Effects of the glyphosate-based herbicide Roundup WeatherMax® on metamorphosis of wood frogs (Lithobates sylvaticus) in natural wetlands

Aquatic Toxicology

Volumn 140-141, Issue , 2013, Pages 48-57

  Lanctot C ^a,d   Robertson, C ^a   Navarro Martin L ^a   Edge, C ^b,c   Melvin, S D ^b,d   Houlahan, J ^b   Trudeau, V L ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITY OF NEW BRUNSWICK   (Canada)

^c UNIVERSITY OF ALABAMA   (United States)

^d CENTRAL QUEENSLAND UNIVERSITY   (Australia)

Author keywords

Amphibian; Endocrine disruption; Glyphosate; Herbicide; Metamorphosis; MRNA

Indexed keywords

GLYPHOSATE; MESSENGER RNA; POTASSIUM SALT; SURFACTANT;

ENDOCRINE DISRUPTOR; FROG; GLYPHOSATE; MESOCOSM; METAMORPHOSIS; POLLUTION EXPOSURE; RNA; SURFACTANT; SURVIVAL;

ANIMAL TISSUE; ANURA; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEVELOPMENTAL TOXICITY; ENVIRONMENTAL EXPOSURE; GENE EXPRESSION; GENE FUNCTION; GROWTH RATE; LITHOBATES SYLVATICUS; METAMORPHOSIS; NONHUMAN; POPULATION ABUNDANCE; PRIORITY JOURNAL; TADPOLE; WETLAND;

AMPHIBIAN; ENDOCRINE DISRUPTION; GLYPHOSATE; HERBICIDE; METAMORPHOSIS; MRNA;

ANIMALS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCINE; HERBICIDES; LARVA; METAMORPHOSIS, BIOLOGICAL; RANIDAE; WATER POLLUTANTS, CHEMICAL; WETLANDS;

AMPHIBIA; LITHOBATES; RANA SYLVATICA;

EID: 84878911025     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2013.05.012     Document Type: Article

References (49)

