Download predator accelerated replacement

THE ROLE OF COMPETITION, PREDATION, AND THEIR INTERACTION IN
INVASION DYNAMICS:
PREDATOR ACCELERATED REPLACEMENT
BY:
BRIAN M. ROTH
A thesis submitted in partial fulfillment of the
requirements for the degree of
MASTER OF SCIENCE
(Limnology and Marine Science)
at the
UNIVERSITY OF WISCONSIN-MADISON
2001
2
Table of Contents
ABSTRACT
Page
iv
ACKNOWLEDGEMENTS
vi
CHAPTER 1
Patterns of Interacting Competition and Predation in
Invasion Dynamics: Predator Accelerated Replacement
Introduction
2
Selective Predation: The Driver of the
Accelerated Replacement Hypothesis
5
General Patterns of Competition Interacting
With Selective Predation
7
Factors Confounding the PAR Hypothesis
9
Management Implications
11
Future Research Considerations
12
Summary
13
Conclusion
14
References
15
Table 1.1
21
CHAPTER 2
Selective Fish Predation on a Crayfish Species Assemblage: Implications
for Rusty Crayfish (Orconectes rusticus) Invasions
Introduction
23
Methods
25
Results
30
3
Discussion
34
Summary and Conclusion
43
References
45
Figure Captions
49
Figures
51
4
ABSTRACT
THE ROLE OF COMPETITION, PREDATION, AND THEIR INTERACTION
IN INVASION DYNAMICS:
PREDATOR ACCELERATED REPLACEMENTS
Brian M. Roth
Under the supervision of Professor James F. Kitchell
Predation is a powerful force capable of influencing community structure.
Predation can affect species interactions, directly through prey removal, or indirectly
by altering competitive interactions among prey species. Previous studies regarding
invasion dynamics have mainly focused on characteristics of the invader and the
invaded system, dispersal rates, and competition between native and exotic species.
I provide a literature review and field study to test the Predator Accelerated
Replacement hypothesis (PAR), the idea that predators facilitate replacement by
exotics through selective predation on native species when both exotics and natives
compete for a finite resource such as food or shelter. Field, laboratory, and
theoretical studies in the literature indicate that invasions meeting predator
accelerated replacement criteria occurred in a broad array of aquatic and terrestrial
ecosystems. I also tested the hypothesis that selective fish predation accelerates
rusty crayfish (Orconectes rusticus) invasions through congener removal in North
Turtle Lake, Wisconsin. Fish diet data was collected on four dates between 29 June
and 27 August 2000, and quantified crayfish abundance at six locations in N. Turtle
Lake. In addition, I estimated crayfish consumption by predators in N. Turtle Lake
during the study period using bioenergetics modeling. Smallmouth bass
(Micropterus dolomieu) and yellow perch (Perca flavescens) relied heavily on
crayfish prey, but avoided rusty crayfish in favor of congeners O. propinquus and O.
virilis. In contrast, rock bass (Ambloplites rupestris) and walleye (Stizostedion
vitreum) were more opportunistic crayfish predators. Orconectes propinquus in diet
samples were similar in size to those found in the environment, but O. rusticus in
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diets were smaller in diets than in the environment. However, O. propinquus and O.
rusticus in diet samples were of equivalent sizes. This suggests that fish prey on
similarly sized crayfish of different species, but since O. rusticus reach a larger adult
size than O. propinquus, the proportion of O. propinquus population vulnerable to
predation is larger than O. rusticus. I suggest future studies regarding invasion
dynamics should consider not only competition for food and shelter resources
between invading and native species, but also consider direct and indirect predation
effects that may contribute to exotic success and native decline.
6
ACKNOWLEDGEMENTS
Completing a Master’s degree in less than two years is no small feat. I could
not have attended the University of Wisconsin, let alone completed my degree
without the help of many people who helped me obtain funding, develop an
interesting research question, complete my field work, and hone my writing skills.
In essence, I did not write my Master’s thesis alone, and in this section, I hope to
give justice to those who helped and encouraged me along the way
First off, I would like to thank my funding sources. The Anna Grant-Birge
Memorial Fund financed most of my field supplies, as well as my hourly assistant.
Also, I must acknowledge the Integrated Graduate Education Research Traineeship
(IGERT) program and the University of Wisconsin Graduate School, who provided
me with funding for the four semesters of my Master’s.
I am somewhat amazed at the route my life has taken. I still get shivers
when I think that I actually can get paid (at some point) for studying fish. I must
thank my Uncle Ron who took me fishing at a very young age and taught me the
fine art of “Hooking”. These early fishing experiences stayed with me throughout
my college education. Dr. Gilbert Pauly was my first research advisor and
enlightened me to smallmouth bass research. Dr. Thomas Sibley and Dr. Daniel
Schindler both taught me about the broad possibilities of research in freshwater
ecology at the University of Washington.
7
My experience at The Center for Limnology has been nothing short of the
most intense, most positive learning environment I have ever been in. I cannot
accurately express how helpful all the students and professors have been since I
have been here. Steeped in a world of whole-lake experiments, ecosystem ecology,
modeling, and statistics, I have learned more about ecology, and science in general,
in the past year than I had previously in my entire lifetime.
My fellow graduate students have been exceptionally helpful. I must thank
Greg Sass and Jefferson Hinke, who not only helped me in the field, they gave me
encouragement and editorial advice in my constant battles with scientific writing.
Together with Jon West, Greg and Jefferson were adept at keeping me loose and
having fun, even when things got tough. Karen Wilson, my fellow crayfishite, has
helped me tremendously by volunteering her vast knowledge of biological invasions
and rusty crayfish, and helped me hone the first chapter of this thesis.
The Kitchell lunch group, as a whole, helped me refine my ideas regarding
the Accelerated Replacement Hypothesis, as well as steered me in the right direction
regarding data analysis of my second chapter. Tim Essington, Sean Cox, and Isaac
Kaplan all helped me enormously on the first chapter, which began as a puddle of
random thoughts about invasions, and ended up being a pretty good paper
regarding invasion dynamics.
Jaime Laluzerne (my hourly), Jesse Lepak, Adam Ray, Michelle Leubke,
Carrie Byron, among others all braved angry cabin owners and mosquito swarms to
help me collect all the fish and crayfish data I needed from North Turtle Lake. In
8
addition, they helped Wednesday nights in Sayner become a highlight of my
summer.
I would like to thank my committee, who spent time with me even if they
didn’t have any to spare. I am indebted to my advisor, Jim Kitchell, who spent
enough energy honing my research question and writing skills to light a small city.
I could not be the person I am today without my family. I must thank my
mother, father, and sister for all their support. I am grateful for the love and kind
words they have given me, even when I felt incapable of doing quality research.
Without them, I’d be lost.
9
Chapter 1
Patterns of Interacting Competition and
Predation in Invasion Dynamics:
Predator Accelerated Replacement
"This interaction between competition and predation forms a
central conceptual element of community ecology."
--Earl Werner 1991.
INTRODUCTION
What makes an ecosystem invasible or resistant to invasion is hotly debated
(Ehrlich 1989, Case 1990, Lodge 1993, Moyle and Light 1996). Abiotic constraints
ultimately dictate which species might potentially invade an ecosystem (e.g. Carlton
1985, Moyle and Light 1996, Buchan and Padilla 1999). However, invasion success
or failure is highly variable (within acceptable abiotic conditions), and may depend
on both ecosystem properties (such as low native diversity, absence of fire in
evolutionary history, high predator numbers) (e.g. Elton 1958, Ehrlich 1989, Case
1990, Lodge 1993, Vermeij 1996) and exotic attributes (such as high reproductive
potential, long life span, broad diet, etc.) (e.g. Ehrlich 1989, Lodge 1993, Hastings
1996, Hart and Gardner 1997, Kolar and Lodge 2001). Evidence suggests that most
exotic species introductions will fail (Ehrlich 1989, Simberloff and Stiling 1996, Mack
et al 2000, Kolar and Lodge 2001). Inevitably, some exotic species do become
established.
Factors that determine community assemblage, such as predation,
competition, and their interaction, have long been debated in ecological literature
(e.g. Slobodkin 1961, Paine 1966, Woodward 1983, Strong 1992, Carpenter and
Kitchell 1994, Gamradt and Kats 1996). These studies suggest that predators not
11
only affect prey through direct removal of individuals, but also through indirect
effects such as changes in foraging behavior and spatial distribution as a response
to predation risk (e.g. Seghers 1974, Sih 1982, Woodward 1983, Erneberg 1999,
Lawler et al 1999, Werner 1991). Indirect predation effects can exacerbate
competition between prey species that contribute to local reduction or extirpation of
weaker competitors (e.g. Woodward 1983, Wilbur et al 1983, Werner 1991, Facelli
et al. 1988, Olsen et al 1991, Pettit et al 1995, Hart and Gardner 1997). Conversely,
direct predation effects allow weaker competitors to succeed in some instances
(Paine 1966, Wilbur et al 1983, Woodward 1983, Werner 1991, Lawler et al 1999).
