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This is to certify that the
dissertation entitled

EFFECTS OF OMNIVOROUS CRAYFISH ON FISH
POPULATIONS AND THE STRUCTURE OF LITTORAL
COMMUNITIES

presented by

NATHAN JEFFREY DORN

has been accepted towards fulfillment
of the requirements for the

Ph.D. degree in ZOOLOGY

 

 

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EFFECTS OF OMNIVOROUS CRAYFISH ON FISH POPULATIONS
AND THE STRUCTURE OF LITTORAL COMMUNITIES

By

Nathan Jeffrey Dorn

A DISSERTATION

Submitted to
Michigan State University
in partial fulﬁllment of the requirements
for the degree of

DOCTOR OF PHILOSOPHY

W. K. Kellogg Biological Station
Department of Zoology
and
Ecology, Evolutionary Biology, and Behavior Program

2003

ABSTRACT

EFFECTS OF OMNIVOROUS CRAYFISH ON FISH POPULATIONS
AND THE STRUCTURE OF LITTORAL COMMUNITIES

By

Nathan Jeffrey Dom

Crayﬁsh are the largest invertebrate predators in many freshwater systems, they
are broadly omnivorous, and are capable of dominating secondary production and
biomass. Crayﬁsh are widely distributed in waterbodies throughout the globe and have
been introduced to many ecosystems, otherwise beyond their dispersal capacities, for a
variety of reasons. In this study, I explored the effects of crayﬁsh on another large
freshwater predator (sunﬁsh) and on community structure of shallow water habitats.

The effects of crayﬁsh on ﬁsh populations were explored with a literature review
and two replicated experiments in ponds. Crayﬁsh can have a number of relationships
with ﬁsh, and interactions are not limited to the traditional studies of ﬁsh as predators and
crayﬁsh as prey. Other interactions have been less well studied, and one potentially
important interaction is the effect of crayﬁsh as predators of ﬁsh eggs.

To look for evidence of the effects of crayﬁsh on reproductive success and
nesting behavior I performed two experiments (1999 and 2001) with two species of
common sportﬁsh, the pumpkinseed sunﬁsh (Lepomis gibbosus) and bluegill sunfish (L.
macrochirus). Both species of sunﬁsh nest in shallow littoral habitats of lakes and ponds
and nests are guarded by the adult males. In both of the experiments, crayﬁsh inﬁltrated
nests, ate the eggs and had negative impacts on reproductive success of the sunﬁsh. In

the experiment with bluegill sunﬁsh, crayﬁsh stopped reproduction until predator-free

nesting habitats (exclosures) were added to the ponds later in the summer. After the
exclosures were added, adult bluegill in each pond found the exclosures and were able to
reproduce.

Crayﬁsh had additional strong effects on overall community development
(succession) in six ponds studied in 2001-2002. Through direct and indirect effects,
crayﬁsh had signiﬁcant effects on the biomass of zooplankton and phytoplankton
assemblages and peak levels of dissolved oxygen. Crayﬁsh also had strong negative
effects on macrophyte establishment, metaphyton abundance and composition, gastropod
biomass, and the density of bullfrog (Rana catesbiana) tadpoles. Based on these results
and those of other studies of crayﬁsh in lakes and ponds, systems with abundant crayﬁsh
are expected to be structurally simple systems with few macrophytes and gastropods
where ﬁlamentous green algae and some species of amphibians and ﬁsh will perform
poorly, but other organisms may beneﬁt.

In my last experiment I explored the relative impacts of native and exotic
Orconectes crayﬁsh grazing on a common plant type. Using feeding trials in cages I
determined that adults of the exotic crayﬁsh, Orconectes rusticus and the native 0. virilis
had similar grazing rates on Chara macroalgae in two ponds with and without bass, as
long as no direct interactions with the bass were possible. However, when direct
interactions were possible, 0. rusticus had higher feeding rates than 0. virilis. This result
is consistent with differences in overall predation vulnerability of these species, and
suggests that stronger per biomass effects of exotic crayﬁsh might be obviated in the

presence of predators.

ACKNOWLEDGEMENTS

I would like to thank my advisor Gary Mittelbach for being timely and helpful
and a good mentor, editor, critic, and collaborator. My guidance committee (Kay Gross,
Steve Hamilton, David Lodge, and Ace Samelle) and the members of the Mittelbach lab
(Tara Darcy, Erica Garcia, Jessica Rettig, Chris Steiner, and Jeremy Wojdak) all provided
helpful input and constructive criticism during my degree. J. Conner, N. Dubois, T.
Getty, L. Hayes, R. Hill, G. Houseman, B. Keas, E. Nedeau, A. Tessier, and E. Thobaben
as well as a number of non-MSU. folks including J. Breck, S. Hall, T. Kreps, B. Perry,
B. Roth, T. Smith, R. VanDragt, and K. Wilson all added helpful conversations, ideas,
advice, and/or critiques of my work from time to time.

Several people helped in the ﬁeld experiments and most of these experiments
would not have happened without them. With gratitude I thank Mike Bellware, Tara
Darcy, Meegan Leah Dom, Kevin Dorn, James “Gappy” Gapczynski, Erica Garcia, Gary
Mittelbach, Jon Smedes, Chn's Steiner, Eric Thobaben, Mark Watson, Alan Wilson,
Jeremy Wojdak, C.J. Wykoff, and Pete Wykoff. The Pond Lab Trucks of past and
present and a truck loaned by the Almena Tree Farm (R. Westra) carried me safely from
Hickory Comers to the other “corners” of the Lower Penninsula. Crayﬁsh were provided
by the DNR Saline Fisheries Research Station and from the Denton and Shirley Nelson’s
Lake Michigan frontage in Traverse City. Equipment and analytical advice was
graciously borrowed and received from the labs of Drs. Alan Tessier, Matthew Leibold,
and Steve Hamilton. For equipment and computer technical support I would like to thank

Nina Consolatti and John Gorentz.

iv

I was supported ﬁnancially by several sources including the Department of
Zoology, the K.B.S. Graduate Research Training Grant (RTG) funded by the National
Science Foundation, assistantships with the K-12 Partnership and the K.B.S. Pond Lab,
two G. H. Lauff Research Awards, the EEBB Program, and the Graduate School.

The K.B.S. community has been extremely ﬁiendly to me and my family during
our time at K.B.S. Tim Bergsma, Greg Houseman, Eric Thobaben, and Jeremy Wojdak
have all been good friends for the duration of my time at M.S.U., and Jeremy Wojdak
was an especially important collaborator and colleague over the last two years.

Nike, Asics, Gazelle Sports, PowerBar, and Team Burkhart Chiropractic,
supported me with racing sponsorships, and my former coach (B. Diemer) and teammates
(R. Hyde, G. VanDragt, and others) encouraged my running habit which helped maintain
my physical and mental well-being. Drs. J. R. R. Tolkein and C. S. Lewis indirectly
contributed by providing alternative Middle-Earthian and Namian ecologies which
entertained my mind and renewed my spirit during the writing phase.

My extended family (especially my parents Dan and Ruth Dom) encouraged my
interest in science and the underwater world from a very young age, and along with my
in-laws, have been supportive throughout my degree. I am thankful to my daughter,
Adriana for her many smiles and excitement at my arrival home every day. My loving
wife, Meegan, has made the journey much easier with her help in the ﬁeld, unending
encouragement, enthusiasm, and her self-sacriﬁcial attitude. Last, but most importantly, I
thank my Creator, Lord, and Savior who provided me with curiosity, energy, and a

number of timely insights regarding my research.

TABLE OF CONTENTS

LIST OF TABLES ........................................................................................................... viii
LIST OF FIGURES ........................................................................................................... ix
CHAPTER 1
INRODUCTION: OMN IVORY AND FRESHWATER BENTHIC
COMMUNITIES ................................................................................................................. 1
Crayﬁsh Background ............................................................................................... 2
Dissertation Overview ............................................................................................. 3
References ................................................................................................................ 7
CHAPTER 2
MORE THAN PREDATOR AND PREY: A REVIEW OF INTERACTIONS
BETWEEN FISH AND CRAYFISH ................................................................................ 10
Abstract .................................................................................................................. 11
Keywords ......................................................................................................... 12
Introduction ............................................................................................................ 12
Trophic relationships ............................................................................................. 13
Traditional predator-prey studies ........................................................................... 15
Interactions between crayﬁsh and small benthic ﬁsh ............................................ 18
Potential negative effects of crayﬁsh on ﬁsh ......................................................... 21
Conclusions ............................................................................................................ 23
Acknowledgements ................................................................................................ 24
References .............................................................................................................. 25
CHAPTER 3
EGG PREDATOR EFFECTS ON FISH REPRODUCTIVE SUCCESS AND
NESTING BEHAVIOR ..................................................................................................... 34
Abstract .................................................................................................................. 34
Keywords ......................................................................................................... 35
Introduction ............................................................................................................ 35
Materials and Methods ........................................................................................... 38
1999 Pumpkinseed experiment ........................................................................ 39
2001 Bluegill experiment ................................................................................. 41
Results .................................................................................................................... 42
1999 Pumpkinseed experiment ........................................................................ 42
2001 Bluegill experiment ................................................................................. 44
Discussion .............................................................................................................. 45
Interactions of crayﬁsh and ﬁsh populations ................................................... 48
Egg predators and breeding habitats ................................................................ 48
Viewing and managing the spawning landscape ............................................. 50
Acknowledgements ................................................................................................ 54

vi

TABLE OF CONTENTS

LIST OF TABLES ........................................................................................................... viii
LIST OF FIGURES ........................................................................................................... ix
CHAPTER 1
INRODUCTION: OMNIVORY AND FRESHWATER BENTHIC
COMMUNITIES ................................................................................................................. 1
Crayﬁsh Background ............................................................................................... 2
Dissertation Overview ............................................................................................. 3
References ................................................................................................................ 7
CHAPTER 2
MORE THAN PREDATOR AND PREY: A REVIEW OF INTERACTIONS
BETWEEN FISH AND CRAYFISH ................................................................................ 10
Abstract .................................................................................................................. 11
Keywords ......................................................................................................... 12
Introduction ............................................................................................................ 12
Trophic relationships ............................................................................................. 13
Traditional predator-prey studies ........................................................................... 15
Interactions between crayﬁsh and small benthic ﬁsh ............................................ 18
Potential negative effects of crayﬁsh on ﬁsh ......................................................... 21
Conclusions ............................................................................................................ 23
Acknowledgements ................................................................................................ 24
References .............................................................................................................. 25
CHAPTER 3
EGG PREDATOR EFFECTS ON FISH REPRODUCTIVE SUCCESS AND
NESTING BEHAVIOR ..................................................................................................... 34
Abstract .................................................................................................................. 34
Keywords ......................................................................................................... 35
Introduction ............................................................................................................ 35
Materials and Methods ........................................................................................... 38
1999 Pumpkinseed experiment ........................................................................ 39
2001 Bluegill experiment ................................................................................. 41
Results .................................................................................................................... 42
1999 Pumpkinseed experiment ........................................................................ 42
2001 Bluegill experiment ................................................................................. 44
Discussion .............................................................................................................. 45
Interactions of crayﬁsh and ﬁsh populations ................................................... 48
Egg predators and breeding habitats ................................................................ 48
Viewing and managing the spawning landscape ............................................. 50
Acknowledgements ................................................................................................ 54

vi

LIST OF TABLES

CHAPTER 2

Table 1. Annual production (kg/ha/yr) of crayﬁsh and percentage consumed by predator
ﬁsh in four natural systems. ............................................................................................... 31
Table 2. Results of gut content analyses in several freshwater systems where ﬁsh were
found eating crayﬁsh .......................................................................................................... 32
CHAPTER 4

Table 1. Relative abundance (mean % of total biomass) of zooplankton groups in ponds
with and without crayﬁsh. Large cladocerans = Daphnia and Simocephalus; small
cladocerans = Bosmina, Ceriodaphm’a, Chydorus, and Diaphanosoma; copepods =
calanoids and cyclopoids ................................................................................................... 99

Table 2. Percent cover of green metaphyton (Cladophora and Zygnema algal mats) and
Chara on the bottom of 6 ponds ...................................................................................... 100

Table 3. Percent abundance (% of cells in counts) of algal genera in metaphyton samples
taken from 6 ponds in late August 2001. All taxa that made up _>_ 5% of all cells in at
least one pond are included in the table ........................................................................... 101

CHAPTER 5
Table 1. Analysis of variance results for two grazing trials comparing native (Orconectes
virilis) and exotic (Orconectes rusticus) crayﬁsh feeding on macroalgae (Chara vulgaris)

in two ponds (with and without bass). Mass-speciﬁc consumption was measured for
groups of crayﬁsh grazing inside cages. .......................................................................... 125

viii

References .............................................................................................................. 55

CHAPTER 4
OMNIVOROUS CRAYFISH DEF LECT SUCCESSIONAL PATHWAYS IN POND
COMMUNITIES: AN EXPERIMENTAL STUDY ......................................................... 65
Abstract .................................................................................................................. 65
Keywords ......................................................................................................... 66
Introduction ............................................................................................................ 66
Materials and Methods ........................................................................................... 69
Setup ................................................................................................................ 69
Measurements .................................................................................................. 70
Plankton ..................................................................................................... 70
Dissolved oxygen, light, and seston ........................................................... 71
Benthic community .................................................................................... 72
Crayﬁsh migration between ponds .................................................................. 75
Statistical Analyses .......................................................................................... 75
Results .................................................................................................................... 76
Crayﬁsh abundance .......................................................................................... 76
Plankton ........................................................................................................... 77
Dissolved oxygen, light, and seston ................................................................. 78
Benthic community .......................................................................................... 78
Discussion .............................................................................................................. 81
Crayﬁsh abundance .......................................................................................... 81
Plankton and water quality ............................................................................... 82
Benthic community structure ........................................................................... 83
General implications for community development .......................................... 86
Effects of animals on succession ..................................................................... 88
Acknowledgements ................................................................................................ 91
References .............................................................................................................. 92
CHAPTER 5
COMPARING GRAZING RATES OF NATIVE AND EXOTIC ORCONECTES
CRAYFISH: THE IMPORTANCE OF FISH PREDATORS ......................................... 111
Abstract ................................................................................................................ 111
Keywords ....................................................................................................... 111
Introduction .......................................................................................................... 1 12
Materials and Methods ......................................................................................... 114
Animals .......................................................................................................... 115
Trial 1 - No predator vs. non-lethal threat (closed cages) ............................. 116
Trial 2 - No predator vs. direct threat (open cages) ...................................... 116
Results .................................................................................................................. 118
Trial 1 - No predator vs. non-lethal threat (closed cages) ............................. 118
Trial 2 - No predator vs. direct threat (open cages) ...................................... 118
Discussion ............................................................................................................ 119
Acknowledgements .............................................................................................. 121
References ............................................................................................................ 123

vii

LIST OF FIGURES

CHAPTER 2

Figure 1. Hypothetical relationship between crayﬁsh size (10-30 mm CL), substrate size,
and vulnerability to ﬁsh predation ..................................................................................... 33
CHAPTER 3

Figure 1. Production of young-of-year (YOY) pumpkinseed (L. gibbosus) in ponds with
and without crayﬁsh (0. virilis) during summer 1999. (a) Mean total biomass (numbers x
mean size) of YOY sampled with standardized seining. (b) Mean number of YOY
captured in seines. (c) Mean wet mass (g) of sampled YOY. Error bars represent one
standard error and p-values are from one-way ANOVAs (N = 3) ..................................... 62

Figure 2. Distribution of birthdates of YOY pumpkinseed collected from ponds with and
without crayﬁsh in 1999. Birthdates were estimated by enumeration of otolith daily
growth rings. Distributions were compared with a non-parametric Komolgorov-Smirnov
test ...................................................................................................................................... 63

Figure 3. Tirneline of bluegill (L. macrochirus) nesting and larval recruitment in ponds
with and without crayﬁsh (0. virilis) during summer 2001 (N = 3). (a) Mean number of
active bluegill nests (nests with eggs or fry) per pond. (b) Mean number (+1) of free-
swimming YOY bluegill caught per standardized ichthyoplankton tow/pond. Error bars
denote one standard error. Exclosures were added to crayﬁsh ponds on 5 July ................ 64

CHAPTER 4

Figure 1. Mean zooplankton biomass in ponds with and without crayﬁsh (Orconectes
virilis) with results from repeated measures ANOVA. The ﬁsh symbols and arrows
indicate the estimated timing of the ﬁrst successful ﬁsh recruitment in each treatment for
consideration of trophic interactions between larval ﬁsh and zooplankton. Error bars
denote one standard error. Asterisks indicate signiﬁcant treatment effects (p-values <
0.004) on individual dates when treatments were sliced by time .................................... 102

Figure 2. Mean phytoplankton abundance (ug chlorophyll a - L") in ponds with and
without crayﬁsh (Orconectes virilis) and statistical results from repeated measures
AN OVA. Error bars denote one standard error .............................................................. 103

Figure 3. Mean peak dissolved oxygen in ponds with and without crayﬁsh (Orconectes

virilis) with results from repeated measures ANOVA. Error bars denote one standard
error .................................................................................................................................. 104

ix

Figure 4. Average total particulate matter (TPM) in the water column of ponds with and
without crayﬁsh (Orconectes virilis) in July of 2001. Error bars are one standard error
and refer to the standard errors of the entire bar. The ponds differed for all three measures
of particulates (total, organic, and inorganic, p-values < 0.04, see text). ........................ 105

Figure 5. Results from a choice feeding assay where crayﬁsh were simultaneously
offered the dominant algal metaphyton from control and crayﬁsh ponds (Cladophora and
Gleotrichia). Error bars denote one standard error. The p-value is from a t-test of
differences incorporating mass changes from control buckets in the analysis to control for
variability due to autogenic mass change (see Peterson and Renaud 1989). ................... 106

Figure2 6. Mean abundance of periphyton (algae attached to hard surfaces; pg chlorophyll
0 cm 2') in ponds with and without crayﬁsh (Orconectes virilis) with statistical results
from rm-ANOVA (2002) and one-way ANOVA (2002). Error bars denote one standard
error. The asterisk indicates a signiﬁcant (p < 0.05) treatment effect in June and August
2001 (slicing by time) ...................................................................................................... 107

Figure 7. Size-frequency histogram of chironomids (A) and Caenis mayﬂies (B) collected
from ponds with and without crayﬁsh. The p-value is from a Komolgorov-Smirnov two

sample test of distributions (chironomids: control n = 61, crayﬁsh n = 81; Caenis: control
n = 189, crayﬁsh n = 168) ................................................................................................ 108

Figure 8. A comparison of the generalized community structure expected in lentic
shallow water systems with or without abundant omnivorous crayﬁsh (Decapoda) ....... 110

CHAPTER 5

Figure l. Mass-speciﬁc consumption of Orconectes crayﬁsh feeding on Chara in closed
cages inside ponds with and without bass. Crayﬁsh in the bass pond were exposed to
non-lethal threats (i. e., sight and smell) of largemouth bass (Micropterus salmoides). The
numbers inside the bars indicate the number of replicates within each pond. Wet masses
were used in calculations of consumption ....................................................................... 126

Figure 2. Mass-speciﬁc consumption of Orconectes crayﬁsh feeding on Chara in opened
cages inside ponds with and without bass. Crayﬁsh in the bass pond were exposed to
direct interactions with largemouth bass (Micropterus salmoides). The numbers inside
the bars indicate the number of replicates within each pond. Wet masses were used in
calculations of consumption ............................................................................................ 127

CHAPTER 1

INTRODUCTION: OMN IVORY AND FRESHWATER BENTHIC
COMMUNITIES

One of the long-standing goals of ecology is to understand the mechanisms that
regulate populations and thereby structure communities. The details of consumer-
resource interactions underlie most of the direct and indirect biotic mechanisms thought
to affect community composition (e.g., Paine 1966, Holt 1984, Ricklefs 1987). Although
all animals are consumers, different animals species have different feeding habits; some
animals have restricted diets (specialists) and others feed on several prey types
(generalists). Generalist predators that feed across trophic levels are considered
omnivores. The ubiquity and importance of omnivory (plant-animal omnivory, trophic
omnivory, and others) has been recognized for some time in marine systems (e.g., Menge
and Sutherland 1976, 1987) and has recently gained attention in a variety of ecosystems
(e.g., Polis et a1. 1989, Diehl 1993, McCann and Hastings 1997, Eubanks and Denno
1999). By feeding on multiple trophic levels omnivores can disrupt the general
expectations of simple trophic cascades (Diehl 1993, Pringle and Hamazaki 1998),
maintain or augment their populations through feeding on non-preferred prey (Polis and
Strong 1996, Eubanks and Demo 1999), and stabilize community dynamics (McCann
and Hastings 1997, F agan 1997).

Menge and Sutherland (1987) and Diehl (1993) have suggested that large
omnivores feed indiscriminately on small prey regardless of trophic or taxonomic status.
Thus populations of intermediate consumers and lower resources may respond similarly
to top-down control by large omnivores (Menge and Sutherland 1987, Diehl 1993).

