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The genetic consequences of species-wide declines are rarely quantified because the timing and extent of the decline varies across the species' range. The sea otter (Enhydra lutris) is a unique model in this regard. Their dramatic decline from thousands to fewer than 100 individuals per population occurred range-wide and nearly simultaneously due to the 18th-19th century fur trade. Consequently, each sea otter population represents an independent natural experiment of recovery after extreme population decline. We designed sequence capture probes for 50 Mb of sea otter exonic and neutral genomic regions. We sequenced 107 sea otters from five populations that span the species range to high coverage (18-76×) and three historical Californian samples from ~1500 and ~200 years ago to low coverage (1.5-3.5×). We observe distinct population structure and find that sea otters in California are the last survivors of a divergent lineage isolated for thousands of years and therefore warrant special conservation concern. We detect signals of extreme population decline in every surviving sea otter population and use this demographic history to design forward-in-time simulations of coding sequence. Our simulations indicate that this decline could lower the fitness of recovering populations for generations. However, the simulations also demonstrate how historically low effective population sizes prior to the fur trade may have mitigated the effects of population decline on genetic health. Our comprehensive approach shows how demographic inference from genomic data, coupled with simulations, allows assessment of extinction risk and different models of recovery.
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Lontras , Humanos , Animais , Lontras/genética , Densidade Demográfica , GenômicaRESUMO
Sea otters are apex predators that can exert considerable influence over the nearshore communities they occupy. Since facing near extinction in the early 1900s, sea otters are making a remarkable recovery in Southeast Alaska, particularly in Glacier Bay, the largest protected tidewater glacier fjord in the world. The expansion of sea otters across Glacier Bay offers both a challenge to monitoring and stewardship and an unprecedented opportunity to study the top-down effect of a novel apex predator across a diverse and productive ecosystem. Our goal was to integrate monitoring data across trophic levels, space, and time to quantify and map the predator-prey interaction between sea otters and butter clams Saxidomus gigantea, one of the dominant large bivalves in Glacier Bay and a favoured prey of sea otters. We developed a spatially-referenced mechanistic differential equation model of butter clam dynamics that combined both environmental drivers of local population growth and estimates of otter abundance from aerial survey data. We embedded this model in a Bayesian statistical framework and fit it to clam survey data from 43 intertidal and subtidal sites across Glacier Bay. Prior to substantial sea otter expansion, we found that butter clam density was structured by an environmental gradient driven by distance from glacier (represented by latitude) and a quadratic effect of current speed. Estimates of sea otter attack rate revealed spatial heterogeneity in sea otter impacts and a negative relationship with local shoreline complexity. Sea otter exploitation of productive butter clam habitat substantially reduced the abundance and altered the distribution of butter clams across Glacier Bay, with potential cascading consequences for nearshore community structure and function. Spatial variation in estimated sea otter predation processes further suggests that community context and local environmental conditions mediate the top-down influence of sea otters on a given prey. Overall, our framework provides high-resolution insights about the interaction among components of this food web and could be applied to a variety of other systems involving invasive species, epidemiology or migration.
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Bivalves , Lontras , Animais , Ecossistema , Teorema de Bayes , Cadeia AlimentarRESUMO
Acanthocephalans are common intestinal parasites of marine mammals, the most widespread of which is the genus Corynosoma. In this study, parasite infrapopulations of two closely related species of Corynosoma were examined: Corynosoma enhydri from sea otters (Enhydra lutris) in Alaska (n = 12) and California (n = 19), and Corynosoma strumosum from seals in Germany (n = 22). Prevalence of C. enhydri was 100% in Californian otters, with a mean abundance of 30, and 83% in Alaskan otters, with a mean abundance of 232. In seals, C. strumosum had a prevalence of 65%, with a mean abundance of 33. Female C. enhydri dominated both Californian (82%) and Alaskan (79%) infections, while, in seals, female C. strumosum made up 68% of the parasite population. Reproduction rates for C. enhydri, with 16% (California) and 18% (Alaska) of females mated, were low compared to C. strumosum in seals, of which 40% of females were mated. Habitat selection also differed significantly between the two species. Corynosoma enhydri was found most frequently in the second and third fifths of the small intestine, while C. strumosum was found most frequently in the fourth. The differences in habitat selection and prevalence analysed in this study may be related to a trade-off between growth and reproduction between the two species.
