A Review of Marine Major Ecological Disturbances.

Abstract

The apparent increase in marine morbidity and mass mortality events, the emergence of new diseases across a range of taxa, increases in harmful algal blooms, and the longterm and often unexplained declines of various wildlife populations have heightened concern and debate over human impacts on the marine environment. Resolving the relative extent to which natural and anthropogenic factors drive marine major disturbance events is becoming increasingly important as public health, economic activity, and biodiversity are threatened along various coastal regions. Understanding environmental change within the context of highly complex systems has proven to be difficult, and thus increased scientific focus on large-scale marine disturbances along with more precautionary approaches in managing human activity are warranted.

Concern has mounted over the last 15 to 20 years over what appears to be an increase in the number and scale of disturbances affecting marine species and populations (Harvell et al. 1999; Williams and Bunkley-Williams 2000). The term "marine major ecological disturbance," or MMED, has been coined (Williams and Bunkley-Williams 1990) to loosely describe events occurring over at least a regional scale, are the result of multiple factors, and are characterized by an unusual increase in a syndrome or disease, or in mortality rates. In this brief, we also consider emerging diseases and unprecedented (and often unexplained) population declines as major disturbances. Algal blooms, though natural phenomena, are also included because of the recent increase in their frequency, intensity and geographic distribution and, hence, their growing role in marine morbidity and mortality events.

Marine-based mass mortalities--notably of fish and invertebrates--are not without precedent and have been commonly noted and recorded in the past. Brongersma-Sanders (1957) compiled an exhaustive review of marine wildlife "catastrophes" and categorized the causes as vulcanism (volcanic activity), tectonic earth- and seaquake, change in salinity, temperature change, noxious waterbloom, lack of oxygen, and by poisonous gases, severe storms, as connected with spawning runs, by stranding, or uncertain. The impacts of marine disturbances can be profound. Populations of plant and animal species can be substantially reduced across large geographic regions, and there can be collateral and extended effects on other species and surrounding environments. During the early 1930s, a "wasting disease" caused by a pathogenic strain of slimemold (Labyrinthula spp.) virtually exterminated eelgrass (Zostera marina) throughout its north Atlantic range (Short et al. 1987) and resulted in the extinction of the eelgrass limpet (Lottia alveus alveus) (Carlton 1993), a 75 to 90 percent decline in dark-bellied brent geese (Branta bernicla bernicla), and as much as a 90 percent decline in Atlantic brant (B. b. hrota) (Ganter 2000). Long-spined sea urchin (Diadema antillarum) were virtually eliminated (approximately 95 percent mortality) throughout much of the Caribbean during 1983 and 1984 (Lessios 1988) in what was the most extensive disease event ever recorded for a marine invertebrate. Thick mats of macroalgae overgrew many reefs in the absence of the grazing sea urchins though other factors, natural and anthropogenic, have combined to cause the decline of Caribbean coral reefs over the last decades (Hughes and Connell 1999).

Recent mass mortality episodes involving Mediterranean monk seals (Monachus monachus) and Hooker sea lions (Phocarctos hookeri) highlight the potential impact of MMEDs on endangered species. This would suggest a significant vulnerability to various marine species in the U.S. such as the north Atlantic right whale (Eubalaena glacialis), the Hawaiian monk seal (Monachus schauinslandi) and the Florida manatee (Trichechus manatus latirostris), all of which are still impacted by human activity (Marine Mammal Commission 2000a). On the other hand, Fiori and Cazzaniga (1999) consider that the yellow clam (Mesodesma mactroides) had become a threatened species under IUCN criteria following mysterious mass mortalities across its entire range (southern Brazil to the Negro River in Argentina). In the U.S., disturbances in the Bering Sea/Alaska region have recently prompted ESA listing, or petitions, for four species. Unique environments may also be threatened: Williams et al. (1999) have predicted the disappearance of Atlantic coral cay ramparts, structural habitat formed in large part by elkhorn coral (A. palmata) rubble. They hypothesize that the large reduction in elkhorn coral by major disturbances--disease and bleaching--are reducing the material required for rampart replenishment and thus making existing structures highly susceptible to storm action.