However, the strength of top-down control on speciﬁc organisms will certainly depend

upon prey size, morphology, and anti-predator behaviors (Kerfoot and Sih 1987, Lima
and Dill 1990, Diehl 1993), as well as environmental stress and habitat complexity
(Menge and Sutherland 1987, Polis and Strong 1996).

Freshwater benthic communities have many omnivorous vertebrates and
invertebrates with important feeding links to intermediate consumers and basal resources
(e.g., Warren 1989, Vadas 1990, Havens et al. 1996, Pringle and Hamazaki 1998).
Furthermore, because many large freshwater predators have relatively small early life-
stages, even the largest predators (i.e., ﬁsh) may be susceptible to predation by
intermediate consumers. Abundant omnivory and size-structured populations, coupled
with a diversity of predator and prey sizes, morphs, and behaviors, make freshwater
benthic communities rich systems for studying the direct and indirect effects of
omnivores on populations and community structure.

CRAYFISH BACKGROUND

Crayﬁsh are the largest invertebrate predators in freshwater benthic communities,
and over 300 species can be found in a diversity of habitats in the United States and
Canada (Taylor et a]. 1996). Crayﬁsh are omnivores in a traditional sense; they feed on
living plants (both macrophytes and algae), detritus (and associated decomposers),
invertebrates, and even vertebrate protein if available (Momot 1995). Young-of-year
crayﬁsh are relatively susceptible to ﬁsh predation and can provide an important food
base for large ﬁsh (Chapter 2), but adult crayﬁsh are relatively invulnerable (Stein 1977).
Crayﬁsh can attain high community biomass and production rates in many systems, and

Momot (1995) has hypothesized that crayﬁsh can eliminate vulnerable or preferred

animal prey while maintaining their populations on less proﬁtable food resources
(detritus and plants).

Previous experimental work has documented strong direct and indirect effects of
crayﬁsh on other benthic invertebrates and primary producers (e.g., Creed 1994, Lodge et
a1. 1994, Nystrom et al. 2001). Due to their large body size and omnivorous feeding
habits, crayﬁsh have the potential to inﬂuence the trajectory of community development
(primary or secondary succession) by directly or indirectly affecting the success of a
variety of species residing in littoral habitats.

Understanding the effects of crayﬁsh on community structure and their
interactions with populations of other large consumers, like ﬁsh, is also important for
predicting and understanding the effects of crayﬁsh invasions. Many crayﬁsh species
have been introduced to waterbodies beyond the reach of their natural dispersal abilities
(Hobbs et al. 1989). Introductions have been both intentional - for the purpose of
aquaculture, aquatic plant management, or as forage for ﬁsh, and accidental -— as in the
case of bait bucket introductions (Hobbs et al. 1989, Lodge et al. 2000), and have had a
variety of negative consequences (Lodge et a1. 2000).

DISSERTATION OVERVIEW

I am interested in the effects of crayﬁsh on ﬁsh populations and the structure of
littoral communities. In this dissertation I investigated these interactions through a
literature survey of ﬁsh-crayﬁsh interactions (Chapter 2), and several ﬁeld experiments
utilizing a set of semi-natural experimental ponds, which allowed entire populations of
organisms to interact with and respond to each other (Chapters 3, 4, 5). I addressed the

following questions through my research: (1) What are the known relations and

interactions between crayﬁsh and ﬁsh populations and what interactions have been
poorly studied? (2) Can crayﬁsh be signiﬁcant predators of the early-life-stages (eggs,
fry) of ﬁsh, and how do reproducing ﬁsh respond behaviorally to the presence of safe
nest sites? (4) Can crayﬁsh affect primary succession of pond communities, and in what
ways do pond communities with and without crayﬁsh differ? and (5) Do native and
exotic Orconectes crayﬁsh have impacts of the same nature and magnitude on
macroalgae?

In Chapter 2 I reviewed the known interactions between crayﬁsh and ﬁsh from
the published literature. Much of the literature has documented the energetic importance
of crayﬁsh prey for predatory ﬁsh diets. Additional work has detailed the behavioral
interactions between ﬁsh predators and crayﬁsh prey. Far fewer studies addressed the
following interactions that could potentially have negative consequences for ﬁsh
populations: (a) competition between benthic ﬁsh and crayﬁsh for shelter and food, (b)
predation by crayﬁsh on ﬁsh eggs and fry, and (c) the indirect effects of crayﬁsh on ﬁsh
populations through alteration of important macrophyte habitats.

In Chapter 3 I tested the hypothesis that crayﬁsh could be signiﬁcant predators on
the early life-stages of ﬁsh by performing two ﬁeld experiments. I measured recruitment
success of populations of two species of nesting sunﬁsh (Lepomis) with functionally
different nesting strategies (solitary nesters versus colony nesters) in replicate ponds with
and without crayﬁsh. In the second experiment I added small crayﬁsh-proof exclosures
to the crayﬁsh ponds to determine whether reproducing adult sunﬁsh would respond
favorably to a safe nesting site. The results from these experiments indicate that (1)

crayﬁsh can be signiﬁcant egg predators of both species of sunﬁsh and can cause

reproductive failure at realistic crayﬁsh densities, and (2) sunﬁsh can ﬁnd and will use
safe nesting sites when they are available. These results provide a mechanistic
explanation for the observed decline of ﬁsh populations following invasions (Magnuson
et a1. 1975, Guan and Wiles 1997, Covich et a1. 1999).

Nystrom et a1. (1996) suggested that crayﬁsh could have important effects on the
succession of pond communities. Their study relied on observations of ponds at one
point in time 40 years after they were constructed. To evaluate the effects of crayﬁsh on
early stages of succession I conducted a 13-month experiment of succession in six
recently constructed ponds with and without omnivorous crayﬁsh. Previous experiments
with crayﬁsh have looked at the trophic effects of crayﬁsh in smaller arenas on extant
(equilibrium) communities. This experiment allowed me to consider the effects of a large
benthic omnivore on the colonization and establishment of many species in whole pond
ecosystems. The results from this experiment indicated that direct and indirect effects of
crayﬁsh deﬂected the dynamics of these communities. Populations and assemblages of
zooplankton, phytoplankton, metaphytic algae, macroalgae (Chara vulgaris) periphyton,
benthic invertebrates, and tadpoles as well as suspended sediments and production:
respiration ratios were all affected by crayﬁsh presence.

Crayﬁsh are widely introduced throughout the Midwest and the world (Lodge et
al. 2000), and the effects of exotic crayﬁsh could be greater than the species they replace.
In Chapter 5, I tested the grazing capacities of native (Orconectes virilis) and exotic
(Orconectes rusticus) crayﬁsh to determine whether native and exotic species would have
different impacts on macroalgae (Chara). Because the exotic species (0. rusticus) was

known to be less vulnerable to predation I measured the grazing capacities of each

species inside cages placed in two ponds, with and without bass predators, to determine
whether predator presence changed the relative grazing impact of the two species. The
results of this experiment indicate that the two species respond differently to different
predator environments; in the absence of predators the two species grazed similarly, but
in presence of direct interactions with predators (the condition most like natural lakes) the

exotic species had higher mass-speciﬁc grazing effects on macroalgae.

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Creed, R. P. 1994. Direct and indirect effects of crayﬁsh grazing in a stream community.
Ecology 75: 2091-2103.

Covich, A. P., M. A. Palmer, and T. A. Crow]. 1999. The role of benthic invertebrate
species in freshwater ecosystems. BioScience 49: 119-127.

Diehl, S. 1993. Relative consumer sizes and the strengths of direct and indirect
interactions in omnivorous feeding relationships. Oikos 68: 151-157.

Eubanks, M. D., and R. F. Denno. 1999. The ecological consequences of variation in
plants and prey for an omnivorous insect. Ecology 80: 1253-1266.

Pagan, W. F. 1997. Omnivory as a stabilizing feature of natural communities. American
Naturalist 150: 554-567.

Guan, R. and P. R. Wiles. 1997. Ecological impact of introduced crayﬁsh on benthic
ﬁshes in a British lowland river. Conservation Biology 11: 641-647.

Havens, K. E., L. A. Bull, G. L. Warren, T. L. Crisman, E. J. Philips, and J. P. Smith.
1996. Food web structure in a subtropical lake ecosystem. Oikos 75: 20-32.

Hobbs, H. H., J. P. Jass, and J. V. Huner. 1989. A review of global crayﬁsh introductions
with particular emphasis on two North American species (Decapoda, Cambaridae).
Crustaceana 56: 299-316.

Holt, R. D. 1984. Spatial heterogeneity, indirect interactions, and the coexistence of prey
species. The American Naturalist 124: 377-406.

Kerfoot, W. C., and A. Sih. (eds.) 1987. Predation: direct and indirect impacts on aquatic
communities. University Press of New England, Hanover and London.

Lima, S. L., and L. M. Dill. 1990. Behavioral decisions made under the risk of predation:
a review and prospectus. Canadian Journal of Zoology 68: 619-640.

Lodge, D. M., M. W. Kershner, J. E. Aloi, and A. P. Covich. 1994. Effects of an
omnivorous crayﬁsh (Orconectes rusticus) on a freshwater littoral food web.
Ecology 75: 1265-1281.

Lodge, D. M., C. A. Taylor, D. M. Holdich, and J. Skurdal. 2000. Nonindigenous
crayﬁshes threaten North American freshwater biodiversity: Lessons from Europe.
Fisheries 25:7-19.

Nystrom, P., C. Bronmark, and W. Granéli. 1996. Patterns in benthic foodwebs: a role
for omnivorous crayﬁsh? Freshwater Biology 36: 631-646.

Nystrom, P., O. Svensson, B. Lardner, C. Bronmark, and W. Granéli. 2001. The
inﬂuence of multiple introduced predators on a littoral pond community. Ecology 84:
1023-1039.

Magnuson, J. J ., G. M. Capelli, J. G. Lorrnan, and R. A. Stein. 1975. Consideration of
crayﬁsh for macrophyte control. pgs. 66-74. In P. L. Brezonik and J. L. Fox [ed.]
The proceedings of a symposium on water quality management through biological
control. Rep. No. ENV 07-75-1, University of Florida, Gainesville, F L.

McCann, K., and A. Hastings. 1997. Re-evaluating the omnivory-stability relationship in
food webs. Proceedings of the Royal Society of London Series B-Biological Sciences
264: 1249-1254.

Menge, B. A. and J. P. Sutherland. 1976. Species diversity gradients: synthesis of the
roles of predation, competition, and temporal heterogeneity. American Naturalist 110:
351-369.

Menge, B. A. and J. P. Sutherland. 1987. Community regulation: variation in
disturbance, competition, and predation in relation to environmental stress and
recruitment. The American Naturalist 130: 730-757.

Momot, W. T. 1995. Redeﬁning the role of crayﬁsh in aquatic ecosystems. Reviews in
Fisheries Science 3: 33-63.

Paine, R. T. 1966. Food web complexity and species diversity. The American Naturalist
100: 65-75.

Polis, G. A., C. A. Myers, and R. D. Holt. 1989. The ecology and evolution of intraguild
predation: potential competitors that eat each other. Annual Review of Ecology and
Systematics 20: 297-330.

Polis G. A., and D. R. Strong. 1996. Food web complexity and community dynamics.
The American Naturalist 147: 813-846.

Pringle, C. M., and T. Hamazaki. 1998. The role of omnivory in a neotropical stream:
separating diurnal and nocturnal effects. Ecology 79: 269-280.

Ricklefs, R. E. 1987. Community diversity: relative roles of local and regional processes.
Science 235: 167-171.

Stein, R. A. 1977. Selective predation, optimal foraging, and the predator-prey interaction
between ﬁsh and crayﬁsh. Ecology 58: 1237-1253.

Taylor, C. A., M. L. Warren, J. F. Fitzpatrick, H. H. Hobbs III, R. F. Jezerinac, W. L.
Pﬂieger, and H. W. Robison. 1996. Conservation status of crayﬁshes of the United
States and Canada. Fisheries 21: 25-38.

Warren, P. H. 1989. Spatial and temporal variation in the structure of a freshwater food
web. Oikos 55: 299-311.

Vadas, R. L. 1990. The importance of omnivory and predator regulation of prey in
freshwater ﬁsh assemblages of North America. Environmental Biology of Fishes 27:
285-302.

CHAPTER 2

Dom N. J ., and G. G. Mittelbach. 1999. More than Predator and Prey: a review of

interactions between ﬁsh and crayﬁsh. Vie et Milieu 49: 229-237.

10

CHAPTER 2

MORE THAN PREDATOR AND PREY: A REVIEW OF INTERACTIONS
BETWEEN FISH AND CRAYFISH

with Gary G. Mittelbach
ABSTRACT

Crayﬁsh are a major constituent of benthic invertebrate production in both lentic
and lotic habitats. Crayﬁsh also provide an important food resource for many ﬁsh.
Because of their abundance and relatively large body size, the interactions between ﬁsh
and crayﬁsh can have profound effects on the rest of the benthic community. In this
paper we will 1) review the well-studied trophic and ecological relationships between ﬁsh
and crayﬁsh and 2) posit other potentially important but less-studied interactions. Fish
and crayﬁsh have generally been viewed as predator-prey. Crayﬁsh are not easy prey for
many ﬁsh because of their large size and defensive armor, and a number of studies have
shown that the relative size of ﬁsh and crayﬁsh is a major factor affecting the predator-
prey interaction between these species. Crayﬁsh may also compete with small benthic
ﬁsh for food and shelter. Further, crayﬁsh have been implicated in the declines of ﬁsh
populations due to direct predation on ﬁsh eggs, and crayﬁsh may indirectly affect ﬁsh
populations through their destruction of macrophyte beds, which are important juvenile
ﬁsh habitats. Many of these more subtle interactions between ﬁsh and crayﬁsh were ﬁrst
observed when exotic species of crayﬁsh were introduced to a new system (either
intentionally or accidentally). More experimental work and long-term data sets are
necessary to discover the importance of these less-studied interactions between crayﬁsh

and ﬁsh. Careful consideration should be given to the multiple pathways of ﬁsh-crayﬁsh

ll

interactions when managing, farming, introducing, or studying these aquatic

macroconsumers .

KEYWORDS: competition, crayﬁsh, egg predation, ﬁsh, predator, prey

INTRODUCTION

Recent research in freshwater systems has documented a rich array of ecological
interactions between ﬁsh and benthic invertebrates. These interactions include top-down
effects of ﬁsh on benthos; e.g., effects of ﬁsh on invertebrate densities (Diehl 1995,
Batzer 1998), invertebrate size-structure (Mittelbach 1988), species composition (Power
1992, McPeek 1990), behaviour (Wooster and Sih 1995, Lima 1998), and morphology
(J ohansson and Samuelsson 1994). Similarly, bottom-up effects of benthic invertebrates
may signiﬁcantly inﬂuence ﬁsh diets (Crowder and Cooper 1982), habitat use (Werner et
al. 1983a), growth rates (Diehl and Kornijow 1998), and abundances (McIvor and Odum
1988). In many of these interactions, body size plays an important role. For example,
most freshwater ﬁsh are size-selective foragers (Wootton 1990, Gerking 1994), often
feeding preferentially on large invertebrates (Mittelbach 1988). Consequently, intense
ﬁsh predation may shift the size-structure of benthic invertebrate communities towards
smaller individuals and smaller species (Strayer 1991).

In most cases, ﬁsh are much larger than the benthic invertebrates they feed upon.
When this is true, the relationship between invertebrate size and ﬁsh foraging preference
is relatively simple — bigger is better. Larger invertebrate prey generally provide the

highest energetic gain (Mittelbach 1981, Persson and Crowder 1998), and ﬁsh growth

12

rates have been shown to be positively correlated with the abundance of large, benthic
invertebrates (Mittelbach 1988). However, some benthic invertebrates may reach large
enough sizes, or may be sufﬁciently well armored, that larger individuals are no longer
vulnerable to most ﬁsh predators. When this is the case, trophic interactions between ﬁsh
and benthos become more complex.

Crayﬁsh (Decopoda) are among the largest freshwater benthic invertebrates. As
they often dominate benthic invertebrate biomass, crayﬁsh provide a rich prey resource
for some freshwater ﬁsh. Due to their large size and defensive armor, crayﬁsh are not
easy prey for all ﬁsh, which complicates the trophic interactions. In this paper, we ﬁrst
document the importance of crayﬁsh to benthic invertebrate production in many
freshwater systems, and the importance of crayﬁsh to the diets of benthic-feeding ﬁsh.
We then examine predator-prey interactions between ﬁsh and crayﬁsh. Lastly, we
explore some less well-studied direct and indirect interactions between these two
freshwater macroconsumers.

TROPHIC RELATIONSHIPS

Crayﬁsh are often signiﬁcant components of benthic invertebrate production
(Rabeni et al. 1995, Momot 1995), and many studies report crayﬁsh dominating benthic
standing stock biomass (Huryn and Wallace 1987, Grifﬁth et a1. 1994, Momot 1995).
Because crayﬁsh are omnivores, they provide direct links from both primary production
and detrital-based food webs to ﬁsh (V annote and Ball 1972, Rabeni 1992, Roell and
Orth 1993). Fish have been shown to be important consumers of annual crayﬁsh
production in many systems (Table 1), and ﬁsh predation may provide top-down control

on crayﬁsh densities. For example, Mather and Stein (1993) and Lodge and Hill (1994)

13

found a signiﬁcant inverse relationship between densities of predaceous ﬁsh and crayﬁsh.
Svardson (1972) further showed that in Sweden, where eels (Anguilla anguilla) and
crayﬁsh (Astacus astacus) are largely allopatric, the introduction of eels generally leads to
the local extermination of crayﬁsh. Largemouth bass (Micropterus salmoides) have also
been shown to signﬁcantly reduce or eliminate crayﬁsh from aquaculture ponds (0.1-4 ha)
(Taub 1972, Rickett 1974). In contrast to the above studies, Gowing and Momot (1979)
concluded that predation by brook trout (Salvelinusfontanilis) had little control of
crayﬁsh production in an inland Michigan (USA) lake. However, due to gape limitation,
brook trout in this study were only able to feed upon juvenile crayﬁsh, limiting their
ability to control crayﬁsh numbers. Additional long-term experimental studies using
natural densities of crayﬁsh and their predators are needed to determine the extent of
"top-down" inﬂuences on crayﬁsh abundances.

The importance of crayﬁsh in diets of several ﬁsh species is summarized in Table
2. Some ﬁsh species feed heavily on crayﬁsh (e.g., smalhnouth bass, Micropterus
dolumieu, rock bass, Ambloplites rupestris, and ﬂathead catﬁsh, Pylodictis olivaris),
while other ﬁsh are more opportunistic and consume crayﬁsh infrequently (e. g., walleye,
Stizostedion vitreum, black bullhead, Ictalurus melas, northern pike, Esox lucius). Small,
gape-limited ﬁsh or fully pelagic ﬁsh are likely to feed on only the smallest crayﬁsh.

