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Combined Effects of Pesticides and Trematode Infections on Hourglass Tree Frog Polypedates cruciger

Abstract

The impact of widespread and common environmental factors, such as chemical contaminants, on infectious disease risk in amphibians is particularly important because both chemical contaminants and infectious disease have been implicated in worldwide amphibian declines. Here we report on the lone and combined effects of exposure to parasitic cercariae (larval stage) of the digenetic trematode, Acanthostomum burminis, and four commonly used pesticides (insecticides: chlorpyrifos, dimethoate; herbicides: glyphosate, propanil) at ecologically relevant concentrations on the survival, growth, and development of the common hourglass tree frog, Polypedates cruciger Blyth 1852. There was no evidence of any pesticide-induced mortality on cercariae because all the cercariae successfully penetrated each tadpole host regardless of pesticide treatment. In isolation, both cercarial and pesticide exposure significantly decreased frog survival, development, and growth, and increased developmental malformations, such as scoliosis, kyphosis, and also edema and skin ulcers. The combination of cercariae and pesticides generally posed greater risk to frogs than either factor alone by decreasing survival or growth or increasing time to metamorphosis or malformations. The exception was that lone exposure to chlorpyrifos had higher mortality without than with cercariae. Consistent with mathematical models that suggest that stress should increase the impact of generalist parasites, the weight of the evidence from the field and laboratory suggests that ecologically relevant concentrations of agrochemicals generally increase the threat that trematodes pose to amphibians, highlighting the importance of elucidating interactions between anthropogenic activities and infectious disease in taxa of conservation concern.

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References

  1. Aponso, G. L. M., Magamage, C., Ekanayake, W. M., & Manuweera, G. K. (2003). Analysis of water for pesticides in two major agricultural areas of the dry zone. Annals of the Sri Lanka Department of Agriculture 5:7–22.

  2. Berven KA (1990). Factors affecting population fluctuations in larval and adult stages of the Wood Frog (Rana sylvatica). Ecology 71:1599-1608.

  3. Blanar CA, Munkittrick KR, Houlahan J, MacLatchy DL, and Marcogliese DJ (2009). Pollution and parasitism in aquatic animals: A meta-analysis of effect size. Aquatic Toxicology 93:18-28.

  4. Blaustein AR, and Kiesecker JM (2002). Complexity in conservation: lessons from the global decline of amphibian populations. Ecology Letters 5:597-608.

  5. Bridges C, Little E, Gardiner D, Petty J, and Huckins J (2004). Assessing the toxicity and teratogenicity of pond water in north-central Minnesota to amphibians. Environmental Science and Pollution Research 11:233-239.

  6. Bridges CM (2000). Long-term effects of pesticide exposure at various life stages of the southern leopard frog (Rana sphenocephala). Archives of Environmental Contamination and Toxicology 39:91-96.

  7. Budischak SA, Belden LK, and Hopkins WA (2008). Effects of malathion on embryonic development and latent susceptibility to trematode parasites in ranid tadpoles. Environmental Toxicology and Chemistry 27:2496-2500.

  8. Budischak SA, Belden LK, and Hopkins WA (2009). Relative toxicity of malathion to trematode-infected and noninfected Rana palustris tadpoles. Archives of Environmental Contamination and Toxicology 56:123-128.

  9. Cahill AE, Aiello-Lammens ME, Fisher-Reid MC, Hua X, Karanewsky CJ, Ryu HY, et al. (2013). How does climate change cause extinction? Proceedings of the Royal Society B-Biological Sciences 280:20121890.

  10. Civitello DJ, Cohen J, Fatima H, Halstead NT, Liriano J, McMahon TA, et al. (2015). Biodiversity inhibits parasites: broad evidence for the dilution effect. Proceedings of the National Academy of Sciences of the United States of America 112:8667–8867.

  11. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, et al. (2012). Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186-194.

  12. Goodman BA, and Johnson PTJ (2011). Disease and the Extended Phenotype: Parasites Control Host Performance and Survival through Induced Changes in Body Plan. PLoS One 6:e20193.

  13. Gotelli, NJ, and Ellison AM. (2004). A Primer of Ecological Statistics, Sinauer Associates, Inc., Sunderland, Massachusetts, pg. 348.