However, while north Atlantic eelgrass recovery has been slow, and it is unlikely that sea urchins will ever rebound to past abundances in the Caribbean, many mass mortality events are ephemeral. Herring (Clupea harengus) populations in the Gulf of St. Lawrence recover quickly after severe epizootics involving the fungus Ichthyophonus hoferi, an event that occurs at roughly quarter century intervals (Sindermann 1958). Fish and benthic communities suffering massive mortalities during an unprecedented Chrysochromulina polylepis bloom covering approximately 75,000 [km.sup.2] of Scandinavian waters in 1988, were found to have generally recovered within five years (Gjosaeter et al. 2000).

A variety of events have underlined the perception that MMEDs have increased over recent years. Some of the more significant of these include:

Marine mammal mass mortalities Morbilliviruses have emerged as an important factor in marine mammal epizootics and were implicated in mass mortalities involving bottlenose dolphins (Tursiops truncatus) along the U.S. Atlantic coast (1987 to 1988) and Gulf of Mexico (1993 to 1994), harbor seals (Phoca vitulina) in the North Sea (1988), striped dolphins (Stenella coeruleoalba) in the Mediterranean Sea (1990 to 1992) and common dolphins (Delphinus delphis) in the Black Sea (1994) (Birkun et al. 1999; Geraci et al. 1999; Lipscomb et al. 1994; Taubenberger et al. 1996).

Over the same period, algal toxins have also been increasingly correlated with mortalities. Geraci et al. (1989) considered saxitoxin vectored by mackerel (Scomber scombrus) as the cause of 14 humpback whale (Megaptera novaeangliae) mortalities in the Cape Cod Bay area during late 1988 and early 1989. A die-off of highly endangered Mediterranean monk seals in 1997 off the western Sahara coast, which reduced that population by over 50 percent, was also attributed to saxitoxin (Costas and Lopez-Rodas 1998) though this is controversial; others (e.g., van de Bildt et al. 1999) have emphasized a morbillivirus as the cause (though see Harwood (1998) for a multifactorial explanation). Brevetoxin, produced by the dinoflagellate Gymnodinium breve, killed approximately 150 Florida manatee, another endangered species, in 1996 (Bossart et al 1998), and was likely the cause for a smaller die-off in 1982 (O'Shea et al. 1991). G. breve blooms have also been associated with recent bottlenose dolphin mortalities in the Gulf of Mexico (Marine Mammal Commission 2000 in prep) though given the frequent overlap of living dolphins and red tides in this region it remains perplexing why so few mortality events are reported. In 1998, domoic acid associated with a bloom of the diatom Pseudonitzschia australis killed over 400 California sea lions (Zalophus californianus) along the central California coast over a short period in 1998 (Scholin et al. 2000). High numbers of sea lion strandings during the latter half of 2000, and in the same general region, appear also to have been domoic acid related (Marine Mammal Commission in prep).

At least 1,600 Hooker sea lions perished in a mysterious mass mortality event in the Aukland Islands during early 1998 (MUCIC 1998); this species' range and abundance is vastly reduced from historical times and numbered some 12,500 animals prior to the event (Gales and Fletcher 1999). Two separate mortality events involving a number of marine mammal species occured during the early 1990s in the Gulf of California; algal toxins were deemed the likely cause (Ochoa et al. 1997) but no supporting information was made available. In addition, gray whales (Eschrichtius robustus) have succumbed in high numbers along their migratory route from Mexico to Alaska during both 1999 and 2000; 273 and 355 animals were found respectively (Marine Mammal Commission in prep). During the previous ten years, the highest number of strandings reported for any one year was 87. Le Boeuf et al. (2000) have argued that malnourishment was the likely factor based on the discovery of a number of emaciated animals and have postulated that this could have been due to climate-related declines of their principal prey of benthic amphipods or to the whales having surpassed their carrying capacity. This conclusion, however, may be premature as many of the other stranded animals were reported as appearing in good nutritional condition (Marine Mammal Commission in prep).

