Sarcomas in three free-ranging northern sea otters (Enhydra lutris kenyoni) in Alaska

Three sarcomas were diagnosed in wild northern sea otters (Enhydra lutris kenyoni) during the mid- to late 1990s. Histologically, the tumors were a chondrosarcoma and two low-grade fibrosarcomas with myofibroblastic cell differentiation. The three sea otters were surviving in the wild and were killed by hunters.     

Persistent organic pollutants in the blood of free-ranging sea otters (Enhydra lutris ssp.) in Alaska and California

As part of tagging and ecologic research efforts in 1997 and 1998, apparently healthy sea otters of four age-sex classes in six locations in Alaska and three in California were sampled for persistent organic pollutants (POPs) and other chemicals of ecologic or environmental concern (COECs). Published techniques for the detection of POPs (specifically ∑polychlorinated biphenyls [PCBs], ∑DDTs, ∑hexachlorocyclohexanes [HCHs], ∑polycyclic aromatic hydrocarbons [PAHs], ∑chlordanes [CHLs], hexachlorobenzene [HCB], dieldrin, and mirex) in the tissue of dead otters were modified for use with serum from live sea otters. Toxic equivalencies (TEQs) were calculated for POPs with proven bioactivity. Strong location effects were seen for most POPs and COECs; sea otters in California generally showed higher mean concentrations than those in Alaska. Differences in contaminant concentrations were detected among age and sex classes, with high levels frequently observed in subadults. Very high levels of ∑DDT were detected in male sea otters in Elkhorn Slough, California, where strong freshwater outflow from agricultural areas occurs seasonally. All contaminants except mirex differed among Alaskan locations; only ∑DDT, HCB, and chlorpyrifos differed within California. High levels of ∑PCB (particularly larger, more persistent congeners) were detected at two locations in Alaska where associations between elevated PCBs and military activity have been established, while higher PCB levels were found at all three locations in California where no point source of PCBs has been identified. Although POP and COEC concentrations in blood may be less likely to reflect total body burden, concentrations in blood of healthy animals may be more biologically relevant and less influenced by state of nutrition or perimortem factors than other tissues routinely sampled.     

Patterns of mortality in southern sea otters (Enhydra lutris nereis) from 1998-2001

Detailed postmortem examination of southern sea otters (Enhydra lutris nereis) found along the California (USA) coast has provided an exceptional opportunity to understand factors influencing survival in this threatened marine mammal species. In order to evaluate recent trends in causes of mortality, the demographic and geographic distribution of causes of death in freshly deceased beachcast sea otters necropsied from 1998-2001 were evaluated. Protozoal encephalitis, acanthocephalan-related disease, shark attack, and cardiac disease were identified as common causes of death in sea otters examined. While infection with acanthocephalan parasites was more likely to cause death in juvenile otters, Toxoplasma gondii encephalitis, shark attack, and cardiac disease were more common in prime-aged adult otters. Cardiac disease is a newly recognized cause of mortality in sea otters and T. gondii encephalitis was significantly associated with this condition. Otters with fatal shark bites were over three times more likely to have pre-existing T. gondii encephalitis suggesting that shark attack, which is a long-recognized source of mortality in otters, may be coupled with a recently recognized disease in otters. Spatial clusters of cause-specific mortality were detected for T. gondii encephalitis (in Estero Bay), acanthocephalan peritonitis (in southern Monterey Bay), and shark attack (from Santa Cruz to Point A?o Nuevo). Diseases caused by parasites, bacteria, or fungi and diseases without a specified etiology were the primary cause of death in 63.8% of otters examined. Parasitic disease alone caused death in 38.1% of otters examined. This pattern of mortality, observed predominantly in juvenile and prime-aged adult southern sea otters, has negative implications for the overall health and recovery of this population.     