Some studies argue that biotic interactions between native and exotic
species within the invaded systems are often minimal because most exotic species
enter vacant niches (Case 1990, Forys and Allen 1999, Mack et al 2000). In
contrast, there are many examples of invasions where the exotic directly competes
with native species, contributing to native decline (e.g. Capelli and Munjal 1982,
Brenchley 1983, Ehrlich 1989, Okubo 1989, Simberloff 1991, Huckins et al 2000,
Williamson 1999, Fullerton et al 1998). Also, several examples exist where exotic or
native predators contribute to native decline and exotic success (Jones et al 1995,
Krueger et al 1995, Ogle et al 1996, Case 1996, Gamradt and Kats 1996, MacIsaac
et al 1999, Didonato and Lodge 1993). Studies regarding predation in invasion
dynamics suggest that invaders less susceptible to predators than natives may have
an advantage persisting in a new system (Case 1996, Hastings 1996, Hart and
Gardner 1997, Mack et al 2000).
12
Surprisingly, few studies have applied direct and indirect predation theories to
invasion dynamics (but see Facelli et al 1988, Noy-Meir et al 1989, Didonato and
Lodge 1993, Garvey et al 1994). Therefore, I use knowledge of direct and indirect
predation effects in this investigation to formulate the Predator Accelerated
Replacement hypothesis (PAR). The two defining criteria of predator accelerated
replacements are: 1) competition between native and exotic species for a finite
resource, and 2) selective predation favoring the exotic. Invasions meeting predator
accelerated replacement criteria occur in a broad array of aquatic and terrestrial
ecosystems, including those where grazers act as predators in grasslands (Table
1.1). The few examples of invasions meeting PAR criteria in the literature may be
less numerous than other types of invasions, such as those where the exotic invades
an empty niche (e.g. Forys and Allen 1999), or where the habitat is so disrupted
that resistance to invasion may be compromised (Case 1990). However, the
defining criteria of the PAR hypothesis are few and uncomplicated. Therefore, I
suspect that other studies may have overlooked invasions accelerated by predators.
In the following sections, I first introduce how competition and selective
predation can influence invasion dynamics. Second, I discuss several patterns of
competition and selective predation that, when interacting, produce outcomes that
may determine exotic species success or failure. I also discuss possible confounding
factors to the PAR hypothesis, and follow with future research considerations.
Unlike other studies that generalize characteristics of ‘good’ invaders and
‘vulnerable’ ecosystems (e.g. Elton 1958, Ehrlich 1989, Lodge 1993, Kolar and Lodge
13
2001), I discuss general patterns of competition and predator-prey relationships that
interact to accelerate native species replacement by exotics. I hope to contribute to
productive debate of invasion success by assessing complex invasion dynamics in a
community context.
SELECTIVE PREDATION: THE DRIVER OF
PREDATOR ACCELERATED REPLACEMENTS
The underlying mechanism of PAR is the greater vulnerability of native
species to predators relative to the exotic. Anti-predator defense often involves
morphology, behavior, or life history traits (Mack et al 2000, also see Werner 1991
for references). The PAR hypothesis assumes that predators are selective, which is
well founded (Brooks and Dodson 1965, Noy-Meir et al 1989, Didonato and Lodge
1993, Ogle et al. 1996, Roth Chapter 2). Optimal foraging theory and empirical
evidence suggest that predators consider cost and benefits of foraging (e.g.
Schoener 1971, Pyke et al 1977, Werner 1974, Werner and Hall 1974, Hodgson and
Kitchell 1987, Schindler et al 1997). That is, predators should maximize fitness by
maximizing their energy gain, while minimizing their energy costs (e.g. Werner
1974, Stein 1977, Sih 1984). Where alternative prey are available, predators
maximize their energy gain by preying selectively on species that are easiest to
capture and consume while avoiding prey species that are more difficult. Simply
stated, predators maximize fitness by being selective (Brooks and Dodson 1965).
The PAR hypothesis assumes that the native is more vulnerable to predation than
14
the exotic, therefore making it energetically beneficial for the predator to selectively
prey upon the native.
Selective predation may depend on the history (or lack thereof) of the exotic
with native predators (e.g. Lodge 1993, Moller 1996, Mack et al. 2001), and
therefore may not be a product of any invader characteristic. Predators may take
time to learn to feed on a new prey item (Ware 1971). In the case of invasions, the
learning process may force the predator to continue preying on the native following
exotic introduction. However, selective predation due to the lack of evolutionary
history is indistinguishable from selectivity caused by morphological, behavioral, or
life history defenses because the result of predation events (prey mortality) is the
same.
Selective predation caused by prey competition regimes, prey morphological
differences, or both, drive the PAR. Therefore, I call predation ‘selective’ if mortality
risks among competing prey species differ. Hence, predators can actively avoid
exotic species (e.g. when chemical defenses are present), or passively choose native
species made vulnerable by competitive interactions with the exotic.
I describe in the following section how selective predation can enhance or
reverse prey competition regimes caused by differences in prey morphology and
behavior traits. Without selective predation, the invasion might be drastically slower
or fail all together, particularly if the exotic is competitively inferior to the native
species.
15
GENERAL PATTERNS OF COMPETITION
INTERACTING WITH SELECTIVE PREDATION
When the Exotic is Competitively Superior to the Native
Competitively inferior species have been shown to increase their search time
for resources in areas not occupied by the dominant species, thus increasing
exposure to predators (Wilbur 1982, Woodward 1983). Increased exposure to
predators increases selective predation pressure over that which would occur if both
species were competitively equal (Wilbur 1982, Werner et al. 1983, Wilbur et al.
1983, Woodward 1983, Werner 1991). Predators thereby lower the density of
inferior species, releasing the dominant species from both inter- and intra-specific
competition (Wilbur et al 1983, Case 1996). For example, Eurasian ruffe
(Gymnocephalus cernuum) and rusty crayfish (Orconectes rusticus) invasions follow
this pattern of competitive superiority and lower predation susceptibility. Rusty
crayfish and Eurasian ruffe are able to out compete native congeners for shelter and
food, respectively (Capelli and Munjal 1982, Fullerton 1998). In addition, both
species have morphological traits (fin spines and chelae size) that allow lower
predation susceptibility relative to natives (Garvey et al 1993, Ogle et al. 1996).
When the Exotic is Competitively Inferior to the Native
Predator accelerated native replacement may also occur when the exotic is
competitively inferior to the native. For example, exotic broad-leaf herbs and annual
grasses have become established in the Flooding Pampas region of Argentina in
16
areas that are grazed by cattle (Facelli et al 1998). Grazing favors low growth-form
annuals in the Flooding Pampas, and in some parts of Australia as well (Leigh et al.
1989, Pettit et al 1995, Facelli et al 1998). Most of the native grasses have tall
growth forms, and are able to shade out exotics when grazing is absent.
Differential predation risk among native frogs and exotic bullfrogs (Rana
catasbeina) has been implicated as a possible mechanism contributing to the decline
of native anurans (Lawler et al 1999). The larval bullfrog’s ability to compete for
food is weak compared to natives. However, bullfrog tadpole survivorship is
elevated, relative to the native, when a predation risk is present (Woodward 1983,
Lawler 1989). Predation is thought to enhance the larval bullfrog’s survivorship by
shifting the competition balance among tadpoles (Lawler et al 1999). Although
bullfrog tadpoles forage less than natives and grow slower (Lawler et al 1999),
greater survivorship out-weighs the weaker competitive ability, primarily in
permanent ponds where native tadpoles are subjected to a greater diversity of
predators (Woodward 1983).
When the Native is Exposed to a Novel Predation Threat
Many successful invasions occur when native prey species do not have an
evolutionary history with an introduced predator (e.g. Atkinson 1985, Facelli et al
1988, Case 1996, Pettit et al 1999) because native prey did not evolve adequate
defense mechanisms (Case 1996, Lodge 1993). Conversely, exotic prey species
often come from predator-rich systems and have evolved effective defenses in order
17
to persist in their native ranges (Case 1996). Island fauna tend to be particularly
susceptible to novel predators (Atkinson 1985, Case 1996, Kolar and Lodge 2001).
Case (1996) and Atkinson (1985) both suggest that introduced predators enhance
the success of exotic bird species on islands by moderating competition between
natives and less vulnerable exotics.
When the Exotic has Characteristics that Directly Contribute to Native Decline
Possibly the most dramatic form of predator accelerated replacement occurs
when the exotic species has multiple attributes that contribute to its success (Lawler
et al. 1999). For example, the cane toad (Bufo marinus) has several characteristics
that permit higher survivorship than natives in eastern Australia. Cane toads in all
life stages are toxic to predators, out compete several native anuran tadpoles for
food in pond communities, and prey upon native anurans (Williamson 1999).
