Download How parasites affect interactions between competitors and predators

Ecology Letters, (2006) 9: 1253–1271
REVIEW AND
SYNTHESIS
1
Melanie J. Hatcher, Jaimie T. A.
Dick2 and Alison M. Dunn3
1
School of Biological Sciences,
University of Bristol, Woodland
Road, Bristol BS8 1UG, UK
2
School of Biological Sciences,
Queen’s University Belfast, MBC,
97 Lisburn Road, Belfast BT9
7BL, UK
3
Institute of Integrative and
Comparative Biology, Faculty of
Biological Sciences, University of
Leeds, Leeds LS2 9JT, UK
*Correspondence: E-mail:
mel.hatcher@bristol.
ac.uk
doi: 10.1111/j.1461-0248.2006.00964.x
How parasites affect interactions between
competitors and predators
Abstract
We present a synthesis of empirical and theoretical work investigating how parasites
influence competitive and predatory interactions between other species. We examine the
direct and indirect effects of parasitism and discuss examples of density and parasiteinduced trait-mediated effects. Recent work reveals previously unrecognized complexity
in parasite-mediated interactions. In addition to parasite-modified and apparent
competition leading to species exclusion or enabling coexistence, parasites and predators
interact in different ways to regulate or destablize the population dynamics of their joint
prey. An emerging area is the impact of parasites on intraguild predation (IGP). Parasites
can increase vulnerability of infected individuals to cannibalism or predation resulting in
reversed species dominance in IGP hierarchies. We discuss the potential significance of
parasites for community structure and biodiversity, in particular their role in promoting
species exclusion or coexistence and the impact of emerging diseases. Ongoing invasions
provide examples where parasites mediate native/invader interactions and play a key role
in determining the outcome of invasions. We highlight the need for more quantitative
data to assess the impact of parasites on communities, and the combination of
theoretical and empirical studies to examine how the effects of parasitism scale up to
community-level processes.
Keywords
Parasite, coexistence, indirect effect, competitor, predator, intraguild predation,
community module, parasite-modified interactions, parasite-mediated interactions,
reservoir.
Ecology Letters (2006) 9: 1253–1271
INTRODUCTION
One of the biggest challenges facing ecologists today is to
understand how, and to what extent, interspecific interactions influence community structure, species coexistence
and biodiversity. Coupled with this is an increasing
awareness of the potential importance of parasites and
pathogens in determining the outcomes of trophic interactions (MacNeil et al. 2003a; Tompkins et al. 2003; Malmstrom et al. 2006) and community processes (de Castro &
Bolker 2005; Mouritsen & Poulin 2005a; Collinge & Ray
2006; Wilmers et al. 2006). One way we can attempt to
characterize a community is to decompose it into subsets of
strongly interacting species (a community module: Holt
1997). Given that any realistic community is composed of
many (hundreds) of modules (see, for example, Bascompte
& Melian 2005), the resulting dynamics are potentially very
complex and, indeed, a fully analytical understanding of how
interactions between species translate into community
structure may never be possible. Despite this potential
intractability, a first step is to understand interactions within
modules, and then attempt to examine the consequence of
these module-level processes as they propagate through a
community (Holt 1997). Although some modules have been
examined in depth both empirically and theoretically, there
are still many areas of uncertainty, particularly where
modules involving parasitism are concerned (Holt &
Dobson 2006). Here, we present a synthesis of current
knowledge and indicate future directions for research into
how parasites influence competitive and predatory interactions between the species they infect.
Parasites can potentially be important players in many
different community modules, and can enter into a given
module in different positions. For example, two species that
Ó 2006 Blackwell Publishing Ltd/CNRS
1254 M. J. Hatcher, J. T. A. Dick and A. M. Dunn
Review and Synthesis
The modern approach to predicting the population
dynamics of the two-species interaction between host and
parasite was developed by Anderson & May (1981). One
host–one parasite models such as these demonstrate that the
population dynamics of hosts and parasites depend crucially
on many different factors, including parasite transmission
(rates or functions), stages in the parasite life-cycle, host
mortality (parasite-induced or otherwise), and host immune
or defence responses to infection. When additional interactions with other species or the environment are added, the
scope for complexity of outcomes is enhanced (see, for
example, Altizer et al. 2006; Keesing et al. 2006). In
particular, the combination of two interactions involving
three species can lead to dynamics that cannot be predicted
from an analysis of the pairwise interactions alone (see, for
example, Hochberg et al. 1990).
One reason why we cannot extrapolate multispecies
interactions from pairwise components is that indirect
interactions are also involved. Indirect effects occur when
share a parasite may be competitors, intraguild predators,
one may be prey for the other, or they may interact only via
the effects of the parasite (Fig. 1). Furthermore, parasites
can influence interactions between species even if they do
not share the parasite. For instance, a parasite can, in
principle, reduce the competitive strength of infected hosts
against a non-host species. Alternatively, it can infect the
prey but not the predator, or vice versa, altering prey capture
rates as a result of effects on activity levels or behaviour of
the infected host. In this review we synthesize theoretical
and empirical studies that examine how parasites influence
interactions in different community modules, namely, the
modules of apparent competition via a shared parasite
(Fig. 1a); resource competition between the hosts of a
shared parasite (Fig. 1b); a specialist parasite of one of a
competing species pair (Fig. 1c); predator–prey modules
where the parasite infects the prey (Fig. 1d) or the predator
(Fig. 1e) or both (Fig. 1f); and intraguild predation (IGP)
with a shared parasite (Fig. 1g).
(a)
(b)
Parasite C
Parasite C
–
–
+
Host A
–
Host B
–
+
Resource A’
–
–
+
+
Host A
–
+
+
Host B
–b –
+
+
Resource
Resource B’
(c)
–a
(e)
(d)
Parasite
Parasite C
Parasite
Predator
–
–
+
–
+
–a
Host A
–b
–
–
+
Host
Host
Host B
–
+
+
Resource
–
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(g)
(f)
–
Parasite C
Predator
+
–
–
–
+
+
+
+c
Host A
Host B
–d
Host
–
+
–
–
+
Resource
Resource
Ó 2006 Blackwell Publishing Ltd/CNRS
+
Resource
+
–
+
Prey
Resource
–
Parasite
+
+
Figure 1 Interactions involving parasites. (a)
Apparent competition (Holt 1977; Holt &
Pickering 1985); (b) interspecific resource
competition with shared parasite (after Price
et al. 1986, who include interference competition as denoted by arrows a and b); (c)
interspecific resource competition and a
specialist (not shared) parasite (modelled by
Anderson & May 1986 in which interference
a ¼ b ¼ 0); (d) predator–prey interaction
with infected prey (the parasite and predator
compete for prey resource); (e) predator–
prey interaction with infected predator (conforming to a simple food chain); (f) predator
and prey with shared parasite (as may occur
for intermediate/definitive host/vector
transmission relationships); (g) parasite
infecting two intraguild predators (in this
case competitor B eats A more frequently, or
obtains more benefit than A eating B, as
denoted by arrows +c and )d).
Review and Synthesis
the impact of one species on another is mediated by the
action of a third species. Abrams (1992) distinguishes two
types of indirect effect: those mediated through population
density effects propagated through an intervening species
and those resulting from behavioural responses by one or
more species to the presence or density of another. In
principle, both types of indirect effect can be mediated by
parasites, and in this review we will discuss potential
examples of each. A classic example of the former, densitymediated indirect effect is apparent competition (Holt
1977), where two species that share a natural enemy have
reciprocal negative effects ()) on each other’s population
density via the positive numerical response of the enemy
population. Behaviourally mediated indirect effects that
affect the shared predation module include those generated
by a predator’s aggregative response to patchily distributed
prey and its functional response within patches, or prey
refuge-seeking behaviour and reduced foraging in the
presence of predators (Holt & Kotler 1987; Abrams 1992;
Abrams & Matsuda 1996). Density and behaviourally
mediated indirect effects are likely to act at different
timescales (Holt & Kotler 1987; Abrams 1992). Densitymediated indirect effects result from changes in the density
of one species affecting the demographic response of
others, and so should take longer to propagate to other
species than the effects of direct interactions between
species. Behavioural effects occur on the same, or shorter,
timescale as direct effects (Holt & Kotler 1987; Abrams
1992). Holt & Kotler (1987) examine how behavioural
responses of predators can generate ()) indirect effects
between prey species; this Ôshort-term apparent competitionÕ
is quite distinct from the classical numerical responseinduced variety elucidated by Holt (1977).