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Acantocéfalos , Ecossistema , Helmintíase Animal , Intestinos/parasitologia , Lontras , Focas Verdadeiras/parasitologia , Alaska , Animais , Feminino , Alemanha , Lontras/parasitologiaRESUMO
Five Mycoplasma strains have been isolated from the oropharynx of southern sea otters (Enhydra lutris nereis) from the Central California Coast, USA. These strains were phenotypically and genetically characterized and compared to other established Mycoplasma species. All five strains hydrolysed arginine but not urea, but did not produce acid from glucose, and all were isolated and propagated under anaerobic and aerobic atmospheric conditions at +35-37 ËC using either SP4 or PPLO medium supplemented with arginine. Colonies on solid medium showed a typical fried-egg appearance and transmission electron microscopy revealed a typical mycoplasma cellular morphology. Molecular characterization included assessment of the following genetic loci: 16S rRNA, 16S-23S rRNA ITS, rpoB, rpoC, polC, topIIA, tufB, arcA and smc. Complete 16S rRNA gene sequence analysis indicated that these strains were most closely related to M.ycoplasma phocicerebrale, and to M.ycoplasma arginini, M.ycoplasma gateae and M.ycoplasma canadense with nucleotide similarities of 99 and 98â%, respectively. Nucleotide analysis of other genetic loci revealed 73-91â% nucleotide similarity to the corresponding genes of the above closely related species. All five strains clustered into a distinct group on the 16S rRNA and rpoB phylogenetic trees. Serological testing via growth inhibition and metabolic inhibition tests employing antiserum to type strains of M. phocicerebrale, M. arginini, M. gateae and M. canadense failed to recognize these novel strains. Our results suggest that the strains isolated from southern sea otters represent a novel species of the genus Mycoplasma, for which the name Mycoplasma enhydrae sp. nov. is proposed; the type strain is 6243-11T (=DSM 106704T=ATCC TSD-140T).
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Mycoplasma/classificação , Lontras/microbiologia , Faringe/microbiologia , Filogenia , Animais , Técnicas de Tipagem Bacteriana , Composição de Bases , California , DNA Bacteriano/genética , Genes Bacterianos , Mycoplasma/isolamento & purificação , RNA Ribossômico 16S/genética , Análise de Sequência de DNARESUMO
Population dynamics vary in space and time. Survey designs that ignore these dynamics may be inefficient and fail to capture essential spatio-temporal variability of a process. Alternatively, dynamic survey designs explicitly incorporate knowledge of ecological processes, the associated uncertainty in those processes, and can be optimized with respect to monitoring objectives. We describe a cohesive framework for monitoring a spreading population that explicitly links animal movement models with survey design and monitoring objectives. We apply the framework to develop an optimal survey design for sea otters in Glacier Bay. Sea otters were first detected in Glacier Bay in 1988 and have since increased in both abundance and distribution; abundance estimates increased from 5 otters to >5,000 otters, and they have spread faster than 2.7 km/yr. By explicitly linking animal movement models and survey design, we are able to reduce uncertainty associated with forecasting occupancy, abundance, and distribution compared to other potential random designs. The framework we describe is general, and we outline steps to applying it to novel systems and taxa.
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Ecologia , Lontras , Animais , Dinâmica PopulacionalRESUMO
The recovery of predators has the potential to restore ecosystems and fundamentally alter the services they provide. One iconic example of this is keystone predation by sea otters in the Northeast Pacific. Here, we combine spatial time series of sea otter abundance, canopy kelp area, and benthic invertebrate abundance from Washington State, USA, to examine the shifting consequences of sea otter reintroduction for kelp and kelp forest communities. We leverage the spatial variation in sea otter recovery to understand connections between sea otters and the kelp forest community. Sea otter increases created a pronounced decline in sea otter prey-particularly kelp-grazing sea urchins-and led to an expansion of canopy kelps from the late 1980s until roughly 2000. However, while sea otter and kelp population growth rates were positively correlated prior to 2002, this association disappeared over the last two decades. This disconnect occurred despite surveys showing that sea otter prey have continued to decline. Kelp area trends are decoupled from both sea otter and benthic invertebrate abundance at current densities. Variability in kelp abundance has declined in the most recent 15 years, as it has the synchrony in kelp abundance among sites. Together, these findings suggest that initial nearshore community responses to sea otter population expansion follow predictably from trophic cascade theory, but now, other factors may be as or more important in influencing community dynamics. Thus, the utility of sea otter predation in ecosystem restoration must be considered within the context of complex and shifting environmental conditions.
