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Advances in Marine Biology 39 PDF

324 Pages·2001·19.69 MB·English
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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 crus- taceans, 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. X 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,S chool 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 Char l es H. P e t e r s o n University o f North Carolina at Chapel Hill, Institute of Marine Sciences, Morehead City, North Carolina 28557, USA FAX." 252-726-2426 e-mail: 2 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, how- ever, many subtidal infaunal invertebrates increased in abundance, espe- cially 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, i f sustained, could lead to additional indirect effects of the spill. Scavenging terrestrial birds, such as bald eagles and northwes- tern 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 sen- sitivity 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 abun- dance 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 o f adult harlequin ducks continued in 1995-96, 1996-97 and 1997-98. Delays in the recovery o f avian and mammalian predators o f 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 expendi- tures 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 ecologi- cal 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 4 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 informa- tion 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 taxonomi- cally 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 com- mences 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 ecosys- tem. 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 6 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 fish- ing 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 oppor- tunities, 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. Approxi- mately 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 Peninsula- lower 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 Depart- ment 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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