Hookworm infection,anaemia and genetic variability of the New Zealand sea lion

Hookworms are intestinal blood-feeding nematodes that parasitize and cause high levels of mortality in a wide range of mammals, including otariid pinnipeds. Recently, an empirical study showed that inbreeding (assessed by individual measures of multi-locus heterozygosity) is associated with hookworm-related mortality of California sea lions. If inbreeding increases susceptibility to hookworms, effects would expectedly be stronger in small, fragmented populations. We tested this assumption in the New Zealand sea lion, a threatened otariid that has low levels of genetic variability and high hookworm infection rates. Using a panel of 22 microsatellites, we found that average allelic diversity (5.9) and mean heterozygosity (0.72) were higher than expected for a small population with restricted breeding, and we found no evidence of an association between genetic variability and hookworm resistance. However, similar to what was observed for the California sea lion, homozygosity at a single locus explained the occurrence of anaemia and thrombocytopenia in hookworm-infected pups (generalized linear model, F = 11.81, p < 0.001) and the effect was apparently driven by a particular allele (odds ratio = 34.95%; CI: 7.12–162.41; p < 0.00001). Our study offers further evidence that these haematophagus parasites exert selective pressure on otariid blood-clotting processes.     

Neonatal survival of Steller sea lions (Eumetopias jubatus)

Neonatal survival of Steller sea lions ( Eumetopias jubatus ) are often considered inconsequential to their population dynamics. However, observations of dead animals on rookeries and in surrounding waters suggest that early mortality is not uncommon. This study used the natural markings of adult females in a mark and resighting framework to estimate the apparent survival (φ) of pups with the Cormack–Jolly–Seber model at two sites on Lowrie Island, Alaska from birth to 3 wk old. Estimates varied greatly by site and year; 2002 Area 5:     (95% CI: 0.199, 0.684; n = 21), 2002 Area 1:     (0.437, 0.916; n = 21), 2003 Area 5:     (0.414, 0.738; n = 56), and 2003 Area 1:     (0.695, 0.997; n = 32). The mean estimate across the four area × year combinations was     (0.569, 0.772). Survival was lowest on the first day of life and then leveled off at a higher rate. None of the four environmental covariates we considered (swell height, interaction of tide and swell heights, density, or birth date) were significantly related to neonatal survival. Our results suggest that estimates of first-year survival that do not account for mortality prior to dispersal from the natal rookery may significantly overestimate survival rate.     

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     

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.     

Demographics and spatio‐temporal signature of the biotoxin domoic acid in California sea lion (Zalophus californianus) stranding records

California sea lions (Zalophus californianus) in otherwise good nutritional condition have been consistently affected by the marine biotoxin domoic acid since the late 1990s. In this study we evaluated the temporal and spatial stranding patterns of suspected and confirmed cases of domoic acid intoxicated sea lions from 1998 to 2006, using records of strandings along the California coast obtained from members of the California Marine Mammal Stranding Network. The majority of domoic acid cases were adult females (47%–82% of the total annual domoic acid cases), a contrast to strandings that were not related to domoic acid, which were generally dominated by juveniles and pups. Exposure to this biotoxin led to a 6.67‐fold increase in adult female strandings in 2000, and a 5.44‐fold increase in adult female deaths in 2006, relative to strandings and deaths of adult female not affected by domoic acid. Domoic acid cases have occurred annually since 1998 (except for 1999) between April and August, with clusters centered primarily at Pismo Beach (San Luis Obispo County), as well as at other beaches in San Luis Obispo, Monterey, Santa Cruz, Santa Barbara, Orange, and San Diego counties. The larger ecological and population level implications of increased domoic acid strandings and deaths, particularly among adult female sea lions, warrant further attention and need to be investigated.     

Pseudo‐nitzschia blooms,domoic acid,and related California sea lion strandings in Monterey Bay,California

Blooms of the toxin‐producing diatom Pseudo‐nitzschia commonly occur in Monterey Bay, California, resulting in sea lion mortality events. The links between strandings of California sea lions suffering from domoic acid (DA) toxicity, toxic cell numbers, and their associated DA concentration in Monterey Bay and in sea lion feces were examined from 2004 to 2007. While Pseudo‐nitzschia toxic cells and DA concentrations were detectable in the water column most of the time, they were often at low levels. A total of 82 California sea lions were found stranded in the Bay between 2004 and 2007 with acute or chronic signs associated with DA poisoning. The highest number with detectable DA in feces occurred in April 2007 and corresponded with the presence of a highly toxic bloom in the Bay. Higher DA levels occurred in feces from sea lions stranding with acute toxicosis and lower concentrations in feces of sea lions exhibiting signs of chronic DA poisoning or not exhibiting any neurologic signs. Results indicated that sea lions are likely exposed to varying levels of DA through their prey throughout the year, often at sublethal doses that may contribute to a continued increase in the development of chronic neurologic sequelae.     

