Abstract

The southern sea otter (SSO; Enhydra lutris nereis), like many threatened carnivores, faces many threats to recovery, and effective conservation depends on a clear understanding of causes of mortality and associated risk factors. To address this knowledge gap and update our understanding of the causes of mortality, our multi-agency team compiled data from 560 SSO necropsies between 1998 –2012. Enrollment was limited to fresh carcasses (minimal tissue decomposition), with detailed necropsy performed from 1998 through 2012, including all eligible subadult (1–4 years), adult (4–10 years), or aged adult (>10 years) otters of either sex; younger animals were excluded due to limited examination by veterinary pathologists, and lower probability of guiding key conservation decisions. Our sample population included a subset of opportunistically collected animals, and all tagged otters that fit the above selection criteria. The primary and contributing cause(s) of death were determined based on gross lesions, histopathology and diagnostic tests, including systematic serology and biochemical testing. A standardized hierarchy was established to rank primary and contributing cause(s) of death, and sequelae such as secondary bacterial infection. In addition to updating collective knowledge regarding “classical” causes of SSO death, such as white shark (Carcharodon carcharias) predation⁸, protozoal infection^2,4,5,6 and Profilicollis sp.-associated acanthocephalan peritonitis^2,6, we also present findings on less well-characterized processes, such as domoic acid (DA) intoxication2,3, cardiomyopathy2,3 and end-lactation syndrome (ELS)^1,7 that could be impacting SSO population recovery. Spatial scan statistics were used to identify high or low-risk locations for common diseases, and potential connections between common causes of SSO death. Multivariate logistic regression models highlighted associations among key causes of death and demographic characteristics, comorbidities, and environmental variables. Shark bite was the most prevalent primary cause of death (28%), followed by acanthocephalan peritonitis (11%), probable DA intoxication (9%), cardiomyopathy (8%), ELS (8%), and primary bacterial infection (7%), while important contributing causes of death included all the above as well as gastrointestinal erosions/ melena and protozoal infection. Substantial spatial, temporal, or space-time clustering was noted for several common causes of death, including shark bite, acanthocephalan peritonitis, protozoal disease, ELS, cardiomyopathy and coccidioidomycosis. Shark bite was significantly more common as a cause of death during later years (2008–2012), in subadults stranding in good nutritional condition, and for SSO stranding from August through January. Acanthocephalan peritonitis was most common in emaciated subadults, and otters stranding near Moss Landing from 2002 through 2007. Bacterial infections as sequelae were important contributors to death from shark bite and acanthocephalan peritonitis. Significant risk factors for Toxoplasma gondii as a cause of death included subadult age, concurrent cardiomyopathy, and stranding in the southern portion of the range. Risk factors for death due to Sarcocystis neurona included subadult age, male sex, emaciated condition, concurrent cardiomyopathy, stranding during the late wet and early dry season, and stranding from Guadalupe to Cayucos during March/April, 2004. ELS-associated death was most common in older females that stranded during spring, and areas with greater kelp cover and higher SSO density. Detailed findings for DA and cardiomyopathy will be covered in an accompanying presentation.

Acknowledgements

We gratefully acknowledge assistance from many contributors, including Patricia Conrad, Tracey Goldstein, Walter Boyce, Alyssa Capuano, Stori Oates, Jonna Mazet, Mike Ziccardi, Matthew Blake, Kirsten Gilardi, Linda Lowenstine, Lavonne Hull, Woutrina Smith, Katie Greenwald, Angie Reed, Jack Ames, Dave Jessup, Jessica Kunz, Ben Shaw, Mike Sowby, Eva Berberich, Sharon Toy-Choutka, Gina Bartlett, Luz deWit, Christen Bechert, Sara Huckabone, Sarah Chinn, Raphe Kudela, Brian Hatfield, Joe Tomoleoni, Ben Weitzman, Mike Murray, Michelle Staedler, Karl Mayer, Andy Johnson, Marissa Young, Karen Worcester, David Paradies, Mary Adams, Lilian Carswell, Frances Gulland, Padraig Duignan, Amanda Foss, Mark Aubel, Eric Delwart, Juliana Siqueira, Terry Ng, Linlin Li, Xutao Deng, Katie Colegrove, Kathi Lefebvre, Kathy Burek, the UCD VMTH histology and microbiology staff, and CAHFS staff for their outstanding diagnostic work. Our team would also like to express their sincere appreciation to the citizens of California for making this work possible through contributions to the California Sea Otter Fund (Sea Otter Tax Checkoff) through the California State Coastal Conservancy, and the California Department of Fish and Wildlife, Office of Spill Prevention and Response.

* Presenting author

Literature Cited

1.  Chinn SM, Miller MA, Tinker MT, Staedler MM, Batac FI, Dodd EM, Henkel LA. 2016. The high cost of motherhood: end-lactation syndrome in southern sea otters (Enhydra lutris nereis) on the central California Coast, USA. J Wildl Dis. 52:307–318.

2.  Kreuder C, Miller MA, Jessup DA, Lowenstein LJ, Harris MD, Ames JA, Carpenter TE, Conrad PA, Mazet JAK. 2003. Patterns of mortality in southern sea otters (Enhydra lutris nereis) from 1998–2001. J Wildl Dis. 39:495–509.

3.  Kreuder, CM, Miller MA, Lowenstine LJ, Conrad PA, Carpenter TE, Jessup DA, Mazet JK. 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. 66:289–299.

4.  Miller MA, Conrad PA, Harris M, Hatfield B, Langlois G, Jessup DA, Magargal SL, Packham AE, Toy-Choutka S, Melli AC, Murray MA. 2010. A protozoal-associated epizootic impacting marine wildlife: Mass-mortality of southern sea otters (Enhydra lutris nereis) due to Sarcocystis neurona infection. Vet Parasitol.172:183–194.

5.  Thomas NJ, Dubey JP, Lindsay DS, Cole RA, Meteyer CU. 2007. Protozoal meningoencephalitis in sea otters (Enhydra lutris): a histopathological and immunohistochemical study of naturally occurring cases. J Comp Path. 137:102–121.

6.  Thomas NJ, Cole RA. 1996. The risk of disease and threats to the wild population. Special issue: Conservation and management of the southern sea otter. Endangered Species Update. National Wildlife Health Center. 13(12):23–7.

7.  Thometz NM, Kendall TL, Richter BP, Williams TM. 2016. The high cost of reproduction in sea otters necessitates unique physiological adaptations. J Exper Biol. 219:2260–2264.

8.  Tinker MT, Hatfield BB, Harris MD, Ames JA. 2016. Dramatic increase in sea otter mortality from white sharks in California. Mar Mam Sci. 32:309–326.