The importance of crayﬁsh in ﬁsh diets increases with ﬁsh age and size. In
general, YOY (young of the year) ﬁsh rarely consume crayﬁsh due to limitations in
mouth gape (Rabeni 1992, Roell and Orth 1993). For those ﬁsh species that feed
extensively on crayﬁsh, the percentage of crayﬁsh in the diet increases during ontogeny

(Keast 1977, Dehli 1981, Roell and Orth 1993). These ontogenetic diet shifts are due to

14

changes in the relative vulnerability of crayﬁsh as ﬁsh size increases (Stein 1977). The
proportion of crayﬁsh in a species’ diet may also vary widely among systems (Table 2).
For example, Gowing and Momot (1979) found that trout from lakes with high trout
stocking densities consumed more crayﬁsh than trout stocked into lakes at low density.
Wells (1980) found that perch foraging over rocky substrate in Lake Michigan utilized
crayﬁsh to a greater degree than perch foraging over sandy bottoms. Crayﬁsh are
generally more common in rocky substrate (J anssen and Quinn 1985, Kershner and Lodge
1995) and therefore perch may consume crayﬁsh in proportion to their abundance.
Experiments in large enclosures or ponds are necessary to verify these contentions. Ward
and Neumann (1998) suggested that largemouth bass consumption of crayﬁsh changes
with seasons (most eaten during summer-fall), and that bass consume'more crayﬁsh in
systems where forage ﬁsh are scarce. Seasonal variation in average crayﬁsh size and
molting stage also affects their vulnerablity to ﬁsh predation. Most crayﬁsh molt 1-3
times per growing season. Following a molt, even a large crayﬁsh can be extremely
vulnerable to predation (Stein 1977). Below we consider in more detail the factors that
inﬂuence the predator-prey interaction between ﬁsh and crayﬁsh.
TRADITIONAL PREDATOR-PREY STUDIES
Effects of body size and substrate
A number of studies have examined interactions between predatory ﬁsh and their
crayﬁsh prey. Stein and Magnuson (1976) and Stein (1977) report a series of
experiments in which smallmouth bass preyed upon crayﬁsh (Orconectes propinquus). In
these experiments, crayﬁsh size was inversely related to feeding preference with the

smallest crayﬁsh eaten ﬁrst. Reproductive (Fl) males and gravid females were the least

15

vulnerable life stages, while recently molted crayﬁsh were the most vulnerable. Stein
(1977) also found that the interaction between ﬁsh and crayﬁsh size was inﬂuenced by
substrate size. If we assume that absolute vulnerability to ﬁsh predation cannot increase
above that experienced on bare sand, we can hypothesize the interaction between crayﬁsh
size and substrate size looks something like Figure 1. At small substrate sizes (sand),
small crayﬁsh have the highest vulnerability to predation. When substrate (rock) size
increases to a threshold value, the smallest crayﬁsh (10 mm) experience a refuge from
predation by using the substrate as shelter. Consequently, intermediate-sized crayﬁsh (20
mm) are most vulnerable and eaten ﬁrst. As substrate size increases still further, a greater
number of these intermediate size crayﬁsh can utilize the substrate. Largest crayﬁsh can
utilize only large rocks for shelter but maintain relatively low vulnerability regardless of
the substrate size. Although this relationship is consistent with experimental evidence in
gravel bottom pools, the ability of crayﬁsh to burrow in soft sediments or clay may
change the interaction substantially (see Vorburger and Ribi 1999).
Eﬁfacts on fish on crajﬁsh behaviours

In the presence of predatory ﬁsh, crayﬁsh alter their microdistn'butions (Stein
1977, Hill and Lodge 1994) and activity levels (Stein and Magnuson 1976, Resetarits
1991). Field studies and experiments indicate crayﬁsh use more cobble habitat (or
otherwise structured habitat) and use less open sand in the presence of predaceous ﬁsh
(Stein and Magnuson 1976, Stein 1977, Hill and Lodge 1994, Lodge and Hill 1994,
Kershner and Lodge 1995, Mather and Stein 1993). In the absence of predatory ﬁsh,
crayﬁsh tend to prefer the substrate which provides the greatest food availability, while in

the presence of predators crayﬁsh prefer substrate with the most available refuge (Hill and

16

Lodge 1994). Regardless of the presence of ﬁsh predators, crayﬁsh become more evenly
distributed across sand, cobble, and macrophyte habitats at night (Hill and Lodge 1994).
Crayﬁsh foraging activity is generally suppressed in the presence of predatory ﬁsh
(Stein and Magnuson 1976, Resetarits 1991), while chelae displays and other behaviors
reducing vulnerability increase (Stein and Magnuson 1976). Crayﬁsh with large chelae
(males) seem to be affected least by the presence of ﬁsh predators (Stein 1977, Stein and
Magnuson 1976). Blake and Hart (1993) studied the effects of chemical and visual
predator cues on crayﬁsh activity levels. Crayﬁsh (Pacifasticus leniusculus) given
chemical stimuli of either perch (Percaﬂuviatilis) or eels (Anguilla anguilla) reduced
activity levels during both night and day periods. When given visual stimuli without
prior chemical cues, crayﬁsh only changed behavioral patterns during the day. Hamrin
(1987) also found that patterns of crayﬁsh diel activity levels were altered by the presence
of ﬁsh predators. However, in Hamrin’s study, total crayﬁsh activity actually increased in
the presence of crepuscular ﬁsh predators. Hamrin’s (1987) result runs counter to the
ﬁndings of Stein and Magnuson (1976), Resetarits (1991), and Blake and Hart (1993).
This result was probably due to predatory treatments that did not involve both visual and
chemical cues. In the predator treatments, crayﬁsh were placed in plexiglass tubes, which
likely limited the chemical signals necessary for crayﬁsh to alter (decrease) nighttime
activity levels. In summary, the presence of predatory ﬁsh has negative affects on
crayﬁsh activity levels. Further, these reductions in activity have been shown to have
signiﬁcant negative effects on crayﬁsh growth rates (Resetarits 1991, Hill and Lodge

1999). In addition, Hill and Lodge (1995) found increased macrophyte and

17

macroinvertebrate densities in mesocosms where crayﬁsh experienced the presence of
bass.

Crayﬁsh species are differentially susceptible to ﬁsh predation (Didonato and
Lodge 1993, Garvey et al. 1994), and ﬁsh predation may facilitate invasions by exotic
crayﬁsh species (Hill and Lodge 1998, deerback 1994). For example, in northern
Wisconsin (USA), Orconectes rusticus (the rusty crayﬁsh) has invaded lakes previously
occupied by two congeners (0. propinquus and 0. virilis) (Olsen et al. 1991, Hobbs et al.
1989). 0. rusticus has excluded the native crayﬁsh in these lakes and the evidence
suggests that ﬁsh predation is a signiﬁcant mechanism involved in the replacement of the
native crayﬁsh species by 0. rusticus (Didonato and Lodge 1993, Garvey et al. 1994,
Hobbs et al. 1989, Hill and Lodge 1998). In mixed species assemblages, 0. rusticus is
more successful at obtaining available shelters and is relatively less vulnerable to ﬁsh
predation on open sand (Garvey et al. 1994). As a result, bass selectively feed on the
exposed and relatively more vulnerable 0. virilis and 0. propinquus, while 0. rusticus
are avoided (and thereby persist). Overall, 0. rusticus is able to maintain higher growth
and lower mortality than the two native Orconectes in the presence of predaceous ﬁsh
(Hill and Lodge 1999). This example is likely analogous to the replacement of Astacus
astacus by the introduced Pacifasticus leniusculus in Swedish lakes where the data
indicate preferential perch predation on the native A. astacus (deeer 1994).

INTERACTIONS BETWEEN CRAYFISH AND SMALL BENTHIC FISH

Although small benthic ﬁsh like sculpins (European bullheads -Cottus spp.) or
darters (Etheostoma spp.) are generally too small to feed on crayﬁsh, these ﬁsh species

share common adult sizes, food resources, and predators with crayﬁsh. Therefore,

18

crayﬁsh and smaller benthic ﬁsh may interact competitively. However, these interactions
are less well-studied than the standard predator-prey interactions of ﬁsh and crayﬁsh.
Studies of interactions between small benthic ﬁsh and crayﬁsh include competition for
limited shelters (Guan and Wiles 1997), competition for food (Miller et al. 1992),
behavioral interactions in the presence of predators (McNeely et al. 1990), and
combinations of these interactions (Rahel and Stein 1988, Wojdak and Miner
unpublished manuscript).

In studies of competition for shelters, the results are mixed and dependent upon
the species of ﬁsh and crayﬁsh studied. Guan and Wiles (1997) found signiﬁcant
competition for shelter between the introduced crayﬁsh Pacifasticus leniusculus and two
benthic ﬁsh (Cottus sp. and Neomacheilus sp.) in a British lowland river. In laboratory
experiments, crayﬁsh excluded ﬁsh from shelters, and ﬁeld surveys showed inverse
correlations between ﬁsh and crayﬁsh abundances (Guan and Wiles 1997). Rahel and
Stein (1988) found similar results with darters (Etheostoma sp.) and the crayﬁsh 0.
rusticus. In the laboratory, crayﬁsh evicted darters from shelters and caused them to
increase overall activity; this increased darter susceptibility to smallmouth bass predation.
Wojdak and Miner (unpublished manuscript) found that an introduced ﬁsh species, the
round goby (Neogobius melanostomus) had the opposite effect on the crayﬁsh
(Orconectes rusticus). In laboratory experiments, gobies competitively excluded crayﬁsh
from shelters and exposed the crayﬁsh to increased bass predation. Thus, results of
competition for shelter seem dependent upon the speciﬁc pair of species under study.

McNeely et al. (1990) found a complex behavioral interaction between 0.

putnami and the mottled sculpin (C. bairdi). In the presence of bass and crayﬁsh,

19

sculpins experienced less predation. This interaction involved a change in predator-
avoidance behavior by the sculpin, dependent upon crayﬁsh presence or absence. When
crayﬁsh were absent the sculpin utilized few shelters and employed a stationary behavior
to avoid predator detection. In the presence of crayﬁsh, sculpin increased use of shelter to
avoid predation. The crayﬁsh in this study were relatively invulnerable to predation and
did not alter shelter use dependent upon bass presence or absence. However, the
increased benthic activity of crayﬁsh was thought to “draw the attention of the bass away
from the sculpin” (McNeely et al. 1990).

Crayﬁsh and equivalent-sized small benthic ﬁsh share common predators and
shelters. From the above studies it is clear that competitive outcomes for common
refugia are less than predictable. Complex behavioral interactions and agonistic
exclusions act to make the outcomes of these interactions speciﬁc to particular ﬁsh-
crayﬁsh pairs. If introduced species of benthic ﬁsh and crayﬁsh competitively exclude
natives, this could lead to restructuring of the benthic food web as carnivorous benthic
ﬁsh and omnivorous crayﬁsh replace each other. Competition between benthic ﬁsh and
crayﬁsh for common food resources is a virtually unstudied area that deserves future
research.

Trophic energy transfer, predator-prey interactions, and competition are the most
obvious ways in which ﬁsh and crayﬁsh may interact. However, there are a number of
other potential pathways by which ﬁsh and crayﬁsh populations may be linked. In the
next section, we outline a few of the more subtle interactions that may occur between ﬁsh
and crayﬁsh. Much of the impetus for this section comes from studies that have

examined the effects of exotic crayﬁsh introductions (Hobbs et al. 1989) which have led

20

to many insights about the roles of crayﬁsh in freshwater communities (Lodge et al.
1998).
POTENTIAL NEGATIVE EFFECTS OF CRAYFISH ON FISH
Egg predation

In some northern Wisconsin lakes (USA), the decline of gameﬁsh populations has
been attributed to the invasion of the exotic crayﬁsh 0. rusticus (Hobbs et al. 1989). Egg
predation has been proposed as one mechanism causing declines in bass, sunﬁsh
(Centrarchidae), walleye, and lake trout (Salvelinus namaycush). Observations indicate
that sunﬁsh only nest in areas where 0. rusticus have been experimentally removed (K.
Wilson, University of Wisconsin, Madison, USA -pers. comm.) In experiments, crayﬁsh
(Orconectes spp.) ate lake trout eggs (Savino and Miller 1991, Horns and Magnuson
1981), and rates of egg predation ranged from 2-5 eggs-crayﬁsh"-day", depending upon
temperature, substrate, and crayﬁsh species. Given this rate of predation, Savino and
Miller (1991) concluded that predation by crayﬁsh on lake trout eggs will only be
important over a restricted set of conditions: high crayﬁsh density and/or low egg density
within cobble habitat.

The potential for crayﬁsh to consume the eggs of warmwater ﬁsh may be greater.
Bass and sunﬁsh spawn at much warmer temperatures than lake trout, and Horns and
Magnuson (1981) have shown that the rate of egg consumption by crayﬁsh increases with
temperature. Further, most bass and sunﬁsh concentrate their eggs in shallow, littoral
zone nests, which may make them more vulnerable to crayﬁsh predation than the widely
scattered eggs of trout or walleye. If crayﬁsh can inﬁltrate these nests and/or feed

unnoticed at night, egg predation on warmwater gameﬁsh may be signiﬁcant.

21

Destruction of macrophyte beds and eﬁfects on ﬁsh recruitment

Macrophytes are known to disappear in the presence of crayﬁsh (F eminella and
Resh 1989, Matthews and Reynolds 1992, Lodge et al. 1994, Olsen et al. 1991, Chambers
et al. 1990). Some of the macrophyte destruction is due to active crayﬁsh feeding, while
a substantial amount is due to non-consumptive fragmentation (Lodge and Lorman 1987,
Olsen et al. 1991). In this manner, crayﬁsh may be viewed as ecosystem engineers -
modifying the structural complexity of littoral zones through non-consumptive means
(Lawton 1994, Jones et al. 1994).

For many ﬁsh species, macrophyte beds serve as important juvenile habitat
(Mittelbach 1981). Dense stands of littoral-zone macrophytes provide shelter from
predatory ﬁsh (Werner et al. 1983b), and also provide a source of vegetation-dwelling
invertebrate prey (Osenberg and Mittelbach 1989, Persson and Greenberg 1990).
Complex structural habitats (macrophyte beds) decrease the efﬁciency of piscivorous ﬁsh
(Persson and Crowder 1998) affording protection for growing juvenile ﬁsh. When
juveniles of different ﬁsh species take advantage of this littoral vegetated habitat,
competition may occur (Mittelbach 1984, 1988). Ifmacrophyte beds shrink following
crayﬁsh introductions, competition between juvenile ﬁsh for the remaining macrophyte
refuge or associated invertebrate prey may increase. A loss of vegetated habitat may also
lead to changes in competitive advantage between ﬁsh species (Persson 1991).

When exotic crayﬁsh species such as 0. rusticus and Procambarus clarki were
introduced to water bodies, large losses in macrophytes were observed (Lodge and
Lorman 1987, F eminella and Resh 1989, Lodge et al. 1994). Additional studies of P.

leniusculus and 0. virilis in Sweden and Canada respectively, support the hypothesis that

22

exotic crayﬁsh species will have large effects on macrophyte biomass, species richness,
and associated invertebrate community structure/abundance when introduced (N ystrom
and Strand 1996, Chambers et al. 1990, Hanson and Chambers 1995). The link between
macrophyte losses and effects on ﬁsh recruitment are logically sound, yet remain
unexplored.

CONCLUSIONS

Fish and crayﬁsh have traditionally been viewed as predator and prey. Recent

 

 

studies, however, document a wealth of potential interactions between these 1
macroconsumers. Many of these interactions were ﬁrst observed when an exotic species
of crayﬁsh entered a system. Although predatory ﬁsh generally suppress crayﬁsh activity,
growth, and population densities, there are a number of examples where ﬁsh have been
shown to have much smaller impacts on exotic crayﬁsh. In one well-documented
example, ﬁsh were found to accelerate the rate at which an exotic crayﬁsh, 0. rusticus,
invades new lakes (Hill and Lodge 1999).

Although conclusive data are lacking, introduced benthic ﬁsh (e.g., gobies) and
crayﬁsh (P. leniusculus) may competitively exclude native ﬁsh and crayﬁsh with
potentially important consequences for structuring of benthic food webs. Future work in
this area should I) investigate the invasion ecology and competitive arenas between
benthic ﬁsh and crayﬁsh, and 2) examine the trophic effects of swapping carnivorous
benthic ﬁsh and omnivorous crayﬁsh in benthic food webs.

While most studies have focused on the predatory effects of ﬁsh on crayﬁsh, there
are a number of ways in which crayﬁsh may negatively affect or control ﬁsh production.

For example, crayﬁsh eat ﬁsh eggs, and warmwater ﬁsh species may be especially

23

vulnerable to crayﬁsh egg predation. Crayﬁsh also destroy macrophytes, which in turn
reduces important habitat for juvenile ﬁsh (Mittelbach 1984, Persson and Crowder 1998).
Future research in these areas should concentrate on the consequences of egg predation
and macrophyte destruction (ecosystem engineering) for warmwater ﬁsh production.
Between species differences in egg predation and macrophyte destruction should be
examined to highlight potential consequences of crayﬁsh introductions. Understanding
the mechanisms of interaction between ﬁsh and crayﬁsh is crucial if we are to be able to
predict the consequences of species introductions, both intentional and accidental (Lodge

et al. 1998).

ACKNOWLEDGEMENTS
We thank Nicole Coineau for the invitation to contribute to this special issue of
Vie et Milieu. David Lodge, Bill Perry, Jeremy Wojdak, Karen Wilson, and an
anonymous reviewer provided thoughtful comments on earlier versions of the manuscript.
This work was supported by the Graduate Research Training Group at the Kellogg

Biological Station (NSF grant DIR-9602252) and it is KBS contribution number 895.

24

 

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30

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33

CHAPTER 3

EGG PREDATOR EFFECTS ON FISH REPRODUCTIVE SUCCESS AND
NESTING BEHAVIOR

with Gary G. Mittelbach
ABSTRACT
Early-life—stage predators can have profound effects on species population
dynamics and community structure. The early life stages of ﬁsh are vulnerable to a suite

of potential predators, yet relatively little is known about the impacts of egg- and ﬂy-

 

stage predators on ﬁsh reproductive success or breeding behavior. Crayﬁsh are l:
traditionally viewed as primary consumers and prey items for large ﬁsh, yet they are
capable of feeding on substrate-bound ﬁsh eggs and fry and their introductions have been
blamed for declining or disappearing ﬁsh populations in Europe and North America. We
manipulated crayﬁsh presence and absence in two replicated pond experiments and
measured their effects on the reproductive success of two species of sunﬁsh - bluegill
(Lepomis macrochirus) and pumpkinseed (L. gibbosus). In both experiments, crayﬁsh
delayed (or prevented) successful reproduction, and the biomass of larval ﬁsh produced
by the sunﬁsh was signiﬁcantly lower in the presence of crayﬁsh. In the experiment with
bluegill, crayﬁsh inhibited all successful reproduction. However, when we added
crayﬁsh-proof exclosures to the experiment, the ﬁsh located the crayﬁsh-free habitat and
reproduced successfully. This work highlights the importance of egg/nest predation to
ﬁsh reproductive success and nest site selection and it has important implications for
understanding how early-life-stage predators may impact the spawning landscape of ﬁsh.

These experimental results also provide evidence for egg predation as a mechanism that

34

can explain observed declines in ﬁsh populations following the invasion or purposeful

introductions of crayﬁsh.

KEYWORDS: bluegill, crayﬁsh, egg predation, Lepomis, nest habitat, nest site choice,

Orconectes, predator-prey, pumpkinseed, sunﬁsh

INTRODUCTION

The early-life-stages of species are especially vulnerable to predators and high
mortality on these stages can have strong effects on the recruitment dynamics of
populations (Werner and Gilliam 1984, Martin 1993, Howe and Brown 2000). However,
early-life-stage mortality events can be difﬁcult to observe and quantify in the ﬁeld,
hindering our ability to identify important stage-speciﬁc predators and measure their
impacts. Losses of recruits to predators begins at the egg and seed stage for animals and
plants respectively. Egg/nest predation has been well-studied in avian systems, and nest
predation (in combination with habitat features or fragmentation) has been cited as a
major factor determining habitat-partitioning, species coexistence, community
composition and recruitment failure for birds (Martin 1993, Robinson et al. 1995).
Likewise, in grasslands and forests, seed predation can have profound impacts on plant
populations and community structure (Schupp 1990, Howe and Brown 1999, 2000). The
importance of egg/nest predators for ﬁsh behaviors, populations, and communities is
comparatively unknown.

For many species of ﬁsh, the earliest egg and fry stages are closely associated

with benthic substrates or vegetation for days to months (Breder and Rosen 1966). In

35

these substrate-bound habitats the eggs and fry are vulnerable to a suite of predators that
pose little or no threat to larger and more mobile life-stages. A variety of species are
known to feed on the early-life-stages of ﬁsh (e.g., Gross and MacMillan 1981, Deblois
and Leggett 1993, M01 1996, Selgeby 1998, Dom and Mittelbach 1999), however
surprisingly little is known about the potential impact of any of these predators on
species’ reproductive success or spawning habitat use. This is in contrast to the well-
studied effects of piscivorous predators on ﬁsh feeding behaviors and foraging habitat
choice (e.g., Lima and Dill 1990, Mittelbach 2002).

Theory developed for avian systems predicts that predation rates on nests can be
inﬂuenced by nest site characteristics (Schmidt 1999), and that favorable nests should
therefore be defendable, cryptic, or located in habitats where brood predators are rare. If
reproducing animals can discriminate amongst breeding sites, then nest defensibility, the
spatial heterogeneity of nest/egg predators, or the presence of predator-free nest-space,
may be important features determining the habitat choice and reproductive success of
individuals and populations. While some animals seem to aggregate their nests for group
defense (e. g., Tyler 1995, Wiklund and Andersson 1994), other animals breed in sites or
habitats where the frequency of encounter with brood predators is low (e. g., Marzluff
1988, Clark and Shutler 1999, Schmidt 1999, Ostlund-Nilsson 2000). For example,
ducks and other waterfowl are commonly observed nesting in high densities on islands
that lack mammalian nest predators (Clark and Shutler 1999). A few observations
suggest that ﬁsh might be selecting breeding sites based on relative predation risk to their

eggs (Beaucharnp et al. 1992, Knapp 1993, Takemon and Nakanishi 1998, (5de-

36

Nilsson 2000), but direct experimental tests of the effects of egg predators on the
reproductive success and nesting habitat use of ﬁsh populations are lacking.

