Is There Such Thing as a Parasite Free Lunch? The Direct and Indirect Consequences of Eating Invasive Prey Grégory Bulté, Stacey A. Robinson, Mark R. Forbes & David. J. Marcogliese EcoHealth Conservation Medicine: Human Health:Ecosystem Sustainability Official journal of International Association for Ecology and Health ISSN 1612-9202 Volume 9 Number 1 EcoHealth (2012) 9:6-16 DOI 10.1007/s10393-012-0757-7 1 23 Your article is protected by copyright and all rights are held exclusively by International Association for Ecology and Health. This eoffprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your work, please use the accepted author’s version for posting to your own website or your institution’s repository. You may further deposit the accepted author’s version on a funder’s repository at a funder’s request, provided it is not made publicly available until 12 months after publication. 1 23 Author's personal copy EcoHealth 9, 6–16, 2012 DOI: 10.1007/s10393-012-0757-7 Ó 2012 International Association for Ecology and Health Forum Is There Such Thing as a Parasite Free Lunch? The Direct and Indirect Consequences of Eating Invasive Prey Grégory Bulté,1 Stacey A. Robinson,1 Mark R. Forbes,1 and David. J. Marcogliese2 1 Department of Biology, Carleton University, 1125 Colonel By, Ottawa, ON K1S 5B6, Canada; robinson.stacey@gmail.com Fluvial Ecosystem Research Section, Aquatic Ecosystem Protection Research Division, Water Science and Technology Directorate, Science and Technology Branch, St. Lawrence Centre, Environment Canada, 105 Rue McGill, 7th Floor, Montreal, QC H2Y 2E7, Canada 2 Abstract: As the number of invasive species increases globally, more and more native predators are reported to shift their diet toward invasive prey. The consequences of such diet shifts for the health of populations of native predators are poorly studied, but diet shifts are expected to have important parasitological and immunological consequences, ultimately affecting predator fitness. We reviewed evidence that diet shifts from native to invasive prey can alter parasite exposure directly and also indirectly affect immune functions via changes in condition and contaminant exposure. We highlight relevant conceptual and methodological tools that should be used for the design of experiments aimed at exploring important links between invasive prey and parasitism, contaminants and fitness of their native predators. Keywords: contaminants, ecoimmunology, ecotoxicology, parasitology, predator–prey relationships, trophic transfer INTRODUCTION By regulating prey abundance, predators can have a profound impact on the structure of populations, communities, and ecosystems (Estes and Palmisano 1974; Ripple and Beschta 2005) and may even influence the emergence of zoonotic diseases (Ostfeld and Holt 2004). Understanding the factors influencing the population of predators is thus essential for the management of wildlife and ecosystems (Estes 1996). One inevitable consequence of biological invasions is the alteration of predator–prey interactions. Hyper-successful non-indigenous species (hereafter referred to as invasive species) are a ubiquitous component of the diet of native predators (e.g., King et al. 2006; Johnson et al. Published online: March 27, 2012 Correspondence to: Grégory Bulté, e-mail: Gregory_Bulte@carleton.ca 2010a, b; Madenjian et al. 2011) and it is clear that native predators can rapidly shift their diet to feed on invasive prey (Carlsson et al. 2009). Despite the growing tendency of native predators to forage on invasive species, the population response of native predators to changes in prey base remains largely unknown (Carlsson et al. 2009). There is indirect evidence that diet shifts from native to invasive prey influence the fitness of native predators (reviewed by Carlsson et al. 2009). Changes in fitness-related variables such as condition and growth have been reported in predators following a diet shift from native to invasive prey (e.g., Pothoven et al. 2001; King et al. 2006; Table 1). However, the mechanisms responsible for these changes are not well understood. Moreover, it is largely unknown how changes in fitness (or fitness-related traits) are influencing the populations of native predators (Table 1). For example, Author's personal copy Effects of Invasive Prey on Parasitism 7 Table 1. Summary Field Studies Investigating the Response of Native Predator Feeding on Two Widespread Aquatic Invaders in North America: The Round Goby and the Zebra Mussel