The Lethal Impacts of Roundup and Predatory Stress on Six Species of North American Tadpoles

  • R A RelyeaEmail author


The decline in amphibians across the globe has sparked a search for the causes, and recent evidence suggests a connection with pesticides. However, for most pesticides, tests on amphibians are rare and conducted only for short durations (1 to 4 days) and without natural stressors. Recent studies have discovered that the stress of predator cues in the water can make insecticides much more lethal to larval amphibians, but it is unknown whether this phenomenon can be generalized to other types of pesticides. Using six species of North American amphibian larvae (Rana sylvatica, R. pipiens, R. clamitans, R. catesbeiana, Bufo americanus, and Hyla versicolor), I examined the impact of a globally common herbicide (Roundup) on the survival of tadpoles for 16 days with and without the chemical cues emitted by predatory newts (Notophthalmus viridescens). LC5016-d estimates varied from 0.55 to 2.52 mg of active ingredient (AI)/L, which was considerably lower than the few previous studies using Roundup (1.5 to 15.5 mg AI/L). Moreover, in one of the six species tested (R. sylvatica), the addition of predatory stress made Roundup twice as lethal. This discovery suggests that synergistic interactions between predatory stress and pesticides may indeed be a generalizable phenomenon in amphibians that occurs with a wide variety of pesticides.


Glyphosate Malathion Roundup Carbaryl Wood Frog 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



My thanks to Josh Auld, Jason Hoverman, Laura Howell, Adam Marko, Christine Relyea, and Nancy Schoeppner for assisting with the experiments. I thank Josh Auld, Jason Hoverman, April Randle, and Nancy Schoeppner for reviewing the manuscript. This research was supported by the National Science Foundation.


