Dissolved organic carbon modulates the effects of copper on olfactory-mediated behaviors of chinook salmon

Environmental Toxicology and Chemistry

Volumn 31, Issue 10, 2012, Pages 2281-2288

  Kennedy, Christopher J ^a   Stecko, Pierre ^b   Truelson, Bob ^c   Petkovich, David ^d  

^a SIMON FRASER UNIVERSITY   (Canada)

^b Minnow Environmental   (Canada)

^c Yukon Environment   (Canada)

^d Access Consulting Group   (Canada)

Author keywords

Behavior; Chinook salmon; Copper; Dissolved organic carbon; Iron; Olfaction; Oncorhynchus tshawytscha

Indexed keywords

BEHAVIOR; CHINOOK SALMON; DISSOLVED ORGANIC CARBON; OLFACTION; ONCORHYNCHUS TSHAWYTSCHA;

AMINO ACIDS; COPPER; FISH; IRON; MODULATION;

STREAM FLOW;

COPPER; DISSOLVED ORGANIC CARBON; HISTIDINE; IRON; ORGANIC CARBON; UNCLASSIFIED DRUG;

AMINO ACID; BEHAVIORAL RESPONSE; CONCENTRATION (COMPOSITION); COPPER; DISSOLVED ORGANIC CARBON; DOSE-RESPONSE RELATIONSHIP; INHIBITION; IRON; JUVENILE; OLFACTION; POLLUTION EFFECT; POLLUTION EXPOSURE; SALMONID;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; ENVIRONMENTAL EXPOSURE; NONHUMAN; ONCORHYNCHUS TSHAWYTSCHA; PRIORITY JOURNAL; SMELLING;

ANIMALS; BEHAVIOR, ANIMAL; CARBON; COPPER; FEMALE; HISTIDINE; MALE; SALMON; SMELL; WATER POLLUTANTS, CHEMICAL;

ONCORHYNCHUS TSHAWYTSCHA;

EID: 84866371667     PISSN: 07307268     EISSN: 15528618     Source Type: Journal    
DOI: 10.1002/etc.1948     Document Type: Article

References (44)

