Abstract
Carbaryl has been applied in Willapa Bay, Washington, for five decades to control burrowing shrimp (Neotrypaea californiensis and Upogebia pugettensis) on commercial oyster (Crassostrea gigas) beds. Concerns about effects on nontarget species, including fishes, have led to restrictions in use despite a lack of data on in situ exposure. We measured brain acetylcholinesterase (AChE) activity in adult Shiner perch (Cymatogaster aggregata) and juvenile Chinook salmon (Oncorhynchus tshawytscha) after operational applications. We hypothesized that exposure in Shiner perch would be greater than in juvenile Chinook salmon because of their greater site fidelity and benthic foraging. However, Shiner perch exhibited no statistically significant AChE inhibition. Enzyme activity was statistically decreased (≤14 %) in juvenile Chinook salmon after a second spray event; however, inhibition was less than that associated with overt effects and was similar to controls by 48 h after the spray. Diet analyses confirmed that Shiner perch were primarily feeding on benthic invertebrates and that juvenile Chinook salmon were feeding primarily within the water column. Composition of Shiner perch diets and amount of food consumed varied little among channels and time periods; however, Shiner perch on beds consumed more food 6 h after application than those at other time points and locations. There were no consistent differences in the diets of juvenile Chinook salmon within channels among time periods. Results suggest (1) that carbaryl applications pose little hazard to fish in the bay having habitat and dietary preferences similar to those of Shiner perch and juvenile Chinook salmon and (2) that quantification of direct exposure in the field is essential to adequately assess risk.
Similar content being viewed by others
References
Baldwin DH, Spromberg JA, Collier TK, Scholz NL (2009) A fish of many scales: extrapolating sublethal pesticide exposures to the productivity of wild salmon populations. Ecol Appl 19:2004–2015
Banas NS, Hickey BM, MacCready P, Newton JA (2004) Dynamics of Willapa Bay, Washington: a highly unsteady, partially mixed estuary. J Phys Oceanogr 34:2413–2427
Banas NS, Hickey BM, Newton JA, Ruesink JL (2007) Tidal exchange, bivalve grazing, and patterns of primary production in Willapa Bay, Washington, USA. Mar Ecol Prog Ser 341:123–139
Bane G, Robinson M (1970) Studies on the Shiner Perch, Cymatogaster aggregata Gibbons, in Upper Newport Bay, California. Wasmann J Biol 28:259–268
Barry JP, Yoklavich MM, Cailliet GM, Ambrose DA, Antrim BS (1996) Trophic ecology of the dominant fishes in Elkhorn Slough, California, 1974–1980. Estuaries 19:115–138
Bi HS, Ruppel RE, Peterson WT (2007) Modeling the pelagic habitat of salmon off the Pacific Northwest (USA) coast using logistic regression. Mar Ecol Prog Ser 336:249–265
Bollens SM, Hooff RV, Butler M, Cordell JR, Frost BW (2010) Feeding ecology of juvenile Pacific salmon (Oncorhynchus spp.) in a northeast Pacific fjord: diet, availability of zooplankton, selectivity for prey, and potential competition for prey resources. Fish Bull 108:393–407
Chipps SR, Garvey JE (2007) Assessment of diet and feeding patterns. In: Guy CS, Brown MJ (eds) Analysis and interpretation of inland fisheries data. American Fisheries Society, Bethesda, pp 473–514
Duffy EJ, Beauchamp DA, Sweeting RM, Beamish RJ, Brennan JS (2010) Ontongenic diet shifts of juvenile Chinook salmon in nearshore and offshore habitats of Puget Sound. Trans Am Fish Soc 139:803–823
Dumbauld BR, Brooks KM, Posey MH (2001) Response of an estuarine benthic community to application of a pesticide carbaryl and cultivation of Pacific oysters (Crassotrea gigas) in Willapa Bay, Washington. Mar Pollut Bull 42:826–844
Ellman GL, Courtney KD, Andreas V Jr, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95
Erickson W, Turner L (2003) Carbaryl analysis of risks to endangered and threatened salmon and steelhead. Office of Pesticide Programs, US Environmental Protection Agency, Washington, DC
Eschmeyer WN, Herald ES, Hammann H (1983) A field guide to Pacific coast fishes of North America. Houghton Mifflin, Boston, p 228
Feldman KL, Armstrong DA, Dumbauld BR, DeWitt TH, Doty DC (2000) Oysters, crabs, and burrowing shrimp: review of an environmental conflict over aquatic resources and pesticide use in Washington State’s (USA) coastal estuaries. Estuaries 23:141–176
Felsot AS, Ruppert JR (2002) Imidacloprid residues in Willapa Bay (Washington State) water and sediment following application for control of burrowing shrimp. J Agric Food Chem 50:4417–4423
Fulton MH, Key PB (2001) Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environ Toxicol Chem 20:37–45
