Assessing the ecology in ecotoxicology: A review and synthesis in freshwater systems

Ecology Letters

Volumn 9, Issue 10, 2006, Pages 1157-1171

  Relyea, Rick ^a   Hoverman, Jason ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Biodiversity; Density mediated indirect effects; Ecosystem function; Fungicide; Herbicide; Insecticide; Trait mediated indirect effects

Indexed keywords

FRESH WATER; PESTICIDE;

ECOTOXICOLOGY; ENVIRONMENTAL PROTECTION; FRESHWATER ECOSYSTEM; HABITAT SELECTION; NONTARGET ORGANISM; PESTICIDE; PESTICIDE RESISTANCE; POLLUTION EFFECT;

ARTICLE; CHEMISTRY; ECOSYSTEM; ENVIRONMENTAL PROTECTION; WATER POLLUTANT; WATER POLLUTION;

CONSERVATION OF NATURAL RESOURCES; ECOSYSTEM; FRESH WATER; PESTICIDES; WATER POLLUTANTS; WATER POLLUTION;

EID: 33748742425     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/j.1461-0248.2006.00966.x     Document Type: Article

References (92)

1. Abrams, P.A. (1995). Implications of dynamically variable traits for identifying, classifying, and measuring direct and indirect effects in ecological communities. Am. Nat., 146, 112-134.
2. Abrams, P.A., Menge, B.A., Mittelbach, G.G., Spiller, D.A. & Yodiz, P. (1996). The role of indirect effects in food webs. In: Food Webs: Integration of Patterns and Dynamics (eds Polis, G.A. & Winemiller, K.O.). Chapman and Hall, New York, pp. 371-395.
3. Barry, M.J. & Logan, D.C. (1998). The use of temporary pond microcosms for aquatic toxicity testing: direct and indirect effects of endosulfan on community structure. Aquat. Toxicol., 41, 101-124.
4. Boone, M.D. & Semlitsch, R.D. (2001). Interactions of an insecticide with larval density and predation in experimental amphibian communities. Conserv. Biol., 15, 228-238.
5. Boone, M.D. & Semlitsch, R.D. (2002). Interactions of an insecticide with competition and pond drying in amphibian communities. Ecol. Appl., 12, 307-316.
6. Boone, M.D. & Semlitsch, R.D. (2003). Interactions of bullfrog tadpole predators and an insecticide: predation release and facilitation. Oecologia, 137, 610-616.
7. Boone, M.D., Semlitsch, R.D., Fairchild, J.F. & Rothermel, B.B. (2004). Effects of an insecticide on amphibians in large-scale experimental ponds. Ecol. Appl., 14, 685-691.
8. Brewer, S.K., Little, E.E., DeLonay, A.J., Beauvais, S.L., Jones, S.B. & Ellersieck, M.R. (2001). Behavioral dysfunctions correlate to altered physiology in rainbow trout (Oncorynchus mykiss) exposed to cholinesterase- inhibiting chemicals. Arch. Environ. Contam. Toxicol., 40, 70-76.
9. Bridges, C.M. (1997). Tadpole swimming performance and activity affected by acute exposure to sublethal levels of carbaryl. Environ. Toxicol. Chem., 16, 1935-1939.
10. Bridges, C.M. (2000). Long-term effects of pesticide exposure at various life stages of the southern leopard frog (Rana sphenocephala). Arch. Environ. Contam. Toxicol., 39, 91-96.
11. Bridges, C.M. & Semlitsch, R.D. (2001). Genetic variation in insecticide tolerance in a population of southern leopard frogs (Rana sphenocephala): implications for amphibian conservation. Copeia, 2001, 7-13.
12. Brock, T.C.M., Lahr, J. & Van den Brink, P.J. (2000a). Ecological risks of pesticides in freshwater ecosystems. Part 1: Herbicides. Alterra-Report 088, Wageningen, The Netherlands.
13. Brock, T.C.M., Van Wijngaarden, R.P.A. & Van Geest, G. (2000b). Ecological risks of pesticides in freshwater ecosystems. Part 2: Insecticides. Alterra-Report 089, Wageningen, The Netherlands.
14. Broomhall, S.D. (2002). The effects of endosulfan and variable water temperature on survivorship and subsequent vulnerability to predation in Litoria citropa tadpoles. Aquat. Toxicol., 61, 243-250.