Invasive prey Predator Response variable (direction of the effect) Source Round goby Fish Fish Reptile Reptile Bird Bird Fish Fish Fish Fish Fish Reptile Thiamine status (;) Individual growth rate (:) Concentration of organochlorine in tissue Individual growth rate and body size (:) Population density (:) Concentration of organochlorine in tissue Concentration of organochlorine in tissue Individual growth rate (:/;) Body condition (;) Concentration of organochlorine in tissue Individual growth rate (:) Clutch size (=) Fitzsimons et al. (2009) Steinhart et al. (2004) Fernie et al. (2008) King et al. (2006) Petrie and Knapton (1999) Mazak et al. (1997) Andraso (2005) French and Bur (1996) Pothoven et al. (2001) Mercer et al. (1999) Mercer et al. (1999) Bulté and Blouin-Demers (2008) Zebra mussel the zebra mussel (Dreissena polymorpha) and the round goby (Neogobius melanostomus) are two of the most problematic freshwater invaders in North America. We reviewed studies documenting predation on these invasive species (see Table 2 for list of references). We searched for studies in ISI web of science using different combinations of the name (common and scientific) of both prey species and the words ‘‘predator’’ and ‘‘predation.’’ We documented the type of predators and whether the study measured changes in predators in terms of individual variables, population variable, contaminant burden, and parasitism. We found 30 studies documenting predation on either zebra mussels or round goby by 35 species of native predators including invertebrates, fishes, birds, reptiles, and mammals. Of the 30 studies, 18 (60%) focused only on predation and 12 included some other measures of interest in the predator (see Table 1). Seven studies (24%) looked at changes in individual metrics (e.g., growth, condition, fecundity, nutrition), four (14%) looked at contaminants, and one (3.5%) looked at predator’s population response. No studies examined parasitism. The fitness response of native predators to invasive prey will be mediated by multiple factors. Integrative research is necessary to shed light on the mechanisms at play and on their subsequent impact on predator populations. We argue here that changes in the fitness of native predators following a diet shift to more invasive prey can be mediated by changes in parasitism caused by direct and indirect mechanisms. Parasites are considered one of the strongest known selective pressures in nature (Schulenburg et al. 2009). Hosts rely in great part on their immune system to counter (=) (:) (=) (;) the detrimental effects of parasites. However, mounting an immune response can be costly energetically. The amount of resources allocated to reduce and eliminate an infection (hereafter referred to as immune functions) is thought to represent a balance between the costs and the benefits of allocating energy to these functions versus to other biological processes (Sheldon and Verhulst 1996; Schulenburg et al. 2009). Any changes in exposure to parasites, or in factors modulating immune functions, are expected to influence the impact of parasites on their hosts (Sheldon and Verhulst 1996; Schulenburg et al. 2009). We reviewed evidence that diet shifts from native to invasive prey hold huge potential to alter both exposure to parasites and the ability of hosts to resist parasitic infections. Our goal is to address a growing need for research specifically aimed at understanding the immunological, parasitological, and toxicological consequences of diet shifts from native to invasive prey. We first describe how diet shift can affect both parasitism and immune functions. Some links between diet and parasitism or immune functions may appear obvious at first glance. Yet, these links are largely neglected (see Table 1) and should be examined critically. We then propose directions for future research. Aquatic ecosystems have arguably been the most severely impacted by invasive species and thus many of our examples involve aquatic species; however, we stress the concepts presented here are relevant to other ecosystems. In this article, we focus our discussion on macroparasites whose life cycles depend on predator–prey interactions within food webs. It should be noted that other type of pathogens including viral diseases might infect native predators by their preying Author's personal copy 8 Grégory Bulté et al. Table 2. Field Studies Documenting Predation on Invasive Zebra Mussel (Dreissena polymorpha) and Round Goby (Neogobius