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In situ effects of pesticides on amphibians in the Sierra Nevada

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Abstract

For more than 20 years, conservationists have agreed that amphibian populations around the world are declining. Results obtained through laboratory or mesocosm studies and measurement of contaminant concentrations in areas experiencing declines have supported a role of contaminants in these declines. The current study examines the effects of contaminant exposure to amphibians in situ in areas actually experiencing declines. Early larval Pseudacris regilla were translocated among Lassen Volcanic, Yosemite and Sequoia National Parks, California, USA and caged in wetlands in 2001 and 2002 until metamorphosis. Twenty contaminants were identified in tadpoles with an average of 1.3–5.9 (maximum = 10) contaminants per animal. Sequoia National Park, which had the greatest variety and concentrations of contaminants in 2001, also had tadpoles that experienced the greatest mortality, slowest developmental rates and lowest cholinesterase activities. Yosemite and Sequoia tadpoles and metamorphs had greater genotoxicity than those in Lassen during 2001, as determined by flow cytometry. In 2001 tadpoles at Yosemite had a significantly higher rate of malformations, characterized as hemimelia (shortened femurs), than those at the other two parks but no significant differences were observed in 2002. Fewer differences in contaminant types and concentrations existed among parks during 2002 compared to 2001. In 2002 Sequoia tadpoles had higher mortality and slower developmental rates but there was no difference among parks in cholinesterase activities. Although concentrations of most contaminants were below known lethal concentrations, simultaneous exposure to multiple chemicals and other stressors may have resulted in lethal and sublethal effects.

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References

  • Albert AK, Drouillard G, Haffner D, Dixon B (2007) Dietary exposure to low pesticide doses causes long-term immunosuppression in the leopard frog (Rana pipiens). Environ Toxicol Chem 26:1179–1185

    Article  CAS  Google Scholar 

  • Angermann JE, Fellers GM, Matsumura F (2002) Polychlorinated biphenyls and toxaphene in Pacific tree frog tadpoles (Hyla regilla) from the California Sierra Nevada, USA. Environ Toxicol Chem 21:2209–2215

    Article  CAS  Google Scholar 

  • Ankley G et al (1998) Overview of a workshop on screening method for detecting potential (anti-)estrogenic/androgenic chemicals in wildlife. Environ Toxicol Chem 17:68–87

    Article  CAS  Google Scholar 

  • Balch GC, Velez-Espino LA, Sweet C, Alaee M, Metcalfe CD (2006) Inhibition of metamorphosis in tadpoles of Xenopus laevis exposed to polybrominated diphenyl ethers (PBDEs). Chemosphere 64:328–338

    Article  CAS  Google Scholar 

  • Bickham JW, Mazet JA, Blake J, Smolen MJ, Lou YG, Ballachey BE (1998) Flow cytometric determination of genotoxic effects of exposure to petroleum in mink and sea otters. Ecotoxicology 7:191–199

    Article  CAS  Google Scholar 

  • Boone MD, James SM (2003) Interactions of an insecticide, herbicide, and natural stressors in amphibian community mesocosms. Ecol Appl 13:829–841

    Article  Google Scholar 

  • Boone MD, Semlitsch RD, Little EE, Doyle MC (2007) Multiple stressors in amphibian communities: effects of chemical contamination, bullfrogs, and fish. Ecol Appl 17:291–301

    Article  Google Scholar 

  • Calef GW (1973) Natural mortality of tadpoles in a population of Rana aurora. Ecology 54:741–758

    Article  Google Scholar 

  • Carey C, Alexander MA (2003) Climate change and amphibian declines: is there a link? Diver Distrib 9:111–121

    Article  Google Scholar 

  • Carlsson G, Kulkarni P, Larsson P, Norrgren L (2007) Distribution of BDE-99 and effects on metamorphosis of BDE-99 and -47 after oral exposure in Xenopus tropicalis. Aquat Toxicol 84:71–79

