|The Effects of Crude Oil on Wild Fish Populations:
Lessons Learned from the Exxon Valdez Oil Spill
Gary D. Marty, DVM, PhD, Diplomate, ACVP (anatomic pathology)
Fish Pathologist, Animal Health Centre, Ministry of Agriculture,
Abbotsford, British Columbia, Canada (Gary.Marty@gov.bc.ca)
Anticipate spills. Choose keystone species. Document natural population variability and response to contaminant exposure through observational field studies and controlled laboratory studies.
Consider differentials. Highly dynamic ecosystems, populations, and organisms interact in complex ways. Determine whether observed effects are due to natural variability, contaminant exposure, or some combination.
Expect recovery. Populations and ecosystems have a tremendous capacity to recover. Lethal oil spill effects tend to be short term (weeks to months), although focal “scars” might remain for years.
On March 24, 1989, the Exxon Valdez ran aground on Bligh Reef in the northeastern part of Prince William Sound (PWS), Alaska, spilling about 40 × 106 L of crude oil. At the time, it was the largest ever crude oil spill in U.S. waters, and it occurred in what was otherwise a relatively pristine, highly productive, but highly sensitive ecosystem1. Control was difficult due to variable weather conditions and tide cycles that ranged up to 6 m. The oil came ashore along a trajectory of approximately 750 km from PWS to the southern Kodiak Archipelago and Alaska Peninsula.
Oiled birds and mammals, particularly sea otters, sustained most of the international press coverage after the spill. In contrast, many of the people in the small local communities affected by the spill were more concerned about the effects of the spill on their livelihood. They were concerned about fish and shellfish. Because of the potential for oil contamination of edible products, subsistence and commercial fisheries were closed in PWS during 1989. By 1990, cleanup efforts and natural processes had removed most of the oil from PWS, and fisheries were opened in 1990 and thereafter without concern for oil contamination.
Damage Assessment and Restoration
Damage assessment activities were managed by the State of Alaska and three federal agencies acting together as Natural Resource Trustees as provided by the Comprehensive Environmental Response, Compensation, and Liability Act (CERCLA)1. This act also provided the statutory basis for compensating the public for injuries to natural resources resulting from spills of hazardous substances. The legal framework transitioned to the restoration phase after the government settled its legal claims against Exxon in October 1991, with total payment from Exxon to the government of about $1 billion, paid in $100 million annual installments over 10 years2. These funds allowed future government efforts to focus on research, land acquisition, and restoration rather than legal proceedings.
I was responsible for most of the fish histopathology work contracted by the Natural Resource Trustees after the spill, first as a graduate student in the laboratory of Dr. David Hinton at the University of California, Davis, and later as research faculty, also at UCD; my doctoral dissertation focused on larval fish histopathology.
Effect on Larval Fish
Most fish research after the spill focused on two keystone species: pink salmon (Oncorhynchus gorbuscha) and Pacific herring (Clupea pallasii). These species were chosen because they were (i) likely to have been exposed to spilled oil, (ii) important for subsistence and commercial users, and (iii) decades of available data provided a basis for estimating changes in population structure related to the spill.
Adult Pacific herring gather in large aggregations for their annual spring spawning event. Pacific herring in PWS first spawn when they are 3 – 5 years old, and they rarely survive more than 12 years. Mass nearshore spawning in PWS begins in March and peaks in April and May. I have observed individual spawning aggregations that spanned several kilometers. In 1989, only about 5% of the spawn occurred along visibly oiled shorelines3, but analysis of dissolved total polycyclic aromatic hydrocarbons (PAH) in water and mussels provided evidence that 25–32% of the embryos were damaged3. Fish rapidly metabolize petroleum hydrocarbons, whereas mussels do not; therefore, mussel tissues are a better biomarker for estimating exposure over time4,5.
Ascites was probably the most important lesion in Pacific herring larvae after the spill, affecting 16% of larvae from oiled areas but only 1% of larvae from reference areas6. Although ascites is a nonspecific lesion, ascites prevalence of 16% is consistent with continuous laboratory exposure to ~0.3 mg/L PAH7: well within documented PAH levels in PWS in April and May 19898,9. Recruitment of the 1989 year class into the adult population in 1992 was poor, but recruitment of this year class in areas outside of PWS was also poor, leading to the conclusion that oceanographic variables were probably more significant in limiting recruitment of the 1989 year class in PWS than was the oil spill6.