These short-term processes are of interest for several
reasons. Firstly, they can produce a much greater variety of
interactions than those resulting from density alone; for
instance, in the two prey-one shared enemy module
(Figs 1a,b) all the combinations of indirect interactions
()), (+)), ()+) and (++) between the prey are theoretically
possible (Holt & Kotler 1987; Abrams 1992; Abrams &
Matsuda 1996). Secondly, because these are relatively fast
processes, they could potentially be powerful in structuring
populations and communities (Bolker et al. 2003). Thirdly,
the variety of (often, counter-intuitive) relationships generated can have knock-on effects for community structure and
stability, for instance generating (++) relationships between
top predators and middle predators (Abrams 1992). There
has been a recent resurgence of interest in short-term
effects, now termed trait-mediated indirect effects (TMIEs),
which include morphological, physiological and life-history
changes as well as behaviour (e.g. Bolker et al. 2003; Werner
& Peacor 2003). Most of the theoretical and empirical
research on TMIEs has concentrated on predator–prey
Parasite-modified interactions 1255
relationships, in part because there are clear examples of
predator/prey foraging responses known from the discipline
of behavioural ecology. Less work has focused on TMIEs in
parasite–host relationships; one reason being that concepts
from foraging theory and behavioural ecology have seldom
been applied to parasites. For instance, there is no obvious
analogue for parasites of handling time or predator
functional response. Nevertheless, as parasites rarely kill
their host (at least, not immediately), host population density
is not the only characteristic that parasites can influence, so
there should be great scope for TMIEs in parasitism
modules. The degree to which short-term effects are
important in parasite modules will thus depend on the type
of TMIEs, if any, induced by parasites; we will also discuss
possible examples of these.
In this review we take a bottom-up approach to
understanding the role of parasites in community structure,
concentrating on their role in community modules (see Holt
& Dobson 2006 for a similar approach). We restrict our
review to interactions involving parasites and pathogens
(organisms that feed on a host individual, usually living on
or in it and often causing harm but not immediate death),
and do not include predators, parasitoids or herbivores
(unless they are part of a parasite module). Interactions
involving these other natural enemies and their victims have
been very well reviewed elsewhere (Chase et al. 2002; Bolker
et al. 2003; van Veen et al. 2006). Because our aim is to
examine how parasites influence interactions between other
species, the interactions considered here necessarily involve
three (or more) species and we ignore the large and
important literature on simple pairwise host–parasite interactions. We consider how parasites enter into and influence
interactions for all the modules depicted in Fig. 1, reviewing
the theoretical and empirical state of understanding for each.
Apparent competition via a shared parasite (Fig. 1a),
resource competition between hosts of a shared parasite
(Fig. 1b), and a specialist parasite of one of a competing pair
(Fig. 1c) are considered under the heading ÔParasites and
competitorsÕ; in the section ÔParasites and PredatorsÕ we
examine predator–prey interactions where the parasite
infects the prey (Fig. 1d) or predator (Fig. 1e), or both
(Fig. 1f). We also consider plant, plant pathogen and
herbivore interactions (structurally similar to Fig. 1d) and
IGP with a shared parasite (Fig. 1g). Whilst we do not
examine them in general, simple tri-trophic food chains are
represented by the prey–predator–parasite module of
Fig. 1e and omnivory by the IGP module of Fig. 1g. Where
theory or empirical examples allow, we also extrapolate to
community-level outcomes of these module-level interactions. One omission is the competition module of parasite–
parasite–host (for a recent overview see Holt & Dobson
2006); another omission is the simple food chain host–
parasite–hyperparasite, which has received relatively little
Ó 2006 Blackwell Publishing Ltd/CNRS
1256 M. J. Hatcher, J. T. A. Dick and A. M. Dunn
research and undoubtedly deserves more (Holt & Hochberg
1998). We cover interactions involving plants and their
pathogens and endophytes, but not in as much depth as we
cover animal–parasite interactions. We go on to discuss the
potential significance of parasites for community structure
with reference to a relatively well-studied situation, namely
the on-going Ônatural experimentsÕ represented by biological
invasions. We conclude with a discussion of future research
challenges, identifying a number of areas where theoretical
and empirical data might be integrated to further our
understanding of parasite influences on community structure.
PARASITES AND COMPETITORS
Apparent and parasite-mediated competition
A classic controlled study of the effects of parasites on
competition was conducted by Park (1948), who demonstrated that infection by the shared parasite Adelina tribolii reversed
the outcome of competition between two species of flour
beetle (Tribolium castaneum and T. confusum)1. Two terms have
been used to describe this type of interaction. Two species that
do not compete directly for resources can have deleterious
effects on each other’s population sizes via a shared natural
enemy; this is termed apparent competition (Holt 1977; Fig. 1a).
Parasites, predators and parasitoids can be responsible for this
effect (Holt 1977; Holt & Pickering 1985; Holt & Lawton
1993, 1994). More recently, parasite-mediated competition has
been used to describe the situation when two species compete
with one another, and a parasite (which may or may not be
shared in both species) influences this competitive interaction
(Fig. 1b,c). If the parasite has differential effects on the fitness
of competing species, relative competitive strengths and
hence population outcomes can be altered (Price et al. 1986;
Hudson & Greenman 1998).
It might be argued that real systems will tend to lie
somewhere on a continuum, with varying relative strengths
of indirect effect mediated by the natural enemy and direct
competition. Apparent competition was initially defined as a
reciprocal negative relationship ()) between prey species
(Holt 1977), but a recent analysis suggests that it is
frequently asymmetric (Chaneton & Bonsall 2000).
Although the original theoretical formulation of apparent
competition assumes no direct competition between the
victim species sharing a natural enemy (Holt 1977), in
principle the process can nevertheless be important in
modules with direct competition. Deconstructing systems
1
Later studies by Park et al. (1965), however, showed that these species
engaged in Ôcannibalistic predationÕ, what we would now call intraguild
predation, and it is unclear if this latter interaction was parasite mediated in
the original ÔcompetitionÕ experiments.
Ó 2006 Blackwell Publishing Ltd/CNRS
Review and Synthesis
into direct and indirect effects helps to clarify the problem:
two competing species that share a parasite interact directly
via use of the shared resource and indirectly via effects of
the parasite on the other’s population size. In some cases
(when resources are not depleted), the system is dominated
by the indirect effects and resembles pure apparent
competition (Fig. 1a). In contrast, when competition is
severe because resources are strongly limiting, the module is
dominated by the direct interaction (which could, nonetheless, be strongly influenced by parasite modification of
competitive strength: Fig. 1b). The term Ôparasite-mediated
competitionÕ has not been explicitly defined and is often
used when elements of apparent competition apply. In
addition, it can be difficult to determine the strength of the
direct competitive component, making it difficult to assess
the relative importance of parasite-mediated apparent and
direct competition (Hudson & Greenman 1998; Chaneton
& Bonsall 2000). In this review, we will therefore use the
term Ôapparent competitionÕ to refer to situations where the
population processes involve indirect effects on population
density mediated by the parasite, and the term Ôparasitemodified competitionÕ to describe situations where there is
evidence of a direct effect of the parasite on the competitive
ability of one (or more) of its hosts.
Theoretical and empirical examples
Apparent competition mediated by parasites was first
considered explicitly by Holt & Pickering (1985), who
examined two host species sharing one microparasite. The
hosts did not compete intra- or inter-specifically, the aim
being to examine whether the parasite alone could be
responsible for regulating the host populations (Fig. 1a).
The lack of any direct competition meant that, in the
absence of the parasite, the host species would coexist
(indeed, both populations would grow unchecked as they
were not internally regulated). With the parasite present,
three outcomes were possible, analogous to outcomes for
interspecific competition: (i) repeatable exclusion of one
host species (the one most affected by the parasite; if
interspecific transmission is the same as or greater than
intraspecific transmission and virulence differences
between host species are of sufficient magnitude); (ii) both
hosts coexist (if interspecific transmission is less than
intraspecific transmission, but the two species are similarly
affected by the parasite); (iii) exclusion of either species
depending on initial (population density) conditions (this
occurs when interspecific transmission is higher than
intraspecific transmission). The two exclusion results capture the essence of apparent competition: the outcomes look
like the result of interspecific competition, but no direct
competition is involved. One host species acts as a reservoir
for enemies of the other host and vice versa; the species that
Review and Synthesis
can tolerate more parasites (because it is infected less
frequently, or suffers less parasite-induced mortality)
excludes the other. However, the second possibility, that
of species coexistence, deserves equal attention. This result
differs crucially to those for predators (Holt 1977) and
parasitoids (Holt & Lawton 1993). These natural enemies
can be responsible for apparent competition and exclusion
(reviewed in van Veen et al. 2006) but, in contrast to the
parasite model, in the absence of other limiting or
complicating factors, they cannot persist stably with both
prey species (Holt 1977; Holt & Lawton 1993, 1994). This is
because no analogue to intra- and inter-specific transmission
exists for predators or parasitoids (without population
structure or predator preference, the two host/prey species
are attacked at random). This difference serves to underline
the observation that parasites cannot necessarily be
subsumed within predator or parasitoid models; the
dynamics of parasite systems of apparent competition are
considerably richer.
Anderson & May (1986) reviewed and developed a
number of simple community models, including the case for
two species that compete intra- and interspecifically, one of
which was also host to a microparasite (Fig. 1c). In the
absence of the parasite, the standard three outcomes for
interspecific competition apply: the superior competitor
wins, there is stable coexistence, or the outcome depends on
initial conditions. If the parasite infects the inferior
competitor, there is no change in outcome. However, if it
infects the superior competitor, it can enable the otherwise
excluded competitor to persist. Parasite-modified competition where the parasite is not generally shared affects the
distribution of Anolis lizards in the caribbean (Schall 1992).
Anolis gingivinius is a stronger competitor than A. wattsi and
sympatric populations are found only when the malarial
parasite Plasmodium azurophilum is present. This parasite
rarely infects A. wattsi but can be common in A. gingivinius.
