Series Contents for Last Ten Years* VOLUME 27, 1990. Dall, W., Hill, B. J., Rothlisberg, E C. and Sharpies, D. J. The biology of the Penaeidae, pp. 1-461. VOLUME 28, 1992. Heath, M. R. Field investigations of the early life stages of marine fish. pp. 1-174. James, M. A., Ansell, A. Q. D., Collins, M. J., Curry, G. B., Peck, L. S. and Rhodes, M. C. Biology of living brachiopods, pp. 175-387. Trueman, E. R. and Brown, A. C. The burrowing habit of marine gastropods, pp. 389--431. VOLUME 29, 1993. Kicrboe, T. Turbulence, phytoplankton cell size, and the structure of pelagic food webs. pp. 1-72. Kuparinen, K. and Kuosa, H. Autotrophic and heterotrophic picoplankton in the Baltic Sea. pp. 73-128. Subramoniam, T. Spermatophores and sperm transfer in marine crustaceans, pp. 129-214. Horwood, J. The Bristol Channel sole (Solea solea (L.)): a fisheries case study, pp. 215-367. VOLUME 30, 1994. Vincx, M., Bett, B. J., Dinet, A., Ferrero, T., Gooday, A. J., Lambshead, E J. D., Pfannkiiche, O., Soltweddel, T. and Vanreusel, A. Meiobenthos of the deep Northeast Atlantic. pp. 1--88. Brown, A. C. and Odeandaal, E J. The biology of oniscid Isopoda of the genus Tylos. pp. 89-153. Ritz, D. A. Social aggregation in pelagic invertebrates, pp. 155-216. Ferron, A. and Legget, W. C. An appraisal of condition measures for marine fish larvae, pp. 217-303. Rogers, A. D. The biology of seamounts, pp. 305-350. VOLUME 31, 1997. Vinogradov, M. E. Some problems of vertical distribution of meso- and macroplankton in the ocean, pp. 1-92. Gebruk, A. K., Galkin, S. V., Vereshchaka, A. J., Moskalev, L. I. and Southward, A. J. Ecology and biogeography of the hydrothermal vent fauna of the Mid-Atlantic Ridge. pp. 93-144. *The full list of contents for volumes 1-37 can be found in volume 38.
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CONTENTS FOR LAST TEN YEARS
Parin, N. V., Mironov, A. N. and Nesis, K. N. Biology of the Nazca and Sala y Gomez submarine ridges, an outpost of the Indo-West Pacific fauna in the eastern Pacific Ocean: composition and distribution of the fauna, its communities and history, pp. 145-242. Nesis, K. N. Ganotid squids in the subarctic North Pacific: ecology, biogeography, niche diversity and role in the ecosystem, pp. 243-324. Vinogradova, N. G. Zoogeography of the abyssal and hadal zones, pp. 325-387. Zezina, O. N. Biogeography of the bathyal zone. pp. 389-426. Sokolova, M. N. Trophic structure of abyssal macrobenthos, pp. 427-525. Semina, H. J. An outline of the geographical distribution of oceanic phytoplankton, pp. 527-563. VOLUME 33, 1998. Mauchline, J. The biology of calanoid copepods, pp. 1-660. VOLUME 34, 1998. Davies, M. S. and Hawkins, S. J. Mucus from marine molluscs, pp. 1-71. Joyeux, J. C. and Ward, A. B. Constraints on coastal lagoon fisheries, pp. 73-199. Jennings, S. and Kaiser, M. J. The effects of fishing on marine ecosystems. pp. 201-352. Tunnicliffe, V., McArthur, A. G. and McHugh, D. A. biogeographical perspective of the deep-sea hydrothermal vent fauna, pp. 353-442. VOLUME 35, 1999. Creasey, S. S. and Rogers, A. D. Population genetics of bathyal and abyssal organisms, pp. 1-151. Brey, T. Growth performance and mortality in aquatic macrobenthic invertebrates, pp. 153-223. VOLUME 36, 1999. Shulman, G. E. and Love, R. M. The biochemical ecology of marine fishes. pp. 1-325. VOLUME 37, 1999. His, E., Beiras, R. and Seaman, M. N. L. The assessment of marine pollution - bioassays with bivalve embryos and larvae, pp. 1-178. Bailey, K. M., Quinn, T. J., Bentzen, P. and Grant, W. S. Population structure and dynamics of walleye pollok, Theragra chalcogramma, pp. 179-255. VOLUME 38, 2000 Blaxter, J. H. S. The enhancement of marine fish stocks, pp. 1-54. Bergstr6m, B. I. The biology of Pandalus. pp. 55-245.
CONTRIBUTORS TO VOLUME 39
C. D. ELVIDGE,Office of the Director, NOAA National Geophysical Data
Center, 325 Broadway, Boulder, CO 80303, USA W. S. JOHNSON, Department of Biological Sciences, Goucher College,
Towson, MD 21204, USA C. H. PETERSON,University of North Carolina at Chapel Hill, Institute of Marine Sciences, Morehead City, North Carolina 28557, USA P. G. RODHOUSE,British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, UK M. STEVENS,Department of Biology, Ripon College, 300 Seward Street, Ripon, WI 54971, USA P. N. TRATHAN, British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, UK L. WATLING,School of Marine Science, Darling Marine Center, University of Maine, Walpole, ME 04573, USA
The "Exxon Valdez" Oil Spill in Alaska: Acute, Indirect and Chronic Effects on the Ecosystem C h a r l e s H. P e t e r s o n
University of North Carolina at Chapel Hill, Institute of Marine Sciences, Morehead City, North Carolina 28557, USA FAX." 252-726-2426 e-mail:
[email protected] 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. History and Fate o f the Oil Spilled f r o m the " E x x o n Valdez". . . . . . . . . . . . . . . . . . 3. Biological C o n s e q u e n c e s o f the Oil Spill in the Intertidal Z o n e . . . . . . . . . . . . . . . 3.1. E x p o s u r e to oil and c o n t a m i n a t i o n o f o r g a n i s m s . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. C h a n g e s in species a b u n d a n c e s and c o m m u n i t y c o m p o s i t i o n of rocky s h o r e s 4. Biological C o n s e q u e n c e s o f the Oil Spill in the Subtidal Z o n e . . . . . . . . . . . . . . . . 4.1. Effects on eelgrass c o m m u n i t i e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Effects on d e e p e r benthic systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Effects on kelp c o m m u n i t i e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Impacts on Vertebrates That Use S h o r e l i n e Habitats . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1. Terrestrial m a m m a l s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. Terrestrial birds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3. Fishes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4. M a r i n e m a m m a l s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.5. Shorebirds, seaducks, and seabirds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Discussion 6.1. Interaction w e b s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2. Ecotoxicology vs field a s s e s s m e n t as a p p r o a c h e s . . . . . . . . . . . . . . . . . . . . . . . . . 6.3. U n d e r s t a n d i n g d e l a y e d recoveries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7. S u m m a r y and Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements ................................................................... References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3 6 13 13 16 34 34 39 40 43 43 45 48 60 64 70 70 75 79 81 83 84
Following the oil spill in Prince William Sound, Alaska, in 1989, effects were observed across a wide range of habitats and species. The data allow us to evaluate direct and indirect links between shoreline habitats and the
ADVANCES IN MARINE BIOLOGY VOL. 39 ISBN 0-124)26139-1
Copyright © 2001 Academic Press Limited All rights of reproduction in any form reserved
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CHARLES H. PETERSON
coastal ecosystem in general The intertidal zone suffered from direct oiling and clean-up treatments such as pressurized hot water, resulting in freeing of bare space on rocks and reductions in fucoid algal cover. Grazing limpets, periwinkles, mussels and barnacles were killed or removed. Subsequent indirect effects included colonization of the upper shore by ephemeral algae and an opportunistic barnacle and, in some regions, spread ofFucus gardneri into the lower shore where it inhibited return o f red algae. The loss of habitat provided by the Fucus canopy slowed recovery on high shores, and lowered abundance o f associated invertebrates. Abundance of sediment infauna declined and densities of clams were reduced directly. Their recovery was still incomplete by 1997 on oiled and treated shores where fine sediments had been washed down slope during treatment. Impacts in subtidal habitats were less intense than in the intertidal zone. Kelps were reduced in 1989 but recovered rapidly through re-colonization by 1990. Abundances of a dominant crab and seastar were reduced greatly, with recovery of the more mobile species, the crab, occurring by 1991. For about 4 years, there was reduced eelgrass density and hence less habitat for associated animals. Abundance o f several toxin-sensitive amphipods declined dramatically and had not recovered by 1995. In general, however, many subtidal infaunal invertebrates increased in abundance, especially oligochaetes and surface deposit-feeding polychaetes. This may have resulted from increases in sediment hydrocarbon-degrading bacteria, but may also reflect reduction o f predators. Along northern Knight Island, where sea otter populations had not recovered by 1997, green sea-urchins were larger, compared with those in un-oiled parts of Montague Island. This initial response from reduced predation by sea otters, if sustained, could lead to additional indirect effects of the spill. Scavenging terrestrial birds, such as bald eagles and northwestern crows, suffered direct mortality as adults and reproductive losses, although eagles recovered rapidly. Numbers o f intertidal benthic fishes were 40% lower on oiled than on un-oiled shores in 1990, but recovery was underway by 1991. Small benthic fishes living in eelgrass showed sensitivity to hydrocarbon contamination until at least 1996, as evidenced by hemosiderosis in liver tissues and P450 1A enzyme induction. Oiling of intertidal spawning habitats affected breeding o f herring and pink salmon. Pink salmon, and possibly Dolly Varden char and cut-throat trout, showed slower growth when foraging on oiled shorelines as older juveniles and adults, which for pink salmon implies lower survival The pigeon guillemots that suffered from the oil spill showed reduced feeding on sand eels and capelin, which may also have been affected by the spill, and this may have contributed to failure of guillemot recovery. There was an analogous failure of harbor seals to recover. Sea otters declined by approximately 50%, and juvenile survival was depressed on oiled shores for