Pink salmon eggs are deposited in the stream beds in the fall, often in the lower reaches of streams in areas of tidal (salt water) influence10. Eggs incubate and hatch over the winter. When yolk reserves are depleted, juvenile fish emerge from the gravel and immediately migrate into seawater. In PWS this migration usually occurs during May, which in 1989 was the same time that Exxon Valdez oil was being washed ashore. Pink salmon that emigrated into oiled regions of PWS had decreased growth11, and this was associated with induction of the enzyme that metabolizes petroleum hydrocarbons, cytochrome P4501A (CYP1A). CYP1A induction was estimated using immunohistochemistry12. The relation of PAH exposure, CYP1A induction, and poor marine survival was replicated under controlled conditions13. In 1999, ten years after the spill, CYP1A was still induced in larval pink salmon sampled from two of six PWS streams that had been heavily oiled in 198914.
One study reported that pink salmon egg mortalities were greater in oiled streams than in non-oiled streams15. However, the relation between elevated egg mortalities and PAH exposure was not replicated16, and elevated egg mortalities were more likely a result of variables independent of oil exposure17.
Effect on Adult Pacific herring
Adult Pacific herring were exposed to Exxon Valdez oil in 198918, and hepatocellular necrosis was more frequent in fish from oiled areas. However, results from partly controlled laboratory study suggest that hepatocellular necrosis was a result of an outbreak of the endemic viral disease viral hemorrhagic septicemia (VHS) rather than a direct effect of oil exposure19.
Commercial harvests from 1990 – 1992 were greater than nearly any year during the previous three decades, but the PWS Pacific herring population declined during the winter of 1993, resulting in the closure of all commercial fisheries in 199320. Many of the fish exposed to the spill as larvae or yearlings in 1989 would have been spawning for the first time in spring 1993, and some people were concerned that these young adults might be disproportionately affected. However, adult mortality in 1993 was independent of fish age20, and none of the fish had been exposed to significant concentration of oil since 198918. Because petroleum hydrocarbons are rapidly metabolized by fish tissues, the hypothesis that population decline was a delayed effect of the spill is not plausible. Instead, the evidence better supports the conclusion that increased mortality was due to poor fish condition—resulting from poor food resources21—and increased prevalence of disease22.
Morphologic changes in the liver provide evidence that conditions during the winter of 1993 had a greater impact on adult Pacific herring than did the 1989 oil spill. Pigmented macrophage aggregates (PMA) are irregularly spherical structures that are a normal component of the liver of most fish species; lipofuscin and iron are the most common pigments23. In a retrospective study being prepared for publication, I found that the volume of hepatic pigmented macrophage aggregates was not different between the 1988 and 1994 year classes when both were 3 and 4 years old. These year classes were compared because the 1988 year class had been exposed to both the 1989 oil spill and the 1993 population decline, but the 1994 year class was exposed to neither event. The volume of hepatic pigmented macrophage aggregates was significantly greater in the 1988 year class when both year classes were 6, 7, and 8 years old (i.e., the 1988 year class in 1994 – 1996 vs. the 1994 year class in 2000 – 2002). These findings support the conclusion that the 1988 year class was not significantly affected by the Exxon Valdez oil spill but was affected by population-level stress in 1993, and pigmented macrophage aggregates provided a biomarker of this stress that was maintained in the year class for at least 3 years.
1. Marty, G.D. 2008. Effects of the Exxon Valdez oil spill on Pacific herring in Prince William Sound, Alaska, in The Toxicology of Fishes, R.T. Di Giulio and D.E. Hinton, Editors. CRC Press. p. 925-932.
2. Exxon Valdez Oil Spill Trustee Council - Settlement. [viewed 2013 August 10]; Available from: http://www.evostc.state.ak.us/facts/settlement.cfm.
3. Carls, M.G., G.D. Marty, and J.E. Hose. 2002. Synthesis of the toxicological impacts of the Exxon Valdez oil spill on Pacific herring (Clupea pallasi) in Prince William Sound, Alaska, U.S.A. Can. J. Fish. Aquat. Sci. 59(1):153-172.
4. Collier, T.K. and U. Varanasi. 1991. Hepatic activities of xenobiotic metabolizing enzymes and biliary levels of xenobiotics in English sole (Parophrys vetulus) exposed to environmental contaminants. Arch. Environ. Contam. Toxicol. 20:462-473.
5. Thomas, R.E., M.G. Carls, S.D. Rice, and L. Shagrun. 1997. Mixed function oxidase induction in pre- and post-spawn herring (Clupea pallasi) by petroleum hydrocarbons. Comp. Biochem. Physiol. 116C:141-147.
6. Marty, G.D., J.E. Hose, M.D. McGurk, E.D. Brown, and D.E. Hinton. 1997. Histopathology and cytogenetic evaluation of Pacific herring larvae exposed to petroleum hydrocarbons in the laboratory or in Prince William Sound, Alaska, after the Exxon Valdez oil spill. Can. J. Fish. Aquat. Sci. 54:1846-1857.
