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Immediate and lag effects of pesticide exposure on parasite resistance in larval amphibians

Published online by Cambridge University Press:  11 January 2017

KATHERINE M. POCHINI  and
JASON T. HOVERMAN
KATHERINE M. POCHINI*
Affiliation:
Department of Forestry and Natural Resources, Purdue University, 715 West State Street, West Lafayette, IN 47907, USA
JASON T. HOVERMAN
Affiliation:
Department of Forestry and Natural Resources, Purdue University, 715 West State Street, West Lafayette, IN 47907, USA
*
*Corresponding author: Department of Forestry and Natural Resources, Purdue University, 715 West State Street, West Lafayette, IN 47907, USA. E-mail: kpochini4@gmail.com
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Summary

Across host–parasite systems, there is evidence that pesticide exposure increases parasite loads and mortality following infection. However, whether these effects are driven by reductions in host resistance to infection or slower rates of parasite clearance is often unclear. Using controlled laboratory experiments, we examined the ability of larval northern leopard frogs (Lithobates pipiens) and American toads (Anaxyrus americanus) to resist and clear trematode (Echinoparyphium sp.) infections following exposure to the insecticide carbaryl. Northern leopard frogs exposed to 1 mg L−1 of carbaryl had 61% higher parasite loads compared with unexposed individuals, while there was no immediate effect of carbaryl on parasite encystment in American toads. However, when tadpoles were exposed to carbaryl and moved to freshwater for 14 days before the parasite challenge, we recovered 37 and 63% more parasites from carbaryl-exposed northern leopard frogs and American toads, respectively, compared with the control. No effects on clearance were found for either species. Collectively, our results suggest that pesticide exposure can reduce the ability of amphibians to resist parasite infections and that these effects can persist weeks following exposure. It is critical for researchers to incorporate species interactions into toxicity studies to improve our understanding of how contaminants affect ecological communities.