1. Applied Biosystems Relative Quantitation of Gene Expression 1997, PE Applied Biosystems, Foster City, CA.
2. Boorse G.C., Kholdani C.A., Seasholtz A.F., Denver R.J. Corticotropin-releasing factor is cytoprotective in Xenopus tadpole tail: coordination of ligand, receptor, and binding protein in tail muscle cell survival. Endocrinology 2006, 147:1498-1507.
3. Brown D.D., Cai L. Amphibian metamorphosis. Developmental Biology 2007, 306:20-33.
4. Byer J.D., Struger J., Klawunn P., Todd A., Sverko E. Low cost monitoring of glyphosate in surface waters using the ELISA method: an evaluation. Environmental Science and Technology 2008, 42:6052-6057.
5. Clements C., Ralph S., Petras M. Genotoxicity of select herbicides in Rana catesbeiana tadpoles using the alkaline single-cell gel DNA electrophoresis (comet) assay. Environmental and Molecular Mutagenesis 1997, 29:277-288.
6. Collins J.P. Intrapopulation variation in the body size at metamorphosis and timing of metamorphosis in the bullfrog, Rana catesbeiana. Ecology 1979, 60:738-749.
7. Denver R.J., Glennemeier K.A., Boorse G.C. Endocrinology of complex life cycles: amphibians. Hormones, Brain and Behavior 2002, vol. 2:469-513.
8. Denver R.J. Stress hormones mediate environment-genotype interactions during amphibian development. General and Comparative Endocrinology 2009, 164:20-31.
9. Duarte-Guterman P., Ryan M.J., Hogan N.S., Trudeau V.L. Developmental profiles and thyroid hormone regulation of brain transcripts in frogs: a species comparison with emphasis on Physalaemus pustulosus. Brain, Behavior and Evolution 2012, 79:98-112.
10. Edge C.B., Gahl M.K., Pauli B.D., Thompson D.G., Houlahan J.E. Exposure of juvenile green frogs (Lithobates clamitans) in littoral enclosures to a glyphosate-based herbicide. Ecotoxicology and Environmental Safety 2011, 74:1363-1369.
11. Edge C.B., Thompson D.G., Hao C., Houlahan J.E. A silviculture application of the glyphosate-based herbicide Visionmax to wetlands has limited direct effects on amphibian larvae. Environmental Toxicology and Chemistry 2012, 31:2375-2383.
12. Edge C.B., Gahl M.K., Thompson D.G., Houlahan J.E. Laboratory and field exposures of two species of juvenile amphibian to a glyphosate-based herbicide and Batrachochytrium dendrobatidis. Science of the Total Environment 2013, 444:145-152.
13. Folmar L.C., Sanders H.O., Julin A.M. Toxicity of the herbicide glyphosate and several of its formulations to fish and aquatic invertebrates. Archives of Environment Contamination and Toxicology 1979, 8:269-278.
14. Fort D.J., Degitz S., Tietge J., Touart L.W. The hypothalamic-pituitary-thyroid (HPT) axis in frogs and its role in frog development and reproduction. Critical Reviews in Toxicology 2007, 37:117-161.
15. Galton V.A. The role of thyroid hormone in amphibian metamorphosis. Trends in Endocrinology & Metabolism 1992, 3:96-100.
16. Giesy J.P., Dobson S., Solomon K.R. Ecotoxicological risk assessment for Roundup herbicide. Reviews of Environment Contamination and Toxicology 2000, 167:35-120.
17. Gosner K.L. A simplified table for staging anuran embryos larvae with notes on identification. Herpetologica 1960, 16:183-190.
18. Hao C., Morse D., Morra F., Zhao X., Yang P., Nunn B. Direct aqueous determination of glyphosate and related compounds by liquid chromatography/tandem mass spectrometry using reversed-phase and weak anion-exchange mixed-mode column. Journal of Chromatography A 2011, 1218:5638-5643.
19. Harkey G.A., Semlitsch R.D. Effects of temperature on growth, development, and color polymorphism in the ornate chorus frog Pseudacris ornata. Copeia 1988, 1988(4):1001-1007.
20. Heckmann L.H., Sørensen P.B., Krogh P.H., Sørensen J.G. NORMA-Gene: a simple and robust method for qPCR normalization based on target gene data. BMC Bioinformatics 2011, 12:250.
21. Holmstrup M., Sørensen J.G., Heckmann L.-H., Slotsbo S., Hansen P., Hansen L.S. Effects of ozone on gene expression and lipid peroxidation in adults and larvae of the red flour beetle, Tribolium castaneum. Journal of Stored Products Research 2011, 47:378-384.
22. Howe C.M., Berrill M., Pauli B.D., Helbing C.C., Werry K., Veldhoen N. Toxicity of glyphosate-based pesticides to four North American frog species. Environmental Toxicology and Chemistry 2004, 23:1928-1938.
23. ® and amphibians: the importance of concentration, application time, and stratification. Environmental Toxicology and Chemistry 2010, 29:2016-2025.
24. ® more deadly to larval amphibians. Environmental Toxicology and Chemistry 2011, 30:446-454.