melanostomus) in North America Prey Predator Source Round goby Brown bullhead (Ameiurus nebulosus) Burbot (Lotta lotta) Burbot (Lotta lotta) Channel catfish (Ictalurus punctatus) Lake Trout (Salvelinus namaycush) Lake Trout (Salvelinus namaycush) Lake Trout (Salvelinus namaycush) Northern pike (Essox lucius) Sauger (Sander canadensis) Smallmouth bass (Micropterus dolomieu) Smallmouth bass (Micropterus dolomieu) Walleye (Sander vitreus) Walleye (Sander vitreus) Yellow perch (Perca flavescens) Yellow perch (Perca flavescens) Lake Erie watersnake (Nerodia sipedon insularum) Lake Erie watersnake (Nerodia sipedon insularum) Double crested cormorant (Phalacrocorax auritas) Double crested cormorant (Phalacrocorax auritas) Red-breasted merganzer (Mergus serrator) Blue crab (Callinectes sapidus) Blue catfish (Ictalurus furcatus) Blue catfish (Ictalurus furcatus) Bluegill (Lepomis macrochirus) Bluegill (Lepomis macrochirus) Bluegill (Lepomis macrochirus) Bufflehead (Bucephala albeola) Common carp (Cyprinus carpio) Common carp (Cyprinus carpio) Flathead catfish (Pylodictis olivaris) Freshwater drum (Aplodinotus grunniens) Freshwater drum (Aplodinotus grunniens) Freshwater drum (Aplodinotus grunniens) Freshwater drum (Aplodinotus grunniens) Freshwater drum (Aplodinotus grunniens) Lake whitefish (Coregonus clupeaformis) Pumpkinseed (Lepomis gibbosus) Pumpkinseed (Lepomis gibbosus) Pumpkinseed (Lepomis gibbosus) Quillback carpsucker (Carpiodes cyprinus) Redear sunfish (Lepomis microlophus) Redhorse suckers (Moxostoma spp.) Rock bass (Ambloplites rupestris) Yellow perch (Perca flavescens) Yellow perch (Perca flavescens) Yellow perch (Perca flavescens) Reyjol et al. (2010) Madenjian et al. (2011) Jacobs et al. (2010) Reyjol et al. (2010) Dietrich et al. (2006) Fitzsimons et al. (2009) Jacobs et al. (2010) Reyjol et al. (2010) Reyjol et al. (2010) Reyjol et al. (2010) Steinhart et al. (2004) Reyjol et al. (2010) Bur et al. (2008) Reyjol et al. (2010) Truemper and Lauer (2005) King et al. (2006) Fernie et al. (2008) Johnson et al. (2010) Somers et al. (2003) Bur et al. (2008) Boles and Lipcius (1997) Herod et al. (1997) Magoulick and Lewis (2002) Andraso (2005) Bartsch et al. (2005) Mercer et al. (1999) Mazak et al. (1997) Tucker et al. (1996) Bartsch et al. (2005) Bartsch et al. (2005) French and Bur (1996) Magoulick and Lewis (2002) Bartsch et al. (2005) Watzin et al. (2008) Morrison et al. (1997) Pothoven et al. (2001) Andraso (2005) Watzin et al. (2008) Mercer et al. (1999) Bartsch et al. (2005) Magoulick and Lewis (2002) Bartsch et al. (2005) Watzin et al. (2008) Watzin et al. (2008) Morrison et al. (1997) Mercer et al. (1999) Zebra mussel Author's personal copy Effects of Invasive Prey on Parasitism 9 Table 2. continued Prey Predator Source Musk turtle (Sternotherus odoratus) Northern map turtle (Graptemys geographica) Northern map turtle (Graptemys geographica) Bufflehead (Bucephala albeola) Bufflehead (Bucephala albeola) Canvasback (Aythya valisneria) Greater Scaup (Aythya marila) Greater Scaup (Aythya marila) Greater Scaup (Aythya marila) Lesser Scaup (Aythya affinis) Lesser Scaup (Aythya affinis) Lesser Scaup (Aythya affinis) Lesser Scaup (Aythya affinis) Mallard (Anas platyrhynchos) Mallard (Anas platyrhynchos) Redhead (Aythya americana) Musk rat (Ondatra zibethicus) Patterson and Lindeman (2009) Lindeman (2006) Bulté and Blouin-Demers (2008) Petrie and Knapton (1999) Wormington and Leach (1992) Mazak et al. (1997) Mazak et al. (1997) Petrie and Knapton (1999) Wormington and Leach (1992) Mazak et al. (1997) Petrie and Knapton (1999) Wormington and Leach (1992) Wormington and Leach (1992) Mazak et al. (1997) Wormington and Leach (1992) Mazak et al. (1997) Sietman et al. (2003) References used to determine the number of larval parasites using the yellow perch (Perca flavescens) and the round goby (Neogobius melanostomus) as intermediate hosts to infect piscivorous birds in the Great Lakes and St-Lawrence river system (North America; see Fig. 2). on invasive species (Butler et al. 2004). Such transmissions could have both direct and indirect consequences for ecosystems (Perkins et al. 2008; Dunn 2009). INVASIVE PREY AND TROPHICALLY TRANSMITTED PARASITES Many different groups of parasites use prey as intermediate or paratenic hosts to infect predators (Lafferty 1999). Virtually all macroparasites and many microparasites with complex life cycles rely on trophic transmission (Kuris 2003). The abundance and diversity of trophically transmitted parasites acquired