Short‐term survival of Steller sea lion (Eumetopias jubatus) pups: Investigating the effect of health status on survival

We estimated survival probabilities for Steller sea lion (Eumetopias jubatus) pups from 3 wk to 6 wk old and from 6 wk to 1 yr at three rookeries in southeastern Alaska. We also investigated the effect of mass, body condition, health variables, and the genetic origin on 3–6 wk survival. Survival differed substantially among rookeries and between sexes, with survival lowest at Hazy Islands, intermediate at White Sisters, and highest at Graves Rocks and survival lower for males than females. Body mass, body condition, and hematocrit were positively related to survival and blood %H₂O and haptoglobin level (for females; no relationship for males) were negatively related to survival. Taking predictor variables collectively, sea lion pups at Hazy Islands, which had the lowest survival probability, had the lowest mass, hematocrit, and hemoglobin, and had high levels of blood %H₂O, and hookworm infection. Values from Graves Rocks, which had the highest survival, were the opposite of those from Hazy Island (e.g., high mass, body condition, hematocrit, and hemoglobin), while those from White Sisters (intermediate survival) had varying means (e.g., high hematocrit and hemoglobin and low hookworms, but also low body condition); these patterns suggest that physiological factors potentially underlie rookery differences in survival.     

Age-specific birth rates of California sea lions (Zalophus californianus) in the Gulf of California, Mexico

Estimates of demographic parameters are essential for assessing the status of populations and assigning conservation priority. In light of the difficulties associated with obtaining such estimates, vital rates are rarely available even for well-studied species. We present the first estimates of age-specific birth rates for female California sea lions ( Zalophus californianus ) >10 yr of age. These rates were estimated from the reproductive histories of five cohorts of animals branded as pups between 1980 and 1984 at Los Islotes colony in the Gulf of California, Mexico. Age-specific birth rates varied among age classes and ranged between 0.06 and 0.80. The highest birth rates were observed for females between 10 and 15 yr of age, with decreased birth rates among older females. The effect of age, year, and resighting effort were explored using logistic regression analysis. Based on Akaike Information Criteria, birth rates were best explained by female age, while year and resighting effort did not have a significant effect. The odds ratio of producing a pup decreased with age but did not change significantly for middle-aged females. Our estimates of age-specific birth rates are consistent with general patterns observed for other large vertebrates.     

Age‐ and sex‐specific survival of California sea lions (Zalophus californianus) at San Miguel Island,California

We conducted a mark‐recapture study of California sea lions (Zalophus californianus) using pups branded on San Miguel Island, California, from 1987 to 2014, and annual resightings from 1990 to 2015. We used the Burnham model (Burnham 1993), an extension of the Cormack‐Jolly‐Seber mark‐recapture model, which includes recoveries of dead animals, to analyze age, sex, and annual patterns in survival. Generally, females had higher survival than males. For female pups, the average annual survival was 0.600 and for male pups it was 0.574. Yearling survival was 0.758 and 0.757 for females and males, respectively. Peak annual survival was at age 5 and was 0.952 for females and 0.931 for males. Pups with larger mass at branding had higher survival as pups and yearlings, but the effect was relative within each cohort because of large between‐cohort variability in survival. Annual variability in sea surface temperature (SST) affected survival. For each 1°C increase in SST, the odds of survival decreased by nearly 50% for pups and yearlings; negative SST anomalies yielded higher survival. Annual variation in male survival was partly explained by leptospirosis outbreaks. Our study provides a unique view of one demographic parameter that contributed to the successful recovery of the California sea lion population.     

An immunogenetic basis for the high prevalence of urogenital cancer in a free-ranging population of California sea lions (Zalophus californianus)

In response to an unprecedented prevalence of cancer recently identified in free-ranging populations of California sea lions [(CSL) (Zalophus californianus], we examined the role of the immunologically important major histocompatibility (MHC) genes in this disease epidemic. Associations between MHC genes and cancer have been well established in humans, but have never before been investigated in wildlife. Using a previously developed technique employing sequence-specific primer-based PCR with intercalating dye technology, MHC genotypes were examined from 27 cancer-positive and 22 cancer-negative CSL stranded along the California coastline. Analyses elucidated an underlying immunogenetic component to the high prevalence of urogenital cancer in sea lions. Furthermore, these results demonstrate the functional relevance of CSL class II MHC by revealing a non-random nature of cancer susceptibility associated with the presence of specific genes.     