The parasite reduces the host’s competitive ability, permitting coexistence of the lizard species (Schall 1992). In this
instance, the parasite appears to be responsible for
maintaining species diversity. Holt & Dobson (2006)
examine theoretically the conditions under which parasites
play such pivotal (keystone) roles in a variety of community
modules.
Begon et al. (1992) examined the case for a shared
parasite, examining a microparasite and two host species
with intraspecific competition but no interspecific competition. As above, repeatable exclusion, coexistence or
exclusion dependent on initial conditions were the possible
outcomes. The Begon et al. (1992) model is a more realistic
representation of real communities as the hosts are regulated
in absence of the parasite, but the similarity of general
outcomes to Holt & Pickering’s (1985) simpler model is not
surprising; the parasite simply imposes additional regulation
Parasite-modified interactions 1257
onto that imposed by intraspecific competition. Bowers &
Turner (1997) incorporated interspecific competition into
this framework and showed that parasites could enhance or
reverse the effects of direct competition. The outcome
depends on which species can tolerate or support a higher
prevalence of infection. If the parasite is more virulent in the
superior competitor, it can reverse competitive outcomes,
enabling the inferior competitor (which might otherwise
have been excluded) to persist (i.e. it is a keystone parasite;
Holt & Dobson 2006), or even excluding the superior
competitor. If the parasite is more virulent in the inferior
competitor, it can lead to elimination of that species. An
empirical example of this is the replacement of the native
Eurasian red squirrel in the UK by the introduced grey
squirrel, which harbours a parapox virus that is avirulent in
greys but highly virulent in reds (e.g. Tompkins et al. 2003).
Model parameterization indicates that whilst competition
alone cannot explain the speed and pattern of replacement,
inclusion of the virus produces a very close fit to the data
(Rushton et al. 2000; Tompkins et al. 2003). In field and
laboratory manipulations of isopod crustaceans (Porcellio
scaber and P. laevis), Grosholz (1992) discriminated between
interspecific competition, intraspecific competition and viral
parasitism to show that the shared virus caused apparent
competition and reduced interspecific competitive ability in
P. scaber. Many other empirical studies of microparasites
(Schall 1992; Aliabadi & Juliano 2002; Juliano & Lounibos
2005) and macroparasites (Hanley et al. 1995) that have not
been tested quantitatively appear to support these general
findings. Several examples of pathogen-modified competition have been reported in plants (Alexander & Holt 1998;
Power & Mitchell 2004; Malmstrom et al. 2005, 2006). Some
grass species infected with Barley and Cereal Yellow Dwarf
Viruses (B/CYDVs) suffer reduced competitive ability
against other grasses that are less prone to the infection
(Power & Mitchell 2004; Malmstrom et al. 2006). The
replacement of native perennial bunchgrasses by invasive
annual grasses has been attributed, in part, to the greater
impact of B/CYDV on the competitive ability of the native
(Malmstrom et al. 2005, 2006). Many plant–endophyte
interactions show the reverse pattern: fungal endophytes
that form symbioses with their hosts enhance the ability of
the host in intra- and interspecific competition (reviewed in
Clay & Schardl 2002). Such endophyte-induced effects can
reduce plant diversity (Clay & Holah 1999) with important
consequences for community structure at other trophic
levels (Rudgers et al. 2004; discussed below).
Models for macroparasites bear out the general conclusions drawn for microparasites (Begon et al. 1992; Yan 1996;
Greenman & Hudson 2000). However, macroparasite
models tend to be tailored to specific systems owing to
the peculiarities of parasite life history. Even relatively
simple one host-one parasite systems can have dramatically
Ó 2006 Blackwell Publishing Ltd/CNRS
1258 M. J. Hatcher, J. T. A. Dick and A. M. Dunn
different dynamics depending on aspects of parasite
lifecycle, so these models are best examined in the context
of the systems they represent. A well-studied case is that of
the shared nematode parasite (Heterakis gallinarum) which
may underpin exclusion of the native UK grey partridge by
the introduced ring-necked pheasant (Tompkins et al.
2000a). The decline in partridge numbers over the last
50 years has been attributed partially to apparent competition mediated by the parasite, which has a much larger
impact on host fitness in the partridge. Parameterization of
models revealed that the parasite cannot be maintained in
partridge populations alone as its basic reproductive rate is
too low in this host (Tompkins et al. 2000a). However, when
the pheasant is present, it acts as a reservoir, boosting the
density of susceptible hosts above the threshold required for
parasite establishment (Tompkins et al. 2000b).
A frequently cited case where parasites change the
outcome of inter-specific competition is that of the
nematode Parelaphostrongylus tenuis, its gastropod intermediate
hosts, its definitive host the white-tailed deer (Odocoileus
virginianus) and at least two alternative hosts, moose (Alces
alces) and caribou (Rangifer tarandus). Widespread declines in
moose and caribou have been attributed to the parasite
because it is largely benign in deer but usually fatal in moose
and caribou, and the deer is thought to be an inferior
competitor (e.g. Holt & Pickering 1985; Price et al. 1986).
Schmitz & Nudds (1994) develop a detailed model of this
system, deriving equations for the population dynamics of
deer, moose, gastropods and three parasite life stages. The
model has three basic outcomes reminiscent of the general
microparasite models above: (i) competitive exclusion of
deer (when parasitism is infrequent but competitive
differences large); (ii) exclusion of moose (when parasite
virulence and transmission are high and competitive
differences small); (iii) stable or unstable coexistence of
moose and deer (for other combinations of these factors).
They conclude that although exclusion of moose is
theoretically possible, co-existence is equally likely, and
more robust estimates of parameters from empirical data are
required to predict the outcomes of this interaction.
Complexity in multiple host systems
The potential complexity of systems is illustrated by the tickborne louping ill virus in red grouse (Lagopus lagopus scoticus;
Fig. 2). The virus is amplified in grouse, in which it causes
substantial mortality. The virus is transmitted by a vector,
the sheep tick (Ixodes ricinus) which feeds on a range of
vertebrate species, but can only complete its lifecycle on
larger mammals; virus can also be transmitted nonviraemically by co-feeding of ticks on mountain hare (e.g.
Gilbert et al. 2001). On managed gamebird estates in upland
Britain, three types of host are relevant: Red deer (Cervus
Ó 2006 Blackwell Publishing Ltd/CNRS
Review and Synthesis
Tick
Louping ill
virus
+
–
+
Hare
–
0
(–)
–
Grouse
+
–
–
+
+
+
Sheep
Deer
Figure 2 Interaction web of the tick-borne louping ill virus and
hosts of the virus and tick vector (see Norman et al. 1999; Gilbert
et al. 2001). Grouse and sheep amplify the virus and suffer fitness
costs from infection; deer amplify the tick and hares amplify both.
Sheep are usually removed from the system via vaccination against
louping ill and use of accaricides. Hare–grouse communities can
support louping ill, with hare and grouse in apparent competition
via amplification of the tick and transmission of the virus to tick in
hares. Deer–grouse communities can support louping ill, with deer
and grouse in apparent competition via deer amplification of the
vector only. At high deer densities, the effect is reversed as deer
become a sink to the virus. In both cases the effects are
asymmetric, as there is no measurable cost to hares from the virus,
and little fitness cost to deer or hares of (low-density) tick
infestation.
elephus) amplify the tick but do not amplify virus; mountain
hares (Lepus timidus) amplify both tick and virus, and grouse
amplify the virus but not the tick. A combination of models
and empirical data have been used to investigate this system
(Norman et al. 1999; Gilbert et al. 2001). Because of the
asymmetries in vector/virus amplification, deer and grouse
alone cannot maintain the virus. But in combination, the
two host species can maintain viral infections. Likewise, the
virus can be maintained in a hare–grouse community and is
almost always maintained in the three-host species community. This system provides interesting insights into apparent
competition: firstly, in agreement with Chaneton & Bonsall
(2000), apparent competition can be asymmetric; for
example, in the deer–grouse community, grouse suffer from
apparent competition but deer do not. Secondly, vectors can
also cause apparent competition, as deer amplify vector but
not virus, but nevertheless their presence results in increased
mortality for grouse. Vector-mediated apparent competition
is also implicated in native/invasive grassland systems
infected with B/CYDVs; in California, the invasive annual
grass Avena fatua is more attractive to the aphid vectors and
supports larger colonies than the more susceptible native
perennial bunchgrass (Malmstrom et al. 2005). The louping
ill system also serves to demonstrate some issues relevant to
community composition. The suggestion from this system is
that more complex communities of hosts are more likely to
support a disease. This can be seen as an example of the
reservoir effect of alternative host species. From the
perspective of the grouse, hares and deer are reservoirs
for the vector and hares are also a reservoir for the virus. A
Review and Synthesis
similar situation exists in B/CYDV and grass systems:
A. fatua, a reservoir for the aphid vectors (Malmstrom et al.
2005), is also a reservoir for the virus (Power & Mitchell
2004). In experimental communities, these reservoir effects
resulted in large increases in pathogen prevalence in other
grass species when grown with infected A. fatua (Power &
Mitchell 2004). This had knock-on effects for community
composition via a combination of direct and pathogenmodified competition; adding BYDV reduced the competitive ability of A. fatua against a less susceptible grass, which
then excluded two competitively inferior species (Power &
Mitchell 2004).
