Abstract
The southern sea otter (Enhydra lutris nereis) is listed as “threatened” under the Endangered Species Act (ESA). Once thought to be extinct, this subspecies appeared to be recovering and had increased in number and geographic distribution since the 1920s. The recovery appeared to falter during the late 1970s but resumed in the early 1980s after bans on net fisheries moved them away from most sea otter habitats. The recovery has once again faltered with an approximately 12% decline since the spring of 1995.1
The sea otter is a “keystone species,” one which strongly influences the abundance and diversity of the other species within its kelp forest ecosystem, primarily by preying upon sea urchins which eat the kelp stipe and holdfast and can reduce a kelp forest to an urchin barren. It is also an excellent bioindicator species. It eats approximately 25% of its body weight per day in shellfish and other invertebrates and can concentrate their contaminants. Since many of these shellfish are also used for human food, its role as a bioindicator has implications for human as well as marine animal health. Sea otters are very susceptible to marine pollutants such as petroleum, which may be directly toxic and/or alter their fur’s insulating properties. This became abundantly clear during the 1989 Exxon Valdez incident and was one of the primary concerns of draft sea otter recovery plans written for the California population in the 1980s and 1990s.
The recent southern sea otter decline has been viewed with some alarm by conservationists and indeed, if the present trend continues, this “threatened” population may be a candidate for “endangered” status within 2–3 years. Higher mortality rather than depressed recruitment appears to underlie the decline. A good deal of debate has centered on the role of infectious diseases and parasites, exposure to contaminants, nutrition and prey availability, net and pot fishery interactions and other sources of mortality. We will review the relative contributions of the major classes of mortality to the current decline.
The southern sea otters’ unique characteristics (ESA listed, bioindicator, keystone species, top of the food web, pollution and disturbance sensitive) may make it an excellent ecosystem health monitoring species. Marine ecosystem health is a relatively new and ill-defined concept. It is generally agreed, however, that healthy ecosystems are those that:
1. Do not have obvious environmental degradation, frequent pollution events or serious anthropogenic effects due to over harvest.
But, previous work suggests that contaminants (e.g., tributyltin) may predispose southern sea otters to dying from infectious diseases.2 It has been observed that mortality rates appear to follow years of higher than normal runoff and subsequent release of a variety of contaminants into the near shore environment. Recently, we collected typical sea otter prey items in Elkhorn Slough, an area with historic contaminant problems, and found that relatively high levels of organochlorine pesticides and their residues are still present. With our continued dependence on oil, California receives over 200 million gallons of crude oil a day and the threat of a major oil spill continues to loom over the sea otter. Incidental drowning of sea otters in nets and potentially in fish traps has been a cause for renewed concern and has resulted in observer programs and mandated changes in fishing regulations.
2. Do not have a high frequency of new or emerging diseases/intoxications with negative implications for human and wildlife health.
But, several new diseases and intoxications have been identified. Rudimentary mapping of sea otter infections with Toxoplasma show clustering in areas with sewage outfalls into the ocean. From both ecologic and regulatory perspectives, if traditional contaminants or pathogen pollution is killing sea otters or predisposing them to infectious diseases that subsequently kill them, there may be reason to call for regulatory and management actions. Several hypotheses have been developed to explain the apparent increase in thorny headed worm caused mortality including increased parasite pathogenicity, shifts in host species populations, and shifts in foraging habitat by sea otters.
3. Have stable, or at least not declining, species abundance and diversity.
But, abundance of many harvested fish and shellfish, including species used by otters for food, is depressed or fluctuates widely. Several traditional sea otter prey species including red, black and white abalone are in serious decline or on the brink of extinction (at least in part due to introduction of pathogens and parasites). Starvation is a relatively common finding in sea otters, although it is unclear whether it is primary or secondary to diseases and parasites. If sea otter numbers decline further, the structure of their kelp forest ecosystem may be altered, via reduction in their “keystone species” role, with resulting further reduction in species abundance and diversity.
4. Do not have frequent die-offs or similar stochastic events, particularly those involving “indicator” or “keystone” species.
But, notable (and still unexplained) focal sea otter mortality events occurred in 1995 and 1998, and since 1995 the southern sea otter rangewide has declined by 12%, apparently due primarily to increased mortality. This decline preceded and has spanned both the El Nino and La Nina oceanic cycles.
Metallic and organohalide contaminants have been identified at disturbing levels in southern sea otter tissues and sea otter food items. In 1998 a toxic algal bloom (Pseudo-nizschia australis) may have caused the death of at least one sea otter (and at least 70 sea lions).3 This type of algal intoxication is very rare in the Pacific Ocean and has never before been reported in sea otters, or any other marine mammal.
