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1.  Latitudinal Range Influences the Seasonal Variation in the Foraging Behavior of Marine Top Predators 
PLoS ONE  2011;6(8):e23166.
Non-migratory resident species should be capable of modifying their foraging behavior to accommodate changes in prey abundance and availability associated with a changing environment. Populations that are better adapted to change will have higher foraging success and greater potential for survival in the face of climate change. We studied two species of resident central place foragers from temperate and equatorial regions with differing population trends and prey availability associated to season, the California sea lion (Zalophus californianus) (CSL) whose population is increasing and the endangered Galapagos sea lion (Zalophus wollebaeki) (GSL) whose population is declining. To determine their response to environmental change, we studied and compared their diving behavior using time-depth recorders and satellite location tags and their diet by measuring C and N isotope ratios during a warm and a cold season. Based on latitudinal differences in oceanographic productivity, we hypothesized that the seasonal variation in foraging behavior would differ for these two species. CSL exhibited greater seasonal variability in their foraging behavior as seen in changes to their diving behavior, foraging areas and diet between seasons. Conversely, GSL did not change their diving behavior between seasons, presenting three foraging strategies (shallow, deep and bottom divers) during both. GSL exhibited greater dive and foraging effort than CSL. We suggest that during the warm and less productive season a greater range of foraging behaviors in CSL was associated with greater competition for prey, which relaxed during the cold season when resource availability was greater. GSL foraging specialization suggests that resources are limited throughout the year due to lower primary production and lower seasonal variation in productivity compared to CSL. These latitudinal differences influence their foraging success, pup survival and population growth reflected in contrasting population trends in which CSL are more successful and potentially more resilient to climate change.
doi:10.1371/journal.pone.0023166
PMCID: PMC3154271  PMID: 21853081
2.  The Cost of Male Aggression and Polygyny in California Sea Lions (Zalophus californianus) 
PLoS ONE  2010;5(8):e12230.
In polygynous mating systems, males often increase their fecundity via aggressive defense of mates and/or resources necessary for successful mating. Here we show that both male and female reproductive behavior during the breeding season (June–August) affect female fecundity, a vital rate that is an important determinant of population growth rate and viability. By using 4 years of data on behavior and demography of California sea lions (Zalophus californianus), we found that male behavior and spatial dynamics—aggression and territory size—are significantly related to female fecundity. Higher rates of male aggression and larger territory sizes were associated with lower estimates of female fecundity within the same year. Female aggression was significantly and positively related to fecundity both within the same year as the behavior was measured and in the following year. These results indicate that while male aggression and defense of territories may increase male fecundity, such interactions may cause a reduction in the overall population growth rate by lowering female fecundity. Females may attempt to offset male-related reductions in female fecundity by increasing their own aggression—perhaps to defend pups from incidental injury or mortality. Thus in polygynous mating systems, male aggression may increase male fitness at the cost of female fitness and overall population viability.
doi:10.1371/journal.pone.0012230
PMCID: PMC2923196  PMID: 20808931
3.  Weak Polygyny in California Sea Lions and the Potential for Alternative Mating Tactics 
PLoS ONE  2012;7(3):e33654.
Female aggregation and male territoriality are considered to be hallmarks of polygynous mating systems. The development of genetic parentage assignment has called into question the accuracy of behavioral traits in predicting true mating systems. In this study we use 14 microsatellite markers to explore the mating system of one of the most behaviorally polygynous species, the California sea lion (Zalophus californianus). We sampled a total of 158 female-pup pairs and 99 territorial males across two breeding rookeries (San Jorge and Los Islotes) in the Gulf of California, Mexico. Fathers could be identified for 30% of pups sampled at San Jorge across three breeding seasons and 15% of sampled pups at Los Islotes across two breeding seasons. Analysis of paternal relatedness between the pups for which no fathers were identified (sampled over four breeding seasons at San Jorge and two at Los Islotes) revealed that few pups were likely to share a father. Thirty-one percent of the sampled males on San Jorge and 15% of the sampled males on Los Islotes were assigned at least one paternity. With one exception, no male was identified as the father of more than two pups. Furthermore, at Los Islotes rookery there were significantly fewer pups assigned paternity than expected given the pool of sampled males (p<0.0001). Overall, we found considerably lower variation in male reproductive success than expected in a species that exhibits behavior associated with strongly polygynous mating. Low variation in male reproductive success may result from heightened mobility among receptive females in the Gulf of California, which reduces the ability of males to monopolize groups of females. Our results raise important questions regarding the adaptive role of territoriality and the potential for alternative mating tactics in this species.
doi:10.1371/journal.pone.0033654
PMCID: PMC3303858  PMID: 22432039
4.  Cyclical changes in seroprevalence of leptospirosis in California sea lions: endemic and epidemic disease in one host species? 