Mustelid herpesvirus-2, a novel herpes infection in northern sea otters (Enhydra lutris kenyoni)

Oral ulcerations and plaques with epithelial eosinophilic intranuclear inclusions were observed in northern sea otters (Enhydra lutris kenyoni) that died or were admitted for rehabilitation after the 1989 Exxon Valdez oil spill (EVOS) in Alaska, USA. Transmission electron microscopy demonstrated the presence of herpesviral virions. Additionally, a serologic study from 2004 to 2005 found a high prevalence of exposure to a herpesvirus in live-captured otters. Tissues from 29 otters after the EVOS and nasal swabs from 83 live-captured otters in the Kodiak Archipelago were tested for herpesviral DNA. Analysis identified a novel herpesvirus in the gamma subfamily, most closely related to Mustelid herpesvirus-1 from badgers. Results indicated that this herpesvirus is associated with ulcerative lesions but is also commonly found in secretions of healthy northern sea otters.     

Lymphosarcoma in a sea otter (Enhydra lutris)

Lymphoblastic lymphosarcoma involving the mesenteric lymph node and thymus was discovered in a 4 yr old male sea otter (Enhydra lutris). Diagnosis was based on gross and light microscopic studies. The cause of this neoplasm was not determined. This is the first case of lymphosarcoma reported in sea otters.     

Biological and molecular characterizations of Toxoplasma gondii strains obtained from southern sea otters (Enhydra lutris nereis)

Toxoplasma gondii was isolated from brain or heart tissue from 15 southern sea otters (Enhydra lutris nereis) in cell cultures. These strains were used to infect mice that developed antibodies to T. gondii as detected in the modified direct agglutination test and had T. gondii tissue cysts in their brains at necropsy. Mouse brains containing tissue cysts from 4 of the strains were fed to 4 cats. Two of the cats excreted T. gondii oocysts in their feces that were infectious for mice. Molecular analyses of 13 strains indicated that they were all type II strains, but that they were genetically distinct from one another.     

Clinical pathology and assessment of pathogen exposure in southern and Alaskan sea otters

The southern sea otter (Enhydra lutris nereis) population in California (USA) and the Alaskan sea otter (E. lutris kenyoni) population in the Aleutian Islands (USA) chain have recently declined. In order to evaluate disease as a contributing factor to the declines, health assessments of these two sea otter populations were conducted by evaluating hematologic and/or serum biochemical values and exposure to six marine and terrestrial pathogens using blood collected during ongoing studies from 1995 through 2000. Samples from 72 free-ranging Alaskan, 78 free-ranging southern, and (for pathogen exposure only) 41 debilitated southern sea otters in rehabilitation facilities were evaluated and compared to investigate regional differences. Serum chemistry and hematology values did not indicate a specific disease process as a cause for the declines. Statistically significant differences were found between free-ranging adult southern and Alaskan population mean serum levels of creatinine kinase, alkaline phosphatase, alanine aminotransferase, aspartate aminotransferase, calcium, cholesterol, creatinine, glucose, phosphorous, total bilirubin, blood urea nitrogen, and sodium. These were likely due to varying parasite loads, contaminant exposures, and physiologic or nutrition statuses. No free-ranging sea otters had signs of disease at capture, and prevalences of exposure to calicivirus, Brucella spp., and Leptospira spp. were low. The high prevalence (35%) of antibodies to Toxoplasma gondii in free-ranging southern sea otters, lack of antibodies to this parasite in Alaskan sea otters, and the pathogen's propensity to cause mortality in southern sea otters suggests that this parasite may be important to sea otter population dynamics in California but not in Alaska. The evidence for exposure to pathogens of public health importance (e.g., Leptospira spp., T. gondii) in the southern sea otter population, and the na?veté of both populations to other pathogens (e.g., morbillivirus and Coccidiodes immitis) may have important implications for their management and recovery.     

