Unhealthy herds and the predator spreader: understanding when predation increases disease incidence and prevalence
Robert L. Richards1*, Bret D. Elderd1, and Meghan A. Duffy2
1 Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana, USA
2 Department of Ecology & Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA
* Correspondence: Robert L. Richards, Louisiana State University, Baton Rouge, LA, USA; email:robbielrichards@gmail.com
ORCID:
Richards: 0000-0003-4131-2732
Elderd: 0000-0001-5853-1136 Duffy: 0000-0002-8142-0802
Article type: Perspective
Running title: Unhealthy herds and the predator spreader
Keywords: healthy herds, predator-spreader, tritrophic interaction, predator-prey-parasite interactions, predator-host-parasite interactions, pathogen, parasitoid
# of words in Abstract: 200
# of words in Main Text: 5924
# of words in Text box 1: 416
# of words in Text box 2: 309
# of words in Text box 3: 660
# of words in Text box 4: 463
# of References: 123
# of Figures, Tables and Text boxes: 7
Statement of authorship: RLR, MAD, and BDE conceived of this review. RLR wrote the first draft of the manuscript. All authors contributed substantially to revisions.
Data accessibility statement: This article contains no data.
Abstract
Disease ecologists now recognize the limitation behind examining host-parasite interactions in isolation: community members – especially predators – dramatically affect host-parasite dynamics. Although the initial paradigm was that predation should reduce disease in prey populations (“healthy herds hypothesis”), researchers have realized that predators sometimes increase disease in their prey. These “predator-spreaders” are now recognized as critical to disease dynamics, but empirical research on the topic remains fragmented. In a narrow sense, a “predator-spreader” would be defined as a predator that mechanically spreads parasites via feeding. However, predators affect their prey and, subsequently, disease transmission in many other ways such as altering prey population structure, behavior, and physiology. We review the existing evidence for these mechanisms and provide heuristics that incorporate features of the host, predator, parasite, and environment to understand whether or not a predator is likely to be a predator-spreader. We also provide guidance for targeted study of each mechanism and quantifying the effects of predators on parasitism in a way that yields more general insights into the factors that promote predator-spreading. We aim to offer a better understanding of this important and underappreciated interaction and a path towards being able to predict how changes in predation will influence parasite dynamics.
Introduction
Because food web members can dramatically impact host-parasite dynamics through a wide variety of mechanisms, disease ecologists now recognize the limitation of examining host-parasite interactions in isolation. This potential for food web members to alter host-parasite dynamics is central to the healthy herds hypothesis, which posits that predators can substantially decrease parasitism in their prey by directly consuming infected individuals (Packer et al. 2003). The formalization of this hypothesis spurred decades of subsequent empirical work testing this prediction with a variety of systems and study designs. Perhaps surprisingly, the net outcome of this work has been the realization that the effect of predators on parasites in their prey is highly variable (Duffy et al. 2019; Lopez & Duffy 2021; Richards et al.2022). In fact, predators often increase parasitism in their prey, raising the question: Is it possible to predict a prioriwhat the impact of predation will be for a particular predator-prey-parasite system? Being able to make these predictions is both of fundamental ecological interest and potential conservation importance.
Although the depth of our understanding of the mechanisms by which predators increase parasitism in their prey varies, it is clear that a range of mechanisms can produce this outcome, even in a single system (e.g., in zooplankton (Duffy et al. 2019)). The variety of studies of predators increasing parasitism in their prey pales in comparison to the number of unique mechanisms by which predators may positively influence parasitism (Holt & Roy 2007; Cáceres et al.2009; Stephenson et al. 2015; Buss & Hua 2018; Duffy et al. 2019; Lopez & Duffy 2021; Richards et al. 2022), making an assessment of the most common mechanisms and the circumstances under which they occur difficult. However, these mechanisms of predator spreading exist along a spectrum that we can use to help us understand when predators might increase parasitism in their prey.
Here, we identify and consider six mechanisms by which predators can increase parasitism in their prey populations (Fig. 1), describing them in order from the mechanism most directly related to consumption of prey to the most indirect effects of predators. We also provide a set of theory- and evidence-based heuristics with which to predict what mechanism may be at play – and, therefore, whether a particular predator is likely to increase parasitism in its prey. These heuristics are based on an understanding of the ways that prey, parasite, and predator traits, as well as aspects of the environment, predispose the system to include certain mechanisms. (Note: throughout this manuscript, for simplicity, we use “prey” to indicate the prey/host species.) Finally, we provide guidance on how researchers can best select systems, design studies to investigate specific mechanisms, and report findings so that we can better understand and predict the outcomes of predator-prey-parasite interactions.