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Agrochemicals increase trematode infections in a declining amphibian species

Abstract

Global amphibian declines have often been attributed to disease1,2, 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.

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Figure 1: Proposed mechanisms for the relationship between atrazine and larval trematodes in amphibians.
Figure 2: Relationships between melanomacrophage aggregates and atrazine, phosphate and larval trematode loads.

References

  1. Stuart, S. N. et al. Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783–1786 (2004)

    ADS  CAS  Article  Google Scholar 

  2. Daszak, P., Cunningham, A. A. & Hyatt, A. D. Infectious disease and amphibian population declines. Divers. Distrib. 9, 141–150 (2003)

    Article  Google Scholar 

  3. Hudson, P. J., Dobson, A. P. & Newborn, D. Prevention of population cycles by parasite removal. Science 282, 2256–2258 (1998)

    ADS  CAS  Article  Google Scholar 

  4. de Castro, F. & Bolker, B. Mechanisms of disease-induced extinction. Ecol. Lett. 8, 117–126 (2005)

    Article  Google Scholar 

  5. Lafferty, K. D. & Gerber, L. R. Good medicine for conservation biology: The intersection of epidemiology and conservation theory. Conserv. Biol. 16, 593–604 (2002)

    Article  Google Scholar 

  6. Schotthoefer, A. M., Cole, R. A. & Beasley, V. R. Relationship of tadpole stage to location of echinostome cercariae encystment and the consequences for tadpole survival. J. Parasitol. 89, 475–482 (2003)

    Article  Google Scholar 

  7. Johnson, P. T. J. & Sutherland, D. R. Amphibian deformities and Ribeiroia infection: An emerging helminthiasis. Trends Parasitol. 19, 332–335 (2003)

    Article  Google Scholar 

  8. Skelly, D. K. et al. in Disease Ecology: Community Structure and Pathogen Dynamics (eds Collinge, S. K. & Ray, C.) 153–167 (Oxford Univ. Press, 2006)

    Book  Google Scholar 

  9. Beasley, V. R. et al. in Status and Conservation of U.S. Amphibians (ed. Lannoo, M. J.) 153–167 (Univ. Chicago Press, 2003)

    Google Scholar 

  10. Johnson, P. T. J. et al. Aquatic eutrophication promotes pathogenic infection in amphibians. Proc. Natl Acad. Sci. USA 104, 15781–15786 (2007)

    ADS  CAS  Article  Google Scholar 

  11. Johnson, P. T. J., Lunde, K. B., Ritchie, E. G. & Launer, A. E. The effect of trematode infection on amphibian limb development and survivorship. Science 284, 802–804 (1999)

    ADS  CAS  Article  Google Scholar 

  12. Schotthoefer, A. M., Koehler, A. V., Meteyer, C. U. & Cole, R. A. Influence of Ribeiroia ondatrae (Trematoda: Digenea) infection on limb development and survival of northern leopard frogs (Rana pipiens): effects of host stage and parasite-exposure level. Can. J. Zool. 81, 1144–1153 (2003)

    Article  Google Scholar 

  13. Rorabaugh, J. C. in Amphibian Declines: The Conservation and Status of United States Species (ed. Lannoo, M. J.) (Univ. California Press, 2005)

    Google Scholar 

  14. Rohr, J. R., Raffel, T. R., Sessions, S. K. & Hudson, P. J. Understanding the net effects of pesticides on amphibian trematode infections. Ecol. Appl. (in the press)

  15. Kiely, T., Donaldson, D. & Grube, A. Pesticide Industry Sales and Usage: 2000 and 2001 Market Estimates (U.S. Environmental Protection Agency, 2004)

    Google Scholar 

  16. Gammon, D. W. Atrazine Risk Characterization Document (California Department of Pesticide Regulation, 2001)

    Google Scholar 

  17. Brock, T. C. M., Lahr, J. & Van den Brink, P. J. Ecological Risks of Pesticides in Freshwater Ecosystems Part 1: Herbicides Alterra-Rapport 088 (Alterra, Green World Research, 2000)

    Google Scholar 

  18. Brodkin, M. A., Madhoun, H., Rameswaran, M. & Vatnick, I. Atrazine is an immune disruptor in adult northern leopard frogs (Rana pipiens). Environ. Toxicol. Chem. 26, 80–84 (2007)

    CAS  Article  Google Scholar 

  19. Kiesecker, J. M. Synergism between trematode infection and pesticide exposure: A link to amphibian limb deformities in nature? Proc. Natl Acad. Sci. USA 99, 9900–9904 (2002)