FACTORS CONFOUNDING THE PAR HYPOTHESIS
Disturbance
Habitat disturbance may open a window into ecosystems for invasions by
removing or weakening links in the food web, causing the community to become
more susceptible (Case 1990, Forys and Allen 1999). Severe disturbance may
supercede any possible biotic interactions, making predation and/or grazing less
relevant in the replacement of native species. In particular, human induced
disturbance may bring receptive communities in closer contact with domestic,
18
semiferal, and feral biota such as rats, cats, and ‘weeds’ (Lodge 1993). However,
determining which ecosystems are ‘disturbed’ and which are not is difficult because
human influence is omnipresent (Mack et al 2000).
The introduction (whether purposeful or accidental) of predators to areas
without an evolutionary history of predator influence is often classified as
‘disturbance’ (Lodge 1993). Separating ‘disturbance’ from accelerated replacement
is difficult in these cases because the mechanism for native replacement is the
same.
Apparent vs Actual Competition
Apparent competition occurs when the population dynamics of two prey
species appear to be the result of exploitative competition, but instead are the result
of differential mortality from a shared predator (Holt 1977, Holt and Kotler 1987,
Holt et al 1994). By definition, competition between the two prey species may or
may not occur, but divergent numerical responses of the preferred prey species and
the less preferred prey species, as a result of selective predation, mimics
competitive superiority of the less preferred prey species (Holt 1977, Holt and Kotler
1987, Holt et al 1994). Juliano (1998) suggests that apparent competition between
exotic and native mosquitoes in North America caused by a protozoan parasite
causes native replacement. Apparent competition confounds the PAR hypothesis
because without ‘real’ competition, one of the PAR criteria fails to materialize, and
the invasion is no longer a replacement. However, detecting whether competition is
19
apparent but nonexistent for resources, or apparent with real competition for
resources is difficult without means to differentiate the causal mechanisms (e.g.
Juliano 1998). As with disturbance, separating invasions with apparent and
nonexistent or apparent with real competition is difficult because selective predation
still leads to native replacement by exotics.
MANAGEMENT IMPLICATIONS FOR
INTENTIONAL SPECIES INTRODUCTIONS
Biological control has been used historically to combat exotic pests that
humans have difficulty removing. ‘Classic’ biological control, when an exotic
predator is introduced to control an exotic prey, has lead to many harmful
introductions (Howarth 1991, Nechols and Kauffman 1992, Simberloff and Stiling
1996, Mack et al 2000). Examples of biocontrol agents that negatively affect nontargeted native prey are numerous, and detailed elsewhere (e.g. Civeyrel and
Simberloff 1995, Simberloff and Stiling 1996). Hindsight now illustrates that
introducing a generalist predator as biological control for a single pest species can
be extremely dangerous to native biota (Moyle and Light 1996, Simberloff and
Stiling 1996, Mack et al 2000).
This review suggests that the PAR should be considered when evaluating
future biological control introductions. I recommend that biological control agents
should be vigorously tested not only for their predation efficiency on the targeted
pest, but also in the context of the community in which they are to be introduced.
20
In light of the PAR, competitive interactions between the native and the exotic prey
species, as well as selective behavior of the biological control agent, must be
quantified to avoid any potential ecological disaster as a result of biological control
introduction.
FUTURE RESEARCH CONSIDERATIONS
Quantifying the degree to which selective predation accelerates an exotic
species invasion (acceleration rate) may be difficult. Any research program
attempting to quantify an accelerated replacement would first need to find an exotic
that invaded several ecosystems. Each ecosystem would then have to have
substantially different predators or predator densities to determine predation effects
on competing prey species. Ideally, an exotic prey species would simultaneously
invade one system with no predators and another with many predators. The
contrasting ecosystems, and biota therein, could then be studied over time to
monitor predator diets (to test for selectivity), as well as the numerical response of
exotic and native species populations to predation. In addition, the relationship
between exotic and native species must be quantified to define competition effects.
Realistically speaking, this research scenario is unlikely. However, some invasions,
such as the rusty crayfish invasion in northern Wisconsin, do fit most of the above
criteria (Capelli 1982, Olsen et al 1991, Hill et al 1993). Still, more data must be
obtained regarding predator populations in invaded lakes to define the degree to
which predators accelerate rusty crayfish invasions (see Chapter 2). More important
21
than defining the acceleration rate, is to define whether predators are accelerating
the invasion. Knowing whether predators accelerate an invasion or not may be of
more utility than knowing the exact acceleration rate to develop an effective
remediation plan.
I found little literature that explicitly studied complex invasion dynamics
involving selective predation and competition. For instance, several studies
investigating invasive crabs (e.g. green crab (Carcinus maenas), Chinese mitten crab
(Eriocheir sinensis), and blue crab (Callinectes sapidus)) were directed more towards
identifying prey items and range expansions than quantifying trophic structure
changes and community linkages (Carlton 1985, Grozholz and Ruiz 1996, Gerard et
al. 1999), despite evidence that suggests crabs are important predators of bivalves
and other crustaceans (Virnstein 1977, Hall et al 1990, Gerard et al 1999), as well as
prey to fish and birds (West and Williams 1986, Baird and Ulanowicz 1989). I
recommend that future research involving invasion dynamics consider the idea of
the Predator Accelerated Replacement hypothesis.
SUMMARY
I reviewed the interaction of selective predation and competition in invasion
dynamics. I hypothesized that predators facilitate the invasion of exotic species by
selectively removing native species that compete with exotics for finite resources. I
found that the role of predation and competition has received a great deal of
attention in community ecology literature, but is underutilized in describing invasion
22
dynamics. I found in an extensive literature review several examples of invasions
that meet PAR criteria. However, a large majority of the reviewed literature did not
explicitly study complex invasion dynamics involving more than one trophic level.
Using knowledge derived from studies of indirect and direct predation effects, I
described several general patterns of competition regimes interacting with selective
predation that can accelerate native species replacement by invading exotic species.
I then described future research avenues that may help quantify the degree to
which predators aid invasions, but concluded that knowledge of whether predators
are accelerating the invasion or not is more important than describing the
acceleration rate.
CONCLUSION
Scientists cannot truly understand the impact of any exotic without
understanding the community context in which it invades. By quantifying invasions
on a single context, we may be grossly underestimating both individual and
community-level variables influencing the outcome of exotic species introductions.
Understanding the community context in which the exotic invades is an
important prerequisite to development of remediation plans. It is unlikely that a
single foolproof method to control exotic species exists. Nevertheless,
understanding the invasion in the context of communities and ecosystems may
reveal removal methods that do not help remediation efforts, or those that have
unexpected negative consequences.
23
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21
Table 1.1. Locations and biota therein meeting Accelerated Replacement Hypothesis criteria.
This table also includes hypothetical acceleration rates based on a comparison of
competition and predation patterns and apparent strength of predator/prey interactions
(from cited reference
Location
Exotic
Native
Predator
Competitio
n and
Predation
Pattern
Acceleratio
n Rate
References
Coastal
California
Argentine
ants
harvester ants
coastal
horned
lizard
Superior
Predator
Defense
Slow
Suarex et al.
2000, Holway
1998
SE United
States
fire ants
Many
hymenoptera
Many
Lack of fire
ant
predators
Slow
Simberloff and
Stiling 1996,
Moller 1996
N. Wisconsin
lakes
rusty
crayfish
clearwater
crayfish/ virile
crayfish
Fish
Exotic
Competitively
Superior
Medium
Capelli 1982,
Capelli and
Munjal 1982,
Didonato and
Lodge 1993
Great Lakes
Eurasian
ruffe
yellow perch
Fish
Exotic
Competitively
Superior
Medium
Fullerton et al
1998, Ogle et
al 1996
Argentinian
Pampas
Annual
grasses/
broad leafs
Perennial
grasses
Cows,
mostly
Lower
susceptibilty,
disturbance
Medium/Fast
Facelli et al
1988
Australian
savannah
Shrubs,
annual
grasses,
broad leafs
Perennial
grasses
Cows,
sheep,
rabbits
Lower
susceptibilty,
disturbance
Medium/Fast
Leigh et al
1989, Pettit et
al 1995
Many Islands
Birds
Birds
Variety of
non-native
predators
Novel
Predator
Fast
King 1984,
Atkinson 1985,
Simberloff and
Boecklin 1991,
Case 1996
Permanent
ponds,
Chihuahuan
desert
bullfrog
tadpoles
red-legged
frog and other
tadpoles
Coyotes,
raccoons,
adult
bullfrogs
Omnivory,
intensified
competition
Fast
Woodward
1983, Lawler et
al 1999
Permanent
ponds,
Australia
cane toad
tadpoles
native anuran
tadpoles
Dingos,
birds, other
native/
exotic
predators,
adult cane
toads
Omnivory,
superior
predator
defense,
competitively
superior
Extremely
fast
Williamson
1999
Chapter 2
Selective Fish Predation on a
Crayfish Species Assemblage:
Implications for Rusty Crayfish
(Orconectes rusticus) Invasions
23
INTRODUCTION
Biological invasions have received a great deal of attention in current
literature owing to increased rates of species introductions (Carlton 1985, Mills
1993, Mack et al 2000). Exotic species introductions can cause increased
extinction rates and displacements of endemic and rare species, particularly on
islands (e.g. Case 1996). The role of predation, competition, and their
interaction shapes community structure (e.g. Sih 1982, Wilbur 1982, Woodward
1983, Werner 1991, Garvey et al 1994), but often remains unquantified in
shaping invasion dynamics (see Ch. 1).
