Disease organisms, contaminants, and nutrients, all coming from terrestrial sources, are very significant contributors to mortality in the southern sea otter population. Mortality due to diseases and parasites, particularly in prime age adult females, are driving population performance. Epidemics of some diseases, and the synergistic effects of pathogen exposure and ecological factors such as density-dependent diet change and nutritional stress, as well as increased exposure to toxins, have resulted in record mortalities in recent years. In the winter of 2004, we brought a group of disease ecology, epidemiology and species experts together to review current information on sea otter morbidity and mortality. From the assembled data it became clear that several anthropogenic sources of pathogen, chemical and nutrient pollution accounted for a very significant proportion of southern sea otter mortality. We believe this is the first demonstration that diseases and a complicated set of land sea connections, a “dirty ocean,” are limiting the potential for recovery of an ESA listed “threatened” and ecological keystone marine mammal species. Sea otters appear to not only be a very sensitive sentinel of this “dirty ocean,” but their health problems help identify specific threats to nearshore ecosystems. Some of the problems identified are amenable to immediate improvement, such as enforcement of existing pollution laws, reduction of routes of entry for opossum and cat feces into marine environments; others will be more difficult to fix. We can “save” southern sea otters or move toward population recovery if we can improve the health of their nearshore habitats, but this will take significant commitment and investment.
Sea otters (Enhydra lutris) were hunted to near extinction during the Pacific maritime fur trade. Further hunting was prohibited by international treaty in 1911, at which time a dozen or so remnant colonies survived. The southern sea otter (E. l. nereis) is descended from one of these remnant colonies that survived along the Big Sur coastline of central California and contained perhaps fewer than 50 individuals at the beginning of the 20th century. Over the last century the population has grown slowly, much more slowly than its theoretical maximum, and now numbers approximately 2800.
Coastal oceans are arguably among the most vulnerable habitats to human development. Humans live by the sea in disproportionately large numbers (20 million Californians live in its coastal counties), and the coastal oceans are the ultimate receptacles of urban, industrial and agricultural effluents. Furthermore, the coastal oceans are heavily utilized for recreation and food and as a transport medium for the goods and materials needed to fuel a growing global economy. As a high-trophic level obligate nearshore predator, sea otters may be more vulnerable to these activities than most other species, and as such may serve as sentinels of the health of California’s coastal oceans. For these reasons, and because our findings on sea otter mortality suggested terrestrial sources for many pathogens and chemicals, we reviewed the magnitude, patterns and causes of southern sea otter mortality and a growing body of evidence of land-sea connections.
Methods and Results
The participants reviewed numerous published papers2-6,9,10 and other unpublished studies. The demographics and population performance patterns of the southern sea otter population for the last century, recent trends in population performance, recent trends in mortality and both general and specific causes of mortality, clustering or mortality, as well as evidence for sources of pathogens and pollutants were reviewed.
Overall patterns of mortality in California sea otters are remarkably different from those reported for sea otters elsewhere, typically late winter associated with food deprivation and harsh weather.11 In California, mortality often peaks in summer and in recent years of record high carcass recovery, an additional spring peak in mortality has also been noted. Another oddity in California is the relatively high probability of death for prime age females. The typical pattern elsewhere is elevated mortality of dependent animals and pups, recently weaned juveniles and very old individuals, but low mortality for prime-age animals.11
A number of novel diseases, parasites and intoxications have been identified in southern sea otters over the last decade.1,6-8,10,12,13 Between 1992 and 2004, approximately 647 southern sea otters received complete postmortem examinations; this represents 29% of all animals whose bodies were recovered during that time period. There are few death assemblages for wild species that are comparable in detail, longevity, and percentage of the population examined. If we assume that sea otters found fresh dead are representative of the population as a whole, during the early to mid-1990s, diseases and parasites accounted for approximately 40% of mortality.13 This proportion appears to have increased to 50% for 241 otters examined at the MWVCRC from 1998–2003. When intoxication and all forms of diseases were considered, they accounted for 64% of 105 sea otters examined between 1998 and 2001.6 As the leading general cause of death in California sea otters, diseases are an important limiting factor to population growth. Spatial and temporal patterns of protozoal infection and mortality suggest terrestrial sources.6,9 Miller et al. 2002 showed a clear association between proximity to freshwater inputs into the ocean and proportion of otters infected with Toxoplasma. Kreuder et al. (2005) reported clusters of mortality from May through November 2000 due to cardiomyopathy and myocarditis just north and south of Morro Bay, respectively. Other causes of southern sea otter mortality exhibit similar clustering patterns in embayment areas with adjacent denser human populations.
