New effects of Roundup on amphibians: Predators reduce herbicide mortality; Herbicides induce antipredator morphology

Ecological Applications

Volumn 22, Issue 2, 2012, Pages 634-647

  Relyea, Rick A ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

American toads (Bufo americanus or Anaxyrus americanus); Amphibian decline; Dragonflies (Anax junius); Glyphosphate; Inducible defense; Leopard frogs (Rana pipiens or Lithobates pipiens); Newts (Notophthalmus viridescens); Phenotypic plasticity; Synergy; Wood frogs (Rana sylvatica or Lithobates sylvaticus)

Indexed keywords

DRUG DERIVATIVE; GLYCINE; GLYPHOSATE; HERBICIDE;

ADAPTATION; ALGA; AMPHIBIAN; ANTIPREDATOR DEFENSE; DRAGONFLY; ENVIRONMENTAL STRESS; HERBICIDE; LEAF LITTER; MESOCOSM; MIMICRY; MORTALITY; NONTARGET ORGANISM; PHENOTYPIC PLASTICITY; POPULATION DECLINE; PREDATOR-PREY INTERACTION; SYNERGISM; WATER COLUMN; WETLAND; ZOOPLANKTON;

ANIMAL; ANURA; ARTICLE; DRUG EFFECT; GROWTH, DEVELOPMENT AND AGING; LARVA; PHYSIOLOGY; POLLUTANT; PREDATION; SALAMANDRIDAE; WETLAND;

ANIMALS; ANURA; ENVIRONMENTAL POLLUTANTS; GLYCINE; HERBICIDES; LARVA; PREDATORY BEHAVIOR; SALAMANDRIDAE; WETLANDS;

ALGAE; AMPHIBIA; ANAX JUNIUS; ANISOPTERA (DRAGONFLIES); ANURA; BUFO AMERICANUS; LITHOBATES; NOTOPHTHALMUS VIRIDESCENS; PANTHERA PARDUS; RANA PIPIENS; RANA SYLVATICA; SALAMANDRIDAE; VERTEBRATA;

EID: 84859522752     PISSN: 10510761     EISSN: None     Source Type: Journal    
DOI: 10.1890/11-0189.1     Document Type: Article

References (69)

