Is There Such Thing as a Parasite Free Lunch? The Direct and Indirect Consequences of Eating Invasive Prey

Article (PDF Available)inEcoHealth 9(1):6-16 · March 2012with107 Reads
DOI: 10.1007/s10393-012-0757-7 · Source: PubMed
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.
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EcoHealth
Conservation Medicine: Human
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Volume 9
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EcoHealth (2012) 9:6-16
DOI 10.1007/s10393-012-0757-7
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
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Is There Such Thing as a Parasite Free Lunch? The Direct
and Indirect Consequences of Eating Invasive Prey
Gre
´
gory Bulte
´
,
1
Stacey A. Robinson,
1
Mark R. Forbes,
1
and David. J. Marcogliese
2
1
Department of Biology, Carleton University, 1125 Colonel By, Ottawa, ON K1S 5B6, Canada; robinson.stacey@gmail.com
2
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
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 pro-
found impact on the structure of populations, communi-
ties, 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.
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 popu-
lation 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). How-
ever, 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,
Published online: March 27, 2012
Correspondence to: Gre
´
gory Bulte
´
, e-mail: Gregory_Bulte@carleton.ca
EcoHealth 9, 6–16, 2012
DOI: 10.1007/s10393-012-0757-7
Forum
Ó 2012 International Association for Ecology and Health
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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 pre-
dators 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 inverte-
brates, 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 nec-
essary 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 mecha-
nisms.
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 bio-
logical 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
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 Thiamine status (;) Fitzsimons et al. (2009)
Fish Individual growth rate (:) Steinhart et al. (2004)
Reptile Concentration of organochlorine in tissue (=) Fernie et al. (2008)
Reptile Individual growth rate and body size (:) King et al. (2006)
Zebra mussel Bird Population density (:) Petrie and Knapton (1999)
Bird Concentration of organochlorine in tissue (:) Mazak et al. (1997)
Fish Concentration of organochlorine in tissue (=) Andraso (2005)
Fish Individual growth rate (:/;) French and Bur (1996)
Fish Body condition (;) Pothoven et al. (2001)
Fish Concentration of organochlorine in tissue (;) Mercer et al. (1999)
Fish Individual growth rate (:) Mercer et al. (1999)
Reptile Clutch size (=) Bulte
´
and Blouin-Demers (2008)
Effects of Invasive Prey on Parasitism
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Table 2. Field Studies Documenting Predation on Invasive Zebra Mussel (Dreissena polymorpha) and Round Goby (Neogobius mela-
nostomus) in North America
Prey Predator Source
Round goby Brown bullhead (Ameiurus nebulosus) Reyjol et al. (2010)
Burbot (Lotta lotta) Madenjian et al. (2011)
Burbot (Lotta lotta) Jacobs et al. (2010)
Channel catfish (Ictalurus punctatus) Reyjol et al. (2010)
Lake Trout (Salvelinus namaycush) Dietrich et al. (2006)
Lake Trout (Salvelinus namaycush) Fitzsimons et al. (2009)
Lake Trout (Salvelinus namaycush) Jacobs et al. (2010)
Northern pike (Essox lucius) Reyjol et al. (2010)
Sauger (Sander canadensis) Reyjol et al. (2010)
Smallmouth bass (Micropterus dolomieu) Reyjol et al. (2010)
Smallmouth bass (Micropterus dolomieu) Steinhart et al. (2004)
Walleye (Sander vitreus) Reyjol et al. (2010)
Walleye (Sander vitreus) Bur et al. (2008)
Yellow perch (Perca flavescens) Reyjol et al. (2010)
Yellow perch (Perca flavescens) Truemper and Lauer (2005)
Lake Erie watersnake (Nerodia sipedon insularum) King et al. (2006)
Lake Erie watersnake (Nerodia sipedon insularum) Fernie et al. (2008)
Double crested cormorant (Phalacrocorax auritas) Johnson et al. (2010)
Double crested cormorant (Phalacrocorax auritas) Somers et al. (
2003)
Red-breasted merganzer (Mergus serrator) Bur et al. (2008)
Zebra mussel Blue crab (Callinectes sapidus) Boles and Lipcius (1997)
Blue catfish (Ictalurus furcatus) Herod et al. (1997)
Blue catfish (Ictalurus furcatus) Magoulick and Lewis (2002)
Bluegill (Lepomis macrochirus) Andraso (2005)
Bluegill (Lepomis macrochirus) Bartsch et al. (2005)
Bluegill (Lepomis macrochirus) Mercer et al. (1999)
Bufflehead (Bucephala albeola) Mazak et al. (1997)
Common carp (Cyprinus carpio) Tucker et al. (1996)
Common carp (Cyprinus carpio) Bartsch et al. (2005)
Flathead catfish (Pylodictis olivaris) Bartsch et al. (2005)
Freshwater drum (Aplodinotus grunniens) French and Bur (1996)
Freshwater drum (Aplodinotus grunniens) Magoulick and Lewis (2002)
Freshwater drum (Aplodinotus grunniens) Bartsch et al. (2005)
