Laboratory and field exposure of two species of juvenile amphibians to a glyphosate-based herbicide and Batrachochytrium dendrobatidis

Science of the Total Environment

Volumn 444, Issue , 2013, Pages 145-152

  Edge, Christopher B ^a,c   Gahl, Megan K ^a,d   Thompson, Dean G ^b   Houlahan, Jeff E ^a  

^a UNIVERSITY OF NEW BRUNSWICK   (Canada)

^b GREAT LAKES FORESTRY CENTRE   (Canada)

^c UNIVERSITY OF ALABAMA   (United States)

^d UNIVERSITY OF ALASKA SOUTHEAST   (United States)

Author keywords

Amphibian; Chytridiomycosis; Glyphosate; Herbicide; Long Term Experimental Wetlands Area; Roundup

Indexed keywords

AMPHIBIAN; CHYTRIDIOMYCOSIS; GLYPHOSATES; LONG TERM EXPERIMENTAL WETLANDS AREA; ROUNDUP;

AGRICULTURE; EXPERIMENTS; WEED CONTROL;

HERBICIDES;

GLYPHOSATE;

AMPHIBIAN; CONCENTRATION (COMPOSITION); EXPERIMENTAL STUDY; FUNGUS; GLYPHOSATE; JUVENILE; LABORATORY METHOD; LARVA; TOXICITY;

ANIMAL HEALTH; ARTICLE; CAUSAL ATTRIBUTION; CHYTRIDIOMYCOSIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; FIELD STUDY; FUNGICIDE APPLICATION; JUVENILE ANIMAL; LABORATORY TEST; NONHUMAN; PRIORITY JOURNAL; RANA CLAMITANS; RANA PIPIENS; SURVIVAL; TOXICITY TESTING;

ANIMALS; CHYTRIDIOMYCOTA; GLYCINE; HERBICIDES; LABORATORIES; LARVA; MORTALITY; MYCOSES; NEW BRUNSWICK; RANA CLAMITANS; RANIDAE;

AMPHIBIA; BATRACHOCHYTRIUM DENDROBATIDIS; LITHOBATES;

EID: 84871370231     PISSN: 00489697     EISSN: 18791026     Source Type: Journal    
DOI: 10.1016/j.scitotenv.2012.11.045     Document Type: Article

References (54)