Background
Leptospirosis is a zoonotic disease infecting a broad range of mammalian hosts, and is re-emerging globally. California sea lions (Zalophus californianus) have experienced recurrent outbreaks of leptospirosis since 1970, but it is unknown whether the pathogen persists in the sea lion population or is introduced repeatedly from external reservoirs.
Methods
We analyzed serum samples collected over an 11-year period from 1344 California sea lions that stranded alive on the California coast, using the microscopic agglutination test (MAT) for antibodies to Leptospira interrogans serovar Pomona. We evaluated seroprevalence among yearlings as a measure of incidence in the population, and characterized antibody persistence times based on temporal changes in the distribution of titer scores. We conducted multinomial logistic regression to determine individual risk factors for seropositivity with high and low titers.
Results
The serosurvey revealed cyclical patterns in seroprevalence to L. interrogans serovar Pomona, with 4–5 year periodicity and peak seroprevalence above 50%. Seroprevalence in yearling sea lions was an accurate index of exposure among all age classses, and indicated on-going exposure to leptospires in non-outbreak years. Analysis of titer decay rates showed that some individuals probably maintain high titers for more than a year following exposure.
Conclusion
This study presents results of an unprecedented long-term serosurveillance program in marine mammals. Our results suggest that leptospirosis is endemic in California sea lions, but also causes periodic epidemics of acute disease. The findings call into question the classical dichotomy between maintenance hosts of leptospirosis, which experience chronic but largely asymptomatic infections, and accidental hosts, which suffer acute illness or death as a result of disease spillover from reservoir species.
doi:10.1186/1471-2334-7-125
PMCID: PMC2186333  PMID: 17986335
5.  Intraperitoneal implantation of life-long telemetry transmitters in otariids 
Background
Pinnipeds, including many endangered and declining species, are inaccessible and difficult to monitor for extended periods using externally attached telemetry devices that are shed during the annual molt. Archival satellite transmitters were implanted intraperitoneally into four rehabilitated California sea lions (Zalophus californianus) and 15 wild juvenile Steller sea lions (Eumetopias jubatus) to determine the viability of this surgical technique for the deployment of long-term telemetry devices in otariids. The life history transmitters record information throughout the life of the host and transmit data to orbiting satellites after extrusion following death of the host.
Results
Surgeries were performed under isoflurane anesthesia and single (n = 4) or dual (n = 15) transmitters were inserted into the ventrocaudal abdominal cavity via an 8.5 to 12 cm incision along the ventral midline between the umbilicus and pubic symphysis or preputial opening. Surgeries lasted 90 minutes (SD = 8) for the 19 sea lions. All animals recovered well and were released into the wild after extended monitoring periods from 27 to 69 days at two captive animal facilities. Minimum post-implant survival was determined via post-release tracking using externally attached satellite transmitters or via opportunistic re-sighting for mean durations of 73.7 days (SE = 9.0, Z. californianus) and 223.6 days (SE = 71.5, E. jubatus).
Conclusion
The low morbidity and zero mortality encountered during captive observation and post-release tracking periods confirm the viability of this surgical technique for the implantation of long-term telemetry devices in otariids.
doi:10.1186/1746-6148-4-51
PMCID: PMC2621145  PMID: 19077193
6.  DETERMINATION OF A SEDATIVE PROTOCOL FOR USE IN CALIFORNIA SEA LIONS (ZALOPHUS CALIFORNIANUS) WITH NEUROLOGIC ABNORMALITIES UNDERGOING ELECTROENCEPHALOGRAPHIC EXAMINATION 
Sedation in sea lions exhibiting abnormal neurologic signs may require modification of established sedation protocols because of the likely interaction between effects of the sedative and physiologic changes in diseased animals. The effects of two sedative combinations, 0.07 mg/kg medetomidine and 0.07 mg/kg medetomidine plus 0.2 mg/kg butorphanol, were compared between California sea lions (Zalophus californianus) with signs of neurologic dysfunction (n = 33) and without neurologic signs (n = 8). Sedation depth was scored on a scale of 0 (no effect) to 4 (profound sedation) assessed by response to auditory, tactile, and visual stimuli at the time of perceived maximal sedative effect. In the medetomidine-alone group, sea lions with neurologic signs attained a median sedation score of 4 compared to a median sedation score of 1 in the clinically normal sea lions. Sea lions with and without neurologic signs given medetomidine–butorphanol attained a median sedation score of 4. No statistically significant difference in time to induction and respiratory rate was found between the two sedation protocols in all sea lions. In the sea lions with neurologic signs, the recovery time from medetomidine–butorphanol sedation was prolonged (P < 0.01) and minimum recorded heart rates, although remaining within normal physiologic limits, were lower (P = 0.02) when compared to the sea lions administered medetomidine alone. Muscle jerks were observed in many animals given medetomidine–butorphanol and were detrimental to the diagnostic quality of the electroencephalogram (EEG) recording. Medetomidine alone at a dose rate of 0.07 mg/kg thus provides adequate and safe sedation in sea lions with neurologic signs undergoing EEG evaluation.
