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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 5 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. 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Biol. 52: 137-154. Reusch, T.B.H. 1998. Native predators contribute to invasion resistance to the non-indigenous bivalve Musculista senhousia in southern California, USA. Mar.Ecol.Prog.Ser. 170:159-168. 27 Ricciardi, A. a. J. B. Rasmussen. 1998. Predicting the identity and impact of future biological invaders: a priority for aquatic resource management. Can.J.Fish.Aquat.Sci. 55:1759-1765. Schoener, T.W. 1971. Theory of feeding strategies. Annu. Rev. Ecol. Syst. 2: 369404. Sih, A. 1982. Foraging strategies and the avoidance of predation by an aquatic insect, Notonecta hoffmanni. Ecology 63(3):786-796. Sih, A. 1984. Optimal behavior and density-dependent predation. The American Naturalist 123(3): 314-326. Simberloff, D. and W. Boecklin. 1991. Patterns of extinction in the introduced Hawaiian avifauna: a reexamination of the role of competition. American Naturalist 138:300-327. Simberloff, D. and P. Stiling. 1996. Risks of species introduced for biological control. Biological Conservation 78:185-192. Stein, R. A. 1977. Selective predation, optimal foraging, and the predator-prey interaction between fish and crayfish. Ecology 58:1237-1253. Strong, D.R. 1992. All trophic cascades all wet? The redundant differentiation in trophic architecture of high diversity ecosystems. Ecology 73:747-754. Suarez, A.V., J.Q. Richmond, and T.J. Case. 2000. Prey selection in horned lizards following the invasion of Argentine ants in southern California. Ecological Applications 10(3):711-725. Vermeij, G.J. 1996. An agenda for invasion biology. Biological Conservation 78:3-9. Virnstein, R.W. 1977. The importance of predation by crabs and fishes on benthic infauna in Chesapeake Bay. Ecology 58:1199-1217. Ware, D.M. 1971. Predation by rainbow trout (Salmo gairdneri): The effect of experience. J.Fish.Res.Bd.Canada 28:1847-1852. 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. 28 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. Werner, E.E., G.G. Mittelbach, and D.J. Hall. 1981. The role of foraging profitability and experience in habitat use by the bluegill sunfish. Ecology 62(1): 116-125. Werner, E.E. 1991. Nonlethal effects of a predator on competitive interactions between two anuran larvae. Ecology 72(5):1709-1720. West, D.L. and H. Williams. 1986. Predation by Callinectes spidus (Rathbun) within Spartina alterniflora (Loisel) marshes. J.Exp.Mar.Biol.Ecol. 100:75-95. Wilbur, H.M. 1982. Competition between tadpoles of Hyla femoralis and Hyla gratiosa in laboratory experiments. Ecology 63(2): 278-282. Wilbur, H.M., P.J. Morin, and R.N. Harris. 1983. Salamander predation and the structure of experimental communities: Anuran responses. Ecology 64(6):1423-1429. Williamson, I. 1999. Competition between the larvae of the introduced cane toad Bufo marinus (Anura: Bufonidae) and native anurans from the Darling Downs area of southern Queensland. Australian Journal of Ecology 24:363643. Woodward, B.D. 1983. Predator-prey interactions and breeding-pong use of temporary-pond species in a desert anuran community. Ecology 64(6):1549-1555. 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 REFERENCES Capelli, G. M. 1982. Displacement of northern Wisconsin crayfish by Orconectes rusticus (Girard). Limnology and Oceanography 27:741-745. Capelli, G. M. and B. L. Munjal. 1982. Aggressive interactions and resource competition in relation to species displacement among crayfish of the genus Orconectes. Journal of Crustacean Biology 2:486-492. Capelli, G. M. and J. J. Magnuson. 1983. Morphoedaphic and biogeographic analysis ofcrayfish distribution in northern Wisconsin. Journal of Crustacean Biology 3:548-564. Carlton, J.T. 1985. Transoceanic and interoceanic dispersal of coastal marine organisms: The biology of ballast water. Oceanogr.Mar.Biol.Ann.Rev. 23:313-371. Case, T.J. 1996. global patterns in the establishment and distribution of exotic birds. Biological Conservation 78: 69-96. DiDonato, G. T. and D. M. Lodge. 1993. Species replacements among Orconectes crayfishes in Wisconsin lakes: the role of predation by fish. 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 45 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 7(4):363-368. Lodge, D. M., A.L. Beckel, and J.J. Magnuson. 1985. Lake-Bottom Tyrant. Natural History 1985:33-37. Lodge, D. M., M.W. Kershner, J.E. Aloi, and A.P. Covich. 1994a. Effects of an omnivorous crayfish (Orconectes rusticus) on a freshwater littoral food web. Ecology 75:1265-1281. 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, population size, and productivity of cool-water crayfishes. Nordic.J.Freshw.Res. 69:111-136. Lodge, D. M.and J. G. Lorman 1987. Reductions in sumversed macrophyte biomass and species richness by the crayfish Orconectes rusticus. Can.J.Fish.Aquat.Sci. 44:591-597. Lorman. 1975. MS Thesis. University of Wisconsin-Madison 46 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. Journal of Great Lakes Research 19(1):1-54. 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. Wisconsin Department of Natural Resources. 1984. Food habits of adult yellow 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.