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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

Applied zooarchaeology and Oregon Coast sea otters (Enhydra lutris)

The sea otter (Enhydra lutris) was nearly driven to extinction on the Pacific Coast in the 19th century due to intensive commercial hunting and the maritime fur trade. Despite successful reintroduction efforts elsewhere in North America, the Oregon sea otter population remains locally extirpated and listed as endangered. Prior study addressed precontact sea otter teeth from Oregon and found they were not significantly different in absolute size from modern California sea otter (Enhydra lutris nereis) teeth, and smaller than modern Alaska sea otter (Enhydra lutris lutris) teeth. These geographic groupings were later confirmed by an ancient DNA study. The conclusion that distinct geographic populations exist based on tooth size was founded on small samples. Larger samples of teeth, as well as new data on humeri and femora, indicate dimensions vary significantly along a latitudinal cline from California to Alaska. Morphometric analyses of ancient animal remains can be used to examine spatial relationships of phenotypic features and inform conservation biology decisions.     

Predicting reproduction in captive sea otters (Enhydra lutris)

The sea otter (Enhydra lutris) is a threatened species. It is also a popular exhibit animal in many zoos and aquariums worldwide. Unfortunately, sea otters reproduce successfully in only a small number of facilities. Pregnancies vary in duration, and are thought to involve a delayed implantation of about 2–3 months, followed by an implanted phase of 4–5 months. In this study we attempted to identify estrus and pregnancy states, and predict the date of birth in one female sea otter (Mali) housed at the Lisbon Oceanarium. We used different techniques to evaluate her reproductive status, including monitoring behavior to determine estrus, assessing weight changes to determine pregnancy and parturition date, and analyzing fecal hormone samples to determine estrus, pregnancy, and parturition date. During this study, Mali became pregnant four times. Her gestational length varied between 188–255 days. Weight increases >29 kg or 15% above baseline weight suggested pregnancy, and parturition was estimated to occur approximately 3 months thereafter. Fecal hormone (progestagens and estrogen) metabolite data gathered during two of her pregnancies showed that Mali's delayed implantation phase of pregnancy lasted 43–109 days (a typical duration in other sea otters is 100–110 days). Mali's implanted phase lasted a relatively long time (140–145 days compared to an average of 117 days in other sea otters). The combination of the three measurements was a powerful tool that enabled us to determine pregnancy and anticipate the arrival of a new sea otter pup. Zoo Biol 24:73–81, 2005. © 2005 Wiley‐Liss, Inc.     

Reductions in the dietary niche of southern sea otters (Enhydra lutris nereis) from the Holocene to the Anthropocene

The sea otter (Enhydra lutris) is a marine mammal hunted to near extinction during the 1800s. Despite their well‐known modern importance as a keystone species, we know little about historical sea otter ecology. Here, we characterize the ecological niche of ancient southern sea otters (E. lutris nereis) using δ¹³C analysis and δ¹⁵N analysis of bones recovered from archaeological sites spanning ~7,000 to 350 years before present (N = 112 individuals) at five regions along the coast of California. These data are compared with previously published data on modern animals (N = 165) and potential modern prey items. In addition, we analyze the δ¹⁵N of individual amino acids for 23 individuals to test for differences in sea otter trophic ecology through time. After correcting for tissue‐specific and temporal isotopic effects, we employ nonparametric statistics and Bayesian niche models to quantify differences among ancient and modern animals. We find ancient otters occupied a larger isotopic niche than nearly all modern localities; likely reflecting broader habitat and prey use in prefur trade populations. In addition, ancient sea otters at the most southerly sites occupied an isotopic niche that was more than twice as large as ancient otters from northerly regions. This likely reflects greater invertebrate prey diversity in southern California relative to northern California. Thus, we suggest the potential dietary niche of sea otters in southern California could be larger than in central and northern California. At two sites, Año Nuevo and Monterey Bay, ancient otters had significantly higher δ¹⁵N values than modern populations. Amino acid δ¹⁵N data indicated this resulted from shifting baseline isotope values, rather than a change in sea otter trophic ecology. Our results help in better understanding the contemporary ecological role of sea otters and exemplify the strength of combing zooarchaeological and biological information to provide baseline data for conservation efforts.     

Stress-related hormones and genetic diversity in sea otters (Enhydra lutris)

Sea otters ( Enhydra lutris ) once ranged throughout the coastal regions of the north Pacific, but were extirpated throughout their range during the fur trade of the 18th and 19th centuries, leaving only small, widely scattered, remnant populations. All extant sea otter populations are believed to have experienced a population bottleneck and thus have lost genetic variation. Populations that undergo severe population reduction and associated inbreeding may suffer from a general reduction in fitness termed inbreeding depression. Inbreeding depression may result in decreased testosterone levels in males, and reduced ability to respond to stressful stimuli associated with an increase in the stress-related adrenal glucocorticoid hormones, cortisol and corticosterone. We investigated correlations of testosterone, cortisol, and corticosterone with genetic diversity in sea otters from five populations. We found a significant negative correlation between genetic diversity and both mean population-level ( r ²= 0.27, P < 0.001) and individual-level ( r ²= 0.54, P < 0.001) corticosterone values, as well as a negative correlation between genetic diversity and cortisol at the individual level ( r ²= 0.17, P = 0.04). No relationship was found between genetic diversity and testosterone ( P = 0.57). The strength of the correlations, especially with corticosterone, suggests potential negative consequences for overall population health, particularly for populations with the lowest genetic diversity.