robbielrichards@gmail.com
Keywords: predator, parasite, disease ecology, healthy herds hypothesis,
meta-analysis, trophic interaction
Statement of authorship: RLR, JMD, and VOE conceived of the
study. RLR performed literature search, collected and analyzed data, and
wrote the first draft of publication. All authors contributed
substantially to revisions.
Data accessibility statement: Data and code used in these
analyses will be published on figshare upon acceptance of the manuscript
and a do will be included in the article. Prior to acceptance data and
code can be accessed at this private figshare link:https://figshare.com/s/ae13262817c42e4e82d9
Abstract: 149 Words
Main Text: 4314 Words
Number of figures: 3
Number of Tables: 3
Number of References: 53
ABSTRACT
Ecological theory suggests that predators should keep prey populations
healthy by reducing parasite burdens. However, empirical studies show
that predators often have minimal effects on, or even increase,
parasitism in prey. To quantify the overall magnitude and direction of
the effect of predation on parasitism in prey, we conducted a
meta-analysis of 48 empirical studies. We also examined how key
attributes of these studies, including parasite type, study design, and
predator interaction type (consumptive vs. non-consumptive) contributed
to variation in the predator-prey-parasite interaction. We found that
the overall effect of predation on parasitism differed between parasites
and parasitoids and that predator interaction type, and whether a
predator was a non-host spreader of parasites were the most important
traits predicting the parasite response. Our results suggest that the
mechanistic basis of predator-prey interactions strongly influences the
effects of predators on parasites and that these effects, while context
dependent, are predictable.
INTRODUCTION
Organisms navigate a complex set of interspecific interactions, among
the most important of these being victimization by natural enemies. Both
predators (Krebset al. 1995, 2018) and parasites
(Hudson et al.1992b; Tompkins & Begon 1999) can affect the population demography and
dynamics of the species they attack. However, few organisms are victim
to only a single natural enemy. Competition between predators of a
single prey population
(Holt & Lawton 1994;
Holt & Polis 1997; Tallian et al. 2017) and between parasites
within a single host organism
(Pedersen & Fenton
2007; Jolles et al. 2008; Ezenwa & Jolles 2011) have both been
studied for the effects that these interactions have on natural enemy
and victim populations. But predators and parasites of a single victim
population also interact in a variety of potentially important ways.
Parasites may weaken their hosts, making them easier to catch and
consume (Hudsonet al. 1992a; Moore 2002), while the killing and consuming of
prey by predators also kills parasites
(Hatcher et al.2006; Borer et al. 2007), except when the predator itself
becomes the next host
(Lafferty 1999; Kuris
2003; Logiudice 2003). Therefore, like other natural enemy
interactions, interactions between predators and parasites are important
to understanding the dynamics of natural populations.
Ecologists have long recognized the importance of predator-prey-parasite
interactions (Hudsonet al. 1992a). Among the most influential hypotheses about the
consequences of predator-prey-parasite interactions is
Packer et al.(2003)’s prediction, based on a mathematical model, that predators
reduce parasitism in their prey. This Healthy Herds Hypothesis (HHH)
phenomenon might be produced by multiple mechanisms. First, predators
directly, and often preferentially, kill infected individuals,
decreasing the number of infected individuals in the population. Second,
predators often reduce prey population sizes, which can decrease the
spread of parasites with density dependent transmission. Empirical
studies have tested the underlying predictions of the HHH in a variety
of systems, but results are conflicting. Some studies show a strong
negative effect of predators on parasites, while others show strong
positive effects. For example, experimentally increased bird predation
on lizard hatchlings (Acanthodactylus beershebensis ) decreased
parasitic trombiculid mite loads in the lizards
(Hawlena et al.2010), while sunfish (Lepomis gibbosus ) predators introduced
into tanks with infected tadpoles (Lithobates spp. ), increased
trematode cercarial load in tadpole prey
(Szuroczki &
Richardson 2012). Interestingly, these empirical studies differ along
multiple axes, including the transmission traits of the parasite
(Holt & Roy 2007; Roy
& Holt 2008) and the type of predator or predatory interaction
manipulated (Cácereset al. 2009; Strauss et al. 2016; Duffy et al.2019) which may help explain the variation in outcomes. While early
syntheses of the literature on predator-prey-parasite interactions
argued
for
the importance of predators in disease ecology and human health (Ostfeld
and Holt 2004) and contextualized these interactions within the broader
landscape of ecological interactions (Hatcheret al. 2006),
more recently, Duffy et al. (2019) laid out a framework of eight
different types of mechanisms by which predators may influence
parasitism in prey, all of which can result in either increases or
decreases in parasitism under different circumstances. We draw on this
framework, along with additional theoretical and empirical work to
establish hypotheses about the effect of parasite and interaction type
on predator-prey-parasite interactions.
