Disease in wildlife or exotic speciesThe Dental Pathology of Southern Sea Otters (Enhydra lutris nereis)
Introduction
The sea otter (Enhydra lutris) ranks second largest amongst members of the family Mustelidae and second smallest amongst marine mammal species. Southern sea otters (E. lutris nereis) average 129.1 cm (males) and 119.8 cm (females) in length, and the corresponding predicted average weights of healthy animals are 29.0 kg and 19.8 kg (Riedman and Estes, 1990). Their current range includes the Pacific coast of central California (US Fish and Wildlife Service, California, 2008), while historically their range stretched from Baja California, Mexico, to Alaska (Riedman and Estes, 1990). Throughout the 18th and 19th centuries, the Pacific maritime fur trade reduced the population from 300,000 to a pocket of at least 32 individuals in the early 1900s (Kenyon, 1969). Despite protection afforded by the International Fur Seal Treaty of 1911, the recovery of the subspecies has not been as robust as sympatric marine mammal species (Kreuder et al., 2003). The southern sea otter was listed as threatened in 1977 under the US Endangered Species Act due to small population size, limited distribution, slow growth rate and vulnerability to oil spills (Estes et al., 2003).
The adult southern sea otter has 32 teeth (Fig. 1), with a dental formula of I3/2, C1/1, P3/3, M1/2 (Kenyon, 1969). Sea otter dentition varies from most other carnivores, as they have only two mandibular incisors and lack maxillary and mandibular first premolar teeth. Additionally, they lack the typical carnassial premolar and molar teeth of most carnivores; shearing functionality has been replaced by a crushing dentition characterized by bunodont molar teeth (Riedman and Estes, 1990). The dome-like teeth of sea otters dissipate tensile stresses produced by high occlusal forces, which are necessary to masticate hard food items (Constantino et al., 2011). The maxillary first molar tooth is the largest tooth, providing a broad, flat surface against which mandibular first and second molar teeth can crush prey items (Riley, 1985).
Sea otter prey includes 60 different macroinvertebrate species (Russell, 2003), such as clams, mussels, abalone, snails, crabs and sea urchins (Murie, 1940). Prey preferences vary across populations, but all sea otters appear to include hard foods in their diets (Estes et al., 2003). While it has been noted that sea otters are amongst the few non-human species known to utilize tools while foraging (Fisher, 1939; Riedman and Estes, 1990), the majority of shelled prey are chewed whole (Kenyon, 1969). In consuming sea urchins, sea otters chew through part of the sea urchin's masticatory apparatus known as Aristotle's lantern, one of the hardest natural biogenic composites (Constantino et al., 2011).
The integrity and functionality of sea otter dentition is an integral component of their overall health. Sea otters have an extremely high dietary energy requirement; this is necessary to regulate body temperature since sea otters lack an insulating blubber layer typical of other marine mammal species (Costa and Kooyman, 1982). They produce heat at 2.4–3.2 times the rate of comparably sized terrestrial mammals (Costa and Kooyman, 1982; Riedman and Estes, 1990). To fuel these metabolic needs, captive adult sea otters consume 189–253 kcal/kg body weight/24 h, equating to 20–25% of their total body weight (Kenyon, 1969). A 20 kg adult otter in captivity would therefore require between 4,295 and 5,750 kcal per day. Free-ranging sea otters have even higher metabolic energy requirements; they consume the equivalent of 23–33% of their body weight (Riedman and Estes, 1990).
Knowledge of variation in dentition is an essential area of zoological research (Miyazaki, 2002); however, little is known about dental pathology in wild animals in general and marine mammals in particular (Gulland et al., 2001; Cowan, 2002; Abbott and Verstraete, 2005). Dental lesions, which are common in certain populations of wild animals, may be important contributors to morbidity and mortality (Verstraete et al., 1996a, b). A greater knowledge of oral pathology may augment our understanding of behavioural and feeding habits of animals in their natural habitat.
