Synergistic effects of glyphosate formulation and parasite infection on fish malformations and survival

Journal of Applied Ecology

Volumn 47, Issue 2, 2010, Pages 498-504

  Kelly, David W ^a,b   Poulin, Robert ^b   Tompkins, Daniel M ^a   Townsend, Colin R ^b  

^a LANDCARE RESEARCH   (New Zealand)

^b UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Disease; Fish populations; Glyphosate; Malformation; Multiple stressors; Parasite; Roundup; Toxicity tests

Indexed keywords

ANTHROPOGENIC EFFECT; ANTHROPOGENIC SOURCE; AQUATIC COMMUNITY; DISEASE VECTOR; FLATWORM; FRESHWATER ECOSYSTEM; GLYPHOSATE; HOST RANGE; INFECTIVITY; INTERMEDIATE HOST; JUVENILE; PARASITE INFESTATION; RISK FACTOR; SNAIL; SUBLETHAL EFFECT; SURVIVAL; SYNERGISM; TELEOST; TOXICITY TEST;

NEW ZEALAND;

CERCARIA (TREMATODE GENUS); GALAXIAS ANOMALUS; GASTROPODA; OPISTHORCHIS; POTAMOPYRGUS ANTIPODARUM; TELOGASTER OPISTHORCHIS; TREMATODA; VERTEBRATA;

EID: 77951167222     PISSN: 00218901     EISSN: 13652664     Source Type: Journal    
DOI: 10.1111/j.1365-2664.2010.01791.x     Document Type: Article

References (49)