Grue CE, Gardner SC, Gibert PL (2002) On the significance of pollutant-induced alterations in the behavior of fish and wildlife. In: Dell’Omo G (ed) Behavioural ecotoxicology. John Wiley & Sons, Ltd., West Sussex, pp 1–90
Labenia JS, Baldwin DH, French BL, Davis JW, Scholz NL (2007) Behavioral impairment and increased predation mortality in cutthroat trout exposed to carbaryl. Mar Ecol Prog Ser 329:1–11
Mayer FL, Ellersieck (1986) Manual of acute toxicity: interpretation and data base for 410 chemicals and 66 species of freshwater animals. Resource publication 160. USDI Fish and Wildlife Service, Washington, DC
Mineau P (ed) (1991) Cholinesterase-inhibiting insecticides—their impact on wildlife and the environment. Elsevier, Amsterdam
Morrow JE (1980) The freshwater fishes of Alaska. Alaska Northwest Publishing, Alaska Geographic Society, Anchorage
National Oceanic and Atmospheric Administration Fisheries, Office of Science and Technology (2011) NMFS landing query results. Annual commercial landing statistics. Available at: ttp://www.st.nmfs.noaa.gov/pls/webpls/MF_ANNUAL_LANDINGS.RESULTS. Accessed 20 Mar 2013
Odenweller DB (1975) The life history of the shiner surfperch Cymatogaster aggregata Gibbons, in Anaheim Bay, California. In: Lane ED, Hill CW (eds) The marine resources of Anaheim Bay. California Department of Fish and Game, Sacramento, pp 107–115
Post G, Leasure RA (1974) Sublethal effect of malathion to three salmonid species. Bull Environ Contam Toxicol 12:312–319
Sandahl JF, Baldwin DH, Jenkins JJ, Scholz NL (2005) Comparative thresholds for acetylcholinesterase inhibition and behavioral impairment in coho salmon exposed to chlorpyrifos. Environ Toxicol Chem 24:136–145
Stewart NE, Millemann RE, Breese WP (1967) Acute toxicity of the insecticide Sevin and its hydrolytic product l-naphthol to some marine organisms. Trans Am Fish Soc 96:25–30
Tierney K, Casselman M, Takeda S, Farrell T, Kennedy C (2007) The relationship between cholinesterase inhibition and two types of swimming performance in chlorpyrifos-exposed coho salmon (Oncorhynchus kisutch). Environ Toxicol Chem 26:998–1004
Tufts DF (1989) Control of burrowing shrimp on oyster beds in Willapa Bay and Grays Harbor. Special shellfish report no. 4, Washington Department of Fisheries, Olympia, WA
United States Fish and Wildlife Service (2012) Willapa National Wildlife Refuge. Available at: http://www.fws.gov/willapa. Accessed 6 Jun 2012
Washington Department of Fisheries and Washington Department of Ecology (1992) Use of the insecticide carbaryl to control ghost and mud shrimp in oyster beds of Willapa Bay and Grays Harbor. Supplemental environmental impact statement. Washington Department of Fisheries and Washington Department of Ecology, Olympia, WA
Williams GD (1994) Effects of habitat modification on distribution and diets of intertidal fishes in Grays Harbor Estuary. Thesis. University of Washington, Seattle
Zar JH (2010) Biostatistical analyses (4th ed). Prentice-Hall, Upper Saddle River
Zinkl JG, Shea PJ, Nakamoto RJ, Callman J (1987) Brain cholinesterase activity of juvenile rainbow trout poisoned by carbaryl. Bull Environ Contam Toxicol 38:29–35
Zinkl JG, Lockhart WL, Kenny SA, Ward FJ (1991) The effects of cholinesterase inhibiting insecticides on fish. In: Mineau P (ed) Cholinesterase-inhibiting insecticides—their impact on wildlife and the environment. Elsevier, Amsterdam, p 233
Acknowledgments
We thank Willapa Grays Harbor Oyster Growers Association (WGHOGA), Washington State Commission for Pesticide Registration, Washington State Legislature, and the Washington Cooperative Fish and Wildlife Research Unit (WACFWRU) for financial support. WACFWRU is financially supported by the United States Geological Survey, University of Washington, Washington State University, and the Washington Departments of Ecology, Fish and Wildlife, and Natural Resources. Tim Morris (Coast Seafoods), Steven Booth, (WGHOGA [Integrated Pest Management Coordinator]), and Stephen Thun (PAL) assisted with field logistics, and Cristiane Elfes, John Frew, Andrew Keach, Erin Lowery, Kaitlyn Martel, Marissa Smith, Michael Smith, and Amy Yahnke (WACFWRU) assisted in the field and/or with the laboratory analyses. We also thank Erin Lowery and three anonymous reviewers for comments on earlier drafts.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Troiano, A.T., King, K.A., Grue, C.E. et al. Brain Acetylcholinesterase Activity in Shiner Perch (Cymatogaster aggregata) and Juvenile Chinook Salmon (Oncorhynchus tshawytscha) After Application of Carbaryl to Control Burrowing Shrimp Within Willapa Bay, Washington. Arch Environ Contam Toxicol 65, 779–789 (2013). https://doi.org/10.1007/s00244-013-9951-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00244-013-9951-z