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