1. Allan JD. Landscapes and riverscapes: the influence of land use on stream ecosystems. Annual Review of Ecology and Systematics 2004, 35:257-284.
2. Battaglin WA, Rice KC, Focazio MJ, Salmons S, Barry RX. The occurrence of glyphosate, atrazine, and other pesticides in vernal pools and adjacent streams in Washington, DC, Maryland, Iowa, and Wyoming, 2005-2006. Environmental Monitoring and Assessment 2009, 155:281-307.
3. Budischak SA, Belden LK, Hopkins WA. Effects of malathion on embryonic development and latent susceptibility to trematode parasites in ranid tadpoles. Environmental Toxicology and Chemistry 2008, 27:2496-2500.
4. Conners DE, Black MC. Evaluation of lethality and genotoxicity in the freshwater mussel Utterbackia imbecillis (Bivalvia: Unionidae) exposed singly and in combination to chemicals used in lawn care. Archives of Environmental Contamination and Toxicology 2004, 46:362-371.
5. Contardo-Jara V, Klingelmann E, Wiegand C. Bioaccumulation of glyphosate and its formulation Roundup Ultra in Lubriculus variegatus and its effects on biotransformation and antioxidant enzymes. Environmental Pollution 2009, 157:57-63.
6. Coors A, Decaestecker E, Jansen M, De Meester L. Pesticide exposure strongly enhances parasite virulence in an invertebrate host model. Oikos 2008, 117:1840-1846.
7. Culp JM, Baird DJ. Establishing cause-effect relationships in multi-stressor environments. Methods in Stream Ecology 2006, 835-854. Hauer FR, Lamberti GA. 2nd edn, eds, pp, Elsevier, Oxford, UK
8. Cunningham ME, Markle DF, Watral VG, Kent ML, Curtis LR. Patterns of fish deformities and their association with trematode cysts in the Willamette River, Oregon. Environmental Biology of Fishes 2005, 73:9-19.
9. Cushing D. Towards a science of recruitment in fish populations. Excellence in Ecology Series 1996, 175. Kinne O. ed, pp, Ecology Institute, Oldendorf/Luhe
10. Daszak P, Cunningham AA, Hyatt AD. Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica 2001, 78:103-116.
11. New Zealand Threat Classification System Lists 2005, Science & Technical Publishing, Wellington, New Zealand
12. Duncan JR, Lockwood JL. Extinction in a field of bullets, a search for causes in the decline of the world's freshwater fishes. Biological Conservation 2001, 102:97-105.
13. El-Gendy KS, Aly NM, El-Sebae AH. Effects of edifenphos and glyphosate on the immune response and protein biosynthesis of Bolti fish (Tilapia nilotica). Journal of Environmental Science and Health, Part B 1998, 2:135-149.
14. Evaluation and Review Report Decision: Application HSR03010. 2005
15. Folmar LC, Sanders HO, Julin AM. Toxicity of the herbicide glyphosate and several of its formulations to fish and aquatic invertebrates. Archives of Environmental Contamination and Toxicology 1979, 8:269-278.
16. Forson DD, Storfer A. Atrazine increases Rana virus susceptibility in the tiger salamander, Ambystoma tigrinum. Ecological Applications 2006, 16:2325-2332.
17. Giesy JP, Dobson S, Solomon KR. Ecotoxicological risk assessment of Roundupt herbicide. Reviews of Environmental Contaminantion and Toxicology 2000, 167:35-120.
18. Griggs JL, Belden LK. Effects of atrazine and metolachlor on the survivorship and infectivity of Echinostoma trivolvis trematode cercariae. Archives of Environmental Contamination and Toxicology 2008, 54:195-202.
19. Hoole D, Lewis JW, Schuwerack PMM, Chakravarthy C, Shrive AK, Greenhough TJ, Cartwright JR. Inflammatory interactions in fish exposed to polltants and parasites: a role for apoptosis and C reactive protein. Parasitology 2003, 126:S71-S85.
20. Hu J, Zhang Z, Wei Q, Zhen H, Zhao Y, Peng H, Wan Y, Giesy JP, Li L, Zhang B. Malformations of the endangered Chinese sturgeon, Acipenser sinensis, and its causal agent. Proceedings of the National Academy of Sciences, USA 2009, 106:9339-9344.
21. Johnson PTJ, Chase JM. Parasites in the food web: linking amphibian malformations and aquatic eutrophication. Ecology Letters 2004, 7:521-526.
22. Johnson PTJ, Chase JM, Dosch KL, Hartson RB, Gross JA, Larson DJ, Sutherland DR, Carpenter SR. Aquatic eutrophication promotes pathogenic infection in amphibians. Proceedings of the National Academy of Sciences, USA 2007, 104:15781-15786.
23. Kelly DW, Thomas H, Thieltges DW, Poulin R, Tompkins DM. Trematode infection causes malformations and population effects in a declining New Zealand fish. Journal of Animal Ecology 2010, 79:445-452.
24. Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM. Has the introduction of brown trout altered disease patterns in native New Zealand fish? Freshwater Biology 2009, 54:1805-1818.