  1. Alford, RA, Richards, SJ 1999Global amphibian declines: A problem in applied ecologyAnnu Rev Ecol Syst30133165CrossRefGoogle Scholar
  2. Aspelin AL, Grube AH (1999) Pesticide industry sales and usage: 1996 and 1997 market estimates (publication no. 733-R-99-001). Office of Pesticide Programs, U.S. Environmental Protection Agency.Google Scholar
  3. American Society for Testing and Materials1996Annual book of ASTM standardsAmerican Society for Testing and MaterialsPhiladelphia, PAGoogle Scholar
  4. Berger, L, Speare, R, Daszak, P, Green, DE, Cunningham, AA 1998Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central AmericaProc Natl Acad Sci U S A9590319036CrossRefPubMedGoogle Scholar
  5. Bishop, CA, Mahony, NA, Struger, J, Ng, P, Pettit, KE 1999Anuran development, density and diversity in relation to agricultural activity in the Holland River watershed, Ontario, Canada (1990–1992)Environ Monit Assess572143CrossRefGoogle Scholar
  6. Blaustein, AR, Kiesecker, JM 2002Complexity in conservation: Lessons from the global decline of amphibian populationsEcol Lett5597608CrossRefGoogle Scholar
  7. Blaustein, AR, Wake, DB, Sousa, WP 1994Amphibian declines: Judging stability, persistence, and susceptibility of populations to local and global extinctionsConserv Biol86071CrossRefGoogle Scholar
  8. Boone, MD, Semlitsch, RD 2001Interactions of an insecticide with larval density and predation in experimental amphibian communitiesConserv Biol15228238CrossRefGoogle Scholar
  9. Boone, MD, Semlitsch, RD 2002Interactions of an insecticide with competition and pond drying in amphibian communitiesEcol Appl12307316Google Scholar
  10. Boone, MD, Bridges, CM 1999The effect of temperature on the potency of carbaryl for survival of tadpoles of the green frog (Rana clamitans)Environ Toxicol Chem1814821484CrossRefGoogle Scholar
  11. Cooney, JD 1995Freshwater testsRand , GM eds. Fundamentals of aquatic toxicologyTaylor and FrancisLondon, United Kingdom71102Google Scholar
  12. Davidson, C, Shaffer, HB, Jennings, MR 2002Spatial tests of the pesticide drift, habitat destruction, UV-B, and climate-change hypotheses for California amphibian declinesConserv Biol1615881601CrossRefGoogle Scholar
  13. Edginton, AN, Sheridan, PM, Stephenson, GR, Thompson, DG, Boermans, HJ 2004Comparative effects of pH and Vision® herbicide on two life stages of four anuran amphibian speciesEnviron Toxicol Chem23815822PubMedGoogle Scholar
  14. Feng, JC, Thompson, DG, Reynolds, PE 1990Fate of glyphosate in a Canadian forest watershed. 1. Aquatic residues and off-target deposit assessmentJ Agric Food Chem3811101118Google Scholar
  15. Fisher, RN, Shaffer, HB 1996The decline of amphibians in California’s Great Central ValleyConserv Biol1013871397Google Scholar
  16. Giesy, JP, Dobson, S, Solomon, KR 2000Ecotoxicological risk assessment for Roundup herbicideRev Contam Toxicol16735120Google Scholar
  17. Goldsborough, LG, Brown, DJ 1989Rapid dissipation of glyphosate and aminomethylphosphonic acid in water and sediments of boreal forest pondsEnviron Toxicol Chem1211391147Google Scholar
  18. Gosner, KL 1960A simplified table for staging anuran embryos and larvae with notes on identificationHerpetologica16183190Google Scholar
  19. Hayes, TB, Collins, A, Lee, M, Mendoza, M, Noriega, N, Stuart, AA,  et al. 2002Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant dosesProc Natl Acad Sci USA9954765480PubMedGoogle Scholar
  20. Horner, LM 1990Dissipation of glyphosate and aminomethylphosphonic acid in forestry sites. Unpublished report MSL-9940Monsanto CompanySt. Louis, MOGoogle Scholar
  21. Houlihan, JE, Findlay, CS, Schmidt, BR, Meyers, AH, Kuzmin, SL 2001Quantitative evidence for global amphibian population declinesNature404752755Google Scholar
  22. Kats, LB, Dill, LM 1998The scent of death: Chemosensory assessment of predation risk by prey animalsEcoscience5361394Google Scholar
  23. Kiesecker, JM, Blaustein, AR, Belden, LK 2001Complex causes of amphibian population declinesNature410681684PubMedGoogle Scholar
  24. Lajmanovich, RC, Sandoval, MT, Peltzer, PM 2003Induction of mortality and malformation in Scinax nasicus tadpoles exposed to glyphosate formulationsBull Environ Contam Toxicol70612618PubMedGoogle Scholar
  25. LeNoir, JS, McConnell, LL, Fellers, GM, Cahill, TM, Seiber, JN 1999Summertime transport of current-use pesticides from California’s central valley to the Sierra Nevada Mountain range, USAEnviron Toxicol Chem1827152722Google Scholar
  26. Lohner, TW, Fisher, SW 1990Effects of pH and temperature on the acute toxicity and uptake of carbaryl in the midge, Chironomus ripariusAquat Toxicol16335354Google Scholar
  27. Mann, RM, Bidwell, JR 1999The toxicity of glyphosate and several glyphosate formulations to four species of southwestern Australian frogsArch Environ Contam Toxicol26193199Google Scholar
  28. Newton, M, Howard, KM, Kelpsas, BR, Danhaus, R, Lottman, CM, Dubelman, S 1984Fate of glyphosate in an Oregon forest ecosystemJ Agric Food Chem3211441151Google Scholar
  29. Pechmann, JHK, Scott, DE, Semlitsch, RD, Caldwell, JP, Vitt, LJ, Gibbons, JW 1991Declining amphibian populations: The problem of separating human impacts from natural fluctuationsScience253892895Google Scholar
  30. Pechmann, JHK, Wilbur, HM 1994Putting declining amphibian populations in perspective: Natural fluctuations and human impactsHerpetologica506584Google Scholar
  31. Perkins, PJ, Boermans, HJ, Stephenson, GR 2000Toxicity of glyphosate and triclopyr using the frog embryo teratogenesis assay-XenopusEnviron Toxicol Chem19940945Google Scholar
  32. Relyea, RA 2001Morphological and behavioral plasticity of larval anurans in response to different predatorsEcology82523540Google Scholar
  33. Relyea, RA 2003Predator cues and pesticides: A double dose of danger for amphibiansEcol Appl1315151521Google Scholar
  34. Relyea, RA 2004aSynergistic impacts of malathion and predatory stress on six species of North American tadpolesEnviron Toxicol Chem2310801084Google Scholar
  35. Relyea, RA 2004bThe growth and survival of five amphibian species exposed to combinations of pesticidesEnviron Toxicol Chem2310801084Google Scholar
  36. Relyea, RA, Mills, N 2001Predator-induced stress makes the pesticide carbaryl more deadly to grey treefrog tadpoles (Hyla versicolor)Proc Nat Acad Sci USA9824912496PubMedGoogle Scholar
  37. Skelly, DK, Yurewicz, KL, Werner, EE, Relyea, RA 2003Quantifying decline and distributional change in amphibiansConserv Biol17744751Google Scholar
  38. Smith, GR 2001Effects of acute exposure to a commercial formulation of glyphosate on the tadpoles of two species of anuransBull Contam Toxicol67483488Google Scholar
  39. Sparling, DW, Fellers, GM, McConnell, LS 2001Pesticides and amphibian population declines in California, USAEnviron Toxicol Chem2015911595PubMedGoogle Scholar
  40. Thompson, DG, Wojtaszek, BF, Staznik, B, Chartrand, DT, Stephenson, GR 2004Chemical and biomonitoring to assess potential acute effects of Vision® herbicide on native amphibian larvae in forest wetlandsEnviron Toxicol Chem23843849PubMedGoogle Scholar
  41. Tsui, MT, Chu, LM 2003Aquatic toxicity of glyphosate-based formulations: Comparison between different organisms and the effects of environmental factorsChemosphere5211891197PubMedGoogle Scholar
  42. U. S. Environmental Protection Agency, Hazard Evaluation Division1985aStandard evaluation procedure: Acute toxicity for freshwater invertebrates (PB86-129269)U. S. Environmental Protection AgencyWashington, DCGoogle Scholar
  43. U. S. Environmental Protection Agency, Hazard Evaluation Division1985bStandard evaluation procedure: Acute toxicity for freshwater fish (PB86-129277)U. S. Environmental Protection AgencyWashington, DCGoogle Scholar
  44. U. S. Environmental Protection Agency (1992) Pesticide tolerance for glyphosate. Fed. Reg. 57:8739 40, 10–98Google Scholar
  45. Wake, DB 1998Action on amphibiansTree13379380Google Scholar
  46. Wojtaszek, BF, Staznik, B, Chartrand, DT, Stephenson, GR, Thompson, DG 2004Effects of Vision® herbicide on mortality, avoidance response, and growth of amphibian larvae in two forest wetlandsEnviron Toxicol Chem23832842PubMedGoogle Scholar
  47. Zaga, A, Little, EE, Raben, CF, Ellersieck, MR 1998Photoenhanced toxicity of a carbamate insecticide to early life stage anuran amphibiansEnviron Toxicol Chem172543255Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2004

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of PittsburghPittsburghUSA

Personalised recommendations