1. U.S. Environmental Protection Agency. 2007. Aquatic life ambient freshwater quality criteria-Copper. 2007 Revision. EPA-822/R-07/001. Office of Water, Washington, DC.
2. Tierney KB, Baldwin DH, Hara TJ, Ross PS, Scholz NL, Kennedy CJ. 2010. Olfactory toxicity in fishes. Aquat Toxicol 96: 2-26.
3. Winberg S, Bjerselius R, Baatrup E, Doving KB. 1992. The effect of Cu (II) on the electro-olfactogram (EOG) of the Atlantic salmon (Salmo salar L.) in artificial freshwater of varying inorganic carbon concentrations. Ecotoxicol Environ Saf 24: 167-178.
4. 2+ protects olfactory receptor function against acute Cu (II) toxicity in Atlantic salmon. Aquat toxicol 25: 125-137.
5. Hansen JA, Marr JCA, Lipton J, Cacela D, Bergman HL. 1999. Differences in neurobehavioral responses of chinook salmon (Oncorhynchus tshawytscha) and rainbow trout (Oncorhynchus mykiss) exposed to copper and cobalt: Behavioral avoidance. Environ Toxicol Chem 18: 1972-1978.
6. Hansen JA, Rose JD, Jenkins RA, Gerow KG, Bergman HL. 1999. Chinook salmon (Oncorhynchus tshawytscha) and rainbow trout (Oncorhynchus mykiss) exposed to copper: Neurophysiological and histological effects on the olfactory system. Environ Toxicol Chem 18: 1979-1991.
7. Beyers DW, Farmer MS. 2001. Effects of copper on olfaction of Colorado pikeminnow. Environ Toxicol Chem 20: 907-912.
8. Baldwin DH, Sandahl JF, Labenia JS, Scholz NL. 2003. Sublethal effects of copper on coho salmon: Impacts on nonoverlapping receptor pathways in the peripheral olfactory nervous system. Environ Toxicol Chem 22: 2266-2274.
9. Sandahl JF, Baldwin DH, Jenkins JJ, Scholz NL. 2004. Odor-evoked field potentials as indicators of sublethal neurotoxicity in juvenile coho salmon (Oncorhynchus kisutch) exposed to copper, chlorpyrifos, or esfenvalerate. Can J Fish Aquat Sci 61: 404-413.
10. Sandahl JF, Miyasaka G, Koide N, Ueda H. 2006. Olfactory inhibition and recovery in chum salmon (Oncorhynchus keta) following copper exposure. Can J Fish Aquat Sci 63: 1840-1847.
11. Sandahl JF, Baldwin DH, Jenkins JJ, Scholz NL. 2007. A sensory system at the interface between urban stormwater runoff and salmon survival. Environ Sci Technol 41: 2998-3004.
12. Carreau ND, Pyle GG. 2005. Effect of copper exposure during embryonic development on chemosensory function of juvenile fathead minnows (Pimephales promelas). Ecotoxicol Environ Saf 61: 1-6.
13. McIntyre JK, Baldwin DH, Meador JP, Scholz NL. 2008. Chemosensory deprivation in juvenile coho salmon exposed to dissolved copper under varying water chemistry conditions. Environ Sci Technol 42: 1352-1358.
14. McIntyre JK, Baldwin DH, Meador JP, Scholz NL. 2008. Supplemental Information: Chemosensory deprivation in juvenile coho salmon exposed to dissolved copper under varying water chemistry conditions. Environ Sci Technol 42: 1352-1358.
15. McIntyre JK, Baldwin DH, Meador JP, Scholz NL. 2008. Additions and Corrections: Chemosensory deprivation in juvenile coho salmon exposed to dissolved copper under varying water chemistry conditions. Environ Sci Technol 42: 6774-6775.
16. Green WW, Mirza RS, Wood CM, Pyle GG. 2010. Copper binding dynamics and olfactory impairment in fathead minnows (Pimephales promelas). Environ Sci Technol 44: 1431-1437.
17. Saucier D, Astic L. 1995. Morpho-functional alterations in the olfactory system of rainbow trout (Oncorhynchus mykiss) and possible acclimation in response to long-lasting exposure to low copper levels. Comp Biochem Physiol A 112: 273-284.
18. Saucier D, Astic L, Rioux P, Godinot F. 1991. Histopathological changes in the olfactory organ of rainbow trout (Oncorhynchus mykiss) induced by early chronic exposure to a sublethal copper concentration. Can J Zool 69: 2239-2245.
19. Julliard AK, Saucier D, Astic L. 1996. Time-course of apoptosis in the olfactory epithelium of rainbow trout exposed to a low copper level. Tissue Cell 28: 367-377.
20. Bettini S, Ciani F, Franceschini V. 2006. Recovery of the olfactory receptor neurons in the African Tilapia mariae following exposure to low copper level. Aquat Toxicol 76: 321-328.
21. Hara TJ, Law Y, MacDonald S. 1976. Effects of mercury and copper on the olfactory response in rainbow trout, Salmo gairdneri. J Fish Res Board Can 33: 1568-1573.
22. Di Toro DM, Allen HE, Bergman HL, Meyer JS, Paquin PR, Santore RC. 2001. Biotic ligand model of the acute toxicity of metals. 1. Technical basis. Environ Toxicol Chem 20: 2383-2396.
