifted toward larger
individuals of D. pulex can be seen in the development of the tail spine. In the early
spring, tail spine length declined with increased body size (Figure 6), implying that
larger individuals were less susceptible to predation. Later in the spring, tail spine
length was positively correlated with body size (Figure 6), suggesting that larger
individuals were now more vulnerable.

If the early, large-sized D. pulex is entering diapause as a means of avoiding
predation, is the smaller form that follows less susceptible to these same predators? In
preliminary feeding experiments with Acilius larvae, first instars attacked any prey
over 1 mm long. Second instars showed little interest in D. pulex < 1.5 mm long, but
readily attacked individuals > 2.0 mm long. Most of the late-season D. pulex would fall

below the preferred prey size 2 1.3 mm for Ambystoma. The size at first reproduction

81

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82

for the late-season form is 0.9 mm, well below the preferred prey size of both
Ambystoma and Acilius larvae. At the other end of the predator size spectrum, the two
most important potential predators on smaller individuals are Chaoborus americanus
larvae and the cyclopoid copepod, Diacyclops navus. Somewhat surprisingly,
Chaoborus was found not to be an important predator of D. pulex in WG-l. An
examination of 20 guts of C. americanus third and fourth instars found only 2 D. pulex
remains. Calanoid copepods (probably Aglaodiaptomus leptopus) were most common,
followed by soft-bodied rotifers (Hexarthra), and Ceriodapm’a reticulata. Moore
(1988) found rotifers to be the most abundant prey in all instars of C. punctipennis, and
Brambilla (1982) also found Chaoborus larvae to be insignificant predators on D. pulex
in a temporary pond near Ann Arbor, MI. The prey preferences of D. navus are not
known for the field, but Brambilla (1982) observed that D. navus readily consumed first
and second instar D. pulex in the laboratory. Therefore, it can be assumed that this
copepod, although never abundant in WG-l , would prey on early instar D. pulex in the
field.

The other two cladoceran species present in WG-l, Ceriodaphnia reticulata and
Simocephalus exspinosus, showed relatively little size variation through the season
compared to D. pulex. Both of these species were found primarily in shallow water
along the pond margin, with S. exspinosus capable of withstanding the higher
temperatures of this area of the pond (LaBerge and Hann 1990). Simocephalus
exspinosus, like other members of this genus, spends much of its time attached to plant
material by a sticky mucus on the dorsum of its carapace. In WG-l, individuals

attached themselves to detritus on the bottom of the pond, making this species more

83

benthic than planktonic. The predators that occupy this habitat—Odonate and beetle
larvae—are sit—and-wait predators, attacking prey that move within their sensory range.
By reducing movement through the water column, S. exspinosus reduced its encounter
rate with these predators (Havel et al. 1993). Body size for S. exspinosus, therefore,
was probably less important in reducing predation than simply reducing its encounter
rate. Ceriodaphm'a reticulata, averaging a little over 0.5 mm, was probably below the
electivity range of many larger late-season predators.
CONCLUSIONS

The cladoceran communities of temporary woodland ponds appear to follow a
reasonably predictable succession of species. Seasonal changes in community structure
and body sizes appear to be closely linked with shifts in the predator community.
Although this study represents but one pond and one season, similar trends in
succession and body size relationships were observed in less-intensive studies of 4 other
woodland ponds in the Lansing, Michigan area. In two of these, S. exspinosus was
replaced by S. vetulus (O.F.Mtiller) and C. reticulata was replaced by C. quadrangula
(O.F.Milller). There appears to be a relatively small pool of potential cladoceran
species capable of inhabiting these temporary woodland ponds.

This primarily descriptive study has raised some important questions regarding the
cladoceran communities of temporary woodland ponds. Clearly, there is much research
to be conducted on the zooplankton communities that occupy these relatively small,

ephemeral habitats:

84

. What are the cues that trigger ephippia production in D. ephemeralis and the larger
form of D. pulex? Are they directly predator induced (unlikely for D. ephemeralis
but certainly possible for D. pulex), or are they environmentally-induced?

. What role do seasonal changes in the algal community play in cladoceran
succession? Although it appears that predation plays the major role in shaping the
cladoceran community, it is doubtful that food resources are not influential in some
manner.

. What is the genetic relationship between the early and late forms of D. pulex? If
they are different genotypes, is the later form also present early in the season as well
as the larger form? If it is not present early, what cue triggers its appearance?

. What is the relationship of the larger filtering organisms such as mosquito larvae
and fairy shrimp to the cladoceran community? Do they play an important role in
nutrient cycling or are they simply competitors of cladocerans for algal resources?

. What are the quantitative advantages of the two forms of D. pulex when exposed to
their respective predators? Morphological traits infer certain advantages. Does the
smaller, large-spined form have an advantage over the larger, small-spined form

when exposed to salamander predation?