EFFECTS OF "EXXON VALDEZ" OIL SPILL
3
at least four winters Both black oystercatchers, shorebirds that feed on intertidal invertebrates, and also harlequin ducks showed reduced abundance on oiled shores that persisted for years after the spill. Oystercatchers consumed oiled mussels from beds where contamination by only partially weathered oil persisted until at least 1994, with a resulting impact on productivity o f chicks A high over-winter mortality of adult harlequin ducks continued in 1995-96, 1996-97 and 1997-98. Delays in the recovery o f avian and mammalian predators of fishes and invertebrates through chronic and indirect effects occurred long after the initial impacts o f the spill. Such delayed effects are not usually incorporated into ecotoxicity risk assessments which thus substantially underestimate impacts o f a spill. Detection o f delayed impacts requires rigorous long-term field sampling, so as to observe the dynamics o f recovery processes.
1.
INTRODUCTION
The high mortality of wildlife, contamination of pristine habitats, and loss of natural ecosystem products such as subsistence and fishing (Wells et al., 1995; Rice et al., 1996) render the oil spill from the tanker "Exxon Valdez" in 1989 an environmental mishap of international concern and significance. Yet the event also represents an opportunity to use the locally intensive perturbation of the oil spill to extract valuable new understanding of ecological interconnections within the ecosystem. The costs of a planned perturbation on this scale and the costs of evaluation of ecosystem response are far higher than could ever be funded by traditional sources of scientific support. Following the oil spill, however, substantial expenditures of funds both by the government trustees for public natural resources and also independently by Exxon Corporation supported extensive field studies of impacts and recovery from the oil spill (Paine et al., 1996). Whereas the initial field studies were largely devoted to assessing injuries to individual species, as required by attorneys for litigation, early studies of coastal habitats possessed a broader community perspective from the start. Subsequent studies of affected species in other habitats conducted after settlement of federal and state claims for compensation also adopted an integrative and functionally based ecological approach to understanding recovery processes (Cooney, 1998; Duffy, 1998; Holland-Bartels et al., 1998; Okey and Pauly, 1998). There is now an immense body of literature on the "Exxon Valdez" spill. Scanning of just one database on CD-ROM shows several hundred publications on Alaskan oil pollution since 1990, and some authors have managed to produce three publications a year in this period. Thus a review
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CHARLES H. PETERSON
is urgently needed to bring this large body of data before a wider readership. The information now available on the response of the coastal ecosystem of Alaska to the oil spill permits a synthesis of direct acute and also chronic and indirect effects of the spill, providing new insights into the functional importance and roles of nearshore habitats. There are two basic scientific approaches available by which to assess biological impacts from an oil spill (Gilbert, 1987). One approach involves modelling the likely impacts based upon laboratory information on toxicological responses of a limited set of individual species to varying concentrations of oil, typically in dissolved phase or as a function of sediment mass. These toxicological data are then used along with information on (1) pre-spill densities of all species, (2) concentration, exposure and uptake of oil, and (3) the transport, transformation and fate of the oil to model the expected mortality (French et al., 1996). Knowledge of the in situ exposure dosage and the time function of exposure dosage are always incomplete and uncertain. Typically, data on toxicological response are available for only a few of the species of interest so that other taxonomically related species are then used as proxies for modelling effects. Toxicity is a function of temperature, so the application of study results at a fixed temperature to field conditions requires some assumptions about how changing temperature would influence the toxicity thresholds. In the absence of field surveys there is great uncertainty over the pre-spill abundances of many of the species in the affected area. The alternative holistic, non-reductionist approach involves use of sampling theory to design field studies of impact. If funds are available, this approach is to be preferred because of several advantages. First, it integrates all mechanisms of impact rather than estimating response by often only a single mechanism, toxicity of dissolved oil. Secondly, chronic effects can be evaluated empirically with an adequate long-term sampling design. Third, this field-based approach can incorporate the web of ecological interactions that induce indirect as well as direct effects of the oil spill (NRC, 1981; Gilbert, 1987; Johnson et al., 1989; Clements and Kiffney, 1994). The field assessment implicitly includes indirect effects driven by changes in habitat, predators, prey and competitors, thereby providing a more realistic, albeit complex, understanding of impacts to the ecological system (Underwood and Peterson, 1984; Peterson, 1993). To some degree, these two approaches can be complementary: toxicology can illuminate mechanistic contributions of one or more pathways of direct impact early in the spill and identify sensitive species, while field-based assessment provides an integration of all pathways including chronic delayed and indirect effects. However, in practice, the toxicological approach is typically adopted simply to minimize the costs of assessment of damages to biological resources despite the penalty of greater uncer-
EFFECTS OF "EXXON VALDEZ" OIL SPILL
5
tainty and exclusion of many potential mechanisms of injury (Kimball and Levin, 1985; Clements and Kiffney, 1994). An oil spill at sea can be dissected into at least three separate phases (NRC, 1985; Wolfe et al., 1994). During the first phase, the oil floats on the sea surface, where injury is inflicted on organisms that use the surface and on those exposed to toxic fumes released by volatilization into the local atmosphere. If wave action is sufficiently intense, the oil may also be mixed to some depth in the water column, where sensitive organisms are exposed and injured. It was during this first phase of the "Exxon Valdez" oil spill that most of the recorded mortality of seabirds and marine mammals occurred (Piatt and Lensink, 1989). The second phase commences with the deposition of the oil on intertidal land masses. Here impacts occur through multiple mechanisms to the plants and animals that occupy the intertidal zone as well as to the abiotic habitat itself. The length of time spent floating at sea affects the physical and chemical nature of the oil once grounded, so it is an important determinant of impact. The third phase of the spill involves deposition of oil in particulate form onto the subtidal sea floor, where it can affect plants, animals, and the nursery and foraging habitats for various species. If the spilled oil never encounters the shore, this third phase can occur in the absence of the second. This review addresses the impacts of these latter two (depositional) phases of the "Exxon Valdez" oil spill and uses data from intensive field assessments to evaluate the network of ecological responses to shoreline oiling and subsequent treatments as a perturbation to the coastal ecosystem. In synthesizing direct as well as chronic and indirect impacts of shoreline oiling, the review is a response to recent appeals for additional scientific study of longer-term impacts of petroleum exposures in the environment (Gray, 1982; NRC, 1985; Boesch et al., 1987; Capuzzo. 1987). The intertidal and shallow subtidal zones of the sea are occasionally dismissed as irrelevant by oceanographers because of the small proportion of the ocean that they occupy. Such a narrow view overlooks the tremendous biological significance of this region of the sea (Mann, 1982; Raffaelli and Hawkins, 1996). The intertidal zone occupies the unique triple interface among land, sea and atmosphere. The land provides a substratum for occupation by intertidal organisms, the seawater is a vehicle for transport and supply of nutrients and larvae, and the air a medium for passage of solar energy and a source of physical stress (ConneU, 1972). Interfaces between separate systems are locations of typically intense biological activity. As a triple interface, the intertidal zone is exceptionally productive (Leigh et al., 1987). Wind and tidal energy combine to subsidize the intertidal zone with planktonic foods produced in the photic zone of the coastal ocean. Runoff from adjacent land injects
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CHARLES H. PETERSON
new supplies of inorganic nutrients to fuel the high coastal plant production (Mann, 1982; Nixon et al., 1986). The consequent abundance and diversity of life and life forms in the intertidal zone serves many valued consumers, including humans, coming to use this habitat from land, sea and air. The aesthetic and cultural values of the intertidal zone and its resources augment its significance. Yet, the same physical transport processes that are responsible for their high level of biological productivity also place the intertidal habitats at great risk to floating pollutants, such as oil. The adjacent shallow subtidal habitats share a high level of biological productivity and typically provide critical biogenic habitat that serves as vital spawning, nursery and foraging grounds. Shallow subtidal areas are also at high risk of injury from oil spills because of their exposure to wave-mixed oil and their role as repositories of sedimented hydrocarbons. Thus, the intertidal and shallow subtidal zones become a natural focal point for understanding injuries and recovery from a coastal oil spill.