7. Carls, M.G., S.D. Rice, and J.E. Hose. 1999. Sensitivity of fish embryos to weathered crude oil: Part 1. Low-level exposure during incubation causes malformations, genetic damage, and mortality in larval Pacific herring (Clupea pallasi). Environ. Toxicol. Chem. 18(3):481-493.
8. Neff, J.M. and W.A. Stubblefield. 1995. Chemical and toxicological evaluation of water quality following the Exxon Valdez oil spill, in Exxon Valdez oil spill: fate and effects in Alaskan waters, P.G. Wells, J.N. Butler, and J.S. Hughes, Editors. ASTM STP 1219 American Society for Testing and Materials: Philadelphia, PA. p. 141-177.
9. Short, J.W. and P.M. Harris. 1996. Chemical sampling and analysis of petroleum hydrocarbons in near-surface seawater of Prince William Sound after the Exxon Valdez oil spill. Am. Fish. Soc. Symp. 18:17-28.
10. Helle, J.H., R.S. Williamson, and J.E. Bailey. 1964. Intertidal ecology and life history of pink salmon at Olsen Creek, Prince William Sound, Alaska, U.S. Fish and Wildlife Service: Washington, D.C.
11. Wertheimer, A.C. and A.G. Celewycz. 1996. Abundance and growth of juvenile pink salmon in oiled and non-oiled locations of western Prince William Sound after the Exxon Valdez oil spill. Am. Fish. Soc. Symp. 18:518-532.
12. Weidmer, M., M.J. Fink, J.J. Stegeman, R. Smolowitz, G.D. Marty, and D.E. Hinton. 1996. Cytochrome P450 induction and histopathology in pre-emergent pink salmon from oiled streams in Prince William Sound, Alaska. Am. Fish. Soc. Symp. 18:509-517.
13. Carls, M.G., R.A. Heintz, G.D. Marty, and S.D. Rice. 2005. Cytochrome P4501A induction in oil-exposed pink salmon Oncorhynchus gorbuscha embryos predicts reduced survival potential. Mar. Ecol. Prog. Ser. 301:253-265.
14. Carls, M.G., S.D. Rice, G.D. Marty, and D.K. Naydan. 2004. Pink salmon spawning habitat is recovering a decade after the Exxon Valdez oil spill. Trans. Am. Fish. Soc. 133:834-844.
15. Bue, B.G., S. Sharr, S.D. Moffitt, and A.K. Craig. 1996. Effects of the Exxon Valdez oil spill on pink salmon embryos and preemergent fry. Am. Fish. Soc. Symp. 18:619-627.
16. Marty, G.D., J.W. Short, D.M. Dambach, N.H. Willits, R.A. Heintz, S.D. Rice, J.J. Stegeman, and D.E. Hinton. 1997. Ascites, premature emergence, increased gonadal cell apoptosis, and cytochrome-P4501A induction in pink salmon larvae continuously exposed to oil-contaminated gravel during development. Can. J. Zool. 75:989-1007.
17. Brannon, E.L., K.C.M. Collins, L.L. Moulton, and K.R. Parker. 2001. Resolving allegations of oil damage to incubating pink salmon eggs in Prince William Sound. Can. J. Fish. Aquat. Sci. 58(6):1070-1076.
18. Marty, G.D., M.S. Okihiro, E.D. Brown, D. Hanes, and D.E. Hinton. 1999. Histopathology of adult Pacific herring in Prince William Sound, Alaska, after the Exxon Valdez oil spill. Can. J. Fish. Aquat. Sci. 56(3):419-426.
19. Carls, M.G., G.D. Marty, T.R. Meyers, R.E. Thomas, and S.D. Rice. 1998. Expression of viral hemorrhagic septicemia virus in pre-spawning Pacific herring (Clupea pallasi) exposed to weathered crude oil. Can. J. Fish. Aquat. Sci. 55(10):2300-2309.
20. Marty, G.D., E.F. Freiberg, T.R. Meyers, J. Wilcock, T.B. Farver, and D.E. Hinton. 1998. Viral hemorrhagic septicemia virus, Ichthyophonus hoferi, and other causes of morbidity in Pacific herring Clupea pallasi spawning in Prince William Sound, Alaska, USA. Dis. Aquat. Org. 32(1):15-40.
21. Elston, R.A., A.S. Drum, W.H. Pearson, and K. Parker. 1997. Health and condition of Pacific herring Clupea pallasi from Prince William Sound, Alaska, 1994. Dis. Aquat. Org. 31(2):109-126.
22. Marty, G.D., T.J. Quinn, II, G. Carpenter, T.R. Meyers, and N.H. Willits. 2003. Role of disease in abundance of a Pacific herring (Clupea pallasi) population. Can. J. Fish. Aquat. Sci. 60(10):1258-1265.
23. Wolke, R.E. 1992. Piscine macrophage aggregates: a review. Ann. Rev. Fish Dis. 2:91-108.