85

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Aly, C. 1988. Filtration rates of mosquito larvae in suspensions of latex microspheres
and yeast cells. Entomologia Experimentalis et Applicata 46: 55-61.

Ameen, M. and T. M. Iversen. 1978. Food of Aedes larvae (Diptera: Culicidae) in a
temporary forest pool. Archiv ftir Hydrobiologie 83: 552-564.

Arts, M. T ., E. J. Maly, and M. Pasitschniak. 1981. The influence of Acilius
(Dytiscidae) predation on Daphnia in a small pond. Limnology and
Oceanography 26: 1172-1175.

Bergquist, A. M., S. R. Carpenter, and J. C. Latino. 1985. Shifts in phytoplankton size
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Black, A. R. and S. I. Dodson. 1990. Demographic costs of Chaoborus-induced
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Brambilla, D. J. 1982. Seasonal variation of egg size and number in a Daphnia pulex
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Brand], Z. and C. H. Fernando. 1974. Feeding of the copepod Acanthocyclops vemalis
on the cladoceran Ceriodaphnia reticulata under laboratory conditions.
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Brooks, J. L. and S. I. Dodson. 1965. Predation, body size and composition of plankton.
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Cox, E. J. 1996. Identification of Freshwater Diatoms From Live Material. Chapman
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Crosetti, D. and F. G. Margaritora. 1987. Distribution and life cycles of cladocerans in
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Dodson, S. I. 1974. Zooplankton competition and predation: An experimental test of the
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Fryer, G. 1957. The food of some freshwater cyclopoid copepods and its ecological
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86

Gliwicz, Z. M. 1990. Food thresholds and body size in cladocerans. Nature 343: 638-
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Haven.

90

CHAPTER 4
PHENOLOGY, BODY SIZE, AND PREDATION
IN A TEMPORARY WOODLAND POND
ABSTRACT

Temporary ponds are characterized by annual cycle of flooding and drying, which
requires aquatic organisms that occupy these habitats to adapt to these conditions. In
these ephemeral environments, there are no large overwintering predators, and the
aquatic community is reset each spring. Organisms that are particularly well adapted to
life in temporary woodland ponds include Aedes mosquito larvae, fairy shrimp, and the
cladoceran Daphnia ephemeralis. All of these are filtering or gathering collectors that
begin development as soon as the pond floods early in the spring. None of these
organisms exhibit any strong morphological defenses to predation, despite a substantial
predatory community that occupies these ponds during the course of the wet phase. As
a consequence of beginning development early in the season, potential prey taxa such as
these are exposed to fewer and smaller predators early than they would be if
development was initiated later in the season. These organisms minimize predation
early by being exposed to few predators, and later by reaching body sizes that are
beyond the capturing/handling size of most available predators.

INTRODUCTION

Understanding the forces that shape community composition has been of interest to
ecologists for many years. Aside from the physical and nutritional requirements
necessary for organisms to survive, biotic interactions among and within species have

been viewed as a major driving force in community organization. While competition

91

has traditionally been viewed as being of primary importance to community structure
(e. g., Tilman 1982), more recently, the importance of predation has been emphasized,
particularly in aquatic environments (Connell 1975; Zaret 1980; Kerfoot and Sih 1987;
Sih 1987; Wellborn et al. 1996; Schneider 1997). The term "predation" is used here in
the traditional sense meaning one animal consuming another, and does not include
aquatic herbivory (Bronmark and Hansson 1998).

Zaret (1980) recognized two types of predators in aquatic communities, gape-limited
and size—dependent predators. Gape-limited predators essentially capture prey with
their mouth and are therefore limited in the size of prey they can capture by the size of
their gape. Size-dependent predators do not ingest prey whole, and are limited to the
size of prey that they can effectively capture and handle. Planktivorous fish and
salamander larvae (e.g., Ambystoma) are examples of gape-limited predators reported
by Zaret ( 1980). I would also include dytiscid beetle larvae in this category as they
capture prey with their mandibles and subsequently suck fluids from their prey.
Examples of size-dependent predators given by Zaret (1980) include phantom midge
larvae (Mochlonyx and Chaoborous), which capture prey with modified antennae. It is
important to note that in both of these categories of predators, potential prey that exceed
the size limitations are effectively immune to capture. Large prey body size relative to
predators can be a significant defense to lessen or even eliminate predation risk,
particularly in invertebrate predator/prey relationships. Cohen et al. (1993) examined
body sizes of predators and prey in 70 different communities and found a strong

positive correlation for size in invertebrate predator/prey relationships, with most

92

predators consuming prey that were equal to or smaller than them in size (Peters 1983;
Cohen et al. 1993).