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Kelp , Lontras , Animais , Ecossistema , Cadeia Alimentar , Florestas , WashingtonRESUMO
Ecological invasions and colonizations occur dynamically through space and time. Estimating the distribution and abundance of colonizing species is critical for efficient management or conservation. We describe a statistical framework for simultaneously estimating spatiotemporal occupancy and abundance dynamics of a colonizing species. Our method accounts for several issues that are common when modeling spatiotemporal ecological data including multiple levels of detection probability, multiple data sources, and computational limitations that occur when making fine-scale inference over a large spatiotemporal domain. We apply the model to estimate the colonization dynamics of sea otters (Enhydra lutris) in Glacier Bay, in southeastern Alaska.
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Modelos Teóricos , Lontras/fisiologia , Animais , Ecologia , Ecossistema , Dinâmica PopulacionalRESUMO
Sarcocystis neurona is a terrestrial parasite that can cause fatal encephalitis in the endangered Southern sea otter (Enhydra lutris nereis). To date, neither risk factors associated with marine contamination nor the route of S. neurona infection to marine mammals has been described. This study evaluated coastal S. neurona contamination using California mussels (Mytilus californianus) as sentinels for pathogen pollution. A field investigation was designed to test the hypotheses that (1) mussels can serve as sentinels for S. neurona contamination, and (2) S. neurona contamination in mussels would be highest during the rainy season and in mussels collected near freshwater. Initial validation of molecular assays through sporocyst spiking experiments revealed the ITS-1500 assay to be most sensitive for detection of S. neurona, consistently yielding parasite amplification at concentrations ⩾5 sporocysts/1 mL mussel haemolymph. Assays were then applied on 959 wild-caught mussels, with detection of S. neurona confirmed using sequence analysis in three mussels. Validated molecular assays for S. neurona detection in mussels provide a novel toolset for investigating marine contamination with this parasite, while confirmation of S. neurona in wild mussels suggests that uptake by invertebrates may serve as a route of transmission to susceptible marine animals.
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Monitoramento Ambiental/métodos , Mytilus/parasitologia , Sarcocystis/fisiologia , Espécies Sentinelas/parasitologia , Animais , California , Reprodutibilidade dos Testes , Estações do Ano , Sensibilidade e EspecificidadeRESUMO
Mycobacterium avium subsp. avium is pathogenic mainly to birds, although cases of mycobacteriosis caused by these bacteria have also been reported in other animals and humans. Not much is known about the effects of this pathogen on otters. The aim of this study was to report for the first time the isolation of M. avium subsp. avium in wild otter and to describe its multidrug resistance profile. A female otter injured in a car accident was found dead and subjected to postmortem examination. Apart from the trauma changes, no other macroscopic pathological changes were detected. Bacteriologic examination revealed the presence of acid-fast bacilli in the lymph nodes, which were confirmed by molecular methods as M. avium subsp. avium. Antimicrobial susceptibility testing revealed susceptibility to clarithromycin and amikacin, but resistance to linezolid, moxifloxacin, streptomycin, isoniazid, trimethoprim/sulfamethoxazole, ciprofloxacin, doxycycline, and ethionamide. This is unusual for wild species, which generally should not come into contact with antimicrobials, and may suggest that multidrug-resistant MAC strains are circulating between wild and domestic animals. These results emphasise the need for additional epidemiological studies on non-tuberculous mycobacteria in wildlife and their implications for one health.
