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.