Keywords

agrochemicalcarbamatehelminthdisease ecologyacetylcholinesterase inhibitor
Type
Research Article
Information
Parasitology , Volume 144 , Issue 6 , May 2017 , pp. 817 - 822
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Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Baker, N. and Stone, W. W. (2015). Estimated annual agricultural pesticide use for counties of the conterminous United States, 2008–2012. U.S. Geological Survey Data Series 907, 1–9.Google Scholar
Beauvais, S. L., Jones, S. B., Parris, J. T., Brewer, S. K. and Little, E. E. (2001). Cholinergic and behavioral neurotoxicity of carbaryl and cadmium to larval rainbow trout (Oncorhynchus mykiss). Ecotoxicology and Environmental Safety 49, 84–90.CrossRefGoogle ScholarPubMed
Boots, M. (2008). Fight or learn to live with the consequences. Trends in Ecology and Evolution 23, 248–250.CrossRefGoogle ScholarPubMed
Bradley, C. A. and Altizer, S. (2007). Urbanization and the ecology of wildlife diseases. Trends in Ecology & Evolution 22, 95–102.CrossRefGoogle ScholarPubMed
Bridges, C. M., Dwyer, F. J., Hardesty, D. K. and Whites, D. W. (2002). Comparative contaminant toxicity: are amphibian larvae more sensitive than fish? Bulletin of Environmental Contamination and Toxicology 69, 562–569.Google Scholar
Brühl, C. A., Schmidt, T., Pieper, S. and Alscher, A. (2013). Terrestrial pesticide exposure of amphibians: an underestimated cause of global decline? Scientific Reports 3, 1135–1138.CrossRefGoogle ScholarPubMed
Budischak, S. A., Belden, L. K. and Hopkins, W. A. (2008). Effects of malathion on embryonic development and latent susceptibility to trematode parasites in ranid tadpoles. Environmental Toxicology and Chemistry, 27, 2496–2500.CrossRefGoogle ScholarPubMed
Christin, M.-S., Gendron, A. D., Brousseau, P., Ménard, L., Marcogliese, D. J., Cyr, D., Ruby, S. and Fournier, M. (2003). Effects of agricultural pesticides on the immune system of Rana pipiens and on its resistance to parasitic infection. Environmental Toxicology and Chemistry/SETAC 22, 1127–1133.Google Scholar
Coors, A., Decaestecker, E., Jansen, M. and De Meester, L. (2008). Pesticide exposure strongly enhances parasite virulence in an invertebrate host model. Oikos 117, 1840–1846.Google Scholar
Daszak, P., Cunningham, A. and Hyatt, A. (2003). Infectious disease and amphibian population declines. Diversity and Distributions 9, 141–150.Google Scholar
De Castro, F. and Bolker, B. (2004). Mechanisms of disease-induced extinction. Ecology Letters 8, 117–126.Google Scholar
Di Prisco, G., Cavaliere, V., Annoscia, D., Varricchio, P., Caprio, E., Nazzi, F., Gargiulo, G. and Pennacchio, F. (2013). Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proceedings of the National Academy of Sciences of the United States of America 110, 18466–18471.Google Scholar
Egea-Serrano, A., Relyea, R. A., Tejedo, M. and Torralva, M. (2012). Understanding of the impact of chemicals on amphibians: a meta-analytic review. Ecology and Evolution 2, 1382–1397.CrossRefGoogle ScholarPubMed
Fineblum, W. L. and Rausher, M. (1995). Tradeoff between resistance and tolerance to herbivore damage in a morning glory. Nature 377, 517–520.CrossRefGoogle Scholar
Gill, R. J., Ramos-Rodriguez, O. and Raine, N. E. (2012). Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491, 105–108.Google Scholar
Gosner, K. L. (1960). A simplified table for staging anuran embryos larvae with notes on identification. Herpetologica 16, 183–190.Google Scholar
Grube, A., Donaldson, D., Kiely, T. and Wu, L. (2011). Pesticides industry sales and usage: 2006 and 2007 market estimates. U.S. Environmental Protection Agency 1–33.Google Scholar
Hammond, J. I., Jones, D. K., Stephens, P. R. and Relyea, R. A. (2012). Phylogeny meets ecotoxicology: evolutionary patterns of sensitivity to a common insecticide. Evolutionary Applications 5, 593–606.Google Scholar
Hoverman, J. T., Hoye, B. J. and Johnson, P. T. (2013). Does timing matter? How priority effects influence the outcome of parasite interactions within hosts. Oecologia 173, 1471–1480.CrossRefGoogle ScholarPubMed
Hua, J., Buss, N., Kim, J., Orlofske, S. A. and Hoverman, J. T. (2016). Population-specific toxicity of six insecticides to the trematode Echinoparyphium sp . Parasitology 143, 1–9.CrossRefGoogle Scholar
Johnson, P. T. J. and McKenzie, V. J. (2009). Effects of environmental change on helminth infections in amphibians: Exploring the emergence of Ribeiroia and Echinostoma infections in North America. In The Biology of Echinostomes (ed. Fried, B. and Toledo, R.), pp. 250–275. Springer, New York, NY.Google Scholar
Johnson, P. T. J., de Roode, J. C. and Fenton, A. (2015). Why infectious disease research needs community ecology. Science (New York, NY) 349, 1069–1078.CrossRefGoogle ScholarPubMed
Kanev, I., Fried, B., Dimitrov, V. and Radev, V. (1995). Redescription of Echinostoma trivolvis (Cort, 1914) (Trematoda: Echinostomatidae) with a discussion on its identity. Systematic Parasitology 32, 61–70.Google Scholar
Kiesecker, J. M. (2002). Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature? Proceedings of the National Academy of Sciences of the United States of America 99, 9900–9904.Google Scholar
Köhler, H.-R. and Triebskorn, R. (2013). Wildlife ecotoxicology of pesticides: can we track effects to the population level and beyond? Science (New York, NY) 341, 759–765.Google Scholar
Koprivnikar, J. (2010). Interactions of environmental stressors impact survival and development of parasitized larval amphibians. Ecological Applications 20, 2263–2272.CrossRefGoogle ScholarPubMed