Genetic diversity and population parameters of sea otters, Enhydra lutris, before fur trade extirpation from 1741-1911

All existing sea otter, Enhydra lutris, populations have suffered at least one historic population bottleneck stemming from the fur trade extirpations of the eighteenth and nineteenth centuries. We examined genetic variation, gene flow, and population structure at five microsatellite loci in samples from five pre-fur trade populations throughout the sea otter's historical range: California, Oregon, Washington, Alaska, and Russia. We then compared those values to genetic diversity and population structure found within five modern sea otter populations throughout their current range: California, Prince William Sound, Amchitka Island, Southeast Alaska and Washington. We found twice the genetic diversity in the pre-fur trade populations when compared to modern sea otters, a level of diversity that was similar to levels that are found in other mammal populations that have not experienced population bottlenecks. Even with the significant loss in genetic diversity modern sea otters have retained historical structure. There was greater gene flow before extirpation than that found among modern sea otter populations but the difference was not statistically significant. The most dramatic effect of pre fur trade population extirpation was the loss of genetic diversity. For long term conservation of these populations increasing gene flow and the maintenance of remnant genetic diversity should be encouraged.     

Coastal freshwater runoff is a risk factor for Toxoplasma gondii infection of southern sea otters (Enhydra lutris nereis)

The association among anthropogenic environmental disturbance, pathogen pollution and the emergence of infectious diseases in wildlife has been postulated, but not always well supported by epidemiologic data. Specific evidence of coastal contamination of the marine ecosystem with the zoonotic protozoan parasite, Toxoplasma gondii, and extensive infection of southern sea otters (Enhydra lutris nereis) along the California coast was documented by this study. To investigate the extent of exposure and factors contributing to the apparent emergence of T. gondii in southern sea otters, we compiled environmental, demographic and serological data from 223 live and dead sea otters examined between 1997 and 2001. The T. gondii seroprevalence was 42% (49/116) for live otters, and 62% (66/107) for dead otters. Demographic and environmental data were examined for associations with T. gondii seropositivity, with the ultimate goal of identifying spatial clusters and demographic and environmental risk factors for T. gondii infection. Spatial analysis revealed clusters of T. gondii-seropositive sea otters at two locations along the coast, and one site with lower than expected T. gondii seroprevalence. Risk factors that were positively associated with T. gondii seropositivity in logistic regression analysis included male gender, older age and otters sampled from the Morro Bay region of California. Most importantly, otters sampled near areas of maximal freshwater runoff were approximately three times more likely to be seropositive to T. gondii than otters sampled in areas of low flow. No association was found between seropositivity to T. gondii and human population density or exposure to sewage. This study provides evidence implicating land-based surface runoff as a source of T. gondii infection for marine mammals, specifically sea otters, and provides a convincing illustration of pathogen pollution in the marine ecosystem.     

Coccidioidomycosis in a California sea otter (Enhydra lutris).

A weak and emaciated California sea otter (Enhydra lutris) was found stranded on Atascadero Beach in Morro Bay, California. It died three weeks after capture. A diagnosis of coccidioidomycosis was confirmed by histology, serology and culture. This is believed to be the first reported case of this disease from the Morro Bay area of San Luis Obispo County, California as well as the first reported case in a free-ranging marine mammal.     

An unusual genotype of Toxoplasma gondii is common in California sea otters (Enhydra lutris nereis) and is a cause of mortality

Toxoplasma gondii-associated meningoencephalitis is a significant disease of California sea otters (Enhydra lutris nereis), responsible for 16% of total mortality in fresh, beachcast carcasses. Toxoplasma gondii isolates were obtained from 35 California otters necropsied between 1998 and 2002. Based on multi-locus PCR-restriction fragment length polymorphism and DNA sequencing at conserved genes (18S rDNA, ITS-1) and polymorphic genes (B1, SAG1, SAG3 and GRA6), two distinct genotypes were identified: type II and a novel genotype, here called type x, that possessed distinct alleles at three of the four polymorphic loci sequenced. The majority (60%) of sea otter T. gondii infections were of genotype x, with the remaining 40% being of genotype II. No type I or III genotypes were identified. Epidemiological methods were used to examine the relationship between isolated T. gondii genotype(s) and spatial and demographic risk factors, such as otter stranding location and sex, as well as specific outcomes related to pathogenicity, such as severity of brain inflammation on histopathology and T. gondii-associated mortality. Differences were identified with respect to T. gondii genotype and sea otter sex and stranding location along the California coast. Localised spatial clustering was detected for both type II (centred within Monterey Bay) and x (centred near Morro Bay)-infected otters. The Morro Bay cluster of type x-infected otters overlaps previously reported high-risk areas for sea otter infection and mortality due to T. gondii. Nine of the 12 otters that had T. gondii-associated meningoencephalitis as a primary cause of death were infected with type x parasites.     