2.
HISTORY AND FATE OF OIL SPILLED FROM THE "EXXON VALDEZ"
Prince William Sound is the water body in which the "Exxon Valdez" oil spill originated. Prince William Sound, on the margin of the northern Gulf of Alaska, is home to a diverse and productive coastal ecosystem, in which charismatic marine mammals and seabirds are especially evident (SAI, 1980; Hood and Zimmerman, 1986). The affected region, from Prince William Sound along the outer Kenai Peninsula and lower Cook Inlet coast to the Kodiak Island Archipelago and out along the Alaska Peninsula, is notable for its wilderness areas and parks, rich fishing grounds, recreational opportunities and cultural heritage for native Americans. The rugged shoreline reflects its recent and, in places, ongoing glaciation. Historically, the northern Gulf of Alaska has seen major changes in its marine ecosystem caused by both natural and anthropogenic perturbations Over-exploitation of sea otters during the fur trade of the 19th and early 20th centuries virtually eliminated sea otters from the system (Simenstad et al., 1978). This produced major alterations in the coastal ecosystem, as sea urchin populations expanded and overgrazed kelps in the nearshore (Estes and Palmisano, 1974; Estes and Duggins, 1995). Conservation measures allowed the return of the sea otter, which has resulted in a restoration of the alternate state of the ecosystem in which sea-urchins are less abundant and kelps and associated organisms dominate the nearshore rocky coasts. The earthquake of 1964 caused massive impacts to the shoreline communities, with uplift of shorelines in
EFFECTS OF "EXXON VALDEZ" OIL SPILL
7
Prince William Sound ranging from 1-3 m. In the mid 1970S, the ocean climate of the northern Gulf of Alaska began a major change that dramatically modified the marine ecosystem. The demersal system of the northern Gulf of Alaska around Kodiak Island, previously dominated by crabs and shrimps, changed to one in which groundfish such as walleye pollock and flatfishes now dominate (NRC, 1996; Anderson and Piatt, 1999). Because of the valuable fisheries, wildlife, recreational opportunities, and cultural significance, there was much discussion over the wisdom of permitting the oil pipeline from the North Slope to terminate in Prince William Sound. Indeed, the "Exxon Valdez" tanker ran aground in the process of transporting north-slope crude oil from the pipeline terminus in Valdez. The "Exxon Valdez" grounded on Bligh Reef late on the night of 24 March 1989. An estimated 10.8 million gallons (35 000 tonnes out of a total cargo of 175 000 tonnes) of Alaskan North Slope (ANS) crude oil were released into northern Prince William Sound (Pain, 1989; Dayton, 1990; Spies et al., 1996). ANS, or Prudhoe Bay oil, as it is sometimes referred to, is rich in volatile hydrocarbons (Pain, 1989). The tonnage of oil released in this spill was exceeded by many previous oil spills worldwide. Nevertheless, the magnitude of ecological effects of the "Exxon Valdez" spill makes it by most standards the world's most damaging, because of its proximity to a coastal ecosystem so rich in seabirds, marine mammals and shoreline-dependent species. Approximately 40-45% of the oil was estimated by Wolfe et al. (1994) to have been deposited on intertidal shores of Prince William Sound (Figure 1). About 25% was transported by winds and ocean currents out of the sound, most of which later grounded on shores of the Kenai Peninsulalower Cook Inlet area or the Kodiak Archipelago-Alaska Pensinsula region (Table 1). Two sets of aerial surveys reveal grossly similar extents of shoreline oiling (Table 2). Aerial surveys by the Alaska Department of Natural Resources (ADNR, 1991) showed that by the end of summer 1989: (1) out of 1891 km of Prince William Sound shoreline observed, 446km exhibited light to heavy oil impact; (2) out of 1662km of Kenai-Cook Inlet shoreline observed, 260km exhibited very light to heavy oil impact; and (3) out of 2960 km of Kodiak-Alaska Peninsula shoreline observed, 943 km exhibited very light to heavy oil impact. Heavy stranding of oil was most prevalent nearer the spill site along Prince William Sound shores, where 144km were characterized as heavily contaminated by oil in these aerial surveys, as compared with 28 km in the Kenai-Cook Inlet region and nine in the Kodiak-Alaska Peninsula region. Beachwalk surveys organized by the Alaska Department of Environment and Conservation confirmed the accuracy of the aerial measures of the extent of shoreline oiling. Neff et al. (1995)
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CHARLES H. PETERSON
Figure 1 Map of Prince William Sound and, inset, the northern Gulf of Alaska to Kodiak Island, showing the area transited by floating "Exxon Valdez" oil (coarse stipple), using results integrated from all sources. The oil was released in northern Prince William Sound at Bligh Reef, where the oil track narrows to a point. (Adapted from Babcock et al., 1996.)
9
EFFECTS OF "EXXON VALDEZ" OIL SPILL
Table 1 Fate of the approximately 10.8 million gallons of Alaskan North Slope crude oil spilled from the "Exxon Valdez", as percentages on 1 May 1989 (from Wolfe et al., 1994).
% of spilled oil Beached in Prince William Sound Beached on the Kenai Peninsula Transported past Cape Douglas into the Shelikof Strait and probably beached on Alaska Peninsula and Kodiak Archipelago Remained floating in Kenai region (and probably beached later in Shelikof Strait)
41.0
5.2 1.8
Table 2 Estimated extent and intensity of shoreline oiling by "Exxon Valdez" spilled oil by the end of summer (August) 1989.