PMCID: PMC3005622  PMID: 19110694
California sea lion; Zalophus californianus; medetomidine; butorphanol; neurologic; electroencephalogram
7.  Immune Activity, Body Condition and Human-Associated Environmental Impacts in a Wild Marine Mammal 
PLoS ONE  2013;8(6):e67132.
Within individuals, immunity may compete with other life history traits for resources, such as energy and protein, and the damage caused by immunopathology can sometimes outweigh the protective benefits that immune responses confer. However, our understanding of the costs of immunity in the wild and how they relate to the myriad energetic demands on free-ranging organisms is limited. The endangered Galapagos sea lion (Zalophus wollebaeki) is threatened simultaneously by disease from domestic animals and rapid changes in food availability driven by unpredictable environmental variation. We made use of this unique ecology to investigate the relationship between changes in immune activity and changes in body condition. We found that during the first three months of life, changes in antibody concentration were negatively correlated with changes in mass per unit length, skinfold thickness and serum albumin concentration, but only in a sea lion colony exposed to anthropogenic environmental impacts. It has previously been shown that changes in antibody concentration during early Galapagos sea lion development were higher in a colony exposed to anthropogenic environmental impacts than in a control colony. This study allows for the possibility that these relatively large changes in antibody concentration are associated with negative impacts on fitness through an effect on body condition. Our findings suggest that energy availability and the degree of plasticity in immune investment may influence disease risk in natural populations synergistically, through a trade-off between investment in immunity and resistance to starvation. The relative benefits of such investments may change quickly and unpredictably, which allows for the possibility that individuals fine-tune their investment strategies in response to changes in environmental conditions. In addition, our results suggest that anthropogenic environmental impacts may impose subtle energetic costs on individuals, which could contribute to population declines, especially in times of energy shortage.
doi:10.1371/journal.pone.0067132
PMCID: PMC3695956  PMID: 23840603
8.  Clinical relevance of novel Otarine herpesvirus-3 in California sea lions (Zalophus californianus): lymphoma, esophageal ulcers, and strandings 
Veterinary Research  2012;43(1):85.
Herpesviruses have been recognized in marine mammals, but their clinical relevance is not always easy to assess. A novel otarine herpesvirus-3 (OtHV3) was detected in a geriatric California sea lion (Zalophus californianus), and using a newly developed quantitative PCR assay paired with histology, OtHV3 was associated with esophageal ulcers and B cell lymphoblastic lymphoma in this animal. The prevalence and quantities of OtHV3 were then determined among buffy coats from 87 stranded and managed collection sea lions. Stranded sea lions had a higher prevalence of OtHV3 compared to managed collection sea lions (34.9% versus 12.5%; p = 0.04), and among the stranded sea lions, yearlings were most likely to be positive. Future epidemiological studies comparing the presence and viral loads of OtHV3 among a larger population of California sea lions with and without lymphoid neoplasia or esophageal ulcers would help elucidate the relevance of OtHV3-associated pathologies to these groups.
doi:10.1186/1297-9716-43-85
PMCID: PMC3567969  PMID: 23234600
9.  Zebrafish Seizure Model Identifies p,p′-DDE as the Dominant Contaminant of Fetal California Sea Lions That Accounts for Synergistic Activity with Domoic Acid 
Environmental Health Perspectives  2009;118(4):545-551.
Background
Fetal poisoning of California sea lions (CSLs; Zalophus californianus) has been associated with exposure to the algal toxin domoic acid. These same sea lions accumulate a mixture of persistent environmental contaminants including pesticides and industrial products such as polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs). Developmental exposure to the pesticide dichlorodiphenyltrichloroethane (DDT) and its stable metabolite 1,1-bis-(4-chlorophenyl)-2,2-dichloroethene (p,p′-DDE) has been shown to enhance domoic acid–induced seizures in zebrafish; however, the contribution of other co-occurring contaminants is unknown.
Objective
We formulated a mixture of contaminants to include PCBs, PBDEs, hexachlorocyclohexane (HCH), and chlordane at levels matching those reported for fetal CSL blubber to determine the impact of co-occurring persistent contaminants with p,p′-DDE on chemically induced seizures in zebrafish as a model for the CSLs.
Methods
Embryos were exposed (6–30 hr postfertilization) to p,p′-DDE in the presence or absence of a defined contaminant mixture prior to neurodevelopment via either bath exposure or embryo yolk sac microinjection. After brain maturation (7 days postfertilization), fish were exposed to a chemical convulsant, either pentylenetetrazole or domoic acid; resulting seizure behavior was then monitored and analyzed for changes, using cameras and behavioral tracking software.
Results
Induced seizure behavior did not differ significantly between subjects with embryonic exposure to a contaminant mixture and those exposed to p,p′-DDE only.
