Exposure of sea otters and harlequin ducks in Prince William Sound, Alaska, USA, to shoreline oil residues 20 years after the Exxon Valdez oil spill

Environmental Toxicology and Chemistry

Volumn 30, Issue 3, 2011, Pages 659-672

  Neff, Jerry M ^a   Page, David S ^b   Boehm, Paul D ^c  

^a Neff and Associates   (United States)

^b BOWDOIN COLLEGE   (United States)

^c EXPONENT INC   (United States)

Author keywords

Enhydra lutris; Exxon Valdez oil spill; Histrionicus histrionicus; PAH; Subsurface oil residues

Indexed keywords

ENHYDRA LUTRIS; EXXON VALDEZ OIL SPILL; HISTRIONICUS HISTRIONICUS; PAH; SUBSURFACE OIL RESIDUES;

ANIMALS; AROMATIC HYDROCARBONS; BIOCHEMISTRY; OIL SPILLS; POLYCYCLIC AROMATIC HYDROCARBONS;

WATER POLLUTION;

ASPHALT; POLYCYCLIC AROMATIC HYDROCARBON; WATER;

ASPHALT; BENTHOS; BIOAVAILABILITY; BIVALVE; INTERTIDAL ENVIRONMENT; MARINE MAMMAL; OIL SPILL; PAH; POLLUTION EFFECT; POLLUTION EXPOSURE; PREY CAPTURE; SHORELINE; SUBTIDAL ENVIRONMENT; WATERFOWL;

ARTICLE; BENTHOS; CLAM; DRY WEIGHT; DUCK; ENVIRONMENTAL EXPOSURE; FORAGING; INVERTEBRATE; MARINE SPECIES; NONHUMAN; OIL SPILL; PREY; PRIORITY JOURNAL; SEA OTTER; SEASHORE; UNITED STATES; WILDLIFE;

ALASKA; ANIMALS; BIOLOGICAL MARKERS; CHEMICAL HAZARD RELEASE; CYTOCHROME P-450 CYP1A1; DUCKS; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL MONITORING; FEEDING BEHAVIOR; FEMALE; MALE; OTTERS; PETROLEUM; POLYCYCLIC HYDROCARBONS, AROMATIC; RNA, MESSENGER; WATER POLLUTANTS, CHEMICAL;

ALASKA; PRINCE WILLIAM SOUND; UNITED STATES;

BIVALVIA; ENHYDRA; ENHYDRA LUTRIS; HISTRIONICUS; HISTRIONICUS HISTRIONICUS; INVERTEBRATA;

EID: 79551606566     PISSN: 07307268     EISSN: 15528618     Source Type: Journal    
DOI: 10.1002/etc.415     Document Type: Article

References (57)

