Agrochemicals increase trematode infections in a declining amphibian species

Abstract

Global amphibian declines have often been attributed to disease, but ignorance of the relative importance and mode of action of potential drivers of infection has made it difficult to develop effective remediation. In a field study, here we show that the widely used herbicide, atrazine, was the best predictor (out of more than 240 plausible candidates) of the abundance of larval trematodes (parasitic flatworms) in the declining northern leopard frog Rana pipiens. The effects of atrazine were consistent across trematode taxa. The combination of atrazine and phosphate--principal agrochemicals in global corn and sorghum production--accounted for 74% of the variation in the abundance of these often debilitating larval trematodes (atrazine alone accounted for 51%). Analysis of field data supported a causal mechanism whereby both agrochemicals increase exposure and susceptibility to larval trematodes by augmenting snail intermediate hosts and suppressing amphibian immunity. A mesocosm experiment demonstrated that, relative to control tanks, atrazine tanks had immunosuppressed tadpoles, had significantly more attached algae and snails, and had tadpoles with elevated trematode loads, further supporting a causal relationship between atrazine and elevated trematode infections in amphibians. These results raise concerns about the role of atrazine and phosphate in amphibian declines, and illustrate the value of quantifying the relative importance of several possible drivers of disease risk while determining the mechanisms by which they facilitate disease emergence.

Evolved pesticide tolerance influences susceptibility to parasites in amphibians

“…Past amphibian studies have also suggested scenarios that may lead to evolutionary responses to parasites. For example, high‐nutrient agricultural run‐off may indirectly facilitate trematode abundance by increasing the amount of algal resources available to the first intermediate hosts (snails) of trematodes (Koprivnikar & Redfern, 2012; Koprivnikar et al., 2006; Rohr, Schotthoefer, et al., 2008). Higher abundances of Echinoparyphium may select for increased resistance or tolerance to Echinoparyphium in amphibian populations near agriculture.…”

Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease

“…We suspect that, to thoroughly understand climatic effects on Bd-related declines, investigators will need to explicitly test how climate affects interactions between Bd and amphibian hosts, as well as consider other factors altering host-parasite dynamics or host fitness directly (39,(42)(43)(44). Additionally, the influence of climate on amphibians will almost certainly depend on the local scales at which organisms experience climatic conditions.…”

Pesticide concentrations in frog tissue and wetland habitats in a landscape dominated by agriculture

“…Pesticides have the potential to increase susceptibility (Mann et al, 2009) while elevated nutrient concentrations have the potential to increase the incidence of disease in amphibian populations (Johnson et al, 2007). On the other hand, studies have documented the relationship between pesticides and susceptibility to infections by trematodes (Rohr et al, 2008). These parasitic infections have the potential to negatively impact populations causing malformations (Reeves et al, 2013) which can lead to impaired mobility, decreased food intake, and an increased susceptibility to predators (Blaustein and Johnson, 2003).…”

“…Increased eutrophication due to nitrogen based fertilizers, coupled with pesticide application, may cause trophic cascades resulting in increased rates of parasitism in wetlands and has been linked to immunosuppression in amphibians (Brodkin et al, 2007;Johnson et al, 2007). Although a direct link has been made between pesticide exposure and infection by trematodes (Rohr et al, 2008;Kiesecker, 2002), a general understanding of these interactions in the field is lacking because results vary by species and land-use (King et al, 2007).…”