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PCBs and organochlorine pesticide residues in otters (Lutra lutra) and in otter spraints from SW England and their likely impact on populations.

PCB and organochlorine pesticide residues were determined in otter (Lutra lutra) spraints (faeces) from nine catchment regions in SW England over the period 1989-1991. Results of analyses of tissues from 22 otters are also presented. Dieldrin occurred in the majority of spraint samples and p,p-DDE and total PCBs in all. Lindane occurred mainly in samples collected in spring. Lindane was not found in otter tissues collected after 1991, but dieldrin, p,p-DDE and PCBs were found in all tissues. Dieldrin and p,p-DDE concentrations were strongly correlated in otter tissues, but there were no correlations with lindane or PCBs. Mean concentrations of contaminants varied widely between catchments. It was considered that PCBs were the compounds of most concern in influencing otter populations and that levels in spraints from one catchment were likely to be sufficiently high to exert a negative effect on populations. While levels of PCBs were elevated above background level in several other catchments and some individual otters had high levels of PCBs, it was considered that they were not sufficient to significantly hinder further population consolidation of otters in SW England.

Animals↗

Genetic consequences of population decline in the European otter (Lutra lutra): an assessment of microsatellite DNA variation in Danish otters from 1883 to 1993.

The European otter (Lutra lutra) was common in Denmark until the 1960s, but its present distribution encompasses only a minor part of the country. The aim of this study was to assess whether the recent population decline has resulted in loss of genetic variability and to gain further insight into the dynamics of the population decline. This was done by analysing microsatellite DNA variation in contemporary and historical samples, the latter encompassing DNA samples extracted from museum specimens covering a time-span from the 1880s to the 1960s. Tests for differences in expected heterozygosity and the numbers of alleles in contemporary versus historical samples and a test for detecting population bottlenecks provided few indications of a recent bottleneck and loss of variability. However, a procedure for detecting population expansions and declines, based on the genealogical history of microsatellite alleles, suggested that a drastic long-term population decline has taken place, which could have started more than 2000 years ago, possibly due to ancient anthropogenic pressure. Finally, assignment tests and pairwise F(ST) values suggested weak but statistically significant genetic differentiation between the extant population and historical samples of otters from other regions in Denmark, more likely reflecting differentiation among original populations rather than recent drift.

Animals↗

[Primary structure of otter (Lutra lutra L.) myoglobin. II. Pepsin peptides of trypsin hydrolysate. Reconstruction of the polypeptide chain of the otter myoglobin globin component].

13 peptic peptides have been isolated from the insoluble (at pH 5.0) fraction of the tryptic hydrolysate of main chromatographic component of otter myoglobin and their amino acid composition and N-terminal amino acid sequences have been determined. The isolated peptides contain in total 40 amino acid residues. The results obtained, along with those on tryptic peptides and the comparison with homologous portions of myoglobins of the known primary structure, allowed reconstructing the complete amino acid sequence of otter myoglobin.

Amino Acid Sequence↗

Polychlorinated biphenyls in the Eurasian otter (Lutra lutra).

Several authors have suggested that contamination by polychlorinated biphenyls (PCBs) constitutes one of the major causes of the decline of the Eurasian otter (Lutra lutra) in large parts of Europe. This chapter provides an overview of available information regarding PCBs in European otters. Data on PCB concentrations in European otter tissues differ qualitatively among authors. Variations may be found in the organs used for analysis, the analytical method, and format of reported data (lipid weight vs. fresh weight, total PCB vs. congener-specific), which complicates a comparison of all data. Further, concentrations may be highly variable within an otter population, or even among individuals inhabiting the same area. Generally, average PCB levels in otters appear to be highest in areas where the species is in decline (mean levels ranging from 50 to 180 mg/kg fat) and thriving otter populations are correlated with low mean PCB tissue concentrations (mean levels less than 30 mg/kg fat). However, high levels have recently been found in thriving otter populations in Scotland, especially Shetland, leading some researchers to the conclusion that the alleged role of PCBs in the decline of the otter is likely to have been exaggerated. However, it is neither possible to dismiss the role of PCBs in the otter's decline as exaggerated nor to assume their important role as proven. The data presented in this review include information in support of both views. Most studies on PCBs in otters report total PCBs only, congener-specific data being quite rare. Information on levels of non-ortho congeners, the most toxic PCBs, is even more limited. Because congener patterns may vary between different otters, the total PCB concentration may not always be an accurate estimator of toxicity. To make a proper assessment of the impact of environmental PCB levels on the performance of otter populations and to establish "safe PCB levels" in sediment and fish, a number of toxicokinetic processes have to be elucidated. In general, the following chain of effects should be studied: concentrations in sediment-->concentrations in prey organisms-->concentrations in otter-->physiological effects-->population effects. Recommendations are made regarding possible areas of research.