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Characterizing the genetic mechanisms underlying Alzheimer's disease (AD) dementia is crucial for developing new therapeutics. Proteome-wide association study (PWAS) integrating proteomics data with genome-wide association study (GWAS) summary data was shown as a powerful tool for detecting risk genes. The identified PWAS risk genes can be interpretated as having genetic effects mediated through the genetically regulated protein abundances. Existing PWAS analyses of AD often rely on the availability of individual-level proteomics and genetics data of a reference cohort. Leveraging summary-level protein quantitative trait loci (pQTL) reference data of multiple relevant tissues is expected to improve PWAS findings for studying AD. Here, we applied our recently developed OTTERS tool to conduct PWAS of AD dementia, by leveraging summary-level pQTL data of brain, cerebrospinal fluid (CSF), and plasma tissues, and multiple statistical methods. For each target protein, imputation models of the protein abundance with genetic predictors were trained from summary-level pQTL data, estimating a set of pQTL weights for considered genetic predictors. PWAS p-values were obtained by integrating GWAS summary data of AD dementia with estimated pQTL weights. PWAS p-values from multiple statistical methods were combined by the aggregated Cauchy association test to yield one omnibus PWAS p-value for the target protein. We identified significant PWAS risk genes through omnibus PWAS p-values and analyzed their protein-protein interactions using STRING. Their potential causal effects were assessed by the probabilistic Mendelian randomization (PMR-Egger). As a result, we identified a total of 23 significant PWAS risk genes for AD dementia in brain, CSF, and plasma tissues, including 7 novel findings. We showed that 15 of these risk genes were interconnected within a protein-protein interaction network involving the well-known AD risk gene of APOE and 5 novel findings, and enriched in immune functions and lipids pathways including positive regulation of immune system process, positive regulation of macrophage proliferation, humoral immune response, and high-density lipoprotein particle clearance. Existing biological evidence was found to relate our novel findings with AD. We validated the mediated causal effects of 14 risk genes (60.8%). In conclusion, we identified both known and novel PWAS risk genes, providing novel insights into the genetic mechanisms in brain, CSF, and plasma tissues, and targeted therapeutics development of AD dementia. Our study also demonstrated the effectiveness of integrating public available summary-level pQTL data with GWAS summary data for mapping risk genes of complex human diseases.
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Monitoring reproductive physiology in wildlife can be a useful tool for assessing population dynamics for conservation and management purposes. Utilizing non-invasive approaches for this, such as quantifying reproductive hormone metabolites from faeces, can be challenging when defaecation events are not observed, or when cryptic species like African clawless otters (Aonyx capensis) are involved. Additionally, test systems for quantifying hormone metabolites in a species for the first time must first be reliably validated prior to use. Our results indicate that Epiandrosterone and Progesterone EIAs are most suitable for determining fAM and fPM concentrations in African clawless otter spraints. The fAM:fPM ratio and respective thresholds are more reliable in sex identification compared to the separate use of individual hormone classes. Sex-related hormone metabolite concentrations remained comparable for up to 12hrs post-defaecation in both sexes.â¢We screened two androgen and two progestagen enzyme-immunoassays (EIAs) for suitability and reliable quantification of faecal androgen metabolites (fAM) and faecal progestagen metabolites (fPM) in African clawless otters.â¢We assessed whether the ratio of fAM:fPM concentrations can be used to assign sex to faecal samples from unknown individuals.â¢We tested the stability of fAM and fPM concentrations post-defaecation to determine the effects of environmental exposure and bacterial metabolism.
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Captive animal welfare research focuses on husbandry, enrichment, enclosure space, visitor effects, and opportunities for species-typical behavior (e.g., foraging, territoriality, and social interaction). And yet, one of the most biologically relevant opportunities for species-typical behavior, parenting, has received little attention. The goal of this longitudinal investigation was to explore the differential variability of repetitive behavior across three parenting conditions (i.e., No parenting, parenting, and foster parenting) among captive, wild-rescued, North American river otters. This study represents anatural ABAC design, the conditions reflect differential parenting phases: No parenting (A), Parenting biological pups (B), and Alloparenting nonbiological pups (C). The behavior of two adult North American river otters at the Oregon Zoo were observed from April2016 through March2020 during the different parenting contexts. The frequency of repetitive behaviors was lowest during parenting and highest during the non-parenting conditions. Although data for season, weather, and visitor variables were also collected throughout this study; parenting condition was the only consistent moderator of abnormal repetitive behavior observed.
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Lontras , Animais , Estudos LongitudinaisRESUMO
The Asian small-clawed otter (Aonyx cinereus) is an endangered species that is common in zoologic collections. A 17-y-old female Asian small-clawed otter under human care, with a clinical history of chronic renal disease, was euthanized because of deteriorating health. Histologically, the jejunal wall was infiltrated by a monomorphic population of small neoplastic lymphocytes that expanded the lamina propria of the villi and crypts, and on rare occasions invaded the submucosa. The tumor was composed of T cells (CD3+) with a proliferation index of 16%. Based on the World Health Organization (WHO) Classification of Hematopoietic Neoplasms in Domestic Animals, this lymphoma was classified as an enteropathy-associated T-cell lymphoma (EATL) type 2. We also present here a review of the literature on intestinal lymphoma in the subfamily Lutrinae (otters).