23. Playle RC, Gensemer RW, Dixon DG. 1992. Copper accumulation on gills of fathead minnows: Influence of water hardness, complexation and pH of the gill microenvironment. Environ Toxicol Chem 11: 381-391.
24. Welsh PG, Skidmore JF, Spry DJ, Dixon DG, Hodson PV, Hutchinson NJ, Hickie BE. 1993. Effect of pH and dissolved organic carbon on the toxicity of copper to larval fathead minnow (Pimephales promelas) in natural lake waters of low alkalinity. Can J Fish Aquat Sci 50: 1356-1362.
25. Meyer JS, Adams WJ. 2010. Relationship between biotic ligand model-based water quality criteria and avoidance and olfactory responses to copper by fish. Environ Toxicol Chem 29: 2096-2103.
26. Hara TJ. 2006. Olfactory responses to amino acids in rainbow trout: Revisited. In Reutter K, Kapoor BG, eds., Fish Chemosenses. Science Publishers, Enfield, NH, USA, pp 31-64.
27. Tierney KB, Singh CR, Ross PS, Kennedy CJ. 2007. Relating olfactory neurotoxicity to altered olfactory-mediated behaviors in rainbow trout exposed to three currently-used pesticides. Aquat Toxicol 81: 55-64.
28. Ishida Y, Kobayashi H. 1995. Avoidance behavior of carp to pesticides and decrease of the avoidance threshold by addition of sodium lauryl sulfate. Fish Sci Tokyo 61: 441-446.
29. Idler DR, Fagerlund U, Mayoh H. 1956. Olfactory perception in migrating salmon: I. L-serine, a salmon repellent in mammalian skin. J Gen Physiol 39: 889.
30. Shparkovskiy IA, Pavlov ID, Troshicheva NV, Klets DV. 1983. Response of Pink salmon, Oncorhynchus gorbusha, and Atlantic salmon, Salmo salar, to amino acids during spawning migration. J Ichthyol 21: 135-140.
31. Mirza RS, Green WW, Connor S, Weeks A, Wood CM, Pyle GG. 2009. Do you smell what I smell? Olfactory impairment in wild yellow perch from metal-contaminated waters. Ecotoxicol Environ Saf 72: 677-683.
32. Rehnberg BC, Schreck CB. 1986. Acute metal toxicology of olfaction in coho salmon: Behavior, receptors, and odor-metal complexation. Bull Environ Contam Toxicol 36: 579-586.
33. Lorz HW, McPherson BP. 1976. Effects of copper or zinc in fresh water on the adaptation to sea water and ATPase activity, and the effects of copper on migratory disposition of coho salmon (Oncorhynchus kisutch). J Fish Res Board Can 33: 2023-2030.
34. Lorz HW, McPherson BP. 1977. Effects of copper and zinc on smoltification of coho salmon. EPA 600/3-77/032. Oregon Department of Fish and Wildlife and U.S. Environmental Protection Agency, Environmental Research Laboratory, Corvallis, OR.
35. Sprague J, Elson P, Saunders R. 1965. Sublethal copper-zinc pollution in a salmon river-A field and laboratory study. Int J Air Water Pollut 9: 531-543.
36. Irving H, Williams R. 1953. The stability of transition-metal complexes. J Chem Soc 637: 3192-3210.
37. Stumm W, Morgan JJ. 1996. Aquatic Chemistry. Chemical Equilibria and Rates in Natural Waters, 3rd ed. Wiley-Interscience, New York, NY, USA, pp 668.
38. Ma H, Kim SD, Cha DK, Allen HE. 1999. Effect of kinetics of complexation by humic acid on toxicity of copper to Ceriodaphnia dubia. Environ Toxicol Chem 18: 828-837.
39. Playle RC, Dixon DG, Burnison K. 1993. Copper and cadmium binding to fish gills: Estimates of metal-gill stability constants and modelling of metal accumulation. Can J Fish Aquat Sci 50: 2678-2687.
40. Linbo TL, Baldwin DH, McIntyre JK, Scholz NL. 2009. Effects of water hardness, alkalinity, and dissolved organic carbon on the toxicity of copper to the lateral line of developing fish. Environ Toxicol Chem 28: 1455-1461.
41. McGeer JC, Szebedinszky C, McDonald DG, Wood CM. 2002. The role of dissolved organic carbon in moderating the bioavailability and toxicity of Cu to rainbow trout during chronic waterborne exposure. Comp Biochem Physiol C 133: 147-160.
42. DeForest DK, Meyer JS, Gensemer RW, Shepard BK, Adams WJ, Dwyer RL, Gorsuch JW, Van Genderen EJ. 2011. Are ambient water quality criteria for copper protective of olfactory impairment in fish? Integr Environ Assess Manag 7: 145-146.
43. Smith KS, Ranville JF, Dietrich DJ, McKnight DM, Sofield RM. 2009. Consideration of iron-organic matter interactions when predicting aquatic toxicity of copper in mineralized areas. Proceedings. Securing the Future and 8th International Conference on Acid Rock Drainage (ICARD), Skelleftea, Sweden, June 22-26, p 9.
44. Canadian Council of Ministers of the Environment. 1999. Canadian Environmental Quality Guidelines. Winnipeg, MB, Canada.