    Article  CAS  Google Scholar 

  • Castanaga LA, Asorey CM, Sandoval MT, Perez-Coll CS, Argibay TI, Herkovits J (2009) Stage-dependent teratogenic and lethal effects exerted by ultraviolet b radiation on Rhinella (Bufo) arenarum embryos. Environ Toxicol Chem 28:427–433

    Article  CAS  Google Scholar 

  • Coyle TL, Karasov WH (2010) Chronic, dietary polybrominated diphenyl ether exposure affects survival, growth, and development of Rana pipiens tadpoles. Environ Toxicol Chem 29:133–141

    Article  Google Scholar 

  • Datta S, Hansen L, McConnell L, Baker J, LeNoir J, Seiber JN (1998) Pesticides and PCB contaminants in fish and tadpoles from the Kaweah River basin, California. Bull Environ Contam Toxicol 60:829–836

    Article  CAS  Google Scholar 

  • Davidson C (2004) Declining downwind: amphibian population declines in california and historical pesticide use. Ecol Appl 14:1892–1902

    Article  Google Scholar 

  • Davidson C, Shaffer HB, Jennings MR (2002) Declines of the California red-legged frog: climate, UV-B, habitat, and pesticides hypotheses. Ecol Appl 11:464–479

    Article  Google Scholar 

  • Drost CA, Fellers GM (1996) Collapse of a regional frog fauna in the Yosemite Area of the California Sierra Nevada, USA. Cons Biol 10:414–425

    Article  Google Scholar 

  • Ellman GL, Courtney KD, Andres V Jr, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–90

    Article  CAS  Google Scholar 

  • Fellers GM, Drost CA (1993) Disappearance of the Cascades frog Rana cascadae at the southern end of its range, California, USA. Biol Cons 65:177–181

    Article  Google Scholar 

  • Fellers GM, Kleeman PM (2007) California red-legged frog (Rana draytonii) movement and habitat use: implications for conservation. J Herpetol 41:276–286

    Article  Google Scholar 

  • Fellers GM, McConnell LL, Pratt D, Datta S (2004) Pesticides in mountain yellow-legged frogs (Rana muscosa) from the Sierra Nevada Mountains of California, USA. Environ Toxicol Chem 23:2170–2177

    Article  CAS  Google Scholar 

  • Fisher RN, Shaffer HB (1996) The decline of amphibians in California’s great central valley. Cons Biol 10:1387–1397

    Article  Google Scholar 

  • Goodman BA, Johnson PTJ (2011) Disease and the extended phenotype: parasites control host performance and survival through induced changes in body plan. PlosOne. doi:10.1371/journal.pone.0020193

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190

    Google Scholar 

  • Hageman KJ, Simonich SL, Campbell DH, Wilson GR, Landers DH (2006) Atmospheric deposition of current-use and historic-use pesticides in snow at national parks in the Western United States. Environ Sci Technol 40:3174–3180

    Article  CAS  Google Scholar 

  • Harris ML, Bogart JP (1997) A cage for evaluation of in situ water quality using frog eggs and tadpoles. Herpetol Rev 28:134–135

    Google Scholar 

  • Hopkins WA, DuRant SE, Staub BP, Rowe CL, Jackson BP (2006) Reproduction, embryonic development and maternal transfer of contaminants in the amphibian Gastrophryne carolinensis. Environ Health Perspec 114:661–666

    Article  CAS  Google Scholar 

  • Houlahan JE, Findlay CS (2003) The effects of adjacent land use on wetland amphibian species richness and community composition. Can J Fish Aquat Sci 60:1078–1094

    Article  Google Scholar 

  • Houlahan JE, Findlay CS, Schmidt BR, Meyers, Kuzmin SL (2000) Quantitative evidence for global amphibian population declines. Nature 404:752–754

    Article  CAS  Google Scholar 

  • Johnson CS, Schwarzbach SE, Henderson JD, Wilson BW, Tjeerdema RS (2005) Influence of water temparature on acetylcholinestersase activity in Pacific treefrogs (Hyla regilla). Environ Toxicol Chem 24:2074–2077

