Understanding the net effects of pesticides on amphibian trematode infections.

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.