Conclusion
These studies demonstrate that p,p′-DDE—in the absence of PCBs, HCH, chlordane, and PBDEs that co-occur in fetal sea lions—accounts for the synergistic activity that leads to greater sensitivity to domoic acid seizures.
doi:10.1289/ehp.0901301
PMCID: PMC2854733  PMID: 20368122
Danio rerio; DDT; domoic acid; epilepsy; PBDE; PCB; seizures; zebrafish
10.  High Natality Rates of Endangered Steller Sea Lions in Kenai Fjords, Alaska and Perceptions of Population Status in the Gulf of Alaska 
PLoS ONE  2010;5(4):e10076.
Steller sea lions experienced a dramatic population collapse of more than 80% in the late 1970s through the 1990s across their western range in Alaska. One of several competing hypotheses about the cause holds that reduced female reproductive rates (natality) substantively contributed to the decline and continue to limit recovery in the Gulf of Alaska despite the fact that there have been very few attempts to directly measure natality in this species. We conducted a longitudinal study of natality among individual Steller sea lions (n = 151) at a rookery and nearby haulouts in Kenai Fjords, Gulf of Alaska during 2003–2009. Multi-state models were built and tested in Program MARK to estimate survival, resighting, and state transition probabilities dependent on whether or not a female gave birth in the previous year. The models that most closely fit the data suggested that females which gave birth had a higher probability of surviving and giving birth in the following year compared to females that did not give birth, indicating some females are more fit than others. Natality, estimated at 69%, was similar to natality for Steller sea lions in the Gulf of Alaska prior to their decline (67%) and much greater than the published estimate for the 2000s (43%) which was hypothesized from an inferential population dynamic model. Reasons for the disparity are discussed, and could be resolved by additional longitudinal estimates of natality at this and other rookeries over changing ocean climate regimes. Such estimates would provide an appropriate assessment of a key parameter of population dynamics in this endangered species which has heretofore been lacking. Without support for depressed natality as the explanation for a lack of recovery of Steller sea lions in the Gulf of Alaska, alternative hypotheses must be more seriously considered.
doi:10.1371/journal.pone.0010076
PMCID: PMC2851612  PMID: 20386691
11.  Normal Morphology and Hormone Receptor Expression in the Male California sea lion (Zalophus californianus) Genital Tract 
Histomorphology and estrogen α (ER α), and progesterone receptor (PR) expression were evaluated in free-ranging stranded male California sea lions (Zalophus californianus). Hormone receptor expression was evaluated using an immunohistochemical technique with monoclonal antibodies. Estrogen and progesterone receptors were identified in the efferent ductules, prostate gland, corpus cavernosa, corpus spongiosium, penile urethra, and in the epithelium and stroma of both the penis and prepuce. In the some tissues, ER α expression was more intense in the stroma, emphasizing the importance of the stroma in hormone – mediated growth and differentiation of reproductive organs. To our knowledge, this is the first study to localize ER α and PR to the epithelium of the glans penis. The results of this investigation add to the general knowledge of male California sea lion reproduction and suggest that estrogens could have a role in the function of the male reproductive tract.
doi:10.1002/ar.21008
PMCID: PMC2871535  PMID: 19768750
California sea lion; estrogen receptor; progesterone receptor; male reproductive tract; urogenital cancer
12.  Hippocampal neuropathology of domoic acid-induced epilepsy in California sea lions (Zalophus californianus) 
The Journal of comparative neurology  2014;522(7):1691-1706.
California sea lions (Zalophus californianus) are abundant human-sized carnivores with large gyrencephalic brains. They develop epilepsy after experiencing status epilepticus when naturally exposed to domoic acid. We tested whether sea lions previously exposed to DA (chronic DA sea lions) display hippocampal neuropathology similar to that of human patients with temporal lobe epilepsy. Hippocampi were obtained from control and chronic DA sea lions. Stereology was used to estimate numbers of Nissl-stained neurons per hippocampus in the granule cell layer, hilus, and the pyramidal cell layer of CA3, CA2, and CA1 subfields. Adjacent sections were processed for somatostatin-immunoreactivity or Timm-stained, and the extent of mossy fiber sprouting was measured stereologically. Chronic DA sea lions displayed hippocampal neuron loss in patterns and extents similar but not identical to those reported previously for human patients with temporal lobe epilepsy. Similar to human patients, hippocampal sclerosis in sea lions was unilateral in 79% of cases, mossy fiber sprouting was a common neuropathological abnormality, and somatostatin-immunoreactive axons were exuberant in the dentate gyrus despite loss of immunopositive hilar neurons. Thus, hippocampal neuropathology of chronic DA sea lions is similar to that of human patients with temporal lobe epilepsy.
doi:10.1002/cne.23509
PMCID: PMC4100486  PMID: 24638960
hippocampal sclerosis; mossy fiber sprouting; somatostatin; stereology; dentate gyrus; Oswald Steward; Associate Editor
13.  No Evidence of Metabolic Depression in Western Alaskan Juvenile Steller Sea Lions (Eumetopias jubatus) 
PLoS ONE  2014;9(1):e85339.