1. Beard K., Vogt K., Kulmatiski D.A. Top-down effects of a terrestrial frog on forest nutrient dynamics. Oecologia 2002, 133:583-593.
2. Beard K.H., Eschtruth A.K., Vogt K.A., Scatena F.N. The effects of the frog Eleutherodactylus coqui on invertebrates and ecosystem processes at two scales in the Luquillo Experimental Forest, Puerto Rico. J Trop Ecol 2003, 19:607-617.
3. Bernal M., Solomon K., Carrasquilla G. Toxicity of formulated glyphosate (glyphos) and cosmo-flux to larval and juvenile Columbian frogs 2. Field and laboratory microcosm acute toxicity. J Toxicol Environ Health A 2009, 72:966-973.
4. Boyle D.G., Boyle D.B., Olsen V., Morgan J.A.T., Hyatt A.D. Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis Aquat Organ 2004, 69:141-148.
5. Carey C. Hypothesis concerning the causes of the disappearance of boreal toads from the mountains of Colorado. Conserv Biol 1993, 7:355-362.
6. Carey C., Cohen N., Rollins-Smith L. Amphibian declines: an immunological perspective. Dev Comp Immunol 1999, 23:459-472.
7. Cohen J. A power primer. Psychol Bull 1992, 112:155-159.
8. Daszak P., Berger L., Cunningham A.A., Hyatt A.D., Green D.E., Speare R. Emerging infectious diseases and amphibian population declines. Emerg Infect Dis 1999, 5:735-748.
9. Daszak P., Strieby A., Cunningham A.A., Longcore J.E., Brown C.C., Porter D. Experimental evidence that the bullfrog (Rana catesbeiana) is a potential carrier of chytridiomycosis, an emerging fungal disease of amphibians. J Herpetol 2004, 14:201-207.
10. Degenhardt D., Humphries D., Cessna A.J., Messing P., Badiou P.H., Raina R., et al. Dissipation of glyphosate and aminomethylphosphonic acid in water and sediment of two Canadian prairie wetlands. J Environ Sci Health B 2012, 47:631-639.
11. Dinehart S.K., Smith L.M., McMury S.T., Anderson T.A., Smith P.N., Haukos D.A. Toxicity of a glufosinate- and several glyphosate-based herbicides to juvenile amphibians from the Southern High Plains, USA. Sci Total Environ 2009, 407:1065-1071.
12. Duke S.O., Powles S.B. Glyphosate: a once-in-a-century herbicide. Pest Manag Sci 2008, 64:319-325.
13. Durkin P.R. Glyphosate - human health and ecological risk assessment report 2003, Syracuse Environmental Research Associates Inc. USDA-FS (Ed.).
14. 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. Ecotoxicol Environ Saf 2011, 74:1363-1369.
15. 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. Environ Toxicol Chem 2012, 31:2375-2383.
16. Edginton A.N., Sheridan P.M., Stephenson G.R., Thompson D.G., Boermans H.J. Comparative effects of pH and Vision herbicide on two life stage of four anuran amphibian species. Environ Toxicol Chem 2004, 23:815-822.
17. Feng J., Thompson D., Reynolds P. Fate of glyphosate in a Canadian forest watershed. 1. Aquatic residues and off-target deposit. J Agric Food Chem 1990, 38:1110-1118.
18. Forson D.D., Storfor A. Atrazine increases ranavirus susceptibility in the tiger salamander, Ambystoma tigrinum. Ecol Appl 2006, 16:2325-2332.
19. Gahl M.K., Pauli B.D., Houlahan J.E. Effects of chytrid fungus and a glyphosate-based herbicide on survival and growth of wood frogs (Lithobates sylvaticus). Ecol Appl 2011, 21:2521-2529.
20. Garland S., Wood J., Skerratt J.F. Comparison of sensitivity between real-time detection of a TaqMan assay for Batrachochytrium dendrobatidis and conventional detection. Dis Aquat Organ 2011, 94:101-105.
21. Gibble R.E., Baer K.N. Effects of atrazine, agricultural runoff, and selected effluents on antimicrobial activity of skin peptides in Xenopus laevis. Ecotoxicol Environ Saf 2011, 74:593-599.
22. Giesy J., Dobson S., Solomon K. Ecotoxicological risk assessment of Roundup® herbicide. Rev Environ Contam Toxicol 2000, 167:35-120.
23. Goldsborough L.G., Beck A.E. Rapid dissipation of glyphosate in small forest ponds. Arch Environ Contam Toxicol 1989, 18:537-544.
24. Greenless M.J., Brown G.P., Webb J.K., Phillips B.L., Shine R. Effects of an invasive anuran [the cane toad (Bufo marinus)] on the invertebrate fauna of a tropical Australian floodplain. Anim Conserv 2006, 9:431-438.
25. Hanselman R., Rodriquez A., Lampo M., Fajardo-Ramos L., Aguirre A.A., Kilpatrick A.M., et al. Presence of an emerging pathogen of amphibians in introduced bullfrogs Rana catesbeiana in Venezuela. Biol Conserv 2004, 120:115-119.
26. Houlahan J.E., Findlay C.S., Schmidt B.R., Meyer A.H., Kuzmin S.L. Quantitative evidence for global amphibian population declines. Nature 2000, 404:752-755.
27. 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. Environ Toxicol Chem 2004, 23:1928-1938.
