The interactive effects of pesticide exposure and infectious disease on amphibian hosts

Natural systems are home to a multitude of natural and anthropogenic stressors, which draw an array of effects on ecological communities. While these effects have been investigated individually, it is important, given the routine co-occurrence of these stressors, to understand their interactive effects. Pesticide exposure and infectious disease are two common, co-occurring stressors that each have documented detrimental effects on species and, as evidence suggests, may have interactive effects. Moreover, existing research suggests that these interactive effects are highly context dependent, eliciting different results based on species, disease agent, toxin, and environment. Given the variability with which species may experience multiple stressors, it is imperative that we form a detailed understanding of these interactions in diverse systems. Amphibians are an ideal study system due to the pervasiveness of pesticide contamination in wetland habitats and the various disease agents contributing to their global population declines. Here I sought to contribute a more comprehensive understanding of pesticide-disease interactions in amphibians by (1) examining this interaction using an understudied disease agent, ranavirus, and (2) exploring how pesticides affect the mechanisms by which hosts and parasites increase their fitness during their relationship. In a series of experiments using larval wood frogs (Lithobates sylvaticus) and two insecticides (carbaryl and thiamethoxam), I found that prior ranavirus infection increased the toxicity of both pesticides, reducing median lethal concentrations (LC50 estimates) by 72 and 55% for carbaryl and thiamethoxam, respectively. Importantly, these reductions matched concentrations found in natural surface waters. Moreover, when pesticide exposure preceded ranavirus infection, I found that carbaryl exacerbated disease-induced mortality. However, these effects were ameliorated if individuals were given the opportunity to metabolize the pesticide. There was minimal effect of pesticides on susceptibility to or transmission of ranavirus. These results highlight the context-dependency of pesticide-disease interactions and emphasize the importance of examining these interactions in detail. To further this idea, I conducted several experiments using larval northern leopard frogs (Lithobates pipiens), the trematode Echinoparyphium spp., and carbaryl to examine how pesticide exposure affects both a host’s ability to increase its fitness when challenged with a parasite (i.e. resistance and tolerance) and a parasite’s ability to successfully infect a host. I found that pesticide exposure of hosts did not affect the resistance mechanisms of parasite avoidance or clearance, and that exposure of parasites did not affect their ability to infect hosts. However, pesticide exposure influenced infection tolerance by decreasing time to metamorphosis in more highly infected individuals by a factor of 31%. Collectively, these results underscore that pesticide-disease interactions are context-dependent and have variable outcomes on hosts and parasites. Importantly, they affirm that individual examinations of stressors, particularly of pesticide toxicity, are not sufficient predictors of the effects of stressors in complex systems. It is essential in a progressively human-influenced environment that research addresses the various ways that stressors interact and the consequences of these interactions for populations and communities