Interannual variation in the at‐sea behavior of California sea lions (Zalophus californianus)

To be successful, marine predators must alter their foraging behavior in response to changes in their environment. To understand the impact and severity of environmental change on a population it is necessary to first describe typical foraging patterns and identify the underlying variability that exists in foraging behavior. Therefore, we characterized the at‐sea behavior of adult female California sea lions (n = 32) over three years (2003, 2004, and 2005) using satellite transmitters and time‐depth recorders and examined how foraging behavior varied among years. In all years, sea lions traveled on average 84.7 ± 11.1 km from the rookery during foraging trips that were 3.2 ± 0.3 d. Sea lions spent 42.7% ± 1.9% of their time at sea diving and displayed short (2.2 ± 0.2 min), shallow dives (58.5 ± 8.5 m). Among individuals, there was significant variation in both dive behavior and movement patterns, which was found in all years. Among years, differences were found in trip durations, distances traveled, and some dive variables (e.g., dive duration and bottom time) as sea lions faced moderate variability in their foraging habitat (increased sea‐surface temperatures, decreased upwelling, and potential decreased prey abundance). The flexibility we found in the foraging behavior of California sea lions may be a mechanism to cope with environmental variability among years and could be linked to the continuing growth of sea lion populations.     

Habitat use and spatial fidelity of male South American sea lions during the nonbreeding period

Conditions experienced during the nonbreeding period have profound long‐term effects on individual fitness and survival. Therefore, knowledge of habitat use during the nonbreeding period can provide insights into processes that regulate populations. At the Falkland Islands, the habitat use of South American sea lions (Otaria flavescens) during the nonbreeding period is of particular interest because the population is yet to recover from a catastrophic decline between the mid‐1930s and 1965, and nonbreeding movements are poorly understood. Here, we assessed the habitat use of adult male (n = 13) and juvenile male (n = 6) South American sea lions at the Falkland Islands using satellite tags and stable isotope analysis of vibrissae. Male South American sea lions behaved like central place foragers. Foraging trips were restricted to the Patagonian Shelf and were typically short in distance and duration (127 ± 66 km and 4.1 ± 2.0 days, respectively). Individual male foraging trips were also typically characterized by a high degree of foraging site fidelity. However, the isotopic niche of adult males was smaller than juvenile males, which suggested that adult males were more consistent in their use of foraging habitats and prey over time. Our findings differ from male South American sea lions in Chile and Argentina, which undertake extended movements during the nonbreeding period. Hence, throughout their breeding range, male South American sea lions have diverse movement patterns during the nonbreeding period that intuitively reflects differences in the predictability or accessibility of preferred prey. Our findings challenge the long‐standing notion that South American sea lions undertake a winter migration away from the Falkland Islands. Therefore, impediments to South American sea lion population recovery likely originate locally and conservation measures at a national level are likely to be effective in addressing the decline and the failure of the population to recover.     

Aerial hearing thresholds and detection of hearing loss in male California sea lions (Zalophus californianus) using auditory evoked potentials

Auditory evoked potential (AEP) measurements are useful for describing the variability of hearing among individuals in marine mammal populations, an important consideration in terms of basic biology and the design of noise mitigation criteria. In this study, hearing thresholds were measured for 16 male California sea lions at frequencies ranging from 0.5 to 32 kHz using the auditory steady state‐response (ASSR), a frequency‐specific AEP. Audiograms for most sea lions were grossly similar to previously reported psychophysical data in that hearing sensitivity increased with increasing frequency up to a steep reduction in sensitivity between 16 and 32 kHz. Average thresholds were not different from AEP thresholds previously reported for male and female California sea lions. Two sea lions from the current study exhibited abnormal audiograms: a 26‐yr‐old sea lion had impaired hearing with a high‐frequency hearing limit (HFHL) between 8 and 16 kHz, and an 8‐yr‐old sea lion displayed elevated thresholds across most tested frequencies. The auditory brainstem responses (ABRs) for these two individuals and an additional 26‐yr‐old sea lion were aberrant compared to those of other sea lions. Hearing loss may have fitness implications for sea lions that rely on sound during foraging and reproductive activities.     

The energetic consequences of behavioral variation in a marine carnivore

Intraspecific variability in foraging behavior has been documented across a range of taxonomic groups, yet the energetic consequences of this variation are not well understood for many species. Understanding the effect of behavioral variation on energy expenditure and acquisition is particularly crucial for mammalian carnivores because they have high energy requirements that place considerable pressure on prey populations. To determine the influence of behavior on energy expenditure and balance, we combined simultaneous measurements of at‐sea field metabolic rate (FMR) and foraging behavior in a marine carnivore that exhibits intraspecific behavioral variation, the California sea lion (Zalophus californianus). Sea lions exhibited variability in at‐sea FMR, with some individuals expending energy at a maximum of twice the rate of others. This variation was in part attributable to differences in diving behavior that may have been reflective of diet; however, this was only true for sea lions using a foraging strategy consisting of epipelagic (<200 m within the water column) and benthic dives. In contrast, sea lions that used a deep‐diving foraging strategy all had similar values of at‐sea FMR that were unrelated to diving behavior. Energy intake did not differ between foraging strategies and was unrelated to energy expenditure. Our findings suggest that energy expenditure in California sea lions may be influenced by interactions between diet and oxygen conservation strategies. There were no apparent energetic trade‐offs between foraging strategies, although there was preliminary evidence that foraging strategies may differ in their variability in energy balance. The energetic consequences of behavioral variation may influence the reproductive success of female sea lions and result in differential impacts of individuals on prey populations. These findings highlight the importance of quantifying the relationships between energy expenditure and foraging behavior in other carnivores for studies addressing fundamental and applied physiological and ecological questions.     