Kilometers of oiled shore Geographic area
Shoreline aerially surveyed (km)
Light
Moderate
Heavy
1891 1662 2960
190 182 867
112 50 67
144 28 9
1450
549*
94
141
from A D N R (1991)
Prince William Sound Kenai-Cook Inlet Kodiak-Alaska Peninsula from Neff et al. (1995)
Prince William Sound
* Includes very light as well as light oiling.
reported lengths of oiled shoreline by oiling intensity and geographic region that revealed similar patterns (Table 2). The hundreds of kilometers of oiled shorelines within the spill area included segments of all types of intertidal habitats, including exposed rocky shores, exposed wave-cut platforms, sheltered rocky shores, boulder, gravel and cobble beaches, coarse-grained sand beaches, fine-grained sand beaches, exposed and sheltered tidal flats, and salt marshes (see RPI, 1983 for geomorphologic definitions). Of these, the exposed rocky shores, the sheltered rocky shores, and the gravel, cobble and boulder ("coarsetextured") beaches received the large majority of the heavy oiling (Page et al., 1995). The beaches with mostly fine-grained sediments and the salt marshes comprised much less of the potentially, and of the actually, oiled coastline (ADNR, 1991). In the summers of 1989 and 1990, and again at reduced intensity in the summer of 1991, extensive and intensive shoreline
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CHARLES H. PETERSON
Figure 2 An example of the intensive nature of the clean-up operations after the "Exxon Valdez" spill. Spraying a beach with pressurized hot water. Photograph courtesy of "Exxon Valdez" Oil Spill Trustee Council.
treatments were conducted in an attempt to speed removal oil from intertidal shores in the spill area. Several techniques were employed: especially wiping rocks with absorbent cloth, manual bagging and removal of oiled rocks, low-, medium-, and high-pressurized hot-water washing, bioremediation of two main types (fertilization to stimulate bacterial degradation of the hydrocarbons), and hand and mechanical raking and tilling to expose buried pools of oil (Mearns, 1996). Figure 2 gives an idea of the intensity of the clean-up operations. The movement of the oil away from its initial location floating on the sea surface was documented by several studie~ First, direct sampling of the water column by NOAA (Short and Harris, 1996a) and by Exxon researchers (Neff and Stnbblefield, 1995) detected low concentrations of oil (1--8 ppb of total aromatic hydrocarbons) in the first 1-5 weeks after the spill when large masses of floating oil were still moving through Prince William Sound. By the end of the 1989 summer, water-column oil was difficult to detect by direct sampling of the water (Neff and Stubblefield, 1995). Its continued presence in biologically available form was, however, documented by contamination of experimentally transplanted clean mussels (Mytilus trossulus Gould) into cages held at different depths below the
EFFECTS OF "EXXON VALDEZ" OIL SPILL
11
sea surface at several locations within the spill area (Short and Harris, 1996b). Mussels filter particles from large volumes of water so that they concentrate polycyclic aromatic hydrocarbons (PAH) and other lipophilic contaminants, making them better indicators of the presence of biologically active contaminants than water samples. Short and Harris (1996b) used gas chromatography-mass spectrometry (GC-MS) analysis to show that this oil was derived from particulate sources and was not limited to the lighter more water-soluble fractions. Shigenaka and Henry (1995) deployed mussels and a semipermeable membrane sampler at a heavily oiled site at Smith Island and showed that in summer 1992 there was still an operative pathway of exposure and contamination through the water column: the PAH composition spectrum in the experimentally deployed mussels resembled that of oiled sediments and surface oil sheens, suggesting the likely pathways of transport. Studies of the sedimentary habitat also confirmed the transport and deposition of "Exxon Valdez" oil onto shallow subtidal sediments. Sediment traps deployed in the subtidal environment near oiled beaches in 1990 and 1991 collected contaminated sediments, demonstrating one mechanism of movement of the oil to the sea floor (Short et al., 1996). Oil was transported subtidally in association with sediment particles, probably originating from the intertidal beaches, for at least as long as 1-2 years after the spill. PAH composition of these oiled particles matched the "Exxon Valdez" oil (Short et al., 1996). Sampling of the sediments in 1989 and 1990 (Carlson and Kvenvolden, 1996; O'Clair et al., 1996) showed widespread oil contamination in the 0-20 m depth zone within the spill region, and that concentrations were generally highest at shallower depths and from sites near the most heavily contaminated beaches. Hydrocarbon contamination was sometimes detected at 40 and 100 m depths; however, in most cases, the components of the hydrocarbons did not correspond to the "Exxon Valdez" crude oil (Bence and Burns, 1995; O'Clair et al., 1996). Outside Prince William Sound, the concentrations of "Exxon Valdez" hydrocarbons in subtidal sediments were low and patchy, reflecting the discontinuous nature of the oil slick and oiling pattern in the Gulf of Alaska region (O'Clair et al., 1996). Oil concentrations in shallow subtidal sediments decreased greatly from July 1989, when a maximum average concentration was recorded at 0 m on Disk Island of 12 729 ng g-l, to summer 1990, when total PAH concentrations in most intertidal sediments had declined to 100-200ngg -1. By then PAHs recognizably matching "Exxon Valdez" oil were found in shallow subtidal sediments at only a few locations (O'Clair et al., 1996). PAH contamination of shallow subtidal sediments in and around oiled eelgrass beds in Prince William Sound persisted at low (100-200 ng g-~) but statistically significant levels as compared with unoiled control
12
CHARLES H. PETERSON
seagrass beds until at least 1995, when sampling in and around eelgrass ended (Jewett et al., 1999). The persistence and weathering processes of grounded oil varied with physical conditions of the oiled habitat. Visible surface oil was reduced relatively rapidly through shoreline treatment and natural action of winter storms, so that, by 1991, surface oil was found only in small amounts (Owens, 1991; Michel and Hayes, 1993). On sheltered shores, surface oil was more persistent, with "asphalt pavements" and "mousse" remaining in many upper intertidal locations at least until 1993 (Gibeaut and Piper, 1997) and 1994 (Irvine et al., 1999). The continued persistence of oil blemishes in National Parks such as Katmai and Kenai Fjords, on state public trust lands, and on native lands that are the basis for culture and subsistence represents a long-lived injury to human uses and values. The rate of disappearance of surface oil slowed through time, especially in sheltered habitats (Michel and Hayes, 1993; Hayes and Michel, 1999). Surface oil and subsurface oil remained in protected sites on heavily oiled beaches in positions where boulder and cobble armouring protected it from physical disturbance by waves (Owens, 1991; Gibeaut and Piper, 1997; Irvine et al., 1999). As of summer 1993, at least 4.8 km of shoreline in Prince William Sound retained surface oil, while at least 7 km retained subsurface oil-saturated sediments (Gibeaut and Piper, 1997). Additional beach treatments using chemical injections were conducted in summer 1997 on a trial basis to try to remove some of this recalcitrant subsurface oil (Broderson, 1998). The weathering of the oil was rapid except in sheltered rubble shores and armoured subsurface pockets of oil, where physical disturbance and oxygen penetration were limited. For example, by August 1992, the PAHs in sheltered rubble shores still contained some two-ring PAHs (Michel and Hayes, 1993), which are typically considered too volatile to persist for years after an oil spill and represent some of the most toxic constituents of the petroleum hydrocarbon mix. Oil removal and weathering were also inhibited in another type of armoured habitat, underneath mussel beds (Babcock et al., 1996; Boehm et al., 1996; Carls et al., 2000). The persistence of slowly weathering oil underneath mussels has biological significance because the oil is being ingested and concentrated in the mussels (Harris et al., 1996), and because the mussels are such important prey organisms for so many intertidal consumer species. Finally, oil persisted for a long time in another armoured habitat, in the subsurface rocks and cobbles along the intertidal banks of anadromous fish streams (Murphy et al., 2000). This environment was not subjected to pressurized hot-water treatments for fear of harming the salmon eggs. However, the tidal pumping of subtidal oil and slow release into the stream continued for eight or more years after the oil spill and represents a major pathway for chronic biological injury (Heintz et al., 1999).
EFFECTS OF "EXXON VALDEZ" OIL SPILL
3.
3.1.