by a predator are a direct reflection of its diet (e.g., Bertrand et al. 2008; Valtonen et al. 2010). Diet shifts from native to invasive prey are thus expected to directly affect parasite acquisition (Fig. 1a). Invasive prey theoretically could increase the trophic transmission of certain parasites to native predators through spillback or spillover effects. Parasite spillover occurs when an invasive species introduces an exotic parasite capable of infecting native wildlife; spillover occurs often, and can lead to declines in native wildlife, but examples currently do not include trophically transmitted parasites (Daszak et al. 2000). Parasite spillover theoreti- cally can affect both the diversity and the abundance of parasites that predators acquire trophically. However, spillover of trophically transmitted parasites is expected to be uncommon because many parasites using trophic transmission require multiple hosts to complete their life cycle. Their low establishment success is explained in part by the challenges associated with finding multiple suitable hosts in a novel environment (Torchin et al. 2002). Parasite spillback, in comparison, may be more common with parasites requiring trophic transmission. Parasite spillback occurs when an alien species becomes a suitable host for a native parasite (Kelly et al. 2009a; Mastitsky and Veres 2010). If an invasive prey becomes a suitable intermediate or paratenic host for a native parasite, the parasite can subsequently be transmitted to a native host via predation. Because parasite spillback involves native parasites, this phenomenon has the potential to increase the intensity of infection in native predators by increasing exposure to certain parasites (Kelly et al. 2009a; Mastitsky and Veres 2010). The intensity of a parasitic infection may have an important effect on host fitness because host condition is expected to decline with increasing infection intensity (Beldomenico and Begon 2010). Alternatively, invasive species may not be competent hosts for common native parasites or they may act as sinks Author's personal copy 10 Grégory Bulté et al. Figure 1. Feeding on invasive prey can affect the trophic transmission of parasites (a), the nutritional value of the diet (b), and the exposure to contaminants (c). Parasite release or dilution will decrease parasitism while parasite spillback and spillover will increase parasitism. The nutritional value of the prey will alter immune functions and parasitism through its effects on predator condition. A change in condition or parasitism can trigger a feedback loop increasing or decreasing parasitism and condition. Predation on invasive prey can affect the trophic transfer of contaminants with immunomodulatory effects positively or negatively affecting parasitism. for native parasites (Kelly et al. 2009b). In such cases, the intensity of infection by these parasites would be expected to decrease as the proportion of invasive prey in the diet increases. Even if the invasive prey acquires some native parasites, a decline in the intensity of infection will occur as long as the invasive prey is a less suitable host than the native prey. Lower exposure to parasites may explain, at least in part, why some native predators exhibit increases in condition and growth rate following a diet shift from native to invasive prey. For instance, smallmouth bass (Micropterus salmoides) exhibit an increase in growth rate following an almost complete diet shift from native species to invasive round gobies (Neogobius melanostomus; Steinhart et al. 2004). Lower exposure to parasites may have contributed to these changes because round goby have fewer parasites than native fishes (Kvach and Stepien 2008; Gendron et al. 2012) which would reduce the predator’s exposure to certain parasites and their potential deleterious effects. Diet shifts from native to invasive prey also can affect the diversity of parasites trophically acquired by a predator (Fig. 2). The tendency of invasive species to have a lower level of parasitism (parasite release) is a well-documented phenomenon (reviewed by Torchin et al. 2002; Dunn 2009). Invasive species have on average half the number of species of parasites of their native counterparts (Torchin et al. 2003; cf. Kelly et al. 2009b). In addition, once established in their introduced range, invasive species become hosts to fewer parasites compared to their native counterparts (Torchin et al. 2003; Gendron et al. 2012). The loss of parasites during