The concept of enemy free space (Jeffries and Lawton 1984) has been used to
describe the role of predation in shaping ecological niches, in both contemporary and
evolutionary time frames. Enemy free space refers to any trait that reduces or
eliminates a species' vulnerability to predation (Jeffries and Lawton 1984). Such traits
may be behavioral, morphological, physiological, and even phenological. Predation
involves three components: detection, pursuit, and capture (Holling 1966), and a given
prey's defense may be involved in any of these. Defensive traits are not mutually
exclusive, and a given species may exhibit more than one, particularly in different life
stages. Connell (1975) recognized the potential advantage for a prey species to outgrow
its predators, but also noted that such a defense is less effective in younger (smaller)
individuals. By employing other defensive traits in the more vulnerable early life
stages, however, outgrowing potential predators may be an effective defense.

Temporary ponds are ideal habitats in which to study seasonal changes in predator-
prey relationships. Due to the dry phase of these ponds, the aquatic communities within
them are "reset" each year. In temporary woodland ponds in Michigan, there are no
large overwintering predators. Flooding in the spring triggers a succession of species,
with most of the earliest species hatching from resting eggs. Many predators appear
later in the spring, either hatching from resting eggs or arriving as immigrants from
permanent water refuges (Wiggins et al. 1980; Higgins and Merritt 1999). Among the
earliest to appear in the spring are Aedes mosquito larvae, Eubranchipus fairy shrimp,

and the cladoceran, Daphnia ephemeralis. All of these organisms are extremely well

93

adapted to life in temporary ponds. They all have freeze and drought-resistant eggs and
are capable of surviving and growing in the cold water temperatures ice cover of early
spring (Wiggins et al. 1980; Westwood et al. 1983; Schwartz and Hebert 1985). None
of these organisms, however, has any particular morphological adaptation against
predators. Because predators are very abundant in temporary pond communities
(Higgins and Merritt 1999), the general lack of morphological defenses to reduce
predation suggests that other means of reducing or eliminating predation risk are more
important.

I hypothesize that organisms that are well adapted to temporary habitats reduce their
exposure to predators by beginning development early and by reaching body sizes that
are larger than can be effectively handled by most available predators. Such a strategy
can be effective only in environments like temporary ponds, where the communities
must restart each season and where there are no large overwintering predators.

MATERIALS AND METHODS
Study Site

Research was conducted at a small woodland pool, Wild Ginger #1 (WG-l), near
Haslett, Michigan, USA (42° 45' 30"N, 84° 23' 50"W). This pond is approximately 600
m2 when completely flooded, with a maximum depth of 0.8 m. In an average year, the
pond begins to fill with water during the late autumn, and reaches its maximum size and
depth in March from snowmelt and rainfall. The pond loses all surface water between
mid July and early August. Water temperatures range from < 5° C in March to > 25° C
in June and July. The basin is situated within a 60-70 year-old deciduous woodlot of 70

ha and is surrounded by trees and shrubs, primarily red maple (Acer rubrum), American

94

elm (Ulmus americana), black ash (F raxinus nigra), swamp white oak (Quercus
bicolor), and northern swamp dogwood (Camus racemosa). The canopy does not
completely close over the pond, but after the trees leaf out, most sunlight reaching the
surface is indirect. Leaves from trees near the basin and the surrounding upland
(predominantly sugar maple and white oak) contribute to the extensive detritus that
provides the energy source for the temporary pond community in the spring (Higgins
and Merritt 1999).
Field Studies

In order to examine successional trends, the aquatic invertebrate community was
sampled every 2 weeks in 1996-1998, from the time ice began to melt along the margins
of the pond until it dried, usually March-July. Samples were taken with a D-frame
aquatic net (mesh size 0.5 mm) and a standard 500 ml mosquito dipper. Samples were
preserved in 70% ethyl alcohol and identified using keys in Merritt and Cummins
(1996) and Pennak (1989). Individual body lengths of both predators and prey were
measured with an ocular micrometer on a dissecting microscope to the nearest 0.1 mm.
Because predator and prey size was being considered, each larval instar of the insects
was treated as a separate predator or prey organism in this study. Thus, if two larval
instars of the same predatory species were present in the pond at the same time, there
would most likely be differences in electivity of prey size between them and were
therefore treated as different predators.