Crayﬁsh (Decapoda) have historically been considered detritivores and
herbivores (Momot 1995) and have been commonly introduced to lakes and streams as
forage for ﬁsh, to reduce unwanted macrophytes (Hanson and Chambers 1995), or to
provide human food (Gherardi and Holdich 1999). However, crayﬁsh are relatively large
invertebrates with polytrophic feeding habits, leading some to suggest that crayﬁsh are
important aquatic predators (e. g., Momot 1995) and potentially important predators of
ﬁsh eggs (Hanson and Chambers 1995, Dorn and Mittelbach 1999). Recent studies from
Europe and North America implicate introduced crayﬁsh in the decline of ﬁsh
populations in rivers, lakes, and streams (Guan and Wiles 1997, Covich et al. 1999,
Nystrom 1999, Wilson 2002, Bryan et al. 2002). The mechanisms for the negative
effects of crayﬁsh on ﬁsh are largely unknown, but predation on substrate-bound eggs or
fry is one oft-cited hypothesis. In this paper we report the results from two ﬁeld
experiments designed to examine the impacts of crayﬁsh egg predation on the
reproductive success and nesting behavior of two species of North American sunﬁsh:
bluegill (Lepomis macrochirus, Raﬁnesque) and pumpkinseed (Lepomis gibbosus,
Linnaeus).

Sunﬁsh (Centrarchidae) are distributed throughout much of Eastern North
America. The bluegill and pumpkinseed are two of the most common species, both are
medium-sized ﬁsh (adults 10-20 cm standard length (SL)) and in southern Michigan they
often account for >75% of total ﬁsh biomass in small lakes and ponds (Werner et al.

197 7). Bluegill and pumpkinseed reproduce repeatedly over several weeks in the late

37

spring/early summer after water temperatures reach 18-20°C. Large adult males
construct depressions (nests) by fanning the substrate with their caudal ﬁns. Males
defend the nest, solicit eggs from females, and guard the brood until the young swim off
the nest (6-10 days post egg deposition). Male pumpkinseeds tend to nest in a solitary
manner while bluegill usually aggregate their nests into colonies. Colony nesting is
thought to have evolved as a defense against egg predators (Gross and MacMillan 1981).
MATERIALS AND METHODS

We conducted two ﬁeld experiments to examine the effects of crayﬁsh on the
reproductive success and nesting behavior of sunﬁsh. The experiments were conducted
at the Kellogg Biological Station’s experimental pond facility in southwestern Michigan.
The crayﬁsh Orconectes virilis (Hagen) was stocked into previously crayﬁsh-free ponds
in our experiments. 0. virilis is widely distributed throughout the eastern United States »
and Canada and is considered native to the upper midwest, however, it has been
introduced to previously crayﬁsh-free streams in Arizona (USA, Bryan et al. 2002) and
lakes in western North America (Hepworth and Dufﬁeld 1987, Hanson and Chambers
1995). 0. virilis can be found in several lakes around the Kellogg Biological Station,
including the lake from which we collected the ﬁsh. For the experiments we collected
crayﬁsh in large numbers from ponds at the Michigan Department of Natural Resources
research station in Saline, Michigan. The 1999 experiment examined the effects of
crayﬁsh on pumpkinseed reproductive success, while the 2001 experiment examined the

effects of crayﬁsh on bluegill reproductive success and nesting behavior.

38

1999 Pumpkinseed experiment

Six 30-year-old ponds (each 26 m dia.) were used for the 1999 experiment. These
ponds had a heavy cover of macrophytes that reached to the pond surface by mid-summer
and they were surrounded by a border of cattails (Typha). The ponds were drained in
March 1999 and were allowed to sit empty for approximately 2 months, after which they
were reﬁlled to 1.6 m depth in May. In June, twelve adult pumpkinseeds (6 of each sex)
were collected ﬁom a local lake and added to each pond (average standard lengths were
112-122 mm for males and 104-114 mm for females). Three of the 6 ponds were stocked
with crayﬁsh (mean carapace length (CL) of 38.5 mm) at 1.5 individuals/m2 (26 g wet
mass/m2) prior to ﬁsh addition, and three ponds served as no-crayﬁsh controls (hereafter
referred to as “crayﬁsh” or “no-crayﬁsh” ponds). Crayﬁsh reproduction in the ponds was
extremely low in our experiments, as most females had already dropped their young prior
to stocking. We used standardized trapping techniques (Lodge et al. 1986) on 3-4 dates
throughout each summer to quantify crayﬁsh activity-density. Crayﬁsh were trapped
overnight (15-18 hr sets) using 2-4 Gee minnow traps (Nylon Net Co.) per pond with
openings adjusted to 4 cm. Traps were baited with 120 g of beef liver and set in the
ponds (at least 5 m apart) at 17-1 8:00 on each trap date.

Nighttime observations of active nests and crayﬁsh predation were made from the
shoreline at 2-4 day intervals from the beginning of the experiment (12 June) through 14
July. In both experiments, an active nest was deﬁned as any unmolested nest containing
eggs or ﬂy. Nesting observations were analyzed using repeated measures AN OVA (SAS

5.0, SAS Institute).

39

Young-of-the-year (YOY) ﬁsh were sampled in July and September 1999. In
July (when ﬁsh were very small) we sampled with a wall seine (2.3 x 2.9 m with 1.8-mm-
mesh fabric) attached to two wooden poles and operated by two swimmers (as in Rettig
and Mittelbach 2002). The seine was placed in the middle of the pond and swum through
the water towards shore, seining one radius of the pond. In September, when YOY ﬁsh
were larger, the ponds were sampled with a bag seine (23 m long with 3.2-mm-mesh)
covering approximately 15% of the pond area in one seine haul. All collected ﬁsh were
euthanized with M8222 and preserved in 10% formalin or 95% ethanol. We calculated
total biomass sampled for each pond using average lengths (N=35 ﬁsh) and pond speciﬁc
length-wet mass regressions. Biomass, mean individual mass, and numbers of YOY
were analyzed using ANOVA (Systat 9.0).

We used otolith analysis to examine the effects of crayﬁsh on the timing of
successful larval production. Otoliths (ﬁsh ear bones) were removed from a random
sample of at least 35 YOY collected from each pond in September, and prepared using
standard methods (Stevenson and Campana 1992). Brieﬂy, sagittal otoliths were
extracted and placed in a clear glue (Crystalbond Adhesive 509, Aremco Products Inc.)
on a microscope slide. The otoliths were polished when necessary and viewed under a
compound microscope at 10—40x magniﬁcation. Daily rings (Taubert and Coble 1977)
on the right otolith were counted twice and averaged to determine ﬁsh age. If the two
counts differed by >2 days, we made a third count and used the average of the two most
similar counts. A few ﬁsh (<5) were discarded due to the inability to clearly read the

daily rings. Differences between treatments in YOY age were analyzed using both

40

parametric tests of pond-speciﬁc averages and a non-parametric test of the summed
distributions.

We also checked for differences in YOY growth rates between treatments by
regressing ﬁsh mass against ﬁsh age in each pond, and then using ANOVA to compare
the ﬁtted slopes of the regression lines (estimates of the increase in mass per day).

2001 Bluegill experiment

The six ponds used in the 1999 experiment were renovated during the summer of
2000 as part of an overall pond renovation at the experimental pond facility. Sediments
and plastic liners were removed and replaced, with each pond receiving ~ 25 cm of a
homogeneous sand and clay mixture. Ponds were ﬁlled to 2 m deep (29 m dia.) in
November of 2000 and were allowed to colonize naturally with algae, macrophytes, and
invertebrates from nearby ponds. At the beginning of the experiment the ponds had
substantial populations of zooplankton, benthic invertebrates, clouds of ﬁlamentous
metaphytic green algae (Zygnema and Cladophora spp.), and sparse macrophytes. F orty-
ﬁve reproductive bluegill were stocked into each pond in June 2001. The populations
stocked into each pond included 15 females (range of pond mean lengths = 129-131 mm
SL), 15 large males (129-131 mm SL) and 15 small males (67-69 mm SL). The two male
sizes correspond to the two commonly observed reproductive strategies described by
Gross (1982) as “parentals” (larger nest-builders and guarders) and “sneakers”. Crayﬁsh
were stocked at a similar density as in the 1999 experiment (1.4S/m2), however the

crayﬁsh were smaller (mean CL = 29 mm) and therefore the biomass was lower (9.5

g/mz).

41

A complete census of nesting activity in each pond was conducted every 2-3 days
from 12 June - 3 August by divers using mask and snorkel or SCUBA. On each sampling
date, the entire pond bottom was censused for active nests as well as evidence of nest
attempts. Successful reproduction, as measured by recruitment to the free-swimming
larval stage, was quantiﬁed with nighttime (22:00) ichthyoplankton net tows pulled
across the surface of the pond once per week. Nighttime tows were employed to reduce
the effects of net avoidance. Equal sampling effort was applied to each pond. The
ichthyoplankton net (0.5-mm-mesh with opening of 68 cm diameter) was towed 27 m at
0.75 m/s, and captured larval ﬁsh (<8-10 mm SL) in the upper 68 cm of the water
column. Larvae were preserved in 10% formalin, enumerated, and a random sample was
measured for standard length.

On 5 July, one crayﬁsh-proof exclosure was added to each of the three crayﬁsh
ponds. The exclosures measured 1.9 m2 in area with walls made of 50-cm tall aluminum
ﬂashing and bottoms of ﬁberglass screen (1 .2-mm-mesh). Each exclosure was ﬁlled with
approximately 5 cm of substrate taken from the pond bottom. Exclosures were placed
approximately 4 m from the center of the pond (away from the area of previously
attempted nesting).

RESULTS
1999 Pumpkinseed experiment

Crayﬁsh did not have a signiﬁcant effect on the number of active nests observed
in the ponds through time (rmAN OVA treatment and treatment‘time effect p values
>036). On several nights in June and early July, crayﬁsh were observed feeding on

pumpkinseed eggs or fry inside nests (>10 crayﬁsh in a single nest on one occasion).

42

Pumpkinseeds attempted to defend their nests by rushing at the crayﬁsh with open
mouths, and occasionally biting the crayﬁsh on top of the carapace. In response, crayﬁsh
would either raise their chelae in defense, or back away from the nest. Crayﬁsh activity-
density over the summer averaged 1.9 individuals per trap-night (S.E.=0.2, N=3 dates).

YOY ﬁsh biomass sampled in July and September was signiﬁcantly lower in the
crayﬁsh ponds than in no-crayﬁsh ponds (July F1,4=11.76, p=0.027; September
F1,4=10.39, p=0.032; Figure 1a). One crayﬁsh pond failed to produce any YOY ﬁsh by
the July sampling date. Nest destruction was observed several times in that pond and the
ﬁrst successful reproduction occurred in late July. The mean number of ﬁsh sampled per
pond was lower on average in crayﬁsh ponds (Figure lb), but was not statistically
different (July F1,4=1.43, p=0.3; September F .,4=l.1, p=0.35; Figure lb). YOY ﬁsh in
crayﬁsh ponds were signiﬁcantly smaller in July (F.,4=21.06, p=0.01) and were generally
smaller in September as well (F.,4=3.68, p=0.128; Figure lc).

Results of the otolith analysis indicated that YOY ﬁsh were born later in ponds
containing crayﬁsh (Figure 2). The distribution of YOY birthdates was signiﬁcantly
different when analyzed with a non-parametric Komolgorov-Smimov two-tailed test of
distributions (max. diff. = 0.575 two-sided p<0.001). The median birthdate also differed
by about 12 days between treatments (ANOVA F 1,4=7.175 p=0.055).

YOY ﬁsh mass correlated positively with age in all six of the ponds, however
there was no signiﬁcant difference between the slopes of the regressions for the two
treatments (F 1,5=0.401 , p=0.56), suggesting the YOY ﬁsh grew at similar rates in crayﬁsh

and no-crayﬁsh ponds.

43

2001 Bluegill experiment

In the no-crayﬁsh ponds, active nests (e. g., those with eggs or larvae) were ﬁrst
discovered on 14 June (2 days after addition of females), and bluegill in those ponds
continued to nest actively until 3 July (3-4 bouts of reproduction). By 14 June in crayﬁsh
ponds, bluegill had excavated nests in a similar spatial arrangement to the active nests
observed in the no-crayﬁsh ponds, and they kept them swept clean through mid-July.
However, no nests with eggs or fry were observed in the crayﬁsh ponds during the ﬁrst 4
weeks of the experiment (Figure 3a), and on two dates (14 and 29 June) we found
crayﬁsh destroying nests in two of the ponds. In each case, more than 30 crayﬁsh were
found swarming 4-5 nests that contained a few remaining bluegill eggs. Overall crayﬁsh
activity-density was higher in 2001 than in 1999 (2001 average activity=9.44 crayﬁsh per
trap-night, S.E.=0.92, N=4 dates).

On 5 July we added one crayﬁsh-proof exclosure to each crayﬁsh pond to
determine whether adult bluegill would be able to reproduce when given a crayﬁsh-free
nesting habitat. Eleven days later (16 July) active nests were observed inside the
exclosure in one pond. Within a few more days, male bluegill in the other ponds were
observed nesting within the exclosures; nesting activity continued until 3 August (Figure
3a). No crayﬁsh were observed inside the exclosures and active nests were never found
outside of the exclosures. Aﬁer nesting commenced in the exclosures, male bluegill
stopped sweeping off nests at the sites of previous nest attempts.

Larval bluegill were ﬁrst collected in the no-crayﬁsh ponds 14 days aﬁer the start
of the experiment (26 June), and abundant larvae were caught in tow samples for the

following 3 weeks (Figure 3b). After 16 July, most larval ﬁsh in the no-crayﬁsh ponds

had grown to a size (>10 mm Standard Length (SL)) at which they were able to avoid
capture by our towed ichthyoplankton net. However, divers in the no-crayﬁsh ponds
continued to observe YOY ﬁsh throughout the remainder of the experiment. In the
crayﬁsh ponds, no larval ﬁsh were captured prior to the addition of the exclosures (Figure
3b). However, bluegill larvae were caught in the crayﬁsh ponds 18 days after the
exclosures were added (23 July), and larval recruitment was especially strong on 30 July.
DISCUSSION

Effective species management and conservation requires scientists and managers
be able to identify important stage-speciﬁc interactions within and between species. It
has been well recognized that seed and nest predators can have profound impacts on the
population dynamics and community structure of plants and birds (Schupp 1990, Martin
1993, Robinson et a1. 1995, Howe and Brown 2000). Egg predators can also have major
impacts on population reproductive success of amphibians and reptiles (Petranka and
Kennedy 1999, Chalcraft and Andrews 1999). While a host of freshwater animals,
including many species recently introduced to the Great Lakes region (Segelby 1988,
Chotkowski and Marsden 1999, Lodge et al. 2000), are known to eat the early life-stages
of ﬁsh, little is known about the impacts of any of these organisms on ﬁsh reproductive
success, spawning behavior, or population size. Some attempts have been made to
quantify the impact of egg predators by extrapolating estimates of predator feeding rates
(e. g., M01 1996, F itzsimons et al. 2002), however, no experimental studies have
examined ﬁsh reproduction in the presence and absence of putative egg/fry predators.
Our results indicate that egg predation can be extremely important to the reproductive

success of sunﬁsh.

45

While our experimental ponds are small relative to most natural lakes, they are
good mimics of the shallow habitats where Lepomis sunﬁsh breed and the densities and
average activity-densities (i.e., trap CPUE) of crayﬁsh in our experiments were well
within the ranges observed for Orconectes crayﬁsh in Midwest (USA) lakes, ponds, and
streams. For example, Momot et al. (1978) report densities of 1.2-21.2 Orconectes
crayﬁsh/m2 (4.6-95.2 g/mz) ﬁom a variety of systems, and 0. virilis in particular was

found at densities of 1.9-6.1 crayﬁsh/ m2 (4.6-21.2 g/mz) in low productivity marl-bottom

 

Michigan lakes for several consecutive years. Activity-density (trap CPUE) of crayﬁsh
should give a good metric for comparing the potential impacts of crayﬁsh across systems
because it incorporates densities and system-speciﬁc foraging behavior, which could be
inﬂuenced by food levels (hunger) and predators. Activity-densities of Orconectes
crayﬁsh in lakes can range up to 30 or more (adult crayﬁsh) per trap (Capelli and
Magnuson 1983, Collins et al. 1983, Olsen et al. 1991, Lodge and Hill 1994, Richards et
al. 1996). Although many lakes with 0. virilis have activity densities < 2/trap (Capelli
and Magnuson 1983), a number of lakes have been found with activity-densities of 3.6 to
11.6/trap (Capelli and Magnuson 1983, Olsen et al. 1991). The invasive 0. rusticus and
another congener (0. proprinquus) can be found at much higher activity-densities (Olsen
et al. 1991, K. Wilson 2002 and personal communication).

The difference in YOY biomass between the crayﬁsh and no-crayﬁsh ponds in the
1999 pumpkinseed experiment was caused by a combination of YOY size and density.
The smaller average size of pumpkinseed YOY in the presence of crayﬁsh was consistent
with differences in age; YOY ﬁsh were born later on average in the ponds with crayﬁsh.

There was no evidence of differential YOY growth between the pond types. The

46

observed later YOY birth dates could be the result of pumpkinseeds becoming more
successful over time in the presence of crayﬁsh, either by adjusting their spawning
behaviors or changing nest site selection. Although we observed crayﬁsh completely
destroying nests on several occassions, male pumpkinseeds were persistent in their
reproductive attempts and variable in their nest site use. In some cases we found nests in
extremely shallow water (<20 cm), next to the bank, or in small aggregated groups.
These nesting behaviors may have led to the eventual successful production of larvae in
the presence of crayﬁsh and suggest that pumpkinseeds may adjust their nest site
selection or behavioral strategies in response to crayﬁsh egg predation.

Further evidence of changing nest site selection in response to crayﬁsh was
observed in the 2001 bluegill experiment when no YOY were produced in the crayﬁsh
ponds until after the addition of crayﬁsh exclosures. Active nests were never found in the
crayﬁsh ponds before the addition of crayﬁsh exclosures and crayﬁsh were observed
eating ﬁsh eggs on two occasions. The successful reproduction we observed following
the addition of crayﬁsh-exclosures indicates that adult ﬁsh had sufﬁcient resources to
reproduce, but simply lacked a safe nesting habitat. It is interesting to note that in the no-
crayﬁsh ponds bluegill reproduction followed the normal course of reproduction
observed in local lakes; most nesting occurs during 3-4 weeks in June and ceases early in
July. However, in the crayﬁsh ponds reproduction occurred much later and only after we
added the crayﬁsh exclosures. Clearly, bluegill have the ability to breed later into the
season. Active nesting may have ceased in the no-crayﬁsh ponds due to competition
between YOY ﬁsh and adults for zooplankton prey. Macrozooplankton in the no-

crayﬁsh ponds disappeared quickly after the YOY ﬁsh were produced while large

47

zooplankton in the crayﬁsh ponds remained abundant until the ﬁsh reproduced later in
the summer (Chapter 4).
Interactions of crayﬁsh and fish populations

Crayﬁsh have been introduced to waterbodies throughout the globe for purposes
of augmenting ﬁsh forage or controlling macrophytes (Hobbs et al. 1989, Hanson and
Chambers 1995). In addition to purposeful introductions, crayﬁsh have also been
inadvertently introduced to waterbodies through vectors like the bait trade (Lodge et al.
2000). While recent work indicates strong impacts of crayﬁsh on macrophyte,
macroinvertebrate, and amphibian populations (Chambers et al. 1990, Lodge et al. 1994,
Gamradt and Kats 1996, Nystrom 1999), there have been relatively few studies
examining the effects of crayﬁsh on ﬁsh populations (Dom and Mittelbach 1999).
Introduced crayﬁsh have been implicated in the demise of ﬁsh populations in European
rivers (Guan and Wiles 1997, Nystrom 1999) and North American lakes (Lodge et al.
1985, Covich et al. 1999, Wilson 2002), and 0. virilis, the crayﬁsh used in our
experiments, is believed to have negative impacts on native ﬁsh populations in Arizona
streams (Bryan et a1. 2002). In a recent study of crayﬁsh feeding rates and densities,
Fitzsimons et a1. (2002) indicate that Orconectes crayﬁsh could be important egg
predators of a coldwater, broadcast-spawning ﬁsh species (Lake trout - Salvelinus
namaycush) as well. Our experimental results provide the best evidence to date, and the
only experimental work, indicating that crayﬁsh are important egg predators of ﬁsh.