invasion is especially likely for parasites requiring multiple hosts (Torchin et al. 2002). Therefore, native predators foraging on invasive prey should be exposed to a lower diversity of trophically transmitted parasites than those feeding on native prey (Fig. 2). Moreover, the diversity of trophically transmitted parasites acquired by a predator increases with the diversity of prey consumed (Rossiter and Sukhdeo 2011; Valtonen et al. 2010). Thus, if diet shifts from native to invasive prey lead to a decline in the diversity of prey consumed, a reduction in the diversity of trophically transmitted parasites should follow and lead to an increase in fitness (see Bordes and Morand 2009). Alternatively, the inclusion of invasive species might increase the diversity of prey ingested by a predator, potentially increasing the diversity of parasites. The loss (or gain) of parasites might have important cascading effects on likelihood of other parasitic infections if, for example, a loss or gain affected condition or immune functions of hosts. Author's personal copy Effects of Invasive Prey on Parasitism 11 Figure 2. Invasive round goby (a; Neogobius melanostoma) replaced native species in the diet of double crested cormorant (b; Phalacrocorax auritus) in Lake Ontario (c; Johnson et al. 2010a, b). The round goby is an intermediate host for only 7 species of parasites infecting piscivorous birds in North America. In contrast, the native yellow perch (Perca flavescens) is an intermediate host for at least 16 species of parasites using piscivorous birds as their ultimate host in the Great Lakes and St Lawrence area alone. For references on yellow perch and round goby parasites see Dechtiar and Christie (1988), Dechtiar et al. (1988), Dechtiar and Lawrie (1988), Dechtiar and Nepszy (1988), Gendron et al. (2012), Kvach and Stepien (2008), Marcogliese et al. (2010), Muzzall (1999), and Muzzall and Whelan (2011). INVASIVE PREY, NUTRITIONAL STATUS, AND IMMUNE FUNCTIONS Fig. 1b). Diet quality can greatly influence immune functions in animals (Grimble 2001; Kidd 2004). For example, Jones et al. (2011) showed that immunization of lactating rats against an intestinal nematode depends on the amount of proteins in their diet, which influences the accumulation of mucosal mast cells (and eosinophils) in the small intestine. Food availability (i.e., diet quantity) can also affect immune functions (AlonsoAlvarez and Tella 2001) which translate into magnitude of parasite effects (Krist et al. 2004). For instance, Krist et al. (2004) found that the New Zealand mud snail (Potamopyrgus antipodarum) experimentally infected by trematodes experiences higher parasite-mediated mortality when maintained on Invasive species can differ from native prey in terms of nutritional value (Ruetz et al. 2009). Moreover, the amount of energy required for a predator to catch and process a prey may also differ between native and invasive prey (Richman and Lovvorn 2004). Thus diet shifts from native species to invasive species can have repercussions on the nutritional status and energy budget of native predators. Changes in energy budget can in turn influence immune functions and thus the ability of the host to reduce parasitic infection (parasite resistance; Author's personal copy 12 Grégory Bulté et al. a low food diet compared to those on a high food diet. Food level was also shown to influence the proliferation of T-cells in birds (Alonso-Alvarez and Tella 2001). There are numerous indications that invasive prey can affect the nutritional status of native predators (feeding on infective stages of invasive parasites also could become important, cf. Johnson et al. 2010a, b). Body condition and growth rate are two traits directly affected by nutritional status (Evans 1973; Jakob et al. 1996). Positive and negative changes in these traits have been reported following diet shifts from native to invasive prey (Suarez et al. 2000; Pothoven et al. 2001; Steinhart et al. 2004; King et al. 2006). Positive changes are expected to occur when the invading species is a better nutritional alternative than native prey (e.g., King et al. 2006). In contrast, negative changes are expected to occur when the invading species is replacing a native prey with a greater nutritional value (e.g., Pothoven et al. 2001; Suarez et al. 2000). We are not aware of studies addressing the immunological ramifications of diet shift from native to invasive prey but such studies would be extremely valuable given the intrinsic