    ADS  CAS  Article  Google Scholar 

  20. Forson, D. & Storfer, A. Effects of atrazine and iridovirus infection on survival and life-history traits of the long-toed salamander (Ambystoma macrodactylum). Environ. Toxicol. Chem. 25, 168–173 (2006)

    CAS  Article  Google Scholar 

  21. Grace, J. B. Structural Equation Modeling and Natural Systems (Cambridge Univ. Press, 2006)

    Book  Google Scholar 

  22. Dezfuli, B. S. et al. Histopathology and ultrastructure of Platichthys flesus naturally infected with Anisakis simplex S.L. larvae (Nematoda: Anisakidae). J. Parasitol. 93, 1416–1423 (2007)

    Article  Google Scholar 

  23. Reyes, J. L. & Terrazas, L. I. The divergent roles of alternatively activated macrophages in helminthic infections. Parasite Immunol. 29, 609–619 (2007)

    CAS  Article  Google Scholar 

  24. Agius, C. & Roberts, R. J. Melano-macrophage centres and their role in fish pathology. J. Fish Dis. 26, 499–509 (2003)

    CAS  Article  Google Scholar 

  25. Rohr, J. R. & Crumrine, P. W. Effects of an herbicide and an insecticide on pond community structure and processes. Ecol. Appl. 15, 1135–1147 (2005)

    Article  Google Scholar 

  26. Rohr, J. R., Kerby, J. L. & Sih, A. Community ecology as a framework for predicting contaminant effects. Trends Ecol. Evol. 21, 606–613 (2006)

    Article  Google Scholar 

  27. Davidson, C., Shaffer, H. B. & Jennings, M. R. Declines of the California red-legged frog: Climate, UV-B, habitat, and pesticides hypotheses. Ecol. Appl. 11, 464–479 (2001)

    Article  Google Scholar 

  28. Hayes, T. B. et al. Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proc. Natl Acad. Sci. USA 99, 5476–5480 (2002)

    ADS  CAS  Article  Google Scholar 

  29. Storrs, S. I. & Kiesecker, J. M. Survivorship patterns of larval amphibians exposed to low concentrations of atrazine. Environ. Health Perspect. 112, 1054–1057 (2004)

    CAS  Article  Google Scholar 

  30. Rohr, J. R., Sager, T., Sesterhenn, T. M. & Palmer, B. D. Exposure, postexposure, and density-mediated effects of atrazine on amphibians: Breaking down net effects into their parts. Environ. Health Perspect. 114, 46–50 (2006)

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank J. Murphy, A. Antolin, K. Beckman, R. Cole, A. Koehler, C. Hall, T. Hollenhorst and J. Romansic for collection and compilation of field, parasitological or land cover data; R. Cole, M. Martin, M. Mescher, J. Romansic, J. Runyon and the O. Bjørnstad, C. De Moraes, E. Holmes, P. Hudson, B. Grenfell and M. Poss laboratories for comments and suggestions on this work; and J. Grace for reviewing sections of the paper on structural equation modelling. We also thank the USGS National Wildlife Health Center for laboratory space and support. Funds came from National Science Foundation (DEB-0809487) and US Department of Agriculture (NRI 2008-00622 and 2008-01785) grants to J.R.R., and US Environmental Protection Agency STAR grants to V.R.B. (R825867) and J.R.R. and T.R.R (R833835). This work does not necessarily reflect the views of these agencies.

Author Contributions For the field survey, V.R.B. and L.B.J. designed the data collection. C.M.J., P.K.S., C.L. and A.M.S. conducted the survey. C.M.J. coordinated data collection, assembly and management. M.D.P. conducted all analyte analyses. A.M.S. performed amphibian necropsies of R. pipiens for parasite quantification. C.L. quantified amphibian immunity. For the mesocosm study, J.R.R., T.R.R. and J.T.H. designed and implemented the experiment. J.R.R. oversaw all components the study. T.R.R. and N.H. processed amphibian samples and quantified amphibian immune parameters. H.J.C. quantified periphyton and phytoplankton. J.R.R. conducted all statistical analyses and wrote the paper. A.M.S. wrote parts of the Supplementary Methods. The paper was edited by all authors.

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Correspondence to Jason R. Rohr.

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This file contains Supplementary Methods and Discussion, Supplementary Tables S1-S8, and Supplementary Figures S1-S6. Supplementary Table S8 for this Letter should have been uploaded at the time of publication. This oversight was rectified no 06 January 2009 (PDF 2553 kb)

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Rohr, J., Schotthoefer, A., Raffel, T. et al. Agrochemicals increase trematode infections in a declining amphibian species. Nature 455, 1235–1239 (2008). https://doi.org/10.1038/nature07281

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