Parasite transmission in complex communities: Predators and alternative hosts alter pathogenic infections in amphibians

Abstract

While often studied in isolation, host-parasite interactions are typically embedded within complex communities. Other community members, including predators and alternative hosts, can therefore alter parasite transmission (e.g., the dilution effect), yet few studies have experimentally evaluated more than one such mechanism. Here, we used data from natural wetlands to design experiments investigating how alternative hosts and predators of parasites mediate trematode (Ribeiroia ondatrae) infection in a focal amphibian host (Pseudacris regilla). In short-term predation bioassays involving mollusks, zooplankton, fish, larval insects, or newts, four of seven tested species removed 62-93% of infectious stages. In transmission experiments, damselfly nymphs (predators) and newt larvae (alternative hosts) reduced infection in P. regilla tadpoles by -50%, whereas mosquitofish (potential predators and alternative hosts) did not significantly influence transmission. Additional bioassays indicated that predators consumed parasites even in the presence of alternative prey. In natural wetlands, newts had similar infection intensities as P. regilla, suggesting that they commonly function as alternative hosts despite their unpalatability to downstream hosts, whereas mosquitofish had substantially lower infection intensities and are unlikely to function as hosts. These results underscore the importance of studying host-parasite interactions in complex communities and of broadly linking research on predation, biodiversity loss, and infectious diseases.

Predator diversity, intraguild predation, and indirect effects drive parasite transmission

“…We focused on larval odonates as our predator guild because they are important predators of cercariae in ponds (23)(24)(25) and some species can also be predators of tadpole hosts (e.g., ref.…”

It’s a predator–eat–parasite world: how characteristics of predator, parasite and environment affect consumption

“…trophic transmission ;Lafferty 1999;Hall et al 2007); on the other hand, predators can directly consume parasites and thereby reduce transmission or persistence. Examples range from the grooming of ectoparasites to the consumption of free-living infectious stages encountered in the environment (Hopper et al 2008;Thieltges et al 2008;Prinz et al 2009;Johnson et al 2010;Orlofske et al 2012). A specific example is the predation of trematode parasites by aquatic invertebrates, which was found to reduce transmission to tadpole hosts by 50 % in laboratory trials (Orlofske et al 2012).…”

Using an ecosystem‐level manipulation to understand host‐parasite interactions and how they vary with study venue

“…For example, while amphibian hosts in laboratory experiments are often raised in isolation under artificial conditions, hosts in nature occur alongside numerous factors with the potential to alter transmission or pathology, including predators, competitors, and physicochemical variation. Aquatic predators, for example, can reduce amphibian avoidance behavior and thereby infection risk (Thiemann and Wassersug 2000), or actively consume free-swimming parasites and reduce amphibian infections (Schotthoefer et al 2007, Orlofske et al 2012. Predators and other 'natural stressors' can also amplify patterns of mortality observed under laboratory conditions, as found in studies of certain contaminants in aquatic systems (e.g., Relyea and Mills 2001).…”