Coral disturbances

It has been well documented (Jameson et al 1995) that many of the world's tropical coral reefs have been in decline or have been destroyed over the last decades--typically the result of fisheries, land-use changes increasing sedimentation, and nutrient pollution. While these are considered the most important and immediate threats to reefs, coral bleaching and disease have emerged as large-scale disturbances that would seem to portend an acceleration of coral decline.

Coral bleaching, which results from the loss of the endosymbiotic algae that reside in the cells of the coral host, is a generalized stress response and if prolonged will lead to a decrease in growth and reproduction; extended bleaching will eventually result in the death of entire colonies (Glynn 1996). Prior to the 1980s, bleaching other than on local scales appears to have been extremely rare. Since then the frequency of bleaching has increased substantially (Williams and Bunkley-Williams 1990) with impacts having expanded to regional and global scales. Six bleaching events affecting corals worldwide have occurred since 1980, with the 1998 mass bleaching event considered the most extensive and severe on record (Hoegh-Guldberg 2000). An estimated 16 percent of global coral was killed with highest mortalities occurring in the Middle East and wider Indian Ocean (Wilkinson 2000). 1998 was also characterized by the highest sea surface temperatures ever recorded (Hansen et al. 1999). It is now considered (e.g., ISRS 1998) that the most probable cause of the overall bleaching increase has been the rise of global temperature and associated meteorological extremes.

Increases in reports of coral diseases, including potential disease states and syndromes, generally parallel the rise of bleaching events though any causal connections between the two are obscure. The first three diseases to be reported in coral--black and white band disease and white plague--were not described until the 1970s (Richardson 1998), and highly destructive effects were only first noted during the early 1980s with the recognition that structurally-important acroporid corals were being eliminated by white band disease throughout areas of the Caribbean (Gladfelter 1982). Twenty-six additional "diseases" have been reported in the literature since then (Green and Bruckner 2000) though not without some confusion: different names may have been given to different stages of the same disease; and it is unclear in many cases that what has been described is actually a disease (Hayes and Goreau 1998; Richardson 1998).

A soil fungus, Aspergillus sydowii, however, was clearly determined as the pathogen behind a major epizootic involving sea fan corals which has been ongoing throughout the Caribbean since the mid-1990s (Geiser et al. 1998)--and similar disease symptoms suggest that it was the likely factor in mass mortalities of the species during the early 1980s. A. sydowii spores have been isolated from dust atmospherically transported from Africa and were successfully innoculated in healthy sea fans (Weir et al. 2000 as cited in Shinn et al. 2000); the "dust hypothesis" has now been added to the large number of potential factors involved in the gradual demise of Caribbean reefs (Shinn et al. 2000). The unprecedented nature of some recent coral disturbance events has been demonstrated in cores extracted from Belizean reefs: two recent mass mortality events--involving staghorn coral (Acropora cervicornis) and white band disease in the late 1980s, and lettuce coral (Agaricia tenuifolia) during the 1998 bleaching complex--have had no historical equivalent there in a record extending back 3,000 years (Aronson et al. 2000).