1. Neff JM, Owens EH, Stoker SW, McCormick DM. 1995. Condition of shorelines in Prince William Sound following the Exxon Valdez oil spill: Shoreline oiling. In Wells PG, Butler JN, Hughes JS, eds, Exxon Valdez Oil Spill: Fate and Effects in Alaskan Waters. STP 1219. American Society for Testing and Materials, Philadelphia, PA, pp 312-346.
2. Short JW, Lindeberg MR, Harris PM, Maselko J, Pella JJ, Rice SD. 2004. Estimate of the oil persisting on the beaches of Prince William Sound 12 years after the Exxon Valdez oil spill. Environ Sci Technol 38:19-25.
3. Short JW, Irvine GV, Mann DH, Maselko JM, Pella JJ, Lindeberg MR, Payne JM, Driskell WB, Rice SD. 2007. Slightly weathered Exxon Valdez oil persists in Gulf of Alaska beach sediments after 16 years. Environ Sci Technol 41:1245-1250.
4. Rice SD, Balsiger JW. 2002. Materials pertaining to the National Oceanic and Atmospheric Administration 2001 shoreline program. Freedom of Information Act Request 02-133, responses of April 24, 2002, and March 3, 2003. NOAA, National Marine Fisheries Service, Juneau, AK.
5. Short JW, Maselko JM, Lindeberg MR, Harris PM, Rice SD. 2006. Vertical distribution and probability of encountering intertidal Exxon Valdez oil on shorelines of three embayments within Prince William Sound, Alaska. Environ Sci Technol 40:3723-3729.
6. Fredericks BS. 2006. Materials pertaining to the National Oceanic and Atmospheric Administration 2003 shoreline program. Freedom of Information Act requests 2004-0131, 2004-0132. U.S. Department of Commerce, Washington, DC.
7. Taylor E, Reimer PD. 2008. Oil persistence on beaches in Prince William Sound: A review of SCAT surveys conducted from 1989 to 2002. Mar Pollut Bull 40:458-474.
8. Michel J, Nixon Z, Cotsapas L. 2006. Evaluation of oil remediation technologies for lingering oil from the Exxon Valdez oil spill in Prince William Sound, Alaska. Exxon Valdez Oil Spill Restoration Project 050778. Final Report. National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Juneau, AK, USA.
9. Integral Consulting. 2006. Information synthesis and recovery recommendations for resources and services injured by the Exxon Valdez oil spill. Exxon Valdez Oil Spill Restoration Project 060783. Final Report. Integral Consulting, Mercer Island, WA, USA.
10. Page DS, Boehm PD, Neff JM. 2008. Shoreline type and subsurface oil persistence in the Exxon Valdez spill zone of Prince William Sound, Alaska. Proceedings, 31st Arctic and Marine Oilspill Program Technical Seminar, Environmental Contamination and Response, Calgary, AB, Canada, June 3-5, pp 545-564. Environment Canada, Ottawa, ON.
11. Garshelis DL, Johnson CB. 2001. Sea otter population dynamics and the Exxon Valdez oil spill: Disentangling the confounding effects. J Appl Ecol 38:19-35.
12. Bodkin JL, Ballachey BE, Dean TA, Fukuyama AK, Jewett SC, McDonald L, Monson DH, O'Clair CE, VanBlaricom GR. 2002. Sea otter population status and the process of recovery from the 1989 Exxon Valdez oil spill. Mar Ecol Prog Ser 241:237-253.
13. Esler D, Bowman TD, Trust KA, Ballachey BE, Dean TA, Jewett SC, O'Clair CE. 2002. Harlequin duck population recovery following the Exxon Valdez oil spill: Progress, process and constraints. Mar Ecol Prog Ser 241:271-286.
14. Esler D, Trust KA, Ballachey BE, Iverson SA, Lewis TL, Rizzolo DJ, Mulcahy DM, Miles AK, Wooden BR, Stegeman JJ, Henderson JD, Wilson BW. 2010. Cytochrome P4501A biomarker indication of oil exposure in harlequin ducks up to 20 years after the Exxon Valdez oil spill. Environ Toxicol Chem 29:1138-1145.
15. Bodkin J, Ballachey B, Esler D, Dean T. 2003. Patterns and processes of population change in selected nearshore predators. Exxon Valdez Oil Spill Restoration Project 030423. Final Report. U.S. Geological Survey, Alaska Science Center, Anchorage, AK.
16. Harwell MA, Gentile JH, Johnson CB, Garshelis DL, Parker KR. 2010. A quantitative ecological risk assessment of the toxicological risks from Exxon Valdez subsurface oil residues to sea otters at Northern Knight Island, Prince William Sound, Alaska. Human Ecology and Risk Assessment 16:727-761.
17. Harwell MA, Gentile JH, Parker KR, Murphy SM, Day RH, Bence AE, Neff JM, Wiens JA. 2010. Quantitative assessment of current risks to harlequin ducks from the Exxon Valdez oil spill. Human Ecology and Risk Assessment (in press).
18. Neff JM. 2002. Bioaccumulation in Marine Organisms: Effects of Contaminants from Oil Well Produced Water. Elsevier Science, Amsterdam, The Netherlands.