Rusty crayfish (Orconectes rusticus) were introduced into northern
Wisconsin lakes approximately 30 years ago from the Ohio River Valley, probably
as a bait release (Capelli and Magnuson 1983, Lodge 1985). Rusty crayfish
continue to spread to new lakes in northern Wisconsin through human-mediated
and natural mechanisms despite the 1983 ban on the use of crayfish as bait in
Wisconsin (Lodge 1985). Grazing and predation by the omnivorous rusty
crayfish has a dramatic negative impact, relative to other crayfish, on aquatic
macrophyte and benthic invertebrate communities (Lodge et al. 1985, Lodge and
Lorman 1987, Olsen et al 1991, Lodge et al 1994, Wilson submitted manuscript).
Evidence also indicates that rusty crayfish have a negative impact on important
game fish such as bluegill sunfish (Lepomis macrochirus), pumpkinseed sunfish
(L. gibbosus) and walleye (Stizostedion vitreum) by removing macrophytes and
24
nest depredation (Capelli 1982, Lodge 1985, Wilson submitted manuscript).
Rusty crayfish tends to rapidly replace its congeners Orconectes virilis and
Orconectes propinquus in northern Wisconsin (Capelli 1982, Capelli and Munjal
1982, Lodge 1985, Garvey and Stein 1993). Orconectes propinquus is a previous
invader to the area, but is generally considered ecologically benign despite
displacing O.virilis in many N. Wisconsin lakes (Capelli 1982).
Selective predation by fish on crayfish has been implicated as component
of the species replacement process in N. Wisconsin and other locales (Capelli and
Munjal 1982, Didonato and Lodge 1993, Mather and Stein 1993, Garvey et al
1994). Predators may select preferentially for other Orconectes species due to
unique morphological and behavioral traits of O. rusticus. Rusty crayfish reach
larger adult sizes than O. propinquus, and are more aggressive than O. virilis. In
addition, adult O. rusticus chelae grow larger than either adult O. virilis or O.
propinquus (Capelli and Munjal 1982, Garvey and Stein 1993, Hill et al 1993).
Chelae size is positively correlated with successful inter- and intra-specific
contests for food and shelter (Stein and Magnuson 1976, Capelli and Munjal
1982, Garvey et al 1994). Moreover, chelae size is negatively correlated with
vulnerability to predation (Stein 1977).
Predation (top-down control) has been shown to shape a host of aquatic
and terrestrial communities (Kerfoot and Sih 1987, Pace et al. 1999). In
particular, fishes have been shown to alter aquatic community structure through
selective predation and the subsequent trophic cascades (Brooks and Dodson
25
1965, Carpenter et al. 1985, Moyle and Light 1996). Evidence to date suggests
that fish predation can act as a catalyst in rusty crayfish invasion dynamics in
northern Wisconsin lakes. I hypothesize that fish predators accelerate
replacement by rusty crayfish through selective predation on congeners (e.g.
Wilbur et al 1983), which allows rusty crayfish to rapidly establish population
dominance in newly invaded lakes.
As a test of this hypothesis, I designed a field study to test for predator
selectivity among three competing crayfish species O. rusticus, O. propinquus,
and O. virilis. The goals of this study were to quantify a) the extent selective
predation on a mixed crayfish assemblage as it occurs in nature, and b) which of
several fish species are most selective as predators. In addition, I quantified
rates of crayfish consumption by important crayfish predators.
METHODS
Study Site
I used a preliminary survey of several northern Wisconsin lakes to find a
lake with a mixed crayfish assemblage. I postulated that predators in a lake with
a mixed crayfish assemblage would show the greatest selectivity for native
crayfish, if selection were indeed occurring. I defined ‘mixed species
assemblage’ prior to the survey as any lake that had approximately 50% O.
rusticus and 50% other crayfish species. The survey was based on previous
studies of crayfish distribution in N. Wisconsin (Capelli and Magnuson 1983,
26
Olsen et al. 1991, Lodge and Hill 1994, Tom Hrabik personal communication). To
sample crayfish species assemblage in each lake, I used minnow traps with
enlarged openings and baited with 100 g of beef liver. The crayfish traps were
set for 24 hours at 1-2m depths at twelve equally spaced locations around the
lake.
North Turtle Lake in northwest Vilas County, Wisconsin was found to have
a mixed crayfish species assemblage. The traps contained 199 crayfish that
consisted of 39% O. propinquus, 46% O. rusticus, and 1% O. virilis. Hybrid O.
propinquus/O. rusticus made up 14% of the total catch. No other lake surveyed
(n=9) contained more than 15% O. propinquus or O. virilis (Figure 2.1).
North Turtle Lake is a 149-hectare mesotrophic lake that lies directly north
of S. Turtle Lake (studied by Capelli 1982 and Olsen et al. 1991), and directly
south of Rock Lake. The three lakes are connected via small waterways for small
boats. Cobble is the predominant littoral substrate in N. Turtle, although
macrophytes rooted in muck and sand substrate dominate the northern end.
Cabins and cottages are numerous on both N. and S. Turtle Lakes. Boat access
is possible via launches in the small stream between Rock and N. Turtle Lakes
and at the northern end of S. Turtle Lake. The fish species assemblage in North
Turtle Lake is similar to that in many lakes of the Northern Highlands Lake
District, and contains walleye (Stizostedion vitreum), smallmouth bass
(Micropterus dolomeiui), yellow perch (Perca flavescens), rock bass (Ambloplites
rupestris), northern pike (Esox lucius), muskellunge (E. masquinongy), bluegill
27
(Lepomis macrochirus), pumpkinseed (L. gibbosus), black crappie (Pomoxis
nigromaculatus), plus several species of darters (Etheostoma spp.), minnows
(Cyprinidae), and suckers (Catastomidae).
Diet Collection and Analysis
A six-person field crew collected fish for diet analysis using an electric
boom shocking boat on June 29, July 11, August 17, and August 27 of year
2000. We initially collected bluegill, pumpkinseed, rock bass, smallmouth bass,
yellow perch, and walleye. Preliminary analysis revealed no crayfish in either
bluegill or pumpkinseed diets, and these fishes were excluded from further
collection efforts. I used gastric lavage to collect fish stomach contents
(Hodgson and Kitchell 1987). I flushed stomach contents into a 500μm filter
using a modified SOLO backpack sprayer filled with potable water. I preserved
individual stomach contents in two-ounce scintillation vials filled with 95%
ethanol.
I analyzed diets of individual fish using a dissecting microscope. Prey
categories were separated by family, with the exception of crayfish and fish
which were identified to species when possible. I measured crayfish chelae and
carapace lengths when possible using the protocol found in Hobbs and Jass
(1988). After identification, the stomach content of each fish was dried at 57°C
for 48 hours and weighed to the nearest 0.001 gram.
28
Crayfish Species Composition
Crayfish species composition was determined at six locations in North
Turtle Lake between 15-17 August. A plastic ring that enclosed an area of 3m2
was deployed by SCUBA divers. The ring was anchored with a 30cm wide piece
of bottom-weighted netting attached to the circumference of the ring. The
netting prevented crayfish from escaping the ring during collection. Divers
collected crayfish on top of the substrate as well as those under rocks. Divers
collected as many crayfish from within the ring as possible, but young of year
(YOY) crayfish would occasionally escape capture owing to their small size
(<10mm carapace length). Divers considered the ring empty when they found
no crayfish after 5 minutes of searching.
We identified captured crayfish to species and sex, and measured
carapace length using a stainless steel caliper. I then averaged the abundance
of crayfish over all ring samples to compare against the species abundance in
fish diets.