15. Broomhall, S.D. (2004). Egg temperature modifies predator avoidance and the effects of the insecticide endosulfan on tadpoles of an Australian frog. J. Appl. Ecol., 41, 105-113.
16. Brust, K., Licht, O., Hultsch, V., Jungmann, D. & Nagel, R. (2001). Effects of terbutryn on aufwuchs and Lumbriculus variegatus in artificial indoor streams. Environ. Toxicol. Chem., 20, 2000-2007.
17. Caswell, H. (2001). Martix Population Models: Construction, Analysis, and Interpretation, 2nd edn. Sinauer Associates, Inc., Sunderland, MA.
18. Christin, M.S., Gendron, A.D., Brousseau, P., Menard, L., Marcogliese, D.J., Cyr, D. et al. (2003). Effects of agricultural pesticides on the immune system of Rana pipiens and on its resistance to parasitic infection. Environ. Toxicol. Chem., 22, 1127-1133.
19. Christin, M.S., Menard, L., Gendron, A.D., Ruby, S., Cyr, D., Marcogliese, D.J. et al. (2004). Effects of agricultural pesticides on the immune system of Xenopus laevis and Rana pipiens. Aquat. Toxicol., 67, 33-43.
20. Cuppen, J.G.M., Van den Brink, P.J., Van der Woude, H., Zwaardemaker, N. & Brock, T.C.M. (1997). Sensitivity of macrophyte-dominated freshwater microcosms to chronic levels of the herbicide linuron. 2. Community metabolism and invertebrates. Ecotoxicol. Environ. Saf., 38, 25-35.
21. Cuppen, J.G.M., Crum, S.J.H., Van den Heuvel, H.H., Smidt, R.A. & Van den Brink, P.J. (2002). Effects of a mixture of two insecticides in freshwater microcosms: I. Fate of chlorpyrifos and lindane and responses of macroinvertebrates. Ecotoxicology, 11, 165-180.
22. Desneux, N., Pham-Delegue, M.H. & Kaiser, L. (2004). Effects of sublethal and lethal doses of lambda-cyhalothrin on oviposition experience and host-searching behaviour of a parasitic wasp, Aphidius ervi. Pest Manag. Sci., 60, 381-389.
23. Dodson, S.I., Hanazato, T. & Gorski, P.R. (1995). Behavioral responses of Daphnia pulex exposed to carbaryl and Chaoborus kairomone. Environ. Toxicol. Chem., 14, 43-50.
24. Donaldson, D., Kiely, T. & Grube, A. (2002). Pesticide Industry Sales and Usage. USEPA Report No. 733-R-02-001. United States Environmental Protection Agency, Washington, DC.
25. Downing, H.F., Delorenzo, M.E., Fulton, M.H., Scott, G.I., Madden, C.J. & Kucklick, J.R. (2004). Effects of the agricultural pesticides atrazine, chlorothalonil, and endosulfan on South Florida microbial assemblages. Ecotoxicology, 13, 245-260.
26. Edginton, A.N., Sheridan, P.M., Stephenson, G.R., Thompson, D.G. & Boermans, H.J. (2004). Comparative effects of pH and vision (R) herbicide on two life stages of four anuran amphibian species. Environ. Toxicol. Chem., 23, 815-822.
27. Fairchild, W.L. & Eidt, D.C. (1993). Perturbation of the aquatic invertebrate community of acidic bog ponds by the insecticide fenitrothion. Arch. Environ. Contam. Toxicol., 25, 170-183.
28. Fleeger, J.W., Carman, K.R. & Nisbet, R.M. (2003). Indirect effects of contaminants in aquatic ecosystems. Sci. Total Environ., 317, 207-233.
29. Forson, D. & Storfer, A. (2006). Effects of atrazine and iridovirus infection on survival and life-history traits of the long-toed salamander (Ambystoma macrodactylum). Environ. Toxicol. Chem., 25, 168-173.
30. Gendron, A.D., Marcogliese, D.J., Barbeau, S., Christin, M.S., Brousseau, P., Ruby, S., Cyr, D. & Fournier, M. (2003). Exposure of leopard frogs to a pesticide mixture affects life history characteristics of the lungworm Rhabdias ranae. Oecologia, 135, 469-476.
31. Glennemeier, K.A. & Denver, R.J. (2001). Sublethal effects of chronic exposure to an organochlorine compound on northern leopard frog (Rana pipiens) tadpoles. Environ. Toxicol., 16, 287-297.
32. Hanazato, T. (1991). Effects of long- and short-term exposure to carbaryl on survival, growth, and reproduction of Daphnia ambigua. Environ. Pollut., 74, 139-148.