    Article  CAS  Google Scholar 

  • Kerby JL, Storfer A (2009) Combined effects of atrazine and chlorpyrifos on susceptibility of the tiger salamander to Ambystoma tigrinum virus. EcoHealth 6:91–98

    Article  Google Scholar 

  • Knapp RA (2005) Effects of nonnative fish and habitat characteristics on lentic herpetofauna in Yosemite National Park, USA. Biol Cons 121:265–279

    Article  Google Scholar 

  • Lannoo MJ (1998) Status and conservation of midwestern Amphibians. University of Iowa Press, Iowa

    Google Scholar 

  • Lehotay SJ, Mastovska K, Jong Y (2005) Evlauation of two fast and easy methods for pesticide residue analysis in fatty food matrices. J Assoc Off Analyt Chem 88:630–638

    CAS  Google Scholar 

  • LeNoir JS, McConnell LL, Fellers GM, Cahill TM, Seiber JN (1999) Summertime transport of current-use pesticides from California’s Central Valley to the Sierra Nevada Mountain Range, USA. Environ Toxicol Chem 18:2715–2722

    Article  CAS  Google Scholar 

  • Lowcock LA, Sharbel TF, Bonin J, Ouellet M, Rodrigue J, DesGrange JL (2011) Flow cytometric assay for in vivo genotoxic effects of pesticides in green frogs (Rana clamitans). Aquat Toxicol 38:241–255

    Article  Google Scholar 

  • McCallum ML (2007) Amphibian decline or extinction? Current declines dwarf background extinction rate. J Herpetol 41:483–491

    Article  Google Scholar 

  • McConnell LL, LeNoir JS, Datta S, Seiber JN (1998) Wet deposition of current-use pesticides in the Sierra Nevada Mountain Range, California, USA. Environ Toxicol Chem 17:1908–1916

    Article  CAS  Google Scholar 

  • Meteyer CU, Loeffler IK, Fallon JF, Converse KA, Green E, Helgen JC, Kersten S, Levey R, Eaton-Poole L, Burkhart JG (2000) Hind limb malformations in free-living northern leopard frogs (Rana pipiens) from Maine, Minnesota, and Vermont suggest multiple etiologies. Teratology 62:151–171

    Article  CAS  Google Scholar 

  • Orton F, Carr JA, Handy RD (2006) Effects of nitrate and atrazine on larval development and sexual differentiation in the northern leopard frog Rana pipiens. Environ Toxicol Chem 25:65–71

    Article  CAS  Google Scholar 

  • Petranka JW (2007) Evolution of complex life cycles of amphibians: bridging the gap between metapopulation dynamics and life history evolution. Evol Ecol 21:751–764

    Article  Google Scholar 

  • Relyea RA (2003) Predator cues and pesticides: a double dose of danger for amphibians. Ecol Appl 13:1515–1521

    Article  Google Scholar 

  • Relyea RA (2007) Getting out alive: how predators affect the decision to metamorphose. Oecologia 152:389–400

    Article  Google Scholar 

  • Rohr JR, Crumrine PW (2005) Effects of an herbicide and an insecticide on pond community structure and processes. Ecol Appl 15:1135–1147

    Article  Google Scholar 

  • Rohr JR, Raffel TR, Romansic JM, McCallum H, Hudson PJ (2008) Evaluating the links between climate, disease spread, and amphibian declines. Proc Natl Acad Sci USA 105:17436–17441

    Article  CAS  Google Scholar 

  • Rorabaugh J (2005) Rana pipiens Schreber, 1782, northern leopard frog. In: Lannoo M (ed) Amphibian declines: the conservation status of United States species. University of California, Berkeley, pp 563–566

    Google Scholar 

  • Sawin VL, McBee K, Bickham JW (1987) Flow-cytometry as a short-term assay for invivo clastogenicity: effects in various tissues. Environ Mutagen 9:94

