Exxon Valdez oil spill [EVOS] legacy: Synthesis of long-term ecosystem responses

Riki Ott, Charles H. “Pete” Peterson & Stanley “Jeep” Rice

Theme: Chronic effects of decade-long contamination of key shoreline habitats and indirect interactions are important

1994 EVOS oil, Prince William Sound, AK

Delayed, chronic, and indirect effects of shoreline oiling/treatment

• Treat EVOS as an ecosystem perturbation

• Capitalize on vast research effort

• Synthesis focused on shoreline habitats

• Contrast of NRDA based on old ecotoxicity risk models vs. field-based sampling

Assumptions about oil toxicology in 1989

•Alaska's Water Quality Standard for PAHs was 10 ppb and provided conservative protection of natural resources

•Oil toxicity declined very rapidly in a matter of days/weeks

•Acute toxicity tests of lab animals adequately predicted risk

•Contact with feathers and fur was the only significant route of injury to birds and mammals

•Oil spill impacts could be assessed on a species-by-species basis with no regard for dependencies within the ecosystem

Contrasting terms

• Acute vs. Chronic exposure (= short- vs. long-term)

• Lethal vs. Sublethal impacts (= mortality vs. growth, reproduction, body condition)

• Immediate vs. Delayed response (= rapid vs. postponed)

• Direct vs. Indirect effect (= A B vs. A C B)

• Trophic cascade vs. Biogenic habitat loss (= change in predator affects its prey, which affects its prey, etc. vs. change in an organism that provides structural living space for other organisms)

Benefits of EVOS field sampling approach

• Employs statistical sampling design• Integrates responses across all

mechanisms• Includes chronic effects on long

time scales• Includes interactions of oil and

other stressors• Includes indirect interactions from

trophic cascades, habitat modifications, etc.

Synthesis of long-term ecosystem

responses

• Shows old assumptions of oil ecotoxicity to be inadequate

• Weathered oil persists

• Weathered oil remains bioavailable in important environments

• Weathered oil (multi-ring PAHs) induces toxicity during chronic exposure

Water column PAH contamination after EVOS

• Low (1-8 ppb) even during weeks 1-5 in 1989

• Essentially below detection by end of summer 1989 using traditional water sampling

• But filter-feeding mussels revealed exposure and bioavailability even into summer 1992 via filtration of contaminated particulates

Persistence of oil

• Asphalts high on shore - biologically inactive

• Biologically available pockets in protected sites for >10 yrs

– Under armor of mussel beds with relatively unweathered oil contaminating mussels at least into summer 1994 at study’s end

– In groundwater of deltas of anadromous streams yrs later

– In sediments among boulders on oiled beaches for yrs

• Transported on particles to shallow subtidal where elevated PAHs persisted until 1995 at study’s end

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

Distribution of oil 12 years later

Upperintertidal

Biologicalzone

(lower intertidal) Oil below sampling grid = YesHow far down = ?

Tidalzone (m)

+ 4.8+ 4.3+ 3.3+ 2.8+ 2.3+ 1.8

< 1m

Surface oil(# of pits)

375658604029

5286991

123117

Subsurface oil(# of pits)

Shoreline treatments

• Intense in 1989, 1990 summers with some extending into 1991

• Invasive including wiping surfaces, pressurized washes with hot and cold water, bioremediation, rock washing, tilling, and berm relocation

• Had major impacts on shoreline habitat, plants and animals

Direct effects on rocky intertidal species• Fucus removal - high and mid

shore• Limpet Tectura persona decline

high on shore• Balanoid barnacle decline• Blue mussel decline• Periwinkle Littorina sitkana

decline• Drilling predator Nucella

lamellosa decline• Main cause - pressurized washing

Indirect effects on rocky intertidal community

• Modest bloom of ephemeral algae in absence of Fucus competition and with low grazing

• Absent nearby canopy, Fucus spore arrival is limited and recruits desiccate high on shore

• Opportunistic barnacle colonizes heavily

• Fucus colonizing barnacle tests is uprooted

• Fucus expansion into low shore inhibits red algae

0

100

0

100

0

100

unoiled

oiled & not cleaned

oiled & cleaned

1990 1991 1992

% c

over

Fuc

usR

ed a

lgae

Possible indirect effects on rocky

intertidal

• Potential induction of unstable cycle in Fucus cover as single-aged colonist plants senesce in synchrony 5 yrs later