Harmful algal blooms

Numerous recent reports and reviews (e.g., Morand et al. 1996; Smayda, 1990) have provided compelling evidence for an increase in the frequency, intensity, duration, and geographic distribution of seaweed and phytoplankton blooms, and toxicity events. Previously benign or unknown species have emerged as problematic (Burkholder et al. 1992; Ito et al. 2000; Todd 1993) and there has been a concomitant increase in reports of associated disruptions on flora and fauna, human health, tourism, aquaculture, and on recreational and commercial fisheries (Burkholder 1998; Van Dolah 2000). Yet the magnitude of human influence still remains largely unclear and increased reporting of such events would be expected given rapidly growing coastal populations and increased human exposure (e.g., via shellfish consumption), and the considerable expansion in surveillance programs and scientific attention. Likewise, the explosive growth in coastal finfish aquaculture may have promoted localized blooms by nutrient enrichment or by providing visible targets for bloom effects, or both. Definitively quantifying any increase is further prevented by the absence of data sets long enough to factor out cyclical fluxes and climate variability. The balance of evidence, nonetheless, suggests that human influence via nutrient enrichment and eutrophication, alteration of nutrient ratios, and by shipping- and aquaculture-mediated introductions has been a critical factor.

Sea turtle fibropapilloma disease

Though originally described in the late 1930s in green sea turtles (Chelonia mydas) in the Florida Keys, the conspicuous external tumors associated with fibropapilloma disease were anecdotally noted in this species in Florida around 1900 (Jacobson et al. 1991), and noticed for the first time in Hawaii in 1958 (Balazs 1991). It appears to have been quite rare until the late 1970s before its expansion into epizootic proportions in green turtles at multiple sites in those two states--in 52 percent (70 out of 134) of strandings in the Florida Keys between 1983 and 1989 (Jacobson et al. 1991), a prevalence of 72.5 percent (121 out of 167); in the Indian River Lagoon in 1998 (Lackovich et al. 1999); and a prevalence of 44.9 percent (n=581) from a capture and tagging program in Kaneohe Bay in Hawaii between 1989 and 1997 (Balazs et al. in press). Other areas, even with minimal geographic separation from affected populations, have remained virtually free of the disease. Since 1985 fibropapillomas have been reported in green turtles from Australia (Limpus & Miller 1994) and from fourteen Caribbean countries (Williams et al. 1994), with a considerable increase in Puerto Rico and Columbia. The disease appears to have recently emerged in loggerhead turtles (Caretta caretta) with prevalences of up to 11 percent in Florida Bay (Landsberg et al. 1999), and has been reported in prevalences of 1 to 10 percent in the large population of olive ridley turtles (Lepidochelys olivacea) nesting at Ostional on the Pacific coast of Costa Rica (Aguirre et al 1999).

Sea turtle fibropapilloma disease can severely debilitate afflicted animals causing stranding and death, though in some cases tumors remain minimal or can regress (Herbst 1994). A herpes virus and retrovirus have been identified in association with the disease (Casey et al. 1997; Herbst 1994) but the primary cause and modes of transmission are unknown. Landsberg et al. (1999) have suggested the possible role of okadaic acid, a tumor promoter associated with the toxic benthic dinoflagellates Prorocentrum spp., and epiphytic on forage plants.

Disturbances in U.S. coastal waters

The Health Ecological and Economic Dimensions (HEED) of Global Change Program, in a review of marine disturbances from the U.S. Atlantic and Gulf coasts and the Caribbean (1945 to 1996), concluded that anomalous morbidity and mortality events had increased since the early 1970s (Epstein et al. 1998; Sherman 2000). Recent events in Florida coastal waters (Table 1) are representative of the range and types of disturbances currently being reported for the wider Caribbean (see Williams et al. 2000), and suggest a larger regional phenomena. The increase in coral disease and reef decline has been particularly noticeable. In extensive surveys (160 monitoring stations) throughout the Florida Keys, Porter et al. (1999) and Jaap et al. (2000) documented increases in areas with disease (from 26 stations in 1996 to 131 in 1998) and in numbers of species affected (from 11 species in 1996 to 31 in 1998). Furthermore, 67 percent of the monitoring stations lost species between 1996 and 2000, and stony coral cover decreased by about 40 percent between 1996 and 1999. Some 75 percent of all Florida Key coral species now present disease symptoms but the question of why so many have become simultaneously susceptible to a variety of pathogens has yet to be answered (Porter et al. 1999).

