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 lipid-rich 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?

2001 Survey Results:

91 sites with 9,000 total pits

- 53 sites with oil - 38 sites without oil

100 Miles

Prince WilliamSound

Alaska

Gulf ofAlaska

N

•Light Oil Residue

•Moderate Oil Residue

•Heavy Oil Residue

Subsurface oil:

LOR MOR

HOR

0

200

400

600

800

1000

TP

AH

(ng

/g d

ry w

t)

Clams

Ribbo

n wor

ms

gunn

elHer

mit

crab

Dog w

helk

Spind

le whe

lkM

usse

ls

4,400

Herring Bay1999

Is oil still bioavailable?

Prey species

Is oil still bioavailable?

1996 – 98 sea otters

1996 – 98 sea ducks

• Elevated P450 in oiled areas

• Poor population recovery in oiled areas (1989-99)

Predators

Paradigm shift in ecotoxicity

1970s: 1-2 rings

Mono Di PAH

WSF

1990s: 3-5 PAH rings

Mono Di PAH

Weathered oil

LC50 = 1 ppm

effects = 1-20 ppb

Different toxic mechanisms from different toxic compounds

Acute LC50narcosis

Long-term“reduced fitness”

Mono Di PAH

WSF

Mono Di PAH

Weathered oil

Reduced fitness results:

in survival from-

in deformities

in growth

in predator avoidance

in reproductive success

Supported by field and laboratory studies

Decreased survival in pink salmon

89

Egg

sur

viva

l

EVOSpre - spill

90 9192 93

Field: ADFG

Elevated egg mortality in oiled streams

Field research

-Extra fins

- Deformed mouth

- Metabolism problems

Increased deformities: pink salmon alevin at emergence

Exposure to eggs (ppb PAH)Lab research

Decreased survival in pink salmon

• Eggs incubating in oiled gravel reduces survival to eyeing

Lab research

% s

urvi

val t

o e y

ed e

gg

Aqueous PAH concentration (ppb)

0.8 1.3 3.6 7.8 18 31 4850

55

60

65

70

75

* *

*

Effects of egg exposure on subsequent pink salmon fry growth

Aqueous PAH concentration (ppb)0 9 18 27 36 45

1

1.2

1.4

1.6

1.8

% in

crea

se in

wei

ght p

er d

ay

Lab research

Delayed growth: effects on adult salmon returns

Lab research

% s

urvi

val o

f re

t ur n

ing

a dul

t s

Control 5.2 19.40

0.5

1

1.5

*

*

Aqueous PAH concentration (ppb)

Summary

Residual oil with 3-5 ring PAHs

- can persist- is toxic- affects fitness

= 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, long-term 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

–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)

Evaluating risk of seabirds to oil

• New recognition after EVOS

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

• 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

• Old 1970’s approach - based on lab bioassays of acute narcosis mortality of individual species to short-lived water-soluble fraction of oil (mostly BTEX plus napthalene)