1. Altwegg, R., and H.-U. Reyer. 2003. Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57:872-882. (Pubitemid 36573208)
2. Babbitt, K. J. 2001. Behaviour and growth of southern leopard frog (Rana sphenocephala) tadpoles: effects of food and predation risk. Canadian Journal of Zoology 79:809-814. (Pubitemid 32752542)
3. Barolo, D. 1993. Reregistration eligibility decision for glyph-osate. EPA 738-R-93-014. Reregistration Report. U.S. Environmental Protection Agency, Washington, D.C., USA.
4. Barry, M. J. 1998. Endosulfan-enhanced crest induction in Daphnia longicephala: Evidence for cholinergic innervation of kairomone receptors. Journal of Plankton Research 20:1219-1231. (Pubitemid 28362075)
5. Barry, M. J. 1999. The effects of a pesticide on inducible phenotypic plasticity in Daphnia. Environmental Pollution 104:217-224. (Pubitemid 29060760)
6. Barry, M. J. 2000. Effects of endosulfan on Chaoborus-induced life-history shifts and morphological defenses in Daphnia pulex. Journal of Plankton Research 22:1705-1718.
7. Baylis, A. D. 2000. Why glyphosate is a global herbicide: strengths, weaknesses and prospects. Pesticide Management Science 56:299-308. (Pubitemid 30167603)
8. Beketov, M. A., and M. Liess. 2005. Acute contamination with esfenvalerate and food limitation: chronic effects on the mayfly, Cleon dipterum. Environmental Toxicology and Chemistry 24:1281-1286. (Pubitemid 40627954)
9. Bernal, M. H., K. R. Solomon, and G. Carrasquilla. 2009. Toxicity of formulated glyphosate (Glyphos) and Cosmo-Flux to larval Colombian frogs 1. Laboratory acute toxicity. Journal of Toxicology and Environmental Health, Part A 72:961-965.
10. Boutin, C., K. E. Freemark, and C. J. Keddy. 1995. Overview and rationale for developing regulatory guidelines for nontarget plant testing with chemical pesticides. Environmental Toxicology and Chemistry 14:1465-1475.
11. Chen, C. Y., K. M. Hathaway, and C. L. Folt. 2004. Multiple stress effects of Visiont herbicide, pH, and food on zooplankton and larval amphibian species from forest wetlands. Environmental Toxicology and Chemistry 23:823-831. (Pubitemid 38418631)
12. Clements, W. H., and J. R. Rohr. 2009. Community responses to contaminants: using basic ecological principles to predict ecotoxicological effects. Environmental Toxicology and Chemistry 28:1789-1800.
13. Dinehart, S. K., L. M. Smith, S. T. McMurry, P. N. Smith, T. A. Anderson, and D. A. Haukos. 2010. Acute and chronic toxicity of Roundup Weathermaxt and Ignitet 280SL to larval Spea multiplicata and S. bombifrons from the Southern High Plains, USA. Environmental Pollution 158:2610-2617.
14. Edginton, A. N., P. M. Sheridan, G. R. Stephenson, D. G. Thompson, and H. J. Boermans. 2004. Comparative effects of pH and Visiont herbicide on two life stages of four anuran amphibian species. Environmental Toxicology and Chemistry 23:815-822. (Pubitemid 38418630)
15. Edwards, W. M., G. B. Triplett, Jr., and R. M. Kramer. 1980. A watershed study of glyphosate transport in runoff. Journal of Environmental Quality 9:661-665. (Pubitemid 11166581)
16. Giesy, J. P., S. Dobson, and K. R. Solomon. 2000. Ecotoxi-cological risk assessment for Roundupt herbicide. Reviews of Environmental Contamination and Toxicology 167:35-120.
17. Glennemeier, K. A., and R. J. Denver. 2002. Small changes in whole-body corticosterone content affect larval Rana pipiens fitness components. General and Comparative Endocrinology 127:16-25.
18. Gosner, K. L. 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpeto-logica 16:183-190.
19. Hanazato, T. 1991. Pesticides as chemical agents inducing helmet formation in Daphnia ambigua. Freshwater Biology 26:419-424.
20. Hanazato, T. 1999. Anthropogenic chemicals (insecticides) disturb natural organic chemical communication in the plankton community. Environmental Pollution 105:137-142. (Pubitemid 29094757)
21. Hanazato, T., and H. Hirokawa. 2004. Changes in vulnerability of Daphnia to an insecticide application depending on the population phase. Freshwater Biology 49:402-409. (Pubitemid 38448305)
22. Howe, C. M., M. Berrill, P. D. Pauli, C. C. Helbring, K. Werry, and N. Veldhoen. 2004. Toxicity of glyphosate-cased pesticides to four North American frog species. Environmental Toxicology and Chemistry 23:1928-1938. (Pubitemid 39006864)
23. Jones, D. K., J. R. Hammond, and R. A. Relyea. 2010. Roundupt and amphibians: the importance of concentration, application time, and wetland stratification. Environmental Toxicology and Chemistry 29:2016-2025.