Egg predators and breeding habitats
In addition to their impact on reproductive success, egg/nest predators may also

affect nesting strategies or breeding site selection. Colonial breeding in birds and ﬁsh is

48

probably the best-known example of an anti-predator nesting strategy (Wiklund and
Andersson 1994, Tyler 1995 ), but strategic nest placement can also lower predation risk
(Martin 1993, Schmidt 1999). For Lepomis, nest site selection is traditionally assumed to
be a response to habitat structure (Breder and Rosen 1966, Colgan and Ealey 1973, Bietz
1981, Popiel et al. 1996). However, if egg predators have signiﬁcant effects on ﬁsh
reproductive success, and ﬁsh are able to recognize areas of high and low egg predator
risk, then habitat selection may occur as a response to spatial variation in predation risk
as well (Gross and MacMillan 1981). Crayﬁsh are most abundant in cobble habitats
which provide a refuge from predaceous ﬁsh (Lodge and Hill 1994), leading to
heterogeneous distributions of this egg predator in lakes with multiple habitats.
Likewise, small ﬁsh (various species) and bullheads (Ictalurus spp.), which are known
egg predators of sunﬁsh (Gross and MacMillan 1981, Popiel et al. 1996), are most
abundant in vegetated habitats (Gross and MacMillan 1981, Werner et al. 1983). Bluegill
and pumpkinseeds would therefore reduce exposure to both types of predators if they
nested in relatively open habitats, which matches their observed breeding sites in lakes
and ponds (Colgan and Ealey 1973, Gross and MacMillan 1981, Breder and Rosen 1966).
Our 2001 experiment suggests that bluegill can discriminate between safe and
risky nesting habitats. No crayﬁsh were observed inside the exclosures in the crayﬁsh
ponds and active nests were never found outside of the exclosures. There also was no
evidence of ﬁsh attempting to nest in any other areas of the pond (except for the original,
abandoned, nest sites) suggesting that bluegills selected nesting locations inside the
exclosures (which occupied <1% of the pond bottom) to avoid crayﬁsh egg predation.

Other aspects of the exclosure besides the absence of crayﬁsh may have stimulated

49

nesting, and we cannot rule this out directly because we did not have a crayﬁsh-
permeable control structure. However, if bluegill were attracted to some physical feature
of the exclosure then we might have expected nesting attempts on both sides of the
exclosure walls (inside and out), which did not occur.

Other researchers have observed correlations between spawning sites or preferred
nest sites and lower levels of egg predation risk (e.g., Beauchamp et a1. 1992, Knapp
1993, Clark and Shutler 1999, Ostlund-Nilsson 2001). However our study is the ﬁrst to
experimentally manipulate egg predator presence, offering ﬁsh an environment with
variable predation risk. Observations of birds (Martin 1993, Schmidt 1999, Clark and
Shutler 1999) and experiments with mites (J anssen et al. 2002) indicate that other animals
may lower exposure to egg predators by breeding in selective habitats. Waterfowl are
known to nest in high densities on islands lacking mammalian nest predators (Clark and
Shutler 1999). However, in this case, it is not known if birds are actively choosing to
nest on islands in response to predator absence or whether selection has simply favored a
return to safe or natal nesting habitats. On a landscape scale, predator-free nesting
habitats or islands could be extremely important for the long-term reproductive success of
populations. Future experimental work is needed to fully evaluate the relative roles of
brood predators, environmental structure, and other factors in determining the breeding
site choices of ﬁsh and other animals.

Viewing and Managing the Spawning Landscape

Little is known about the impacts of early-life-stage predators on the reproductive

success or population size of any ﬁsh. Observational studies based on extrapolation of

egg and fry survival rates or predator feeding rates suggest that egg and fry predators may

50

strongly inﬂuence reproductive success and population size in both marine and
freshwater systems (e.g., Deblois and Leggett 1991, Wisenden 1994, M01 1996,
Fitzsimons et al. 2002). The introduction of new species or types of predators may be
especially critical for ﬁsh populations.

If introduced predator species have different patterns of habitat use or higher
overall densities, then their appearance may change the spawning landscape in ways that
become more hazardous for early-life-stages of ﬁsh. For example the introduced
crayﬁsh, Orconectes rusticus has displaced 0. virilis and another congener, 0.
propinquus, in many Midwestern lakes (Lodge et al. 2000). 0. rusticus and 0. virilis
have similar feeding habits but 0. rusticus is less vulnerable to ﬁsh predators and is
thought to utilize open non-cobble habitats to a greater degree than the species they
replace (Capelli and Magnuson 1983, Lodge et al. 1985). Open habitats generally have
low crayﬁsh densities could provide adequate nesting areas the activity-density of
crayﬁsh increases on those habitats. In some invaded lakes, crayﬁsh activity-densities on
non-cobble habitats exceed 20/trap (K. Wilson, personal communication, unpublished
data), which is more than twice the activity-density we measured in our 2001 experiment
when bluegill reproduction failed completely. After 0. rusticus invaded Trout Lake
(WI), crayﬁsh activity-density increased several-fold and populations of bluegill and
pumpkinseeds virtually disappeared (Wilson 2002). Similar reports of disappearing
sunﬁsh populations in association with crayﬁsh invasions have occurred in the past (e. g.,
Magnuson et al. 1975), and our experiments point to egg predation as an important
mechanism capable of explaining these observations. In many southern Michigan lakes

around Kellogg Biological Station, 0. virilis is present at low densities, probably due to

51

poor environmental conditions (anoxia, soft organic sediments), and seems to have little
impact on populations of Lepomis sunﬁsh. However, in hard-bottom lakes with abundant
crayﬁsh (native or introduced) Lepomis populations may suffer unless safe spawning
sites exist.

Future considerations of available or appropriate spawning habitat should
consider a “ﬁsh-eye view” of both the physical habitat structure and the distribution of
early-life-stage predators. Because ﬁsh breed consistently in particular habitat types,
spawning habitat has been generally identiﬁed and quantiﬁed using metrics of physical
structure or other abiotic variables (e.g., Takemon and Nakanishi 1998, Bernier-
Bourgault and Magnan 2002). However, egg and fry predator densities can vary ﬁ'om
site to site as well (Wisenden 1994, F itzsirnons et al. 2002), and natural selection should
produce inverse correlations between breeding activity and egg predator abundance. In
the Great lakes, lake trout spawn on reefs and other rocky areas and are believed to
respond to appropriate structural and abiotic features of the habitat (Marsden et al.
1995a). Egg predators have historically been considered unimportant (e. g., Wagner
1981), but there has been increasing interest in determining the impacts of egg/fry
predators on reproductive success and spawning habitat use (Marsden et al. 1995b,
Fitzsimons et al. 2002). Beauchamp et al. (1992) reported that the self-sustaining
population of lake trout in Lake Tahoe (CA) spawned in a non-traditional habitat - over
macroalgae (Chara delicatula) located on deepwater mounds surrounded by even deeper
(>100 m) water. Egg predators were uncommon on the mounds (few sculpins — Cottus
spp. and no crayﬁsh) and it was postulated that trout spawned on these sites, rather than

in other deep rocky areas, in response to the paucity of egg predators (Beauchamp et al.

52

1992). Spawning habitat use of lake trout, sunﬁsh (this study), cichlids (Wisenden 1994,
Takemon and Nakanishi 1998), and other species of ﬁsh in other contexts, may be a
reﬂection of their behavioral and/or selected responses to variable densities of important
egg predators as well as physical habitat variables.

Adding artiﬁcial structures to lakes and other systems to enhance ﬁsheries, restore
degraded habitats, or meet a variety of other types of goals is a common management
practice (e.g., D’Itri 1985, Jude and Deboe 1996). It has also been a goal in some cases
to introduce these structures as breeding habitats for ﬁsh (Peck 1986). Unfortunately,
some organisms, including crayﬁsh and benthic ﬁsh (e.g., gobies (Neogobius spp.) and
sculpins), that inhabit these structures are considered both ﬁsh forage (Janssen and Quinn
1985, Jude and Deboe 1996) and egg predators (Chotkowski and Marsden 1999,
Fitzsimons et al. 2002). These benthic predator species are believed to be limited in
distribution and density by available shelters (J anssen and Quinn 1985, Lodge and Hill
1994), and by adding structure where there was previously little, managers and others
may be inadvertantly enhancing egg predators (see also Jude and DeBoe 1996). If
artiﬁcial structures (e.g., reefs, docks, riprap, and breakwalls) allow crayﬁsh or other egg
predator populations to colonize new habitats or increase overall densities (due to
increased juvenile survival), then the predation rates on ﬁsh eggs and fry will increase.

Although early-life-stage predators of ﬁsh have been overlooked compared to
their counterparts in terrestrial ecosystems (e. g., avian nest predators, seed predators), our
ﬁndings indicate that egg/nest predators can be very important to ﬁsh breeding behaviors
and reproductive success. Speciﬁcally, aquatic resource managers assessing the impacts

of past or future introductions of crayﬁsh should consider their potential negative effects

53

on ﬁsh populations, as well as their potential beneﬁts as ﬁsh prey. In general, egg/nest
predators may play an important role in determining the overall quality of the
reproductive landscape. Hopefully, the results of this study and others will give
managers a better “search-image” for identifying factors that determine quality spawning
habitat and for recognizing potentially hazardous management plans that may damage the

reproductive landscape for ﬁsh and other taxa.

ACKNOWLEDGMENTS

We thank T. Darcy, K. Dom, M. L. Dom, E. Garcia, J. Rettig, J. Smedes, C.
Steiner, E. Thobaben, M. Watson, A. Wilson, K. Wilson, J. Wojdak, and P. Wykoff for
advice and help with the experiments, and T. Darcy, E. Garcia, K. Gross, S. Hamilton, T.
Kreps, D. Lodge, A. Sarnelle, and J. Wojdak for valuable comments and suggestions on
the manuscript. The Zoology department (MSU), the G. H. Lauff Fund, and the Kellogg
Biological Station (KBS) Graduate Research Training Grant funded by NSF grants DIR-
09113598 and DBI-9602252 provided ﬁnancial support. GGM acknowledges support
during manuscript preparation from the National Center for Ecological Analysis and
Synthesis, a Center funded by the NSF (DEB-0072909), the University of California, and

the Santa Barbara campus.

54

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59

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60

 

Figure 1. Production of young-of-year (YOY) pumpkinseed (L. gibbosus) in ponds with
and without crayﬁsh (0. virilis) during summer 1999. (a) Mean total biomass (numbers x
mean size) of YOY sampled with standardized seining. (b) Mean number of YOY
captured in seines. (c) Mean wet mass (g) of sampled YOY. Error bars represent one

standard error and p-values are from one-way ANOVAs (N = 3).

61

Figure 1

Number of Fish Fish Biomass

Fish Size

 

400

300

200

100

I crayﬁsh

no crayﬁsh
p = 0.032

p = 0.026
1

JULY SEPTEMBER

 

 

800
700
600
500
400
300
200
100

    

JULY SEPTEMBER

 

0.7
0.6
0.5
0.4
0.3
0.2
0.1

0.0—

 

l l

p=0.128 -

p = 0.01
l
L
JULY SEPTEMBER

 

62

 

0.25

i no crayﬁsh
p < 0.001 I crayﬁsh

.9
N

Frequency

 

 

may

r;

27-Jun 6-Jul 15-Ju1 24-Jul 2-Aug ll-Aug
Birthdate

Figure 2. Distribution of birthdates of YOY pumpkinseed collected from ponds with and
without crayﬁsh in 1999. Birthdates were estimated by enumeration of otolith daily
growth rings. Distributions were compared with a non-parametric Komolgorov-Smirnov

test.

63

 

 

 

 

 

 

 

 

 

 

'3 a Exclosures added _0_ no crayﬁsh
§ 8 ‘ o . +crayﬁsh
8.
a 6 - o o
O
C:
0
.2. 4 ‘
g o 0
<2

2 d

' l
OJ. .‘ 10000000...

 

12-Jun 22-Jun 2-Jul 12-Jul 22-Jul l-Aug
1000

 

    

b
3
9.
a... 100‘
0
a.
'5
to:
"a
S 10‘
1-1

 

    

 

 

1 V IVA

12-Jun 22-Jun 2-Jul 12-Jul 22-Jul l-Aug

   

 

.crﬁ

 

Figure 3. Timeline of bluegill (L. macrochirus) nesting and larval recruitment in ponds
with and without crayﬁsh (0. virilis) during summer 2001 (N = 3). (a) Mean number of
active bluegill nests (nests with eggs or fry) per pond. (b) Mean number (+1) of ﬁ'ee-
swimming YOY bluegill caught per standardized ichthyoplankton tow/pond. Error bars

denote one standard error. Exclosures were added to crayﬁsh ponds on 5 July.

64

 

CHAPTER 4

OMNIVOROUS CRAYFISH DEF LECT SUCCESSIONAL PATHWAYS IN
POND COMMUNITIES: AN EXPERIMENTAL STUDY

with Jeremy M. Wojdak
ABSTRACT

Studies of succession in freshwater habitats have been primarily limited to the
seasonal succession of planktonic communities in lakes, whereas successional dynamics
in the littoral zone has been largely ignored. In this study we followed the development
of benthic and planktonic communities in six newly created, replicate, experimental
ponds in the presence and absence of crayﬁsh, an important benthic omnivore. Over the
period June 2001 - June 2002, we measured the following community and ecosystem
properties; zooplankton and phytoplankton abundance, water quality (dissolved oxygen,
particulates, light), abundance of benthic primary producers, and success of invertebrate
and vertebrate populations.

Zooplankton biomass was higher in crayﬁsh ponds throughout the study,
primarily the result of failed ﬁsh recruitment due to egg predation by crayﬁsh. Patterns
of phytoplankton biomass did not reﬂect the expected cascade in 2001, and were higher
in the crayﬁsh ponds as well. The higher levels of phytoplankton biomass observed in
crayﬁsh ponds in 2001 was probably due to resuspended nutrients (crayﬁsh ponds had
lower light and higher suspended solids). Peak dissolved oxygen levels were lower in the
crayﬁsh ponds throughout the study, indicating that they had a lower primary production:
respiration ratio. In control ponds, Chara and a few macrophyte species covered 34% of
pond bottoms by June 2002, whereas Chara and macrophytes were completely absent

from crayﬁsh ponds. Crayﬁsh also had pronounced effects on the metaphyton and

65

periphyton communities in the ponds, a result of both direct consumption of algae and
indirect interactions through other herbivorous species. For example, exclusion by
crayﬁsh of two important grazer groups (tadpoles and gastropods) was associated with
higher periphyton levels in the crayﬁsh ponds at the end of 2001 . Total benthic
invertebrate biomass did not respond to crayﬁsh presence, but Caenis mayﬂies and
chironomids had altered size-distributions. These results indicate that omnivorous
crayﬁsh can have strong impacts on succession and community structure of shallow

freshwater ecosystems.

KEYWORDS: Chara, Cladophora, crayﬁsh, community, gastropod, Gleotrichia,

herbivory, metaphyton, omnivory, Orconectes, periphyton, succession, tadpole

INTRODUCTION

Community structure of insular systems like ponds and lakes may be strongly
inﬂuenced by the colonization and extinction of key species (Magnuson 1976). For
example, the presence or absence of ﬁsh can have profound impacts on trophic-level
biomass relationships, nutrient cycles, species composition, and size-structure of
producers and consumers in lakes (Leibold 1989, McPeek 1990, Carpenter and Kitchell
1993, Mittelbach et al. 1995, Schindler et al. 2001). Zimmer et al. (2001, 2002) show
that in wetlands naturally undergoing periodic ﬁsh colonization and extinction events, the
presence or absence of ﬁsh has consistent inﬂuences on community structure and water

quality. While effects of ﬁsh on community structure are fairly predictable, other large-

66

bodied consumers, particularly herbivores or omnivores, also may have strong impacts on
succession and community structure in shallow freshwater environments.

Experimental studies in terrestrial and marine intertidal communities have
demonstrated the important role of herbivores and omnivores in determining successional
outcomes. For example, herbivores may speed up succession (e.g., Sousa 1979,
Lubchenco 1983), slow it down (e.g., Brown 1985, Sarnelle 1993, Howe and Brown
2001, Cadenasso et a1. 2002), or even deﬂect its path (sensu Godwin 1929, Hixon and
Brostoff 1996, Gibson and Brown 1992). Deﬂections, as distinguished from changes in
rates, follow different pathways to different endpoints (Hixon and Brostoff 1996), which
Godwin (1929) called “specialized climaxes” and others refer to as alternate stable states
(Petraitis and Dudgeon 1999). Understanding the biotic factors that determine the
consistency or contingency of successional dynamics remains a central goal in
community ecology (Walker 1987, Berlow 1997), reinforced in part by its important
ramiﬁcations for ecosystem restoration (Palmer et al. 1997). However, while
experimental studies of succession are common in terrestrial and marine intertidal
systems, relatively few studies have used controlled experiments to examine the factors
inﬂuencing succession in freshwater systems, outside of studies examining the seasonal
succession of plankton in lakes (e.g., Sommer 1989, Samelle 1993).

Small lakes and ponds undergo succession over many time scales. For example,
temperate systems show seasonal succession in species composition and relative
abundances due to annual variation in temperature and/or precipitation. Over decades,
lakes and ponds may undergo succession due to eutrophication, accumulation of

sediments, or changes in regional hydrological regimes (at the extreme drying up and

67

 

reﬁlling). Over very long time scales (hundreds or thousands of years), most lakes and
ponds gradually ﬁll in and eventually disappear. Lakes and ponds are also subject to the
chance colonization and/or extinction of species (Magnuson 1976, Zirnmer et al. 2001)
and as a consequence we might expect these species to inﬂuence successional pathways.
Here, we focus on the potential role of crayﬁsh in inﬂuencing pond succession.

Crayﬁsh are relatively large invertebrates with polytrophic feeding habits (Momot
1995). Their diets include algae, aquatic vascular macrophytes, detritus, invertebrates,
ﬁsh eggs, and carrion, and they can attain relatively high biomass and production rates in
some systems (Momot 1995). The presence, absence, and relative abundance of crayﬁsh
in shallow water ecosystems can be inﬂuenced by colonization through overland
watercourses, changes in water levels, deletions or introductions of predaceous ﬁsh,
habitat modiﬁcation, winterkill, acidiﬁcation, and disease, as well as human introductions
(Lodge and Hill 1994, Gherardi and Holdich 1999). Over longer time scales of primary
succession in temperate zones, rates of glacial retreat and recolonization rates will
determine if and when systems colonize with crayﬁsh.

In a survey of 42 ponds, Nystrdm et al. (1996) found that systems with more
crayﬁsh had sparser and less diverse macrophyte communities, lower benthic invertebrate
biomass, shifts in invertebrate community composition, and lower organic matter content
of the sediment. From this correlative study, Nystrbm et al. (1996) hypothesized that
crayﬁsh may have important impacts on the succession of shallow aquatic ecosystems.
We tested this prediction experimentally, by examining the effects of crayﬁsh on pond
successional dynamics in six replicate ponds at the Kellogg Biological Station (KBS) in

southwestern Michigan, USA.

68

METHODS
Setup

The 18 ponds at the KBS experimental pond facility (each 29 m dia., 2 m
maximum depth) were constructed in 1972. The pond site is about 800 m (and uphill)
from the nearest source of crayﬁsh and there has been no natural colonization by
crayﬁsh. In October 2002, nine of the 18 ponds were renovated by ﬁrst draining the
ponds and then bulldozing out the existing sediments and plastic liners. The ponds were
then relined with plastic and covered with a sand-gravel-clay sediment mixture (20-25 cm
deep). Ponds were ﬁlled in November 2000 with water from an on-site reservoir and
allowed to colonize naturally with organisms from nearby ponds (except for the planned
addition of ﬁsh and crayﬁsh, described below). We followed the ﬁrst-year successional
dynamics of these ponds, with and without crayﬁsh. Because of their identical
construction and close proximity to one another (31-36 m between pond centers), the
ponds provide an excellent experimental opportunity to examine the direct and indirect
effects of crayﬁsh on early pond succession.

Crayﬁsh (Orconectes virilis, Hagen) were collected from the Michigan
Department of Natural Resources Fisheries Research Station in Saline, Michigan and
were stocked into three of the six ponds at approximately 1.4 individuals ° rn'2 (9.3 g ' m'
2). Because I suspected gradients from the front of the pond array to the back (especially
in bird and turtle use of the ponds), the treatments were interspersed across the array.
Crayﬁsh were stocked on 31 May (after their yearly reproductive cycle) at an average
carapace length (CL) of 29 m. We monitored crayﬁsh trap capture rate (an estimate of

density or activity-density) using standardized (e.g., Lodge and Lorman 1986) baited

69

minnow traps set overnight (2-4 traps - pond" - night"). Stocking densities and trap
capture rates of crayﬁsh in our experiment were well within the natural range of crayﬁsh
densities in ponds as well as Orconectes crayﬁsh for a number of systems (e. g.,
Abrahamsson 1966, Momot et al. 1978, Capelli and Magnuson 1983, Olsen et al. 1991).
Stocking densities in our ponds were considerably lower than the density of 0. virilis that
develops naturally (i.e., without supplemental feed) in the source ponds (10-15 crayﬁsh -
m'z, J. Gapczynski personal communication). F urtherrnore, in three low-productivity
marl-bottom lakes in Michigan, 0. virilis were found found at densities of 1.9-6 crayﬁsh -
rn'2 (4.6-21.2 g -m'2) for 5 consecutive years (Momot et al. 1978, Momot and Gowing
1977).

In late May and early June 2001, 30 large (129-131 mm standard length, SL) and
15 small (67-69 mm SL) bluegill sunﬁsh (Lepomis macrochirus, Raﬁnesque) were added
to each pond. The bluegill were seined from a local lake and added in equivalent sex
ratios and sizes to each pond (see Chapter 3). At the time ﬁsh and crayﬁsh were added to
the ponds, the ponds had already been colonized by plankton, benthic invertebrates,
ﬁlamentous metaphyton (e. g., Cladophora and Zygnema), and a few macrophytes.

