Synergistic effects of predators and trematode parasites on larval green frog (Rana clamitans) survival

Abstract

Parasites and predators can have complex, nonadditive effects on a shared group of victims, which can have important consequences for population dynamics. In particular, parasites can alter host traits that influence predation risk, and predators can have nonconsumptive effects on prey traits which influence susceptibility (i.e., infection intensity and tolerance) to parasites. Here, we examined the combined effects of trematode parasites (Digenea: Echinostomatidae) and odonate (Anax) predators on the survival of larval green frogs (Rana clamitans). First, in a large-scale mesocosm experiment, we manipulated the presence or absence of parasites in combination with the presence of no predator, caged predators, or free predators, and measured survival, traits, and infection. Parasites, caged predators, and free predators decreased survival, and we found a strong negative synergistic effect of parasites in combination with free predators on survival. Importantly, we then examined the potential mechanisms that explain the observed synergistic effect of parasites and predators in a series of follow-up experiments. Results of the follow-up experiments suggest that increased predation susceptibility due to elevated activity levels in the presence of free-swimming parasite infective stages (i.e., an avoidance response) is the most likely mechanism responsible for the observed synergism. These results suggest a potential trade-off in susceptibility to parasites and predators, which can drive nonadditive effects that may have important consequences for natural enemy interactions in natural populations and amphibian conservation.

Competition and host size mediate larval anuran interactions with trematode parasites

“…Furthermore, we did not observe a negative effect of parasitism on survival that we had previously observed (Marino & Werner, 2013). Furthermore, we did not observe a negative effect of parasitism on survival that we had previously observed (Marino & Werner, 2013).…”

“…Nevertheless, other recent studies have similarly reported no effect (Raffel et al, 2010;Marino & Werner, 2013) or even a positive effect (Johnson et al, 2013;Wojdak et al, 2014) of density on larval amphibian trematode infection at the mesocosm scale. Our sample sizes for dissection were limited and necessarily did not include animals that died during the experiments, as dead tadpoles are typically not visible in the large mesocosms and rapidly degrade.…”

“…Echinostomes can have a range of effects on amphibian hosts, such as reduced growth rates, impaired kidney function and death at high infection intensities (Fried, Pane & Reddy, 1997;Holland et al, 2007), although such effects may be dose-and scale-dependent (Marino & Werner, 2013;Marino et al, 2014). Larger tadpoles at later developmental stages tend to be more tolerant of infection (Schotthoefer, Cole & Beasley, 2003;Holland et al, 2007).…”

“…To test our hypotheses, we performed two new mesocosm experiments, which were then compared to two experiments from a previously published study (Marino & Werner, 2013). In the first experiment, we manipulated parasite presence, host density and the presence of predator cue.…”

Behavioural influences on disease risk: implications for conservation and management

“…1). Green frog tadpoles, Lithobates clamitans, exposed to free-living stages of trematode parasites increased their activity levels as an avoidance response (Marino & Werner, 2013). As a result, tadpoles experienced greater predation rates by larval dragonflies, which target highly active prey.…”