Journal list menu
THE IMPACT OF INSECTICIDES AND HERBICIDES ON THE BIODIVERSITY AND PRODUCTIVITY OF AQUATIC COMMUNITIES
Rick A. Relyea
Department of Biological Sciences, 101 Clapp Hall, University of Pittsburgh, Pittsburgh, Pennsylvania 15260 USA
E-mail: [email protected]
Search for more papers by this authorRick A. Relyea
Department of Biological Sciences, 101 Clapp Hall, University of Pittsburgh, Pittsburgh, Pennsylvania 15260 USA
E-mail: [email protected]
Search for more papers by this authorCorresponding Editor: J. A. Logan
Abstract
Pesticides constitute a major anthropogenic addition to natural communities. In aquatic communities, a great majority of pesticide impacts are determined from single-species experiments conducted under laboratory conditions. Although this is an essential protocol to rapidly identify the direct impacts of pesticides on organisms, it prevents an assessment of direct and indirect pesticide effects on organisms embedded in their natural ecological contexts. In this study, I examined the impact of four globally common pesticides (two insecticides, carbaryl [Sevin] and malathion; two herbicides, glyphosate [Roundup] and 2,4-D) on the biodiversity of aquatic communities containing algae and 25 species of animals.
Species richness was reduced by 15% with Sevin, 30% with malathion, and 22% with Roundup, whereas 2,4-D had no effect. Both insecticides reduced zooplankton diversity by eliminating cladocerans but not copepods (the latter increased in abundance). The insecticides also reduced the diversity and biomass of predatory insects and had an apparent indirect positive effect on several species of tadpoles, but had no effect on snails. The two herbicides had no effects on zooplankton, insect predators, or snails. Moreover, the herbicide 2,4-D had no effect on tadpoles. However, Roundup completely eliminated two species of tadpoles and nearly exterminated a third species, resulting in a 70% decline in the species richness of tadpoles. This study represents one of the most extensive experimental investigations of pesticide effects on aquatic communities and offers a comprehensive perspective on the impacts of pesticides when nontarget organisms are examined under ecologically relevant conditions.
Literature Cited
- Alford, R. A., and S. J. Richards . 1999. Global amphibian declines: a problem in applied ecology. Annual Review of Ecology and Systematics 30: 133–165.
- Aly, O. M., and M. A. El-Dib . 1971. Studies on the persistence of some carbamate insecticides in the aquatic environment–I: hydrolysis of sevin, baygon, pyrolan and dimetilan in waters. Water Research 5: 1191–1205.
- Audo, M. C., T. M. Mann, T. L. Polk, C. M. Loudenslager, W. J. Diehl, and R. Altig . 1995. Food deprivation during different periods of tadpole (Hyla chrysoscelis) ontogeny affects metamorphic performance differently. Oecologia 103: 518–522.
- Bishop, C. A., N. A. Mahony, J. Struger, P. Ng, and K. E. Pettit . 1999. Anuran development, density and diversity in relation to agricultural activity in the Holland River watershed, Ontario, Canada (1990–1992). Environmental Monitoring and Assessment 57: 21–43.
- Blaustein, A. R., and J. M. Kiesecker . 2002. Complexity in conservation: lessons from the global decline of amphibian populations. Ecology Letters 5: 597–608.
- Boone, M. D., and S. M. James . 2003. Interactions of an insecticide, herbicide, and natural stressors in amphibian community mesocosms. Ecological Applications 13: 829–841.
- Boone, M. D., and R. D. Semlitsch . 2001. Interactions of an insecticide with larval density and predation in experimental amphibian communities. Conservation Biology 15: 228–238.
- Boone, M. D., and R. D. Semlitsch . 2002. Interactions of an insecticide with competition and pond drying in amphibian communities. Ecological Applications 12: 307–316.
- Bridges, C. M. 1997. Tadpole swimming performance and activity affected by acute exposure to sublethal levels of carbaryl. Environmental Toxicology and Chemistry 16: 1935–1939.
- Chase, J. M., and M. A. Leibold . 2002. Spatial scale dictates the productivity–biodiversity relationship. Nature 416: 427–430.
- Davidson, C., H. B. Shafer, and M. R. Jennings . 2001. Declines of the California red-legged frog: climate, UV-B, habitat, and pesticides hypotheses. Ecological Applications 11: 464–479.
- Davidson, C., H. B. Shafer, and M. R. Jennings . 2002. Spatial tests of the pesticide drift, habitat destruction, UV-B, and climate-change hypotheses for California amphibian declines. Conservation Biology 16: 1588–1601.
- Diana, S. G., W. J. Resetarits, Jr, D. J. Shaeffer, K. B. Beckman, and V. R. Beasley . 2000. Effects of atrazine on amphibian growth and survival in artificial aquatic communities. Environmental Toxicology and Chemistry 19: 2961–2967.