33. Hanazato, T. & Hirokawa, H. (2004). Changes in vulnerability of Daphnia to an insecticide application depending on the population phase. Freshw. Biol., 49, 402-409.
34. Hanazato, T. & Yasuno, M. (1990). Influence of time of application of an insecticide on recovery patterns of a zooplankton community in experimental ponds. Arch. Environ. Contam. Toxicol., 19, 77-83.
35. Havens, K.E. (1994). An experimental comparison of effects of two chemical stressors on a freshwater zooplankton assemblage. Environ. Pollut., 84, 245-251.
36. Havens, K.E. (1995). Insecticide (carbaryl, 1-napthyl-N-methyl carbamate) effects on a freshwater plankton community: zooplankton size, biomass, and algal abundance. Water Air Soil Pollut., 84, 1-10.
37. Havens, K.E. & Hanazato, T. (1993). Zooplankton community responses to chemical stressors: a comparison of results from acidification and pesticide contamination research. Environ. Pollut., 82, 277-288.
38. Hayes, T.B., Case, P., Chui, S., Chung, D., Haeffele, C., Haston, K. et al. (2006). Pesticide mixtures, endocrine disruption, and amphibian declines: are we underestimating the impact? Environ. Health Perspect, 114(suppl.1), 40-50.
39. Hayes, T., Haston, K., Tsui, M., Hoang, A., Haeffele, C. & Vonk, A. (2002). Herbicides: feminization of male frogs in the wild. Nature, 419, 895-896.
40. Ibrahim, W.L.F., Furu, P., Ibrahim, A.M. & Christensen, N.O. (1992). Effect of the organophosphorous insecticide, chlorphyrifos (Dursban), on growth, fecundity and mortality of Biomphalaria alexandrina and on the production of Schistosoma mansoni cercariae in the snail. J. Helminthol., 66, 79-88.
41. Juttner, I., Peither, A., Lay, J.P., Kettrup, A. & Ormerod, S.J. (1995). An outdoor mesocosm study to assess ecotoxicological effects of atrazine on a natural plankton community. Arch. Environ. Contam. Toxicol., 29, 435-441.
42. Kasai, F. & Hanazato, T. (1995). Effects of the triazine herbicide, Simetryn, on freshwater plankton communities in experimental ponds. Environ. Pollut., 89, 197-202.
43. Kiesecker, J.M. (2002). Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature? Proc. Natl Acad. Sci. USA, 99, 9900-9904.
44. Kiesecker, J.M. & Skelly, D.K. (2000). Choice of oviposition site by gray treefrogs: the role of potential parasitic infection. Ecology, 81, 2939-2943.
45. Knapp, C.W., Caquet, T., Hanson, M.L., Lagadic, L. & Graham, D.W. (2005). Response of water column microbial communities to sudden exposure to deltamethrin in aquatic mesocosms. FEMS Microbiol. Ecol., 54, 157-165.
46. Knight, T.M., McCoy, M.W., Chase, J.M., McCoy, K.A. & Holt, R.D. (2005). Trophic cascades across ecosystems. Nature, 437, 880-883.
47. Kolpin, D.W., Furlong, E.T., Meyer, M.T., Thurman, E.M., Zaugg, S.D., Barber, L.B. et al. (2002). Pharmaceuticals, hormones, and other organic wastewater contaminants in US streams, 1999-2000: a national reconnaissance. Environ. Sci. Technol., 36, 1202-1211.
48. Kreutzweiser, D.P., Back, R.C., Sutton, T.M., Thompson, D.G. & Scarr, T.A. (2002). Community-level disruptions among zooplankton of pond mesocosms treated with a neem (azadirachtin) insecticide. Aquat. Toxicol., 56, 257-273.
49. LeNoir, J.S., Mcconnell, L.L., Fellers, G.M., Cahill, T.M. & Seiber, J.N. (1999). Summertime transport of current-use pesticides from California's Central Valley to the Sierra Nevada Mountain Range, USA. Environ. Toxicol. Chem., 18, 2715-2722.
50. Mills, N.E. & Semlitsch, R.D. (2004). Competition and predation mediate the indirect effects of an insecticide on southern leopard frogs. Ecol. Appl., 14, 1041-1054.
51. Murphy, P.J. (2003). Does reproductive site choice in a neotropical frog mirror variable risks facing offspring? Ecol. Monogr., 73, 45-67.
52. Newman, M.C. (1998). Fundamentals of Ecotoxicology. Ann Arbor Press, Chelsea, MI.