  14. Halstead NT, Civitello DJ, and Rohr JR (2015). Comparative toxicities of organophosphate and pyrethroid insecticides to aquatic macroarthropods. Chemosphere 135:265-271.

  15. Halstead NT, McMahon TA, Johnson SA, Raffel TR, Romansic JM, Crumrine PW, et al. (2014). Community ecology theory predicts the effects of agrochemical mixtures on aquatic biodiversity and ecosystem properties. Ecology Letters 17:932-941.

  16. Jayawardena UA, Navaratne AN, Amerasinghe PH, and Rajakaruna RS (2011). Acute and chronic toxicity of four commonly used agricultural pesticides on the Asian common toad, Bufo melanostictus Schneider. Journal of the National Science Foundation of Sri Lanka 39:267-276.

  17. Jayawardena UA, Rajakaruna RS, Navaratne AN, and Amerasinghe PH (2010a). Monostome cercariae induced malformations in amphibians: effect of infection at the pre-limb-bud stage tadpoles of Polypedates cruciger Blyth. Journal of the National Science Foundation of Sri Lanka 38:241-248.

  18. Jayawardena UA, Rajakaruna RS, Navaratne AN, and Amerasinghe PH (2010b). Toxicity of Agrochemicals to Common Hourglass Tree Frog (Polypedates cruciger) in Acute and Chronic Exposure. International Journal of Agriculture and Biology 12:641-648.

  19. Jayawardena UA, Tkach VV, Navaratne AN, Amerasinghe PH, and Rajakaruna RS (2013). Malformations and mortality in the Asian Common Toad induced by exposure to pleurolophocercous cercariae (Trematoda: Cryptogonimidae). Parasitology International 62:246-252.

  20. Johnson PTJ, Chase JM, Dosch KL, Hartson RB, Gross JA, Larson DJ, et al. (2007). Aquatic eutrophication promotes pathogenic infection in amphibians. Proceedings of the National Academy of Sciences of the United States of America 104:15781-15786.

  21. Johnson PTJ, Lunde KB, Ritchie EG, and Launer AE (1999). The effect of trematode infection on amphibian limb development and survivorship. Science 284:802-804.

  22. Johnson PTJ, Lunde KB, Zelmer DA, and Werner JK (2003). Limb deformities as an emerging parasitic disease in amphibians: Evidence from museum specimens and resurvey data. Conservation Biology 17:1724-1737.

  23. Johnson PTJ, Rohr JR, Hoverman JT, Kellermanns E, Bowerman J, and Lunde KB (2012). Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk. Ecology Letters 15:235-242.

  24. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, et al. (2008). Global trends in emerging infectious diseases. Nature 451:990-U994.

  25. Kelly DW, Poulin R, Tompkins DM, and Townsend CR (2010). Synergistic effects of glyphosate formulation and parasite infection on fish malformations and survival. Journal of Applied Ecology 47:498-504.

  26. Kiesecker JM (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.

  27. Koprivnikar J (2010). Interactions of environmental stressors impact survival and development of parasitized larval amphibians. Ecological Applications 20:2263-2272.

  28. Koprivnikar J, Marcogliese DJ, Rohr JR, Orlofske SA, Raffel TR, and Johnson PTJ (2012). Macroparasite infections of amphibians: what can they tell us? EcoHealth 9:342-360.

  29. Lafferty KD, and Holt RD (2003). How should environmental stress affect the population dynamics of disease? Ecology Letters 6:654-664.

  30. Linzey DW, Burroughs J, Hudson L, Marini M, Robertson J, Bacon JP, et al. (2003). Role of environmental pollutants on immune functions, parasitic infections and limb malformations in marine toads and whistling frogs from Bermuda. International Journal of Environmental Health Research 13:125-148.

  31. Martin LB, Hopkins WA, Mydlarz LD, and Rohr JR (2010). The effects of anthropogenic global changes on immune functions and disease resistance. Annals of the New York Academy of Sciences 1195:129-148.