    Google Scholar 

  • Sayim F (2010) Toxicity of trifluralin on the embryos and larvae of the red-bellied toad, Bombina bombina. Turkish J Zool 34:479–486

    CAS  Google Scholar 

  • Sparling DW (2003) A review of the role of contaminants in amphibian declines. In: Hoffman D, Rattner BA, Cairns J (eds) Handbook of ecotoxicology. Lewis Publishers, Boca Raton, pp 1099–1128

    Google Scholar 

  • Sparling DW, Fellers G (2007) Comparative toxicity of chlorpyrifos, diazinon, malathion and their oxon derivatives to larval Rana boylii. Environ Poll 147:535–539

    Article  CAS  Google Scholar 

  • Sparling DW, Fellers GM (2009) Toxicity of two insecticides to California, USA, anurans and its relevance to declining amphibian populations. Environ Toxicol Chem 28:1696–1703

    Article  CAS  Google Scholar 

  • Sparling DW, Fellers GM, McConnell LL (2001) Pesticides and amphibian population declines in California, USA. Environ Toxicol Chem 20:1591–1595

    Article  CAS  Google Scholar 

  • Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786

    Article  CAS  Google Scholar 

  • U.S. Fish Wildlife Service (2002) Endangered and threatened wildlfie and plants: determination of endangered status for the southern California distinct vertebrate population status of the mountain yellow-legged frog (Rana muscosa). Federal Register 50 CFR Part 17, 44382–44392

  • Wake D (1991) Declining amphibian populations. Science 253:860

    Article  CAS  Google Scholar 

  • Weir SM, Yu S, Salice CJ (2012) Acute toxicity of herbicide formulations and chronic toxicity of technical-grade trifluralin to larval green frogs (Lithobates clamitans). Environ Toxicol Chem 31:2029–2034

    Article  CAS  Google Scholar 

  • Whiles MR, Lips KR, Pringle CM, Kilham SS, Bixby RJ, Brenes R, Connelly S, Colon-Gaud JC, Hunte-Brown M, Huryn AD, Montgomery C, Peterson S (2006) The effects of amphibian population declines on the structure and function of Neotropical stream ecosystems. Front Ecol Environ 4:27–34

    Article  Google Scholar 

  • Wilbur HM, Collins JP (1973) Ecological aspects of amphibian metamorphosis. Science 182:1305–1314

    Article  CAS  Google Scholar 

  • Yin X, Zhu G, Li X, Liu SY (2009) Genotoxicity evaluation of chlorpyrifos to amphibian Chinese toad (Amphibian: Anura) by comet assay and micronucleus test. Mut Gen Toxicol Environ Mutagen 680:2–6

    Article  CAS  Google Scholar 

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Acknowledgments

Field assistants for this project included Erika Cowman Schetter, Shenandoah Marr, Deborah Purce, Pamela Widder and Patrick Kleeman. National Park staff including David Graber, Annie Esperanza, Harold Werner, Steve Thompson, Louise Johnson, Jonathan Arnold, and Sara Koenig provided logistical support. David Bradford and Holly Puglis provided comments on an earlier draft of this manuscript. Use of trade, product, or firm names does not imply U.S. Government endorsement.

Funding

This study was funded by the United States Geological Survey project “The Role of Pesticides in the Decline of Amphibians in the Sierra Nevada Mountains,” Amphibian Research and Monitoring Initiative (USGS) from 2000–2003. Additional support was provided by the United States Fish and Wildlife Service, Endangered Species Division, and the Caesar Kleberg Chair in Wildlife Ecology at Texas A&M University.

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The authors declare that they have no conflict of interest.

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Correspondence to Thomas Lacher.

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Sparling, D.W., Bickham, J., Cowman, D. et al. In situ effects of pesticides on amphibians in the Sierra Nevada. Ecotoxicology 24, 262–278 (2015). https://doi.org/10.1007/s10646-014-1375-7

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