Abstract
We tested the hypothesis that exposure of leopard frogs (Rana pipiens) to agricultural pesticides can affect the infection dynamics of a common parasite of ranid frogs, the lungworm Rhabdias ranae. After a 21-day exposure to sublethal concentrations of a pesticide mixture composed of atrazine, metribuzin, aldicarb, endosulfan, lindane and dieldrin, or to control solutions (water, dimethyl sulfoxide), parasite-free juvenile frogs were challenged with 30 infective larvae of R. ranae. Approximately 75% of the larvae penetrated the skin and survived in both exposed and control animals, suggesting that pesticides did not influence host recognition or penetration components of the transmission process. Rather, we found that the migration of R. ranae was significantly accelerated in hosts exposed to the highest concentrations of pesticides, leading to the establishment of twice as many adult worms in the lungs of frogs 21 days post-infection. Pesticide treatment did not influence the growth of lungworms but our results indicate that they matured and reproduced earlier in pesticide-exposed frogs compared to control animals. Such alterations in life history characteristics that enhance parasite transmission may lead to an increase in virulence. Supporting evidence shows that certain components of the frog immune response were significantly suppressed after exposure to the pesticide mixture. This suggests that the immune system of anurans exerts a control over lungworm migration and maturation and that agricultural contaminants can interfere with these control mechanisms. Our results also contribute to the ongoing debate regarding the role that anthropogenic factors could play in the perplexing disease-related die-offs of amphibians observed in several parts of the world.
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Acknowledgements
Lucie Ménard, Alain Branchaud and Stéphanie Gagné are acknowledged for their assistance in the laboratory and with frog rearing. We are also grateful to Dr Cameron Goater for sharing his expertise with culturing of lungworms and experimental infection of frogs. The image-analysing system of the Université de Montréal was used with permission from Bernadette Pinel-Aloul and technical assistance of Louise Pelletier. We thank Drs Cameron Goater and Robert Poulin, as well as two anonymous reviewers, for commenting on the manuscript. This project received the financial support of the Toxic Substances Research Initiative program (grant no. 46).
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Gendron, A.D., Marcogliese, D.J., Barbeau, S. et al. Exposure of leopard frogs to a pesticide mixture affects life history characteristics of the lungworm Rhabdias ranae . Oecologia 135, 469–476 (2003). https://doi.org/10.1007/s00442-003-1210-y
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DOI: https://doi.org/10.1007/s00442-003-1210-y