Coccidioidomycosis in a California sea lion (Zalophus californianus)

Coccidioidomycosis in an adult male California sea lion (Zalophus californianus) is described. The animal was housed in a zoo in Tucson, Arizona, for approximately 5 years. This is believed to be the first reported case of coccidioidomycosis in a marine mammal.     

Foreflipper propulsion in the California sea lion, Zalophus californianus

The family Otariidae comprises the only group of marine mammals that habitually use their pectoral appendages to generate propulsive forces during swimming. This method of propulsion was examined in the California sea lion ( Zalophus californianus ), a representative member of the family. High-speed films were taken as a sea lion swam against a water current generated inside a large flow channel. Thrust production was determined by examining the body's movement at various stages of the propulsive cycle. Sea lions generate thrust continuously throughout the stroke. Over its initial three-quarters, foreflippers act as hydrofoils creating forward thrust and lift as they move vertically through the water. Thrust production is greatest, however, near the end of the stroke, when flippers are used as paddles and are oriented broad side to the oncoming flow. The force generated by this three-phased system of propulsion is likely to be greater than that attainable by either an exclusively lift-based hydrofoil or drag-based paddling style of swimming.
The kinematic changes that enable sea lions to change speed were also investigated. Film records revealed that stroke amplitude became greater with speed, although total stroke duration remained essentially constant. Sea lions increase stroke frequency with velocity but large variations in the measured values suggest that changes in amplitude and flipper angle of attack are also important parameters for modulating swimming speed.     

Limb movements and locomotor function in the California sea lion (Zalophus californianus)

The peculiar amphibious mode of life of California sea lions suggests that their locomotor systems may contain adaptations both to life on land and in the water. Previous studies of their locomotor behaviour have been either superficial or based on inferences which were derived from limb structure. Limb movements associated with locomotor behaviour in California sea lions are described on the basis of frame-by-frame analysis of slow motion cinematography of typical aquatic and terrestrial locomotor sequences. Results are compared to reports of terrestrial and aquatic locomotor behaviour in fissiped carnivores, whose locomotor behaviour is presumed to reflect the framework from which the locomotor behaviour of sea lions was derived. The major distinction between sea lions and fissipeds in terms of aquatic locomotor behaviour involves the use of the forelimb in sea lions. Propulsive thrust is generated by medial rotation, adduction and retraction of the forelimbs in sea lions, in contrast to nearly pure limb retraction in fissipeds. The major features which distinguish terrestrial locomotor behaviour in sea lions from that of fissipeds are use of the manus as a transverse rather than sagittal propulsive lever and extensive use of posterior axial and head and neck movements rather than hindlimb movements. The biomechanical implications of these movements are used to elucidate their potentially adaptive features.     

Tactile size discrimination by a California sea lion (Zalophus californianus) using its mystacial vibrissae

The capability of a blindfolded California sea lion (Zalophus californianus) to discriminate diameter differences of circular discs by means of active touch with its mystacial vibrissae was studied. Using a forced choice paradigm the sea lion was required to choose the larger of two simultaneously presented perspex discs. Absolute difference thresholds (D) were determined for 3 standard discs (1.12 cm Ø, 2.52 cm Ø, 8.74 cm Ø) by the psychophysical method of constants. Increasing disc size resulted in an increase in the absolute difference threshold from 0.33 cm for the smallest disc size to 1.55 cm for the largest disc size. The relative difference threshold (Weber fraction) remained approximately constant at a mean value of 0.26. According to a video analysis the sea lion did not move its vibrissae when touching the discs. Instead, it performed precisely controlled lateral head movements, with the touched disc located centrally between the vibrissae of both sides of the muzzle. Since the extent of these head movements was identical at discs to be compared, discs of different size must have led to different degrees of deflection of vibrissae involved in the tactile process, resulting in quantitatively different mechanical stimulations of mechanoreceptors in the follicles. This suggests that the accuracy of the sea lion's size discrimination was determined by the efficiency of two sensory systems: the mechanosensitivity of follicle receptors as well as kinaesthesis.Abbreviations D starting stimulus size - D _i size of the interpolated comparison disc at 75% correct choices - D absolute difference threshold     

Antemortem diagnosis of a ventricular septal defect in a California sea lion Zalophus californianus

A yearling California sea lion Zalophus californianus stranded in poor body condition, and on physical examination a heart murmur was audible bilaterally. The sea lion was diagnosed with a left-to-right shunting membranous ventricular septal defect (VSD) using B-mode, color-flow Doppler and continuous-wave Doppler echocardiography. A left-to-right intracardiac shunting lesion was confirmed during cardiac angiographic computed tomography. The VSD defect was verified during the necropsy examination. On histologic examination concurrent mild multifocal myocarditis with focal mild ventricular free-wall myocardial necrosis were identified. A specific cause for the myocarditis and myocardial necrosis was not found, and association with the VSD and resultant myocardial dysfunction was presumed. This is the first report of the antemortem diagnosis of a VSD in a marine mammal and the first report of a VSD in a California sea lion.     