Zooplankton samples were collected weekly in 1999. A plankton net (mesh size 80
um) was towed 3 times on each sampling date just below surface of the pond for a

distance of 1.5 m. In the early spring, the net could not be towed due to ice cover, nor

95

could it be towed in shallow water near shore. To sample near shore and during ice
cover, a standard 500 ml mosquito dipper was used to collect water, which was then
poured through the plankton net. This procedure was repeated 4 times for a total
volume of 2 l at each of 3 sampling locations on each date. All samples were preserved
in 70% ethanol and specimens were identified using keys in Pennak (1989) and Wilson
and Yeatman (1959). Cladoceran body lengths were measured to the nearest 0.03 m
using an ocular micrometer on a dissecting microscope. Body lengths for cladocerans
do not include tail spines.
Predator/Size Experiments

To determine prey size limitations of various predators, laboratory experiments were
conducted using Aedes stimulans (Walker) larvae as prey, with the predators
Mochlonyx, Acilius, and Agabus larvae. The purpose of these experiments was not to
duplicate natural conditions of predator versus prey, but to determine the upper limit of
prey size for different stages of various predators. In order to simultaneously obtain
different larval instars of mosquitoes, first instars were collected in the field and reared
at different temperatures to accelerate or retard their growth. Only 24 third-instar
Agabus were collected, so only 8 replicates were used for that particular experiment.
All other experiments used 10 replicates. Predators were field collected as needed and
starved for 6 hours before each experiment. In experiments with the larval phantom
midge, Mochlonyx, 4 Aedes larvae were placed in each of 10, 30-ml vials with 20 ml of
filtered (125 um) pond water along with 0.5 ml solution of finely-ground TetraMin®
fish food (0.1g/25 ml water) as food for the mosquitoes. Each vial then received one

Mochlonyx larvae in the following combinations: first-instar Mochlonyx separately with

96

first and second-instar Aedes, second-instar Mochlonyx separately with first and second-
instar Aedes, and third-instar Mochlonyx separately with second and third-instar Aedes.

Experiments using the dytiscid beetle larvae, Acilius and Agabus were conducted in
a similar manner using 60 ml plastic cups with 40 ml filtered pond water. Each cup
received 4 mosquito larvae and one predator in the following combinations: first-instar
Acilius separately with second and fourth-instar Aedes, second-instar Acilius separately
with second and fourth-instar Aedes, first-instar Agabus separately with first, second,
and third-instar Aedes, second-instar Agabus separately with first, second, and third-
instar Aedes, and third-instar Agabus separately with second, third, and fourth-instar
Aedes.

All experiments were conducted at a constant temperature of 15° C in an
environmental chamber with 12:12 h light:dark regime. After 48 h the number of Aedes
larvae eaten within each container was recorded.

Crop contents of fourth-instar Mochlonyx larvae were also examined. Larvae were
captured in the field with a mosquito dipper, immediate killed by placing them in hot
water, and then transferred to 70% ethyl alcohol. The crop was removed intact from
each larva with minuten pins and transferred to a clean microslide. A drop of water was
added and the crop contents were teased apart and viewed at 100x and 250x.

RESULTS
Predator Succession

Very early in the season few predators were present (Figure 1). When ice on the

pond first began to melt, the only predators collected were the cyclopoid copepods,

Diacyclops bicuspidatus thomasi (Forbes) and Acanthocyclops vernalis (Fischer).

97

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Shortly thereafter, these were joined by the larger cyclopoid, Macrocyclops albidus

(J urine), and first instars of the phantom rrridge, Mochlonyx cinctipes (Coquillett). The
3 cyclopoid copepod species were not collected beyond the end of April, but another,
smaller cyclopoid, Diacyclops navus (Herrick) was present in May and June.
Mochlonyx larvae (third and fourth instars) were present throughout April, emerging as
adults in early May. As Aedes mosquito larvae began hatching in substantial numbers
when the pond reached maximum size with early spring rain, first instars of the dytiscid
beetle, Agabus erichsoni (Gemminger and Harold) also appeared in collections. This
species was most often found clinging to detritus near the pond's margins. This beetle
developed rapidly, completing larval development by mid to late April.

Odonate larvae of Lestes (primarily dryas Kirby) and Sympetrum (mostly obtrusum
Hagen) began appearing in collections in April. Teneral Lestes and Sympetrum adults
were observed along the margins of the pond by mid to late June. Phantom midge
larvae, Chaoborus americanus (Johannsen) were collected from mid-late April, and
Chaoborus larvae, representing multiple generations, were present in the pond for the
remainder of the season. A surprisingly significant predator of cladocerans in
temporary woodland ponds is the dytiscid beetle larva, Acilius semisulcatus Aubé,
which was first recovered in late April through early May, and was abundant through
the entire month of May. Unlike many other dytiscid larvae that are found clinging to
debris near the margins of ponds, first and second instars of A. semisulcatus were most
often found near the surface in the deeper areas of the ponds. The larvae suspend

themselves within the water column with their respiratory spiracles in contact with the

99

surface and capture prey with their mandibles. Acilius larvae were found to be
important predators of Daphnia pulex in a small pond near Montreal (Arts et al. 1981).

