Clinical Signs and Pathology Associated With Domoic Acid Toxicosis in Southern Sea Otters (Enhydra lutris nereis)

The marine biotoxin domoic acid (DA) is an analog of the neurotransmitter glutamate that exerts potent excitatory activity in the brain, heart, and other tissues. Produced by the diatom Pseudo-nitzschia spp., DA accumulates in marine invertebrates, fish, and sediment. Southern sea otters (Enhydra lutris nereis) feed primarily on invertebrates, including crabs and bivalves, that concentrate and slowly depurate DA. Due to their high prey consumption (25% of body weight/day), sea otters are commonly exposed to DA. A total of 823 necropsied southern sea otters were examined to complete this study; first we assessed 560 subadult, adult, and aged adult southern sea otters sampled from 1998 through 2012 for DA-associated pathology, focusing mainly on the central nervous system (CNS) and cardiovascular system. We applied what was learned to an additional cohort of necropsied sea otters of all demographics (including fetuses, pups, juveniles, and otters examined after 2012: n = 263 additional animals). Key findings derived from our initial efforts were consistently observed in this more demographically diverse cohort. Finally, we assessed the chronicity of DA-associated pathology in the CNS and heart independently for 54 adult and aged adult sea otters. Our goals were to compare the temporal consistency of DA-associated CNS and cardiovascular lesions and determine whether multiple episodes of DA toxicosis could be detected on histopathology. Sea otters with acute, fatal DA toxicosis typically presented with neurological signs and severe, diffuse congestion and multifocal microscopic hemorrhages (microhemorrhages) in the brain, spinal cord, cardiovascular system, and eyes. The congestion and microhemorrhages were associated with detection of high concentrations of DA in postmortem urine or gastrointestinal content and preceded histological detection of cellular necrosis or apoptosis. Cases of chronic DA toxicosis often presented with cardiovascular pathology that was more severe than the CNS pathology; however, the lesions at both sites were relatively quiescent, reflecting previous damage. Sea otters with fatal subacute DA toxicosis exhibited concurrent CNS and cardiovascular pathology that was characterized by progressive lesion expansion and host response to DA-associated tissue damage. Acute, subacute, and chronic cases had the same lesion distribution in the CNS and heart. CNS pathology was common in the hippocampus, olfactory, entorhinal and parahippocampal cortex, periventricular neuropil, and ventricles. The circumventricular organs were identified as important DA targets; microscopic examination of the pituitary gland, area postrema, other circumventricular organs, and both eyes facilitated confirmation of acute DA toxicosis in sea otters. DA-associated histopathology was also common in cardiomyocytes and coronary arterioles, especially in the left ventricular free wall, papillary muscles, cardiac apex, and atrial free walls. Progressive cardiomyocyte loss and arteriosclerosis occurred in the same areas, suggesting a common underlying mechanism. The temporal stage of DA-associated CNS pathology matched the DA-associated cardiac pathology in 87% (n = 47/54) of cases assessed for chronicity, suggesting that the same underlying process (e.g., DA toxicosis) was the cause of these lesions. This temporally matched pattern is also indicative of a single episode of DA toxicosis. The other 13% of examined otters (n = 7/54) exhibited overlapping acute, subacute, or chronic DA pathology in the CNS and heart, suggestive of recurrent DA toxicosis. This is the first rigorous case definition to facilitate diagnosis of DA toxicosis in sea otters. Diagnosing this common but often occult condition is important for improving clinical care and assessing population-level impacts of DA exposure in this federally listed threatened subspecies. Because the most likely source of toxin is through prey consumption, and because humans, sea otters, and other animals consume the same marine foods, our efforts to characterize health effects of DA exposure in southern sea otters can provide strong collateral benefits.

Characterizing the impact of recovering sea otters on commercially important crabs in California estuaries