Steller sea lion (Eumetopias jubatus) populations have undergone precipitous declines through their western Alaskan range over the last four decades with the leading hypothesis to explain this decline centering around changing prey quality, quantity, or availability for this species (i.e., nutritional stress hypothesis). Under chronic conditions of reduced food intake sea lions would conserve energy by limiting energy expenditures through lowering of metabolic rate known as metabolic depression. To examine the potential for nutritional stress, resting metabolic rate (RMR) and body composition were measured in free-ranging juvenile Steller sea lions (N = 91) at three distinct geographical locations (Southeast Alaska, Prince William Sound, Central Aleutian Islands) using open-flow respirometry and deuterium isotope dilution, respectively. Average sea lion RMR ranged from 6.7 to 36.2 MJ d−1 and was influenced by body mass, total body lipid, and to a lesser extent, ambient air temperature and age. Sea lion pups captured in the Aleutian Islands (region of decline) had significantly greater body mass and total body lipid stores when compared to pups from Prince William Sound (region of decline) and Southeast Alaska (stable region). Along with evidence of robust body condition in Aleutian Island pups, no definitive differences were detected in RMR between sea lions sampled between eastern and western populations that could not be accounted for by higher percent total body lipid content, suggesting that that at the time of this study, Steller sea lions were not experiencing metabolic depression in the locations studied.
doi:10.1371/journal.pone.0085339
PMCID: PMC3887069  PMID: 24416394
14.  A Novel Antibody-Based Biomarker for Chronic Algal Toxin Exposure and Sub-Acute Neurotoxicity 
PLoS ONE  2012;7(5):e36213.
The neurotoxic amino acid, domoic acid (DA), is naturally produced by marine phytoplankton and presents a significant threat to the health of marine mammals, seabirds and humans via transfer of the toxin through the foodweb. In humans, acute exposure causes a neurotoxic illness known as amnesic shellfish poisoning characterized by seizures, memory loss, coma and death. Regular monitoring for high DA levels in edible shellfish tissues has been effective in protecting human consumers from acute DA exposure. However, chronic low-level DA exposure remains a concern, particularly in coastal and tribal communities that subsistence harvest shellfish known to contain low levels of the toxin. Domoic acid exposure via consumption of planktivorous fish also has a profound health impact on California sea lions (Zalophus californianus) affecting hundreds of animals yearly. Due to increasing algal toxin exposure threats globally, there is a critical need for reliable diagnostic tests for assessing chronic DA exposure in humans and wildlife. Here we report the discovery of a novel DA-specific antibody response that is a signature of chronic low-level exposure identified initially in a zebrafish exposure model and confirmed in naturally exposed wild sea lions. Additionally, we found that chronic exposure in zebrafish caused increased neurologic sensitivity to DA, revealing that repetitive exposure to DA well below the threshold for acute behavioral toxicity has underlying neurotoxic consequences. The discovery that chronic exposure to low levels of a small, water-soluble single amino acid triggers a detectable antibody response is surprising and has profound implications for the development of diagnostic tests for exposure to other pervasive environmental toxins.
doi:10.1371/journal.pone.0036213
PMCID: PMC3342169  PMID: 22567140
15.  Gas Bubble Disease in the Brain of a Living California Sea Lion (Zalophus californianus) 
A yearling California sea lion (Zalophus californianus) was admitted into rehabilitation with signs of cerebellar pathology. Diagnostic imaging that included radiography and magnetic resonance imaging (MRI) demonstrated space-occupying lesions predominantly in the cerebellum that were filled partially by CSF-like fluid and partially by gas, and cerebral lesions that were fluid filled. Over a maximum period of 4 months, the brain lesions reduced in size and the gas resorbed and was replaced by CSF-like fluid. In humans, the cerebellum is known to be essential for automating practiced movement patterns (e.g., learning to touch-type), also known as procedural learning or the consolidation of “motor memory.” To test the animal in this study for motor memory deficits, an alternation task in a two-choice maze was utilized. The sea lion performed poorly similar to another case of pneumocerebellum previously reported, and contrary to data acquired from a group of sea lions with specific hippocampal injury. The learning deficits were attributed to the cerebellar injury. These data provide important insight both to the clinical presentation and behavioral observations of cerebellar injury in sea lions, as well as providing an initial model for long-term outcome following cerebellar injury. The specific etiology of the gas could not be determined. The live status of the patient with recovery suggests that the most likely etiologies for the gas are either de novo formation or air emboli secondary to trauma. A small air gun pellet was present within and was removed from soft tissues adjacent to the tympanic bulla. While no evidence to support the pellet striking bone was found, altered dive pattern associated with this human interaction may have provided the opportunity for gas bubble formation to occur. The similarity in distribution of the gas bubble related lesions in this case compared with another previously published case of pneumocerebellum suggests that preferential perfusion of the brain, and more specifically the cerebellum, may occur during diving events.
doi:10.3389/fphys.2013.00005
PMCID: PMC3557455  PMID: 23372553
Zalophus, gas bubble disease; diving mammals; brain MRI; veterinary medicine
16.  Galápagos and Californian sea lions are separate species: Genetic analysis of the genus Zalophus and its implications for conservation management 
Frontiers in Zoology  2007;4:20.