In contrast to the reservoir effect, a dilution effect is
possible, whereby the addition of more host species reduces
the prevalence or likely persistence of a disease. This is also
illustrated by louping ill: very high densities of deer cause a
dilution effect because infected ticks are more likely to bite
deer, which do not transmit the infection, rather than
grouse. In another tick-transmitted infection in the USA,
Lyme disease (caused by the spirochaete Borrelia burgdorferi),
higher species richness of small terrestrial mammals results
in decreased disease risk as most of the mammals are
incompetent hosts (Ostfeld & Keesing 2000). The relationship between dilution and reservoir effects is reviewed by
Keesing et al. (2006), who make the point that the effect
seen will depend on whether the most competent reservoir
species is already present when a community undergoes
change. If the best reservoir is already present, increasing
species richness will result in dilution; if the current
community has relatively incompetent hosts, adding more
species, some of which are more competent hosts, will tend
to increase disease incidence. This pattern is borne out by
experimental manipulations of grassland communities
showing that reduced species richness tended to increase
foliar fungal pathogen load (Mitchell et al. 2002). Variation
in outcomes could be attributed to a combination of species
composition effects (pathogen load was higher in speciespoor communities provided the more susceptible grasses
were retained) and spatial effects on transmission (transmission of the more species-specific pathogens is more
efficient in dense stands).
To examine conditions for parasite establishment in twohost communities, Holt et al. (2003) develop a graphical
isocline approach where hosts are treated as resources. They
show how the criterion for parasite establishment depends
on a threshold community composition, an extension of the
concept of the threshold host population size for invasion.
The shape of the threshold depends on how the hosts
interact (e.g. with respect to parasite transmission), and
patterns analogous to resource-consumer isoclines are
produced. Although not providing quantitative predictions
for any particular system, this approach can be useful in
classifying and comparing different systems and could be
Parasite-modified interactions 1259
extended to communities with more host species. For
instance, Holt et al. (2003) observe that, of the many
possible isocline shapes, only one produces a dilution effect;
this shape is only possible for vector-borne diseases or those
with free-living infectious stages, bearing out the dilution
phenomena found for louping ill and Lyme disease. Recent
analyses by Dobson (2004) and Rudolf & Antonovics (2005)
incorporating frequency-dependent parasite transmission
(the likely form for vector-borne diseases) also find a
dilution effect. An interesting implication of these results is
that, in contrast to apparent competition models with
density-dependent transmission, frequency-dependent transmission can induce apparent mutualism (i.e. a ++ interaction between the host species; Abrams & Matsuda 1996),
whereby the presence of one host species enables
persistence of another host that would otherwise be driven
extinct by the parasite (Rudolf & Antonovics 2005). The
implications of this type of positive feedback for
biodiversity are potentially important: reduced biodiversity
could increase disease incidence, causing further extinctions
in a cascading process (Dobson 2004; Keesing et al. 2006).
Evidence for trait-mediated indirect effects
Classically, parasite-mediated apparent competition acts via
long-term density effects (Holt 1977), and the general
models considered here (Holt & Pickering 1985; Begon et al.
1992; Holt et al. 2003) reflect that mechanism. However, in a
community module context, parasite-induced modification
of competitive ability can be seen as a TMIE altering the
dominance relationship between competing species. This
would appear to be the mechanism underlying several of the
plant examples, where parasite-modified competition is
documented (Power & Mitchell 2004; Malmstrom et al.
2005). It is less clear whether parasite modification of
competition occurs between animal species, although it
appears to be a factor for isopods (Grosholz 1992) and may
play a role in the lizard (Schall 1992) and squirrel systems
(Tompkins et al. 2003). The most widely applicable general
population dynamic model for interspecific competition
(Bowers & Turner 1997) does not incorporate this effect
because parasitism only influences outcomes via its effects
on mortality (a density-mediated effect); a model of parasitemodified competition should, strictly speaking, incorporate
competition parameters that depend upon infection status.
Other potential TMIEs do exist in the animal systems:
parasite-induced effects on fecundity can be important and
have been included in some models (Yan 1996; Greenman
& Hudson 2000; Tompkins et al. 2000a); parasite-induced
changes in intermediate host behaviour are another example
(Schmitz & Nudds 1994). Other potential TMIEs arise in
vector-borne parasite systems generally, where vector
foraging behaviour may result in TMIEs common to many
Ó 2006 Blackwell Publishing Ltd/CNRS
1260 M. J. Hatcher, J. T. A. Dick and A. M. Dunn
other arthropod predators (such as a saturating functional
response). For predator–prey systems, these types of
short-term effect are known theoretically to result in
counter-intuitive dynamics that could counteract long-term
processes (Abrams & Matsuda 1996). It is interesting to
note that the model of frequency-dependent transmission
studied by Rudolf & Antonovics (2005) attributes to the
parasite many of the characteristics that are required by
Abrams & Matsuda (1996) to produce apparent mutualism,
and a similar outcome is found.
PARASITES AND PREDATORS
In real systems, parasites affect interactions between species
at the same and also at different trophic levels. Parasites may
impact predatory interactions in different ways, depending
on whether they infect the prey (Fig. 1d), the predator
(Fig. 1e), or both predator and prey (Fig. 1f). Anderson &
May (1986) examined two cases: parasite of prey only
(Fig. 1d) and parasite of predator only (Fig. 1e). They
assumed that a microparasite invades an established
predator–prey interaction, under a range of assumptions
for density dependence, immunity and fitness effects. When
parasites infect prey, if predators hold the prey population
below the threshold density for parasite invasion, the
parasite cannot spread. At the other extreme, the parasite
may regulate the host below the level required to sustain the
predator, in which case the predator is excluded via direct
competition with the parasite. Within these two limits, the
parasite, prey and predator coexist, in some cases with
oscillatory dynamics that would not have occurred in the
absence of the parasite. Similar outcomes are also found for
the case of a parasitoid and pathogen interacting with a
shared arthropod host species (Hochberg et al. 1990).
However, the situation is more complicated because dual
infections within a single host can occur, and the pathogen
and parasitoid can interact directly. Hochberg et al. (1990)
included interference competition between the pathogen
and parasitoid when infecting the same host individual, and
found a wide range of population dynamic outcomes.
Regulation of the host population by both enemies was
possible, but in some cases addition of the second enemy
had a destabilizing effect. Conditions enhancing regulation
included long-lived external pathogen propagules, roughly
symmetrical interference, and aggregated attack by both
enemies. At the other extreme, if attacks by both enemies
were distributed at random, introduction of a second enemy
increased host population size (Hochberg et al. 1990).
Dwyer et al. (2004) show how two enemies can have a
differential impact depending on prey density, resulting in
complex dynamics for the host. Their model was tailored to
forest Lepidoptera such as the gypsy moth Lymantria dispar
and their bacculovirus pathogens; periodic outbreaks of
Ó 2006 Blackwell Publishing Ltd/CNRS
Review and Synthesis
various moth species result in large-scale defoliation.
Previously, pathogens had been implicated as regulatory
factors, but parasite–host models failed to predict the
variable time between outbreaks of the moth. Predator–prey
models also failed to describe the dynamics, predicting
longer cycle times between outbreaks. However, generalist
predators and a specialist pathogen acting together can
explain variable periodic outbursts quite well (Dwyer et al.
2004): there is a low-density equilibrium where the predator
regulates the host and the pathogen is relatively unimportant, and a high-density equilibrium controlled by the
pathogen where the predator is relatively unimportant;
adding a small amount of environmental stochasticity drives
the trajectory unpredictably between the two.
Anderson & May (1986) also investigated a parasite
infecting the predator rather than the prey (Fig. 1e). In this
case, either the parasite cannot be maintained (if the
predator, in the absence of the parasite, is at a density lower
than the threshold for parasite invasion), or all three species
coexist (if the converse is true). As is the case for parasites
of prey interacting with predators, previously stable predator–prey dynamics may become oscillatory when a parasite
of the predator is introduced (Anderson & May 1986). A
recent analysis of population census data demonstrates this
effect and also shows that parasites can indirectly affect
population dynamics for the host and its prey even after the
disease outbreak has been extinguished (Wilmers et al.
2006). In the early 1980s, canine parvovirus (CPV) was
introduced to wolves (Canis lupus) in Isle Royale, USA,
resulting in a dramatic crash of the wolf population. Since
then, the population density of moose (Alces alces) has shown
increased variance with peaks and crashes characteristic of
populations relatively free from predation. Regulation of the
moose population appears to have shifted from top-down
(wolf) to bottom-up control, principally through climatic
effects on moose and their winter food resource (Wilmers
et al. 2006). That pathogen outbreaks may be responsible for
shifts in trophic control is an exciting advance that warrants
further empirical and theoretical attention. Furthermore,
these effects appear to be long-lasting; although CPV is no
longer present on Isle Royale, wolf and moose populations
remain in the post-1980s pattern, possibly because genetic
bottlenecks were generated by the crash and these prevent
recovery of the wolf population.