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Linfoma de Células T Associado a Enteropatia , Lontras , Animais , Feminino , Linfoma de Células T Associado a Enteropatia/veterináriaRESUMO
With climate, biodiversity and inequity crises squarely upon us, never has there been a more pressing time to rethink how we conceptualize, understand and manage our relationship with Earth's biodiversity. Here, we describe governance principles of 17 Indigenous Nations from the Northwest Coast of North America used to understand and steward relationships among all components of nature, including humans. We then chart the colonial origins of biodiversity science and use the complex case of sea otter recovery to illuminate how ancestral governance principles can be mobilized to characterize, manage and restore biodiversity in more inclusive, integrative and equitable ways. To enhance environmental sustainability, resilience and social justice amid today's crises, we need to broaden who benefits from and participates in the sciences of biodiversity by expanding the values and methodologies that shape such initiatives. In practice, biodiversity conservation and natural resource management need to shift from centralized, siloed approaches to those that can accommodate plurality in values, objectives, governance systems, legal traditions and ways of knowing. In doing so, developing solutions to our planetary crises becomes a shared responsibility. This article is part of the theme issue 'Detecting and attributing the causes of biodiversity change: needs, gaps and solutions'.
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Biodiversidade , Justiça Social , Humanos , América do Norte , Clima , Conservação dos Recursos Naturais , EcossistemaRESUMO
The historic extirpation and subsequent recovery of sea otters (Enhydra lutris) have profoundly changed coastal social-ecological systems across the northeastern Pacific. Today, the conservation status of sea otters is informed by estimates of population carrying capacity or growth rates independent of human impacts. However, archaeological and ethnographic evidence suggests that for millennia, complex hunting and management protocols by Indigenous communities limited sea otter abundance near human settlements to reduce the negative impacts of this keystone predator on shared shellfish prey. To assess relative sea otter prevalence in the Holocene, we compared the size structure of ancient California mussels (Mytilus californianus) from six archaeological sites in two regions on the Pacific Northwest Coast, to modern California mussels at locations with and without sea otters. We also quantified modern mussel size distributions from eight locations on the Central Coast of British Columbia, Canada, varying in sea otter occupation time. Comparisons of mussel size spectra revealed that ancient mussel size distributions are consistently more similar to modern size distributions at locations with a prolonged absence of sea otters. This indicates that late Holocene sea otters were maintained well below carrying capacity near human settlements as a result of human intervention. These findings illuminate the conditions under which sea otters and humans persisted over millennia prior to the Pacific maritime fur trade and raise important questions about contemporary conservation objectives for an iconic marine mammal and the social-ecological system in which it is embedded. Supplementary Information: The online version contains supplementary material available at 10.1007/s10021-021-00671-3.
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Smooth-coated otters (Lutrogale perspicillata) and Malayan water monitor lizards (Varanus salvator) occupy similar habitats and interact regularly in Singapore's waterways. These interactions have a range of potential outcomes and are sometimes lethal. Few formal behavioral studies exist for either species. We analyzed interactions between otters and monitor lizards by gleaning data from publicly available videos from citizen scientists to examine what factors influence aggressive and defensive behaviors and what influences vigilance in otters. Behavioral sequence analysis revealed no obvious monitor lizard behavior that predicted otter aggression toward monitors. We found that the presence and number of otter pups are positively associated with otter aggression. Otters also tended to be more vigilant in groups with more pups and more vigilant on land than water. Monitor lizards almost always displayed aggressive and defensive behaviors, regardless of whether otters were aggressive toward the lizards. These observations suggest that otters vary their aggression and vigilance levels depending on their group composition and the physical environment of their interactions with monitor lizards.
