Exposure to domoic acid is an ecological driver of cardiac disease in southern sea otters

• Published in: Harmful algae 2021-01, Vol.101, p.101973, Article 101973
• Main Authors: Moriarty, Megan E., Tinker, M. Tim, Miller, Melissa A., Tomoleoni, Joseph A., Staedler, Michelle M., Fujii, Jessica A., Batac, Francesca I., Dodd, Erin M., Kudela, Raphael M., Zubkousky-White, Vanessa, Johnson, Christine K.
• Format: Article
• Language: English
• Subjects: Animals; Bayes Theorem; Cardiac disease; Climate change; Domoic acid; Ecosystem; Heart Diseases; Kainic Acid - analogs & derivatives; Longitudinal Studies; Otters; Prey preference; Risk model; Sea otter
• ISSN: 1568-9883; 1878-1470
• DOI: 10.1016/j.hal.2020.101973

•Domoic acid exposure increased the risk of fatal cardiac disease in sea otters.•Toxin exposure particularly increased cardiomyopathy hazard among prime-age adults.•Crabs/clams accumulate domoic acid and were high-risk prey for otter heart disease.•Bayesian model combined environmental domoic acid datasets to characterize exposure.•Wildlife disease monitoring revealed chronic health effects of domoic acid exposure. Harmful algal blooms produce toxins that bioaccumulate in the food web and adversely affect humans, animals, and entire marine ecosystems. Blooms of the diatom Pseudo-nitzschia can produce domoic acid (DA), a toxin that most commonly causes neurological disease in endothermic animals, with cardiovascular effects that were first recognized in southern sea otters. Over the last 20 years, DA toxicosis has caused significant morbidity and mortality in marine mammals and seabirds along the west coast of the USA. Identifying DA exposure has been limited to toxin detection in biological fluids using biochemical assays, yet measurement of systemic toxin levels is an unreliable indicator of exposure dose or timing. Furthermore, there is little information regarding repeated DA exposure in marine wildlife. Here, the association between long-term environmental DA exposure and fatal cardiac disease was investigated in a longitudinal study of 186 free-ranging sea otters in California from 2001 – 2017, highlighting the chronic health effects of a marine toxin. A novel Bayesian spatiotemporal approach was used to characterize environmental DA exposure by combining several DA surveillance datasets and integrating this with life history data from radio-tagged otters in a time-dependent survival model. In this study, a sea otter with high DA exposure had a 1.7-fold increased hazard of fatal cardiomyopathy compared to an otter with low exposure. Otters that consumed a high proportion of crab and clam had a 2.5- and 1.2-times greater hazard of death due to cardiomyopathy than otters that consumed low proportions. Increasing age is a well-established predictor of cardiac disease, but this study is the first to identify that DA exposure affects the risk of cardiomyopathy more substantially in prime-age adults than aged adults. A 4-year-old otter with high DA exposure had 2.3 times greater risk of fatal cardiomyopathy than an otter with low exposure, while a 10-year old otter with high DA exposure had just 1.2 times greater risk. High Toxoplasma gondii titers also inc