Scoliosis and uterine torsion in a pregnant sea otter (Enhydra lutris) from California

Scoliosis and uterine torsion are described in a pregnant adult sea otter (Enhydra lutris) tagged 3 yr prior to death. Apparently, severe scoliosis in sea otters can be compatible with good nutritional status and a life-span measured in years. No causal correlation of this condition with the animal's death was established.     

Gene sequences for cytochromes p450 1A1 and 1A2: the need for biomarker development in sea otters (Enhydra lutris)

There has been recent public concern regarding the impacts of environmental pollution on populations of otters. Population level impacts have been seen with otter (Lutra lutra) populations in Europe due to polychlorinated biphenyls, and with some segments of the Prince William Sound, AK, sea otter (Enhydra lutris) population following the Exxon Valdez oil spill. Despite public interest in these animals and their ecological significance, there are few tools that allow for the study of otter's response to contaminant exposure. Cytochrome p450 1A (CYP1A) performs the first step in metabolizing many xenobiotics, including many polychlorinated biphenyls and polycyclic aromatic hydrocarbons. CYP1A induction is a frequently used biomarker of exposure to these compounds. Despite the potential importance of this gene in ecological risk assessment, the complete coding sequence has not been published for any otter species. This study's objective was to isolate the gene for CYP1A1 and CYP1A2 in sea otters using a series of PCR-based approaches. The coding sequences from CYP1A1 and CYP1A2 from sea otters were identified and published in GenBank. Both CYP1A sequences are homologous to those obtained from marine mammals and other carnivores. These sequences will be useful as tools for researchers assessing contaminant exposure in mustelid populations.     

Sarcocysts of an unidentified species of Sarcocystis in the sea otter (Enhydra lutris)

The number of Sarcocystis species that infect sea otters (Enhydra lutris) is unknown. Sea otter tissues were recently shown to harbor sarcocysts of S. neurona and of unidentified species of Sarcocystis. Whereas sarcocysts of S. neurona have walls 1-3 microm thick with type 9 villar protrusions, ultrastructure of a distinct thin-walled sarcocyst (0.5-0.7 microm thick) lacking villar protrusions, but instead exhibiting minute type 1 undulations on the sarcocyst wall, is described in this report. Parasites characterized from a sea otter infection were inferred to be related to, but distinct from, other species belonging to Sarcocystis, based on sequencing and phylogenetic analysis of a portion of the beta subunit of the plastid-encoded RNA polymerase gene.     

Adaptive changes in the cardiac automatism of the sea otter Enhydra lutris

Electrographic investigations in sea otters reveal acute decrease in the heart rate (to 1/2--1/8 of the normal rate) during diving. The longer the dive, the more intense the bradycardia. Each partial exhalation under water causes further decrease in the heart rate. The duration of cardiac cycles (R--R) increases mainly at the expense of the prolongation of diastole (T--P). Variations in the heart rate during submersion result from the increased vagal tone. Atropine injections abolish diving bradycardia. On surfacing, the animals exhibit a pronounced recovery tachycardia.     