Pathology and preliminary characterization of a parapoxvirus isolated from a California sea lion (Zalophus californianus)

Cutaneous pox-like lesions are a common complication in the rehabilitation of pinnipeds. However, the exact identity, taxonomy, and host range of pinniped parapoxviruses remain unknown. During a poxvirus outbreak in May 2003 in California sea lions (Zalophus californianus) at a marine mammal rehabilitation facility, multiple raised, firm, 1-3-cm skin nodules from the head, neck, and thorax of one sea lion weanling pup that spontaneously died were collected. Histologically, the nodules were characterized by inflammation and necrosis of the dermis and epidermis, acanthosis, and ballooning degeneration of the stratum spinosum. Large, coalescing eosinophilic cytoplasmic inclusions were observed in the ballooned cells. A parapoxvirus (sea lion poxvirus 1, SLPV-1) was isolated on early passage California sea lion kidney cells inoculated with a tissue homogenate of a skin nodule. The morphology of the virions on electron microscopy was consistent with that of parapoxviruses. Partial sequencing of the genomic region encoding the putative major virion envelope antigen p42K confirmed the assignment of the sea lion poxvirus to the genus Parapoxvirus. Although SLPV-1 is most closely related to the poxvirus of harbor seals of the European North Sea, it is significantly different from orf virus, bovine papular stomatitis virus, pseudocowpox virus and the parapoxvirus of New Zealand red deer.     

Molecular characterization of expressed DQA and DQB genes in the California sea lion ( Zalophus californianus)

To date, there are no published MHC sequences from the California sea lion (Zalophus californianus), a thriving species that, by feeding high on the marine food web, could be a sentinel for disturbances in marine and coastal ecosystems. In this study, degenerate primers and RACE technology were used to amplify near-full-length (MhcZaca- DQB) and full-length (MhcZaca- DQA) expressed class II MHC gene products from the peripheral blood mononuclear cells of two California sea lions in rehabilitation. Five unique Zaca- DQA sequences and eight unique Zaca- DQB sequences, all encoding functional proteins, were identified in the two animals, indicating the presence of multiple DQ- loci in this species. An additional three Zaca- DQB sequences containing features compatible with pseudogenes or null alleles were also identified. Despite the identification of multiple DQA and DQB sequences, the degree of heterogeneity between them was extremely low. To confirm the limited degree of Zaca-DQ nucleotide variation between individuals, we used denaturing gradient gel electrophoresis to examine putative peptide binding region sequences from the peripheral blood leukocyte-derived RNAs of 19 wild-caught California sea lions from physically distinct populations. The pattern of Zaca-DQ sequence migration was identical between individuals and independent of geographical region. This apparent Zaca-DQ sequence identity between sea lions was confirmed by direct sequencing of individual bands. In combination, these findings raise important questions regarding immunogenetic diversity within this thriving species, and should prompt further research into the existence of a highly polymorphic sea lion class II MHC molecule with sequence features that support traditional peptide binding functions.     

Metastrongyloid nematode (Otostrongylus circumlitus) infection in a stranded California sea lion (Zalophus californianus)--a new host-parasite association

A stranded yearling male California sea lion was admitted to a rehabilitation center June 2003. On presentation, the sea lion was emaciated and had diarrhea and neutrophilia. Two weeks later, the animal became anorexic, blood and mucus were observed around the oral cavity, and corneal opacity was noted in the right eye. Hematology results at that time included leukocytosis consisting of neutrophilia with a left shift, anemia, and thrombocytopenia. Despite supportive care, the sea lion died. On post mortem examination, there were multiple areas of hemorrhage scattered throughout all lung lobes, and pulmonary blood vessels were occluded by fibrin thrombi. Nematodes identified as immature forms of Otostrongylus circumlitus were found in the right ventricle and pulmonary arteries. Histologic findings in the lungs included severe suppurative and necrotizing arteritis with vascular thrombosis, interstitial pneumonia, and large areas of pulmonary hemorrhage. This report of O. circumlitus infection in a California sea lion (Zalophus californianus) might indicate a potentially new host-parasite association.     