Animals↗

Evaluation of cardiac lesions and risk factors associated with myocarditis and dilated cardiomyopathy in southern sea otters (Enhydra lutris nereis).

OBJECTIVE: To describe cardiac lesions and identify risk factors associated with myocarditis and dilated cardiomyopathy (DCM) in beach-cast southern sea otters. ANIMALS: Free-ranging southern sea otters. PROCEDURE: Sea otters were necropsied at the Marine Wildlife Veterinary Care and Research Center from 1998 through 2001. Microscopic and gross necropsy findings were used to classify sea otters as myocarditis or DCM case otters or control otters. Univariate, multivariate, and spatial analytical techniques were used to evaluate associations among myocarditis; DCM; common sea otter pathogens; and potential infectious, toxic, and nutritional causes. RESULTS: Clusters of sea otters with myocarditis and DCM were identified in the southern aspect of the sea otter range from May to November 2000. Risk factors for myocarditis included age, good body condition, and exposure to domoic acid and Sarcocystis neurona. Myocarditis associated with domoic acid occurred predominantly in the southern part of the range, whereas myocarditis associated with S. neurona occurred in the northern part of the range. Age and suspected previous exposure to domoic acid were identified as major risk factors for DCM. A sample of otters with DCM had significantly lower concentrations of myocardial L-carnitine than control and myocarditis case otters. CONCLUSIONS AND CLINICAL RELEVANCE: Cardiac disease is an important cause of death in southern sea otters. Domoic acid toxicosis and infection with S. neurona are likely to be 2 important causes of myocarditis in sea otters. Domoic acid-induced myocarditis appears to progress to DCM, and depletion of myocardial L-carnitine may play a key role in this pathogenesis.

Animals↗

Comparison of trace element concentrations in livers of diseased, emaciated and non-diseased southern sea otters from the California coast.

Infectious diseases have been implicated as a cause of high rates of adult mortality in southern sea otters. Exposure to environmental contaminants can compromise the immuno-competence of animals, predisposing them to infectious diseases. In addition to organic pollutants, certain trace elements can modulate the immune system in marine mammals. Nevertheless, reports of occurrence of trace elements, including toxic heavy metals, in sea otters are not available. In this study, concentrations of 20 trace elements (V, Cr, Mn, Co, Cu, Zn, Rb, Sr, Mo, Ag, Cd, In, Sn, Sb, Cs, Ba, Hg, Tl, Pb, and Bi) were measured in livers of southern sea otters found dead along the central California coast (n=80) from 1992 to 2002. Hepatic concentrations of trace elements were compared among sea otters that died from infectious diseases (n=27), those that died from non-infectious causes (n=26), and otters that died in emaciated condition with no evidence of another cause of death (n=27). Concentrations of essential elements in sea otters varied within an order of magnitude, whereas concentrations of non-essential elements varied by two to five orders of magnitude. Hepatic concentrations of Cu and Cd were 10- to 100-fold higher in the sea otters in this study than concentrations reported for any other marine mammal species. Concentrations of Mn, Co, Zn, and Cd were elevated in the diseased and emaciated sea otters relative to the non-diseased sea otters. Elevated concentrations of essential elements such as Mn, Zn, and Co in the diseased/emaciated sea otters suggest that induction of synthesis of metallothionein and superoxide dismutase (SOD) enzyme is occurring in these animals, as a means of protecting the cells from oxidative stress-related injuries. Trace element profiles in diseased and emaciated sea otters suggest that oxidative stress mediates the perturbation of essential-element concentrations. Elevated concentrations of toxic metals such as Cd, in addition to several other organic pollutants, may contribute to oxidative stress-meditated effects in sea otters.

Animals↗

Measurement of serum immunoglobulin concentration in killer whales and sea otters by radial immunodiffusion.