Short-term and trait-mediated indirect effects: empirical
evidence
Historically, emphasis has been placed on the role of
parasites in behavioural manipulation of prey intermediate
hosts thereby facilitating parasite transmission to the
predator definitive host (Moore 2002). These systems are
examples of the community module where the parasite
Review and Synthesis
infects both predator and prey (Fig. 1f). In a community
context, these parasite-induced behavioural changes can be
regarded as TMIEs that often result in increased exposure
of hosts to predation (Werner & Peacor 2003; Mouritsen &
Poulin 2005a). Although some changes in host behaviour
may be a by-product of infection, for others there is strong
evidence for adaptive manipulation by the parasite (Poulin
1995). For example, behavioural manipulation of the
intermediate amphipod host, Gammarus pulex, by the
acanthocephalan Polymorphus paradoxus coincides with
the infective stage of the parasite and increases predation
risk of the shrimps from the definitive duck hosts (Bethel &
Holmes 1977).
Cezilly & Perrot-Minnot (2005) review a number of
examples of trophically transmitted parasites where manipulation increases predation by both host and non-host
species. For example, although the definitive hosts of the
acanthocephalan Polymorphus minutus are aquatic birds,
P. minutus increased the susceptibility of G. pulex to fish
predators (Marriott et al. 1989). Decreased aggregation of
the tapeworm Echinococcus granulosus in wild moose populations under high levels of wolf predation indicates selective
predation on infected hosts (Joly & Messier 2004). Red
grouse killed by predators were found to have higher
burdens of the nematode Trichostrongylus tenuis, and predator
control lead to an increase in the numbers of heavily
infected birds, indicating that predators selectively prey on
infected birds (Hudson et al. 1992). In a direct test for
parasite-induced predation, field populations of voles
(Microtus townsendii) that were treated with anthelminthics
suffered a 17% reduction in predation in comparison with
untreated (infected) controls (Steen et al. 2002). Hence,
parasitic manipulation may affect predator–prey relationships beyond those involved in the life-cycle of the parasite,
producing TMIEs in modules such as that depicted in
Fig. 1d; indeed, most theoretical treatments of this problem
(described in the following section) examine systems in
which the predators are not part of the parasite lifecycle.
A series of field studies have demonstrated the wide
reaching effects of trematode-induced behavioural changes
in the cockle, Austrovenus stutchuryi (Mouritsen & Poulin
2003, 2005a,b). The trematode Curtuteria australis inhibits the
burrowing behaviour of infected cockles, thereby exposing
them to predation by the avian definitive host (Mouritsen &
Poulin 2003, 2005b). This effect also leads to increased nonlethal predation (foot cropping) of the cockles by fish
(Mouritsen & Poulin 2003). Changes in cockle zonation as a
result of the infection alter the distribution of anemones that
live on the cockles as well as the distribution of whelk and
limpet predators (Mouritsen & Poulin 2005b). Changes in
cockle burrowing lead to alterations in sediment structure,
an increase in the density of some species and an increase in
biodiversity in the intertidal zone, leading Mouritsen &
Parasite-modified interactions 1261
Poulin (2005a) to advocate this parasite as an Ôecosystem
engineerÕ.
Population dynamic and community consequences
Hudson et al. (1992) parameterized a mathematical model of
the grouse–nematode system (an example of Fig. 1d) to
examine the effects of predation. Predators were represented as a parameter (rather than having explicit equations to
represent population numbers), so this model is more
appropriate for long-lived or generalist predators whose
population dynamics are unlikely to be coupled to that of a
single host species. If predators were non-selective or
preferred infected individuals, increased predation reduced
mean parasite burden in the grouse population, resulting in a
reduction in the amplitude of oscillations in grouse
numbers. Hudson et al. (1992) argued that because selective
predation removes a disproportionate fraction of parasites,
it reduces the regulatory role of parasites (in this case,
reducing parasite-driven oscillations caused by delayed
density-dependent effects on host fecundity). In contrast,
Ives & Murray (1997) found that parasitism and predation
acting together increased oscillations in a model of
snowshoe hare (Lepus americanus) populations. They argued
that parasites tend to destabilize predator–prey dynamics as
adding parasites to a Lotka-Volterra predator–prey model
(here, predator dynamics were included) shifted damped
oscillations towards long-term cycles or diverging oscillations, mirroring the results of Anderson & May (1986).
There are a number of possible explanations for this
discrepancy, based on the different perspectives taken:
Hudson et al. (1998) add predators to a host–parasite system
where the parasites have a strong regulatory influence on the
host even in the absence of predation; Ives & Murray add
parasites to a predator–prey system where cycles in prey
numbers are thought to be largely driven by predation.
Importantly, the models differ in their treatment of shortterm effects; Hudson et al. concentrate on short-term
effects, considering the numerical response of predator
density to be independent of prey numbers (this is also a
feature of several other models discussed below); Ives &
Murray include long-term density-mediated effects via
predator population dynamics, both models include TMIEs
in the form of parasite-induced changes in fecundity and
vulnerability to predation.
Two general theoretical papers examine the problem
from these different perspectives with broadly consistent
results. Packer et al. (2003) examine the effect of predation
on host/parasite systems, in relation to strategies for
population management. They show that predator removal,
commonly regarded as a potential strategy for boosting prey
numbers, can harm host populations that are also subject to
parasitic infection; predator dynamics were not modelled
Ó 2006 Blackwell Publishing Ltd/CNRS
1262 M. J. Hatcher, J. T. A. Dick and A. M. Dunn
explicitly. For microparasites, they found that increased
predation always increases the abundance of healthy prey
and reduces the prevalence of infection. Surprisingly, this
occurs even if the predator is unselective. Selectivity is,
however, important in determining the consequences for
total population size (summing infected and uninfected
individuals): if predators select infected hosts, they are
predicted to increase total host population size; if they
prefer uninfected hosts they will reduce population size and
if they are unselective then total population size remains
unaltered. For macroparasites that have an aggregated
distribution among hosts, the effect is more extreme. Even
a low level of predation could in theory result in extinction
of the parasite if predators concentrate on infected prey.
Packer et al. observe that selective predation effectively
increases parasite-induced mortality, thus it tends to increase
the impact of parasitism as a stabilizing/regulatory force on
host populations. If predator removal boosts parasite
numbers, this can have implications for public health, as
many managed populations of mammals and birds harbour
zoonotic diseases (Ostfeld & Holt 2004). The alternative
approach was taken by Hethcote et al. (2004) who modified
a Lotka-Volterra type predator–prey model with a model for
microparasite infection of the prey. In some cases, the
greater vulnerability of infected prey can allow persistence
of a predator which would go extinct in the absence of
infection; in this model the infected prey provide an ÔeasyÕ
resource for the (otherwise too inefficient) predators to
exploit. Predation could also lead to extinction of a parasite
that could otherwise persist in its absence. Like Packer
et al.Õs result, this can occur even if predators are unselective:
predation reduces the host population below the threshold
density required to sustain infection (Anderson & May
1986).
A detailed investigation of the interplay between
predation and parasitism is presented in Hall et al. (2005).
They model predator behaviour assuming that predators
have a saturating (type II) functional response to prey
density, predator density was not modelled explicitly; this,
then, is a study of short-term indirect effects (and, arguably,
TMIEs; cf. Bolker et al. 2003; Werner & Peacor 2003). Once
a saturating response is included, predators that preferentially prey on infected hosts can introduce an Allee effect on
the parasite driving it extinct if it falls below a threshold
population size. Invading parasites not only require a
minimum host population size for invasion, they must also
exceed a critical propagule size of infected individuals.
Parasites are well-known theoretically (e.g. Anderson & May
1981, 1986) and empirically (Hudson et al. 1998) to drive
population oscillations in the absence of any other forces;
the addition of a predator with saturating functional
response can destabilize the system further with the result
that oscillations become catastrophic for the parasite if the
Ó 2006 Blackwell Publishing Ltd/CNRS
Review and Synthesis
Allee critical point is reached. If, on the other hand, the
predator is non-selective (or prefers uninfected hosts), the
combined forces of parasitism and predation acting in
synergy may drive the host to extinction. Why does a type II
functional response have these effects? A saturating
response means that although at high prey densities the
relative impact of predation is lower (compared with a linear
response), at low prey densities it is higher. This has a
destabilizing effect: regulation at high densities is weaker,
and at low densities the prey cannot recover from the
pressure of predation. Hall et al. suggest that these dynamics
might explain empirical observations of epidemic invasions
with very sudden crashes and apparent extinction after only
one or two oscillations. In many lakes in midwestern and
north-eastern USA, the bluegill sunfish Lepomis macrochirus
appears to control outbreaks of the bacterium Spirobacillus
cienkowskii in Daphnia dentifera. Bluegills preying on daphniids
exhibit a type II response and they prey selectively on
infected hosts, characteristics that can generate Allee effects
in the parasite. Epidemics occur in response to seasonal
decreases in fish predation but die out after only a single
oscillation (Duffy et al. 2005); if predation is sufficiently
intense and selective, invasion of the parasite into host
populations may be prevented (Duffy et al. 2005).
PLANT PATHOGENS/ENDOPHYTES AND
HERBIVORES
Plant pathogens can alter their host’s interactions with other
natural enemies, chief among them insect herbivores. There
are numerous empirical examples of negative (and some
positive) direct and indirect effects of pathogens on
phytophagous insects (reviewed in Hatcher 1995; Stout
et al. 2006), but the population dynamic and community
consequences of these interactions are less clear (Stout et al.