Helminth parasites of the southern sea otter Enhydra lutris nereis in central California: abundance,distribution and pathology

From October 1997 to May 2001, the gastrointestinal tracts from 162 beach-cast southern sea otters Enhydra lutris nereis were examined for helminth parasites and associated lesions. Carcasses were collected opportunistically in central California between Pt. San Pedro and Pt. Arguello. The primary goals of this study were to examine spatial and temporal variability in mortality due to parasite infection, identify factors associated with increased risk of infection, and illustrate the process of intestinal perforation by Profilicollis spp. Two genera and 4 species of acanthocephalans (Profilicollis altmani, P. kenti, P. major, Corynosoma enhydri) were found in 46.3% (Profilicollis spp.) and 94.4% (C. enhydri) of the carcasses examined. Three species of Digenea (Microphallus pirum, M. nicolli, Plenosoma minimum) were found in 47% of carcasses, at times in massive numbers (> 3000 per cm2). This is the first report of the latter 2 species from the sea otter. Mortality resulting from infection by Profilicollis spp. occurred in 13.0% (n = 21) of sampled carcasses, either directly, due to perforation of the intestinal wall and peritonitis (9.9%, n = 16), or indirectly, due to inhibition of host nutrient uptake or depletion of host energy reserves to fight chronic infections (3.1%, n = 5). The most massive infections (< 8760 parasites), and all cases of intestinal perforation occurred in carcasses infected by P. altmani and/or P. kenti. Mortality due to infection by Profilicollis spp. occurred more frequently among juvenile and old-adult females (chi2 = 17.479, df = 9, p = 0.045) from sand and mixed habitats in Monterey and Santa Cruz in the north of the sea otter range (chi2 = 9.84, df = 4, p = 0.045). Spatial differences in sea otter mortality coincided with the relative distributions of Profilicollis altmani, P. kenti, and P. major, and may reflect differences in sea otter diet, or differences in intensity of infection in intermediate hosts. Mortality rate due to infection by Profilicollis spp. decreased between 1998 and 2001, though differences were not significant (chi2 = 3.983, df = 3, p = 0.40), and may vary on multi-year cycles due to environmental factors such as density of definitive hosts (e.g. the surf scoter Melanitta perspicillata), or El Ni?o. Corynosoma enhydri did not cause significant damage to the intestine of the host, even when present in great numbers.     

Biological characterisation of Sarcocystis neurona isolated from a Southern sea otter (Enhydra lutris nereis)

Sarcocystis neurona was isolated from the brain of a juvenile, male southern sea otter (Enhydra lutris nereis) suffering from CNS disease. Schizonts and merozoites in tissue sections of the otter's brain reacted with anti-S. neurona antiserum immunohistochemically. Development in cell culture was by endopolyogeny and mature schizonts were first observed at 3 days postinoculation. PCR of merozoite DNA using primer pairs JNB33/JNB54 and restriction enzyme digestion of the 1100 bp product with Dra I indicated the organism was S. neurona. Four of four interferon-gamma gene knockout mice inoculated with merozoites developed S. neurona-associated encephalitis. Antibodies to S. neurona but not Sarcocystis falcatula, Toxoplasma gondii, or Neospora caninum were present in the serum of inoculated mice. This is the first isolation of S. neurona from the brain of a non-equine host.     

Hearing in the sea otter (Enhydra lutris): auditory profiles for an amphibious marine carnivore

In this study we examine the auditory capabilities of the sea otter (Enhydra lutris), an amphibious marine mammal that remains virtually unstudied with respect to its sensory biology. We trained an adult male sea otter to perform a psychophysical task in an acoustic chamber and at an underwater apparatus. Aerial and underwater audiograms were constructed from detection thresholds for narrowband signals measured in quiet conditions at frequencies from 0.125–40 kHz. Aerial hearing thresholds were also measured in the presence of octave-band masking noise centered at eight signal frequencies (0.25–22.6 kHz) so that critical ratios could be determined. The aerial audiogram of the sea otter resembled that of sea lions and showed a reduction in low-frequency sensitivity relative to terrestrial mustelids. Best sensitivity was ?1 dB re 20 µPa at 8 kHz. Under water, hearing sensitivity was significantly reduced when compared to sea lions and other pinniped species, demonstrating that sea otter hearing is primarily adapted to receive airborne sounds. Critical ratios were more than 10 dB higher than those measured for pinnipeds, suggesting that sea otters are less efficient than other marine carnivores at extracting acoustic signals from background noise, especially at frequencies below 2 kHz.