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 # 100 m -2 (+1SE) Telmessus cheiragonus Dermasterias imbricata Avg. density in shallow bays oiled unoiled

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 –P450 detoxification system induced in masked greenling 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 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 before recovering in Chronic exposure effects # of eggs (+ 1SE) 0 2 # of eggs laid in 2 nd nesting after loss of 1 st nest oiled unoiled

Seaducks - consumers of benthic inverts Indirect and chronic exposure effects –harlequin duck - lower adult female over-winter survival evident in , , –harlequin duck - winter counts still declining in western (oiled) compared to eastern PWS through –Barrow’s goldeneye - growing divergence in abundance between oiled and unoiled survey data through 1998 –harlequin duck in 1998 and Barrow’s goldeneye in 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 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 and –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 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