Larvae of salamanders (Ambystoma spp.) were present in WG-l every spring in
1996-1999, although their abundance varied considerably from year to year.
Salamander larvae were abundant in 1996 and 1997, but occurred in very low numbers
in 1998 and 1999. Adult salamanders enter small woodland pools in late March or early
April to breed and lay eggs, and the eggs hatch in 3-5 weeks, depending on temperature
(Harding 1997). Larvae of Ambystoma are the only important vertebrate predators in
small, temporary woodland ponds like WG-l, and they can have a significant impact on
a zooplankton community as size-selective predators (Taylor et al. 1988).

Several predatory larvae appeared later in the spring, most notably hydrophilid
beetles (Hydrochara), dytiscid beetles (Dytiscus and Laccophilus), notonectids
(Notonecta), veliids (Microvelia), and in some years belostomatids (Belostoma). All of
these predators are rrri grant species, the adults of which overwinter in permanent water
and recolonize temporary ponds in the spring to breed (Wiggins et al. 1980).
Predation and Body Size

The results of the predator/size experiments are summarized in Table 1. For
Mochlonyx, it is clear that first and second larval instars are capable of catching and
consuming first and second instar Aedes larvae that are less than or equal to them in
length. After the second instar, Aedes larvae were apparently too large for Mochlonyx
larvae to capture. Although fourth-instar Mochlonyx were not used in any of these
experiments, examination of gut contents from 20 field-collected fourth-instar

Mochlonyx failed to identify any mosquito larvae. First-instar Acilius larvae'were

100

Table l. Predator feeding experiments using 4 larval Aedes stimulans mosquitoes and l
larval predator. Values are percentages of mosquitoes eaten and mean number
consumed per container in parentheses; n: 10 for all except third instar Agabus (n=8).

Mean length of each instar is given in parentheses.

Aedes stimulans

 

 

Instar #
Predator
Instar# 1st 2nd 3rd 4th
(1.9) (4.2) (7.3) (9.7)
Mochlonyx
1st 15.0 0 --- ---
(2.1) (0.6)
2nd 97.5 22.5 --- ---
(3.8) (3.9) (0.9)
3rd --- 72.5 0 ---
(5.2) (2.9)
Acilius
1st --- 95.0 --- 0
(8.4) (3.8)
2nd --- 67.5 --- 50.0
(14.8) (2.7) (2.0)
Agabus
1st 100 95 .0 20.0 ---
(7.4) (4.0) (3.8) (0.8)
2nd 80.0 100 77.5 ---
(11.7) (3.2) (4.0) (3.1)
3rd --- 82.5 81.25 72.5
(18.2) (3.3) (3.25) (2.9)

101

capable of capturing up to second-instar Aedes larvae, but fourth-instar mosquitoes were
apparently beyond their handling size. Second—instar Acilius larvae, however, were
quite capable of capturing fourth-instar Aedes. The larvae of Agabus erichsoni were
capable of capturing a wide range of sizes of mosquito larvae in all three instars. Even
first-instar Agabus could at least occasionally capture third-instar Aedes larvae (Table
1).
Seasonal Changes in Body Size Relationships

Early in the season, very few predators were present in the pond. At the time that
Aedes larvae and Eubranchipus hatched, the predators were first instar Mochlonyx and
Agabus beetle larvae, and cyclopoid copepods, the largest being Macrocyclops. With
the exception of Agabus, all these predators were smaller than or equal to the two prey
taxa in size (Figure 2). As the prey grew, they reached sizes larger than all but Agabus.
Predatory taxa that appeared later in the spring were all smaller than Aedes and
Eubranchipus, with the exception of first instar Dytiscus larvae, which was first
collected in late April. By this time, Eubranchipus had completed its life cycle.
Dytiscus larvae were never abundant in WG-l but they are among the largest beetle
larvae (first instars are 14 mm long) and therefore may be relatively significant
predators (Young 1967). These beetles had abundant fourth instar Aedes larvae on
which they could feed until the mosquitoes pupated and emerged in early May. After
that, it appeared that Dytiscus larvae preyed largely upon tadpoles of wood frogs. By the
time more predators arrived, and others reached larger size, the mosquitoes had

emerged as adults.

102

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The situation was very similar with the cladoceran community in WG-l (Figure 3).
Very early in the spring, the only species present was Daphnia ephemeralis, and
parthenogenetic females reached lengths of 3 mm. Predatory copepods and early larval
instars of Mochlonyx would necessarily prey on much smaller individuals during this
time, with adult D. ephemeralis effectively immune to predation due to their large size.
Juvenile D. ephemeralis exhibit a distinct tail and neck spine, while spines are absent in
adults (Schwartz and Hebert 1985). Tail and neck spines in cladocerans are anti-
predator morphological traits that are often inducible in the presence of predators
(Luning-Krizan 1997; Kolar and Wahl 1998). Daphnia ephemeralis began sexual
reproduction and the production of ephippia in early April, and completed its life cycle
by the end of April, before the appearance of most of the larger predators.