connection between condition and vulnerability to infection or magnitude of parasite effects (Beldomenico and Begon 2010). INVASIVE PREY, CONTAMINANT, AND IMMUNE FUNCTIONS Invasive prey can have different patterns of contaminant bioaccumulation than native prey. A dietary shift by native predators from native to invasive prey could thus alter the trophic transfer of specific contaminants (Mazak et al. 1997; Richman and Lovvorn 2004; Kwon et al. 2006; Southward Hogan et al. 2007; Couillard et al. 2008). For example, in the Great Lakes (Canada), predation on invasive zebra mussels has increased the concentration of organochlorines in diving ducks because zebra mussels bioaccumulate organochlorines to concentrations above levels of the birds’ native prey (Mazak et al., 1997). Similarly, invasive round gobies are an important pathway for the trophic transfer of mercury to smallmouth bass (Southward Hogan et al. 2007). Many contaminants including organochlorines and mercury are immunosuppressive (Grasman et al. 1996; Fairbrother et al. 2004; Kenow et al. 2007). Foraging on invasive species may affect the host’s parasite resistance via the trophic transfer of such contaminants (Fig. 1c). Moreover, invasive species may acquire more native parasites over time (Gendron et al. 2012). Thus, in the case of predators feeding on gobies, the predator would not only bioaccumulate more contaminants but also simultaneously acquire more parasites than seen earlier on in invasion history. These combined effects might lead to sublethal or lethal consequences (Marcogliese and Pietrock 2011). Studies are needed exploring linkages between invasive prey, increased exposure to specific contaminants, and resulting changes in immune function, parasitism, and parasite effects. FUTURE DIRECTIONS The issues presented here fall directly in the mesh of the emerging field of ecoimmunology. This promising avenue of research will shed light on the impacts of environmental changes on the immunological and parasitological status of wildlife, including the impacts of invasive species (Martin et al. 2010). From an ecoimmunological perspective, the biotic and abiotic factors of a host’s environment are viewed as inputs modulating immunological outcomes (Sheldon and Verhulst 1996; Schulenburg et al. 2009). The ecoimmunological approach seeks to understand how these ecological inputs are affecting immune functions and therefore the impact of parasites on their hosts (Sheldon and Verhulst 1996; Schulenburg et al. 2009). Recent reviews and syntheses offer conceptual and methodological tools directly relevant for the design of experiments aiming at linking invasive prey, parasitism, and fitness (Boughton et al. 2011; Graham et al. 2011). It is important to point out that when a native predator shifts its diet from native to invasive prey, exposure to trophically transmitted parasites and contaminants as well as diet quality and quantity can all change simultaneously. Thus, the net impact on parasitism and ultimately on host fitness will depend on the direction and intensity of these changes (see Fig. 1). For instance, foraging on an invasive prey with a poor nutritional value may reduce allocation to immune functions and thus increase vulnerability to infections (Beldomenico and Begon 2010). However, if the invasive prey reduces the trophic transmission of parasites, the same predator may experience a decrease in parasitism. Thus, the net effect on the host and host populations may be positive, negative, or neutral. In addition, the effects are expected to vary temporally or spatially. For instance, a low nutritional status may not lead to increased infection in a pristine environment but may have a great impact in a degraded environment where additional stressors also are present (Beldomenico and Begon 2010; Martin et al. 2010; Marcogliese and Pietrock 2011). Author's personal copy Effects of Invasive Prey on Parasitism Evaluating the relative importance of these changes and quantifying the net effects on predator’s fitness should be the goal of future research in this area. Teasing apart all the mechanisms linking invasive prey, parasitism, and predator fitness will be challenging. For many systems, a major shortcoming will be the lack of historical data (prior to a diet shift) on parasite communities as well as on the diet and fitness-related traits of predators. However, this problem can be partially circumvented by comparing invaded and un-invaded systems with similar characteristics, or