Measurements

Plankton
Zooplankton and phytoplankton were sampled six times during the spring and
summer between 14 June, 2001 to 6 June, 2002. We used an integrated tube sampler (1.5
m deep, 7 cm diameter — similar to Steiner 2002) to sample zooplankton from 5-7
locations around the pond on each date. A total of 16 L of water was collected on each
sampling date. The water was ﬁltered through a 80-urn sieve and zooplankton were

preserved in acid Lugols. Zooplankton were enumerated and identiﬁed to genus with the

70

exception of copepods, which were identiﬁed as calanoids or cyclopoids. The major
cladoceran taxa were Daphnia (>99% D. pulex), Ceriodaphnia, Diaphanosoma,
Simocephalus, Bosmina, and Chydorus. From each sample, we measured the body
lengths of up to 50 haphazardly-chosen individuals of each taxon and converted lengths
to biomasses using published length-dry weight regressions (e. g., Burns 1969, Dumont et
al. 1975).

To estimate phytoplankton biomass, we collected a 300 ml water sample (0.4 m
deep) from a single location near the middle of each pond. For each pond and date, 100-
200 m1 of water was ﬁltered onto Gelman A/E glass ﬁber ﬁlters (pore size 1.0 um). The
ﬁlters were extracted in 20ml of 95% ethanol at 7°C for 18-20 hours. Chlorophyll a (pg °
L") concentration was determined using narrowband ﬂuorometry (Welschmeyer 1994).

Dissolved oxygen, light, and seston

On each plankton sampling date, we also measured peak dissolved oxygen levels
using a YSI Model # 600 XL-lOO-M oxygen meter within an hour of sunset.
Measurements were taken at 0.3 m increments from 0.3 to 1.8 meters deep. The
measurements were averaged across depths for the analysis, however the depth proﬁles
were shallow and did not exhibit any regular differences between the treatments. Water
clarity was measured using a light meter (LI-COR model # LI-185B) in 2001 and a small
secchi disk (16 cm diameter) in 2002. In 2001 we calculated the light extinction
coefficient between the surface and 2 meters depth as (ln(watts at surface) - 1n (watts at 2
m))/2. Light extinction was measured once (11 July) in 2001 - secchi disk depth was
measured twice (May and June) in 2002. Total particulate matter and the component

organic and inorganic fractions were measured on 26 July 2001. Water from each pond

71

was collected and particulate matter was ﬁltered onto preweighed and combusted Gelman
A/E glass ﬁber ﬁlters. Dry mass was determined after drying the ﬁlters for 40 hrs at 60°
C and ash content was determined after combusting in a muffle furnace for 50 minutes at
500° C.. The concentration (mg - L") of total particulates (dry weight — ﬁlter weight),
particulate inorganic matter (ash weight — ﬁlter weight), and particulate organic matter
(difference between total and inorganic) were calculated for each pond. Particulates
were not measured in 2002.
Benthic community
Primary Producers

We visually estimated percent cover of macroalgae (Chara vulgaris) and vascular
macrophytes (always rare) in June of both summers by diving into the ponds (SCUBA)
and using quadrats. Seven haphazardly placed 0.25 m2 quadrats were dispersed
throughout the pond in shallow areas (0.2-1.8 m deep) and ﬁve quadrats were dispersed
throughout deeper (1.8-2 m) areas (reﬂecting the proportionally greater shallow habitat in
the ponds). Two divers made independent estimates of percent cover (to the nearest 5%)
for each quadrat sample. The independent measurements agreed well (R2 = 0.92, slope =
1), and were averaged for each point measurement to calculate mean percent cover in
each pond. In June of 2001 we used the same quadrat method to estimate the abundance
(% cover) of mats of metaphytic green algae (unattached algae dominated by
ﬁlamentous-green forms like Cladophora and Zygnema) found on the pond bottom.
Metaphyton mats were present in the ponds before the treatments were applied in 2001
and these mats (individually up to 8 m2) would regularly rise and fall between the bottom

and the surface on sunny days.

72

We characterized the composition of the metaphyton community on 24 August,
2001 by collecting samples of metaphyton from the surface of each pond. Samples were
homogenized and then enumerated on a Zeiss Axioskop microscope at 400 X
magniﬁcation. At least 300 natural units were counted for each sample. Identiﬁcation
was to genus whenever possible.

Periphytic algal biomass (algae attached to hard substrates like gravel and sand)
was quantiﬁed by placing 12 ceramic tiles (31.5 cmz) in the center (2 m deep) and 24 tiles
on the sloping north shore (0.75 m deep) of each pond on 14 June 2001. The tiles
colonized naturally and three tiles were collected on each sample date (1 deep, 2 shallow)
from each pond. Each tile was extracted in 40 ml of 95% ethanol for 18-20 hours.
Chlorophyll a concentration (expressed as ug - cmz) was determined using a ﬂuorometric
techniques similar to that used for the phytoplankton.

Invertebrates

Benthic invertebrates were sampled on 13 June 2002 using a D-shaped sweep net
(27 cm wide, with l-mm mesh). One sweep was taken ﬁ'om 3 of the 4 quarters of each
pond at 0.5 m depth (one randomly chosen quarter-pond was ignored). The net was
placed on the substrate at each sample point and moved at a constant rate for 0.75 meters
sampling an area of approximately 0.2 m2. The three samples were pooled and then
sorted by placing the contents in white, enameled pans and picking out the live
invertebrates by hand. Invertebrates were preserved in 80% ethanol and later counted
and identiﬁed under a dissecting scope to family or genus. For analyses, invertebrate
taxa were combined into four categories based on their abundance: chironomidae, Caenis

(mayﬂies), gastropods, and other (including Trichoptera, Odonata, Heteroptera, and

73

Hydrachnida) . To estimate biomass and compare size-structure, a random sample of at
least 25 individuals of each major taxa was measured from each sample when possible.
Length-dry mass regressions (unpublished) developed for local organisms were used to
estimate total invertebrate biomass and the biomass of each group. For taxa that were
abundant in all ponds (Caenis and chironomids), we compared their population size
structures by lumping all measured individuals from a treatment into a single size-
frequency distribution.
Vertebrates

Bluegill reproduced in the ponds and we quantiﬁed the abundance of young-of-
year (YOY) ﬁsh in 2001 using a ichthyoplankton net (0.5-mm mesh with a 68-cm dia
opening) towed across the pond at nighttime at regular sampling intervals (see Chapter 3
for details). We also made repeated observations of bluegill nesting behavior using
SCUBA. Only qualitative estimates of ﬁsh abundance were made in 2002. The
abundance of bullfrog (Rana catesbiana) tadpoles was quantiﬁed in August 2002 using
baited minnow traps set overnight in each pond.

Metaphyton choice feeding experiment

To determine whether selective grazing by crayﬁsh caused a shift in metaphyton
composition from ﬁlamentous greens to dominance by the ﬁlamentous blue-green
Gleotrichia, we performed a feeding preference assay following the methodology of
Peterson and Renaud (1989). On 2 August, 9 male crayﬁsh (CL range = 40-42 mm) were
placed in individual plastic containers (25 cm dia., ﬁlled 3.5 cm deep with pond water)
and offered similar wet masses (mean = 9.0 g) of drained and weighed ﬁlamentous green

metaphyton (mostly Cladophora) from a control pond and blue-green Gleotrichia from a

74

crayﬁsh pond. Crayﬁsh ponds had abundant Gleotrichia at this time of the year and all
control ponds had green metaphyton mats similar in appearance to the Cladophora used
in the feeding trials. The crayﬁsh were starved for 6.5 hours prior to the start of the
feeding trials. Both algal types were added simultaneously to the nine containers with
crayﬁsh, and to an additional nine control containers without crayﬁsh. The use of
controls allows for statistical incorporation of variation in autogenic mass change
(Peterson and Renaud 1989). After 20 hours of feeding, the crayﬁsh were removed and
the remaining algae was sorted, drained, and reweighed.
Crayﬁsh migration between ponds

In the late-summer/ early-fall of 2001 a few crayﬁsh invaded the control ponds
from nearby crayﬁsh ponds by moving overland (a common behavior for this species in
the ponds where we collected them — J. Gapczynski, pers. comm). We attempted to
remove the invading crayﬁsh by hand using SCUBA, however, a few individuals eluded .
us and reproduced in the control ponds in mid to late May of 2002. Initially the small
YOY crayﬁsh had little effect on the status of the treatments. However, by mid-July they
had reached relatively large sizes (some > 20 mm CL), were trappable with baited
minnow traps, and were having noticeable impacts on Chara (visible herbivory). Thus,
our treatments effectively homogenized by mid July 2002 and we were forced to end the
experiment.

Statistical Analyses

Data were log-transformed when necessary to normalize distributions or to meet

assumptions of homogeneity of variances. Phytoplankton, zooplankton, oxygen levels,

secchi disk depth, and periphyton measures were analyzed through time and between

75

 

treatments using repeated measures AN OVA (rrn-AN OVA hereafter) with SAS 8.0
(SAS Institute). Data from 2001 and 2002 were analyzed separately for each response
variable (3-4 measures in 2001 and 1-2 measures in 2002) because there was no
correspondence of dates between years. We analyzed our data using Proc Mixed, a
general linear mixed model, which allowed us to optimize the covariance structure for
each analysis. Akaike’s Information Criterion was used to choose the best structure for
each data set - compound symmetry was the best structure for most of our analyses. If
signiﬁcant time x treatment interactions were found, the data were sliced by time
(lsmeans option in Proc Mixed) to look for treatment differences on individual dates.

One-way AN OVAs were used to analyze percent cover of Chara and metaphytic
green algae, invertebrate biomass, amphibian abundance, light extinction coefﬁcients,
and particulate matter. Non-parametric Komolgorov-Smirnov two-sample tests were
used to compare the size-frequency distributions of Caenis and chironomid larvae. Data
from the laboratory feeding assay with Cladophora and Gleotrichia metaphyton were
analyzed with a t-test of differences which incorporates variation ﬁom an equal number
of controls into a test of differences in proportional mass change (Peterson and Renaud
1989)

RESULTS
C rayfish abundance

Mean crayﬁsh abundances ranged from 4.7-12.3 ° trap'I in 2001 (N = 4 dates) to
0.33-2.l - trap'1 in 2002 (N = 3 dates). Differences in crayﬁsh abundances were due to
natural mortality as well as a lack of reproduction in 2001. This species of crayﬁsh has a

maximum lifespan of three years and reproduction occurs once per year in the spring.

76

The crayﬁsh added to the ponds were age 1 and 2, and cohort biomass and numbers of 0.
virilis in lakes (with similar standing stock biomass) naturally declines from age 1 to 2
and 2 to 3 (Momot and Gowing 1977). In fact, cohort numbers often decline by 70-89%
from year 2 to 3 (Momot and Gowing 1983). There was no reproduction in 2001 because
individuals were introduced to the ponds after their spring reproductive cycle. Crayﬁsh
did reproduce in 2002 in the crayﬁsh ponds, but the small YOY did not reach large
enough sizes to recruit to traps by mid-summer.
Plankton

Total zooplankton biomass was highest (~0.9 mg dry mass - L") early in the
summer of 2001, then declined over time (time effect F 3,12 = 38.88, p < 0.0001, Figure 1).
Zooplankton biomass was similar between treatments on the ﬁrst sample date of the
experiment in 2001 (F 1,151, = 0.07, p = 0.7948), but was signiﬁcantly higher in the
crayﬁsh ponds on the last 3 dates of 2001 (sliced by date: F 1,1 5.6 > 11.5, p < 0.004).
Zooplankton composition was very similar between treatments on the ﬁrst date in 2001
(larval ﬁsh recruited into the water column). However, the zooplankton composition
quickly shifted to copepod dominance in the control ponds by the second sample date,
while cladocerans (large and small) remained relatively more abundant for longer in the
crayﬁsh ponds (Table 1). In 2002, zooplankton biomass remained signiﬁcantly higher in
the crayﬁsh ponds (treatment effect F 1,4 = 14.43, p = 0.019).

In 2001, phytoplankton biomass (pg chlorophyll a - L") was signiﬁcantly higher
in the crayﬁsh ponds (treatment effect PM = 14.99, p = 0.018) and increased through time

(time effect F 3,1 2 = 17.19, p = 0.0001) (Figure 2). Treatments reversed direction in 2002,

77

with phytoplankton biomass being higher in the control ponds (treatment effect F 1,4 =
24.55, p = 0.077).
Dissolved oxygen, light, and seston

Mean peak dissolved oxygen (mg 02° L") was higher in control ponds than in
crayﬁsh ponds in 2001 (F4, 12 = 5.62, p = 0.048) and tended to be higher in 2002 as well
(FM = 13.1, p = 0.059, Figure 3). Although the treatment effect was not signiﬁcant in
2002 the largest single difference came on the last date (June 2002) when the crayﬁsh
ponds were undersaturated and all control ponds were supersaturated with oxygen.

Light extinction coefficients were higher in crayﬁsh ponds in 2001 (FM = 30.23, p
= 0.0053) which was consistent with diver observations of reduced visibility in crayﬁsh
ponds throughout the summer. Light extinction coefficients, however, were not related to
water column chlorophyll a concentrations (r = -0.1 1, p =0.82). In 2002, water
transparency (measured by secchi disk depth) was not different between treatments (rrn-
ANOVA treatment and treatment x time interaction p-values > 0.72).

Total particulate matter (mg - L") was signiﬁcantly higher in crayﬁsh ponds (Fm
= 33.4, p = 0.004, Figure 4) in 2001. Both the organic and inorganic fractions were
larger on average in the crayﬁsh ponds (organic FM = 10.3, p = 0.033, inorganic PM =
10.6, p = 0.031), and the inorganic fraction accounted for a much greater proportion of
the total in crayﬁsh ponds (49.8%) compared to control ponds (10.3%).

Benthic community
Primary producers
From June 2001 to June 2002, the percent cover of Chara in control ponds

increased from < 1% cover to an average of 34% cover (Table 1). Chara failed to

78

establish in any of the crayﬁsh ponds - small patches of Chara were occasionally
observed in these ponds, but none persisted. The lack of a signiﬁcant treatment effect on
Chara abundance in 2001 was due to high variability among control ponds during initial
colonization.

There were pronounced difference in the development of the metaphyton
community in ponds with and without crayﬁsh. Mats of metaphytic green algae (mainly
Cladophora and Zygnema) were found in the control ponds in June 2001, but were absent
from the crayﬁsh ponds (Table 1). Late summer (August) samples of the metaphyton
community showed that all ponds had become dominated by blue-green forms (at least
64% of all cells in cell-counts), but Gleotrichia was only found in the crayﬁsh ponds
where it was the dominant metaphytic taxa (Table 2). By 2002, metaphyton was rare or
absent in both pond types, however, small amounts of Gleotrichia were observed in the
crayﬁsh ponds in June 2002. In our feeding trials, crayﬁsh simultaneously offered
Cladophora metaphyton from a control pond and Gleotrichia from a crayﬁsh pond
preferentially consumed the Cladophora (60% mean reduction in wet mass) and virtually
ignored the Gleotrichia (Figure 5, t-test of differences p < 0.0001).

Periphyton biomass changed through time but was dependent upon treatment
(Figure 6; time effect (F23 = 9.77, p = 0.0071) and time x treatment interaction (F23 =
5.54, p = 0.0104)). The control ponds had more periphyton early in July (sliced by date:
F1304 = 11.22, p = 0.0431), but the crayﬁsh ponds were signiﬁcantly higher in August
(F 1,569 = 9.54, p = 0.023). In 2002, the treatments maintained the same rank as at the end
of 2001 (all crayﬁsh ponds had higher chlorophyll a measures than all control ponds), but

they did not differ signiﬁcantly (FM = 3.3, p = 0.144).

79

Invertebrates
Crayﬁsh signiﬁcantly reduced gastropod biomass (Gyraulus, Lymnaea, and
Physa) (F 1,4 = 21.2, p = 0.01; mean dry mass in mg - m'2 (S.E.): control ponds = 8.4 (3.1),
crayﬁsh ponds = 0.34 (0.34)), but had no effect on the biomass of other taxa or on the
biomass (mg - m'z) of all benthic invertebrates combined (F 1,4 = 2.17, p = 0.21).
Chironomids (larvae and pupae) and Caenis (nymphs) showed signiﬁcant differences in
size between treatments, with chironomid sizes shifted towards smaller individuals in
crayﬁsh ponds (Komolgorov-Smimov 2-sample test p = 0.008, Figure 7a), and Caenis
shifted towards larger individuals in the presence of crayﬁsh (p < 0.0001 , Figure 7b).
Vertebrates
Crayﬁsh were signiﬁcant predators on bluegill eggs and larvae and detailed
observations of their effects on bluegill reproductive success are reported in Chapter 3.
In brief, bluegill reproduced throughout June 2001 in the control ponds, but due to egg
predation by crayﬁsh, they were unable to reproduce successfully in the crayﬁsh ponds
until crayﬁsh-proof exclosures were added on 5 July 2001 (Chapter 3). Adult bluegill
began spawning in the crayﬁsh-proof exclosures in mid-late July and produced a pulse of
larval ﬁsh late in the summer (See timing of ﬁrst successful recruitment in Figure 1).
Small larval bluegill densities ranged ﬁom 1-10 - m'3 in the control pond from mid-June
to mid-July (Figure 1) and they were quickly outgrowing the sizes that we could catch
with our ichthyoplankton net. Larval bluegill were never caught in the crayﬁsh pond
during that same period (Chapter 3). We observed bluegill (juveniles and adults) in all
the ponds in spring 2002, indicating that the ﬁsh survived the winter. However, we do

not have detailed measures of their 2002 abundances.

80

Crayﬁsh had a similarly dramatic effect on bullfrog reproductive success. In
more than 70 person-hours of observation with mask and snorkel and from shore, we
never found a bullfrog tadpole in any of the crayﬁsh ponds. Tadpoles were abundant,
however, in 2 of the 3 control ponds in 2001 and in all 3 control ponds during 2002.
Baited crayﬁsh traps placed in all six ponds in August, 2002 captured an average of 7.2
bullfrogs per trap (SE. = 0.72) in the control ponds and 0.0 in the crayﬁsh ponds (p <
0.0001).

DISCUSSION

Crayﬁsh had pronounced effects of the development of benthic and planktonic
communities in our experiment ponds and these effects were due to a combination of
direct and indirect interactions. We discuss these effects below, ﬁrst in the context of our
experiment and then in a more general framework, combining our results with those of
other studies of crayﬁsh to examine the role of crayﬁsh on littoral zone community
development in a wider range of ﬁ'eshwater systems.

Crayﬁsh abundance

Although our initial crayﬁsh stocking densities were reasonable considering
densities in oligo-mesotrophic north-temperate lakes (Momot et al. 1978, Capelli and
Magnuson 1983, France 1985, Olsen et al. 1991, see METHODS) crayﬁsh abundance
declined in the crayﬁsh ponds from 2001 to 2002. Density changes from 2001 to 2002
were a result of natural mortality and a lack of reproduction in 2001 (see Results).
However, even if our stocking densities were at or slightly above the carrying capacity of
the ponds, our observations of the control ponds that were invaded in 2002 indicate that

the outcome would have been very similar had we started the ponds with small numbers

81

of adults and let the population grow naturally. When the ponds were drained in
September of 2002, the YOY that were born into one of the control ponds had attained a
population size of approximately 500 very large YOY (20-30 mm CL), the pond bottom
was barren (in June it had 33% cover of Chara), and the pond was extremely turbid
(personal observations).
Plan/don and water quality

Crayﬁsh had a strong, positive effect on zooplankton biomass, driven by their
negative impacts on ﬁsh recruitment (Chapter 3). Interestingly, this effect on
zooplankton biomass did not cascade down to affect phytoplankton abundance in 2001.
This could be a consequence of bottom-up effects of crayﬁsh via sediment (and nutrient)
resuspension. Crayﬁsh also consumed or excluded benthic macroalgae and macrophytes,
and together these effects of crayﬁsh may have indirectly augmented phytoplankton
production rates. Despite our effort to avoid visible metaphyton in the phytoplankton
samples, it is also possible that some of the samples from 2001 were contaminated by
metaphyton or other suspended benthic algae. However, the blue-green metaphyton
bloom in the crayﬁsh ponds did not begin until late July and therefore could not account
for differences earlier in the summer. If the samples were highly contaminated with
ﬁlamentous green algae early in the summer it should have favored higher values in the
control ponds (where Cladophora mats were abundant). In 2002, zooplankton continued
to be more abundant in the crayﬁsh ponds, whereas phytoplankton differences reversed
such that crayﬁsh ponds had signiﬁcantly less phytoplankton. Higher zooplankton
biomass in crayﬁsh ponds could reﬂect lower numbers of juvenile ﬁsh in 2002, and our

qualitative observations suggest this was the case. Phytoplankton levels in 2002 were

82

consistent with expectations of top-down control by zooplankton, and may have been
realized in 2002 (vs. 2001) if the lower abundance of crayﬁsh had weaker indirect effects
on phytoplankton production (note: water transparency was not different in crayﬁsh vs.
control ponds in 2002).