53. de Noyelles, F., Dewey, S.L., Huggins, D.G. & Kettle, W.D. (1994). Aquatic mesocosms in ecological effects testing: detecting direct and indirect effects of pesticides. In: Aquatic Mesocosm Studies in Ecological Risk Assessment (eds Graney, R.L., Kennedy, J.H. & Rodgers, J.H. Jr). Lewis Publishers, Inc., Boca Raton, FL, pp. 577-603.
54. Peacor, S.D. & Werner, E.E. (2004). How dependent are species-pair interaction strengths on other species in the food web? Ecology, 85, 2754-2763.
55. Preisser, E.L., Bolnick, D.I. & Benard, M.F. (2005). Scared to death? The effects of intimidation and consumption in predator-prey interactions. Ecology, 86, 501-509.
56. Preston, B.L. & Snell, T.W. (2001). Direct and indirect effects of sublethal toxicant exposure on population dynamics of freshwater rotifers: a modeling approach. Aquat. Toxicol., 52, 87-89.
57. Punzo, F. (2005). Effects of insecticide (Carbaryl) exposure on activity and swimming performance of tadpoles of the Rio Grande Leopard Frog, Rana berlandieri (Anura: Ranidae). Tex. J. Sci., 57, 263-272.
58. Rand, G.M., Clark, J.R. & Holmes, C.M. (2000). Use of outdoor freshwater pond microcosms: II. Responses of biota to pyridaben. Environ. Toxicol. Chem., 19, 396-404.
59. Rand, G.M., Clark, J.R. & Holmes, C.M. (2001). The use of outdoor freshwater pond microcosms. III. Responses of phytoplankton and periphyton to pyridaben. Environ. Toxicol., 16, 96-103.
60. Reeder, A.L., Ruiz, M.O., Pessier, A., Brown, L.E., Levengood, J.M., Phillips, C.A. et al. (2005). Intersexuality and the cricket frog decline: historic and geographic trends. Environ. Health Perspect., 113, 261-265.
61. Relyea, R.A. (2001). The relationship between predation risk and antipredator responses in larval anurans. Ecology, 82, 541-554.
62. Relyea, R.A. (2003). Predator cues and pesticides: a double dose of danger for amphibians. Ecol. Appl., 13, 1515-1521.
63. Relyea, R.A. (2004a). Growth and survival of five amphibian species exposed to combinations of pesticides. Environ. Toxicol. Chem., 23, 1737-1742.
64. Relyea, R.A. (2004b). Synergistic impacts of malathion and predatory stress on six species of North American tadpoles. Environ. Toxicol. Chem., 23, 1080-1084.
65. Relyea, R.A. (2005a). The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecol. Appl., 15, 618-627.
66. Relyea, R.A. (2005b). The lethal impacts of roundup and predatory stress on six species of North American tadpoles. Arch. Environ. Contam. Toxicol., 48, 351-357.
67. Relyea, R.A. & Mills, N. (2001). Predator-induced stress makes the pesticide carbaryl more deadly to gray treefrog tadpoles (Hyla versicolor). Proc. Natl Acad. Sci. USA, 98, 2491-2496.
68. Relyea, R.A., Schoeppner, N.M. & Hoverman, J.T. (2005). Pesticides and amphibians: the importance of community context. Ecol. Appl., 15, 1125-1134.
69. Resetarits, W.J.J. & Wilbur, H.M. (1989). Choice of oviposition site by Hyla chrysoscelis role of predators and competitors. Ecology, 70, 220-228.
70. Rohr, J.R. & Crumrine, P.W. (2005). Effects of an herbicide and an insecticide on pond community structure and processes. Ecol. Appl., 15, 1135-1147.
71. Schmitz, O.J., Krivan, V. & Ovadia, O. (2004). Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol. Lett., 7, 153-163.
72. Schulz, R. & Dabrowski, J.M. (2001). Combined effects of predatory fish and sublethal pesticide contamination on the behavior and mortality of mayfly nymphs. Environ. Toxicol. Chem., 20, 2537-2543.
73. Schulz, R. & Liess, M. (2001). Runoff simulation with particle-bound fenvalerate in multispecies stream microcosms: Importance of biological interactions. Environ. Toxicol. Chem., 20, 757-762.