Table 1. Selected disturbances in
Florida marine fauna and flora,
1980 to present.

Year               Species        Disturbance

                                  Indian River Lagoon, Florida Bay,
                                  Florida Keys: high prevalences of
                                  fibropapilloma disease; ongoing
ongoing          sea turtles      since its epizootic emergence in
                                  the mid-1980s; causes are unknown
                                  (Jacobson et al. 1991; Lackovich et
                                  al. 1999; Landsberg et al. 1999)

                                  Indian River to Charlotte Counties:
                                  between September (2000) and
                                  February 7 (2001), 150 sick or dead
                                  turtles have been reported; because
2000-01       loggerhead turtle   most sea turtles do not wash ashore
                                  many more are expected to have
                                  died; unique disease conditions in
                                  afflicted animals though cause(s)
                                  are unknown (Florida Marine
                                  Research Institute 2001)

                                  Indian River Lagoon: increase in
2001          bottlenose          skin lesions; severe dermatitis and
               dolphin            lobomycosis noted in five animals
                                  (Bossart pers comm)

                                  Homosassa Springs: papilloma virus
2000-current       manatee        lesions in isolated population;
                                  first discovery of a virus in
                                  manatee (Kirley 2000)

2000          bottlenose          Atlantic coast: oral papillomas in
               dolphin            12 animals (Bossart pets comm)

                                  Florida Keys: 150 animals stranded,
                                  with at least 31 mortalities, over
2000          bottlenose          a two day period in mid-January;
               dolphin            causes are unknown (Marine Mammal
                                  Commission in prep)

                                  Barnes Key, southeast Florida:
                                  scattered patches of diseased
1999-current       seagrass       seagrasses resembling conditions
                                  associated with massive mortalities
                                  in late 1980s and early 1990s
                                  (Durako, pers comm)

                                  Florida panhandle: 68 dead animals
                                  found between August 8 and October
                                  31; by February 2000 total
1999-2000     bottlenose          strandings numbered approximately
               dolphin            120; brevetoxin suspected (Hull
                                  2000; Marine Mammal Commission in
                                  prep)

                                  Southwest Florida: over 150 animals
1996               manatee        are killed by brevetoxin
                                  intoxication (Bossart et al 1998)

                                  Alligator Reef: first recorded
                                  occurrence of "white plague type
                                  II" disease; the disease ultimately
1995                coral         infected 17 species of
                                  scleractinian corals over ~200 km
                                  along the Florida Keys (Feingold &
                                  Richardson 1999; Richardson et al
                                  1998)

                                  South Florida: immunoblastic
1994-96            dolphins       malignant lymphoma (cancer) noted
                                  in five animals (Bossart et al.
                                  1997)

                                  Florida Keys: first identification
                                  of "yellow-blotch" disease
                                  (originally called "yellow-band"
1994                coral         disease); disease incidence and
                                  associated coral death has
                                  increased in some areas since
                                  (Green & Bruckner 2000; Reeves 1994)

                                  Palm Beach/upper Florida keys: mass
                                  mortality (est. at several
                                  thousands) over a 3 month period;
                                  multiple pathogens found, but no
1993-94           reef fish       one primary suggesting that some
                                  stressor severely weakened the
                                  fish; 1st extensive reef-fish
                                  mortality event reported in Florida
                                  since 1980 (Landsberg 1995)

                                  Florida Bay: further mass
1992-93            sponges        mortalities of sponges coinciding
                                  with cyanobacteria blooms (Butler
                                  et al. 1995)

                                  Florida Bay: mortality of over 80%
                                  of vase, candle and commercial
                                  sponges and over 40% of loggerhead
1991-92            sponges        sponges in an area covering
                                  hundreds of [km.sup.2] and
                                  coinciding with unprecedented
                                  blooms of cvanobacteria (Butler et
                                  al. 1995)

                                  Lower Florida Keys: suspected
1991              sea urchin      disease event reduced densities by
                                  97% (Forcucci 1994)