Trophic level and overlap of sea lions (Zalophus californianus) in the Gulf of California, Mexico

Stable isotope and scat analyses were used in concert to determine trophic level and dietary overlap among California sea lions from different rookeries in the Gulf of California. Isotopic analysis of the fur of sea lion pups revealed differences in δ¹⁵N and δ¹³C values among rookeries during the breeding season. Mean δ¹⁵N and δ¹³C values varied from 20.2‰ to 22.4‰ and from −15.4‰ to −14.0‰, respectively. The pattern of differences among rookeries was similar between years in most cases. Isotopic variations among rookeries were associated with differences in prey consumption. There was a significant correlation between δ¹⁵N value and trophic level, as determined by scat analysis. Joint application of isotopic and scat analyses allowed us to identify how the feeding habits of sea lions vary with location. Our results suggest the presence of spatial structure in available prey as well as the localized use of prey by sea lions across the Gulf of California.     

MHC gene configuration variation in geographically disparate populations of California sea lions (Zalophus californianus)

Major histocompatibility complex (MHC) class II DRB genotypes were examined in two geographically isolated populations of California sea lions (Zalophus californianus) (Gulf of California and California coastal Pacific Ocean). Genomic DNA from 227 California sea lions was examined using eight sequence-specific primer (SSP) pairs flanking the putative peptide-binding site. A total of 40 different Zaca-DRB genotype configurations were identified among the 227 individuals. Using SSP-PCR, significant differences were found between coastal California and Gulf of California Zalophus populations in numbers of DRB sequences per individual and configuration of sequences within individuals. Additionally, unique local patterns of MHC diversity were identified among the Midriff Island animals. These population differences are consistent with either ecologically distinct patterns of selection pressures and/or geographical isolation. The consequences of these partitioned MHC configurations at the population level are as yet unknown; however, the worldwide increase in emerging marine diseases lends urgency to their examination.     

Diet estimation in California sea lions,Zalophus californianus

We performed a captive feeding experiment using California sea lions to assess biases associated with estimating pinniped diet using scats and spews. Sea lions were fed nine of their natural prey species: anchovy, sardine, Pacific mackerel, jack mackerel, hake, steelhead smolts, shortbelly rockfish, pink salmon, and market squid. Recovery percentages varied among prey species using otoliths and were improved for adult salmon and sardine using the all‐structure method. Numerical and graded length correction factors provided better estimates of number and size of prey consumed. Four models used to determine the proportions of prey species consumed by a sea lion population were tested. The all‐structure method and variable biomass reconstruction model, in conjunction with numerical and graded length correction factors, provided more accurate estimates than without. We provide numerical correction factors for all prey species, including correction factors for specific salmon bones: vertebrae, branchials, radials, teeth, gill rakers, and hypurals.     

Islands in the sea: extreme female natal site fidelity in the Australian sea lion, Neophoca cinerea

Pinnipeds (seals, fur seals, sea lions and walrus) form large breeding aggregations with females often remaining faithful to a natal site or area. In these cases, females are philopatric to regional areas on broad geographical scales of hundreds to thousands of kilometers. An investigation of variation in a control region sequence of mtDNA in the Australian sea lion (Neophoca cinerea) has shown a case of extreme female natal site fidelity that has resulted in almost fixed population differentiation across its range (PhiST=0.93). This high level of population subdivision over short geographical distances (approx. 60 km) is unparalleled in any social marine mammal and reflects the unique life-history traits of this rare species. The high level of population subdivision and exclusive female natal site fidelity has important ramifications for conservation management, and poses many interesting questions of both academic and applied interest.     

Hookworm enteritis with bacteremia in California sea lion pups on San Miguel Island

Large breeding populations of California sea lions (Zalophus californianus) are located on San Miguel and San Nicolas Islands in the Southern California Bight. In 2001, there was a substantial increase in pup mortality in late summer and fall. From June 2002 to January 2003, 208 freshly dead pups were examined on San Miguel Island, the most western of the Channel Islands off the coast of southern California. Tissues from 186 of these pups were examined histologically. The primary lesions in 133 (72%) of the pups were an enteritis associated with hookworms and infections in major organs. Emaciation/starvation in 43 pups (26%) was the second most important cause of death.     