19. Di Toro DM, McGrath JA, Stubblefield WA. 2007. Predicting the toxicity of neat and weathered crude oil: Toxic potential and the toxicity of saturated mixtures. Environ Toxicol Chem 26:24-36.
20. Boehm PD, Page DS, Brown JS, Neff JM, Bragg JR, Atlas RM. 2008. Distribution and weathering of crude oil residues on shorelines 18 years after the Exxon Valdez spill. Environ Sci Technol 42:9210-9216.
21. Neff JM, Bence AE, Parker KR, Page DS, Brown JS, Boehm PD. 2006. Bioavailability of polycyclic aromatic hydrocarbons from buried shoreline residues 13 years after the Exxon Valdez oil spill: A multispecies assessment. Environ Toxicol Chem 25:947-961.
22. Long ER, Macdonald DD, Smith SL, Calder FD. 1995. Incidence of adverse biological effects with ranges of chemical concentrations in marine and estuarine sediments. Environ Manag 19:81-97.
23. Page DS, Boehm PD, Stubblefield WA, Parker KR, Gilfillan ES, Neff JM, Maki AW. 2002. Hydrocarbon composition and toxicity of sediments following the Exxon Valdez oil spill in Prince William Sound, Alaska. Environ Toxicol Chem 21:1438-1450.
24. Short JW, Lindeberg MR, Harris PM, Maselko J, Rice SD. 2002. Vertical oil distribution within the intertidal zone 12 years after the Exxon Valdez oil spill in Prince William Sound, Alaska. Proceedings, 25th Arctic and Marine Oilspill Program Technical Seminar, Calgary, AB, Canada, June 11-13, pp 57-72. Environment Canada, Ottawa, ON, Canada.
25. Michel J, Nixon Z, Hayes MO, Short J, Irvine G, Betenbaugh D, Boring C, Mann D. 2010. Distribution of subsurface oil from the Exxon Valdez oil spill. Exxon Valdez Oil Spill Restoration Project Final Report (Restoration Project 070801). National Oceanic and Atmospheric Administration, Juneau, AK, p121+appendix.
26. Boehm PD, Page DS, Neff JM, Johnson CB. 2007. Potential for sea otter exposure to remnants of buried oil from the Exxon Valdez oil spill. Environ Sci Technol 41:6860-6867.
27. Ballachey BE, Bodkin JL. 2006. Lingering oil and sea otters: Pathways of exposure and recovery status. Exxon Valdez Oil Spill Restoration Project //620. Draft Final Report. Exxon Valdez Oil Spill Trustee Council, Anchorage, AK, USA.
28. Adams J, Lavin P, Turrini A. 2002. Prince William Sound Biological Hotspots Workshop. National Wildlife Federation Alaska Office, Anchorage, AK, USA, p 41.
29. Bodkin JL, Esslinger GG, Monson DH. 2004. Foraging depths of sea otters and implications to coastal marine communities. Mar Mamm Sci 20:305-321.
30. Calkins DG. 1977. Feeding behavior and major prey species of the sea otter, Enhydra lutris, in Montague Strait, Prince William Sound, Alaska. Fish Bull 76:125-131.
31. Kvitek RG, Browlby CE, Staedler M. 1993. Diet and foraging behavior of sea otters in southeast Alaska. Mar Mamm Sci 9:168-181.
32. Nickerson RB. 1977. A study of the littleneck clam (Protothaca staminea Conrad) and the butter clam (Saxidomus giganteus Deshayes) in a habitat permitting coexistence, Prince William Sound, Alaska. Proc Nat Shellfish Assoc 67:85-102.
33. McKnight A, Sullivan KM, Irons DB, Stephensen SW, Howlin S. 2006. Marine bird and sea otter population abundance of Prince William Sound, Alaska: Trends following the T/V Exxon Valdez oil spill, 1989-2005 Exxon Valdez Oil Spill Restoration Projects 040159/ 050751. Final Report. U.S. Fish and Wildlife Service, Anchorage, AK.
34. Rosenberg DH, Petrula MJ, Hill DD, Christ AM. 2005. Harlequin duck population dynamics: Measuring recovery from the Exxon Valdez oil spill. Exxon Valdez Oil Spill Restoration Project 040407. Final Report. Alaska Department of Fish and Game, Anchorage, AK, USA.
35. Wiens JA, Day RH, Murphy SM, Fraker MA. 2010. Assessing cause-effect relationships in environmental accidents: Harlequin ducks and the Exxon Valdez oil spill. Curr Ornithol 17:131-190.
36. Rosenberg DH, Petrula MJ. 1998. Status of harlequin ducks in Prince William Sound, Alaska, after the Exxon Valdez oil spill, 1995- 1997. Exxon Valdez Oil Spill Restoration Project 97427. Final Report. Alaska Department of Fish and Game, Anchorage, AK, USA.
37. Fischer JB, Griffin CR. 2000. Feeding behavior and food habits of wintering harlequin ducks at Shemya Island, Alaska. Wilson Bull 112:318-325.
38. Patten SM Jr, Crowe T, Gustin R, Hunter R, Twait P, Hastings C. 2000. Assessment of injury to sea ducks from hydrocarbon uptake in Prince William Sound and the Kodiak Archipelago, Alaska, following the Exxon Valdez oil spill. Exxon Valdez Oil Spill State/Federal Natural Resource Damage Assessment Bird Study No. 11. Final Report. Volume 1. Alaska Department of Fish and Game, Anchorage, AK, USA.