                                  North Biscayne Bay: two studies
                                  note high levels of developmental
                                  abnormalities across a range of
1989-1992            fish         fish species suggesting one common
                                  stressing agent; cause is not
                                  determined (Browder et al. 1993;
                                  Gassman et al. 1994)

                                  Atlantic coast: major mass
                                  mortality event involving the
                                  deaths of ~2,000 animals from
                                  Florida to New Jersey (following a
1987-88       bottlenose          migration trajectory); likely
                dolphin           morbillivirus-related though
                                  environmental contaminants and
                                  brevetoxin may have contributed to
                                  the severity of the event (Geraci
                                  et al. 1999)

                                  Florida Bay: unprecedented mass
                                  mortality event that ultimately
                                  destroys 4,000 ha of Thalessia
1987-1991        turtle grass     seagrass beds while affecting
                                  another 23,000 ha; a complex
                                  etiology suspected (Robblee et al.
                                  1991)

                                  Florida Gulf and Atlantic coasts:
                                  over 13,000 wintering loons may
1983             common loon      have died over a three month
                                  period; a complex etiology was
                                  suspected (Forrester et al. 1997)

                                  southwestern Florida: 37 animals
                                  killed likely via brevetoxin
1982               manatee        ingestion during a red tide bloom;
                                  deaths of cormorants and fish also
                                  reported (O'Shea et al. 1991)

                                  Indian River/Banana River: ~50
1982          bottlenose          animals found dead in a three month
               dolphin            period; likely caused by a
                                  morbillivirus (Duignan et al. 1996)

The preponderance of microalgal involvement in disturbance events in U.S. Atlantic and Gulf waters was also noted by the HEED program and, indeed, a recent review (CENR 2000) concluded that the effects of harmful algal blooms in the U.S. have expanded from a few scattered coastal areas to virtually all coastal states over the past two decades. However, the report noted that the relative roles of increased observer coverage and monitoring, nutrient enrichment, the introduction of exotic species, and naturally-mediated range expansion remain unresolved. The increase in algal blooms globally has occurred in tandem with increases in cultural eutrophication (Smayda 1989; Paerl 1997), a pattern readily evident in U.S. estuaries (Bricker et al. 1999). The recent emergence of predatory and toxic Pfiesteria-like dinoflagellates as a conspicuous feature of massive fish kills ([10.sup.3] to [10.sup.9]) in mid-Atlantic estuaries has been linked, in part, to nutrient enrichment (Burkholder and Glasgow 1997).

A relationship between the toxic effects of Pfiesteria spp. and recent and recurring epidemics of a severe ulcerative disease (ulcerative mycosis) in U.S. southeastern finfish, primarily menhaden (Brevoortia tyrannus), has been proposed (Burkholder and Glasgow 1997; Noga et al. 1996) but has also underlined the complexities of marine pathobiology (see Blazer et al. 1999). The most important feature of diseased fish has been the involvement of the fungal-like organism Aphanomyces spp. but difficulties in fulfilling Koch's postulates with either Pfiesteria or Aphanomyces would suggest that other factors are involved (Dykstra and Kane 2000). Other U.S. marine disturbances have also presented a considerable challenge. Hundreds of thousands of lobsters (Homarus americanus) were estimated to have died in an apparent disease-related event in Long Island Sound over the latter part of 1999. A paramoeba infection is suspected but the predisposing factors are unknown (Van Patten and French 2000). Withering disease has virtually exterminated black abalone (Haliotis cracherodii) from the Channel Islands since emerging during the mid-1980s, and has since spread to populations on the mainland California coast (Altstatt et al. 1996). The pathogen, a rickettsiale, has only recently been confirmed (Friedman 2000) but the factors prompting the emergence of the disease are unknown; its severity, however, is enhanced by increased water temperature (Moore et al. 2000).