Peak levels of dissolved oxygen indicated that crayﬁsh had an impact on the
ecosystem production: respiration ratio in the ponds. Lower peak dissolved oxygen could
have been caused by increased light limitation, exclusion (consumption) of primary
producers, and/or increased respiration of decomposers (through organic matter
processing or aeration of the sediments). Crayﬁsh are clearly important in processors of
organic matter in streams (Usio 2000, Schoﬁeld et al. 2001, Creed and Reed in press),
but further work is necessary to determine the mechanisms by which crayﬁsh inﬂuence
production: respiration ratios in lentic ecosystems. If this impact were to remain
consistent through time, crayﬁsh ponds should accumulate organic matter at a slower rate
than ponds without crayﬁsh (Momot 1995, Angeler et al. 2001), consistent with the
observations by Nystrom et al. (1996), that ponds of similar age with more crayﬁsh had
lower organic matter content in the sediments. Future work on crayﬁsh should pay
attention to this type of engineering role of crayﬁsh that could have important long-term
effects on ecosystem development.

Benthic community structure

Crayﬁsh had strong direct effects on the benthic primary producers in our
experiment. Chara macroalgae and ﬁlamentous alga Cladophora are known to be eaten
by crayﬁsh (Creed 1994, Nystrbm and Strand 1996) and they were strongly reduced by

crayﬁsh in our ponds. The shift in the metaphyton to dominance by the blue-green

83

Gleotrichia was most likely driven by selective consumption of Cladophora by crayﬁsh.
The results ﬁ'om our choice feeding assay demonstrated that crayﬁsh preferred
Cladophora over Gleotrichia, and in our casual observations walking around the pond
edges we noted that crayﬁsh commonly passed over opportunities to feed on Gleotrichia.
It is also possible that the shift in metaphyton communities could have been inﬂuenced
by sediment (and nutrient) resuspension. These results suggest that Gleotrichia is a
relatively unpalatable or unproﬁtable form of algae, and that the metaphyton
communities underwent a compositional shift due to strong top-down grazing.

Observations of plant succession in other KBS ponds (without crayﬁsh) indicate
that succession usually proceeds from green metaphyton mats (year 1) to mostly Chara
(year 2) and then to increasingly more diverse vascular macrophytes in subsequent years
(G. G. Mittelbach, personal communication). The appearance and dominance of
Gleotrichia, and the exclusion of green-algae metaphyton mats and Chara, indicate that
crayﬁsh have dramatically altered the expected successional sequence of benthic primary
producers in these ponds.

Strong trophic cascades from omnivorous crayﬁsh to snails (or tadpoles) to
periphyton have been observed in short-terrn experimental studies (Lodge et al. 1994,
Nystrom and Abjomsson 2000, Nystrom et al. 2001), and our results suggest that a
similar cascade may have occurred in the ponds. Tadpoles and gastropods were abundant
in the control ponds during mid-summer 2001 but were absent or rare in crayﬁsh ponds at
the end of 2001 and in 2002. Crayﬁsh are well-know predators of gastropods (Lodge et
a1. 1994, Nystrbm et al. 1999, 2001), but the mechanism responsible for the absence of

bullﬁ'og tadpoles in crayﬁsh ponds is unclear. Ponds containing Lepomis sunﬁsh are

84

normally good habitat for bullfrog tadpoles because sunﬁsh eliminate the invertebrate
predators (e. g., Odonates) that feed on bullfrog tadpoles (Werner and McPeek 1994,
Smith et al. 1999). Crayﬁsh may have inhibited bullfrog breeding by eliminating the egg
attachment sites; bullfrogs attached their egg masses to Cladophora metaphyton mats and
pond margins in control ponds, but the mats were eliminated from crayﬁsh ponds (also
see Nystrom 1999). It is also possible that crayﬁsh had a direct effect on tadpole
abundance by consuming egg masses laid along the pond margins or that bullfrogs
avoided breeding in ponds due to the presence of crayﬁsh. Crayﬁsh will consume eggs
of many amphibians including Rana frogs (Axelsson et a1. 1997).

Periphyton biomass was signiﬁcantly higher in the crayﬁsh ponds in August
2001, consistent with a trophic cascade from crayﬁsh to tadpoles and snails to
periphyton. Periphyton biomass in 2002 was also higher in all crayﬁsh ponds than the
control ponds, but these differences were not signiﬁcant. Because crayﬁsh exclude some,
but not all, benthic grazers and also consume periphyton, the long-term effects on
periphyton biomass are difficult to predict (N ystrbm et al. 1996).

, Crayﬁsh did not inﬂuence the total biomass of invertebrates or the biomass of
other taxa besides snails. However, crayﬁsh had signiﬁcant effects on the size-structure
of chironomid and Caenis populations. Chironomids, which were smaller in crayﬁsh
ponds, are relatively immobile taxa (like snails) that are easily preyed upon by crayﬁsh.
Creed and Reed (in press) report similar effects of crayﬁsh on the size-structure of
chironomids which suggest crayﬁsh are selectively feeding on larger chironomids. In
contrast, Caenis larvae were larger in crayﬁsh ponds. Mayﬂies are more mobile taxa and

are probably not strongly inﬂuenced by crayﬁsh predation (N ystrom 1999, Nystrbm et al.

85

1999). Elimination of other grazers (tadpoles and snails) may have had indirect positive
effects on Caenis growth rates in crayﬁsh ponds. The higher periphyton biomass in the
crayﬁsh ponds at the end of 2001 suggests there may have been more resource available
for Caenis. Nystrdm et al. (1999) suggested the same indirect mechanism was
responsible for increased mayﬂy biomass in their mesocosm experiment.
General implications for community development

In Figure 8 we offer an illustration of systems with and without abundant crayﬁsh
to serve as 1) a pictorial summary of our results, combined with results from other studies
and 2) a diagram of expected outcomes of succession. These expectations are most
appropriate for ponds, shallow lakes, and littoral zones or shallow bays of deep lakes.
The exact manifestation of the effects will be inﬂuenced by regional species pools,
predators, and abiotic variables (pH, habitat, conductivity; Lodge and Hill 1994), and
may be altered by presence or absence of other strong interactors (e.g., zebra mussels —
Dreissena polymorpha, Stewart et al. 1998, Perry et al. 2000). But, for the purposes of
general discussion, we will consider two similar littoral environments that differ only in
the presence or absence of crayﬁsh. It should be noted that not all crayﬁsh are equal, and
introduced species can sometimes become much more abundant than the species they
replace (e. g., Wilson 2002). These expectations can therefore potentially apply to ponds
or lake margins colonized by at a variety of successional stages.

In systems with few or no crayﬁsh (Figure 8A) we would expect a community
with more abundant and diverse macrophytes and snails. Crayﬁsh decrease the biomass
and species richness of macrophytes (including Chara)(Dean 1969, Feminella and Resh

1989, Chambers et al. 1990, Lodge et al. 1994, Nystrbm et al. 1996, Wilson 2002, this

86

study, and others) and most species of snails are greatly reduced or excluded from
systems with abundant crayﬁsh (Lodge et al. 1994, 1998a, Nystrbm and Perez 1998,
Nystrbm et al. 2001, this study). However, heavily armored snail taxa (e. g., Goniobasis,
Campeloma) can sometimes be found in areas with abundant crayﬁsh (NJD - personal
observations, Lodge et al. 1994).

The strong effects of crayﬁsh on bullfrogs (this study) and on newts (Gamradt
and Kats 1996) indicate that crayﬁsh can have dramatic negative impacts on amphibian
populations. Direct and indirect interactions are probably responsible for these effects
(Gamradt and Kats 1996, Gamradt et a1. 1997, Nystrom 1999, Nystrdm and Abjornsson
2000).

Other effects on invertebrate communities have been represented in Figure 8 by
the differences in size-structure of the sediment dwelling chironomids (this study, Creed
and Reed in press) and mayﬂies (this study, biomass effect — Nystrbm et al. 1999).
These differences reﬂect both direct effects of size-selective predation by crayﬁsh
(chironomids) and indirect positive effects (through exclusion of other grazers) on mobile
insect grazers (mayﬂies).

Figure 8 indicates that crayﬁsh can inﬂuence ﬁsh recruitment through egg
predation (N ystrom 1999, Fitzsimons et al. 2002, Chapter 3), but this effect is just one of
many routes by which crayﬁsh can inﬂuence ﬁsh populations and communities (Dorn
and Mittelbach 1999). Small crayﬁsh (especially YOY) are important prey items and
could thereby positively affect some predatory species of ﬁsh (Rickett 1974, Stein and
Magnuson 1976, Dom and Mittelbach 1999). However, adult crayﬁsh are relatively

invulnerable to ﬁsh predators (Stein 1977) and large populations of crayﬁsh (mostly

87

exotic introductions) have been blamed for failed recruitment and ﬁsh population
declines in ponds, lakes, rivers, and streams (Buck and Thoits 1970, Magnuson et al.
1975, Hepworth and Duffield 1987, Hobbs et al. 1989, Guan and Wiles 1997, Covich et
al. 2000, Bryan et al. 2002, Wilson 2002).

Based on our results, zooplankton and/or phytoplankton may be expected to be
more abundant in shallow systems with abundant crayﬁsh. Depression of larger plants,
predation on ﬁsh eggs (which limited abundance of zooplanktivores), and resuspension of
nutrients could all impact the plankton. In other studies, bioturbation by crayﬁsh
relocated large amounts of sediment (Stazner et al. 2000) and resuspended signiﬁcant
amounts of phosphorous (Angeler et al. 2001, Ottolenghi et al. 2002). Of all the expected
effects illustrated in Figure 8, the effects on plankton and ﬁsh recruitment are probably
the most system- and species-speciﬁc, and we suggest them as hypotheses for future
investigations.

Eﬂects of animals on succession

Increasing attention is being paid to the role of consumers (mostly herbivores) on
successional dynamics of plant communities (e.g., Lubchenco 1983, Bowers 1993,
Samelle 1993, Hixon and Brostoff 1996, Howe and Brown 2001, Cadenasso et al. 2002).
Herbivores can alter the rate of succession, and in some cases herbivores can even change
the trajectory of succession (e. g., Hixon and Brostoff 1996, Gibson and Brown 1992).
Although many have considered invertebrate herbivores to be inconsequential to
succession dynamics of terrestrial plant communities, Carson and Root (1999)
demonstrated that insects can have a strong impact on the rate of succession in oldﬁelds.

They hypothesized that well-defended or outbreaking species of invertebrates will have

88

important effects on vegetation dynamics. In freshwater ecosystems, crayﬁsh are the
largest invertebrate consumers, they grow to predator-invulnerable sizes (Stein 1977),
they can attain high community biomass (Momot 1995), and they are some of the most
important macrophyte herbivores (Lodge et al. 1998b).

Most freshwater ponds and lakes have an insular nature (Magnuson 1976).
Different ponds and lakes colonize with different assemblages of consumer species, and
the major disturbances extinguishing or introducing consumer species occur episodically
over relatively long time scales. Development and persistence of community structure in
ponds and lakes may depend on the introduction, persistence, and size of consumer
populations that exert major structuring effects. Although herbivores commonly change
the rate of succession, the broad diets of omnivores and their potential to maintain their
populations on alternate resources while suppressing populations of other more
vulnerable or preferred species (Polis and Strong 1996) make them prime candidates to
deﬂect the trajectory of community development (Knowlton 1992). In freshwater
ecosystems ﬁsh are the largest predators, many of them are omnivorous (V adas 1990)
and they have strong impacts on community structure as evidenced when they are
introduced or extinguished from a system (e.g., Mittelbach et al. 1995, Zimmer et al.
2001). Deletions and introductions of omnivorous crayﬁsh (native or exotic) can have
similarly large impacts on community structure.

Studies of crayﬁsh deletions in Europe due to the crayﬁsh plague (Aphanomyces
astaci Schikora) have yielded observations consistent with the expectations from our
experiment. In Sweden, the native crayﬁsh Astacus astacus disappeared from 5 ponds (3

m deep, 2 2 ha) that had contained crayﬁsh for 44 years. Pond bottoms that had been

89

previously barren when crayﬁsh were present developed a heavy cover of Chara and
vascular macrophytes one year after the population crashed (Abrahamsson 1966). In
addition, “(t)he number of molluscs and leeches increased markedly and immense
numbers of young tadpoles appeared in the ponds.” Nystrtlm (1999) indicated that the
same 5 ponds have been recolonized by a North American crayﬁsh, Pacifasticus
leniusculus (not susceptible to the plague), and have shifted back to the crayﬁsh
dominated (low macrophyte) condition. Similar changes in Chara and mollusc
populations were documented when the plague eliminated native European crayﬁsh from
littoral zones of larger lakes (100 and 430 ha) in Ireland (Matthews and Reynolds 1992).
Consistent effects of introductions have been observed in wetlands and lakes in the
United States (e.g., F eminella and Resh 1989, Magnuson et al. 1975, Dean 1969).

In conclusion, our data indicate that crayﬁsh can have dramatic impacts on the
succession of pond communities through a variety of direct and indirect effects. Crayﬁsh
colonization of ponds or littoral habitats has the potential to drastically change
community structure to a macrophyte-poor and algae-dominated, structurally simpler
system, having lower productivity: respiration ratios and higher sediment resuspension
rates, where some species may beneﬁt, but others are excluded or do poorly. More
broadly, our results indicate that succession and community structure of shallow
freshwater ecosystems is dependent upon colonization or extinction events of important

benthic invertebrate consumers.

90

ACKNOWLEDGEMENTS
We are grateful to K. Gross, S. Hamilton, D. Lodge, G. Mittelbach, and A.
Sarnelle for helpﬁrl comments and discussions on earlier drafts of the manuscript. T.
Darcy generously provided algal identiﬁcation. J. Gapzinski provided crayﬁsh from the
Saline Fisheries research station ponds. The G. H. Lauff fellowship and an NSF site
improvement grant to G. G. Mittelbach made the experiment and measurements possible.
Graduate Research Training Fellowships funded through NSF grants DIR-09113598 and

DBI-9602252 to KBS provided ﬁnancial support to NJD and JMW.

91

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98

Table 1. Relative abundance (mean % of total biomass) of zooplankton
groups in ponds with and without crayﬁsh. Large cladocerans =

Daphnia and Simocephalus; small cladocerans = Bosmina,

Ceriodaphnia, Chydorus, and Diaphanosoma; copepods = calanoids and

 

 

 

cyclopoids.
2001 2002

mean % 6/14 7/5 7/26 8/24 5/7 6/6
Large 58 23.9 9.3 0 1.3 7.3
Cladocerans 63.3 40 6.3 0 2.4 2.4
Small 0.6 3.6 6.8 2.8 0 4.2
Cladocerans 2.6 37.3 58 0.9 5.8 52.4
Copepods 41.3 72.5 83.9 97.2 98.7 88.5
34.1 22.6 35.5 99.1 91.8 45.2

 

99

Table 2. Percent cover of green metaphyton (Cladophora and Zygnema algal
mats) and Chara on the bottom of 6 ponds

 

 

 

Mean % cover AN OVA results
Date Plant control ponds crayﬁsh ponds F” P
June, 2001 Green metaphyton 7.4 (1.5) 0(0) 103.8 0.0005
June, 2001 Chara 0.73 (0.37) 0 (0) 3.99 0.117
June, 2002 Chara 34 (12.9) 0 (0) 63.57 0.0013

 

100

Table 3. Percent abundance (% of cells in counts) of algal genera in
metaphyton samples taken from 6 ponds in late August 2001. All taxa that

made up 3 5% of all cells in at least one pond are included in the table.

 

 

 

 

Control ponds Crayﬁsh ponds
Form Genus l 2 3 l 2 3
b-g. ﬁl. Gleotrichia 0 0 0 29.5 87.3 51.6
b-g. ﬁl. Leptolyngbya 29.4 28.8 13 25 p 15.5
b-g. ﬁl. Nostoc 0 0 25.9 0
b-g. ﬁl. Pseudoanabaena 10 16.2 10 p p p
b-g. ﬁl. Phoridium 0 23.6 10.7 0 0 0
b-g. ﬁl. C ylindrospermum 14.7 0 0 0 0 0
b-g. ﬁl. Calothrix 0 18.8 0 0 0 0
b-g. col. Aphanocapsa 7.4 p p 0 0 p
g. ﬁl. Mougeotia p p 10.4 0 0 0
diatom Navicula 16.4 p 6.1 16.9 p p
diatom Achanthidium p 0 8 10 p 12.4
diatom Cocconeis 0 0 0 0 0 9.2__

 

b-g. ﬁl. = blue-green ﬁlarmntous, b-g. col. = blue-green colonial, g. ﬁl. = green.
ﬁlamentous. p = present with abundance of < 5%. 0 = not present in the ample.

101

 

 
 
  

 

 

 

 

 

 

 

: "E: 10 2001 @ﬂ —o—control 2002
. 1 - -
OD +crayﬁsh
E5 0.1 « - I
8‘ g 0.01 - _,,.._ , . 9/9
[3 § {41:-313
a 0.001 - -
0.0001 . .
6/8 7/28 9/15 4/30 6/18
Effect df F P (If F P
Treatment 1,4 29.1 0.0057 1,4 14.4 0.0191
Time 3,12 38.9 <0.0001 1,4 4.18 0.1104

Treatmenthime 3,12 5.63 0.0121 1,4 0.01 0.9214

 

Figure 1. Mean zooplankton biomass in ponds with and without crayﬁsh (Orconectes
virilis) with results from repeated measures ANOVA. The ﬁsh symbols and arrows
indicate the estimated timing of the ﬁrst successful ﬁsh recruitment in each treatment for
consideration of trophic interactions between larval ﬁsh and zooplankton. Error bars
denote one standard error. Asterisks indicate signiﬁcant treatment effects (p-values <

0.004) on individual dates when treatments were sliced by time.

102

 

 

 

 

 

 

 

 

 

g 30100 2001 2002
E t: 10 ‘ _ i M
8%.. O 0 \g
338. - F"
f 8 1 "o—control ‘
o
E +crayﬁsh
U
0.1 1 l
6/8 7/28 9/ 15 4/30 6/18
Effect df F P df F P
Treatment 1,4 15.0 0.0180 1,4 24.6 0.0077
Time 3,12 17.8 0.0001 1,4 2.19 0.2131

Treatment x Time 3,12 0.48 0.7032 1,4 8.42 0.6270
Figure 2. Mean phytoplankton abundance (pg chlorophyll a ' L") in ponds with and

without crayﬁsh (Orconectes virilis) and statistical results from repeated measures

ANOVA. Error bars denote one standard error.

103

 

 

 

 

 

 

 

 

 

5 11 2001 2002
g2 10 ‘
g 4‘
13 ’7‘ 9 ‘
.2. §° 3 -
8 V —0—control
.‘2 7 -
D —O—crayﬁsh

6 r t

6/8 7/28 9/15 4/30 6/18
Effect df F P (If F P
Treatment 1,4 5.62 0.048 1,4 13.1 0.059
Time 3,12 8.46 0.038 1,4 16.7 0.513
Treatmenthime 3,12 0.95 0.591 1,4 12.1 0.104

 

Figure 3. Mean peak dissolved oxygen in ponds with and without crayﬁsh (Orconectes

virilis) with results from repeated measures AN OVA. Error bars denote one standard

error.

104

 

 

 

 

 

:1

50 10

5 ”inorganic
a 3 ‘

33 IOI'

<6

2 6‘

D

22:: 4—

5

O

E 2 -

a.

s 0 '
[— control crayﬁsh

Figure 4. Average total particulate matter (TPM) in the water column of ponds with and
without crayﬁsh (Orconectes virilis) in July of 2001. Error bars are one standard error
and refer to the standard errors of the entire bar. The ponds differed for all three measures

of particulates (total, organic, and inorganic, p-values < 0.04, see text).

105

 

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g E -0.2 .
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8. 5 -0.4 _ p<0.0001
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Figure 5. Results from a choice feeding assay where crayﬁsh were simultaneously
offered the dominant algal metaphyton from control and crayﬁsh ponds (Cladophora and
Gleotrichia). Error bars denote one standard error. The p-value is from a t-test of
differences incorporating mass changes from control buckets in the analysis to control for

variability due to autogenic mass change (see Peterson and Renaud 1989).

106

 

 

 

 

 

 

 

 

 

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Effect df F P df F P
Treatment 1,4 0.19 0.7081 1,4 3,30 0,144
Time 3,12 9.77 0.0071
Treatment x Time 3,12 8.54 0.0104

 

Figure 6. Mean abundance of periphyton (algae attached to hard surfaces; pg chlorophyll

a ' cm") in ponds with and without crayﬁsh (Orconectes virilis) with statistical results

from nn-AN OVA (2002) and one-way ANOVA (2002). Error bars denote one standard

error. The asterisk indicates a signiﬁcant (p < 0.05) treatment effect in June and August

2001 (slicing by time).