Background
Accurate formal taxonomic designations are thought to be of critical importance for the conservation of endangered taxa. The Galápagos sea lion (GSL), being appreciated as a key element of the Galápagos marine ecosystem, has lately been listed as 'vulnerable' by the IUCN. To date there is, however, hardly any scientific evidence, whether it constitutes a separate entity from its abundant Californian neighbour (CSL). In this paper, we delineate the taxonomic relationships within the genus Zalophus being comprised of the Galápagos sea lion, the Californian sea lion and the already extinct Japanese sea lion (JSL).
Results
Using a set of different phylogenetic reconstruction approaches, we find support for monophyly of all three taxa without evidence of reticulation events. Molecular clock estimates place time to common ancestry of the Galápagos sea lion and the Californian sea lion at about 2.3 ± 0.5 mya. Genetic separation is further suggested by diagnostic SNPs in the mitochondrial and nuclear genome. Microsatellite markers confirm this trend, showing numerous private alleles at most of the 25 investigated loci. Microsatellite-based estimates of genetic differentiation between the Galápagos sea lion and the Californian sea lion indicate significant genetic differentiation. Gene diversity is 14% lower in the Galápagos sea lion than in the Californian sea lion, but there is no evidence for recent bottleneck events in the Galápagos sea lion.
Conclusion
Based on molecular evidence we build a case for classifying the Galápagos sea lion (Zalophus wollebaeki), the Californian sea lion (Zalophus californianus) and the Japanese sea lion (Zalophus japonicus) as true species. As morphological characters do not necessarily fully reflect the rapid divergence on the molecular level, the study can be considered as a test case for deriving species status from molecular evidence. We further use the results to discuss the role of genetics in conservation policy for an organism that already is under the general protection of the habitat it lives in.
doi:10.1186/1742-9994-4-20
PMCID: PMC2072946  PMID: 17868473
17.  Novel symptomatology and changing epidemiology of domoic acid toxicosis in California sea lions (Zalophus californianus): an increasing risk to marine mammal health 
Harmful algal blooms are increasing worldwide, including those of Pseudo-nitzschia spp. producing domoic acid off the California coast. This neurotoxin was first shown to cause mortality of marine mammals in 1998. A decade of monitoring California sea lion (Zalophus californianus) health since then has indicated that changes in the symptomatology and epidemiology of domoic acid toxicosis in this species are associated with the increase in toxigenic blooms. Two separate clinical syndromes now exist: acute domoic acid toxicosis as has been previously documented, and a second novel neurological syndrome characterized by epilepsy described here associated with chronic consequences of previous sub-lethal exposure to the toxin. This study indicates that domoic acid causes chronic damage to California sea lions and that these health effects are increasing.
doi:10.1098/rspb.2007.1221
PMCID: PMC2593718  PMID: 18006409
amnesic shellfish poisoning; California sea lions; domoic acid; hippocampal atrophy; seizures; harmful algal blooms
18.  Skin histology and its role in heat dissipation in three pinniped species 
Background
Pinnipeds have a thick blubber layer and may have difficulty maintaining their body temperature during hot weather when on land. The skin is the main thermoregulatory conduit which emits excessive body heat.
Methods
Thorough evaluation of the skin histology in three pinniped species; the California sea lion-Zalophus californianus, the Pacific harbor seal-Phoca vitulina richardsi, and the Northern elephant seal-Mirounga angustirostris, was conducted to identify the presence, location and distribution of skin structures which contribute to thermoregulation. These structures included hair, adipose tissue, sweat glands, vasculature, and arteriovenous anastomoses (AVA). Thermal imaging was performed on live animals of the same species to correlate histological findings with thermal emission of the skin.
Results
The presence and distribution of skin structures directly relates to emissivity of the skin in all three species. Emissivity of skin in phocids (Pacific harbor and Northern elephant seals) follows a different pattern than skin in otariids (California sea lions). The flipper skin in phocids tends to be the most emissive region during hot weather and least emissive during cold weather. On the contrary in otariids, skin of the entire body has a tendency to be emissive during both hot and cold weather.