Common cancer in a wild animal: the California sea lion (Zalophus californianus) as an emerging model for carcinogenesis

Naturally occurring cancers in non-laboratory species have great potential in helping to decipher the often complex causes of neoplasia. Wild animal models could add substantially to our understanding of carcinogenesis, particularly of genetic and environmental interactions, but they are currently underutilized. Studying neoplasia in wild animals is difficult and especially challenging in marine mammals owing to their inaccessibility, lack of exposure history, and ethical, logistical and legal limits on experimentation. Despite this, California sea lions (Zalophus californianus) offer an opportunity to investigate risk factors for neoplasia development that have implications for terrestrial mammals and humans who share much of their environment and diet. A relatively accessible California sea lion population on the west coast of the USA has a high prevalence of urogenital carcinoma and is regularly sampled during veterinary care in wildlife rehabilitation centres. Collaborative studies have revealed that genotype, persistent organic pollutants and a herpesvirus are all associated with this cancer. This paper reviews research to date on the epidemiology and pathogenesis of urogenital carcinoma in this species, and presents the California sea lion as an important and currently underexploited wild animal model of carcinogenesis.     

Comparative biology of Uncinaria spp. in the California sea lion (Zalophus californianus) and the northern fur seal (Callorhinus ursinus) in California

Studies on several aspects of the life cycle of hookworms (Uncinaria spp.) in the California sea lion (Zalophus californianus) and northern fur seal (Callorhinus ursinus) were conducted on material collected on San Miguel Island (SMI), California and at The Marine Mammal Center, Sausalito, California in 1997, 1998, and 1999. Examination of Z. californianus intestines for adult hookworms and feces for eggs revealed that longevity of these parasites in pups is about 6-8 mo, and infections are probably not present in older sea lions. Parasitic third-stage larvae (L3) were recovered from the ventral abdominal tissue of Z. californianus, suggesting transmammary transmission. Callorhinus ursinus pups had no hookworm eggs in their feces or adult worms (except for 1 probable contaminant) in their intestines in the fall and early winter, revealing that adult Uncinaria spp. are spontaneously lost at <3 mo of age of the pups. Sand samples from rookeries, used by both Z. californianus and C. ursinus, on SMI were negative for free-living, L3 in summer months but positive in fall and winter months, indicating seasonality occurred.     

Isolation of a novel adenovirus from California sea lions Zalophus californianus

Viral hepatitis associated with adenoviral infection has been reported in California sea lions Zalophus californianus admitted to rehabilitation centers along the California coast since the 1970s. Canine adenovirus 1 (CAdV-1) causes viral hepatitis in dogs and infects a number of wildlife species. Attempts to isolate the virus from previous sea lion hepatitis cases were unsuccessful, but as the hepatitis had morphologic features resembling canine infectious hepatitis, and since the virus has a wide host range, it was thought that perhaps the etiologic agent was CAdV-1. Here, we identify a novel adenovirus in 2 stranded California sea lions and associate the infection with viral hepatitis and endothelial cell infection. Phylogenetic analysis confirmed the classification of the sea lion adenovirus in the Mastadenovirus genus with the most similarity to tree shrew adenovirus 1 (TSAdV-1, 77%). However, as the sea lion adenovirus appeared to be equally distant from the other Mastadenovirus species based on phylogenetic analysis, results indicate that it represents an independent lineage and species. Although sequences from this novel virus, otarine adenovirus 1 (OtAdV-1), show some similarity to CAdV-1 and 2, it is clearly distinct and likely the cause of the viral hepatitis in the stranded California sea lions.     

Performance of African elephants (Loxodonta africana) and California sea lions (Zalophus californianus) on a two-choice object discrimination task

This study documents the ability of African elephants (Loxodonta africana) and California sea lions (Zalophus californianus) to perform a two-choice object discrimination task. Both species were able to perform this task. However, California sea lions took fewer trials overall to reach a criterion of 10 consecutively correct responses than did African elephants. The performance of California sea lions did not change significantly during this study. However, African elephants showed a gradual learning of the task, as exhibited by a gradual decrease in the number of trials needed to reach criterion. This performance difference may reflect differences in either visual abilities or cognitive functioning, which in turn may be influenced by either different evolutionary pressures exerted on herbivores and carnivores, or by the context in which visual information is used in the lives of these animals. © 1994 Wiley-Liss, Inc.     

First findings of Cryptosporidium and Giardia in California sea lions (Zalophus californianus)

We report the detection and identification of Cryptosporidium and Giardia from 1 of 3 species of pinnipeds. Fecal samples were collected from Pacific harbor seal (Phoca vitulina richardsi), northern elephant seal (Mirounga angustirostris), and California sea lion (Zalophus californianus) in the northern California coastal area. By means of fluorescently labeled monoclonal antibodies, Cryptosporidium oocysts were detected in 3 samples from California sea lions, 1 of which also contained Giardia cysts. Oocysts of Cryptosporidium and cysts of Giardia were morphologically indistinguishable from oocysts of C. parvum and cysts of G. duodenalis from other animal origins. Oocysts and cysts were then purified using immunomagnetic separation techniques and identified by polymerase chain reaction (PCR), from which species-specific products were obtained. Sequence analysis revealed that the 452-bp and 358-bp PCR products of Cryptosporidium isolated from California sea lion had identities of 98% with sequences of their template fragments of C. parvum obtained from infected calves. Based on morphological, immunological, and genetic characterization, the isolates were identified as C. parvum and G. duodenalis, respectively. The findings suggested that California sea lions could serve as reservoirs in the environmental transmission of Cryptosporidium and Giardia.     