Total Crayfish Consumption
I estimated crayfish consumption between 29 June and 27 August 2001 using
bioenergetics models (Bioenergetics 3.0, Hanson and Kitchell, 1995). Data used in the
model included crayfish as a percent of diet volume, prey energy density, age-specific
growth (in grams), and lake water temperature. I used Becker (1955) to determine the
average length at age for important crayfish predators among several northern
Wisconsin lakes. I then combined length at age from Becker (1955) with the lengthweight relationship defined from fishes in N. Turtle. This provided an estimate yearly
mass gain for each age class of each fish species. I substituted surface water
29
temperature for N. Turtle Lake with the records for Big Muskellunge Lake, Vilas County,
Wisconsin (LTER, unpublished data), a nearby lake of similar size and depth. I estimated
dry-weight prey energy density from Hanson and Kitchell (1995). Crayfish energy
density came from a wet weight energy density estimate from Roell and Orth (1987)
converted to dry-weight energy density with wet/dry weight regression (R2=0.96) from N.
Turtle Lake (Figure 2.2a). There are no estimates of population density or mortality
rates for fishes in N. Turtle Lake. Therefore, I used the bioenergetics model to estimate
crayfish consumption rates for individual fishes of each age and species.
Crayfish Identification
I identified crayfish in diet samples to species whenever possible using
morphological features I found unique among the three species: coloration, midchelae spine, and areola spacing. However, O. rusticus is known to hybridize
with O. propinquus, confusing some of the key morphological characteristics.
For instance, some crayfish had a ‘rusty spot’ (indicative of rusty crayfish), but
would have an areola or mid-chelae spine representative of O. propinquus.
Based on trap catches, I estimate hybrids compose less than 10% of the total
crayfish population in N. Turtle Lake.
Statistical Analysis
I used Wilcoxon’s signed-rank test to quantify predator selectivity
(Hollander and Wolfe 1973). The application of Wilcoxon’s signed-rank test is
appropriate for diet analysis when few or none of a given prey type are present
in a diet. I used t-tests for all pair-wise comparisons and tested to α=0.05.
30
RESULTS
Diet Composition of Fish Predators
We collected a total of 245 fish for gut content analysis over the four
sample dates. We captured 110 walleye, 42 rock bass, 41 smallmouth bass, and
52 yellow perch. We found prey items in 73% (n=178) of the fish stomachs.
Crayfish made up the majority of diet dry mass for rock bass (79%), smallmouth
bass (89%), and yellow perch (92%). In contrast, walleye were largely
piscivorous (Figure 2.3). Rock bass had the highest frequency of fish with
stomach contents (88%), while yellow perch had the lowest frequency (61%).
Ephemeroptera were the next largest diet group in terms of dry mass after
crayfish or fish across all fish species, but their contribution was relatively small
(Figure 2.3).
Crayfish Species Abundance
The average species composition of ring samples (n=248, excluding
hybrids) was found to be 63% O. propinquus and 37% O. rusticus. No O. virilis
were found in ring samples. The abundance of rusty crayfish in ring samples
decreased modestly in a gradient from south to north sampling stations (Figure
2.4).
31
Crayfish Predation
I found crayfish in 43% of the fish with at least one item in their stomach,
although crayfish consumption differed among fish species. Smallmouth bass
ate 54 crayfish, the most of any species, while walleye ate 15, the fewest,
despite the fact that we collected more than twice as many walleye as
smallmouth bass. Smallmouth bass averaged 1.69 crayfish per individual diet
sample, while walleye averaged only 0.22 crayfish per diet. Rock bass and
yellow perch crayfish consumption was intermediate, averaging 0.69 and 0.65
crayfish/diet, respectively. Fish found with crayfish in their stomach were of
similar size to those without, across all fish species (t=-0.12, -1.04, 1.39, 0.85
for rock bass, smallmouth bass, walleye, and yellow perch, respectively. All pvalues>0.2).
Predator Selectivity
Orconectes propinquus was the most common crayfish identified in fish
diets, comprising 60% of the total identifiable crayfish. Orconectes rusticus was
next most common (22%), followed by O. virilis (18%). One quarter (25%) of
all crayfish in diets were unidentifiable.
Predators exhibited significant negative selection (avoidance, p<0.01) for
rusty crayfish when all diets were included. When analyzed by individual fish
species, rock bass and walleye did not exhibit any selective behavior, while
smallmouth bass and yellow perch significantly avoided rusty crayfish (p-values
32
<0.001). Neither O. propinquus nor O. virilis is significantly selected for or
against when all three species are included in the analysis. Conversely,
predators demonstrated significant positive selection (p<0.01) for O. propinquus
and O. virilis when grouped and compared against O. rusticus (Figure 2.5).
Again, smallmouth bass and yellow perch were selective, while rock bass and
walleye were not. Fish size did not alter selectivity of crayfish. I did not detect
any statistically significant difference in size-specific predation on different
crayfish species across all fish species (all –1<t<1, all p-values >0.3).
The average crayfish present in diets (17.1mm CL +/- 5.62) were similar
sized to the average crayfish in ring surveys (18.1 CL +/- 6.14) (t=1.27, df=324,
p-value>0.2), but the crayfish size-frequency distributions (Figure 2.6a) reveal
that a large proportion of crayfish in diets are around 22-24mm, while the peak
environmental abundance for both O. propinquus and O. rusticus is much
smaller. Orconectes propinquus found in diets were of similar size to those in
ring samples (t=0.65, df=229, p-value>0.2), but O. rusticus in diets were
marginally smaller than those found in the ring samples (t=-0.89, df=93, p-value
<0.2)(Figure 2.6b).
Bioenergetics Model Analysis
Total crayfish consumption for each fish species is displayed in Figure
2.7a. Smallmouth bass consumed the most crayfish biomass per individual fish
in every year class over the analyzed time period. Age 2+ yellow perch ate as
33
many crayfish as rock bass of the same age, but by age 8+ (the last yellow
perch age class analyzed) yellow perch crayfish consumption was equal to that of
walleye. Smallmouth bass consumed significantly more crayfish, averaged
across year classes, than all other species (all t>3.1, all p-values <0.05), while
rock bass consumed significantly less crayfish than all other species (all t<-2.5,
all p-values <0.05). Walleye and yellow perch year classes consumed a similar
amount of crayfish biomass (t=1.2, p-value >0.2). Analysis based on daily
crayfish consumption rates analysis yielded equivalent results (Figure 2.7b).
Yellow perch consumed more crayfish relative to body mass than all other
species (paired t-test, all t>2.5, p-value <0.05 except smallmouth bass t=1.03,
p-value <0.35) (Figure 2.8). Walleye ate significantly less crayfish relative to
body mass than all other species (paired t-tests, all t>2.5, all p-value <0.05).
34
I estimated that walleye (averaged across year classes) consume an
average of 1.15g crayfish/day. This would be the equivalent of one crayfish
approximately 18mm in carapace length (CL) according to carapace
length/weight regression estimates (R2=0.96) (Figure 2.2b), or two 14mm (CL)
crayfish. The average consumption rate for smallmouth was 3.03g/day, the
equivalent of one 23mm (CL) crayfish, or more than five 14mm crayfish (CL).
Yellow perch would consume the equivalent of one 16mm crayfish (CL) per day,
while rock bass would consume one 11mm crayfish (CL) per day.
DISCUSSION
Selective Predation
The aggregate analysis of the predator populations in N. Turtle Lake
revealed significant avoidance of O. rusticus. Smallmouth bass and yellow perch
diet samples contained the majority of crayfish, and both selected against O.
rusticus. Together, smallmouth bass and yellow perch accounted for 64% of the
total crayfish eaten, despite contributing only 36% of all the diets collected.
Rock bass and walleye were more opportunistic crayfish predators. Both
had a higher proportion of fish in their diet than did either smallmouth bass or
yellow perch. In particular, walleye were almost exclusively piscivores, while
rock bass ate more non-crayfish invertebrates than any other species (Figure
2.3).
35
Predators did not exhibit statistically significant selective behavior for O.
propinquus and O. virilis when analyzed individually. However, O. propinquus
and O. virilis were positively selected for when pooled in analysis. This may
seem to be a contradiction but is only an artifact of Wilcoxon’s signed rank test
(discussed later).
Hodgson and Kitchell (1987) suggest that fish predators will be more
specialized when prey are abundant. Therefore, I would expect yellow perch
and smallmouth bass to be the most selective predators based on crayfish
prevalence in their diets. Using optimal foraging theory, Stein (1977) predicted
that smallmouth bass within “a range of sizes” would preferentially prey on
approximately 19mm (CL) crayfish, and supported this idea with experimental
evidence. Several studies have predicted that small crayfish (<16mm CL) are
easiest to prey on (Stein and Magnuson 1976, Stein 1977, Didonato and Lodge
1993, Garvey et al 1993). Subsequently, I would expect that most crayfish
found in diet samples would be <20mm CL. I found that the average crayfish in
diets was roughly of equivalent size to those in ring samples using t-tests.