  32. McMahon T, Boughton R, Crumrine P, Halstead N, Johnson S, Martin LB, et al. (2011). The fungicide chlorothalonil is nonlinearly associated with corticosterone levels, immunity, and mortality in amphibians. Environmental Health Perspectives 119:1098-1103.

  33. McMahon TA, Romansic JM, and Rohr JR (2013). Nonmonotonic and monotonic effects of pesticides on the pathogenic fungus Batrachochytrium dendrobatidis in culture and on tadpoles. Environmental Science & Technology 47:7958-7964.

  34. Meteyer CU (2000). Field guide to malformations of frogs and toads with radiographic interpretations. USGS/BRD/BSR-2000-0005, U.S. Geological Survey.

  35. Monnet-Tschudi F, Zurich MG, and Honegger P (2007). Neurotoxicant-induced inflammatory response in three-dimensional brain cell cultures. Human & Experimental Toxicology 26:339-346.

  36. Morley NJ, Irwin SW, and Lewis JW (2003). Pollution toxicity to the transmission of larval digeneans through their molluscan hosts. Parasitology 126:S5-S26.

  37. Pietrock M, and Marcogliese DJ (2003). Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19:293-299.

  38. Raffel TR, Hoverman JT, Halstead NT, Michel P, and Rohr JR (2010). Parasitism in a community context: Trait-mediated interactions with competition and predation. Ecology 91:1900-1907.

  39. Rajakaruna RS, Piyatissa P, Jayawardena UA, Navaratne AN, and Amerasinghe PH (2008). Trematode infection induced malformations in the common hourglass treefrogs. Journal of Zoology 275:89-95.

  40. Relyea RA (2005a). The lethal impact of roundup on aquatic and terrestrial amphibians. Ecological Applications 15:1118-1124.

  41. Relyea RA (2005b). The lethal impacts of roundup and predatory stress on six species of North American tadpoles. Archives of Environmental Contamination and Toxicology 48:351-357.

  42. Rohr JR, Civitello DJ, Crumrine PW, Halstead NT, Miller AD, Schotthoefer AM, et al. (2015). Predator diversity, intraguild predation, and indirect effects drive parasite transmission. Proceedings of the National Academy of Sciences of the United States of America 112:3008-3013.

  43. Rohr JR, Elskus AA, Shepherd BS, Crowley PH, McCarthy TM, Niedzwiecki JH, et al. (2003). Lethal and sublethal effects of atrazine, carbaryl, endosulfan, and octylphenol on the streamside salamander, Ambystoma barbouri. Environmental Toxicology and Chemistry 22:2385-2392.

  44. Rohr JR, Elskus AA, Shepherd BS, Crowley PH, McCarthy TM, Niedzwiecki JH, et al. (2004). Multiple stressors and salamanders: Effects of an herbicide, food limitation, and hydroperiod. Ecological Applications 14:1028-1040.

  45. Rohr JR, and McCoy KA (2010). A qualitative meta-analysis reveals consistent effects of atrazine on freshwater fish and amphibians. Environmental Health Perspectives 18:20-32.

  46. Rohr JR, and Palmer BD (2013). Climate change, multiple stressors, and the decline of ectotherms. Conservation Biology 27:741-751.

  47. Rohr JR, and Raffel TR (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.

  48. Rohr JR, Raffel TR, and Hall CA (2010). Developmental variation in resistance and tolerance in a multi-host-parasite system. Functional Ecology 24:1110-1121.

  49. Rohr JR, Raffel TR, Halstead NT, McMahon TA, Johnson SA, Boughton RK, et al. (2013). Early-life exposure to a herbicide has enduring effects on pathogen-induced mortality. Prooceedings of the Royal Society B-Biological Sciences 280:20131502.

  50. Rohr JR, Raffel TR, and Sessions SK (2009a). Digenetic trematodes and their relationship to amphibian declines and deformities. Pages 3067-3088 in H. Heatwole, editor. Amphibian Biology; vol. 8, Amphibian Decline: Diseases, Parasites, Maladies, and Pollution. Surrey Beatty & Sons, Chipping Norton, NSW, Australia

  51. Rohr JR, Raffel TR, Sessions SK, and Hudson PJ (2008a). Understanding the net effects of pesticides on amphibian trematode infections. Ecological Applications 18:1743-1753.