25. Krain L.P., Denver R.J. Developmental expression and hormonal regulation of glucocorticoid and thyroid hormone receptors during metamorphosis in Xenopus laevis. Journal of Endocrinology 2004, 181:91-104.
26. Lemly A.D., Richardson C.J. Guidelines for risk assessment in wetlands. Environmental Monitoring and Assessment 1997, 47:117-134.
27. Navarro-Martín L., Lanctôt C., Edge C., Houlahan J., Trudeau V.L. Expression profiles of metamorphosis-related genes during natural transformations in tadpoles of wild wood frogs (Lithobates sylvaticus). Canadian Journal of Zoology 2012, 90:1059-1071.
28. Opitz R., Lutz I., Nguyen N.-H., Scanlan T.S., Kloas W. Analysis of thyroid hormone receptor betaA mRNA expression in Xenopus laevis tadpoles as a means to detect agonism and antagonism of thyroid hormone action. Toxicology and Applied Pharmacology 2006, 212:1-13.
29. Relyea R.A. Growth and survival of five amphibian species exposed to combinations of pesticides. Environmental Toxicology and Chemistry 2004, 23:1737-1742.
30. Relyea R.A. The lethal impact of Roundup on aquatic and terrestrial amphibians. Ecological Applications 2005, 15:1118-1124.
31. Relyea R.A. The lethal impacts of Roundup and predatory stress on six species of North American tadpoles. Archives of Environment Contamination and Toxicology 2005, 48:351-357.
32. Relyea R.A. The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecological Applications 2005, 15:618-627.
33. ®. Wildlife Ecotoxicology: Forensic Approaches 2011, 267-300. Springer, New York. J. Elliott, C. Bishop, C. Morrisey (Eds.).
34. Relyea R.A. New effects of Roundup on amphibians: predators reduce herbicide mortality; herbicides induce antipredator morphology. Ecological Applications 2012, 22:634-647.
35. Relyea R.A., Jones D.K. The toxicity of Roundup Original MAX to 13 species of larval amphibians. Environmental Toxicology and Chemistry 2009, 28:2004-2008.
36. Relyea R.A., Schoeppner N.M., Hoverman J.T. Pesticides and amphibians: the importance of community context. Ecological Applications 2005, 15:1125-1134.
37. Schindler D.W. Detecting ecosystem responses to anthropogenic stress. Canadian Journal of Fisheries and Aquatic Sciences 1987, 44(Suppl. 1):6-25.
38. Semlitsch R.D., Caldwell J.P. Effects of density on growth, metamorphosis, and survivorship in tadpoles of Scaphiopus holbrooki. Ecology 1982, 63:905-911.
39. Shi Y.-B. Amphibian Metamorphosis 2000, Wiley-Liss, New York, Chichester, Weinheim, Brisbane, Singapore, Toronto.
40. Solomon K.R., Thompson D.G. Ecological risk assessment for aquatic organisms from over-water uses of glyphosate. Journal of Toxicology and Environmental Health, Part B: Critical Reviews 2003, 6:289-324.
41. Struger J., Thompson D., Staznik B., Martin P., McDaniel T., Marvin C. Occurrence of glyphosate in surface waters of southern Ontario. Bulletin of Environment Contamination and Toxicology 2008, 80:378-384.
42. Tata J.R. Amphibian metamorphosis as a model for the developmental actions of thyroid hormone. Molecular and Cellular Endocrinology 2006, 246:10-20.
43. Thompson D.G., Pitt D.G. A review of Canadian forest vegetation management research and practice. Annals of Forest Science 2003, 60:559-572.
44. Thompson D.G., Wojtaszek B.F., Staznik B., Chartrand D.T., Stephenson G.R. Chemical and biomonitoring to assess potential acute effects of Vision herbicide on native amphibian larvae in forest wetlands. Environmental Toxicology and Chemistry 2004, 23:843-849.
45. Tsui M.T.K., Chu L.M. Comparative toxicity of glyphosate-based herbicides: aqueous and sediment porewater exposures. Archives of Environmental Contamination and Toxicology 2004, 46:316-323.
46. Williams B.K., Semlitsch R.D. Larval responses of three Midwestern anurans to chronic, low-dose exposures of four herbicides. Archives of Environmental Contamination and Toxicology 2010, 58:819-827.
47. Wojtaszek B.F., Staznik B., Chartrand D.T., Stephenson G.R., Thompson D.G. Effects of Vision herbicide on mortality, avoidance response, and growth of amphibian larvae in two forest wetlands. Environmental Toxicology and Chemistry 2004, 23:832-842.
48. Woodburn A.T. Glyphosate: production, pricing and use worldwide. Pest Management Science 2000, 56:309-312.
49. Yadav S.S., Giri S., Singha U., Boro F., Giri A. Toxic and genotoxic effects of Roundup on tadpoles of the Indian skittering frog (Euflictis cyanophlyctis) in the presence and absence of predator stress. Aquatic Toxicology 2013, 132-133:1-8.