Following D. ephemeralis in succession, Daphnia pulex began to appear in
collections in early April. Sharing the same predators as D. ephemeralis, adult females
achieved lengths up to 2.5-3.0 mm during April. In early May, however, males and
sexually-reproducing females dominated the population, with the subsequent production
of ephippia completed by the end of May. Parthenogenetic females collected during
May were smaller--rarely exceeding 2.0 mm in length--and exhibited longer tail spines
than adults collected in April (Figure 4). Only the smaller form of D. pulex was present
through the remainder of the season. The initiation of sexual reproduction and the
production of ephippia in D. pulex coincided with the appearance of two important
predators in WG-l. Larvae of the dytiscid beetle, Acilius semisulcatus and
salamanders, Ambystoma spp., both hatched in early May. Unlike the early spring

predators, both of these organisms show a preference for larger prey (Brambilla 1980;

104

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Arts et al. 1981). Following their appearance in the pond, adult parthenogenetic
females were much smaller, 3 size reduction that does not coincide with any reduction
in food supply (see Chapter 3). In addition, tail lengths for the smaller form were
longer, and increased with body length, compared to individuals collected in April,
which showed a negative relationship between body size and tail length (Figure 4).
This would suggest heavier predation pressure on larger individuals later as compared
to earlier in the season.
DISCUSSION

In these temporary ponds, there is a definite trend for smaller and fewer predators
early in the season than later in the season. Also, based on the laboratory feeding
experiments, there are size limitations for most potential predators of Aedes. When
Aedes and Eubranchipus hatch early in the spring, the only important predators are
Agabus beetle larvae, Macrocyclops copepods, and perhaps early-instar Mochlonyx
larvae. Although Mochlonyx has been implicated as an important predator of mosquito
larvae (Morrison and Andreadis 1992), laboratory experiments indicate that mosquitoes
can quickly outgrow these predators. These results are similar to those reported by
O'Connor (1959) who found no mosquito remains in the crop contents of 30 third- and
fourth-instar Mochlonyx. Although no feeding experiments were conducted with
Macrocyclops, these predators would likely be important only during the first instar of
the mosquitoes. In addtion, Macrocyclops density was very low (0.1 1") and they had
other prey available, such as Mochlonyx, Daphnia ephemeralis, and other copepods.
The copepod predators, in turn, could also fall prey to later-instar Mochlonyx. Only

Agabus erichsoni larval development closely followed that of Aedes. This species is the

107

earliest dytiscid beetle larvae to appear in temporary woodland ponds (James 1961),
overwintering in the egg stage (James 1969; Wiggins et al. 1980). It is apparently an
important predator of mosquito larvae in the spring. A laboratory-reared A. erichsoni
consumed a total of 252 Aedes larvae during the course of its larval development (James
1969).

The cladoceran community also seems to be heavily influenced by predation. Early
in the season, Daphnia ephemeralis is the only species present. Adults are large with
little morphological defenses to predation (they even lack a tail spine), while juveniles
and smaller sexual forms exhibit both neck and tail spines. Daphnia ephemeralis
completes its life cycle early in the spring, prior to the arrival of larger predators.
Daphnia pulex, which followed D. ephemeralis in succession, initially appeared as large
adults with minimal tail spines. The appearance of larger predators such as Ambystoma
salamanders and Acilius beetle larvae may have triggered the intense period of ephippia
production by D. pulex in May. Predator-induced diapause is not unprecedented
(Hairston and Munns 1984; Hairston 1987; - lusarczyk 1995). Thereafter,
parthenogenetic D. pulex were smaller and possessed long tail spines.

Schneider and coworkers (Schneider and Frost 1996; Schneider 1997; Schneider
1999) have examined the role of pond duration in shaping temporary pond
communities. Long-duration ponds support a much more diverse and, on average,
longer-lived predator community than do short-duration ponds. Such predator
communities may exclude certain taxa from long-duration ponds, or limit population
sizes of other taxa (Schneider and Frost 1996; Schneider 1997). The mechanisms for

such exclusion or limitation may include behavioral tradeoffs (W ellbom et al. 1996).