Although we have significant data suggesting that the “dirty ocean” is central to the southern sea otter recovery problems, some uncertainty remains3 as to the potential influence of more difficult to detect sources of mortality such as predators that might consume sea otters (like killer whales) and some fisheries interactions. At this point we must conclude that disease and intoxications are significant demographic drivers of the California sea otter population and reflect a pathogen-rich environment, but the influence of increased vulnerability due to food limitation, immune dysfunction or some interactive effect of these and other factors remains speculative.
The authors thank Drs. Andy Dobson, Frances Gulland, Rick Ostfeld, Kevin Lafferty, and Mike Murray for their review of and input on this papers concept. We thank the staff of the CDFG-MWVCRC, USGS/BRD and the Monterey Bay Aquarium. Additionally, some of our other collaborators, Drs. K. Arkush and M. Griggs, W. Miller, N. Thomas have been the source of various useful insights and concepts.
1. Cole, R.A., D.S. Lindsay, D.K. Howe, C.L. Roderick, J.P. Dubey, N.J. Thomas, and L.A. Baeten. 2000. Biological and molecular characterizations of Toxoplasma gondii strains obtained from southern sea otters (Enhydra lutris nereis). J Parasitol. 86:526–530.
2. Estes, J.A., Brian B. Hatfield, K. Ralls, and J. Ames. 2003. Causes of mortality in California sea otters during periods of population growth and decline. Mar. Mamm. Sci. 19:198–216.
3. Gerber L.R., M.T. Tinker, D.F. Doak, J.E. Estes, and D.A. Jessup. 2004. Mortality sensitivity in life-stage stimulation analysis: a case study of Southern sea otters. Ecol. Appl. 14(5):1154–1165.
4. Hanni, K.D., J.A.K. Mazet, F.M.D. Gulland, J. Estes, M. Staedler, M.J. Murray, and D.A. Jessup. 2003. Clinical pathological values and assessment of pathogen exposure in southern and Alaskan sea otters. J. Wildl. Dis. 39(4):837–850.
5. Jessup, D.A., M. Miller, J. Ames, M. Harris, P. Conrad C. Kreuder and J.A.K. Mazet. 2004. The southern sea otter (Enhydra lutris nereis) as a sentinel of marine ecosystem health. Ecohealth. 1(3):239–245.
6. Kreuder, C., M. Miller, D. Jessup, L. Lowenstine M.D. Harris, J. Ames, T.E. Carpenter, P.A. Conrad, and J.K. Mazet. 2003. Patterns of mortality in the southern sea otter (Enhydra lutris) from 1998–2001. J Wildl. Dis. 39(3):495–509.
7. Kreuder, C., M. Miller, P. Conrad, L. Lowenstine, T. Carpenter, D. Jessup, and J. Mazet. 2005. Evaluation of cardiac lesions and risk factors associated with myocarditis and dilated cardiomyopathy in southern sea otters (Enhydra lutris nereis). Am. J. Vet. Res. 66(2):289–299.
8. Lindsay D.S., N.J. Thomas, and J.P. Dubey. 2000, Biological characterization of Sarcocystis neurona isolated from a southern sea otter (Enhydra lutris nereis). Int. J. Parasitol. 30:617–624.
9. Miller, M.A., I.A. Gardner, D. Paradies, K. Worcester, D. Jessup, E. Dodd, M. Harris, J. Ames, A. Packham, and P.A. Conrad 2002. Coastal freshwater runoff is a risk factor for Toxoplasma gondii infection of southern sea otters (Enhydra lutris nereis). Int. J. Parasitol. 32:997–1006.
10. Miller M.A., M.E. Griggs, C. Kreuder, E.R. James, A.C. Melli, P.R. Crosbie, D.A. Jessup, J.C. Boothroyd, D. Brownstein, and P.A. Conrad. 2004. An unusual genotype of Toxoplasma gondii is common in California sea otters (Enhydra lutris nereis) and is a cause of mortality. Int. J. Parasitol. 34:275–284.
11. Monson D.H., J.A. Estes, D.B. Siniff and J.B. Bodkin. 2000. Life history, plasticity and population regulation of sea otters. Oikos. 90:457–468.
12. Stavely C.M., K.B. Register, M.A. Miller, S.L. Brockmeier, D.A. Jessup, and S. Jang. 2003. Molecular and antigenic characterization of Bordetella bronchiseptica isolated from a wild southern sea otter (Enhydra lutris nereis) with severe suppurative bronchopneumonia. J. Vet. Diag. Invest. 15(6):570–574.
13. Thomas, N.J. and R.A. Cole. 1996. Risk of disease and threats to wild populations. Endangered Species Update. 13:23–27.