• Reduction of biogenic habitat normally provided by Fucus and blue mussels impacts gastropods and smaller invertebrates

Direct effects on shallow sedimentary communities

• Enhanced hydrocarbon-degrading bacteria

• Reduced shoot densities of eelgrass until 1993

• Reduced clam density (littlenecks, butters)

• Sediment toxicity to amphipods and reduced densities of some amphipod taxa

• Reduction of abundance of seastar Dermasterias and helmet crab Telmessus

Indirect effects in shallow sedimentary communities

• Increases in oligochaetes and surface deposit-feeders (polychaetes) via enhanced microbial food and reduced invert predation

• Continued depression in clam recruitment to 1998 via absence of fine sediments moved down slope during pressurized washing

• Probable enhanced growth of demersal fishes• Probable reduction in phytal eelgrass species

Direct effects in shallow subtidal rocky community

• Size distributions of dominant kelps imply mortality of adults in 1989 followed by rapid recolonization of juveniles in 3 systems

• Reduction in abundance of 2 seastars Dermasterias and Evasterias and helmet crab Telmessus, recovering by 1993

0

4

8

# 10

0 m

-2 (+

1SE

)

Telmessus cheiragonus

Dermasterias imbricata

0

9

18

1990 1991 1992

Avg. density in shallow bays

oile

dun

oile

d

Indirect effects in shallow subtidal rocky

community

• Enhanced abundances and sizes of green sea urchins on northern Knight where sea otters had not recovered by 1998, possibly inducing future trophic cascades

• Possible release of predation on prey of seastars and helmet crabs in kelp and seagrass communities

Resident nearshore fishes• Direct acute effects

– reduced abundance and biomass of intertidal fishes in 1990 with recovery well advanced by 1991

– parasite burden enhanced in some demersal fishes

• Direct effects of chronic exposure– hemosiderosis in intertidal fishes 1990-93– P450 detoxification system induced in masked greenling -

1996

• Indirect effects– in shallow subtidal, juvenile cod and Arctic shanny increased

by >100% at oiled sites perhaps in response to enhanced mytilid prey

Intertidal and shallow-spawning fishes - direct acute effects

• Premature hatch, larval abnormalities and elevated mortality in herring

• Egg mortality enhanced in pink salmon

• Possible egg mortality in sand lance and capelin, important forage fishes that deposit eggs in shallow sediments

Intertidal and shallow-spawning fishes - effects of chronic exposure

• Pink salmon egg mortality enhanced for at least 4 yrs due to exposure to weathered oil in streams.

• Possible genetic damage to pink salmon affecting their rate of straying and reproductive output

• Possible contribution of oiling stress to disease induction that led to 1993 herring crash, which has persisted for at least 8 more yrs

Summer foraging fishes in nearshore - direct acute & chronic effects

• Pink salmon - reduced growth in 1989 with smaller effect in 1990, likely lowering survival at sea

• Dolly Varden and cutthroat trout - reduced growth and possibly survival 1-3 yrs after EVOS

• Chum (and other?) salmon likely experience analogous effects of detoxification costs

• Induction of P450 detoxification system 1-3 yrs after EVOS in pink salmon, Dolly Varden, soles, and others

Shorebirds and seaducks - consumers of intertidal inverts

– large numbers of oiled dead birds collected post spill

– shoreline surveys show detectable declines in some taxa at oiled sites compared with unoiled control sites using a pre-spill survey in 1984-85 to control for spatial variability

• Direct acute effects of EVOS

Shorebirds - consumers of benthic invertebrates

– black oystercatcher - fed chicks more oiled prey to achieve growth, fledged later, laid fewer eggs in second brood upon disturbance

– nesting of black oystercatchers stable on unoiled Montague, while disrupted on oiled Green Island, recovering by 1993

– black oystercatcher - counts declined further from 1989-90 before recovering in 1991-93

• Chronic exposure effects

# of

egg

s (+

1S

E)

0

2

# of eggs laid in 2nd nesting after

loss of 1st nest

oiled unoiled

Seaducks - consumers of benthic inverts

• Indirect and chronic exposure effects

– harlequin duck - lower adult female over-winter survival evident in 1995-96, 1996-97, 1997-98