Museum collections of skulls, such as those that make up this study, are obtained from strandings, carcass recovery and donations by rehabilitation centres. The causes of death in stranded sea otters include trauma (shark bites) and disease (both infections and non-infectious) (Kreuder et al., 2003). Pathological conditions are likely over represented in stranded animals as compared with the general population (Cowan, 2002), and high numbers of stranded animals may be considered sentinels of emerging diseases (Gulland, 1999). The aim of this study was to determine the nature and prevalence of dental pathology in southern sea otters by examining museum specimen skulls.
Section snippets
Materials and Methods
Macroscopic examination of 1,205 skull specimens from the Department of Ornithology and Mammalogy, California Academy of Sciences, San Francisco, was performed. Each skull had been previously labelled with a unique catalogue number and details of sex, collection location and collection date. ‘Young adult’ versus ‘adult’ categorization was determined based on long bone physes, or prominence of cranial sutures when long bones were unavailable. ‘Juvenile’ ageing was based on the presence of
Results
Of the 1,205 skulls in the study, 54.0% were from male animals, 44.7% were from female animals and 1.3% were from animals of unknown sex. Adult, young adult and juvenile skulls comprised 61.2%, 22.5% and 16.3% of the total, respectively. Fig. 2 illustrates the age and sex distribution of the skulls examined. Juvenile skulls were omitted from dental pathology analysis, reducing the total number of specimens to 1,008.
Discussion
The California Academy of Sciences houses the largest collection of southern sea otter specimens worldwide. The collection date of skulls ranged from 1896 to 2011 and all were in relatively similar good condition, regardless of age. Some teeth possessed hairline cracks, artifactual sharp-edged fractures and flaked off enamel due to excessive heating and drying during skull preparation; however, these defects were overlooked and did not obscure true pathology. Teeth were assumed to have been
Acknowledgements
The authors would like to thank M. Flannery of the Department of Ornithology and Mammalogy of the California Academy of Sciences for making its Enhydra skull collection available for this study, and J. Doval for specimen photography. This research was funded by the UC Davis School of Veterinary Medicine Students Training in Advanced Research (STAR) Program, which had no role in the study design, in the collection, analysis and interpretation of data, in the writing of the manuscript, or in the
References (32)
- et al.
The dental pathology of northern elephant seals (Mirounga angustirostris)
Journal of Comparative Pathology
(2005) - et al.
Adaptation to hard-object feeding in sea otters and hominins
Journal of Human Evolution
(2011) - et al.
Somatic and skeletally fixed carotenoids of the purple hydrocoral, Allopora californica
Comparative Biochemistry and Physiology
(1970) - et al.
Predicting failure in mammalian enamel
Journal of the Mechanical Behavior of Biomedical Materials
(2009) - et al.
The dental pathology of feral cats on Marion Island. Part I: congenital, developmental and traumatic abnormalities
Journal of Comparative Pathology
(1996) - et al.
The dental pathology of feral cats on Marion Island. Part II: periodontitis, external odontoclastic resorption lesions and mandibular thickening
Journal of Comparative Pathology
(1996) Supernumerary incisors in Mustelids
Mammal Review
(1970)- et al.
Territoriality and mating behavior in Prince William Sound sea otters
Journal of Mammalogy
(1975) - et al.
Oxygen consumption, thermoregulation, and the effect of fur oiling and washing on the sea otter, Enhydra lutris
Canadian Journal of Zoology
(1982) Pathology
Causes of mortality in California sea otters during periods of population growth and decline
Marine Mammal Science
Habits of the southern sea otter
Journal of Mammalogy
Notes on the teeth of the sea otter
Journal of Mammalogy
Nose scars in female sea otters
Journal of Mammalogy
Chromatology of animal skeletons: wide and diversified color manifestations arise in animal skeletons from either microstructurally induced chromogenesis or the presence of true pigments
American Scientist
Stranded seals: important sentinels
Journal of the American Veterinary Medical Association
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