25. Kiesecker JM. Synergism between trematode infection and pesticide exposure: a link to amphibian deformities in nature? Proceedings of the National Academy of Sciences, USA 2002, 99:9900-9904.
26. Kolpin DW, Thurman EM, Lee EA, Meyer MT, Frlong ET, Glassmeyer ST. Urban contributions of glyphosate and its degradate AMPA to streams in the United States. Science of the Total Environment 2006, 354:191-197.
27. Lafferty KD, Kuris AM. Parasitism and environmental disturbances. Parasitism and ecosystems 2005, 113-123. Thomas F, Guegan JFRenaud F. eds, pp, Oxford University Press, Oxford
28. Leprieur F, Hickey MA, Arbuckle CJ, Closs GP, Brosse S, Townsend CR. Hydrological disturbance benefits a native fish at the expense of an exotic fish. Journal of Applied Ecology 2006, 43:930-939.
29. Manktelow D, Stevens P, Walker J, Gurnsey S, Park N, Zabkiewicz J, Teulon D, Rahman A. Trends in pesticide use in New Zealand: 2004. 2005, Report to the Ministry for the Environment, Project SMF4193
30. Mitchell DG, Chapman PM, Long TJ. Acute toxicity of Roundup and Rodeo herbicides to rainbow trout, chinook, and coho salmon. Bulletin of Environmental Contamination and Toxicology 1987, 39:1028-1035.
31. Morley NJ, Irwin SWB, Lewis JW. Pollution toxicity to the transmission of larval digeneans through their molluscan hosts. Parasitology 2003, 126:S5-S26.
32. Morley NJ, Lewis JW, Hoole D. Pollutant-induced effects on immunological and physiological interactions in aquatic host-trematode systems: implications for parasite transmission. Journal of Helminthology 2006, 80:137-149.
33. New Zealand Threat Classification System lists 2005, Science & Technical Publishing, Wellington, New Zealand
34. Olden JD, Hogan ZS, Vander Zanden MJ. Small fish, big fish, red fish, blue fish,size-biased extinction risk of the world's freshwater and marine fishes. Global Ecology and Biogeography 2007, 16:694-701.
35. Perez GL, Torremorell A, Mugni H, Rodriguez P, Solange vera M, do Nascimento M, Allende L, Bustingorry J, Escaray R, Ferraro M, Izaguirre I. Effects of the herbicide roundup on freshwater microbial communities: a mesocosm study. Ecological Applications 2007, 17:2310-2322.
36. Poulin RP. Toxic pollution and parasitism in freshwater fish. Parasitology Today 1992, 8:58-61.
37. Relyea RA. The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecological Applications 2005a, 15:618-627.
38. Relyea RA. The lethal impacts of roundup and predatory stress on six species of North American tadpoles. Archives of Environmental Toxicology and Chemistry 2005b, 48:351-357.
39. Relyea RA. A cocktail of contaminants: how mixtures of pesticides at low concentrations affect aquatic communities. Oecologia 2009, 159:363-376.
40. Rohr JR, Schotthoefer AM, Raffel TR, Carrick HJ, Halstead N, Hoverman JT, Johnson CM, Johnson LB, Lieske C, Piwoni MD, Schoff PK, Beasley VR. Agrochemicals increase trematode infections in a declining amphibian species. Nature 2008a, 455:1235-1240.
41. Rohr JR, Raffel TR, Sessons SK, Hudson PJ. Understanding the net effects of pesticides on amphibian trematode infections. Ecological Applications 2008b, 18:1743-1753.
42. Ryce EKN, Zale AV, MacConnell E, Nelson M. Effects of fish age versus size on the development of whirling disease in rainbow trout. Diseases of Aquatic Organisms 2005, 63:69-76.
43. Siemering GS, Hayworth JD, Greenfield BK. Assessment of potential aquatic herbicide impacts to California aquatic ecosystems. Archives of Environmental Contamination and Toxicology 2008, 55:415-431.
44. Struger J, Thompson D, Staznik B, Martin P, McDaniel T, Marvin C. Occurrence of glyphosate in surface waters of southern Ontario. Bulletin of Environmental Contamination and Chemistry 2008, 80:378-384.
45. Sures B. Host-parasite interactions in polluted environments. Journal of Fish Biology 2008, 73:2133-2142.
46. Tompkins DM, Dobson AP, Arneberg P, Begon ME, Cattadori IM, Greenman JV, Heesterbeek JAP, Hudson JP, Newborn D, Pugliese A, Rizzoli AP, Rosà R, Rosso F, Wilson K. Parasites and host population dynamics. The Ecology of Wildlife Diseases 2002, 45-62. Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP, eds, pp, Oxford University Press, Oxford
47. Townsend CR, Uhlmann S, Matthaei CD. Individual and combined responses of stream ecosystems to multiple stressors. Journal of Applied Ecology 2008, 45:1810-1819.
48. Wan MT, Watts RG, Moul DJ. Effects of different dilution water types on the acute toxicity to juvenile Pacific salmonids and rainbow trout of glyphosate and its formulated products. Bulletin of Environmental Contamination and Toxicology 1989, 43:378-385.
49. Woo PTK. Fish Diseases and Disorders, Volume 1: Protozoan and Metazoan Infections 2006, 2nd edn, CAB International, Cambridge, MA