Killer whales and sea otters maintained in captivity are the subjects of routine health monitoring programs, and interest in immunologic studies in sea otters has been rising recently in response to potential impacts from infectious disease and environmental pollution on the threatened southern sea otter population. Development of species-specific reagents for immunologic studies in these two marine mammals is currently in its infancy. In this study, killer whale and sea otter immunoglobulin-specific polyclonal antibodies were generated, and used to develop tests for serum Ig concentration in the killer whale (Orcinus orca) and the southern (Enhydra lutris nereis) and northern sea otter (Enhydra lutris lutris). Killer whale serum IgG was purified using caprylic acid/ammonium sulfate precipitation. Sea otter plasma IgG was purified using protein-A-agarose. Polyclonal anti-Ig antisera were produced in rabbits, and specificity confirmed by immunoelectrophoresis. Radial immunodiffusion was used to measure Ig concentration in serum or plasma samples derived from 21 captive killer whales, 18 wild and 4 captive southern sea otters and 15 wild and 4 captive northern sea otters grouped by age. Mean killer whale serum Ig concentration (+/-95% confidence interval) ranged from 15.04 +/- 3.97 g/l for animals aged 0-5 years to 26.65 +/- 9.8 g/l for animals aged >10 years. Mean sea otter serum Ig concentration (+/-95% confidence interval) ranged from 28.39 +/- 11.00 g/l for southern sub-adults to 32.76 +/- 11.58 g/l for southern adults. No significant difference in serum Ig concentration was found between southern and northern sea otters. Serum Ig concentrations in two northern sea otter pups were low compared to those of adult sea otters. The two serum Ig quantitation assays produced were highly specific and reproducible and will be useful additions to the limited number of tests available for immune function in these marine mammal species.

Animals↗

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 Año 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.

Acanthocephala↗

Indirect food web interactions: sea otters and kelp forest fishes in the Aleutian archipelago.

Although trophic cascades-the effect of apex predators on progressively lower trophic level species through top-down forcing-have been demonstrated in diverse ecosystems, the broader potential influences of trophic cascades on other species and ecosystem processes are not well studied. We used the overexploitation, recovery and subsequent collapse of sea otter (Enhydra lutris) populations in the Aleutian archipelago to explore if and how the abundance and diet of kelp forest fishes are influenced by a trophic cascade linking sea otters with sea urchins and fleshy macroalgae. We measured the abundance of sea urchins (biomass density), kelp (numerical density) and fish (Catch per unit effort) at four islands in the mid-1980s (when otters were abundant at two of the islands and rare at the two others) and in 2000 (after otters had become rare at all four islands). Our fish studies focused on rock greenling (Hexagrammos lagocephalus), the numerically dominant species in this region. In the mid-1980s, the two islands with high-density otter populations supported dense kelp forests, relatively few urchins, and abundant rock greenling whereas the opposite pattern (abundant urchins, sparse kelp forests, and relatively few rock greenling) occurred at islands where otters were rare. In the 2000, the abundances of urchins, kelp and greenling were grossly unchanged at islands where otters were initially rare but had shifted to the characteristic pattern of otter-free systems at islands where otters were initially abundant. Significant changes in greenling diet occurred between the mid-1980s and the 2000 although the reasons for these changes were difficult to assess because of strong island-specific effects. Whereas urchin-dominated communities supported more diverse fish assemblages than kelp-dominated communities, this was not a simple effect of the otter-induced trophic cascade because all islands supported more diverse fish assemblages in 2000 than in the mid-1980s.

Animals↗

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.

Aging↗

Histopathologic lesions in sea otters exposed to crude oil.

Following the Exxon Valdez oil spill in Prince William Sound, Alaska, sea otters (Enhydra lutris) that appeared to be contaminated with oil, that were in danger of becoming contaminated, or that were behaving abnormally were captured and taken to rehabilitation centers. Exposure to oil was assessed by visual examination when otters arrived at the centers. Degree of oil exposure was graded according to the following criteria: oil covering greater than 60% of the body--heavily contaminated; oil covering 30-60% of the body--moderately contaminated; oil covering less than 30% of the body or light sheen on fur--lightly contaminated. If there was no oil visible, otters were considered uncontaminated. Tissues from 51 oil-contaminated sea otters (14 males, 37 females) and from six uncontaminated sea otters (three males, three females) that died in rehabilitation centers were examined histologically. Among oil-contaminated sea otters, 19/46 had interstitial pulmonary emphysema, 13/40 had gastric erosion and hemorrhage, 11/47 had centrilobular hepatic necrosis, 14/47 had periportal to diffuse hepatic lipidosis, and 10/42 had renal tubular lipidosis. Of the uncontaminated sea otters, 1/6 had gastric erosion and hemorrhage and 1/6 had diffuse hepatic lipidosis. Histologic examinations were performed on tissues from five sea otters (three males, two females) found dead with external oil present 15 to 16 days after the spill. Periportal hepatic lipidosis and renal tubular lipidosis were found in 3/5, and interstitial pulmonary emphysema was found in 1/5. Tissues from six apparently normal sea otters (four males, two females) collected from an area not affected by an oil spill were examined histologically, and none of these lesions were found. We conclude that interstitial pulmonary emphysema, centrilobular hepatic necrosis, and hepatic and renal lipidosis of sea otters were associated with exposure to crude oil. Gastric erosion and hemorrhage may have been associated with stress of captivity and/or oil exposure.

