Understanding the Net Effects of Pesticides on Amphibian Trematode Infections

Abstract

Anthropogenic factors can have simultaneous positive and negative effects on parasite transmission, and thus it is important to quantify their net effects on disease risk. Net effects will be a product of changes in the survival and traits (e.g., susceptibility, infectivity) of both hosts and parasites. In separate laboratory experiments, we exposed cercariae of the trematode Echinostoma trivolvis, and its first and second intermediate hosts, snails (Planorbella trivolvis) and green frog tadpoles (Rana clamitans), respectively, to one of four common pesticides (atrazine, glyphosate, carbaryl, and malathion) at standardized, ecologically relevant concentrations (201.0, 3700.0, 33.5, and 9.6 microg/L, respectively). We measured effects of pesticide exposure on six mechanisms important to this host-parasite interaction: (1) survival of E. trivolvis cercariae over 26 hours, (2) tadpole survival over two weeks, (3) snail survival over four weeks, (4) snail growth and fecundity, (5) cercarial infectivity, and (6) tadpole susceptibility to a fixed number of cercariae. Pesticides, in general, caused significantly greater mortality of E. trivolvis cercariae than did control treatments, but atrazine was the lone chemical to significantly reduce cercarial survival (LC50 value = 267 mg/L) and then only at concentrations greater than commonly found in aquatic ecosystems (> or =200 microg/L). None of the pesticides significantly enhanced E. trivolvis virulence, decreased tadpole survival, or reduced snail survival, growth, or fecundity. Sublethal exposure of the cercariae to the pesticides (4 h) did not significantly affect trematode encystment in R. clamitans. In contrast, sublethal exposure of R. clamitans to each of the four pesticides increased their susceptibility as measured by the percentage of cercariae that encysted. The reduction in exposure to trematodes due to pesticide-induced cercarial mortality (a density-mediated effect) was smaller than the pesticide-induced increase in amphibian susceptibility (a trait-mediated effect), suggesting that the net effect of exposure to environmentally realistic levels of pesticides will be to elevate amphibian trematode infections. These findings highlight the importance of elucidating the lethal and sublethal effects of anthropogenic factors on both hosts and parasites to understand the mechanisms underlying changes in parasite transmission and virulence, an approach that is especially needed for amphibians, a taxon experiencing global disease-related declines.

Evolved pesticide tolerance influences susceptibility to parasites in amphibians

“…Further, this study provides the first evidence in a vertebrate species that evolutionary responses to pesticides influence susceptibility to parasites. Pesticide‐mediated effects on disease outcomes are commonly documented in the literature, yet the results are often variable with pesticides increasing host tolerance to parasite infection in some cases (Coors, Decaestecker, Jansen, & De Meester, 2008; Kiesecker, 2002; Rohr, Raffel, et al., 2008) but not in others (Griggs & Belden, 2008; Marcogliese et al., 2009; Schotthoefer et al., 2011). We demonstrate that the mechanism underlying the evolution of pesticide tolerance may be critical for assessing susceptibility to parasites.…”

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.…”

Population-specific toxicity of six insecticides to the trematode Echinoparyphium sp.

“…For instance, Coors and De Meester (2008) found that exposure to the insecticide carbaryl had a synergistic effect on Daphnia magna by increasing susceptibility to the parasite Pasteuria ramosa. Similarly, in amphibians, Rohr et al (2008) found that green frog tadpoles exposed to the herbicide atrazine had significantly higher levels of encysted trematodes (Echinostoma trivolvis). Further, Kiesecker (2002) linked pesticide exposure to increased infection and pathology (i.e., limb malformations) in amphibians exposed to the trematode Ribeiroia ondatrae.…”

“…Mounting evidence suggests that pesticides can influence disease outcome directly (e.g., mortality) and indirectly (e.g., immune suppression; Carey et al 1999;Kiesecker, 2002;Christin et al 2004;Rohr et al 2008). For instance, Coors and De Meester (2008) found that exposure to the insecticide carbaryl had a synergistic effect on Daphnia magna by increasing susceptibility to the parasite Pasteuria ramosa.…”