However, qualitative analysis of the size-frequency distribution from my study
reveals a different story (Figure 2.6a). The peak abundance of crayfish in diets
lies between 22-24mm CL, larger than the predicted optimum size in Stein’s
(1977) analysis. In contrast, the peak abundance of crayfish in the environment
is between 12-14mm CL, and gradually declines thereafter. Costs associated with
crayfish predation are related to handling and search time. Therefore, the size-
36
frequency distribution of crayfish in diets should be a compromise between
crayfish abundance and optimal crayfish size. To an extent, this compromise is
apparent in Figure 2.6a. The size of crayfish in diets declines sharply after
22mm CL, indicating that crayfish larger than about 24mm CL have reached a
size refuge. The size of crayfish predicted by Stein (1977) using optimal foraging
to be preferred (19mm CL) lie between two subtle peaks of environmental
abundance, probably as a result of discreet age classes. Therefore, while the
total number of crayfish found in diets that are <19mm CL outnumber those
>19mm CL, predators may be pushing the optimum size higher than what Stein
(1977) predicted using optimal foraging because of the crayfish deficit around
the 19mm CL mark. Stein (1977) concluded similarly from a field study designed
to test his optimal foraging predictions of smallmouth bass and yellow perch
selectivity for O.propinquus. Further in-depth quantitative analysis of the curves
in Figure 2.6a will be left for another time.
Garvey et al (1993) suggest that largemouth bass (Micropterus salmoides)
between 250 and 275mm are more likely to choose a 21mm CL O. virilis over a
18mm CL O. rusticus, but O. propinquus and O. rusticus of equal size are preyed
upon equally. Although my results confirm that fish prey on similar sizes of O.
propinquus and O. rusticus, I found evidence that O. rusticus in diets are slightly
smaller than those found in the environment, while O. propinquus in diets are of
similar size to those in the environment. This observation can be explained with
relative parsimony by arguing that rusty crayfish reach a larger maximum size
37
than O. propinquus (Hobbs and Jass 1988, Garvey and Stein 1993), thus raising
the size of rusty crayfish found in the environment. Why do fish select O.
propinquus more than O. rusticus? On one hand, J.F. Kitchell and J.J. Magnuson
(personal communication) believe that a fish that is feeding optimally will likely
select O. propinquus considering that there will be more O. propinquus smaller
than the size refuge than O. rusticus, who are able to attain the size refuge more
often (Figure 2.9). My results indicate that few O. propinquus in the environment
were larger than the largest crayfish eaten (28mm CL), but several O. rusticus
were >30mm (Figure 2.6a). In contrast, selectivity based only on size does not
consider behavioral attributes of either species or competitive interactions
between the two species that have been illustrated to be important determinants
of susceptibility (Garvey et al 1994). However, based on previous literature that
demonstrate little relative differences in either defensive or competitive abilities
among O. propinquus and O. rusticus, as well as field data that support size
selectivity, I am prone to support the hypothesis proposed by Kitchell and
Magnuson.
Selectivity Indices
Several indices of electivity are available for diet analysis. Kohler and Ney
(1982) compared Ivlev’s electivity index and Wilcoxon’s signed-rank test, and
found Wilcoxon to produce results more representative of ecological
observations. Chesson (1983) proposed a different way of analyzing prey
38
selectivity, the α score. This method has become popular in recent years.
Chesson’s selectivity index is more effective in determining the selectivity of
predators with a large number of prey items in a given diet (Chesson 1983),
rather than the few prey items I found in each fish’s diet.
One property of Wilcoxon’s signed-rank test is that it requires a given prey
type to either appear or not appear a certain amount of times (depending on the
number of individual diet samples) in the diet to detect positive or negative
selection. Wilcoxon’s signed-rank test cannot detect selection for O. virilis
because it did not appear in enough diets, even though it appears as though O.
virilis was eaten more frequently than its environmental abundance might
suggest. The sample size becomes large enough to detect positive selection only
when I pool O. propinquus and O. virilis as a single prey item. Pooling O.
propinquus and O. virilis in selectivity analysis as a single prey item may not fully
represent the dynamic interactions between as an invader and a native,
respectively. Nonetheless, employing a O. rusticus vs O. propinquus and O.
virilis approach can be justified, considering all three crayfish species share one
niche, and O. rusticus is likely to replace both O. virilis and O. propinquus in N.
Turtle Lake based on evidence from other lakes in the region (e.g. Capelli 1982,
Lodge 1985, Hill et al 1993).
Bioenergetics
Bioenergetics modeling of fish predators reveal individual smallmouth bass
consume the most crayfish of any predator analyzed in N. Turtle Lake. However,
39
yellow perch consume the most crayfish, relative to body weight, than all other
fish species, including smallmouth bass. This evidence suggests that fish
population management attempting to control crayfish population size should
consider conserving smallmouth bass and yellow perch populations.
Using information derived from bioenergetics analysis and size selectivity
data, I argue that predators will consume similar-sized O. propinquus and O.
rusticus in N. Turtle Lake. However, fish will consume smaller O. rusticus than
what is ambient in the environment. Capelli (1975) suggests that larger crayfish
have more reproductive potential than smaller crayfish. How does species and
size selectivity interact with reproductive potential? Although highly relevant,
this question is difficult to answer because crayfish size and fecundity is a
function of age. I cannot determine from my data whether the observed
difference in crayfish size from diets and ring samples is indicative of two
separate age classes. Therefore, the impact of species and size-selective
predation on the reproductive potential of O. propinquus is yet to be determined.
Crayfish Identification
The prevalence of O. virilis in predator diets is high relative to the
abundance found in traps and rings. Traps in N. Turtle caught very few O. virilis,
and ring samples caught none. Although the occurrence of O. virilis in diets is a
possible identification error, it is likely that O. virilis find refuge from the O.
rusticus invasion in macrophytes or areas with mucky substrates. Crayfish traps
40
set in both N. and S. Turtle Lakes revealed O. virilis to be only present in
macrophyte-dominated areas. In addition, most O. virilis collected were females,
indicating that O. virilis still maintains a reproductively viable population in both
lakes.
The abundance of O. propinquus/O. rusticus hybrids confounds simple
interpretation of this study. Hybrids are notoriously hard to identify (W. Perry,
unpublished manuscript. Department of Biological Science, University of Notre
Dame, Notre Dame, IN 46556). However, O. propinquus/O. rusticus hybrids
tend to backcross with O. rusticus, and take on morphological and behavioral
traits more similar to O. rusticus than O. propinquus (W. Perry, unpublished
manuscript). Hybrid identification error would tend to overestimate the
abundance and consumption of O. rusticus, not O. propinquus. In effect, this
strengthens the argument that actively feeding fish avoid O. rusticus.
Implications for Other Lakes
Several lakes in the Capelli (1982) and Olsen et al (1991) survey follow
similar crayfish population trajectories; rusty crayfish tend to rapidly replace
congeners. However, rusty crayfish have taken much longer to become
dominant in some lakes, such as South Turtle, Big, and Trout Lakes (Capelli
1982, Lodge et al 1985, Olsen et al 1991,). This interlake variability in the rusty
crayfish invasion rates has puzzled scientists (Capelli 1982, Lodge et al 1985). I
41
believe that the replacement rate of congeners by rusty crayfish may be
positively related to the abundance of selective crayfish predators.
The pattern observed in the Capelli (1982) and Olsen et al (1991) surveys
may point to some, yet undiscovered crayfish abundance threshold where
predators become aware of the interspecific difference in crayfish vulnerability
(Figure 2.10). Hence, the predator detection threshold (Figure 2.10) and the
acceleration rate should depend on the density of the most selective predators.
Furthermore, according to the results found in this study, the acceleration rate
should positively correlate with the density of smallmouth bass and yellow perch.
The curve in Figure 2.10 also predicts that remnant populations of replaced
species are likely to persist for some time after rusty crayfish become dominant.
This prediction is well supported by field observations that confirm relict
populations of O. propinquus and/or O. virilis persisting for several years
following O. rusticus invasions and subsequent dominance (Capelli 1982, Olsen
et al 1991, Lodge unpublished data, Department of Biological Science, University
of Notre Dame, Notre Dame, IN 46556). Testing the dynamics represented in
Figure 2.10 would require an ideal invasion scenario, which is explained in detail
in Chapter 1.
Management
Managing the predator population to reverse a rusty crayfish invasion
would be difficult because no fish species select rusty crayfish. Possibly an
42
invasion can be slowed by managing a lake for a walleye and/or rock bass
dominated fish population. Inevitably, rusty crayfish would still come to
dominate through competitive exclusion or sexual interference of congeneric
crayfish, albeit on a longer time scale. Initiating a catch-and-release fishery on
smallmouth bass, rock bass and yellow perch population could perhaps lower O.
rusticus populations, and thereby reduce negative effects. Rabeni (1992)
estimated that rock bass and smallmouth bass consumed approximately 33% of
the crayfish biomass per year in two Missouri streams. In addition, yellow perch
have been previously shown to be voracious crayfish predators (Stein 1977,
Rettig and Garvey unpublished manuscript, Aquatic Ecology Laboratory,
Department of Zoology, The Ohio State University, Columbus, OH 43212).