13
BIOLOGICAL CONSEQUENCES OF THE OIL SPILL IN THE INTERTIDAL ZONE
Exposure to oil and contamination of organisms
The oil spilled by the "Exxon Valdez" rapidly contaminated biological resources along the path of the spill and entered food chains of intertidal and coastal ecosystems. A full list of affected species discussed in this review and their common names will be found in Appendix 1, pp. 101-103. Suspension-feeding invertebrates filter large volumes of seawater, resulting in a high potential for exposure to, and accumulation of, contaminants such as petroleum hydrocarbons. For this reason, suspension feeders such as the relatively long-lived and hardy blue mussel (Mytilus edulis L.), and the other west coast mussel (M. trossulus Gould), have been employed as sentinels of environmental quality (e.g. NOAA Mussel Watch: Goldberg et al., 1983; O'Connor, 1996). Numerous studies that followed the fate of the "Exxon Valdez" oil assessed the levels of hydrocarbon contamination in tissues of mussels and common species of suspension-feeding clams at sites spanning the spill area and extending for several years after the spill. Results of analysing the petroleum hydrocarbon contamination of mussels and four species of infaunal clams demonstrated widespread, locally long-lasting, and ecologically significant injuries in the intertidal system. First, analyses of water samples and tissues of experimentally introduced mussels during the months and early years following the "Exxon Valdez" oil spill confirmed that the activities of the mussels render them a more sensitive sampler of hydrocarbon contamination than direct water sampling (Short and Harris, 1996a, b). When hydrocarbons recovered from seawater fell below detection limits, mussels still contained substantial levels. This sampling of mussels is also ecologically meaningful because mussels are important members of many coastal food chains. Secondly, mussels sampled in 1977-1980 and in 1989 outside the spill area in the Valdez region of Prince William Sound (Karinen et al., 1993) had much lower hydrocarbon levels than those sampled in 1989 after the "Exxon Valdez" spill inside the spill area (Short and Babcock, 1996). Thirdly, the spatial sampling of mussels and clams of four species for analysis of petroleum hydrocarbon contamination revealed geographically widespread contamination within the spill areas both inside and outside Prince William Sound (Short et al., 1993; Short and Harris, 1996b; Trowbridge et al., 1998). Fourthly, while the levels of tissue contamination from petroleum hydrocarbons in mussels and clams declined over time from 1989 to 1990 and beyond, oiling persisted in many mussel beds. Ebert
14
CHARLES H. PETERSON
and Lees (1996) reported sampling data from mid-intertidal mussel beds in Prince William Sound showing that mean PAH concentrations averaged over the years of 1990-1993 increased from unoiled to oiled-but- untreated to oiled-and-hot-water-washed mussel beds. Pools of only partially weathered oil remained at least until 1996 in the sediments below and among the mats of mussel byssus and cobbles and fine sediments. This oil is protected from weathering processes by the shield of overlying rock, sediment, mussels and byssus threads (Babcock et al., 1996, 1997; Boehm et al., 1996; Harris et al., 1996; Cads et al., 2000). During shoreline treatment, dense mussel beds were generally not subjected to application of pressurized hot-water wash for fear of killing large quantities of the mussel resource known to be of high value to nearshore predators (Harris et al., 1996). Nonetheless, one of the surprises of the spill was the realization in 1991 that many mussel beds still contained relatively high concentrations of oiled sediments, oiled mussels and only partially weathered oil that included some of the more toxic constituents (Babcock et al., 1996). Sediments in 31 oiled mussel beds in Prince William Sound targeted for sampling in 1992 and 1993, because of suspected lingering contamination, contained hydrocarbon (TPH) levels greater than 10 000/zg g-1 wet weight. Five of 18 beds sampled along the Kenai Peninsula had TPH concentrations above 5000/~g g-1 wet weight of sediments. Sampling of the mussel tissues also showed contamination, revealed by PAH fingerprinting to be "Exxon Valdez" oil: concentrations in mussels were about two orders of magnitude lower than in the sediments (Babcock et al., 1996; Harris et al., 1996). Spatial contrasts of the covariance of oiled sediments and mussels demonstrated tremendous patchiness of oiling on even fine scales within the beds (Boehm et al., 1996; Harris et al., 1996). Furthermore, while there existed some correlation between sediment oiling and mussel contamination within beds, the relationship was far stronger among beds. The similarity in composition of the oil in the sediments, in the mussels, and in "Exxon Valdez" crude, combined with the spatial correlations between oiled sediments and oiled mussels, indicates that the oil was continuing to be released from the sediments to contaminate the overlying mussels (Harris et al., 1996). Because mussels depurate petroleum hydrocarbons relatively rapidly, the contamination must have been ongoing and the oil itself was barely weathered, with a PAH composition in sediments resembling week-old "Exxon Valdez" oil (Harris et al., 1996). Repeated sampling of selected oiled mussel beds from 1992-1995 showed that contamination in both the underlying substratum and the overlying mussels diminished at a slow rate. Only about half the beds exhibited significant declines in hydrocarbon concentration at rates that would reach background levels within about 10 years (Babcock et al., 1997;
EFFECTS OF "EXXON VALDEZ" OIL SPILL
15
Carls et al., 2000). Unfortunately, the spatial patchiness of oil within the mussel beds produced high variance and low power to estimate precise times to reach background concentrations. Because reduction of oil levels was observed to be so slow in several oiled mussel beds in highly protected areas, various novel clean-up technologies were directed towards these problem mussel beds in 1993 and 1994. Trenching within the bed failed to induce reduction in hydrocarbon levels anywhere except in the trench itself. Temporary removal of the mussel layer followed by replacement of underlying sediments with clean sediments and then return of the mussels was effective in a short-term assessment a few weeks after treatment (Babcock et al., 1997). Over longer time periods, this technique may prove ineffective if it fails to reduce the subtidal pools of oil sufficiently to prevent recontamination by horizontal movement of subsurface oil. The ecological significance of intertidal reservoirs of partially weathered oil that continued for several years to contaminate overlying mussels, and presumably other nearby suspension feeders such as clams, may be substantial. The mussel (Mytilus trossulus), and to a slightly lesser degree the littleneck clam (Protothaca staminea (Conrad)), butter clam (Saxidomus giganteus (Deshayes)), cockle ( Clinocardium nuttallii (Conrad)) and razor clam (Siliqua patula (Dixon)), represent what could be termed the "universal prey" of the intertidal ecosystem. The mussels and these clams are among the most important prey resources for many valued mammals, such as brown bears (Ursus arctus L.), black bears (Ursus americanus Pallas), sea otters (Enhydra lutris L.), and humans, ducks such as harlequin (Histrionicus histrionicus (L.)), surf scoter (Melanitta perspicillata (L.)), other scoters (Melanitta spp.), goldeneyes (Bucephala spp.), oldsquaw (Clangula hyemalis L.), and shorebirds, such as black oystercatcher (Haematopus bachmani Audubon), surf bird (Aphriza virgata (Gmelin)), and black turnstone (Arenaria melanocephala (Vigors)) (Vermeer, 1981; G6tmark, 1984; Hood and Zimmerman, 1986; Irons et al., 1986; Marsh, 1986). In addition, the mussels and clams are important prey for many invertebrate consumers, including several species of seastars, whelks, octopus and crabs (Kitching and Ebling, 1967; Dayton, 1971; Menge, 1972; Fotheringham, 1974). Mussels are a prominent component of the diet of several demersal fishes whose juveniles forage in intertidal habitats. Consequently, the contamination of mussels and clams introduced relatively unweathered oil from the "Exxon Valdez" into important intertidal food chains, and this process continued at least until 1993, and even into 1996 where no clean-up was done (Babcock et al., 1997). Boehm et al. (1996) computed estimates (only 2-3%) of the proportion of contaminated mussels in two of the bays containing oiled mussel beds, but such a calculation ignores the tendency of predators to forage preferentially in protected areas and where mussel densities are
16
CHARLES H. PETERSON
high. I discuss below the potential ecological significance of indirect effects produced by contamination of mussels and other invertebrate prey.
3.2. 3.2.1.