2006). One extensively studied system is that of dock
(Rumex spp.), attacked by the rust Uromyces rumicis and the
beetle Gastrophysa viridula. In laboratory manipulations, rust
infection of Rumex substantially reduced growth, survivorship and fecundity of the beetle (Hatcher et al. 1994). Field
and laboratory studies demonstrate that beetle grazing
induces resistance to infection by Uromyces and two other
fungal pathogens (Hatcher et al. 1994; Hatcher & Paul
2000). The existence of bidirectional inhibitory interactions
makes it difficult to predict the effect of combined attack by
multiple natural enemies on plants, a potentially important
strategy in biocontrol. Pathogen-induced deleterious effects
on insect herbivores are, in part, caused by reduced
nutritional quality (and, in some cases, quantity) of infected
plants. Another important mechanism mediating pathogen–
herbivore negative effects is that of induced defence:
although pathogens and herbivores may activate different
signalling pathways in the plants they attack, there is
Review and Synthesis
considerable overlap in responses such that plant responses
to pathogen infection confer some resistance to herbivory
and vice versa (reviewed in Hatcher et al. 2004; Stout et al.
2006).
Fungal endophytes also confer resistance to attack by
herbivores. Many fungal endophytes have limited (or no
demonstrable) direct negative effects on their hosts and are
generally considered to be mutualists; however, in many
cases the positive effects they impart on the host are
apparent only when the host interacts with members of
other species. Recent work suggests that endophyte-modified interspecific competition may have important consequences for community structure and ecosystem processes
(Rudgers et al. 2004). Endophyte-infected grasses have
higher alkaloid levels reducing plant nutritional quality and
making them less attractive to insect herbivores (Clay &
Schardl 2002). Such grasses may also support a lower
abundance of aphids, with knock-on effects at higher
trophic levels (Omacini et al. 2001). The combined effects of
endophytes on interspecific competition and herbivory can
alter the balance between trophic levels, implicating these
microbes in extensive trophic cascades. Laboratory experiments suggest that endophytes can reduce plant diversity
through dominance of endophyte-infected species in interspecific competition; this (together with the direct effects on
insect feeding) reduces phytophagous insect abundance,
resulting in reduced species richness of specialist predators
and parasitoids of insect herbivores (Omacini et al. 2001).
Field manipulations demonstrate reduced diversity in
endophyte-infected communities (Clay & Holah 1999;
Rudgers et al. 2004) and suggest that endophytes can also
affect the composition of the detritovore and generalist
predator assemblages (Lemons et al. 2005; Finkes et al.
2006). Pathogen and endophyte modification of plant
quality and defensive strategy, and modification of interspecific competitive ability, can all be regarded as TMIEs.
PARASITES AND INTRAGUILD PREDATORS
Intraguild predation is predation among species that are also
potential competitors (Polis et al. 1989; Holt & Polis 1997).
Recent analyses of real food webs indicate that IGP is
widespread and important in the structuring of communities
(Arim & Marquet 2004; Bascompte & Melian 2005). It often
occurs among closely related species and can be associated
with (and perhaps predicted from) a cannibalistic tendency
(see Polis et al. 1989; Dick et al. 1993), as the ability to kill
and consume conspecifics may easily transcribe into
predation on congenerics/confamilials (e.g. Dick et al.
1993). IGP appears to be particularly prevalent where
competing species have age or stage structure; smaller stage
classes are eaten by the larger classes of competing species
that consume the same general class of resource; in such
Parasite-modified interactions 1263
cases many species may be involved in IGP to varying
degrees (Polis & Holt 1992). Disparate taxa also engage in
IGP, as its definition extends to similarity of resources used
regardless of taxonomy or mode of resource acquisition
(Polis et al. 1989). For instance, pathogen–parasitoid interactions when both enemies attack the same host species,
and the pathogen also infects the parasitoid, can be regarded
as IGP (Rosenheim et al. 1995).
Intraguild predation can be asymmetric (i.e. A eats B
only), symmetric or mutual (i.e. A eats B, B eats A), or
mutual but with different strengths of interaction (Polis et al.
1989; Dick et al. 1993). Mathematical analyses have so far
mainly considered the dynamics and energetics of two
competing species with asymmetric IGP (the IG predator
and IG prey) and their shared resource (Polis et al. 1989;
Holt 1997; Holt & Polis 1997; Ruggieri & Schreiber 2005;
but see Dick et al. 1993; Dick & Platvoet 1996 where mutual
IGP is included). Theory predicts that IGP can produce
complex patterns of population dynamics including oscillations and stable equilibria with species exclusion,
co-existence or alternative stable states (Holt & Polis
1997; Ruggieri & Schreiber 2005). Outcomes depend on
the relative strength of IGP, and the relative efficiency of
exploitation of the basal resource by the competitors; for
IGP to persist, the IG prey must be a more efficient utilizer
of the shared resource than the IG predator (Holt & Polis
1997). The existence of alternative stable states implies that
the eventual outcome depends on initial conditions such as
the order of arrival of species or their initial propagule size;
this might translate into patchwork distributions of particular IGP assemblages within structured habitats (Polis &
Holt 1992).
Theory predicts that IGP can reverse the outcomes
predicted for simple (linear) food chains (Polis & Holt 1992;
Holt & Polis 1997). For instance, in a trophic cascade, an
increase in top predator numbers decreases intermediate
predator densities, allowing herbivores to increase, which
depresses plant biomass. Adding IGP can prevent the
cascade or even reverse it, such that top predators have a
positive impact on plants via their effect on herbivores
(Polis et al. 1989; Polis & Holt 1992). IGP can be disruptive
in biological control, as target prey may be ÔreleasedÕ from
predation due to IGP among bio-control species (Müller &
Brodeur 2002), but it can also be an important factor in
conservation, controlling ÔmesopredatorsÕ that are otherwise
detrimental to prey populations (Müller & Brodeur 2002).
Whilst IGP gains currency as an important factor in
community structure, the role of parasites in mediating IGP
has received less attention (Fig. 1g). This is important as all
the direct and indirect effects of IGP as reviewed above may
be changed by parasite modification of IGP interaction
strength. The same features of hosts that make them
vulnerable to behavioural manipulation by parasites may
Ó 2006 Blackwell Publishing Ltd/CNRS
1264 M. J. Hatcher, J. T. A. Dick and A. M. Dunn
Review and Synthesis
render such hosts more susceptible to intraguild predators.
Parasite-induced effects on host condition, behaviour or
habitat use could, in principle, alter either the prey or
predatory aspects of IGP relationships, whether or not the
parasite is actually shared between species. Two species of
parasite have been shown to influence both the prey and
predatory components of IGP in a guild of native and
invasive amphipods (MacNeil et al. 2003a,b). The freshwaters of Ireland have been invaded by three amphipod
species: Gammarus pulex from mainland Europe and the
North American G. tigrinus and Crangonyx pseudogracilis. The
invaders have excluded the native G. duebeni celticus from
some sites, but in others, natives and invaders co-exist
(MacNeil et al. 2003a). Gammarus d. celticus sits midway in a
hierarchy of IGP with the invading species (Fig. 3). Field
and laboratory experiments show that parasitism alters the
hierarchy of IGP and therefore has the capacity to affect the
outcome of invasions. Infection by the microsporidian
Pleistophora mulleri had no direct effect on the survival of the
native G. d. celticus, but infected adults showed a reduced
capacity to prey on the smaller species G. tigrinus and
C. pseudogracilis and an increased vulnerability to predation by
+
Parasite:
E. truttae
–
Salmo
trutta
–
+
+
Parasite:
P. mulleri
–
–
–
G. pulex
+
–
G. d. celticus
+
–
+
+
+
+
–
–
–
–
+
+
G. tigrinus
–
+
–
+
BIOLOGICAL INVASIONS
C. pseudogracilis
– +
Macroinvertebrates (predation & scavenge), leaf litter
Figure 3 Interaction web of native and invading Gammarus spp.
(see MacNeil et al. 2003a,b). Shown are four amphipod species that
engage in IGP; their common resource base; two parasite species
of gammarids (the microsporidian, P. mulleri, has a direct lifecycle
whereas the acanthocephalan, E. truttae, uses brown trout Salmo
trutta as its definitive host); and a top predator of gammarids
(S. trutta). Not shown are other top predators without direct links to
these parasites or other guild members that do not participate in
IGP with gammarids. Also not shown are probable links between
E. truttae to G. d. celticus and cannibalistic interactions, which occur
within each amphipod species and are also be modified by
parasitism (MacNeil et al. 2003c). Indirect interactions include:
P. mulleri-mediated IGP between (G. pulex, G. d. celticus) and
(G. d. celticus, G. tigrinus); E. truttae-mediated IGP between (G. pulex
and G. d. celticus); behavioural manipulation of G. pulex to enhance
transmission of E. truttae to S. trutta is also documented.
Ó 2006 Blackwell Publishing Ltd/CNRS
G. pulex, none of which are prone to this infection (MacNeil
et al. 2003a). A second parasite, the acanthocephalan
Echinorynchus truttae is more prevalent in the invader
Gammarus pulex than in the native G. d. celticus. Here,
infection reduces predation by G. pulex on G. d. celticus and
may therefore slow the invasion or promote coexistence of
these amphipods (MacNeil et al. 2003b). Parasitism also
alters inter-guild predation (Fielding et al. 2003) and
cannibalistic interactions (MacNeil et al. 2003c) in this
system. All the parasite-induced effects measured in this
system are short-term (sensu Holt & Kotler 1987; Abrams
1992) and can be seen as TMIEs.