Some of the most profound disturbances associated with marine wildlife populations have been ongoing over the past decades in the Alaska region. Northern fur seal (Callorhinus ursinus) numbers fell from 1.25 million in 1974 to 877,000 in 1983, though they have climbed slightly since then to an estimated 1 million, about 50 percent of pre-exploitation size (NMFSa 1999). Steep declines in harbor seal (Phoca vitulina richardsi) numbers were recorded during the 1980s, primarily from the Gulf of Alaska; current overall population size is placed at around 80,000 animals, substantially less than the 270,000 estimated for the early 1970s (Marine Mammal Commission 1998; NMFS 1998). The western stock of Steller sea lions (Eumetopias jubatus) numbered approximately 140,000 in the late 1950s and 30,500 by 1990 when it was designated as an endangered species under the ESA. Numbers have continued to decline and were estimated as slightly over 20,000 in 1998 (NMFS 1999b). Sea otters (Enhydra lutris) in the Aleutian Islands have declined from an estimated 55,100 to 73,700 animals in the mid-1980s to under 10,000 by 2000, and have been listed as a candidate species for listing under the ESA (Federal Register 2000). Estes et al. (1998) consider that increased orca (Orcinus orca) predation has driven the sea otter collapse, a response to vastly reduced numbers of the orca's preferred prey, Steller sea lions and harbor seals. It has been generally considered (e.g., NRC 1996) that the most important factors involved overall are some combination of a natural climate regime shift and fisheries, and perhaps the effects of prior intensive whaling; their effects may have combined to reduce the abundances of nutritionally-adequate forage fishes.

Occurring in tandem have been declines in various populations of Alaska sea ducks including, for example: (1) a 54 percent decline between 1976 and 1994 of nesting common eider (Somateria mollissima) in northern Alaska and the western Canadian arctic; (2) a 2.2 percent annual decline between 1977 and 1998 in black scoter (Melanitta nigra) in western Alaska; (3) a 5.5 percent annual decline of oldsquaw (Clangula hyemalis) in surveyed areas in western Alaska since 1977; (4) over a 90 percent decline in spectacled eider (Somateria fischeri) in the YK-Delta from the 1970s to 1992; and (5) the virtual disappearance of Steller's eiders (Polysticta stelleri) from the YK-Delta since initial surveys in the 1960s (USFWS 1999). Spectacled eiders and the Alaska breeding population of Steller's eiders have been listed as threatened under the ESA. There is, however, little consistency in Alaska sea duck trends: some species have generally remained stable or have increased slightly, and species whose populations have declined in one (or more) area(s) have remained stable or have increased in others. Causes of declines are not known.

Anthropogenic and natural influences

It has only been recently (e.g., Sarokin and Schulkin 1992; Rosenberg et al. 1988; Williams and Bunkley-Williams 1990) that human involvement--for example chemical pollution, nutrient enrichment, and climate change--has been deemed a factor to consider when investigating marine disturbances. In addition, it has been increasingly noticed that disease, biotoxins, and food shortages are important components of some disturbance events (Alaska Sea Grant 1993; Harvell et al. 1999). In most instances, however, little can be said over the relative roles of natural processes and human influence as interactions are complex and cover a spectrum of physical, biological and chemical variables. Levels and causes of disease in marine species and the role of disease in regulating populations are, likewise, poorly understood.