74. Schulz, R., Moore, M.T., Bennett, E.R., Farris, J.L., Smith, S. & Cooper, C.M. (2003). Methyl parathion toxicity in vegetated and nonvegetated wetland mesocosms. Environ. Toxicol. Chem., 22, 1262-1268.
75. Semlitsch, R.D., Bridges, C.M. & Welch, A.M. (2000). Genetic variation and a fitness tradeoff in the tolerance of gray treefrog (Hyla versicolor) tadpoles to the insecticide carbaryl. Oecologia, 125, 179-185.
76. Sih, A., Kerby, J., Bell, A. & Relyea, R. (2004). Response to Schmidt. Pesticides, mortality and population growth rate. Trends Ecol. Evol., 19, 460-461.
77. Slijkerman, D.M.E., Moreira-Santos, M., Jak, R.G., Ribeiro, R., Soares, A. & Van Straalen, N.M. (2005). Functional and structural impact of linuron on a freshwater community of primary producers: the use of immobilized algae. Environ. Toxicol. Chem., 24, 2477-2485.
78. Spawn, R.L., Hoagland, K.D. & Siegfried, B.D. (1997). Effects of alachlor on an algal community from a midwestern agricultural stream. Environ. Toxicol. Chem., 16, 785-793.
79. Thompson, D.G., Wojtaszek, B.F., Staznik, B., Chartrand, D.T. & Stephenson G.R. (2004). Chemical and biomonitoring to assess potential acute effects of Vision® herbicide on native amphibian larvae in forest wetlands. Environ. Toxicol. Chem., 23, 843-849.
80. Tidou, A.S., Moreteau, J.C. & Ramade, F. (1992). Effects of lindane and deltamethrin on zooplankton communities of experimental ponds. Hydrobiologia, 232, 157-168.
81. Truhaut, R. (1977). Ecotoxicology: objectives, principles, and perspectives. Ecotoxicol. Environ. Saf., 1, 151-173.
82. Van den Brink, P.J., van Wijngaarden, R.P.A., Lucassen, W.G.H., Brock, T.C.M. & Leeuwangh, P. (1996). Effects of the insecticide Dursban(R) 4E (active ingredient chlorpyrifos) in outdoor experimental ditches. 2. Invertebrate community responses and recovery. Environ. Toxicol. Chem., 15, 1143-1153.
83. Van den Brink, P.J., Hartgers, E.M., Gylstra, R., Bransen, F. & Brock, T.C.M. (2002). Effects of a mixture of two insecticides in freshwater microcosms: II. Responses of plankton and ecological risk assessment. Ecotoxicology, 11, 181-197.
84. Wallace, J.B., Grubaugh, J.W. & Whiles, M.R. (1996). Biotic indices and stream ecosystem processes: results from an experimental study. Ecol. Appl., 6, 140-151.
85. Wauchope, R.D. & Haque, R. (1973). Effects of pH, light and temperature on carbaryl in aqueous media. Bull. Environ. Contam. Toxicol., 9, 257-260.
86. Weis, J.S., Smith, G., Zhou, T., Santiago-Bass, C. & Weis, P. (2001). Effects of contaminants on behavior: biochemical mechanisms and ecological consequences. Bioscience, 51, 209-217.
87. Wendt-Rasch, L., Friberg-Jensen, U., Woin, P. & Christoffersen, K. (2003). Effects of the pyrethroid insecticide cypermethrin on a freshwater community studied under field conditions. II. Direct and indirect effects on the species composition. Aquat. Toxicol., 63, 373-389.
88. Werner, E.E. & Peacor, S.D. (2003). A review of trait-mediated indirect interactions in ecological communities. Ecology, 84, 1083-1100.
89. van Wijngaarden, R.P.A., Brock, T.C.M. & Douglas, M.T. (2005). Effects of chlorpyrifos in freshwater model ecosystems: the influence of experimental conditions on ecotoxicological thresholds. Pest Manag. Sci., 61, 923-935.
90. Woin, P. (1998). Short- and long-term effects of the pyrethroid insecticide fenvalerate on an invertebrate pond community. Ecotoxicol. Environ. Saf., 41, 137-156.
91. Zaga, A., Little, E.E., Rabeni, C.E. & Ellersieck, M.R. (1998). Photoenhanced toxicity of a carbamate insecticide to early life stage anuran amphibians. Environ. Toxicol. Chem., 17, 2543-2553.
92. Zrum, L. & Hann, B.J. (2002). Invertebrates associated with submersed macrophytes in a prairie wetland: effects of organophosphorus insecticide and inorganic nutrients. Arch. Hydrobiol., 154, 413-445.