39. Robertson GJ, Goudie RI. 1999. Harlequin Duck Histrionicus histrionicus. In Poole A, Gill F, eds, The Birds of North America, No. 466. Cornell Laboratory of Ornithology and the Academy of Natural Sciences, Ithaca, NY, USA.
40. Boehm PD, Neff JM, Page DS. 2007. Assessment of hydrocarbon exposure in the waters of Prince William Sound after the Exxon Valdez oil spill: 1989-2005. Mar Pollut Bull 54:339-367.
41. Neff JM, Burns WA. 1996. Estimation of polycyclic aromatic hydrocarbon concentrations in the water column based on tissue residues in mussels and salmon: An equilibrium partitioning approach. Environ Toxicol Chem 15:2240-2253.
42. Huggett RJ, Neff JM, Stegeman JJ, Woodin B, Parker KR, Brown JS. 2006. Biomarkers of PAH exposure in an intertidal fish species from Prince William Sound, Alaska: 2004-2005. Environ Sci Technol 40:6513-6517.
43. Boehm PD, Page DS, Brown JS, Neff JM, Burns WA. 2004. Polycyclic aromatic hydrocarbon levels in mussels from Prince William Sound, Alaska, USA, document the return to baseline conditions. Environ Toxicol Chem 23:2916-2929.
44. Reynolds JH, Braman N. 2008. Using tolerance intervals to assess recovery of mussel beds impacted by the Exxon Valdez oil spill. Mar Pollut Bull 58:1496-1504.
45. Payne JR, Driskell WB, Short JW, Larsen ML. 2008. Long term monitoring for oil in the Exxon Valdez spill region. Mar Pollut Bull 56:2067-2081.
46. Bence AE, Page DS, Boehm PD. 2007. Advances in forensic techniques for petroleum hydrocarbons: The Exxon Valdez experience. In Wang Z, Stout SA, eds, Oil Spill Environmental Forensics: Fingerprinting and Source Identification. Academic, San Diego, CA, USA, pp 449-487.
47. Stegeman JJ, Hahn ME. 1994. Biochemistry and molecular biology of monooxygenases: Current perspectives on forms, functions and regulation of cytochrome P450 in aquatic species. In Malins DC, Ostrander GK, eds, Aquatic Toxicology: Molecular, Biochemical and Cellular Perspectives. Lewis, Boca Raton, FL, USA, pp 87-206.
48. Lee RF, Anderson JW. 2005. Significance of cytochrome P450 system responses and levels of bile fluorescent aromatic compounds in marine wildlife following oil spills. Mar Pollut Bull 50:705-723.
49. Forbes VE, Palmqvist A, Bach L. 2006. The use and misuse of biomarkers in ecotoxicology. Environ Toxicol Chem 25:272-280.
50. Hylland K, Ruus A, Grung M, Green N. 2009. Relationships between physiology, tissue contaminants, and biomarker responses in Atlantic cod (Gadus morhua L.). J Toxicol Environ Health A 72:226-233.
51. Trust KA, Esler D, Woodin BR, Stegeman JJ. 2000. Cytochrome P450 1A induction in sea ducks inhabiting nearshore areas of Prince William Sound, Alaska. Mar Pollut Bull 40:397-403.
52. Esler D. 2008. Quantifying temporal variation in harlequin duck cytochrome P4501A induction. Exxon Valdez Oil Spill Restoration Project 050777. Final Report. Simon Fraser University, Delta, BC, Canada.
53. Snyder PW, Kondratyuk T, Ballachey B, Vanden Heuvel J. 2002. CYP1A1 gene expression in sea otters (Enhydra lutris): A quantitative reverse transcriptase-polymerase chain reaction to measure CYP1A mRNA in peripheral blood mononuclear cells. In Holland-Bartels LE, ed, Mechanisms of impact and potential recovery of nearshore vertebrate predators following the 1989 Exxon Valdez oil spill. Exxon Valdez Oil Spill Restoration Project 99025. Final Report. Vol 1. U.S. Geological Survey, Alaska Biological Science Center, Anchorage, AK, pp Biomarker Appendices, Appendix BIO-2, pp BIO-02.1-BIO-02.13.
54. Hook SE, Cobb ME, Oris JT, Anderson JW. 2008. Gene sequences for Cytochrome P450 1A1 and 1 A2: The need for biomarker development in sea otters (Enhydra lutris). Comp Biochem Physiol B 151:336-348.
55. Miles KA, Fling PL, Trust KA, Ricca MA, Spring SE, Arrieta DE, Hollmen T, Wilson BW. 2007. Polycyclic aromatic hydrocarbon exposure in Steller's eiders (Polysticta stelleri) and harlequin ducks (Histrionicus histrionicus) in the eastern Aleutian Islands, Alaska, USA. Environ Toxicol Chem 26:2694-2703.
56. Kopponen P, Tarhanen J, Ruuskanen J, Törrönen R, Kärenlampi S. 1993. Peat induces cytochrome P450IA1 in hepa-1-cell line: Comparison with fly ashes from combustion of peat, coal, heavy fuel, oil and hazardous waste. Chemosphere 26:1499-1506.
57. Oris JT, Roberts AP. 2007. Statistical analysis of cytochrome P4501A biomarker measurements in fish. Environ Toxicol Chem 26:1742-1750.