Conclusion
Heat dissipation of the skin directly relates to the presence and distribution of skin structures in all three species. Different skin thermal dissipation patterns were observed in phocid versus otariid seals. Observed thermal patterns can be used for proper understanding of optimum thermal needs of seals housed in research facilities, rescue centers and zoo exhibits.
doi:10.1186/1751-0147-54-46
PMCID: PMC3502088  PMID: 22889205
Skin; Histology; Thermography; Pinnipeds; Thermoregulation
19.  Sublethal toxicant effects with dynamic energy budget theory: application to mussel outplants 
We investigate the effectiveness of a sublethal toxic effect model embedded in Dynamic Energy Budget (DEB) theory for the analysis of field data. We analyze the performance of two species of mussels, Mytilus galloprovincialis and M. californianus, near a diffuser discharging produced water in the Southern California Bight, California. Produced water is a byproduct of oil production consisting of fossil water together with compounds added during the extraction process, and generally contains highly elevated levels of pollutants relative to sea water. Produced water negatively affects the production of somatic and reproductive biomass in both mussel species; we show that these negative effects can be quantified with our DEB-based modeling framework through the estimation of toxic effect scaling parameters. Our analyses reveal that the toxic impact of produced water on growth and reproduction of M. californianus is substantially higher than for M. galloprovincialis. Projections of the expected lifetime production of gonad biomass indicate that the environmental impact of produced water can be as large as 100%, whereas short-term assessment without the use of DEB theory projects a maximum effect of only 30%.
doi:10.1007/s10646-009-0384-4
PMCID: PMC2797407  PMID: 19629682
Toxicity modeling; DEBtox; Dynamic energy budgets; Sublethal effects; Produced water
20.  Lung collapse in the diving sea lion: hold the nitrogen and save the oxygen 
Biology Letters  2012;8(6):1047-1049.
Lung collapse is considered the primary mechanism that limits nitrogen absorption and decreases the risk of decompression sickness in deep-diving marine mammals. Continuous arterial partial pressure of oxygen profiles in a free-diving female California sea lion (Zalophus californianus) revealed that (i) depth of lung collapse was near 225 m as evidenced by abrupt changes in during descent and ascent, (ii) depth of lung collapse was positively related to maximum dive depth, suggesting that the sea lion increased inhaled air volume in deeper dives and (iii) lung collapse at depth preserved a pulmonary oxygen reservoir that supplemented blood oxygen during ascent so that mean end-of-dive arterial was 74 ± 17 mmHg (greater than 85% haemoglobin saturation). Such information is critical to the understanding and the modelling of both nitrogen and oxygen transport in diving marine mammals.
doi:10.1098/rsbl.2012.0743
PMCID: PMC3497143  PMID: 22993241
diving physiology; lung collapse; decompression sickness; marine mammals; partial pressure of oxygen
21.  Underwater audiogram of the California sea lion by the conditioned vocalization technique1 
Conditioning techniques were developed demonstrating that pure tone frequencies under water can exert nearly perfect control over the underwater click vocalizations of the California sea lion (Zalophus californianus). Conditioned vocalizations proved to be a reliable way of obtaining underwater sound detection thresholds in Zalophus at 13 different frequencies, covering a frequency range of 250 to 64,000 Hz. The audiogram generated by these threshold measurements suggests that under water, the range of maximal sensitivity for Zalophus lies between one and 28 kHz with best sensitivity at 16 kHz. Between 28 and 36 kHz there is a loss in sensitivity of 60 dB/octave. However, with relatively intense acoustic signals (> 38 dB re 1 μb underwater), Zalophus will respond to frequencies at least as high as 192 kHz. These results are compared with the underwater hearing of other marine mammals.
Images
doi:10.1901/jeab.1972.17-339
PMCID: PMC1333909  PMID: 5033891
22.  Accuracy of ARGOS Locations of Pinnipeds at-Sea Estimated Using Fastloc GPS 
PLoS ONE  2010;5(1):e8677.
Background
ARGOS satellite telemetry is one of the most widely used methods to track the movements of free-ranging marine and terrestrial animals and is fundamental to studies of foraging ecology, migratory behavior and habitat-use. ARGOS location estimates do not include complete error estimations, and for many marine organisms, the most commonly acquired locations (Location Class 0, A, B, or Z) are provided with no declared error estimate.
Methodology/Principal Findings
We compared the accuracy of ARGOS locations to those obtained using Fastloc GPS from the same electronic tags on five species of pinnipeds: 9 California sea lions (Zalophus californianus), 4 Galapagos sea lions (Zalophus wollebaeki), 6 Cape fur seals (Arctocephalus pusillus pusillus), 3 Australian fur seals (A. p. doriferus) and 5 northern elephant seals (Mirounga angustirostris). These species encompass a range of marine habitats (highly pelagic vs coastal), diving behaviors (mean dive durations 2–21 min) and range of latitudes (equator to temperate). A total of 7,318 ARGOS positions and 27,046 GPS positions were collected. Of these, 1,105 ARGOS positions were obtained within five minutes of a GPS position and were used for comparison. The 68th percentile ARGOS location errors as measured in this study were LC-3 0.49 km, LC-2 1.01 km, LC-1 1.20 km, LC-0 4.18 km, LC-A 6.19 km, LC-B 10.28 km.