Based on the definitions given above of ecosystem health (indicator species die-offs, frequent pollution events, emerging diseases, declining species abundance and diversity), the southern sea otter decline may be a result of, and thereby an indicator of, declining marine ecosystem health. Conversely, this finding may reflect improved diagnostic capabilities, better cooperation and increased monitoring and interest in marine animal mortality events. Or all of these may be occurring simultaneously. Recent diagnosis of two apparently emerging diseases was made possible by very new diagnostic technologies, and agencies and institutions involved in sea otter recovery have developed an excellent cooperative approach in recent years.
Monitoring the health of marine ecosystems is a relatively new concept. But, marine mammals, that are obligate inhabitants of near shore ecosystems, may help monitor short-, medium-, and longer-term disturbances that reflect changes in the health of coastal marine environments. For example, oil spills and depletion of fisheries are often anthropogenic in origin and usually result in short to medium duration changes. Changes in the prevalence of some diseases and parasites may also be the result of human activities. Large scale variation in prey species abundance, ocean nutrient or other cycles, whether natural or due to chronic pollution, global warming, or other things, may cause changes of longer duration. Both long- and medium-term changes may allow or encourage toxic algal blooms, which appear to have increased in recent years. The bottom line is that human caused changes in marine ecosystem health come from a variety of sources that must first be identified and should be mitigated if that is possible.
Current evidence suggests that no one single activity or organism is responsible for the sea otter’s decline. It is not “a shot to the heart” that is killing them, but rather “the death of a thousand cuts.” Several lines of evidence suggest that there are many obvious and more subtle connections to human activities. Approximately 40% of mortalities in fresh necropsied carcasses are due to infectious diseases and parasites.4 Two of these, the protozoal encephalitidies caused by Toxoplasma spp. and Sarcocystis spp., may be emerging diseases of marine mammals. The primary host for one is most likely the domestic cat, and the opossum (an introduced species in California) is a possible host for the other. Two other disease syndromes (some of the bacterial septicemias and coccidioidomycosis [San Joaquin Valley Fever]) may have terrestrial origins and may have human health implications as well. Another major mortality factor, infestation with thorny-headed worms and subsequent peritonitis, may be due to parasite pathogenicity or abundance shifts, shifts in sea otter diet and/or habitat shifts due to changes in abundance of preferred prey species. Sea otter population pressures, pollution, reduced ecosystem carrying capacity or nutrient cycles may be driving these changes.
Mortality events involving different species at various trophic levels have been used as a measure of the health of the Gulf of Mexico and Atlantic Ocean.5 As programs for monitoring causes of marine animal deaths continue, we should try to move towards a fuller understanding of the implications for marine ecosystem health and toward management practices that could preserve and improve the health of the oceans. The California Department of Fish and Game—MWVCRC in cooperation with U.C. Davis and U.C. Santa Cruz is developing a program of marine ecosystem health monitoring and seeks cooperation of other organizations and agencies.
Acknowledgments
We thank the following organizations and individuals for their cooperation and support; the PKD Trust, the Morris Animal Foundation, the Oiled Wildlife Care Network, the Friends of the Sea Otter, Dr. Mike Murray, Michele Staedler and Andy Johnson of the Monterey Bay Aquarium, Dr. Frances Gulland of The Marine Mammal Center, Dr. Jim Estes and Brian Hatfield of USGS/BRD—California Science Center, Drs. Nancy Thomas, Rebecca Cole and Lynn Creekmore USGS/BRD—Wildlife Health Research Center.
Literature Cited
1. Hatfield B. Status of the California sea otter population. USGS/BRD unpublished report. 1999.
2. Kannan K, Gurage KS, Thomas NJ, Tanabe S, Giesy JP. Butyltin residues in Southern sea otters (Enhydra lutris nereis) found dead along California coastal waters. Environmental Science and Technology. 1998;32(9):1169–1175.
3. Scholin C, Gulland F, Doucette GJ, et al. Mortality of sea lions along the central California coast linked to a toxic diatom bloom. Nature. 2000;403(6):80–84.
4. Thomas NJ, Cole RA. Biology and status of the southern sea otter: The risk of disease and threats to the wild population. Endangered Species Update. 1996;13:23–27.
5. Epstein P, Sherman B, Spanger-Siegfried E, Langston A, Prasad S, Mckay B. Marine Ecosystems: Emerging Diseases as Indicators of Change. NOAA/OGP and NASA report on grant NA56GP 0623. 1998.