Some associations between marine disturbances and climate have been reviewed by Harvell et al. (1999). Lavigne and Schmitz (1990) also suggested that rising temperatures associated with anthropogenic climate change could increase epizootics in pinnipeds, particularly in those species that "haul out" at small temperature increases. Higher densities of seals for longer duration could create the conditions appropriate for pathogen invasion. Increased sea water temperature was correlated with a major epizootic involving commercial sponges (Spongia spp., Hippospongia spp.) in the Mediterranean Sea between 1986 and 1990 that decimated populations (above 40 m depth) throughout the eastern part of the basin (Vacelet et al. 1994). The event, likely bacterialrelated, was unprecedented in Mediterranean recorded history. Millions of sea fans (Paramuricea clavata, Eunicella spp.) were estimated to have died in the Ligurian Sea in 1999 in a catastrophic event also correlated with an increase in sea water temperature (Cerrano et al. 2000). Temperature increase was suggested (Vincente 1989) as a possible factor in the extinction of commercial sponges (the same genera as affected in the Mediterranean), in areas throughout the West Indies by the 1950s. Echinoderm mass mortalities in Japan and the Gulf of California were linked to abnormally warm sea water temperature (Dugan et al. 1982; Tsuchiya et al. 1987). Cook et al (1998) noticed a correlation with increasing sea surface temperature and the northward spreading of the protozoan Perkinsus marinus, a serious pathogen of the eastern oyster (Crassostrea virginica).

P. marinus, however, was likely introduced into the U.S. Atlantic and Gulf coasts via aquaculture--an activity which has been the source of many epizootics (see Renault 1996 for a review). A virus, possibly introduced via baitfish for offshore fish farming, is suspected in two massive pilchard (Sardinops sagax neopilchardus) die-offs in Australian waters (1995, 1998 to 99) (Gaughan et al. 2000); in the latter event it was estimated that 60 to 70 percent of total pilchard numbers around western Australia perished. Ballast water dumping practices (Ruiz et al. 2000) and tourism (e.g., Gardner et al. 1997) may also be important sources in the continuing transfer of new microbial pathogens into marine wildlife.

Environmental pollutants, notably the halogenated hydrocarbons have, likewise, been implicated in a variety of marine disturbances (for recent reviews see Oberdorster and Cheek 2000; Vos et al. 2000). Pinnipeds and coastal odontocetes have received particular attention given their high contaminant loading and the recent occurrence of population disturbances that have involved disease or declines in reproductive ability, or both (Marine Mammal Commission 1999).

Polychlorinated biphenyl (PCB) contamination of the resident Puget Sound population of orca may be an important factor in their recent decline (Ross et al. 2000); the population has fallen by 14 percent (from 99 to 84) since 1995 (Forney et al. 2000). PCB levels from live-sampled animals exceed those found to induce immunosuppression and endocrine disruption in harbor seals, though the toxicological significance in orca is not known. Levels of PCBs, DDT, and tributyltin in California southern sea otters are higher in animals dying of infectious disease than from trauma or unknown causes (Kannan et al. 1998; Nakata et al. 1998), and an unusual frequency and variety of diseases in the species have been reported (Thomas et al 1998). The role of contaminants, or disease, in this population's recent decline (Marine Mammal Commission 2000a), however, are likewise not known. Similarly, the impact of environmental pollutants in disease-mediated mass mortality events is not known; however, elevated levels in affected populations (e.g., Kannan et al. 1997; Kuehl et al. 1994) may increase the severity of epizootics through immunosuppressive action (Marine Mammal Commssion 1999).

MMEDs are multifaceted and complex, and teasing out ultimate causes and effects, and the full range of risk factors, has proven elusive in the majority of events (see for example Simmonds and Mayer 1997; Ferguson et al. (2000) for recent case reviews). There is, however, increasing recognition that human activities are now inextricably bound with global processes, and that rapid and unpredicted environmental responses (Streets and Glantz 2000) can ensue from even minor shifts in forcing conditions or from gradual change over extended time periods. Interactions and feedbacks, and the cascades of effects associated with threshold responses, are typical of the dynamic, non-linear, earth system. Nonetheless, MMEDs can provide a warning mechanism into the consequences of human activities and alert the public to potential health threats and deteriorating environmental conditions. As such, MMEDs should receive increased scientific attention. However, the far reaching consequences of environmental disturbances within the context of complexity strongly argues for management initiatives that are precautionary--that is regulatory action before scientific proof of human-related deleterious effects and a shift in the burden-of-proof (concerning an activity's safety or sustainability) from the public onto the proponent.

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