Changes in species abundances and community composition of rocky shores Rocky intertidal community organization
The rocky intertidal ecosystem is probably one of the best known natural communities on earth (ConneU, 1972; Underwood and Denley, 1984; Menge, 1995). Marine ecologists realized over 30 years ago that this system is well suited to experimentation because the habitat is accessible and basically two-dimensional, the organisms are easily observed and they can be manipulated. Consequently, we know a lot about the complex of processes and intense interactions involved in determining patterns of distribution and abundance of rocky intertidal organisms (Branch, 1981; Rafaelli and Hawkins, 1996). Plants and animals of temperate rocky shores exhibit strong patterns of vertical zonation in the intertidal zone. Physical stresses tend to limit the upper distributions of species populations and to be more important higher onshore, whereas competition for space and predation tend to limit distributions lower on the shore (Connell, 1961, 1972). Predation by shorebirds like oystercatchers can also serve to limit the upward extension of some intertidal invertebrates (Raffaelli and Hawkins, 1996). Surface space for attachment is potentially limiting to both plants and animals in the rocky intertidal. In the absence of disturbance, space becomes actually limiting and competition for that limited space results in exclusion of inferior competitors and monopolization of space by a competitive dominant (Paine, 1966; Dayton, 1971; Peterson, 1979). Physical disturbance, biological disturbance and recruitment limitation are all processes that can serve to maintain densities below the level at which competitive exclusion occurs (Menge and Sutherland, 1987). Because of the importance of such strong biological interactions in determining the community structure and dynamics in this system, changes in abundance of certain species can produce intense direct and indirect effects on other species that can influence other components of the ecosystem (Paine, 1966; Menge et al., 1994; Wootton, 1994; Menge, 1995). Intertidal communities are open to utilization by consumers from other systems. The great extent and importance of this habitat as a feeding ground for major marine, terrestrial, and aerial predators render the intertidal system a key to integrating understanding of the damages and responses of the entire coastal ecosystem (see papers in Hood and Zimmerman, 1986). The intertidal habitats of Prince William Sound and
EFFECTS OF "EXXON VALDEZ" OIL SPILL
17
the adjacent geographical areas affected by the "Exxon Valdez" oil spill are critically important feeding grounds for many important mobile consumer species. There are fully marine forms, such as sea otters, juvenile Dungeness (Cancer magister Dana) and other crabs, juvenile shrimps (Pandalus spp.), rockfishes (Sebastes spp.), cod (Gadus macrocephalus Tilesius), cut-throat trout (Oncorhynchus clarki (Richardson)), Dolly Varden char (Salvelinus malma (Walbaum)) and juvenile fishes of other stocks that are exploited commercially, recreationally, and for subsistence, including pink salmon (Oncorhynchus gorbuscha Walbaum). Terrestrial forms include brown bears, black bears, river otters (Lutra canadensis Schreber), Sitka black-tailed deer (Odocoileus hemionus sitkensis (Meriam)), and humans. Avian species include the black oystercatcher and other shorebirds, several gulls (Larus spp.), harlequin duck, surf scoter (Melanitta perspecillata), goldeneyes, other ducks, and the bald eagle (Haliaeetus leucocephalus (L.)). Thus, the intertidal habitat provides vital ecosystem services in the form of prey resources for all coastal habitats, as well as commercial, and subsistence harvesting of shellfishes and aesthetic, cultural, and recreational opportunities. 3.2.2. Impacts of the oil spill on rocky intertidal biota The studies by the Hazardous Materials Response and Assessment Division of NOAA (Hazmat) and initial Exxon-sponsored studies of short-term (3-10 days) impacts of the beach treatments done to displace oil from intertidal shores demonstrated very high rates of mortality of both plants and animals from application of high-pressure hot-water washing (Table 3; see also Figure 2). This treatment was applied over a large fraction of the oiled shoreline in wave-protected habitats (Houghton et al., 1996b; Lees et al., 1996). Injury included high mortality of the brown alga Fucus gardneri Silva and the mussels, two of the functionally most important organisms of the local intertidal community. The Fucus provides habitat and the mussel is both habitat provider and prey. Other shoreline treatments, including chemical applications (Table 3), had smaller impacts (Lees et al., 1996). These observations of the treatment processes can be taken together with the results of experimental testing of the short-term impacts to help interpret the data on long-term consequences of the spill. This is particularly useful for the assessments of rocky shore community composition in Prince William Sound done by NOAA Hazmat over several years following the spill (Houghton et al., 1996a, b, 1997a, b; Coats et al., 1999). By categorizing sites as either unoiled, oiled and treated, or oiled and untreated, the NOAA study provided the only means of separating effects of oiling from those of shoreline treatment, which are confounded on most
,~°
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19
EFFECTS OF " E X X O N VALDEZ" OIL SPILL
percent
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Figure 3 Mean percent cover (-+SE) of Fucus gardneri in mid-intertidal stations observed by the NOAA Hazmat study from 1989-96, comparing unoiled, oiled and oiled and washed sites (after Houghton et al., 1997b).
protected shores in all other data sets. The Hazmat study revealed that shoreline treatment caused greater reductions in abundance and cover of intertidal plants and animals than the oil alone and delayed the pace of recovery relative to untreated shores (Houghton et al., 1996b, 1997a). By July 1991, epibiotic communities on oiled but untreated rocky shores were essentially indistinguishable from unoiled, control shores, whereas some oiled and treated shores continued to exhibit differences into summer 1995. Even those oiled and treated shores that had converged in community composition with control shores by 1992 revealed massive mortality of Fucus gardneri in 1994 and 1995 (Paine et al., 1996; Houghton et al., 1997b: Figure 3). This long-term cycle of changes in cover of Fucus on oiled and treated shores has been interpreted as a possible consequence of the induction of an almost single-aged stand of Fucus on oiled shores by the extensive denuding of the shore, such that natural senility and longevity constraints then affected virtually the entire local population simultaneously (Paine et al., 1996; Houghton et al., 1997b). The control shorelines with mixed age distributions of Fucus did not exhibit such cyclic instability because not all individuals were senescing in synchrony. Such cycles could persist for many more years before becoming damped by gradual attainment of broader age distributions. Long-term
20
CHARLES H. PETERSON
studies of the shoreline communities after the "Torrey Canyon" oil spill in Cornwall likewise demonstrated cyclic damping of re-colonization by Fucus, limpets and barnacles. These cycles were driven by intense biological interactions and delayed full recovery for 10-15 years (Southward and Southward, 1978; Hawkins and Hartnoll, 1983; Hawkins and Southward, 1992). The other major studies (by the government-funded scientists: Highsmith et al., 1996; and by Exxon: GilfiUan et al., 1995a, b) of oil spill response and recovery of intertidal epibiota of rocky shores evaluated the joint and confounded effects of the oil plus the shoreline treatment. These studies are characterized broadly by their tremendous geographical scope (covering not only most of Prince William Sound but also the Kenai Peninsula-Cook Inlet region and the Kodiak archipelago-Alaska Peninsula region: see Figure 1) and their coverage of multiple geomorphologic habitats. They also include some major inconsistencies, which can be best understood as the results of differing methodologies that reduced the statistical power and general ability of the Exxon-funded studies to detect many large effects of the oil spill (Peterson et al., 2000). Consequently, this review of impacts to the rocky shore biota will draw most heavily from the government-sponsored studies. All of the studies of shoreline habitats and resources lacked pre-spill information and used contrasts of oiled to unoiled segments of shoreline to assess effects of the spill. Such contrasts run the risk of confounding natural pre-existing differences with spill-induced differences because they lack the before-after control-impact design (BACI) that allows isolation of impacts (Stewart-Oaten et al., 1986). This design limitation injects some additional uncertainty in the conclusions. The most viable practical means of isolating pre-existing spatial differences from spill impacts under these conditions is to follow recovery until natural pre-existing differences can be assumed to have been restored, thereby allowing adjustment of estimates of injury. In some cases (Jewett et al. 1999), such convergence of species abundances on oiled and unoiled shores did take place, allowing the degree of natural site variability to be estimated. For the governmentsupported studies of intertidal and shallow subtidal shores, the most likely bias is the failure of the oil to beach at random in relation to exposure to current flow regime (Laur and Haldorson, 1996; Highsmith et al., 1997). The oiled shores tended to be those exposed to greater current flux (and thus greater risk of oil exposure). This has the effect of making most estimates of injury conservative in that higher flows imply greater larval delivery, greater recruitment and higher growth rates, processes that would tend to make these oiled shorelines naturally more productive. Higher flows at oiled shores would also help enhance rates of recovery after the spill.