28. Kilpatrick A.M., Briggs C.J., Daszak P. The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends Ecol Evol 2010, 25:109-118.
29. Longcore J.E., Pessier A.P., Nichols D.K. Batrachochytrium dendrobatidis gen et sp nov, a chytrid pathogenic to amphibians. Mycologia 1999, 91:219-227.
30. Longcore J.R., Longcore J.E., Pessier A.P., Halteman W.A. Chytridiomycosis widespread in anurans of Northeastern United States. J Wildl Manag 2007, 71:435-444.
31. Mann R., Bidwell J. The toxicity of glyphosate and several glyphosate formulations to four species of Southwestern Australian frogs. Arch Environ Contam Toxicol 1999, 36:193-199.
32. Moore L.J., Fuentes L., Rodgers J.H., Bowerman W.W., Yarrow G.K., Chao W.Y., et al. Relative toxicity of the components of the original formulation of Roundup® to five North American anurans. Ecotoxicol Environ Saf 2011, 78:128-133.
33. Ollsen C., Knopper L. Task 2a: the history and science of herbicide use at CFB Gagetown from 1952 to present 2006, Jacques Whitford Ltd., Ottawa, Ontario.
34. Relyea R. The lethal impact of Roundup on aquatic and terrestrial amphibians. Ecol Appl 2005, 15:1118-1124.
35. Relyea R. The lethal impacts of Roundup and predatory stress on six species of North American tadpoles. Arch Environ Contam Toxicol 2005, 48:351-357.
36. Relyea R., Jones D. The toxicity of Roundup Original Max to 13 species of larval amphibians. Environ Toxicol Chem 2009, 28:2004-2008.
37. Retallick R.W.R., Miera V., Richards K.L., Field K.J., Collins J.P. A non-lethal technique for detecting the chytrid fungus Batrachochytrium dendrobatidis on tadpoles. Dis Aquat Organ 2006, 71:77-85.
38. Rollins-Smith L.A., Doersam J.K., Longcore J.E., Taylor S.K., Shamblin J.C., Carey C., et al. Antimicrobial peptide defences against pathogens associated with global amphibian declines. Dev Comp Immunol 2002, 26:63-72.
39. Rubin J.L., Gaines C.G., Jensen R.A. Enzymological basis for herbicidal action of glyphosate. Plant Physiol 1982, 70:833-839.
40. Semlitsch R.D. Introduction: general threats to amphibians. Amphibian conservation 2003, 1-7. Smithsonian Books, Washington, DC. R.D. Semlitsch (Ed.).
41. Solomon K.R., Thompson D.G. Ecological risk assessment for aquatic organisms from over-water uses of glyphosate. J Toxicol Environ Health A 2003, 6:289-324.
42. Stuart S.N., Chanson J.S., Cox N.A., Young B.E., Rodrigues A.S., Fischman D.L., et al. Status and trends of amphibian declines and extinctions worldwide. Science 2004, 306:1783-1786.
43. Thompson D.G. Ecological impacts of major forest-use pesticides. Ecological impacts of toxic chemicals 2011, 88-110. Bentham Science Publishers Ltd., Oak Park, Illinois. F. Sanchez-Bayo, P.J. Van den Brink, R.M. Mann (Eds.).
44. Thompson D.G., Pitt D.G., Buscarini T., Staznik B., Thomas D.R. Comparative fate of glyphosate and triclopyr herbicides in the forest floor and mineral soil of an Acadian forest regeneration site. Can J For Res 2000, l30:1808-1816.
45. Thompson D.G., Wojtaszek B.F., Satznik 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. Environ Toxicol Chem 2004, 23:843-849.
46. Thompson D., Chartrand D., Staznik B., Leach J., Hodgins P. Integrating advanced technologies for optimization of aerial herbicide applications. New For 2010, 40:45-66.
47. Travis J. Anuran size and metamorphosis: experimental test of a model based on intraspecific competition. Ecology 1984, 65:1155-1160.
48. Tsui M.T.K., Chu L.M. Comparative toxicity of glyphosate-based herbicides: aqueous and sediment porewater exposures. Arch Environ Contam Toxicol 2004, 46:316-323.
49. Tsui M., Chu L. Environmental fate and non-target impact of glyphosate-based herbicide (Roundup) in a subtropical wetland. Chemosphere 2008, 71:439-446.
50. Verburg P., Pringle C.M., Drake D.L. A stable isotope study of a neotropical stream food web prior to the extirpation of its large amphibian community. J Trop Ecol 2007, 23:643-651.
51. Wang N., Besser J.M., Buckler D.R., Honegger J.L., Ingersoll C.G., Johnson B.T., et al. Influence of sediment on the fate and toxicity of a polyethoxylated tallowamine surfactant system (MON 0818) in aquatic microcosms. Chemosphere 2005, 59:545-551.
52. Williams G.M., Kroes R., Munro I.C. Safety evaluation and risk assessment of the herbicide Roundup and its active ingredient, glyphosate, for humans. Regul Toxicol Pharmacol 2000, 31:117-165.
53. Wojtaszek B.F., Staznik B., Chartand 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. Environ Toxicol Chem 2004, 23:832-842.
54. Woodburn A. Glyphosate: production, pricing and use worldwide. Pest Manag Sci 2000, 56:309-312.