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)
Lessons learned
1. Anticipate spills. Choose keystone species. Document natural population variability
and response to contaminant exposure through observational field studies and
controlled laboratory studies.
2. 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.
3. 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.
The Spill
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
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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
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induction was estimated using immunohistochemistry12. The relation of PAH exposure, CYP1A
induction, and poor marine survival was replicated under controlled conditions 13. 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 nonoiled 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 1989 18, 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 age 20, 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.
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