A Southern Sea Otter (Enhydra lutris nereis) Unusual Mortality Event: Findings from Analysis of Fresh Dead Animals
American Association of Zoo Veterinarians Conference 2004
M. Miller1,2, DVM, PhD, MS; C. Kreuder2, VMD, PhD; J. Mazet2, DVM, PhD; F. Gulland3, BVSC, PhD; F. Van Dolah4, PhD; T. Leighfield4, MS; D. Brownstein1,2, BS; P. Conrad2, DVM, PhD; J. Dugan5, PhD; D. Jessup1, DVM, MPVM, DACZM
1Marine Wildlife Veterinary Care and Research Center, California Department of Fish & Game, Santa Cruz, CA, USA; 2Wildlife Health Center, School of Veterinary Medicine, University of California, Davis, CA, USA; 3The Marine Mammal Center, Sausalito, CA, USA;4NOAA-NMFS Marine Biotoxins Program, Center for Coastal Environmental Health and Biomolecular Research (CCEHBR), Charleston, South Carolina, USA; 5University of California, Santa Barbara, CA, USA

Abstract

The southern sea otter (Enhydra lutris nereis) population, located on the coast of central California, is listed as “threatened” under the Endangered Species Act. Recent surveys estimate that the entire population numbers approximately 2500 animals and that the population has failed to increase significantly since 1995.4 An abundance of evidence suggests that high mortality is a key factor in the slow recovery of this population.4,8 From February through April 2003, southern sea otter carcass recovery rates exceeded 10-year averages and an “unusual mortality event” (UME) was jointly declared by the U.S. Fish and Wildlife Service (FWS) and the National Oceanic and Atmospheric Administration (NOAA).3 Because of ongoing sea otter mortality and documented domoic acid (DA) intoxication in other marine mammals and birds in the Central California region during this same time period, the FWS and NOAA extended the UME investigation to include otters dying between January 1, 2003 and October 1, 2003.

The total number of fresh and non-fresh southern sea otters stranding in 2003 (n=262) was 23% greater than any previous year and was 58% above the 10-year running average of 166 animals per year.3 For fresh dead sea otters, the most common significant and grossly discernable lesions included: acanthocephalan peritonitis (18%); shark predation (15%); cardiomyopathy syndrome (12%,); boat strike (6%); mating trauma (6%); and geriatric (e.g., dental) disease (6%). On histopathology, suspected or confirmed protozoal (Toxoplasma gondii and/or Sarcocystis neurona) meningoencephalitis or systemic disease4 was observed in 12% of otters. Moderate to severe brain lesions consistent with domoic acid (DA) intoxication2,3,7 were observed in at least 11.6% of otters, with further review in progress. In addition, gross or histopathologic lesions consistent with cardiomyopathy syndrome (gross myocardial mottling, fibrosis, necrosis, vacuolization, nonsuppurative inflammation and ganglioneuritis or cardiac dilation)5 were observed for at least 27.5% of freshly dead otters stranding during the UME. The proportion of southern sea otters reported with gross or histopathologic lesions suggestive of cardiomyopathy syndrome has increased in recent years, and this syndrome has been recognized as a significant source of southern sea otter mortality.5 Recent epidemiologic data supports an association between cardiomyopathy syndrome in sea otters and previous or current DA exposure,5 and cardiac abnormalities have been described in other marine mammals with confirmed or suspected DA intoxication.2,7 In the present study, over 70% of fresh dead sea otters had DA present in urine (as detected by receptor binding assay6), with DA levels ranging from 29 to >42,000 ng/ml. Domoic acid was present in sea otter urine in all months tested (January through September, 2003), suggesting that environmental DA exposure may be chronic for otters living along the central California coast. However, a higher proportion of otters with high urine DA concentrations (>200 ng/ml) were detected in late spring 2003, corresponding with a peak in otter mortality and a recognized DA event in other marine wildlife from the same area. Therefore, DA intoxication may have contributed to the high level of southern sea otter mortality observed in 2003.

Acknowledgments

Special thanks to Brian Hatfield, Jim Estes and Tim Tinker for compiling data on overall mortality and data on non-fresh otters, and to Greg Sanders, USFWS, Trevor Spradlin, NOAA and the UME Working Group for facilitating this work. Thanks to Jack Ames, Mike Harris, Brian Hatfield, Jim Estes, Mike Kenner, Greg Sanders, Erin Dodd, Heather Harris, Sharon Toy-Choutka, Eva Berberich, Kat Starzel, Sandra Wong, Dan Rejmanek, Spencer Jang, Barry Puget, Ann Melli, Andrea Packham, Woutrina Smith, Mike Murray, Michelle Staedler, Andy Johnson and Marty Haulena for facilitating carcass collection, necropsy, sample collection and diagnostics. Thanks also to Kathy Burek and Jim Hill for assisting with sea otter histopathology efforts, and to the staff, students and volunteers of the Monterey Bay Aquarium, the Marine Mammal Center, USGS/BRD, University of California, Moss Landing Marine Laboratory and CDFG Marine Wildlife Veterinary Care and Research Center for facilitating carcass recovery and sampling. Miles Reed, Clare Stavely and others assisted with the development and maintenance of the MWVCRC sea otter necropsy database.

Literature Cited

1.  Goldberg, J. D. 2003. Domoic acid in the benthic food web of Monterey Bay, California. Master’s Thesis. CSUS-MLML. 33 pp.

2.  Gulland, F. 2000. Domoic acid toxicity in California sea lions (Zalophus californianus) stranded along the central California coast, May–October 1998. U.S. Department of Commerce. NOAA Technical Memorandum NMFS-OPR-17. 45 pp.

3.  Jessup, D, M. Miller, M. Harris, B. Hatfield and J. Estes. 2004. The 2003 southern sea otter (Enhydra lutris nereis) unusual mortality event: a preliminary report to NOAA and USFWS. Unpublished technical report: California Department of Fish and Game, Marine Wildlife Veterinary care and Research Center and United States Geological Survey. Santa Cruz, CA. 20 pp.

4.  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.

5.  Kreuder, C., M. Miller, L. J. Lowenstine, P. A. Conrad, T. E. Carpenter, D. A. Jessup and J. K. Mazet. Epidemiologic analysis of risk factors for myocarditis and dilated cardiomyopathy in southern sea otters (Enhydra lutris nereis). Submitted Abstract: Proceedings of the Joint Meeting of Wildlife Disease Association and American Association of Zoological Veterinarians. San Diego, California: August, 2004.

6.  Scholin, C., R. Marin, P. Miller, G. Doucette, C. Powell, P. Haydock, J. Howard and J. Ray. 1999. DNA probes and a receptor binding assay for detection of Pseudo-nitzschia species and domoic acid activity in cultured and natural samples. J. Phycol. 35: 1356–1367.

7.  Silvagni, P. A., Lowenstine, L. J., Spraker T., Lipscomb, T. and F. M. D. Gulland. Pathology of domoic acid toxicity in California sea lions (Zalophus californianus). Vet. Pathol. In press.

8.  Thomas, N. and R Cole. 1996. The risk of disease and threats to the wild population. Endangered Species Update. 13: 23–27.

 

Speaker Information
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M. Miller, DVM, PhD, MS
Marine Wildlife Veterinary Care and Research Center
California Department of Fish & Game
Santa Cruz, CA, USA


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