Koprivnikar, J., Forbes, M. R. and Baker, R. L. (2006). On the efficacy of anti-parasite behaviour: a case study of tadpole susceptibility to cercariae of Echinostoma trivolvis . Canadian Journal of Zoology 84, 1623–1629.Google Scholar
Kuris, A. M., Hechinger, R. F., Shaw, J. C., Whitney, K. L., Aguirre-Macedo, L., Boch, C. A., Dobson, A. P., Dunham, E. J., Fredensborg, B. L., Huspeni, T. C., Lorda, J., Mababa, L., Mancini, F. T., Mora, A. B., Pickering, M., Talhouk, N. L., Torchin, M. E. and Lafferty, K. D. (2008). Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454, 515–518.Google Scholar
Lafferty, K. D., Dobson, A. P. and Kuris, A. M. (2006). Parasites dominate food web links. Proceedings of the National Academy of Sciences of the United States of America 103, 11211–11216.CrossRefGoogle ScholarPubMed
LaFonte, B. E. and Johnson, P. T. J. (2013). Experimental infection dynamics: using immunosuppression and in vivo parasite tracking to understand host resistance in an amphibian–trematode system. Journal of Experimental Biology 216, 3700–3708.Google Scholar
Marcogliese, D. J. and Pietrock, M. (2011). Combined effects of parasites and contaminants on animal health: parasites do matter. Trends in Parasitology 27, 123–130.Google Scholar
Mason, R., Tennekes, H., Sanchez-Bayo, F. and Jepsen, P. U. (2013). Immune suppression by neonicotinoid insecticides at the root of global wildlife declines. Journal of Environmental Immunology and Toxicology 1, 3–12.Google Scholar
Norris, L. A., Lorz, H. W. and Gregory, S. V. (1983). Influence of forest and rangeland management on anadromous fish habitat in western North America. USDA Forest Service 1–74.Google Scholar
Orlofske, S. A., Belden, L. K. and Hopkins, W. A. (2009). Moderate Echinostoma trivolvis infection has no effects on physiology and fitness-related traits of larval pickerel frogs (Rana palustris). Journal of Parasitology 95, 787–792.Google Scholar
Orlofske, S. A., Belden, L. K. and Hopkins, W. A. (2013). Larval wood frog (Rana [=Lithobates] sylvatica) development and physiology following infection with the trematode parasite, Echinostoma trivolvis . Comparative Biochemistry and Physiology – a Molecular and Integrative Physiology 164, 529–536.CrossRefGoogle ScholarPubMed
Pochini, K. M. and Hoverman, J. T. (2016). Reciprocal effects of pesticides and pathogens on amphibian hosts: the importance of exposure order and timing. Environmental Pollution. doi: 10.1016/j.envpol.2016.11.086.Google Scholar
Råberg, L., Graham, A. L. and Read, A. F. (2009). Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 37–49.CrossRefGoogle ScholarPubMed
Read, A. F., Graham, A. L. and Råberg, L. (2008). Animal defenses against infectious agents: is damage control more important than pathogen control? PLoS Biology 6, 2638–2641.CrossRefGoogle ScholarPubMed
Relyea, R. A. (2003). Predator cues and pesticides: a double dose of danger for amphibians. Ecological Applications 13, 1515–1521.Google Scholar
Relyea, R. and Hoverman, J. (2006). Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. Ecology Letters 9, 1157–1171.Google Scholar
Rohr, J. R. and Raffel, T. R. (2010). Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease. Proceedings of the National Academy of Sciences of the United States of America 107, 8269–8274.Google Scholar
Rohr, J. R., Schotthoefer, A. M., Raffel, T. R., Carrick, H. J., Halstead, N., Hoverman, J. T., Johnson, C. M., Johnson, L. B., Lieske, C., Piwoni, M. D., Schoff, P. K. and Beasley, V. R. (2008 a). Agrochemicals increase trematode infections in a declining amphibian species. Nature 455, 1235–1240.CrossRefGoogle Scholar
Rohr, J. R., Raffel, T. R., Sessions, S. K. and Hudson, P. J. (2008 b). Understanding the net effects of pesticides on amphibian trematode infections. Ecological Applications 18, 1743–1753.Google Scholar
Rohr, J. R., Raffel, T. R. and Hall, C. A. (2010). Developmental variation in resistance and tolerance in a multi-host-parasite system. Functional Ecology 24, 1110–1121.CrossRefGoogle Scholar
Rohr, J. R., Raffel, T. R., Halstead, N. T., McMahon, T. A., Johnson, S. A., Boughton, R. K. and Martin, L. B. (2013). Early-life exposure to a herbicide has enduring effects on pathogen-induced mortality. Proceedings of the Royal Society – Biological Sciences 280, 1–7.Google Scholar
Roy, B. A. and Kirchner, J. W. (2010). Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54, 51–63.Google Scholar
Schotthoefer, A. M., Cole, R. A. and Beasley, V. R. (2003). Relationship of tadpole stage to location of echinostome cercariae encystment and the consequences for tadpole survival. Journal of Parasitology 89, 475–482.Google Scholar
Skelly, D. K., Bolden, S. R., Holland, M. P., Kealoha Freidenburg, L., Freidenfelds, N. A. and Malcolm, T. R. (2007). Urbanization and disease in amphibians. In Disease Ecology: Community Structure and Pathogen Dynamics (ed. Collinge, S. and Ray, C.), pp. 153–167. Oxford University Press, New York, NY.Google Scholar
Smith, K. F., Sax, D. F. and Lafferty, K. D. (2006). Evidence for the role of infectious disease in species extinction and endangerment. Conservation Biology 20, 1349–1357.Google Scholar
Szuroczki, D. and Richardson, J. M. L. (2009). The role of trematode parasites in larval anuran communities: an aquatic ecologist's guide to the major players. Oecologia 161, 371–385.Google Scholar
Wood, C. L. and Johnson, P. T. J. (2015). A world without parasites: exploring the hidden ecology of infection. Frontiers in Ecology and the Environment 13, 425–434.Google Scholar