Therefore, managing a gamefish population to control a rusty crayfish population
may have some merit.
SUMMARY AND CONCLUSION
I provide empirical evidence to support the hypothesis that fish avoid
eating rusty crayfish. Gowing and Momot (1979) equate fish predation on
crayfish to just another form of natural mortality, and claim that crayfish eaten
by fish would perish for other reasons anyway. This statement downplays fish
predators’ ability to effect crayfish population structure. Rabeni (1992) found
rock bass and smallmouth bass to be rapacious crayfish predators, capable of
consuming a substantial proportion of crayfish production. Conversely, following
43
the hypothesis posed by Kitchell and Magnuson, if we envision a crayfish species
assemblage (just O. propinquus and O. rusticus for simplicity) as the only
components of the crayfish population, then selective predation will cause
greater mortality on O. propinquus (Figure 2.11). This allows O. rusticus greater
survivorship in three ways. First, O. rusticus that are larger than the largest O.
propinquus (>40mm CL) (Hobbs and Jass 1988) are able to secure shelters at all
O. propinquus' expense (Capelli and Munjal 1982, Garvey and Stein 1994). If
shelter is a limiting resource, securing shelter at the expense of other crayfish
not only protects O. rusticus from predation, but makes other crayfish more
vulnerable (Stein 1977, Capelli and Munjal 1982, Garvey and Stein 1994).
Second, since O. rusticus reach a larger adult size than O. propinquus, the
proportion of O. propinquus population vulnerable to predation is larger than O.
rusticus. Thirdly, predators become satiated on O. propinquus, reducing the
chance that fish will be motivated by hunger to feed on a more challenging prey
item (O. rusticus) (Werner 1974, Werner and Hall 1974). These combine to yield
unbalanced mortality rates among crayfish species that may accelerate the
replacement of congeners by rusty crayfish. Managing a fish population to be
dominated by walleye and rock bass to slow a rusty crayfish invasion is plausible,
but it may only delay the inevitability of rusty crayfish dominance. As a result, I
recommend managing the fish population to help reduce the rusty crayfish
population, and hopefully thereby reduce their impact on lake biota.
44
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Capelli, G. M. and B. L. Munjal. 1982. Aggressive interactions and resource
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Capelli, G. M. and J. J. Magnuson. 1983. Morphoedaphic and biogeographic
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Carlton, J.T. 1985. Transoceanic and interoceanic dispersal of coastal marine
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Case, T.J. 1996. global patterns in the establishment and distribution of exotic
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DiDonato, G. T. and D. M. Lodge. 1993. Species replacements among Orconectes
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Can.J.Fish.Aquat.Sci. 50:1484-1488.
Garvey, J. E., R. A. Stein, and H.M. Thomas. 1994. Assessing how fish predation
and interspecific prey competition influence a crayfish assemblage.
Ecology 75:532-547.
Garvey, J. E. and R. A. Stein. 1993. Evaluating how chela size influences the
invasion potential of an introduced crayfish (Orconectes rusticus).
Am.Midl.Nat. 129:172-181.
Gowing, H. and W. T. Momot. 1979. Impact of brook trout (Salvelinus fontinalis)
predation on the crayfish Orconectes virilis in three Michigan lakes.
J.Res.Board Can. 36:1191-1196.
Hart, D.R. and R.H. Gardner. 1997. A spatial model for the spread of invading
organisms subject to competition. J.Math.Biol. 35:935-948.
Hastings, A. 1996. Models of spatial spread: A synthesis. Biological Conservation
78: 143-148.
Hill, A. M., D.M. Sinars, and D.M. Lodge. 1993. Invasion of an occupied niche by
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the crayfish Orconectes rusticus: potential importance of growth and
mortality. Oecologia 94:303-306.
Hill, A. M. and D. M. Lodge 1995. Multi-trophic level impact of sublethal
interactions between bass and omnivorous crayfish. J.N.Am.Benthol.Soc.
14:306-314.
Hobbs, H.H. III. And J.P. Jass. 1988. The crayfishes and shrimp of Wisconsin.
Wisconsin Public Museum, USA. 177pp.
Hollander, M. and D.A. Wolfe. 1973. Nonparametric Statistical Methods. John
Wiley & Sons. USA. 503pp.
Keast,. 1977. Diet overlaps and feeding relationships between the year classes in
the yellow perch (Perca flavescens). Environmental Biology of Fishes
2:53-70.
Keller, T. A. a. P. A. Mather. 2000. Context-specific behavior: crayfish size
influences crayfish-fish interactions. J.N.Am.Benthol.Soc. 19:344-351.
Kohler, C.C. and J.J. Ney. 1982. A comparison of methods for quantitative
analysis of feeding selection of fishes. Environmental Biology of Fishes
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Lodge, D. M., A.L. Beckel, and J.J. Magnuson. 1985. Lake-Bottom Tyrant. Natural
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Lodge, D. M., M.W. Kershner, J.E. Aloi, and A.P. Covich. 1994a. Effects of an
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Lodge, D. M., T.K. Kratz and G.M. Capelli. 1986. Long-term dynamics of three
crayfish species in Trout Lake, Wisconsin. Can.J.Fish.Aquat.Sci. 43:993998.
Lodge, D. M. and A. M. Hill 1994. Factors governing species composition,
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Nordic.J.Freshw.Res. 69:111-136.
Lodge, D. M.and J. G. Lorman 1987. Reductions in sumversed macrophyte
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Can.J.Fish.Aquat.Sci. 44:591-597.
Lorman. 1975. MS Thesis. University of Wisconsin-Madison
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Mather, M. E., and R.E. Stein. 1993. Direct and indirect effects of fish predation
on the replacement of a native crayfish by an invading congener.
Can.J.Fish.Aquat.Sci. 50:1279-1288.
Mills, E.L., J.H. Leach, J.T. Carlton, and C.L. Secor. 1993. Exotic species in the
Great Lakes: A history of biotic crises and anthropogenic introductions.
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Momot, W. T. and H. Gowing. 1977. Response of the crayfish Orconectes virilis
to exploitation. Can.J.Fish.Aquat.Sci. 34:1212-1219.
Moyle, P.B. and T. Light. 1996. Biological invasions of fresh water: empirical rules
and assembly theory. Biological Conservation 78(1996): 149-161.
Olsen, T. M., D.M. Lodge, G.M. Capelli, and R.J. Houlihan. 1991. Mechanisms of
impact of an introduced crayfish (Orconectes rusticus) on littoral
congeners, snails, and macrophytes. Can.J.Fish.Aquat.Sci. 48:1853-1861.
Pace, M.L., J.L. Cole, S.R. Carpenter, and J.F. Kitchell. 1999. Trophic cascades
revealed in diverse ecosystems. TREE 14(12): 483-488.
Probst, W. E., C.F. Rabeni, W.G. Covington, and R.E. Marteney. 1984. Resource
use by stream-dwelling rock bass and smallmouth bass.
Trans.Am.Fish.Soc. 113:283-294.
Rabeni, C.M. 1992. Trophic linkage between stream centrarchids and their
crayfish prey. Can.J.Fish.Aquat.Sci. 49:1714-1721.
Roell, M. J. and D. J. Orth. 1993. Trophic basis of production of stream-dwelling
smallmouth bass, rock bass, and flathead catfish in relation to
invertebrate bait harvest. Trans.Am.Fish.Soc. 122:46-62.
Sih, A. 1982. Foraging strategies and the avoidance of predation by an aquatic
insect predator, Notonecta hoffmani. Ecology 63: 786-796.
Stein, R. A. 1977. Selective predation, optimal foraging, and the predator-prey
interaction between fish and crayfish. Ecology 58:1237-1253.
Stein, R. A. and J. J. Magnuson. 1976. Behavioral response of crayfish to a fish
predator. Ecology 57:751-761.
Werner, E.E. 1974. The fish size, prey size, handling time relation in several
sunfishes and some implications. J.Fish.Res.Board Can. 31: 1531-1536
47
Werner, E.E. and D.J. Hall. 1974. Optimal foraging and the size selection of prey
by the bluegill sunfish (Lepomis macrochirus). Ecology 55: 1042-1052.
Wilbur, H.M., P.J. Morin, and R.N. Harris. 1993. Salamander predation and the
structure of experimental communities: Anuran responses. Ecology
64(6): 1423-1429.
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perch and smallmouth bass in Nebish Lake, Wisconsin. Technical Bulletin
14.
48
FIGURE CAPTIONS
Figure 2.1. Crayfish species collected in traps from 8 lakes in northern
Wisconsin. We found no crayfish in one lake surveyed, Round Lake, which was
excluded from this graph.