24. Jones, D. K., J. R. Hammond, and R. A. Relyea. 2011. Roundupt and amphibians: Competitive stress can make the herbicide Roundupt more deadly to larval amphibians. Environmental Toxicology and Chemistry 30:446-454.
25. Lajmanovich, R. C., M. T. Sandoval, and P. M. Peltzer. 2003. Induction of mortality and malformation in Scinax nasicus tadpoles exposed to glyphosate formulations. Bulletin of Environmental Contamination and Toxicology 70:612-618. (Pubitemid 36373623)
26. Lima, S. L. 2002. Putting predators back into behavioral predator-prey interactions. Trends in Ecology and Evolution 17:70-75. (Pubitemid 34142587)
27. Ma, S., S. C. Kassinos, D. F. Kassinos, and E. Akylas. 2008. Modeling the impact of water withdrawal schemes on the transport of pesticides in the Kouris Dam (Cyprus). Global NEST Journal 10:350-358.
28. Mann, R. M., and J. R. Bidwell. 1999. The toxicity of glyphosate and several glyphosate formulations to four species of southwestern Australian frogs. Archives of Environmental Contamination and Toxicology 36:193-199. (Pubitemid 29058993)
29. Miner, B. G., S. E. Sultan, S. G. Morgan, D. K. Padilla, and R. A. Relyea. 2005. Ecological consequences of phenotypic plasticity. Trends in Ecology and Evolution 20:687-692.
30. Oda, S., Y. Kato, H. Watanabe, N. Tatarazako, and T. Iguchiz. 2011. Morphological changes in Daphnia galeata induce by a crustacean terpenoid hormone and its analog. Environmental Toxicology and Chemistry 30:232-238.
31. Payton, M. E., M. H. Greenstone, and N. Schenker. 2003. Overlapping confidence intervals or standard error intervals: what do they mean in terms of statistical significance? Journal of Insect Science 3:34.
32. Perez, G. L., et al. 2007. Effects of the herbicide Roundup on freshwater microbial communities: a mesocosm study. Ecological Applications 17:2310-2322. (Pubitemid 351323470)
33. Postma, J. F., M. C. Buckert-de Jogn, N. Staats, and C. Davids. 1994. Chronic toxicity of cadmium to Chironomus riparius (Diptera: Chironomidae) at different food levels. Archives of Environmental Contamination and Toxicology 26:143-148. (Pubitemid 24175466)
34. Quinn, G. P., and M. J. Keough. 2002. Experimental design and data analysis for biologists. Cambridge University Press, Cambridge, UK.
35. Relyea, R. A. 2000. Trait-mediated effects in larval anurans: Reversing competition with the threat of predation. Ecology 81:2278-2289.
36. Relyea, R. A. 2001. Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82:523-540. (Pubitemid 32152271)
37. Relyea, R. A. 2002a. Competitor-induced plasticity in tadpoles: consequences, cues, and connections to predator-induced plasticity. Ecological Monographs 72:523-540. (Pubitemid 36198931)
38. Relyea, R. A. 2002b. Local population differences in pheno-typic plasticity: predator-induced changes in wood frog tadpoles. Ecological Monographs 72:77-93. (Pubitemid 34124494)
39. Relyea, R. A. 2003a. How prey respond to combined predators: a review and an empirical test. Ecology 84:1827-1839. (Pubitemid 37435712)
40. Relyea, R. A. 2003b. Predator cues and pesticides: a double dose of danger for amphibians. Ecological Applications 13:1515-1521. (Pubitemid 38362231)
41. Relyea, R. A. 2004a. Fine-tuned phenotypes: tadpole plasticity under 16 combinations of predators and competitors. Ecology 85:172-179. (Pubitemid 38258873)
42. Relyea, R. A. 2004b. Growth and survival of five amphibian species exposed to combinations of pesticides. Environmental Toxicology and Chemistry 23:1737-1742. (Pubitemid 38747246)
43. Relyea, R. A. 2004c. Synergistic impacts of malathion and predatory stress on six species of North American tadpoles. Environmental Toxicology and Chemistry 23:1080-1084. (Pubitemid 38418661)
44. Relyea, R. A. 2005a. The heritability of inducible defenses in tadpoles. Journal of Evolutionary Biology 18:856-866. (Pubitemid 40968538)
45. Relyea, R. A. 2005b. The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecological Applications 15:618-627. (Pubitemid 40441302)
46. Relyea, R. A. 2005c. The lethal impact of Roundup on aquatic and terrestrial amphibians. Ecological Applications 15:1118-1124. (Pubitemid 41061028)
47. Relyea, R. A. 2005d. The lethal impacts of Roundup and predatory stress on six species of North American tadpoles. Archives of Environmental Contamination and Toxicology 48:351-357.