Animals↗

Biomarker responses in river otters experimentally exposed to oil contamination.

Investigations in Prince William Sound (Alaska, USA) following the Exxon Valdez oil spill (EVOS) revealed that river otters (Lontra canadensis) on oiled shores had lower body mass and elevated values of biomarkers, than did otters living on nonoiled shores. In addition, otters from oiled areas selected different habitats, had larger home ranges, and less diverse diets than animals living in nonoiled areas. These differences between river otters from oiled shores and those from nonoiled areas strongly suggested that oil contamination had an effect on physiological and behavioral responses of otters. In this study, we explored the effects of crude oil contamination on river otters experimentally. We hypothesized that exposure to oil would result in elevated values of biomarkers, indicating induced physiological stress. Fifteen wild-caught male river otters were exposed to two levels of weathered crude oil (i.e., control, 5 ppm/day/kg body mass, and 50 ppm/day/kg body mass) under controlled conditions in captivity at the Alaska Sealife Center in Seward (Alaska, USA). Responses of captive river otters to oil ingestion provided mixed results in relation to our hypotheses. Although hemoglobin (Hb, and associated red blood cells) and white blood cells, and possibly interleukin-6 immunoreactive responded in the expected manner, other parameters did not. Aspartate aminotransferase, alanine aminotransferase, and haptoglobin (Hp), did not increase in response to oiling or decreased during rehabilitation. Conversely, principle-component analysis identified values of alkaline phosphatase as responding to oil ingestion in river otters. Our results suggested that opposing processes were concurring in the oiled otters. Elevated production of Hp in response to tissue damage by hydrocarbons likely occurred at the same time with increased removal of Hp-Hb complex from the serum, producing an undetermined pattern in the secretion of Hp. Thus, the use of individual biomarkers as indicators of exposure to pollutants may lead to erroneous conclusions because interactions in vivo can be complicated and act in opposite directions. Additionally, the biomarkers used in investigating effects of oiling on live animals usually are related to the heme molecule. Because of the opposing processes that may occur within an animal, data from a suite of heme-related biomarkers may produce results that are difficult to interpret. Therefore, we advocate the exploration and development of other biomarkers that will be independent from the heme cycle and provide additional information to the effect of oiling on live mammals.

Alaska↗

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 naïveté of both populations to other pathogens (e.g., morbillivirus and Coccidiodes immitis) may have important implications for their management and recovery.

Age Factors↗

Postanesthetic monitoring of core body temperature using telemetry in North American river otters (Lutra canadensis).

Remote thermal telemetry was performed on North American river otters (Lutra canadensis) during the 1995 North Carolina Wildlife Resources Commission Otter Restoration Project. Otters were anesthetized with either ketamine-midazolam (n = 11) or tiletamine-zolazepam (n = 9) combinations. Based upon initial rectal temperatures, mild to moderate hyperthermia (39.4-40.5 degrees C) developed in five otters given ketamine-midazolam and three otters given tiletamine-zolazepam. Following anesthetic induction, each otter received an ingestible temperature transmitter. Dependent upon gastrointestinal transit time and transmitter battery life, core body temperature was monitored for up to 13.75 hr postanesthesia. Thermal telemetry revealed a gradual decline in core temperature in all otters after anesthetic recovery (30-60 min). Median core temperature stabilized subsequently within 0.3 degrees C of resting temperature (38.4 degrees C) 1.75 hr after initial injection in otters given tiletamine-zolazepam and 2.75 hr in otters given ketamine-midazolam. Minor fluctuations in body temperature (less than 1 degree C) occurred in most otters from 6 to 13.75 hr and were attributed to variations in physical activity.

Anesthesia Recovery Period↗