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Exxon Valdez oil spill [EVOS] legacy:
Shifting paradigms in oil ecotoxicology
Riki Ott, Charles H. “Pete” Peterson
& Stanley “Jeep” Rice
Shifting paradigms in ecotoxicology of
oil after EVOS
Part 1: Fish population impacts occur through
chronic exposure of embryos to weathered
oil (highly toxic multi-ring compounds)
Part 2: Taxon-specific risk assessment dogmas
underestimate vertebrate mortalities
Part 3: Chronic effects of decade-long
contamination of key shoreline habitats
and indirect interactions are important
Part 1: Paradigm shift
in fish ecotoxicology
• Old 1970’s paradigm – larval and juvenile fish affected
through acute (days) exposure to water-soluble
fraction (1- and 2-ring aromatic hydrocarbons) at 1
ppm
• New 1990’s paradigm - fish embryos affected by
chronic (months) exposure to more toxic 3-5-ring
PAHs (polycyclic aromatic hydrocarbons) persisting in
weathered oil at 1 ppb
Processes of the new 1990’s paradigm of
fish ecotoxicology
• Bioavailable oil persists for years
in protected bottom habitats
• Hydrocarbons attracted to lipidrich membranes of fish embryos
• Weathered oil fraction of multi-ring PAHs more
toxic in prolonged exposures (at ppb levels)
• Fish population impacts occur over time through
reduced fitness (embryo mortality, deformity, poor
predator avoidance, and low growth)
Residual oil effects:
1. IF Oil is still there
AND
2. IF Oil is biologically available
AND
3. IF there is toxicity paradigm shift
Is the oil still
there?
Prince William
Sound
Alaska
.
en
iP
na
e
K
2001 Survey Results:
P
91 sites with
9,000 total pits
- 53 sites with oil
- 38 sites without oil
ka
as
l
A
la
su
n
i
en
Ko
k Is
dia
Gulf of
Alaska
100 Miles
N
LOR
MOR
Subsurface oil:
•Light Oil Residue
•Moderate Oil Residue
•Heavy Oil Residue
HOR
Is oil still bioavailable?
4,400
TPAH (ng/g dry wt)
1000
800
Herring Bay
1999
600
400
200
0
Prey species
Is oil still bioavailable?
• Elevated P450 in oiled areas
1996 – 98 sea otters
1996 – 98 sea ducks
• Poor population recovery in oiled
areas (1989-99)
Predators
Paradigm shift in ecotoxicity
WSF
1970s:
1-2 rings
LC50 = 1 ppm
Mono Di
PAH
Weathered oil
1990s:
3-5 PAH rings
effects = 1-20 ppb
Mono Di
PAH
Different toxic mechanisms from
different toxic compounds
WSF
Mono Di
PAH
Acute LC50
narcosis
Weathered oil
Mono Di
PAH
Long-term
“reduced fitness”
Reduced fitness results:
i in survival fromh
in deformities
i
in growth
i
in predator avoidance
i
in reproductive success
Supported by field and laboratory studies
Decreased survival in pink salmon
Elevated egg mortality in oiled streams
92 93
89
90 91 Field: ADFG
pre - spill EVOS
Field research
Increased deformities: pink salmon
alevin at emergence
-Extra fins
- Deformed
mouth
- Metabolism
problems
Exposure to eggs (ppb PAH)
Lab research
Decreased survival in pink salmon
75
70
* *
65
60
*
55
50
0.8
1.3
3.6
7.8
18
31
• Eggs
incubating
in oiled
gravel
reduces
survival to
eyeing
48
Aqueous PAH concentration (ppb)
Lab research
% increase in weight per day
Effects of egg exposure on subsequent
pink salmon fry growth
1.8
1.6
1.4
1.2
1
0
9
18
27
36
45
Aqueous PAH concentration (ppb)
Lab research
Delayed growth: effects on adult
salmon returns
1.5
*
*
1
0.5
0
Control
5.2
19.4
Aqueous PAH concentration (ppb)
Lab research
Summary
Residual oil with 3-5 ring PAHs
- can persist
- is toxic
- affects fitness
= i populations
Time table of water quality milestones
•1972 - Passage of federal Clean Water Act
•1970’s - Scientific development of protective standards for
pollutants in water using acute toxicity to WSF
•1989 - Exxon Valdez oil spill
•1990 - OPA ’90 – federal Oil Pollution Act limits field
assessments of oil spill impacts, relying on acute
toxicity models
•1990’s - EVOS-inspired scientific development of a new
paradigm of impacts of chronic exposure to PAHs at
~ 1ppb
•2002
- Federal EPA Phase II Stormwater rules being
developed: will they protect water quality?
