Healthy but smaller herds: Predators reduce pathogen transmission in an amphibian assemblage

Abstract

Predators and pathogens are fundamental components of ecological communities that have the potential to influence each other via their interactions with victims and to initiate density‐ and trait‐mediated effects, including trophic cascades. Despite this, experimental tests of the healthy herds hypothesis, wherein predators influence pathogen transmission, are rare. Moreover, no studies have separated effects mediated by density vs. traits. Using a semi‐natural mesocosm experiment, we investigated the interactive effects of predatory dragonfly larvae (caged or lethal [free‐ranging]) and a viral pathogen, ranavirus, on larval amphibians (grey treefrogs and northern leopard frogs). We determined the influence of predators on ranavirus transmission and the relative importance of density‐ and trait‐mediated effects on observed patterns. Lethal predators reduced ranavirus infection prevalence by 57%–83% compared to no‐predator and caged‐predator treatments. The healthy herds effect was more strongly associated with reductions in tadpole density than behavioural responses to predators. We also assessed whether ranavirus altered the responses of tadpoles to predators. In the absence of virus, tadpoles reduced activity levels and developed deeper tails in the presence of predators. However, there was no evidence that virus presence or infection altered responses to predators. Finally, we compared the magnitude of trophic cascades initiated by individual and combined natural enemies. Lethal predators initiated a trophic cascade by reducing tadpole density, but caged predators and ranavirus did not. The absence of a virus‐induced trophic cascade is ostensibly the consequence of limited virus‐induced mortality and the ability of infected individuals to continue interacting within the community. Our results provide support for the healthy herds hypothesis in amphibian communities. We uniquely demonstrate that density‐mediated effects of predators outweigh trait‐mediated effects in driving this pattern. Moreover, this study was one of the first to directly compare trophic cascades caused by predators and pathogens. Our results underscore the importance of examining the interactions between predators and pathogens in ecology.

Can predators stabilize host–parasite interactions? Changes in aquatic predator identity alter amphibian responses and parasite abundance across life stages

“…Predators have profound effects on aquatic communities (Sih et al, 1985 ; Wellborn et al, 1996 ) and can shape infection dynamics, including those caused by trematodes, through effects on community composition (i.e., density‐mediated effects that change the identity and/or density of community members). For instance, predators may consume free‐swimming parasites such as trematode miracidia or cercariae (Hopkins et al, 2013 ; Orlofske et al, 2015 ) or heavily parasitized prey (Gallagher et al, 2019 ), thus reducing observed parasite infections in hosts and creating “healthier herds” (Packer et al, 2003 ). Likewise, because many parasites use multiple host species (Woolhouse et al, 2001 ), certain predators may reduce parasite abundance in vulnerable hosts by acting as hosts themselves (Hatcher et al, 2006 ).…”

Predation shifts coevolution toward higher host contact rate and parasite virulence

“…Predation is often expected to reduce the incidence, prevalence or transmission of infectious diseases of prey, 'keeping the herds healthy and alert' [1,2] by reducing host density and thus the spread of density-dependent diseases. However, there are certain conditions under which predation can increase, not decrease, disease in its prey [3][4][5]; for example, if predators remove enough recovered individuals, increasing the supply of susceptible individuals in a density-limited host population, then predators can increase infection prevalence [4].…”

Spatial compartmentalization: A nonlethal predator mechanism to reduce parasite transmission between prey species

“…For example, predator-driven nonlethal effects on parasite transmission may include behavioral changes, such as decreases in prey activity ( 6 ) and distribution ( 15 , 16 ), that reduce contact and transmission between infectious and susceptible individuals. Thus, we hypothesize that predators can also shape parasite transmission dynamics through nonlethal effects rather than the largely assumed lethal effects ( 4 , 17 , 18 ). These nonlethal effects may be more important in sustaining a healthy prey population by reducing parasite spillover to aberrant hosts, where the lethal removal of infected individual aberrant hosts would not necessarily affect ongoing transmission within a system ( 11 ).…”

“…Wildlife predators play a key role in the top-down cascade effect paradigm in ecology (1). Although predation drives trophic effects through the lethal removal of individuals within a population of prey, growing evidence highlights the importance of nonlethal effects through changes in prey behavior (2)(3)(4). Predator-induced changes in prey behavior are based on countermeasures to avoid predation (5).…”