Relation of dental wear to the concentrations of essential minerals in teeth of the California sea lion <Emphasis Type="Italic">Zalophus Californianus Californianus</Emphasis>

Tooth wear in marine mammals has been attributed to age, feeding habits, behavior, and contaminants. Advanced tooth wear in some California sea lions, including some of very young age (<5 yr), in the Gulf of California, suggests that there are variations in chemical composition of tooth parts, wherein the concentrations of certain trace minerals might be anomalous, making them more susceptible to erosion. The concentrations of the essential minerals Ca, P, K, Na, Fe, Mg, and Zn in the dentition of Zalophus c. californianus are documented for the first time and are compared for sea lion teeth with different degrees of wear. Canine teeth and molars from 45 skulls collected at 15 localities since 1978 were digested in perchloric acid and analyzed using atomic adsorption spectrometry, the results being expressed in milligrams per 100 g. An index of tooth wear (Id) was established, involving the average wear on the teeth and the age of the organism. No significant difference was detected in the variables, but there was one between ages (p=0.02). A higher degree of wear was observed up to 7 yr of age than from this age onward. Mineral concentrations did not explain the excessive wear observed (correlation, p>0.09; ANOVA, p>0.15); however, the Ca concentration of the teeth was inversely proportional to the age of the animal (sexes combined, p=0.026) and particularly significant for the females (r ²=0.112, r=−0.335, p=0.039). Females could be more prone to decalcification because of their annual bone investment in their offspring. Animals of both sexes were susceptible to tooth wear as their age increased, but the higher frequency of animals between 4 and 7 yr suggests an impact on survival at early stages probably linked to deficient feeding and chronic malnutrition.     

Evidence of Leptospira interrogans infection in California sea lion pups from the Gulf of California

Forty-two urine and 96 blood and serum samples were obtained from California sea lion (Zalophus californianus) pups from the Gulf of California during the 2000 reproductive season. Antibody prevalence to 13 serovars of Leptospira interrogans was determined by microagglutination tests (MAT); presence of pathogenic leptospires was detected by polymerase chain reaction (PCR). Samples with antibody titers > or = 1:25 or 115 bp fragments on ethidium bromidestained 1.5% agarose gels were considered positive. Antibody prevalence was 54% overall with highest prevalence against serovar cynopteri (50% of all positive reactions). Highest antibody titers (1:50) were detected against serovars cynopteri and pomona. Polymerase chain reaction products were observed in two of 42 urine samples, six of 96 blood samples, and one of 96 serum samples. Presence of PCR products in blood and serum was demonstrated in pups that were seronegative. Kruskall-Wallis tests and corresponding post hoc Tukey tests (alpha = 0.05) showed that prevalence of leptospirosis was significantly different among all rookeries. The high seroprevalence (54%), low antibody titers (maximum 1:50), absence of pups showing clinical signs indicative of the disease, and lack of recent reports of increased mortality of sea lions in the Gulf of California are suggestive of the presence of enzootic host-adapted serovars. Crowding in rookeries as well as the presence of bats and rodents on some of the islands may explain infection by L. interrogans (sensu lato) and some of the differences in seroprevalence among reproductive rookeries.     

Specialized foraging habits of adult female California sea lions Zalophus californianus

Individual foraging specialization occurs when organisms use a small subset of the resources available to a population. This plays an important role in population dynamics since individuals may have different ecological functions within an ecosystem related to habitat use and prey preferences. The foraging habitat fidelity and degree of specialization of California sea lions (Zalophus californianus) were evaluated by analyzing the stable isotopes values of carbon and nitrogen in vibrissae collected from 16 adult females from the reproductive colony on Santa Margarita Island, Magdalena Bay, Mexico, in 2012 and 2013. Based on the degree of individual specialization in δ¹⁵N, 62.5% of the females assessed can be considered specialist consumers focusing on the same prey or different prey from the same trophic level. The degree of individual specialization in δ¹³C indicated that 100% of the individuals showed fidelity to their foraging habitat as some fed in the lagoon, others foraged along the coast, and a third group preferred prey from the pelagic environment during both the breeding and nonbreeding seasons, suggesting diversification of foraging areas. Foraging area fidelity persisted despite the 2°C increase in the sea surface temperature over the course of the study period.