- Donaldson, D., T. Kiely, and A. Grube . 2002. Pesticides industry sales and usage: 1998 and 1999 market estimates. USEPA Report Number 733-R-02-001, U.S. Environmental Protection Agency, Washington, D.C., USA.
- Downing, A. L., and M. A. Leibold . 2002. Ecosystem consequences of species richness and composition in pond food webs. Nature 416: 837–841.
- Favari, L., E. Lopez, L. Martinez-Tabche, and E. Diaz-Pardo . 2002. Effect of insecticides on plankton and fish of Ignacio Ramirez reservoir (Mexico): a biochemical and biomagnification study. Ecotoxicology and Environmental Safety 51: 177–186.
- Fordham, C. L., J. D. Tessari, H. S. Ramsdell, and T. J. Keefe . 2001. Effects of malathion on survival, growth, development, and equilibrium posture on bullfrog tadpoles (Rana catesbeiana). Environmental Toxicology and Chemistry 20: 179–184.
- Giesy, J. P., S. Dobson, and K. R. Solomon . 2000. Ecotoxicological risk assessment for Roundup® herbicide. Reviews of Environmental Contamination and Toxicology 167: 35–120.
- Guerrant, G. O., L. E. Fetzer, Jr, and J. W. Miles . 1970. Pesticide residues in Hale County, Texas, before and after ultra-low volume aerial application of malathion. Pesticide Monitoring Journal 4: 14–20.
- Hanazato, T. 1991. Effects of long- and short-term exposure to carbaryl on survival, growth, and reproduction of Daphnia ambigua. Environmental Pollution 74: 139–148.
- Hanazato, T., and M. Yasuno . 1987. Effects of a carbamate insecticide, carbaryl, on summer phyto- and zooplankton communities in ponds. Environmental Pollution 48: 145–159.
- Hanazato, T., and M. Yasuno . 1989. Effects of carbaryl on spring zooplankton communities in ponds. Environmental Pollution 56: 1–10.
- Hanazato, T., and M. Yasuno . 1990. Influence of time of application of an insecticide on recovery patterns of a zooplankton community in experimental ponds. Archives of Environmental Contamination and Toxicology 19: 77–83.
- Harris, M. L., C. A. Bishop, J. Struger, B. Ripley, and J. P. Bogart . 1998. The functional integrity of northern leopard frog (Rana pipiens) and green frog (Rana clamitans) populations in orchard wetlands. II. Genetics, physiology, and biochemistry of breeding adults and young-of-the-year. Environmental Toxicology and Chemistry 17: 1338–1350.
- Havens, K. E. 1994. An experimental comparison of effects of two chemical stressors on a freshwater zooplankton assemblage. Environmental Pollution 84: 245–251.
- Havens, K. E. 1995. Insecticide (carbaryl, 1-napthyl-n-methylcarbamate) effects on a freshwater plankton community: zooplankton size, biomass, and algal abundance. Water Air and Soil Pollution 84: 1–10.
- Havens, K. E., and T. Hanazato . 1993. Zooplankton community responses to chemical stressors: a comparison of results from acidification and pesticide contamination research. Environmental Pollution 82: 277–288.
- Houlihan, J. E., C. S. Findlay, B. R. Schmidt, A. H. Meyers, and S. L. Kuzmin . 2001. Quantitative evidence for global amphibian population declines. Nature 404: 752–755.
- Key, P. B., M. H. Fulton, G. I. Scott, S. L. Layman, and E. F. Wirth . 1998. Lethal and sublethal effects of malathion on three life stages of the grass shrimp, Palaemonetes pugio. Aquatic Toxicology 40: 311–322.
- Lambert, M. R. K. 1997. Environmental effects of heavy spillage from a destroyed pesticide store near Hargeisa (Somaliland) assessed during the dry season, using reptiles and amphibians as bioindicators. Archives of Environmental Contamination and Toxicology 32: 80–93.
- Leight, A. K., and R. F. Van Dolah . 1999. Acute toxicity of the insecticides endosulfan, chlorpyrifos, and malathion to the epibenthic estuarine amphipod Gammarus palustris (Bousefield). Environmental Toxicology and Chemistry 18: 958–964.
- LeNoir, J. S., L. L. McConnell, G. M. Fellers, T. M. Cahill, and J. N. Seiber . 1999. Summertime transport of current-use pesticides from California's central valley to the Sierra Nevada Mountain range, USA. Environmental Toxicology and Chemistry 18: 2715–2722.
- Leonard, A. W., R. V. Hyne, R. P. Lim, and J. C. Chapman . 1999. Effect of endosulfan runoff from cotton fields on macroinvertebrates in the Namoi River. Ecotoxicology and Environmental Safety 42: 125–134.
- 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 26: 193–199.
