Advances in Marine Biology 39

324 Pages·2001·19.69 MB·English

by  Alan J. Southward, Paul A. Tyler, Craig M. Young

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)