Freshwater drum (Aplodinotus grunniens) Watzin et al. (2008)
Freshwater drum (Aplodinotus grunniens) Morrison et al. (1997)
Lake whitefish (Coregonus clupeaformis) Pothoven et al. (2001)
Pumpkinseed (Lepomis gibbosus) Andraso (2005)
Pumpkinseed (Lepomis gibbosus) Watzin et al. (2008)
Pumpkinseed (Lepomis gibbosus) Mercer et al. (1999
)
Quillback carpsucker (Carpiodes cyprinus) Bartsch et al. (2005)
Redear sunfish (Lepomis microlophus) Magoulick and Lewis (2002)
Redhorse suckers (Moxostoma spp.) Bartsch et al. (2005)
Rock bass (Ambloplites rupestris) Watzin et al. (2008)
Yellow perch (Perca flavescens) Watzin et al. (2008)
Yellow perch (Perca flavescens) Morrison et al. (1997)
Yellow perch (Perca flavescens) Mercer et al. (1999)
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on invasive species (Butler et al. 2004). Such transmissions
could have both direct and indirect consequences for eco-
systems (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). Vir-
tually all macroparasites and many microparasites with
complex life cycles rely on trophic transmission (Kuris
2003). The abundance and diversity of trophically trans-
mitted 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 par-
asite 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
Table 2. continued
Prey Predator Source
Musk turtle (Sternotherus odoratus) Patterson and Lindeman (2009)
Northern map turtle (Graptemys geographica) Lindeman (2006)
Northern map turtle (Graptemys geographica) Bulte
´
and Blouin-Demers (2008)
Bufflehead (Bucephala albeola) Petrie and Knapton (1999)
Bufflehead (Bucephala albeola) Wormington and Leach (1992)
Canvasback (Aythya valisneria) Mazak et al. (1997)
Greater Scaup (Aythya marila) Mazak et al. (1997)
Greater Scaup (Aythya marila) Petrie and Knapton (1999)
Greater Scaup (Aythya marila) Wormington and Leach (1992)
Lesser Scaup (Aythya affinis) Mazak et al. (1997)
Lesser Scaup (Aythya affinis) Petrie and Knapton (1999)
Lesser Scaup (Aythya affinis) Wormington and Leach (1992)
Lesser Scaup (Aythya affinis) Wormington and Leach (1992)
Mallard (Anas platyrhynchos) Mazak et al. (1997)
Mallard (Anas platyrhynchos) Wormington and Leach (1992)
Redhead (Aythya americana) Mazak et al. (1997)
Musk rat (Ondatra zibethicus) 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).
Effects of Invasive Prey on Parasitism 9
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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 in-
creases. Even if the invasive prey acquires some native par-
asites, 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 con-
dition 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 cer-
tain 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 phe-
nomenon (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 inva-
sion 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 tro-
phically transmitted parasites than those feeding on native
prey (Fig. 2). Moreover, the diversity of trophically transmit-
ted 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 oftrophically 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.
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.
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INVASIVE PREY,NUTRITIONAL STATUS,
AND IMMUNE FUNCTIONS
Invasive species can differ from native prey in terms of nutri-
tional 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;
Fig. 1b). Diet quality can greatly influence immune functions
in animals (Grimble 2001;Kidd2004). 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 (Alonso-
Alvarez 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 experi-
ences higher parasite-mediated mortality when maintained on
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).
Effects of Invasive Prey on Parasitism
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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 con-
taminants, and resulting changes in immune function, par-
asitism, 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 tro-
phically 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 tempo-
rally 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 addi-
tional stressors also are present (Beldomenico and Begon
2010;Martinetal.2010; Marcogliese and Pietrock 2011).
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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 commu-
nities of prey, predators, and parasites. In addition, a
potentially useful alternative would be to exploit the inter-
individual 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 accu-
mulation 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 immunocom-
petence 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
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 popula-
tion 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
Que
´
becois 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.
Effects of Invasive Prey on Parasitism 13
Author's personal copy
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