Abstract

Blooms of the marine diatom Pseudo-nitzschia often produce domoic acid (DA), a potent neurotoxin that is an important cause of mortality in marine mammals along the Pacific Coast of North America.¹ DA toxicosis and cardiomyopathy have been identified as major causes of mortality in southern sea otters (Enhydra lutris nereis) and previous research has linked DA exposure to cardiomyopathy in otters.^2,3 Among 560 beach-cast sea otters necropsied between 1998–2012, DA intoxication was the primary or contributing cause of death for 20% of otters and cardiomyopathy for 41% of otters. As part of this mortality study, we evaluated DA exposure and potential health impacts. Our provisional case definition of DA intoxication encompassed case history, gross and microscopic lesions, and biochemical tests. Based on preponderance of evidence, sea otters were classified for DA intoxication as a primary or contributing cause of death as probable, possible, unlikely, or unknown. Biochemical testing included liquid chromatography-tandem mass spectrometry (LCMS/MS) and enzyme-linked immunosorbent assay. Urine and/or gastrointestinal content were tested for 336 otters, with LCMS/MS results ranging from <MDL to 420,000 ppb in urine, and <MDL to 84,000 ppb in gastrointestinal content. Our multivariate logistic regression model for DA intoxication included sex, age class, and nutritional condition (n=208). Adults showed the highest prevalence of DA intoxication, with subadults and aged adults less frequently affected (OR=0.6, p=0.3–0.4). Males had 2.4-fold increased odds compared with females (OR=2.4, p=0.008) and otters in fair to excellent nutritional condition were 5.0 times more likely to die of DA intoxication than otters in worse nutritional states (OR=5.0, p<0.0001). A sub-analysis of otters with identifiable stomach contents (n=85) suggested that consumption of crabs (OR=2.6, p=0.2) and clams (OR=8.1, p=0.07) may be associated with DA intoxication. Sea otter cardiomyopathy includes myocarditis and dilated cardiomyopathy and previous research has identified DA exposure and protozoal infection as potential risk factors.³ Cardiomyopathy is also found in California sea lions (Zalophus californianus) with DA toxicosis.⁴ In our current study, the multivariate logistic regression model for cardiomyopathy included age class, DA intoxication, S. neurona and T. gondii infection, a spatial cluster (Moss Landing), and a temporal cluster (March-June 2004) (n=529). Aged adults were 11.5 times more likely to die of cardiomyopathy than subadults (OR=11.5, p<0.0001) and adults were 3.0 times more likely than subadults (OR=3.0, p=0.001). Otters with DA intoxication were substantially more likely to die of cardiomyopathy than those with no evidence of DA exposure (OR=4.6, p<0.0001). Cardiomyopathy was also associated with S. neurona (OR=1.9, p=0.004) and T. gondii infection (OR=2.3, p<0.0001), as well as high risk spatial and temporal clusters (OR=2.9 and 11.9, p<0.0001). Given the pervasiveness of DA-producing blooms in coastal California and invertebrate prey,^5,6 and predictions that blooms will increase with climate change,^7,8 there is an urgent need to better understand the effects of DA toxicosis in sea otters.

Acknowledgements

The authors wish to thank many contributors, including Patricia Conrad, 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, Sharon Toy-Choutka, Christen Bechert, 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, Katie Colegrove, Kathi Lefebvre, Kathy Burek, Robert Poppenga, Elizabeth Torr, and the UCD VMTH histology and microbiology staff for their outstanding 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
+ Student presenter

Literature Cited

1.  Scholin CA, Gulland F, Doucette GJ, et al. 2000. Mortality of sea lions along the central California coast linked to a toxic diatom bloom. Nature. 403:80–84.

2.  Kreuder C, Miller MA, Jessup DA, et al. 2003. Patterns of mortality in southern sea otters (Enhydra lutris nereis) from 1998–2001. J Wildl Dis. 39:495–509.

3.  Kreuder C, Miller MA, Lowenstine LJ, et al. 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.  Zabka TS, Goldstein T, Cross C, et al. 2009. Characterization of a degenerative cardiomyopathy associated with domoic acid toxicity in California sea lions (Zalophus californianus). Vet Path. 46:105–119.

5.  Lewitus AL, Horner RA, Caron DA, et al. 2012. Harmful algal blooms along the North American west coast region: History, trends, causes, and impacts. Harm Alg. 19:133–159.

6.  Kvitek RG, Goldberg JD, Smith GJ, et al. 2008. Domoic acid contamination within eight representative species from the benthic food web of Monterey Bay, California, USA. Mar Ecol Prog Ser. 367:35–47.

7.  Wells ML, Trainer VL, Smayda TJ, et al. 2015. Harmful algal blooms and climate change: Learning from the past and present to forecast the future. Harm Alg. 49:68–93.

8.  McKibben SM, Peterson W, Wood AM, et al. 2017. Climatic regulation of the neurotoxin domoic acid. Proc Nat Acad Sci. 114:239–244.