108

Animals in temporary habitats need to grow quickly and thus forage actively. This
foraging activity, however, results in increased exposure to predation. In short-duration
ponds with limited predator communities, this may not present a problem. In long-
duration and permanent ponds, however, such active foraging may lead to
extermination by predators. Thus, animals that are well adapted to temporary ponds are
often excluded from permanent and semi-permanent ponds (W ellbom et al. 1996).
Such mechanisms are viewed as accessory to life history constraints such as a
prerequisite cold and dry period to initiate egg hatching (e. g., most Aedes mosquitoes).
That many permanent and semi-permanent pond communities contain many temporary
pond taxa and a reduced predator community after a drought (Jeffries 1994; Schneider
and Frost 1996) supports the argument that such taxa are excluded by predation.
Animals such as Aedes and Eubranchipus are common in both short- and medium-
duration temporary ponds. In small, short-duration ponds, there is little or no predation
pressure. In medium-duration ponds like WG-l, predators are relatively scarce early,
but increase in both numbers and size later in the spring. That mosquito larvae and
fairy shrimp begin development very early in the spring in both types of ponds suggests
that this life history trait probably evolved as a consequence of the ephemeral nature of
the habitat and the need to develop rapidly in a shrinking environment. In medium-
duration ponds, early development and relatively rapid growth have also served to
minimize predation potential. Aedes, Eubranchipus, and Daphnia ephemeralis all begin
development before most predators have appeared, and quickly outgrow the effective
handling size of most available predators. By the time predators become abundant,

Eubranchipus and D. ephemeralis have entered a diapausing stage and Aedes have

109

exited the pond as adults. Only one major predator, the dytiscid beetle Agabus
erichsoni, seems to have successfully circumvented this "exaptation" (Gould and Vrba
1982) by adaptinguas its prey has--to the severe physical constraints of pond drying and
the cold temperatures of early spring.

In addition to minimizing predation in time and through larger body size, there is
another advantage to beginning development early that has not been previously
discussed. Given the same sized predator, it is more advantageous for a prey population
to be exposed to this predator later in its development rather than earlier, assuming that
both stages are within the handling capabilities of the predator. A predator feeding on
small prey will consume more individuals in order to become satiated than it will when
feeding on large prey, i.e., predation rate falls with increasing size of prey (Travis et al.
1985). Thus, the same predator will have less of an impact on a prey species that is in
the later stages of development rather than earlier stages because it will consume fewer
large individuals. Potential prey organisms, such as Aedes mosquito larvae in
temporary ponds, begin development early, and by doing so reduce their exposure to
later-appearing predators. If late-instar larvae are exposed to predators (e. g., first-instar
Dytiscus or second-instar Acilius beetle larvae), the impact on the population will be
less than if these predators were preying on earlier instars. Lest I be accused of
invoking group selection, predation rates for the prey population would decline with
increasing body size, as would an individual 's chance of being eaten.

A Model for Predator-Prey Relationships in Temporary Ponds
Predator-prey trends and relationships in temporary woodland ponds are summarized

graphically in Figure 5. All of the biotic interactions are constrained by the physical

110

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environment (e. g., pond drying and cold temperatures early in the season). Species that
are well adapted to temporary ponds have overcome the difficulties imposed by these
environmental constraints and hatch very early in the season. The few predators that
are present at that time are mostly small, and potential prey species can reduce
predation risk by reaching a body size that is beyond the handling capabilities of most
predators. Later in the season, predators are generally larger in size, and taxa like
mosquito larvae, fairy shrimp, and Daphnia ephemeralis enter diapause, or exit the
pond as adults in the case of mosquitoes, transforming to life history stages that are
immune to aquatic predation. Both environmental constraints and predation, however,
also can act as negative feedback to prey body size. Although large body size can
reduce larval predation and could ultimately lead to increased adult fecundity, it can
also increase the duration of the larval stage (Peters 1983). In an ephemeral habitat,
such a tradeoff could potentially lead to increased larval mortality by not reaching
maturity before the pond dried. Also, an increase in the duration of the larval stage may
expose later stages of a prey species to larger predators that appear later in the season,

thus negating any benefit of body size.

112

REFERENCES

Arts, M. T., E. J. Maly, and M. Pasitschniak. 1981. The influence of Acilius
(Dytiscidae) predation on Daphnia in a small pond. Limnology and
Oceanography 26: 1172-1175.

Brambilla, D. J. 1980. Seasonal changes in size at maturity in small pond Daphnia, p.
438-455. In [ed.], W.C.Kerfoot, Evolution and Ecology of Zooplankton
Communities. New England University Press. Hanover, NH.

Bronmark, C. and L.-A. Hansson. 1998. The Biology of Lakes and Ponds. Oxford
University Press. New York.

Cohen, J. E., S. L. Pimm, P. Yodzis, and J. Saldafia. 1993. Body sizes of animal
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Connell, J. H. 1975. Some mechanisms producing structure in natural communities: a
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Gould, S. J. and E. S. Vrba. 1982. Exaptation--a missing term in the science of form.
Paleobiology 8: 4-15.

Hairston, N. G., Jr. 1987. Diapause as a predator avoidance adaptation, p. 281-299. In
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Hairston, N. G., Jr. and W. R. Munns, Jr. 1984. The timing of copepod diapause as an
evolutionarily stable strategy. American Naturalist 123: 733-751.