- Marchal-Segault, D. 1976. Toxicité de quelques insecticides pour des têtards de Bufo bufo (Amphibiens, Anoures). Bulletin Ecology 7: 411–416.
- Marian, M. P., V. Arul, and T. J. Pandian . 1983. Acute and chronic effects of carbaryl on survival, growth, and metamorphosis in the bullfrog (Rana tigrina). Archives of Environmental Contamination and Toxicology 12: 271–275.
- Martinez-Tabche, L., M. M. Galar, H. E. Olvera, R. A. Chehue, E. L. Lopez, L. Gomez-Olivan, and O. T. Sierra . 2002. Toxic effect and bioavailability of malathion spiked in natural sediments from the Ignacio Ramirez dam on the snail Stagnicola sp. Ecotoxicology and Environmental Safety 52: 232–237.
- McConnell, L. L., J. S. LeNoir, S. Datta, and J. N. Seiber . 1998. Wet deposition of current-use pesticides in the Sierra Nevada Mountain range, California, USA. Environmental Toxicology and Chemistry 17: 1908–1916.
- Morin, P. J. 1981. Predatory salamanders reverse outcome of competition among three species of anuran tadpoles. Science 212: 1284–1286.
- Naeem, S. 2002. Ecosystem consequences of biodiversity loss: the evolution of a paradigm. Ecology 83: 1537–1552.
- Perkins, P. J., H. J. Boermans, and G. R. Stephenson . 2000. Toxicity of glyphosate and triclopyr using the frog embryo teratogenesis assay—Xenopus. Environmental Toxicology and Chemistry 19: 940–945.
- Relyea, R. A. 2001. The relationship between predation risk and anti-predator responses in larval anurans. Ecology 82: 541–554.
- Relyea, R. A. 2003a. How prey respond to combined predators: a review and an empirical test. Ecology 84: 1827–1839.
- Relyea, R. A. 2003b. Predator cues and pesticides: a double dose of danger for amphibians. Ecological Applications 13: 1515–1521.
- Relyea, R. A. 2004. Synergistic impacts of malathion and predatory stress on six species of North American tadpoles. Environmental Toxicology and Chemistry 23: 1080–1084.
- Relyea, R. A. In press. The lethal impacts of Roundup and predatory stress on six species of North American tadpoles. Archives of Environmental Contamination and Toxicology.
- Relyea, R. A., and N. Mills . 2001. Predator-induced stress makes the pesticide carbaryl more deadly to grey treefrog tadpoles (Hyla versicolor). Proceedings of the National Academy of Sciences (USA) 98: 2491–2496.
- Relyea, R. A., and K. L. Yurewicz . 2002. Predicting community outcomes from pairwise interactions: integrating density- and trait-mediated effects. Oecologia 131: 569–579.
- Smith, G. R. 2001. Effects of acute exposure to a commercial formulation of glyphosate on the tadpoles of two species of anurans. Bulletin of Environmental Contamination and Toxicology 67: 483–488.
- Sparling, D. W., G. M. Fellers, and L. S. McConnell . 2001. Pesticides and amphibian population declines in California, USA. Environmental Toxicology and Chemistry 20: 1591–1595.
- Tilman, D., P. B. Reich, J. Knops, D. Wedin, T. Mielke, and C. Lehman . 2001. Diversity and productivity in a long-term grassland experiment. Science 294: 843–845.
- USDI [U.S. Fish and Wildlife Service]. 1980. Handbook of acute toxicity of chemicals to fish and aquatic invertebrates. Resource Publication Number 137, U.S. Government Printing Office, Washington, D.C., USA.
- Verschueren, K. 1983. Handbook of environmental data of organic chemicals. Second edition. Van Nostrand Reinhold, New York, New York, USA.
- Wake, D. B. 1998. Action on amphibians. Trends in Ecology and Evolution 13: 379–380.
- Wang, T. 1991. Assimilation of malathion in the Indian River estuary, Florida. Bulletin of Environmental Contamination and Toxicology 47: 238–243.
- Wauchope, R. D., and R. Haque . 1973. Effects of pH, light and temperature on carbaryl in aqueous media. Bulletin of Environmental Contamination and Toxicology 9: 257–260.
- Werner, E. E., and B. R. Anholt . 1996. Predator-induced behavioral indirect effects: consequences to competitive interactions in anuran larvae. Ecology 77: 157–169.
- Wong, C. K., K. H. Chu, and F. F. Shum . 1995. Acute and chronic toxicity of malathion to the fresh-water cladoceran Moina macrocarpa. Water Air and Soil Pollution 84: 399–405.
- Zaga, A., E. E. Little, C. F. Raben, and M. R. Ellersieck . 1998. Photoenhanced toxicity of a carbamate insecticide to early life stage anuran amphibians. Environmental Toxicology and Chemistry 17: 2543–2553.