Figure 2.2. A). Crayfish wet weight/dry weight regression with equation and R2.
The regression pools both O. propinquus and O. rusticus because no difference
in dry weight could be detected among different crayfish species of similar wet
weights. B). Carapace length/Weight regression for crayfish in N. Turtle Lake.
Again, both O. propinquus and O. rusticus were pooled because no difference in
wet weight could be detected among different crayfish species of similar lengths.
Figure 2.3. Cumulative diet proportions of crayfish predators in North Turtle
Lake, over four sample dates between June 29 and August 27. The ‘ Other
Arthropods’ prey group consists primarily of Cladocera, Diptera, Odonata, and
Coleoptera.
Figure 2.4. Species composition in North Turtle Lake ring survey. Note the
abundance of rusty crayfish decreases in a northerly direction, away from S.
Turtle Lake.
Figure 2.5. Selectivity of crayfish predators towards rusty crayfish versus pooled
O. propinquus and O. virilis samples based on Wilcoxon’s signed-rank test,
α=0.05. Asterisks within columns indicate significant selection. Plus signs mean
positive selection, minus signs mean negative selection. The environmental
abundance of rusty crayfish and congeners is represented by “Environment”
category in far right.
Figure 2.6a. Size frequency distribution of O. propinquus and O. rusticus in ring samples,
and all crayfish in diets. O. propinquus frequencies are halved for graphing convenience.
Figure 2.6b. Comparison of crayfish sizes found in ring and diet samples by sampling
method. Error bars denote one standard deviation.
Figure 2.7. Crayfish consumption per individual per age class between 29 June and 27
August 2000 (a.) and average daily consumption (b.). Error bars in Figure 2.6b indicate
the standard deviation of daily crayfish consumption between 29 June and 27 August
2000. Note the log scale in Figure 2.6a.
Figure 2.8. Total crayfish consumption relative to fish body mass for each fish
age class between 29 June and 27 August 2000.
49
Figure 2.9. Handling and pursuit costs divided by nutritional benefit vs. crayfish size,
following from Stein (1977). The largest O. propinquus and O. rusticus are well within a
size refuge from fish predation, where handling costs far outweigh any potential
nutritional gain. The smallest crayfish are edible, but their secretive nature and small
nutritional value cause pursuit costs to rise, and benefits to fall.
Figure 2.10. Hypothetical predator accelerated replacement scenario over time.
Predators accelerate species replacement (dashed line) above the rate
competitive exclusion (solid line) would dictate if no predator were present.
Figure 2.11. How selective predation aids rusty crayfish population through
competitor removal. Selective predation increases O. propinquus mortality when
O. rusticus invades above what is expected in the single species situation,
simultaneously increasing O. rusticus survivorship.
50
Percent of Total Catch
100%
80%
Virilis
Rusticus
Propinquus
60%
40%
20%
ce
Ri
i ld
W
e
hit
W
Va
n
Vl
Sa
nd
iet
g
lin
rk
e
S.
Tu
rtl
Sp
a
e
rtl
Tu
N.
Lil
y
rc
le
Ci
Ar
ro
wh
ea
d
0%
Figure 2.1. Crayfish species (excluding hybrids) collected in traps from 8 lakes in
northern Wisconsin. We found no crayfish in one lake surveyed, Round Lake, which was
excluded from this graph.
51
Log Wet Weight (g)
a.
y = 0.9746x + 0.568
R2 = 0.9576
1.4
1.2
1
0.8
0.6
0.4
0.2
0
-0.2
-0.4
-0.6
-1.5
-1
-0.5
0
0.5
1
Log Dry Weight (g)
0.187x
y = 0.0411e
2
R = 0.9725
b.
Wet Weight (g)
10
1
0.1
0
5
10
15
20
25
30
35
Carapace Length (mm)
Figure 2.2. A). Crayfish wet weight/dry weight regression with equation and R2. The
regression pools both O. propinquus and O. rusticus because no difference in dry weight
could be detected among different crayfish species of similar wet weights.
B). Carapace length/Weight regression for crayfish in N. Turtle Lake. Not the
logarithmic y-axis. Again, both O. propinquus and O. rusticus were pooled because no
difference in wet weight could be detected among different crayfish species of similar
lengths.
52
Crayfish
Fish
Ephemeroptera
Other Arthropods
Proportion of Total Diet Dry Mass
100%
75%
50%
25%
0%
rock bass
smallmouth
bass
yellow perch
walleye
Total
Fish Species
Figure 2.3. Cumulative diet proportions of crayfish predators in North Turtle Lake, over four
sample dates between June 29 and August 27. The ‘ Other Arthropods’ prey group consists
primarily of Cladocera, Diptera, Odonata, and Coleoptera.
53
N
67% propinquus
33% rusticus
85% propinquus
15% rusticus
69% propinquus
31% rusticus
68% propinquus
32% rusticus
61% propinquus
39% rusticus
62% propinquus
38% rusticus
46% propinquus
54% rusticus
200 m
S. Turtle Lake
Figure 2.4. Species composition in North Turtle Lake ring survey. Note the abundance of
rusty crayfish decreases in a northerly direction, away from S. Turtle Lake.
54
Other
O. rusticus
1.2
*
(-)
1
*
(-)
*
(+)
Proportion
0.8
*
(+)
*
(+)
0.6
*
(-)
0.4
0.2
0
rock bass
smallmouth
bass
walleye
yellow perch
Population
Species Group
Figure 2.5. Selectivity of crayfish predators towards rusty crayfish versus pooled O.
propinquus and O. virilis samples based on Wilcoxon’s signed-rank test, α=0.05. Asterisks
within columns indicate significant selection. Plus signs mean positive selection, minus signs
mean negative selection. The environmental abundance of rusty crayfish and congeners is
represented by “Environment” category in far right.
55
a.
rust
prop
diets
20
18
16
Frequency
14
12
10
8
6
4
2
0
0
10
20
30
40
50
Crayfish Length (mm)
30
Carapace Length (mm)
b.
25
20
diets
ring
15
10
5
propinquus
rusticus
Crayfish Species
Figure 2.6a. Size frequency distribution of O. propinquus and O. rusticus in ring samples, and all crayfish in diets. O. propinquus
frequencies are halved for graphing convenience.
56
Figure 2.6b. Comparison of crayfish sizes found in ring and diet samples by sampling
method. Error bars denote one standard deviation.
Total Annual Crayfish Consumption (g)
per Individual Fish
a.
rock bass
walleye
smallmouth bass
yellow perch
1000
100
10
1
0
1
2
3
4
5
6
7
8
9
10
9
10
Estimated Fish Age
rock bass
walleye
b.
smallmouth bass
yellow perch
6
Consumption Rate
-1
(g crayfish day )
5
4
3
2
1
0
0
1
2
3
4
5
6
Estimated Fish Age
7
8
57
Figure 2.7. Crayfish consumption per individual per age class between 29 June and 27
August 2000 (a.) and average daily consumption (b.). Error bars in Figure 2.6b indicate the
standard deviation of daily crayfish consumption between 29 June and 27 August 2000.
Note the log scale in Figure 2.6a.
58
Annual Crayfish Consumption (g)/g Fish
rock bass
walleye
smallmouth bass
yellowperch
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
0
1
2
3
4
5
6
7
Estimated Fish Age
8
9
10
Figure 2.8. Total crayfish consumption relative to fish body mass for each fish age class
between 29 June and 27 August 2000.
59
Size Refuge
Cost
Optimal
Crayfish Size
Largest
propinquus
Largest
rusticus
Crayfish Length
Figure 2.9. Handling and pursuit costs divided by nutritional benefit vs. crayfish size,
following from Stein (1977). The largest O. propinquus and O. rusticus are well within a size
refuge from fish predation, where handling costs far outweigh any potential nutritional gain.
The smallest crayfish are edible, but their secretive nature and small nutritional value cause
pursuit costs to rise, and benefits to fall.
60
.
Stage 1
Stage 2
Stage 3
1
Relic native
population
Proportion of
Exotic
Species
Consumer “switch”
Competitiv
e Exclusion
0
Time since invasion
Figure 2.10. Hypothetical predator accelerated replacement scenario over time. Predators accelerate species replacement (dashed line)
above the rate competitive exclusion (solid line) would dictate if no predator were present.
61
Crayfish Surviving
Single-species Situation
Natural Crayfish
Mortality
(Including predation)
O. propinquus
Some additional
mortality due to
selective predation
O. propinquus
Rusticus Invades
Some additional
survivorship due to
predator avoidance
O. rusticus
Figure 2.11. How selective predation aids rusty crayfish population through competitor
removal. Selective predation increases O. propinquus mortality when O. rusticus
invades above what is expected in the single species situation, simultaneously increasing
O. rusticus survivorship.