Conclusions/Significance
The ARGOS errors measured here are greater than those provided by ARGOS, but within the range of other studies. The error was non-normally distributed with each LC highly right-skewed. Locations of species that make short duration dives and spend extended periods on the surface (sea lions and fur seals) had less error than species like elephant seals that spend more time underwater and have shorter surface intervals. Supplemental data (S1) are provided allowing the creation of density distributions that can be used in a variety of filtering algorithms to improve the quality of ARGOS tracking data.
doi:10.1371/journal.pone.0008677
PMCID: PMC2806907  PMID: 20090942
23.  Killer whales are capable of vocal learning 
Biology Letters  2006;2(4):509-512.
The production learning of vocalizations by manipulation of the sound production organs to alter the physical structure of sound has been demonstrated in only a few mammals. In this natural experiment, we document the vocal behaviour of two juvenile killer whales, Orcinus orca, separated from their natal pods, which are the only cases of dispersal seen during the three decades of observation of their populations. We find mimicry of California sea lion (Zalophus californianus) barks, demonstrating the vocal production learning ability for one of the calves. We also find differences in call usage (compared to the natal pod) that may reflect the absence of a repertoire model from tutors or some unknown effect related to isolation or context.
doi:10.1098/rsbl.2006.0525
PMCID: PMC1834009  PMID: 17148275
marine mammal; learning; acoustics; mimicry
24.  Linking Reproduction and Survival Can Improve Model Estimates of Vital Rates Derived from Limited Time-Series Counts of Pinnipeds and Other Species 
PLoS ONE  2013;8(11):e77389.
We propose a method to model the physiological link between somatic survival and reproductive output that reduces the number of parameters that need to be estimated by models designed to determine combinations of birth and death rates that produce historic counts of animal populations. We applied our Reproduction and Somatic Survival Linked (RSSL) method to the population counts of three species of North Pacific pinnipeds (harbor seals, Phoca vitulina richardii (Gray, 1864); northern fur seals, Callorhinus ursinus (L., 1758); and Steller sea lions, Eumetopias jubatus (Schreber, 1776))—and found our model outperformed traditional models when fitting vital rates to common types of limited datasets, such as those from counts of pups and adults. However, our model did not perform as well when these basic counts of animals were augmented with additional observations of ratios of juveniles to total non-pups. In this case, the failure of the ratios to improve model performance may indicate that the relationship between survival and reproduction is redefined or disassociated as populations change over time or that the ratio of juveniles to total non-pups is not a meaningful index of vital rates. Overall, our RSSL models show advantages to linking survival and reproduction within models to estimate the vital rates of pinnipeds and other species that have limited time-series of counts.
doi:10.1371/journal.pone.0077389
PMCID: PMC3855591  PMID: 24324541
25.  Inter-Population Movements of Steller Sea Lions in Alaska with Implications for Population Separation 
PLoS ONE  2013;8(8):e70167.
Genetic studies and differing population trends support the separation of Steller sea lions (Eumetopias jubatus) into a western distinct population segment (WDPS) and an eastern DPS (EDPS) with the dividing line between populations at 144° W. Despite little exchange for thousands of years, the gap between the breeding ranges narrowed during the past 15–30 years with the formation of new rookeries near the DPS boundary. We analyzed >22,000 sightings of 4,172 sea lions branded as pups in each DPS from 2000–2010 to estimate probabilities of a sea lion born in one DPS being seen within the range of the other DPS (either ‘West’ or ‘East’). Males from both populations regularly traveled across the DPS boundary; probabilities were highest at ages 2–5 and for males born in Prince William Sound and southern Southeast Alaska. The probability of WDPS females being in the East at age 5 was 0.067 but 0 for EDPS females which rarely traveled to the West. Prince William Sound-born females had high probabilities of being in the East during breeding and non-breeding seasons. We present strong evidence that WDPS females have permanently emigrated to the East, reproducing at two ‘mixing zone’ rookeries. We documented breeding bulls that traveled >6,500 km round trip from their natal rookery in southern Alaska to the northern Bering Sea and central Aleutian Islands and back within one year. WDPS animals began moving East in the 1990s, following steep population declines in the central Gulf of Alaska. Results of our study, and others documenting high survival and rapid population growth in northern Southeast Alaska suggest that conditions in this mixing zone region have been optimal for sea lions. It is unclear whether eastward movement across the DPS boundary is due to less-optimal conditions in the West or a reflection of favorable conditions in the East.
doi:10.1371/journal.pone.0070167
PMCID: PMC3734025  PMID: 23940543

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