Mortality of American Bullfrog Tadpoles Lithobates catesbeianus Infected by Gyrodactylus jennyae and Experimentally Exposed to Batrachochytrium dendrobatidis

Abstract

The fungal pathogen Batrachochytrium dendrobatidis (Bd), which causes the disease chytridiomycosis in postmetamorphic amphibians, has been linked to amphibian population declines. Different amphibian species, however, exhibit different susceptibility to Bd pathogenicity. At the same time, agricultural pesticides commonly found contaminating aquatic habitats have been reported to increase the susceptibility of amphibians to pathogens. To investigate whether certain pesticides are able to alter the pathogenicity of Bd to larval amphibians, we exposed larval American bullfrogs Lithobates catesbeianus to end-use formulations of the herbicides atrazine or glyphosate, and then exposed them to Bd. Following the experimental exposures, a preexisting infection of the tadpoles by the monogenean ectoparasite Gyrodactylus jennyae was detected in all experimental and control tadpoles. Gyrodactylus jennyae infection intensity varied, and individuals with heavy G. jennyae infections suffered more skin erosion due to grazing by the parasite. Tadpoles experimentally exposed to Bd, or to Bd and either herbicide, had significantly reduced survival rates compared with untreated tadpoles that were only infected by G. jennyae. Increased mortality was also correlated with degree of skin erosion; survival of tadpoles with severe skin erosion was significantly reduced compared with that of tadpoles with no, or mild, skin erosion. While infected with G. jennyae, the group of tadpoles with the lowest survival rate (exposed only to Bd) included significantly more individuals exhibiting severe skin erosion and significantly fewer individuals without skin erosion, compared with the control group. These results emphasize the potential pathogenicity of gyrodactylid infections in larval amphibian hosts and suggest that concomitant exposures to Bd may enhance infections and effects of G. jennyae in bullfrog tadpoles.

Received February 3, 2012; accepted August 10, 2012

ACKNOWLEDGMENTS

This work was partially funded by Natural Sciences and Engineering Research Council of Canada Discovery Grant A6979 awarded to J.D.M., by a Natural Sciences and Engineering Research Council of Canada Postgraduate Scholarship awarded to L.J.P., and by funds from the Pesticide Science Fund of Environment Canada (to D.J.M. and B.D.P.). The authors thank Roger Cue (McGill University, Montreal) for providing advice on statistical methods. We thank Ken Doe and Paula Jackman (Environment Canada) for providing the tadpoles, Joyce E. Longcore (University of Maine, Orono) for providing the fungal culture, along with Andrée Gendron, Jean-François Lafond, and Stéphanie Arseneault for their assistance with the experiment.