  52. Rohr JR, Sager T, Sesterhenn TM, and Palmer BD (2006). Exposure, postexposure, and density-mediated effects of atrazine on amphibians: Breaking down net effects into their parts. Environmental Health Perspectives 114:46-50.

  53. Rohr JR, Schotthoefer AM, Raffel TR, Carrick HJ, Halstead N, Hoverman JT, et al. (2008b). Agrochemicals increase trematode infections in a declining amphibian species. Nature 455:1235-1239.

  54. Rohr JR, Sesterhenn TM, and Stieha C (2011). Will climate change reduce the effects of a pesticide on amphibians?: Partitioning effects on exposure and susceptibility to pollution. Global Change Biology 17:657-666.

  55. Rohr JR, Swan A, Raffel TR, and Hudson PJ (2009b). Parasites, info-disruption, and the ecology of fear. Oecologia 159:447-454.

  56. Schotthoefer AM, Rohr JR, Cole RA, Koehler AV, Johnson CM, Johnson LB, et al. (2011). Effects of wetland vs. landscape variables on parasite communities of Rana pipiens: links to anthropogenic factors. Ecological Applications 21:1257-1271.

  57. Sears BF, Rohr JR, Allen JE, and Martin LB (2011). The economy of inflammation: when is less more? Trends in Parasitology 27:382-387.

  58. Sears BF, Snyder PW, and Rohr JR (2015). Host life history and host-parasite syntopy predict behavioural resistance and tolerance of parasites. Journal of Animal Ecology 84:625-636.

  59. Semlitsch RD, Scott DE, and Pechmann JHK (1988). Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69:184-192.

  60. Smith DC (1987). Adult recruitment in chorus frogs: Effects of size and date at aetamorphosis. Ecology 68:344-350.

  61. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, et al. (2004). Status and trends of amphibian declines and extinctions worldwide. Science 306:1783-1786.

  62. Voccia I, Blakley B, Brousseau P, and Fournier M (1999). Immunotoxicity of pesticides: a review. Toxicology and Industrial Health 15:119-132.

  63. Vonesh JR, and De la Cruz O (2002). Complex life cycles and density dependence: assessing the contribution of egg mortality to amphibian declines. Oecologia 133:325-333.

  64. Wacksman MN, Maul JD, and Lydy MJ (2006). Impact of atrazine on chlorpyrifos toxicity in four aquatic vertebrates. Archives of Environmental Contamination and Toxicology 51:681-689.

  65. Wake DB, and Vredenburg VT (2008). Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proceedings of the National Academy of Sciences of the United States of America 105:11466-11473.

  66. Wijesinghe MR, Bandara M, Ratnasooriya WD, and Lakraj GP (2011). Chlorpyrifos-induced toxicity in Duttaphrynus melanostictus (Schneider 1799) larvae. Archives of Environmental Contamination and Toxicology 60:690-696.

  67. Wilbur HM, and Collins JP (1973). Ecological aspects of amphibian metamorphosis. Science 182:1305-1314.

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Acknowledgements

Authors thank V. Imbuldeniya and Y.G. Ariyaratne for technical assistance. Financial support was provided by the National Science Foundation of Sri Lanka (NSF/2005/EB/02 to R.S.R.) and the US National Science Foundation (EF-1241889 to J.R.R.), the US Department of Agriculture (NRI 2006-01370 and 2009-35102-0543 to J.R.R), the US Environmental Protection Agency grant (CAREER 83518801 to J.R.R), and the US National Institute Of General Medical Sciences of the National Institutes of Health (R01GM109499 to J.R.R.).

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Correspondence to Rupika S. Rajakaruna.

Additional information

Uthpala A. Jayawardena and Jason R. Rohr have contributed equally to this work.

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Jayawardena, U.A., Rohr, J.R., Navaratne, A.N. et al. Combined Effects of Pesticides and Trematode Infections on Hourglass Tree Frog Polypedates cruciger . EcoHealth 13, 111–122 (2016). https://doi.org/10.1007/s10393-016-1103-2

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Keywords

  • Glyphosate
  • Chlorpyrifos
  • Dimethoate
  • Malformation
  • Propanil