EFFECTS OF "EXXON VALDEZ" OIL SPILL
21
The field assessments of impacts on the intertidal biota of rocky shores were grouped by geographic area (Prince William Sound vs. Gulf of Alaska or vs. Kenai Peninsula-lower Cook Inlet and vs. Kodiak archipelagoAlaska Peninsula), by geomorphological habitat, and by elevation on shore. Because oil quantity and quality varied among strata, because removal rate of oil varied, and because biota varied among strata, the impacts of the oiling and subsequent shoreline treatment differed among combinations of these strata in complex ways that make overall generalization difficult. Nevertheless, the major responses of the biota follow certain patterns. Every stratum experienced some detectable impact of the oil spill, meaning that the geography of impact was extremely wide-ranging, that no habitat type enjoyed immunity from spill effects, and that all levels on shore showed some degree of response. Stekoll et al. (1996) made comparisons using a simple measure of the percentage of all individual species tested that showed significant responses to the oil spill. About 12-15% of tests showed significance, pooling results across all three geographic regions, but Prince William Sound and Kodiak-Alaska Peninsula differed from Kenai-lower Cook Inlet by exhibiting more dominantly negative changes (reductions) in density. The percentage of species tests showing significance did not vary much among habitats, with about 11-17% of tests showing significance, of which about two-thirds represent reduced densities at oiled sites. The magnitudes of responses (Highsmith et al., 1996) imply some differences among habitats, with estuarine habitats responding with the largest declines and wave-exposed rocky shores with the generally smallest declines. There was not a large difference among the three vertical elevations examined, with a range of 12-17% of species tests showing significant responses to the oil spill. The highest percentage occurred at the mid-tide level (the second meter of vertical drop) and the lowest at the lowest tidal level (the third meter of drop). Changes at the high and mid elevations tended to represent abundance declines more often than at the lowest elevation. There were many differences in the way the oil spill influenced rocky intertidal biota, depending on geographic areas, habitats, tide levels, and sampling dates (Highsmith et al., 1996; Stekoll et al., 1996). However, some general patterns emerged that allow a characterization of the typical changes in abundance or cover of dominant species and in community composition (Figure 4). Not only have direct acute effects of oiling and treatment been documented but also indirect and chronic delayed effects (Table 4). Cover, abundance and biomass of the F u c u s were generally reduced greatly at oiled sites (Highsmith et al., 1996; Houghton et al., 1996b; Stekoll et al., 1996; van Tamelen et al., 1997). This is consistent with the massive short-term F u c u s mortality following pressurized hot-water
22
CHARLES H. PETERSON Balanus glandula MVD 1
FUCUS MVD 1 no. 0-1 30
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Bare rock MVD 1 lOO
.
.
.
.
.
.
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1990
1991
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.
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Figure 4 Mean percent cover of the most common algae and marine invertebrates and also bare rock surfaces on sheltered rocky shores in the Prince William Sound, from the Coastal Habitat Injury Assessment study conducted for the "Exxon Valdez" Oil Spill Trustee Council. Data are stratified by level on shore, with meter vertical drop (MVD) indicated as 1-3 on each graph. Stars (* P
o o
40, 20 0
[ ] red algae • Fucus >
0 o
1990
1991
1992
July
Figure 5 Algal cover of rock surfaces in the lower intertidal as a function of oiling and treatment history. Plots illustrate the expansion of Fucus gardneri on shores that were oiled and treated by pressurized hot water and the consequent pre-emption of space that prevented rapid recovery of the red algae typical of that level. Data are taken from the NOAA Hazmat study of Prince William Sound (Houghton et al., 1997a) and represent means of all sheltered rocky sites studied. like Nucella lamellosa (Gmelin) (Ebert and Lees, 1996), which can control barnacle densities, must have enhanced survival of juvenile and adult barnacles. Thus, the sequence of recovery of barnacles before limpets reversed the pattern seen following the "Torrey Canyon" spill (Southward and Southward, 1978). However, on shores affected by the "Torrey C a n y o n " clean-up there was a later decline of limpets when the adult population became too large for the algal resources, and this opened up an opportunity for dense barnacle settlement. The grazing periwinkle Littorina sitkana Philippi generally exhibited higher abundances on unoiled reference shores, although the opposite pattern often prevailed
28
CHARLES H. PETERSON
in the coarse-textured habitat in the Kenai-lower Cook Inlet region (Highsmith et al., 1996). A congener, Littorina scutulata Gould, exhibited many significant responses to the oil spill, but the direction of the effect on its abundance was not consistent (Highsmith et al., 1996). Littorina scutulata produces planktonic larvae, whereas Littorina sitkana is a direct developer producing live crawl-away young. The lack of a consistent pattern of depression in density of Littorina scutulata on oiled shores in 1990 and 1991 may reflect its ability to re-colonize from the planktonic larvae (Highsmith et al., 1996), thus providing good recovery. Analogous early recolonization of littorinids from planktonic larvae occurred on the Cornish coast after the "Torrey Canyon" spill, where species with direct development were much slower to recover (Southward and Southward, 1978). Many of the observed differences in invertebrate abundance narrowed with time from spring 1990 to summer 1991, implying ongoing recovery (Highsmith et al., 1996). The predatory invertebrates of the rocky intertidal zone were not abundant enough in the random samples of this system to allow reliable testing for oil spill effects. Ebert and Lees (1996) did, however, show that the Nucella lamellosa disappeared in markrecapture studies carried out from 1991 to 1992 at higher rates on oiled than on unoiled shores and grew at lower rates on those oiled shores. The higher disappearance rate indicates either higher residual mortality or greater emigration, either cause operating even 2-3 years after the spill. The mechanisms by which the invertebrates of the rocky intertidal shores were affected by the oil spill are not clearly distinguishable. Judging from the short-term demonstrations of mortality of many invertebrates from pressurized hot-water treatments (Houghton et al., 1996b; Lees et al., 1996), much of the immediate loss of animals was probably a consequence of invasive shoreline treatment. Toxicity may have played a role, along with the physical effects of smothering under a layer of oil. However, indirect effects may also have been involved. Experimental removal of the Fucus canopy in Herring Bay on Knight Island was followed by declines in abundance of several rocky shore invertebrates, including the limpet Tectura persona and the periwinkle Littorina sitkana (Highsmith et al., 1997). The fucoid alga evidently provides protection against desiccation and detection by predators. To the degree that such effects of habitat loss determined the abundance of rocky shore invertebrates, recovery of those animals was also delayed by the slow return of the Fucus. This process was demonstrated through experiment by Highsmith et al. (1996) as it affected the limpets and periwinkles that live under and around the Fucus canopy. However, no evaluation was attempted of effects on small mobile crustaceans that also use macroalgae as critical habitat and which are themselves of such value to foraging fishes. Nevertheless, large reductions
EFFECTS OF "EXXON VALDEZ" OIL SPILL
29
in Fucus-associated crustaceans, analogous to the declines in gammarid amphipods and the isopods Idotea spp. and Jaera spp. that followed the "Irini" crude oil spill in Sweden (Notini, 1978), may have occurred after the "Exxon Valdez". Loss of Mytilus also represents a depression in available biogenic habitat that may have affected small invertebrates that live among the byssus threads (Suchanek, 1985), but no study evaluated that possible indirect response. The recovery of Fucus was itself inhibited by an indirect effect involving massive settlement of Chthamalus dalli barnacles (van Tamelen and Stekoll, 1996b). Many Fucus recruits attached to Chthamalus barnacle tests instead of to bare rock or balanoid barnacle tests. Through wave action, those attached to barnacle tests were readily dislodged before the plants could reach maturity (van Tamelen et al., 1997). This loss of Fucus recruits was a consequence of the instability of the substratum to which they were attached, an instability likely to have been enhanced by the substitution of chthamaloid barnacles for Balanus glandula. Chthamalus attaches with a membranous base instead of the more durable calcium carbonate basis secreted by Balanus glandula. Hawkins et al. (1992) describe an analogous instability created for fucoid algae attaching to tests of Semibalanus balanoides, which also has a membranous base.
3.2.3.