Harding, J. H. 1997. Amphibians and Reptiles of the Great Lakes Region. University of
Michigan Press. Ann Arbor.

Higgins, M. J. and R. W. Merritt 1999. Temporary woodland ponds in Michigan:
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D.P.Batzer, R.B.Rader, and S.A.Wissinger, Invertebrates in Freshwater
Wetlands of North America: Ecology and Management. John Wiley and Sons.
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Holling, C. S. 1966. the functional response of invertebrate predators to prey density.
Memoirs of the Entomological Society of Canada 47: 3-86.

113

James, H. G. 1961. Some predators of Aedes stimulans (W alk.) and Aedes tricurus
(Dyar) (Diptera: Culicidae) in woodland pools. Canadian Journal of Zoology -
Journal Canadien de Zoologie 39: 533-540.

James, H. G. 1969. Immature stages of five diving beetles (Coleoptera: Dytiscidae),
notes on their habits and life history, and a key to aquatic beetles of vernal
woodland pools in southern Ontario. Proceedings of the Entomological Society
of Ontario 100: 52-97.

J effries, M. 1994. Invertebrate communities and turnover in wetland ponds affected by
drought. Freshwater Biology 32: 603-612.

Jeffries, M. J. and J. H. Lawton. 1984. Enemy free space and the structure of ecological
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Kerfoot, W. C. and A. Sih.Kerfoot, W. C. and Sih, A. [eds.] 1987. Predation: Direct and
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Hanover, NH.

Kolar, C. S. and D. H. Wahl. 1998. Daphnid morphology deters fish predators.
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Luning-Krizan, J. 1997. Neck-teeth induction in Daphnia hyalina under natural and
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Merritt, R. W. and K. W. Cumrrrins (eds.). 1996. An Introduction to the Aquatic Insects
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Morrison, A. and T. G. Andreadis. 1992. Larval population dynamics in a community
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O'Connor, C. T. 1959. The life history of Mochlonyx cinctipes (Coquillett) (Diptera:
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Peters, R. H. 1983. The Ecological Implications of Body Size. Cambridge University
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Schneider, D. W. 1997. Predation and food web structure along a habitat duration
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Schneider, D. W. 1999. Snowmelt ponds in Wisconsin: Influence of hydroperiod on
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Schneider, D. W. and T. M. Frost. 1996. Habitat duration and community structure in
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86.

Schwartz, S. S. and P. D. N. Hebert. 1985. Daphniopsis ephemeralis sp.n. (Cladocera,
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Sih, A. 1987. Predators and prey lifestyles: an evolutionary and ecological overview, p.
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N .H.

- lusarczyk, M. 1995. Predator-induced diapause in Daphnia. Ecology 76: 1008-1013.

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Wellbom, G. A., D. K. Skelly, and E. E. Werner. 1996. Mechanisms creating
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Westwood, A. R., G. A. Surgeoner, and B. V. Helson. 1983. Survival of spring Aedes
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Wiggins, G. B., R. J. Mackay, and 1. Smith. 1980. Evolutionary and ecological
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Wilson, M. S. and H. C. Yeatman 1959. Free-living Copepoda, p. 735-861. In [eds.],
W.T.Edmondson, H.B.Ward, and G.C.Whipple, Fresh-Water Biology. John
Wiley and Sons. New York.

Young, A. M. 1967. Predation in the larvae of Dytiscus marginalis Linneaus. Pan-
Pacific Entomologist 43: 113-117.

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115

APPENDICES

116

APPENDIX A,

Record of Deposition of Voucher Specimens*

The specimens listed on the following sheet(s) have been deposited in
the named museum(s) as samples of those species or other taxa which were
used in this research. Voucher recognition labels bearing the Voucher
No. have been attached or included in fluid-preserved specimens.

Voucher No.: 2000-3

Title of thesis or dissertation (or other research projects):

Invertebrate Trophic Relationships in Temporary woodland Ponds

in Hichigan
Museum(s) where deposited and abbreviations for table on following sheets:
Entomology Museum, Michigan State University (MSU)

Other Haseums:

Investigator's Name (8) (typed)
Michael J. Higgins

 

 

Date 1 11a; 2000

*Reference: Yoshimoto, C. M. 1978. Voucher Specimens for Entomology in
Nbrth America. Bull. Entomol. Soc. Amer. 24:141-42.

Deposit as follows:

Original: Include as Appendix 1 in ribbon copy of thesis or

dissertation.
Copies: Included as Appendix 1 in copies of thesis or dissertation.

Museum(s) files.
Research project files.

This form is available from and the Voucher No. is assigned by the Curator,
Michigan State University Entomology Mrseum.

117

 

 

 

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