Several recent papers investigating apparent competition
speculate that parasite-mediated IGP might be important
and clearly more work is needed to study this directly
(Hoogendoorn & Heimpel 2002; Juliano & Lounibos 2005).
For example, in a laboratory study, Yan et al. (1998)
investigated the effect of the tapeworm Hymenolepis diminuta
on competition between Tribolium casteneum and T. confusum.
Tribolium casteneum, the stronger competitor, suffers higher
infection and fitness costs from parasitism and thus the
parasite should be expected to reverse the outcome of
competition. However, the reverse occurred with a faster
exclusion of T. confusum than occurred in the absence of
infection. The authors suggested that parasite-induced
changes in surface seeking behaviour might lead to higher
levels of IGP by T. casteneum. This is a fruitful area for
further research, particularly where IGP systems have been
well studied but parasites largely ignored; in this respect,
well-characterized systems, such as Park’s (1948) and Park
et al.Õs (1965) Tribolium competition/cannibalistic predation
experiments, may need to be revisited.
Many empirical examples of parasites and pathogens
changing the outcome of host–host interactions have been
observed during the process of biological invasion
(e.g. Bauer et al. 2000; Aliabadi & Juliano 2002; MacNeil
et al. 2003a,b; Tompkins et al. 2003; Prenter et al. 2004;
Malmstrom et al. 2005). Indeed, ongoing invasions represent
natural experiments in which to study the effect of novel
and endemic parasites on species interactions. Through their
impact on host interactions, parasites can play a key role in
determining the success of an invasion. A review of
empirical studies by de Castro & Bolker (2005) finds strong
evidence for parasite-induced extinction of one species
(usually a native species replaced by an introduced exotic) as
a result of the reservoir effects of apparent competition.
Invaders may lose their natural enemies (including
parasites) through stochastic or selective processes, and this
Ôenemy releaseÕ may be an important factor driving the
success of introduced species (Torchin et al. 2003; Torchin
Review and Synthesis
& Mitchell 2004; but see Colautti et al. 2005). A metaanalysis of 473 plant species naturalized to the United States
from Europe demonstrated that they have, on average, 84%
fewer fungal pathogens and 24% fewer virus species than
those from the native range, and those species with greater
release from enemies were more likely to be reported as
harmful invaders (Mitchell & Power 2003). The invasive
European green crab Carcinus maenas experiences greatly
reduced parasite diversity and prevalence in the invasive
range and the greater biomass in invasive populations has
been attributed to enemy release (Torchin et al. 2001).
Several amphipod species have invaded British Isles waters
and these invaders enjoy a lower diversity, prevalence and
burden of parasites than does the native amphipod
Gammarus d. celticus (Prenter et al. 2004). Infection of the
native amphipod G. d. celticus with the microsporidian
P. mulleri increases its vulnerability to invasions by amphipod
species that are not host to this parasite (MacNeil et al.
2003a; detailed in previous section). However, invaders do
not always benefit from enemy release and, in the same
system, the shared acanthocephalan parasite E. truttae is
more prevalent in the invading G. pulex causing a reduction
in its predatory abilities and slowing invasion and replacement (MacNeil et al. 2003b). For plants, the impact of
invasive species appears to be a function of release from
enemies of the native range and accumulation of novel
enemies in their naturalized range (Mitchell & Power 2003).
In addition, the net effect of multiple enemies is likely to be
temporally and spatially variable, with little correspondence
between escape from different enemies, creating Ôinvasion
opportunity windowsÕ for introduced species (Agrawal et al.
2005).
Parasites that invade with their hosts or vectors experience opportunities for transmission to new species. For
example, in New Zealand, introduction and range expansion
of exotic mosquitoes is likely to increase incidence of avian
malaria, threatening native birds (Tompkins & Poulin 2006).
The parapox virus introduced to the UK with the grey
squirrel is highly virulent to the native red squirrel and is an
important factor in its decline (Tompkins et al. 2003).
Similarly, extinction of populations of the native UK White
Clawed crayfish, Austropotamobius pallipes has been attributed
to crayfish plague (Aphanomyces astaci). This fungus is
thought to have been introduced with the invader Pacifastacus leniusculus in the 1970s. The parasite is widespread in
P. leniusculus where it is rarely lethal, but it can cause high
mortality in A. pallipes (Holdich 2003). That the disease is
more virulent in the native may be an evolutionary accident
and hence intrinsically unpredictable. Alternatively, tests of
local adaptation may be important in predicting the likely
impact of shared parasites on invasions. For example, the
acanthocephalan parasite Pomphorhynchus laevis is shared by
both the native amphipod Gammarus pulex and the invading
Parasite-modified interactions 1265
G. roeseli in rivers in France. Whilst the parasite induces
photophilic behaviour in G. duebeni, it does not alter
phototaxis in the recent invader, probably reflecting their
short coevolutionary history (Bauer et al. 2000). The absence
of behavioural manipulation is likely to lead to less intense
predation of the invader and may therefore facilitate
coexistence with or even exclusion of the native amphipod.
Parasites may determine the speed of invasion, as seen in
the case of red squirrel replacement by greys (Rushton et al.
2000; Tompkins et al. 2003). This is particularly likely where
ÔstrongÕ interactions that result in rapid ecological change,
such as those involving IGP, are concerned. IGP tends to
destabilize interactions between competitors; this can drive
one species extinct faster or over more of the parameter
space than predicted for exploitative competition alone
(Polis et al. 1989; Dick et al. 1993). Classic traits that are
measured as evidence of interspecific competition, such as
growth and fecundity, may have no time to respond
measurably before species exclusion as a result of faster
processes such as IGP. For example, IGP among amphipods can lead to eliminations of the inferior IGP participant
in weeks/months (Dick & Platvoet 2000), with the lifespans
of animals measured in months/years. Some studies (e.g.
Polis et al. 1989; Yasuda et al. 2004) show IGP to be a
powerful interspecific interaction, but competitive effects to
be minimal or absent. Thus, models of IGP and its parasite
mediation may be realistic when excluding competitive
effects because competition may not have the time or
strength to manifest. Indeed, Dick et al. (1993) and Dick &
Platvoet (1996) showed theoretically that even a heavy bias
in favour of the competitive ability of an inferior IGP
participant could not overturn the superior IGP abilities of
the inferior competitor, leading to exclusion of the inferior
IGP participant. Short-term experiments examining IGP
have been criticized for ignoring alternative resources
(Briggs & Borer 2005), however, they may be appropriate
in the situations above where competition is of little
consequence.
FUTURE CHALLENGES
Mathematical tractability
With the addition of more species or more realistic lifehistory assumptions, many models of apparent competition
are analytically intractable, so a complete characterization of
the system is not possible (Hudson & Greenman 1998).
Most of the analyses use simulation to explore the model
(some with mathematical proof for particular cases), and
sometimes, despite extensive exploration of the parameter
space, interesting behaviours are missed (Greenman &
Hudson 1999). A more complete analysis requires the
application of bifurcation theory or related mathematical
Ó 2006 Blackwell Publishing Ltd/CNRS
1266 M. J. Hatcher, J. T. A. Dick and A. M. Dunn
techniques (Hudson & Greenman 1998; Greenman &
Hudson 1999). The message from these analyses is that a
great range of system behaviours is possible. Some
parameter combinations can have alternative stable states,
making quantitative prediction about system behaviour
problematic. There has recently been a move to simplify
the mathematics in order to obtain some general patterns
(Holt et al. 2003). A promising alternative approach that
circumvents the intractability of population dynamics for
multiple species is to use techniques from network theory to
analyse real food webs (reviewed in Proulx et al. 2005). This
can provide a useful test of hypotheses about the relative
contribution of processes at lower scales (such as modulelevel processes) in structuring food webs (for example, Arim
& Marquet 2004; Bascompte & Melian 2005).
Parasite-modified IGP
Emerging from our review of this area there is a clear need
for focused studies of the impact of parasitism on IGP and
its outcomes for the community. There are only two
documented cases of parasite-modified IGP (MacNeil et al.
2003a,b) and both provide evidence that parasitism can alter
IGP and hence community structure. There are also several
tantalizing speculations in the literature that demand further
study (Yan et al. 1998; Hoogendoorn & Heimpel 2002;
Juliano & Lounibos 2005) as well as studies that need to be
revisited (e.g. Park 1948; Park et al. 1965). Interestingly, two
recent food web analyses both find evidence for the
importance of apparent competition and IGP in structuring
communities (Bascompte & Melian 2005; van Veen et al.
2006). To our knowledge, theory for parasite-modified IGP
has yet to be developed. There may be problems with theory
tractability for IGP/parasite or predator/parasite/competitor models, although we may be able to make some
simplifying assumptions by ignoring ÔslowerÕ processes (in
this case, interspecific competition, as discussed above).
Development of theory should parallel the empirical study
of parasite-modified IGP in these systems.