48. Relyea, R. A. 2006. The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities: response. Ecological Applications 15:1527-1532.
49. Relyea, R. A. 2011. Amphibians are not ready for Roundupt. Pages 267-300 in J. Elliott, C. Bishop, and C. Morrisey, editors. Wildlife ecotoxicology-forensic approaches. Springer, New York, New York, USA.
50. Relyea, R. A., and J. R. Auld. 2004. Having the guts to compete: How intestinal plasticity explains costs of inducible defenses. Ecology Letters 7:869-875. (Pubitemid 39175199)
51. Relyea, R. A., and J. R. Auld. 2005. Predator-and competitor-induced plasticity: How changes in foraging morphology affect phenotypic trade-offs. Ecology 86:1723-1729. (Pubitemid 40938773)
52. Relyea, R. A., and J. T. Hoverman. 2006. Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. Ecology Letters 9:1157-1171.
53. Relyea, R. A., and D. K. Jones. 2009. The toxicity of Roundup Original MAXt to 13 species of larval amphibians. Environmental Toxicology and Chemistry 28:2004-2008.
54. Relyea, R. A., and N. Mills. 2001. Predator-induced stress makes pesticide carbaryl more deadly to gray treefrog tadpoles (Hyla versicolor). Proceedings of the National Academy of Sciences USA 98:2491-2496. (Pubitemid 32209509)
55. Relyea, R. A., N. M. Schoeppner, and J. T. Hoverman. 2005. Pesticides and amphibians: the importance of community context. Ecological Applications 15:1125-1134. (Pubitemid 41061029)
56. Relyea, R. A., and E. E. Werner. 1999. Quantifying the relation between predator-induced behavior and growth performance in larval anurans. Ecology 80:2117-2124. (Pubitemid 29432319)
57. Sakamoto, M., K.-H. Change, and T. Hanazato. 2006. Inhibition of development of anti-predator morphology in the small cladoceran Bosmina by an insecticide: Impact of an anthropogenic chemical on prey-predator interactions. Freshwater Biology 51:1974-1983. (Pubitemid 44401130)
58. Schoeppner, N. M., and R. A. Relyea. 2005. Damage, digestion, and defense: The roles of alarm cues and kairomones for inducing prey defenses. Ecology Letters 8:505-512. (Pubitemid 40641139)
59. Schoeppner, N. M., and R. A. Relyea. 2009. Interpreting the smells of predation: How alarm cues and kairomones induce different prey defenses. Functional Ecology 23:1114-1121.
60. Semlitsch, R. D., D. C. Scott, and J. H. K. Pechmann. 1988. Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69:184-192. (Pubitemid 19317739)
61. Smith, D. C. 1987. Adult recruitment in chorus frogs: effects of size and date at metamorphosis. Ecology 68:344-350.
62. Solomon, K. R., and D. G. Thompson. 2003. Ecological risk assessment for aquatic organisms from over-water uses of glyphosate. Journal of Toxicology and Environmental Health-Part B-Critical Reviews 6:289-324. (Pubitemid 36520937)
63. Sudo, M., T. Kawachi, Y. Hida, and T. Kunimatsu. 2004. Spatial distribution and seasonal changes of pesticides in Lake Biwa, Japan. Limnology 5:77-86. (Pubitemid 39250848)
64. Teplitsky, C., H. Piha, A. Laurila, and J. Merila. 2005. Common pesticide increases costs of antipredator defenses in Rana temporaria tadpoles. Environmental Science and Technology 39:6079-6085. (Pubitemid 41170413)
65. Thompson, D. G., B. F. Wojtaszek, B. Staznik, D. T. Chartrand, and G. R. Stephenson. 2004. Chemical and biomonitoring to assess potential acute effects of Visiont herbicide on native amphibian larvae in forest wetlands. Environmental Toxicology and Chemistry 23:843-849. (Pubitemid 38418633)
66. Tsui, M. T. K., and L. M. Chi. 2003. Aquatic toxicity of glyphosate-based formulations: Comparison between different organisms and the effects of environmental factors. Chemosphere 52:1189-1197. (Pubitemid 36781432)
67. Van Buskirk, J. 2002. A comparative test of the adaptive plasticity hypothesis: Relationships between habitat and phenotype in anuran larvae. American Naturalist 160:87-102. (Pubitemid 34674264)
68. Weis, J. S., G. Smith, T. Zhou, C. Santiago-Bass, and P. Weis. 2001. Effects of contaminants on behavior: Biochemical mechanisms and ecological consequences. BioScience 51:209-217. (Pubitemid 32449501)
69. Wojtaszek, B. F., B. Staznik, D. T. Chartrand, G. R. Stephenson, and D. G. Thompson. 2004. Effects of Visiont herbicide on mortality, avoidance response, and growth of amphibian larvae in two forest wetlands. Environmental Contamination and Toxicology 23:832-842. (Pubitemid 38418632)