Protective legislation and management have led to an increase in California’s sea otter Enhydra lutris nereis population. While sea otter recovery has been linked to ecosystem benefits, sea otter predation may negatively affect commercially valuable species. Understanding the potential influence of sea otters is of particular importance as their range expands into estuaries that function as nurseries for commercially valuable species like Dungeness crab Metacarcinus magister. We consider how sea otter predation has affected the abundance and size of juvenile Dungeness crab in Elkhorn Slough, California, USA, and analyzed cancrid crab abundance and size across 4 California estuaries with and without sea otters to understand how biotic and abiotic factors contribute to observed variation in crab size and abundance. We compared trends in southern sea otters relative to Dungeness crab landings in California to assess whether increasing sea otter abundance have negatively impacted landings. In Elkhorn Slough, juvenile Dungeness crab abundance and size have declined since 2012, coinciding with sea otter population growth. However, the impact of sea otters on juvenile Dungeness crab size was habitat-specific and only significant in unvegetated habitat. Across estuaries, we found that cancrid crab abundance and size were negatively associated with sea otter presence. While abiotic factors varied among estuaries, these factors explained little of the observed variation in crab abundance or size. Although we found evidence that sea otters can have localized effects on cancrid crab populations within estuaries, we found no evidence that southern sea otters, at recent population sizes, have negatively impacted Dungeness crab landings in California from 2000-2014.

Predators, Disease, and Environmental Change in the Nearshore Ecosystem: Mortality in Southern Sea Otters (Enhydra lutris nereis) From 1998–2012

We compiled findings from 15 years (1998–2012) of southern sea otter (Enhydra lutris nereis) necropsies, incorporating data from 560 animals. Sensitive diagnostic tests were used to detect biotoxins, bacteria, parasites and fungi. Methods to classify primary and contributing causes of death (COD) and sequelae utilized an updated understanding of health risks affecting this population. Several interesting patterns emerged, including identification of coastal regions of high mortality risk for sea otter mortality due to shark bite, cardiomyopathy, toxoplasmosis, sarcocystosis, acanthocephalan peritonitis and coccidioidomycosis. We identified demographic attributes that enhanced the risk of disease in relation to age, sex, and reproductive stage. Death due to white shark (Carcharodon carcharias) bite increased dramatically during the study period and was the most common primary COD. However, when primary and contributing COD were combined, the most prevalent COD was infectious disease (affecting 63% of otters), especially fatal infections by acanthocephalans (Profilicollis spp.) and protozoa (e.g., Sarcocystis neurona and Toxoplasma gondii). Fatal bacterial infections were also extremely common as a primary process or a sequela, affecting 68% of examined otters. Substantial advances were made in identifying sea otters that died following exposure to the pervasive marine neurotoxin domoic acid (DA), and DA intoxication was conservatively estimated as a primary or contributing COD for 20% of otters. Cardiomyopathy was also highly prevalent as a primary or contributing COD (41%) and exhibited significant associations with DA intoxication and protozoal infection. For adult and aged adult females in late pup care through post-weaning at the time of death, 83% had end lactation syndrome (ELS) as a primary or contributing COD. This comprehensive longitudinal dataset is unique in its depth and scope. The large sample size and extensive time period provided an opportunity to investigate mortality patterns in a changing environment and identify spatial and temporal disease “hot spots” and emerging threats. Our findings will help improve estimates of population-level impacts of specific threats and optimize conservation and environmental mitigation efforts for this threatened species.

Primary intracranial fibrosarcoma in a southern sea otter Enhydra lutris nereis

Southern sea otters Enhydra lutris nereis, a threatened marine mammal species, face numerous environmental and infectious disease challenges in their native habitat of coastal California, USA. However, there are few published cases describing neoplasia in sea otters despite their relatively long life span when cared for in aquarium settings. An 18 yr old neutered male southern sea otter, born and raised in human care, presented with an acute onset of seizures and dull mentation. Magnetic resonance imaging of the head revealed a large, central brain lesion. After no improvement with treatment, euthanasia was elected due to a poor prognosis. Grossly, a poorly demarcated, granular, tan mass expanded the cranial meninges in the longitudinal fissure at the level of the cruciate sulcus and extended into the underlying gray matter and superficial white matter. Histologically, the mass was composed of spindle cells, forming haphazardly arranged interlacing bundles and herringbone patterns, with a high mitotic count, moderate cellular pleomorphism, and prominent vascularization. Neoplastic cells demonstrated positive immunoreactivity for vimentin and negative immunoreactivity for smooth muscle actin, factor VIII-related antigen, S100, melan-A, E-cadherin, desmin, glial fibrillary acidic protein, and cytokeratin AE1/AE3. Based on gross, histologic, and immunohistochemical findings, the mass was most consistent with a primary intracranial fibrosarcoma (PIF). PIFs are a rare neoplasm in both humans and other animals with few reports in the veterinary literature. This is the first recorded case of a PIF in a sea otter.