Broad implications of new paradigm of fish
ecotoxicology
• Water quality standards must
reflect toxicity of long-term
exposure to PAHs at ppb levels
• Where hydrocarbons pool in
protected bottom habitats isolated
from agents of degradation, longterm impacts are likely
• Urban stormwater run-off carries
high risk to streams, rivers, and
estuarine nurseries
Part 2: Taxon-specific risk assessment
dogmas underestimate vertebrate mortalities
Evaluating risk of marine mammals to
oil spills
• Old dogma - high intelligence,
perception, and mobility may
lead to behavioral avoidance
of spills
• New recognition after EVOS
–sea otters often swam into slicks
–killer whales swam through slicks
–harbor seals occupied oiled haul-outs
Evaluating risk of marine mammals to oil
exposure
• Old dogma - the only mechanism of
injury involves oiling of fur, resulting
in acute mortality through loss of
insulation and toxic ingestion during
preening
• New recognition after EVOS
–Smooth-skinned mammals also killed
through lung inhalation of toxic fumes
(harbor seals) and likely of oil (killer
whales)
–Long-term (yrs) exposure and chronic mortality
impacts for benthic foragers (sea otters)
Additional mechanisms
of marine mammal
losses from oil spills
• Disruption of social structures and breeding
(multi-year disintegration of killer whale pods,
AB and AT in PWS)
• Loss of prey base, requiring larger foraging
ranges and abandonment of areas (river otters)
• Possible food shortage of forage fishes
inhibiting recovery (harbor seals)
Evaluating risk of
seabirds to oil
• Old dogma - Mechanism
of risk is acute mortality
from hypothermia after
feather oiling by
encountering surface
slick
Evaluating risk of
seabirds to oil
• New recognition after EVOS
–Egg mortality rate high after encounters with oiled
feathers of roosting parent (bald eagle)
–Sublethal effects on energetics and productivity
through detoxification costs of ingesting oiled prey
(black oystercatcher)
–Chronic exposure for yrs through foraging in oiled
benthic habitats increase adult mortality (harlequin
ducks, likely Barrow’s goldeneye)
Additional mechanisms of population
impacts of oil in seabirds
• Loss of experienced breeders
in colonial breeding seabirds
can disrupt the phenology of
breeding for several years,
imperiling late-fledging
young (murres)
• Reduction of high-quality forage fish prey, possibly by oil
impacts, affects productivity at the nest (murres, puffins,
pigeon guillemots)
Ecotoxicity requires a context of the web
of interacting species
•No species is independent of others
–habitat
–prey
–predator
•Ecosystem engineers - species that provide important
structural habitat (kelps, seagrasses)
•Keystone species – those with disproportionate controlling
influence on community composition (sea otters, herring)
Changing paradigms of oil impacts to
shoreline communities
• Old dogma - Short generation times of plants and
invertebrates and rapid weathering of oil on shore
leads to rapid recovery
• New recognition after EVOS
– strong interspecific interactions create cascades
of delayed effects over many years - keystone
species and habitat engineers
– preemption of space can inhibit recovery
– sensitive taxa (crustaceans) and oil persistence
in protected sediments slow recovery for yrs
Shifting paradigms in ecotoxicology
• Old 1970’s approach - based on lab
bioassays of acute narcosis mortality of
individual species to short-lived watersoluble fraction of oil (mostly BTEX
plus napthalene)
• New 1990’s realizations – persistent biologically available 3-5 ring
PAHs from oil in protected habitats is
toxic with chronic impacts for yrs
– strong interspecific interactions, including
top-down trophic cascades, biogenic
habitat provision, and competition, induce
indirect and delayed effects for yrs