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Foraging plays a vital role in animal life histories, and learning whether unfamiliar food items are palatable is a key part of this process. Animals that engage in extractive foraging must also learn how to overcome the protective measures of their prey. While otters (subfamily Lutrinae) are a taxon known for their extractive foraging behaviour, how they learn about prey palatability and acquire extractive foraging techniques remains poorly understood. Here we investigated (i) how captive Asian short-clawed otters (Aonyx cinereus) learned to interact with, and extract meat from, unfamiliar natural prey and (ii) how their exploitation of such prey compared to their ability to overcome artificial foraging tasks containing familiar food rewards. Network-based diffusion analysis showed that otters learned to interact with unfamiliar natural prey by observing their group mates. However, once interacting with the prey, they learned to extract the meat mainly asocially. In addition, otters took longer to overcome the protective measures of unfamiliar natural prey than those of extractive food puzzles. Asian short-clawed otter populations are declining in the wild. Increasing our understanding of how they learn to overcome novel foraging challenges could help develop pre-release training procedures as part of reintroduction programmes for otter conservation.
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E. coli was isolated from the Salish Sea (Puget Sound) ecosystem, including samples of marine and fresh water, and wildlife dependent on this environment. E. coli isolates were assessed for phenotypic and genotypic resistance to antibiotics. A total of 305 E. coli isolates was characterized from samples collected from: marine water obtained in four quadrants of the Salish Sea; select locations near beaches; fresh water from streams near marine beaches; and fecal samples from harbor porpoises (Phocoena phocoena), harbor seals (Phoca vitulina), river otters (Lontra canadensis), and English sole (Parophrys vetulus). Isolates were evaluated using antimicrobial susceptibility typing, whole-genome sequencing, fumC, and multilocus sequence typing. Resistance and virulence genes were identified from sequence data. Of the 305 isolates from Salish Sea samples, 20 (6.6%) of the E. coli were intermediate, and 31 (10.2%) were resistant to ≥1 class of antibiotics, with 26.9% of nonsusceptible (resistant and intermediate resistant) E. coli isolates from marine mammals and 70% from river otters. The proportion of nonsusceptible isolates from animals was significantly higher than samples taken from marine water (p < 0.0001). A total of 196 unique STs was identified including 37 extraintestinal pathogenic E. coli (ExPEC)-associated STs [ST10, ST38, ST58, ST69, ST73, ST117, ST131, and ST405]. The study suggests that animals may be potential sentinels for antibiotic-resistant and ExPEC E. coli in the Salish Sea ecosystem.
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Southeast Alaska sea otters (Enhydra lutris) have had a rapid rise in their population. As they feed primarily on sessile prey, they are excellent sentinels for examining metals contamination. Objectives of this study on sea otters were to determine: (1) concentrations of metals in different tissues; (2) whether metals biomagnify from stomach contents (i.e., the prey) to other tissues; (3) whether selenium and mercury concentrations indicate an overall health benefit or risk; and (4) if metals concentrations in tissues vary with body size. Brain, kidney, gonad, liver, and stomach contents were collected from freshly harvested sea otters in Icy Strait, Alaska, and analyzed for arsenic (As), cadmium (Cd), copper (Cu), lead (Pb), total mercury (THg), and selenium (Se). Metals concentrations varied significantly, and some were biomagnified, with livers and kidneys harboring the highest concentrations. Lead and arsenic appeared to be readily excreted. This study represents baseline metals concentrations to assist in monitoring the health of sea otters.
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Lontras , Alaska , Animais , Encéfalo , Conteúdo Gastrointestinal , Gônadas , Rim , FígadoRESUMO
Object play refers to the seemingly non-functional manipulation of inanimate items when in a relaxed state. In juveniles, object play may help develop skills to aid survival. However, why adults show object play remains poorly understood. We studied potential drivers and functions of the well-known object play behaviour of rock juggling in Asian small-clawed (Aonyx cinereus) and smooth-coated (Lutrogale perspicillata) otters. These are closely related species, but Asian small-clawed otters perform extractive foraging movements to exploit crabs and shellfish while smooth-coated otters forage on fish. We thus predicted that frequent rock jugglers might be better at solving extractive foraging puzzles in the first species, but not the latter. We also assessed whether species, age, sex and hunger correlated with rock juggling frequency. We found that juvenile and senior otters juggled more than adults. However, rock juggling frequency did not differ between species or sexes. Otters juggled more when 'hungry', but frequent jugglers did not solve food puzzles faster. Our results suggest that rock juggling may be a misdirected behaviour when hungry and may facilitate juveniles' motor development, but it appears unrelated to foraging skills. We suggest future studies to reveal the ontogeny, evolution and welfare implications of this object play behaviour.