by conducting mesocosm experiments with simplified communities of prey, predators, and parasites. In addition, a potentially useful alternative would be to exploit the interindividual variation in foraging behaviour within an invaded population. Numerous studies demonstrate that individual specialization in feeding behaviour occurs within populations (reviewed by Bolnick et al. 2003). Thus, the degree of exploitation of invasive prey may vary between individuals within the same population. Inter-individual variation could thus be used as a basis to investigate the many simultaneous consequences of foraging on invasive prey. It should be kept in mind that populations of native predators might respond to abundance of invasive prey by changing the proportion of diet specialists, rather than by changes in population size per se. Even if any given study cannot tease apart all the mechanisms at play, simple experiments addressing a subset of the effects of invasive prey on the immunocompetence and/or parasitism of native predators would provide important baseline information (i.e., subsets represented by the arrows in Fig. 1). For instance, an experiment measuring the condition and immunocompetence of predators fed different proportions of invasive prey would provide important insights on the expected impact of a complete diet shift on parasitism by native species. With such experiments, multiple responses including parasite acquisition, the accumulation of contaminants, and nutritional status of the host could be monitored simultaneously in the same individual predator. In addition, controlled experiments allow researchers to assess parasite resistance and immunocompetence directly (e.g., Gendron et al. 2003). CONCLUSION We argue here that understanding the parasitological and immunological consequences of diet shifts from native to invasive prey will provide important insights into the 13 fitness responses of native predators to invasive prey. Diet shifts from native to invasive prey could greatly alter both the exposure of native predators to trophically transmitted parasites and their ability to resist parasitic infections. These changes may have subtle yet pervasive impacts on native predators that are directly relevant for their population management. For example, feeding on invasive prey is expected to cause a decrease in the diversity of parasites acquired by native predators. Although a reduction in the number of parasite species infecting native predators may seem desirable from immediate management perspectives, the long-term implications may not be desirable. Parasite diversity appears to be necessary to maintain optimal levels of immunocompetance within populations (Wegner et al. 2003a, b). A reduction in the diversity of parasites may thus lead to an increase in the vulnerability of populations to disease emergence. Understanding the impact of a diet shift is also relevant from a management viewpoint, especially when predators show declining condition (e.g., Pothoven et al. 2001). Indeed, an ensuing cycle of increasing infection and decreasing condition may occur because a decrease in host condition can lead to an increase in infection and vice versa (Beldomenico and Begon 2010). Perturbations, including nutritional stress caused by invasive species, hold the potential to trigger such a negative feedback loop, which also could ultimately lead to disease emergence (Fig. 1; Beldomenico and Begon 2010). The impact of biological invasions on host–parasite relationships is an important area of concern (reviewed by Dunn 2009). However, to date, very few studies have addressed how these complex relationships are affected by predation on invasive species. Experiments are needed to specifically address the immunological and parasitological implications of native to invasive prey diet shifts. Such experiments are crucial to understand fully the impacts of biological invasions on host–parasite relationships and to predict the fitness response of native predators confronted with changes in their prey base. ACKNOWLEDGMENTS Financial support for GB was provided from the Ontario Ministry of Research and Innovation and the Fond Québecois de Recherche sur la Nature et les Technologies. Financial support for SAR was provided by the Natural Sciences and Engineering Research Council of Canada. We thank the reviewers for their constructive comments. Author's personal copy 14 Grégory Bulté et al. 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