Impacts of the oil spill on intertidal biota of sedimentary environments
The oiling of intertidal beaches altered the microbial community in the sediments. Total counts of bacteria per unit weight of sediment were not significantly affected, but counts of hydrocarbon-degrading bacteria were definitely enhanced at two oiled beaches when compared with two control shores (Braddock et al., 1996). The application of fertilizers (bioremediation) in water-soluble form (CUSTOMBLEN) and in oleophilic form (INIPOL) stimulated counts of hydrocarbon-degrading bacteria and increased hexadecane and phenanthrene mineralization potential (Lindstrom et al., 1991). The importance to higher trophic levels of this increase of microbial hydrocarbon degraders was not well established by the field studies. Coffin et al. (1997) used isotope ratios to trace the fate of carbon and nitrogen from the bioremediation fertilizers. They were able to show uptake by bacteria in microcosm experiments but no clear isotopic signal in fieldcollected bacteria at one site in summer 1990 and no isotopic evidence of transfer to higher trophic levels. However, the barnacles, limpets and whelks examined by these workers are not the most likely primary consumers of sediment microbes. They are rocky shore species with diets
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ooo 3 million tonnes in 1996, and for this reason synoptic information might provide insights into these ecological changes in the world's oceans. Analysis of global fisheries generally relies on statistics collected by national governments and reported to FAO. These data are low resolution and there is delay before they become available for scientific use. Given the global nature of change in fisheries there is a need for methods analogous to satellite remote sensing of land use in agriculture for marine systems. Cephalopod fisheries provide such an opportunity. Many of these fisheries are pursued by concentrating the target species with powerful incandescent lights. Large fleets of vessels, mostly from east Asia, operate using lights in various parts of the world's oceans. The recent availability of archived data from the United States Defence Meteorological Satellite Program (DMSP) Operational Linescan System (OLS) provides a novel means of monitoring the activities of whole fleets of light-fishing vessels in near real time (Cho et al., 1999). The OLS has the unique capability to detect low levels of visible and near infra-red radiance at night. Elvidge et al. (1997a, b) have developed algorithms to identify and geolocate VNIR emission sources in night time imagery and have compiled an inventory of light sources present at the Earth's surface. The OLS sensor is an oscillating scan radiometer designed for cloud imaging with a swath width of about 3000 km. The sensor has two spectral bands: the VIS band spans the visible and very near-infrared (VNIR) part of the spectrum (0.5 to 0.9/~m) and the thermal band (10.5 to 12.6/zm). DMSP platforms are stabilized using four gyroscopes providing three axis stabilization. Orientation is adjusted using a star mapper, an earth limb sensor and a solar detector. The wide swath allows global coverage four times per day at dawn, day, dusk and night. Satellites F-10 to F-14 overpass at - 2 0 : 3 0 to 21:30 local time. The sensors measure radiance in the VIS band down to 10-9W cm-2sr -1/~m -1, which is more
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P.G. RODHOUSE, C. D. ELVIDGE AND R N. TRATHAN
than four orders of magnitude more sensitive than the VNIR bands of other sensors used for oceanographic applications such as the NOAA AVHRR. Originally collected for military use, DMSP data were declassified in 1972 but they have only been archived in digital form since 1992 at the NOAA National Geophysical Data Center. Light-fishing vessels are mostly jiggers which catch squid with jigs (lures armed with an array of barbless hooks) and fished in series on lines using automatic machines (Suzuki, 1990) (Plate la). Squid are attracted to the jigs with an array of metal halide, incandescent lights (Plate lb). Small artisanal vessels may deploy a single lamp. Large, industrial vessels operate offshore and use an average of about 150 lamps. Typical lamps are 2 kW but they range from 1-3 kW. The lamps are usually white with a small number of green lamps interspersed (Inada and Ogura, 1988). The principal lamps are suspended above water but on industrial vessels two additional underwater lamps are sometimes used. These are 2-5 kW each, depending on whether they are green or white. A typical east Asian "far seas" squid jigger of 70 m overall length operating in the southwest Atlantic would operate 150 lamps giving a total light power of 300 kW. It would also operate 110 jig lines carrying 25 jigs per line (total 2750 jigs) and would expect to catch 25-30 t of squid (exceptionally 100 t) per night with a crew of 20 persons. Experiments using sonar to detect squid attracted to fishing lamps have shown that in water of optical type "oceanic III" (Jerlov, 1964) squid (Todarodes pacificus) are concentrated in a depth layer between 30 and 70 m in spectral irradiance levels (at 510 nm) of 1.8 × 10 -2 to 5.4 × 10 -5/xWcm-2nm -1 (Arakawa et al., 1998). Combining DMSP-OLS images of the global distribution of light fishing with other spatial data, using a marine Geographical Information System (GIS) developed at The British Antarctic Survey (BAS) (Trathan et al., 1993), enabled the formulation here of a detailed description of the geographical extent of the global light fishery and interpretation of the relationship of the species they are targeting, with the bathymetry and physical and biological oceanography of the regions where they operate. An assessment of the extent of interaction between the stocks of squid exploited by these light fisheries and the groundfish stocks of the continental shelves in their vicinity is presented. Interactions between the target species of the fisheries and higher predators are also examined. The spatial resolution provided by the DMSP-OLS data on the global squid fisheries facilitates relating their distribution to specific ecological provinces (Longhurst, 1998) rather than to the much larger-scale, and less ecologically meaningful, FAO statistical areas. Longhurst (1998) provides a scheme based on physical oceanography and the seasonal response of planktonic algae to seasonal forcing by physical processes as determined from remotely sensed ocean colour data. FAO data are the only global
REMOTE SENSING OF LIGHT FISHING
265
data on fisheries production; they were used for the analysis of global cephalopod fisheries by Caddy and Rodhouse (1998) and are used in this review for comparison of global catches with the distribution of lightfishing fleets (see FAO Yearbook, 1996b which covers the period 19871996).
.
2.1.
DESCRIPTION AND INTERPRETATION OF THE GLOBAL CEPHALOPOD LIGHT FISHERIES IMAGED WITH THE DMSP OLS: INTERACTIONS WITH OCEANOGRAPHY DMSP-OLS images
The images presented here illustrate the geographical distribution of fishing lights over the 6 month period between October 1994 and March 1995 as detected in cloud-free conditions during the dark half of each lunar cycle (see Appendix). They show where lights have been detected at least once during that period. Where fishing fleets shifted their location during that time the same lights will appear in different places on several occasions. On the other hand the images provide a conservative estimate of area fished with light during the period because there may have been areas that were exploited by the fleet during periods of cloud cover that are not included. The images thus quantify the minimum area exploited by light-fishing vessels between October 1994 and March 1995, but cannot be used to quantify fishing effort. Squid fishers generally expect better catch rates during overcast weather and during the dark part of the lunar cycle (PGR, personal observation). The far seas fleets of large vessels from East Asia continue fishing in all conditions of cloud and moonlight but it is possible that small inshore vessels may vary effort according to the prevailing conditions. Because the composite images are based on cloud-free images from satellite passes during the dark half of the lunar cycle it is expected that the coverage of small inshore vessels might be biased. However, the argument still holds that the images provide a conservative estimate of the geographical area fished with light. 2.1.1.
Kuroshio Current
In the waters of the Kuroshio Current and seas to the northeast of Taiwan, fishing lights are more numerous and denser than anywhere else in the world's oceans. They are clearly visible in the Tsushima Strait between the Korean Peninsula and Japan, throughout the southern part of the Sea of
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P.G. RODHOUSE, C. D. ELVIDGE AND R N. TRATHAN
Table 1 Squid catch identified to genera or species in seven ecological provinces where DMSP-OLS imagery reveals light-fishing activity.
Province Kuroshio Current China Sea Shelf Sunda-Arafura Shelves New Zealand California Current Humboldt Current Southwest Atlantic
FAO statistical area(s) in which Province lies 61
Species
Todarodes pacificus Ommastrephes bartrami 61 Loligo spp. (L. chinensis + others) 57 and 71 Loligo spp. 81 Nototodarus sloanii N. gouldi 77 Loligo opalescens 87 Dosidicus g i g a s 41 lllex argentinus Martialia hyadesi Loligo gahi
Catch (103 t.y -1)
% of world squid catch in 1996
1228--716(1987/96) 4248-378(1985/90)
29 5-3
117-24 (1987/96)
**-1
q37-195 (1987/96) ~29-83 (1987/96) 31-39 (1979-93) 278 (1977) 10.3-195(1987/96) 1157-401(1987/96) 10.2-24(1987/96) 144--89 (1987/96)
**7 2 -1 3 6 17