Risk factors for an outbreak of leptospirosis in California sea lions (Zalophus californianus) in California, 2004

Leptospirosis has been reported in California sea lions (Zalophus californianus) since 1970; however, the source of infection and mode of transmission remain unknown. To elucidate these features, demographic and environmental risk factors for leptospirosis were evaluated. California sea lion stranding records from northern California for 2004 were used to identify cases of leptospirosis (n = 316) and controls (n = 143). Demographic characteristics (age class, sex) and environmental factors, representing surrogates for exposure to dogs, cattle, rainfall, and freshwater sources, were compared between cases and controls with the use of a geographic information system (GIS) and logistic regression. Multivariate analyses revealed that summer and autumn seasons, juvenile age class, male sex, high dog-park density, and close proximity to dog parks were significantly associated with leptospirosis in sea lions, whereas county farmland cattle density, rainfall levels 30 days prior to stranding, human density, and proximity to freshwater sources were not associated. Thus, dogs and dog parks, or factors associated with them, might be further investigated to assess their relationship to leptospirosis in sea lions.     

Evidence of injury caused by gas bubbles in a live marine mammal: barotrauma in a California sea lion Zalophus californianus

A yearling male California sea lion Zalophus californianus with hypermetric ataxia and bilateral negative menace reflexes was brought to The Marine Mammal Center, Sausalito, California, U.S.A., in late 2009 for medical assessment and treatment. The clinical signs were due to multiple gas bubbles within the cerebellum. These lesions were intraparenchymal, multifocal to coalescing, spherical to ovoid, and varied from 0.5 to 2.4 cm diameter. The gas composed 21.3% of the total cerebellum volume. Three rib fractures were also noted during diagnostic evaluation and were presumed to be associated with the gas bubbles in the brain. The progression of clinical signs and lesion appearance were monitored with magnetic resonance imaging, cognitive function testing and computed tomography. Gas filled voids in the cerebellum were filled with fluid on follow up images. Clinical signs resolved and the sea lion was released with a satellite tag attached. Post release the animal travelled approximately 75 km north and 80 km south of the release site and the tag recorded dives of over 150 m depth. The animal re-stranded 25 d following release and died of a subacute bronchopneumonia and pleuritis. This is the first instance of clinical injury due to gas bubble formation described in a living pinniped and the first sea lion with quantifiable cerebellar damage to take part in spatial learning and memory testing.     

Mechanics of the limbs of the walrus (Odobenus rosmarus) and the california sea lion (Zalophus californianus)

Moment arms and cross-sectional areas of muscles from the forelimbs and hind limbs of Odobenus and Zalophus were used to estimate relative torques associated with several locomotor movements. Odobenus uses predominantly the hind limbs for aquatic propulsion, while Zalophus only uses the forelimbs. Torques contributing to locomotor movements used during the power and recovery strokes were substantially greater for the hind limbs of Odobenus and for the forelimbs of Zalophus. Apparently, the lineages of these two genera shared an aquatic ancestor during the Miocene; therefore, they also shared a common method of aquatic propulsion. This common method of aquatic propulsion could have been either forelimb, hind limb, or both. Since the Miocene then, the method of aquatic propulsion and the mechanical characteristics of the limbs have diverged for at least one of these two lineages. A model is advanced to explain key mechanical differences between Odobenus and Zalophus that enable Odobenus to maneuver effectively in a head-down posture on the ocean floor.     

Identification of two novel coccidian species shed by California sea lions (Zalophus californianus)

Routine fecal examination revealed novel coccidian oocysts in asymptomatic California sea lions (Zalophus californianus) in a rehabilitation facility. Coccidian oocysts were observed in fecal samples collected from 15 of 410 California sea lions admitted to The Marine Mammal Center between April 2007 and October 2009. Phylogenetic analysis using the full ITS-1 region, partial small subunit 18S rDNA sequence, and the Apicomplexa rpoB region identified 2 distinct sequence clades, referred to as Coccidia A and Coccidia B, and placed them in the Sarcocystidae, grouped with the tissue-cyst-forming coccidia. Both sequence clades resolved as individual taxa at ITS-1 and rpoB and were most closely related to Neospora caninum. Coccidia A was identified in 11 and Coccidia B in 4 of 12 sea lion oocyst samples successfully sequenced (3 of those sea lions were co-infected with both parasites). Shedding of Coccidia A oocysts was not associated with age class, sex, or stranding location, but yearlings represented the majority of shedders (8/15). This is the first study to use molecular phylogenetics to identify and describe coccidian parasites shed by a marine mammal.