Review and Synthesis
1977; Holt & Lawton 1993), although this pattern does not
always prevail (Bonsall & Holt 2003). Anthropogenic
alteration of resources may have knock-on effects on the
community via parasitism. For instance, cultural eutrophication is implicated in increased parasitism by the flatworm,
Ribeiroia ondatrae, in US amphibians via a predator-mediated
shift in the planorbid snail intermediate hosts (Johnson &
Chase 2004).
Population structure
Parasite/host and predator/prey dynamics and coexistence
are well known to be contingent on spatiality. However,
most of the models discussed in this review do not explicitly
consider population structure and there is a need for greater
incorporation of spatial structure in order to examine a
number of issues ranging from the population dynamic
consequences of TMIEs to the evolution of disease
emergence in novel hosts. Metapopulation models of
predators and parasitoids have been developed for apparent
competition scenarios; habitat structure offers opportunity
for refugia from a shared enemy which can promote
coexistence (e.g. Holt & Lawton 1993, 1994; Bonsall &
Hassell 2000). On an evolutionary timescale, however,
structured populations may be subject to inter-demic
selection which can complicate outcomes (see below). In a
spatial context, parasite-modified or apparent competition
can translate into range limitation as the negative impact of
parasitism drives species extinct at the limits of their range
(Case et al. 2005). Wodarz & Sasaki (2004), in a model of
competing species each harbouring a parasite lethal to its
competitor, showed that the parasites could enforce species
boundaries, creating zones where a competitor cannot
invade because of encounter with the lethal parasite.
MacNeil et al. (2004) show that the prevalence of microsporidian infection in the native G. d. celticus is heterogenous
across habitat patches; models demonstrated a ÔbridgeheadÕ
effect, whereby the invasive G. pulex could succeed by first
replacing natives in infected patches; invasion would not
succeed in a homogenous environment.
Inclusion of resource base
This is important for our understanding of IGP (Holt 1997;
Holt & Polis 1997; Briggs & Borer 2005), and for apparent
competition (Holt 1997; Bonsall & Holt 2003). Most of the
models considered in this review do not explicitly include
resources, although Hall et al. (2005) examined the impact of
productivity (by changing prey carrying capacity) in a
predator–parasite–prey system. They showed that high
productivity could destabilize the system as parasites
overexploit the host resource causing oscillations that
predators exacerbate. This mirrors the Ôparadox of enrichmentÕ predicted in other simple community modules (Holt
Ó 2006 Blackwell Publishing Ltd/CNRS
Evolutionary perspective
There is a paucity of work examining parasite-mediated
multi-species interactions over an evolutionary timescale.
Theoretical bases including host–parasite local adaptation
and predator–prey/host–parasite arms races extended to
three-species interactions should prove fruitful. Choo et al.
(2003) show that including predation can have counterintuitive effects on the evolution of virulence. Brown &
Hastings (2003) analyse apparent competition in an
evolutionary context. For a plant species sharing a disease
with a superior competitor, selection favours lower disease
Review and Synthesis
resistance when pathogen transmission is spatially local thus
enhancing its negative impact on the competitor. Similarly,
Wodarz & Sasaki (2004) find that evolutionary outcomes for
parasite-mediated apparent competition depend on the
relative strengths of within- and between-population
selection; for instance, selection on the host can favour
reduced recovery time even though possession of the
parasite provides a weapon against competitors. Empirical
evidence suggests that, in biological invasions, local adaptation of the parasite to its native host may increase
(Tompkins et al. 2003) or decrease (Bauer et al. 2000) its
impact on novel hosts. More work is needed on the
relationship between parasite transmission strategies, virulence and trophic interactions. Many parasites with complex
life-cycles require predation, IGP or a vector for transmission between host species. IGP might also provide
opportunities for disease transmission that could benefit
generalist parasites. However, a high risk of infection could
select for a reduction of IGP in potential hosts or for
selective predation on uninfected hosts. During biological
invasions, IGP might provide opportunities for the infection of new species of host, with the outcome dependent on
the specificity of the parasite. It is interesting to note that,
although P. mulleri is transmitted between G. d. celticus hosts
via cannibalism, IGP of infected individuals did not lead to
infection in any of the three sympatric invading gammarids
(MacNeil et al. 2003a). Grosholz (1992) observed that
P. scaber suffered higher parasite prevalence when in competition with P. laevis than in single species populations and
suggested that intraguild aggression over food could provide
a transmission route for the virus through the haemocoele.
Emerging diseases
Both management strategies such as predator removal and
changes in biodiversity have implications for public health
where species that are zoonotic disease reservoirs are
concerned (Ostfeld & Keesing 2000; Packer et al. 2003;
Ostfeld & Holt 2004; Collinge & Ray 2006). Increasing
numbers of emerging infectious diseases of humans and
wildlife appear to be associated with increased levels of
anthropogenic change including human population expansion into wildlife habitat, intensive husbandry of domesticated species and introductions of exotic species and/or
their pathogens (Daszak et al. 2000). Spillover of pathogens
from reservoir populations (often managed domestic stock
or introduced species) to native wildlife is a major threat to
biodiversity (de Castro & Bolker 2005) and spill-back from
wildlife to crops and managed stock has clear economic and
public health costs (Daszak et al. 2000; Power & Mitchell
2004). In this context, there is increasing need to understand
how trophic interactions affect the evolution of parasite
transmission strategies and virulence (and vice versa).
Parasite-modified interactions 1267
Dennehy et al. (2006) examine the evolution of disease
emergence in novel hosts; while adaptations to the new host
undergo natural selection, the native host acts as a source
and the novel host a sink for the disease. Emergence will
therefore require periodic exposure to the native host whilst
adaptations evolve and have time to be selected.
CONCLUSIONS
From a community perspective, it is clear that we have more
information about the potential role parasites play in some
modules than in others. Apparent competition (Fig. 1a,b) is
relatively well-studied, both empirically and theoretically.
However, to our knowledge there is no general theoretical
treatment of parasite-modified competition, or how it might
interact with apparent competition. More work is also
needed empirically, especially in animal systems, on the
extent to which parasites do modify competition interaction
strengths. Of the predator–prey modules, there are several
thorough combined theory and empirical studies of parasites
of prey only (Fig. 1d), but few theoretical treatments of
Fig. 1f, where both predator and prey are host to the
parasite. This module is of particular interest with regard to
behaviourally mediated interactions, which we know from
the studies of module 1d to have potentially strong
influences. The role of parasites in IGP (Fig. 1g) is also
understudied, theoretically and empirically. Equally, within
modules, there is the potential for a great range of
population dynamic or community outcomes (for instance,
for Fig. 1a, compare short vs. long-term apparent competition; or for Fig. 1d compare the effects of animal parasites,
plant pathogens and endophytes). Hence, if we are to
determine the effects of parasites within whole communities, we need more information about the relative frequency
of these different modules and the types and strengths of
interactions within them.
The addition of parasites within modules, or as links
between modules, might be key to understanding some
outstanding problems in community ecology. For instance, a
recurring theme in IGP theory is the observation that in
many instances, IGP should be unstable (Polis & Holt 1992;
Holt 1997); despite this, IGP appears to be a frequent
component in many ecosystems (Polis et al. 1989; Bascompte & Melian 2005). Another frequently cited problem in
studies of apparent competition concerns the continued
coexistence of both the prey species; in predator- or
parasitoid-driven systems one prey species should, theoretically, be excluded (Holt 1977). Spatial structure is likely to
be important in explaining these discrepancies (Bonsall &
Hassell 2000). Alternatively, interactions between modules
might explain persistence in these cases; one way in which
modules can be linked is via shared parasitism. Parasite
diversity within trophic levels is also likely to be important
Ó 2006 Blackwell Publishing Ltd/CNRS
1268 M. J. Hatcher, J. T. A. Dick and A. M. Dunn
(Memmott et al. 2000; Lafferty et al. 2006). Most species are
host to numerous parasite species and how this diversity is
maintained, and its consequences for community structure,
is as yet poorly understood (Holt & Dobson 2006). A
combination of theoretical and empirical approaches is
required to examine how parasite interactions within and
between modules scale up to community-level processes.
The concluding message of Anderson & May (1986), namely
that we need quantitative data on many population
parameters in order to assess the effects of parasites on
communities, remains salient today. Indeed, with increasing
pressures on biodiversity and anthropogenic influences on
the environment and species introductions, the need to
understand how parasites affect communities has never
been greater.
ACKNOWLEDGEMENTS
The authors acknowledge a NERC UK PopNet grant to
A.M. Dunn, M.J. Hatcher & C. Thomas (ÔThe role of
parasitism in invasion dynamics and community processesÕ).
For valuable discussion we are very grateful to Calum
MacNeil and all our other co-authors on the NERC grant
GR3/12871, and to Chris Thomas and others involved in
the PopNet project. This manuscript was much improved
by the thought-provoking and insightful comments of three
anonymous referees and the helpful suggestions of the
Editors. We would also like to thank Paul Hatcher and Chris
Tofts for useful input and James & Jennifer Hatcher and
Ethan Dunn for developing our understanding of withinfamily parasite-mediated interactions.
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Editor, Michael Hochberg
Manuscript received 16 March 2006
First decision made 26 April 2006
Second decision made 10 July 2006
Manuscript accepted 14 July 2006
Ó 2006 Blackwell Publishing Ltd/CNRS