– harlequin duck - winter counts still declining in western (oiled) compared to eastern PWS through 1997-98

– Barrow’s goldeneye - growing divergence in abundance between oiled and unoiled survey data through 1998

– harlequin duck in 1998 and Barrow’s goldeneye in 1996-97 - elevated P4501A

Avian consumers of forage fish

• Direct acute effects

– oiled dead birds of many species collected on shore

– statistically detectable declines in 1989

• Indirect and chronic effects

– cormorants, mergansers, black-legged kittiwake, murres, pigeon guillemot, and loons show depressed counts through at least 1998 (1993 for loons)

– pigeon guillemot shows lower nest productivity in 1993-98 with reduced availability of high-lipid forage fish like herring

Avian scavengers and omnivores in shoreline habitats

• Direct acute effects

– reduction of 10% in PWS bald eagles in 1989

– reduction of northwestern crows in 1989

– PWS mortality of eagle eggs exposed to oil in 1989

• Indirect and chronic effects

– northwestern crows more concentrated on oiled Kenai shores in 1989

– over yrs PWS counts of bald eagles and glaucous-winged gulls are enhanced

Marine mammals of shoreline habitats

• Direct acute effects of EVOS– sea otter - over 1,000 oiled corpses recovered,

representing an estimated 2,800-5,000 mortalities from encounter with oil

– harbor seal - direct mortality estimated at about 300 individuals in PWS alone

– Steller sea lion - likely mortalities from same mechanism (inhalation of toxic fumes) that affected seals

c Bakhtin

Marine mammals of shoreline habitats

• Indirect and chronic exposure effects– sea otter juveniles over-winter mortality higher in oiled

areas in 1990-91 and 1992-93– sea otter carcass counts show high prime age mortality

for at least 5 yrs following EVOS– sea otter counts not yet recovered in PWS, especially

northern Knight Island– P450 detoxification system induced in sea otters in

1996-98

c Bennett

Marine mammals of shoreline

habitats

• Indirect and chronic exposure effects (cont’d)–harbor seal molt counts have not initiated convergence in PWS through at least 1997

–river otters had larger home ranges in oiled areas, greater abandonment of latrine sites 1990

–reduction of blood hemoglobin in river otters, diminishing oxygen delivery, diving ability

–elevated haptoglobin counts in river otters through 1991

Indirect, chronic, delayed effects

• Abundant evidence of their existence from controlled field sampling over yrs

• Loss of biogenic habitat– Fucus, mussels, eelgrass

• Tend to move up the food chain– organic enrichment of the food chain– sublethal effects of ingesting contaminated

foods with reproductive and population impacts

– loss of forage fish prey

Indirect, chronic, delayed effects

– increases in size and abundance of sea urchins on northern Knight probably reflects reduced predation by sea otters and may lead to localized overgrazing of kelps and loss of fish habitat

– reduction of harbor seals and sea lions may be causing transient killer whales to switch to sea otters with dramatic ecosystem implications

• Possible top-down effects

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 mortality of individual species to short-lived water-soluble fraction of oil (mostly BTEX plus napthalene)

Limitations of old dogma underlying ecotoxicity risk assessment

• Based solely on short-term acute toxicity in lab

• Typically assesses only one mechanism (eg, exposure to WSF – water-soluble fraction)

• Treats species as independent, not linked through food web or habitat responses

•Extrapolates from few lab-rat species to species taxonomically similar but potentially different in ecology and physiology

•Includes no effects of chronic exposure, delayed impacts, or interactions among species

•Includes no sub-lethal impacts on growth, development, or reproduction – all of which can translate to population consequences

Limitations of old dogma underlying ecotoxicity risk assessment

Problems with field-based empirical assessment approach

• Expensive to conduct – who should pay?• Study design begets conclusions – who should design

the study?• Typically lack before data – but rigorous study designs

are still possible • Time-consuming to capture indirect, chronic, and

delayed effects – but necessary • High uncertainty because complex mix of mechanisms

not all elaborated – who should bear the burden of proof?

Implications for future oil spills

• Omission of indirect, chronic, delayed effects in ecotoxicity risk models amounts to a large understatement of oil spill impacts

• Predictive ability of such indirect effects by ecological science lies far in the future, although some strong interactions can be confidently predicted