107

 

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Dry mass (mg)

Figure 7. Size-frequency histogram of chironomids (A) and Caenis mayﬂies (B) collected
from ponds with and without crayﬁsh. The p-value is from a Komolgorov-Smirnov two
sample test of distributions (chironomids: control n = 61, crayﬁsh n = 81; Caenis: control

n = 189, crayﬁsh n = 168).

108

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110

CHAPTER 5

COMPARING GRAZING RATES OF NATIVE AND EXOTIC ORCONEC T ES
CRAYFISH: THE IMPORTANCE OF FISH PREDATORS

ABSTRACT

The invasive crayﬁsh Orconectes rusticus has been replacing native Orconectes
virilis in lakes in the Midwest for several decades, and invaded lakes have suffered losses
of macrophyte biomass and diversity. Previous comparative experimental studies
indicate that per capita grazing capacities of these species do not differ. However,
previous experiments did not incorporate the effects of important predators (i.e., bass)
which may affect the two species differentially, because 0. rusticus is relatively less
vulnerable to bass predation. I measured the grazing capacities of adult 0. virilis and 0.
rusticus feeding on macroalgae (Chara vulgaris) in ponds with and without bass to
determine whether predators inﬂuence the relative grazing rates of these species. Mass-
speciﬁc consumption did not differ between species in the absence of predators or in the
presence of non-lethal bass threats (when cages were closed). When covers were
removed (open cages) and crayﬁsh experienced direct encounters with bass, the two
species responded differently to the predator contexts. Orconectes rusticus ate more than
0. virilis in the bass pond and 0. virilis fed slightly more than 0. rusticus in the control
pond. These results suggest that bass predators can have important effects on relative

impacts of native and non-native crayﬁsh.

KEYWORDS: Chara, crayﬁsh, herbivory, invasive, Micropterus, native, Orconectes

rusticus, Orconectes virilis, predator

111

INTRODUCTION

The predatory impacts of native and exotic animal species are commonly
compared in experimental settings in order to predict or to understand the relative effects
of invasions (e.g., Olsen et al. 1991, Nystrﬁm and Strand 1996, Dick et a1. 2002, Loher
and Whitlatch 2002). The usual protocol involves stocking similar numbers of each
species into controlled experimental arenas and measuring effects on other trophic levels.
Often these experiments do not incorporate the predators of the focal organisms, although
interactions with predators are widely known to inﬂuence animal foraging behavior
(Werner et a1. 1983, Gilliam and Fraser 1987, Lima and Dill 1990). If the two species
respond differently to a natural predator, then the results from an experiment without
predators may have limited relavence to ﬁeld conditions with predators.

Over the past several decades Orconectes rusticus (rusty crayﬁsh) has invaded
many lakes in the Midwest. Introduced primarily through the live bait trade, 0. rusticus
has displaced other Orconectes crayﬁsh (0. virilis and 0. propinquus) and become a
dominant part of the fauna in many lakes (Capelli 1982, Hobbs et al. 1989, Olsen et al.
1991, Hazlett et al. 1992, Hill and Lodge 1999). The mechanisms responsible for the
takeover have been well-documented and include competition for shelter, selective
predation by ﬁsh, and hybridization (Capelli and Munjal 1982, Didonato and Lodge
1993, Garvey et al. 1994, Hill and Lodge 1999, Perry et a1. 2001).

Orconectes rusticus and 0. virilis (the native species it replaces) have similar
feeding habits, similar adult size, and are both known to actively consume and destroy

macrophytes and macroalgae (Chara vulgaris) (Lodge and Lorman 1987, Chambers et al.

112

1990, Lodge et a1. 1994). Several studies have reported that macrophyte beds have been
reduced in biomass and/or species richness in lakes invaded by 0. rusticus (e.g., Capelli
1982, Lodge et a1. 1985, Covich et a1. 1999). Lab and ﬁeld experiments indicate that the
two species have similar grazing abilities (Olsen et al. 1991, Hazlett et a1. 1992), which
has led to the conclusion that the greater effects of 0. rusticus on macrophytes must be
due to higher densities of crayﬁsh in invaded lakes (Olsen et al. 1991 , Hazlett et a1.
1992). However it is also possible that the experimental context in which these studies
were done obscures differences between the species

Previous comparative experiments with these crayﬁsh have been performed in
closed cages or aquaria that did not include direct interactions with predatory ﬁsh. Bass
(Micropterus spp. and Ambloplites spp.) are common and important predators of crayﬁsh
(Rickett 1974, Stein 1977, Dorn and Mittelbach 1999) and the non-lethal effects of
largemouth bass (Micropterus salmoides) presence is known to reduce the grazing rates
of Orconectes crayﬁsh (Hill and Lodge 1995). Orconectes rusticus is also relatively less
vulnerable to ﬁsh predation than native crayﬁsh species because of it’s greater defensive
armor and less-risky behavior (Didonato and Lodge 1993, Garvey and Stein 1993,
Garvey et a1. 1994). If relative vulnerability affects feeding behaviors, then 0. rusticus
should be expected to feed at higher rates in the presence of predatory ﬁsh.

In this experiment, I measured the grazing capabilities of adult 0. virilis and 0.
rusticus feeding on the macroalgae Chara vulgaris. In the ﬁrst feeding trial I measured
grazing in closed cages in two ponds — with and without bass predators. With the cages
closed, crayﬁsh could see and detect the presence of chemical cues from the bass

(Wihnann et al. 1994, Hazlett and Schoolrnaster 1998), but experienced no direct risk of

113

predation. In a second trial I used the same setup but I removed the covers from cages in
both ponds so that bass were able to explore the cages and directly threaten the crayﬁsh.
The second trial incorporated natural predator-prey interactions and also allowed for
emigration (escape) from the habitat. My aim was to determine whether there was any
evidence that 0. rusticus has greater mass-speciﬁc grazing abilities than 0. virilis, and
whether relative effects of the two species depend upon experimental context (predator
effects). I hypothesized that: 1) the relative effects of the species would not differ in the
control pond, 2) overall crayﬁsh feeding rates would be lower in the pond with bass than
in the control pond, 3) consumption by 0. rusticus would be greater than by 0. virilis in
the presence of bass predators.
MATERIALS AND METHODS

The feeding trials were conducted in two experimental ponds at the Kellogg
Biological Station Experimental Pond Facility in Southwestern Michigan. The ponds (29
m diameter, 2 m deep) were less than 2 years old, never contained ﬁsh, and had been
colonized with approximately 20—40% cover Chara vulgaris. Because the predator
context was not replicated (treated as a block) it is potentially confounded with other
differences between the ponds. However, these ponds were in the early stages of
succession and had similar biotic and abiotic (i.e., bathymetry, water source) features
except for bass introductions.

In June 2002, I constructed 32 circular cages ﬁom 50-cm tall metal ﬂashing. The
cages measured 1 m2 in area and had an aluminum screen bottom so that crayﬁsh could
not escape by burrowing under the walls. Each cage had a cover made of a nylon ﬁsh net

(1 cm mesh) stretched out inside a circular piece of black tubing that completely sealed

114

the top of the cage. The covers kept the crayﬁsh ﬁ'om swimming or crawling out but
allowed them to see and sense their environment (bass vs. no predators). Sixteen cages
were placed in the deepest areas of each pond and equal amounts of sand were added to
each to serve as substrate. Three PVC shelters (5 cm diameter, 12-14 cm long) were
added to each cage to give the crayﬁsh a place to refuge.

Animals

Seven large (mean Total Length (s.d.) = 339 mm (32), Range = 285-388 mm)
largemouth bass (Micropterus salmoides) seined ﬁ'om a nearby lake were added to one of
the ponds on 11 July. Because the crayﬁsh in this experiment were rather large, they may
not have been very vulnerable even for large bass predators. However, Lodge and Hill
(1995) found that bass presence had a negative impact on crayﬁsh grazing even though
the predator-prey size relations were such that crayﬁsh were too big to be in serious
danger.

Orconectes virilis and Orconectes rusticus were collected by hand and with baited
traps in West Grand Traverse Bay (Lake Michigan). Because I did not want to introduce
viable populations of 0. rusticus to the ponds, only males were used in this study. All
crayﬁsh were Form 11 males when they were added to the cages, but some of both species
molted during the ﬁrst trial so the crayﬁsh were a mixture of Form I and Form II males
during the second trial. Each species was added (in groups of 3; 3 crayﬁsh - m") to 8
cages in each pond after being measured (Carapace length - CL) and weighed (g wet
mass). Although carapace length (CL) did not differ signiﬁcantly between the species
(mean (s.d.), 0. virilis: 37.2 mm (2.2); 0. rusticus: 35.9 mm (2.9)), O. virilis cages had

slightly more total crayﬁsh mass (mean mass = 48.8 g vs. 46.7 g; t-test p = 0.08).

115

Because of differences in crayﬁsh mass between species, and because some crayﬁsh were
lost from the open cages, I calculated crayﬁsh grazing rates on a mass speciﬁc basis (g -
g") for each cage in each experiment. In cases where crayﬁsh densities were lower in a
cage at the end than at the start of the experiment, I calculated average crayﬁsh mass
during the experiment, assuming either a constant number or a constant proportion of
crayﬁsh was lost per day.

Trial 1 — No predator vs. Non-lethal threat (closed cages).

In the ﬁrst grazing trial the cages were closed (covers on). On 17 July, Chara
vulgaris, with associated epiﬂora and epifauna (hereafter Chara), was collected from the
ponds, lightly rinsed, and allowed to drip dry (in masses of 50-80 g) for approximately
20-30 seconds before being weighed. Each cage received 300-335 g of Chara, and care
was taken to spread it out so that it could not be dominated by a single crayﬁsh. During
the feeding trial, observations were made on two days to record any molting and make
certain crayﬁsh had not completely consumed the Chara. Crayﬁsh were allowed to graze
for 7 days at which time the remaining Chara was carefully collected by a diver using
SCUBA. After the Chara was reweighed, mass-speciﬁc consumption (g - g") was
calculated as (initial wet mass — ﬁnal wet mass) ° crayﬁsh wet mass". Both trials were
analyzed as a randomized block designs (with replication inside blocks) in SAS with Proc
glm (SAS 8.0, SAS institute). Having replicate cages in each pond allowed me to look at
the interaction of predator context (pond) and species.

Trial 2 -- No predator vs. Direct threat (open cages).

Immediately at the end of the ﬁrst trial, I started a second trial with the same

groups of crayﬁsh. In Trial 2, all the cage covers in the bass pond were removed to allow

116

bass predators access to the insides of the cages (i.e., to threaten or eat crayﬁsh). In
addition, the crayﬁsh could potentially crawl or swim out by their own volition.
Although I never observed crayﬁsh climbing up the cage walls, occasionally an
individual 0. rusticus was observed hanging upside-down from the covers during Trial 1.

In the control pond, I left covers on half of the cages to determine whether or not
the crayﬁsh changed grazing behavior simply depending on the presence of a cover (i.e.,
if they stopped grazing and devoted their efforts to escaping). The treatment combination
of 0. rusticus without a cover was replicated only three times because a few crayﬁsh
were lost during setup due to mortality and an escape.

The second trial lasted two days (compared to seven days for Trial 1) and 48-60 g
of Chara was added to each cages. Care was taken to make sure the Chara was spread
out within the cage. At the end of the trial the number of remaining crayﬁsh was counted
at the same time the Chara was removed. When I calculated consumption in Trial 2, I
corrected the crayﬁsh mass to account for crayﬁsh that disappeared from the cages.
Because I did not want to scare the crayﬁsh out of cages by my presence, I did not make
any counts of crayﬁsh during the experiment. Instead I calculated the average number of
crayﬁsh in each cage assuming a constant proportional daily disappearance rate (i.e.,
exponential decay). The disappearance rates were calculated independently for the two
species in each pond. The results of the ﬁnal analysis do not change if the disappearance
rate is calculated based on a constant number instead of a constant proportion. The
average number of crayﬁsh in each cage during the experiment was used to calculate the
average mass of crayﬁsh and the mass-speciﬁc consumption for each cage. I analyzed

the control pond alone as a 2 x 2 factorial AN OVA with crayﬁsh species and presence of

117

cover as the two factors to look for effects of a cover on consumption (i.e., changes in
behavior). In the analysis of both ponds I used only the open cages, but the results do not
change if all cages are used.
RESULTS
Trial 1 -- No predator vs. Non-lethal threat (closed cages).

No crayﬁsh escaped the cages during the seven day trial indicating that the covers
were effective at keeping the crayﬁsh inside. Chara wet mass declined by an average of
72%, and there were no differences in the amount of Chara consumed per gram of
crayﬁsh between the two species. 0. virilis and 0. rusticus also had consumed similar
amounts of Chara in the two ponds (Figure 1, Table 1). Removing cages in which
crayﬁsh molted during the trial from the analysis did not change the results nor did
removing the interaction term from the analysis.

Trial 2 — No predator vs. Direct threat (open cages).

When the covers were removed, crayﬁsh were open to close encounters with the
bass in the predator pond (direct predator threat) and all crayﬁsh in open cages had the
opportunity to escape. Of 48 total crayﬁsh in the bass pond cages at the beginning of the
trial, 65% remained at the end of the experiment (17 total missing). Comparing the
species in the bass pond, 25% (6 of 24) of 0. virilis and 46% (11 of 24) of 0. rusticus
were missing. A larger percentage of total crayﬁsh (52%) disappeared from open cages
in the control pond than in the bass pond and this was due to the large number of missing
0. virilis (58%; 7 of 12). The percentage of 0. rusticus that disappeared (44%; 4 of 9)

was similar in the bass and control ponds.

118

When the control pond was analyzed for effects of the mesh cover on
consumption, Cover and the Cover x Species interaction terms were not signiﬁcant (F 1,”
= 0.26, p = 0.61; F 1,11 = 0.041, p = 0.84), indicating that crayﬁsh in the control pond were
grazing similarly in the presence and absence of a cover.

Crayﬁsh lower feeding rates in the second experiment and that was probably a
result of different Chara stocking densities and functional responses. In the overall
analysis the main effects of species and pond were not signiﬁcant, however the two
species responded in markedly different ways to the opening of the cages in the two
ponds (Figure 2, Table 1; interaction term p = 0.02). Individual T-tests within the ponds
indicated that the remaining 0. virilis had non-signiﬁcantly (p = 0.15) higher
consumption in the control pond, while the remaining 0. rusticus ate signiﬁcantly more
in the bass pond (p = 0.04).

DISCUSSION

In previous feeding assays with these two species, 0. rusticus had a higher per
capita feeding rate on snails (Olsen et al. 1991), but there was no difference in feeding
rates on macrophytes (Olsen et al. 1991, Hazlett et a1. 1992). Olsen et al. (1991)
performed their experiment in laboratory aquaria with no predators present. Hazlett et al.
(1992) do not provide information about predators in the stream where they conducted
their experiment but their closed cages would not have allowed for direct interactions
between crayﬁsh and ﬁsh predators. In Trial 1 of this study, I found no differences in
grazing between the species in a predator free pond and in a pond with non-lethal bass
threats. These contexts are most similar to the contexts used in previous studies (Olsen et

al. 1991, Hazlett et a1. 1992).

119

Interestingly, there was no main effect of pond (bass presence) in either
experimental trial. Bass presence has been shown to inﬂuence crayﬁsh grazing rates in
other studies (e. g., Hill and Lodge 1995). However, the average crayﬁsh in my
experiment was larger than the largest crayﬁsh in the study by Hill and Lodge (1995),
and Didonato and Lodge (1993) showed that larger crayﬁsh are less vulnerable to natural
assemblages of ﬁsh predators.

Although there was no overall effect of bass lowering crayﬁsh grazing, the
crayﬁsh species responded differently to the two predator contexts when cages were
opened and crayﬁsh experienced direct encounters with the bass (Trial 2). 0. virilis ate
slightly more than 0. rusticus in the control pond, but 0. rusticus ate substantially more
in the bass pond. By allowing for natural predator-prey interactions, the bass pond in
Trial 2 incorporated more environmental reality than previous comparisons and the
results suggest that adult 0. rusticus can have substantially greater grazing effects on
macroalgae than the native 0. virilis in the presence of direct encounters with bass.

The slightly higher average consumption by 0. virilis in the control pond is not
inconsistent with the ﬁndings of Olsen et al. (1991) and Hazlett et al. (1992). In both
studies 0. virilis had slightly, albeit statistically non-signiﬁcantly, greater macrophyte
destruction rates than 0. rusticus.

During Trial 2 in the bass pond, 0. msticus ate more and it tended to disappear
from the cages more than 0. virilis (46% O. rusticus vs. 25% 0. virilis were missing).
Missing crayﬁsh could have been eaten by bass or may have escaped. It is possible that
0. rusticus foraged more actively, became more exposed to predation, and experienced

greater mortality. However, this seems unlikely as 0. rusticus has been shown to be less

120

vulnerable to ﬁsh predation in experimental pools and lakes (Didonato and Lodge 1993,
Garvey et al. 1994). Furthermore, a similar percentage of 0. rusticus (44%) disappeared
from cages in the control pond where there were no predators. This suggests that 0.
rusticus was probably escaping rather than being consumed. The fact that more than half
of 0. virilis escaped from cages in the control pond and only 25% were missing in the
bass pond suggests that 0. virilis decreased overall activity (feeding and escape
activities) when exposed to direct predation threats. 0. rusticus appeared more active in
the presence of direct predator threats; it ate more and escaped more often than 0. virilis.

In conclusion, these results indicate that 0. rusticus can have larger mass-speciﬁc
grazing effects than 0. virilis, and that the relative grazing impacts of these species may
depend on predators. Because most lakes have bass or other predatory ﬁsh, the observed
negative effects of introduced 0. rusticus on macrophytes may be due to higher grazing
rates per unit biomass (compared to native crayﬁsh species) as well as higher overall
population densities (Olsen et al. 1991). In general, experiments comparing feeding rates
among species should consider incorporating the effects of predators into the

experimental design.

ACKNOWLEDGMENTS
I am thankful to E. Garcia, E. Thobaben, J. Wojdak, and C. J. Wykoff for help
setting up and scoring the experiment. Denton and Shirley Nelson graciously allowed me
to collect crayﬁsh from their property. N. Dubois, K. Gross, S. Hamilton, D. Lodge, G.
Mittelbach, and E. Thobaben were helpful with advice and comments on the paper. The

work was funded by a Lauff Research Fellowship and a Graduate Research Training

121

Grant (RTG) ﬁinded by the National Science Foundation (grants DIR-09113598 and

DBI-9602252).

122

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Table 1. Analysis of variance results for two grazing trials
comparing native (Orconectes virilis) and introduced
(Orconectes rusticus) crayﬁsh feeding on macroalgae (Chara
vulgaris) in two ponds (with and without bass). Mass-
speciﬁc consumption was measured for groups of crayﬁsh
grazing inside cages.

 

Trial 1. No bass vs. Non-lethal threat (closed cages)

df F P
Pond 1 0.18 0.677
Species 1 0.09 0.765
Pond x Species 1 0.23 0.634
Error 28

Trial 2. No bass vs. Direct bass threat (open cages)

 

Pond l 0.23 0.637
Species 1 0.001 0.984
Pond x Species 1 6.36 0.021
Error 19

125

 

I

[:1 0. virilis
E] 0. rusticus

I

l I

I‘ Q -". '. r
\ O. v , r '.
. r“ 'Zih‘ ,- , _ ..I -.

I .‘- ' 5""
.. .. ,
.. J 3" . .
'35); Xy‘er‘ ‘-

Mass-speciﬁc Consumption
(g g I) mean i 95% Cl
C H N M & VI 01 \l 00 \O

 

 

 

 

 

 

 

 

17

Control Pond Bass Pond

Figure 1. Mass-speciﬁc consumption of Orconectes crayﬁsh feeding on Chara in closed
cages inside ponds with and without bass. Crayﬁsh in the bass pond were exposed to
non-lethal threats (i.e., sight and smell) of largemouth bass (Micropterus salmoides). The
numbers inside the bars indicate the number of replicates. Wet masses were used in

calculations of consumption.

126

 

 

 

.5 _

’5. C2,) 1'2 5 Cl 0. virilis
\

g 3‘ 1 I .0. rusticus

5 ° |

0 +1 0.8 ..

a E O 6- |

g E .

3 '30 0.2 ~ . .5." "

<6 v 4 _- 3. .

2 0 , - I

 

 

 

 

 

 

 

 

Control Pond Bass Pond
Figure 2. Mass-speciﬁc consumption of Orconectes crayﬁsh feeding on Chara in open
cages inside ponds with and without bass. Crayﬁsh in the bass pond were exposed to
direct interactions with largemouth bass (Micropterus salmoides). The numbers inside
the bars indicate the number of replicates. Wet masses were used in calculations of

consumption.

127

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