We conducted a meta-analysis to quantify the overall magnitude and
direction of the effect of predation on parasitism, providing a
synthesis of the empirical work on this topic. We also tested the
prediction that differences among studies explain variation in observed
parasite responses along two key axes: (i) parasite type, and (ii) type
of predatory interaction. Specifically, we predicted that effects of
predators on macroparasites and parasitoids would be more negative than
effects on microparasites, because macroparasites and parasitoids tend
to be highly aggregated among hosts and spatial locations
(Hassell 1982; Chesson
& Murdoch 1986; Shaw & Dobson 1995) allowing small amounts of
selective predation to nearly eliminate parasite populations.
Parasitoids in particular have free-living adult stages which may fall
prey to or avoid predators of their hosts
(Heimpel et al.1997; Brodeur & Rosenheim 2000). In this way, predation should
necessarily affect parasitoids via a wider range of mechanisms than
other parasites, including selective predation, shifts in community
structure, and behavioral effects on the parasitoids themselves (Duffyet al. 2019). We also predicted that consumptive predatory
interactions would have more negative effects on parasites than
non-consumptive interactions, except when consumptive effects facilitate
parasite spread. In this case, consumptive interactions should actually
increase parasitism. The HHH predicts that, on average, consumptive
interactions decrease parasitism because infected individuals are
removed from populations
(Packer et al.2003). However, this average effect of consumption on parasites should
not apply in all circumstances and, in fact, more recent work suggests
that all consumptive mechanisms can potentially increase parasitism
under the right circumstances.
(Duffy et al.2019). In particular, “predator-spreaders,” which, although they
cannot become infected, may facilitate the spread of parasites from
their prey items by dispersing infectious agents more widely
(Cáceres et al.2009). On the other hand, non-consumptive interactions can alter prey
movement and space use behavior
(Brown et al.1988; Spieler 2003; Jones & Dornhaus 2011; Creel et al. 2014)
in ways that predictably increase or decrease parasite transmission
(Ezenwa 2004;
Patterson & Ruckstuhl 2013, Duffy et al. 2019). Given that consumptive
interactions likely also have context dependent effects (Duffy et al.
2019), predicting how consumptive and non-consumptive effects differ on
average is challenging. However, based on the range of examples of
non-consumptive interactions increasing parasitism, we predict that the
effects of non-consumptive interactions on parasites should be less
consistently negative than those of consumptive interactions.
While multiple syntheses of predator-prey-parasite interactions have
been published over the past 20 years
(Ostfeld & Holt 2004;
Hatcher et al. 2006; Duffy et al. 2019), these studies
take a qualitative approach while here we use an approach that
explicitly quantifies the typical effect of predators on parasites in
their prey and the most important drivers of variation in this response.
Here we ask: (i) what is the average overall effect of predators on
parasites in their prey and (ii) does this effect vary by parasite or
interaction type? We expect to find a negative overall effect of
predation on parasitism, but this effect should be more negative for
macroparasites and parasitoids than microparasites and for interactions
involving consumptive than non-consumptive interactions. We also expect
that consumptive interactions involving identified
“predator-spreaders” should have more positive effects than those with
non-spreaders.
MATERIALS AND METHODS