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.     

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.     

Steller sea lion spatial‐use patterns derived from a Bayesian model of opportunistic observations

Despite acquisition of a substantial catalog of telemetry data from Steller sea lions (Eumetopias jubatus) over the past two decades, scientists still lack comprehensive regionally explicit knowledge about Steller sea lion habitat use. The Platforms of Opportunity data contain records of Steller sea lion sightings throughout the species’ entire range and have potential to fill gaps in knowledge about their spatial use; however, the data have not previously been used because effort (e.g., time spent surveying or area sampled) was not recorded when sightings were obtained. For this study a novel approach was used to overcome the lack of effort data through development of an effort index and a Bayesian negative binomial model. The model quantified Steller sea lion encounter rates and associated uncertainty within 15 × 15 km² grid cells across the species’ entire range. Year‐round, as well as breeding and nonbreeding season encounter rates were estimated. The results of this analysis identify several previously undocumented areas of high use by Steller sea lions, indicate that only 37% of Steller sea lion high‐use areas fall within designated critical habitat, and demonstrate that use of depth and distance from shore as indicators of Steller sea lion habitat is contraindicated.     

PINNIPED POPULATION DYNAMICS IN CENTRAL CALIFORNIA: CORRELATIONS WITH SEA SURFACE TEMPERATURE AND UPWELLING INDICES

We investigated effects of marine climate variability on pinniped populations and assessed the initial stages of recovery following implementation of the U. S. Marine Mammal Protection Act (MMPA) based on long-term (1973-1997) population surveys at the South Farallon Islands and Point Reyes Peninsula, central California. California sea lions increased over the study period, with peak numbers observed during and after major El Niño events. The rate of increase for California sea lions appears to have decreased in recent years. Steller sea lions decreased at the South Farallon Islands and remain depleted at Point Reyes Peninsula. Harbor seal populations increased in a logistic and non-linear fashion at Point Reyes Peninsula and the South Farallon Islands, respectively. Harbor seals were more abundant at the South Farallon Islands during years of relatively high sea-surface temperature, which may be related to their inability to find sufficient prey in coastal waters under these conditions. Northern elephant seal abundance increased in a logistic fashion over the study period at both the South Farallon Islands and Point Reyes Peninsula; however, productivity at the South Farallon Islands decreased in recent years. Maximum haulout numbers for elephant seals at the South Farallon Islands increased in the 1970s, maintained an asymptote throughout the 1980s and early 1990s, but recently declined; additional studies are needed to investigate which age classes are associated with this decline. Protection afforded by the MMPA has facilitated partial to full recovery of all populations except for Steller sea lion. Oceanographic relationships do not appear to confound interpretations of population recovery and may help to explain changes in the Steller sea lion population.     

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.     

Using Mountain Lion Habitat Selection in Management

Wildlife agencies are generally tasked with managing and conserving species at state and local levels simultaneously. Thus, it is necessary for wildlife agencies to understand basic ecological processes of a given species at multiple scales to aid decision making at commensurately varied spatial and behavioral scales. Mountain lions (Puma concolor) occur throughout California, USA, and are at the center of a variety of management and conservation issues. For example, they are genetically and demographically at risk in 1 region yet apparently stable and negatively affecting endangered species in another. Currently, no formal plan exists for mountain lions in California to deal with these diverse scenarios involving issues of local mountain lion population viability and problems related to predation of endangered species. To facilitate development of a state-wide management and conservation plan, we quantified habitat selection by mountain lions at 2 spatial scales across the range of environmental conditions in which the species is found in California. Our analyses used location data from individuals (n = 263) collared across the state from 2001–2019. At the home range scale, mountain lions selected habitat to prioritize meeting energetic demands. At the within home range scale, mountain lions avoided areas of human activity. Further, our analyses revealed 165,350–170,085 km², depending on season, of suitable mountain lion habitat in California. Fifty percent of the suitable habitat was on unprotected lands and thus vulnerable to development. These habitat selection models will help in the development of a state-wide conservation and management plan for mountain lions in California by guiding mountain lion population monitoring through time, prioritization of habitat to be conserved for maintaining demographic connectivity and gene flow, and efforts to mediate mountain lion-prey interactions. Our work and application area will help with wildlife policy and management decisions related to depredation problems at the local scale and issues of habitat connectivity at the statewide scale. © 2019 The Wildlife Society.     

In the absence of a “landscape of fear”: How lions,hyenas, and cheetahs coexist

Aggression by top predators can create a “landscape of fear” in which subordinate predators restrict their activity to low‐risk areas or times of day. At large spatial or temporal scales, this can result in the costly loss of access to resources. However, fine‐scale reactive avoidance may minimize the risk of aggressive encounters for subordinate predators while maintaining access to resources, thereby providing a mechanism for coexistence. We investigated fine‐scale spatiotemporal avoidance in a guild of African predators characterized by intense interference competition. Vulnerable to food stealing and direct killing, cheetahs are expected to avoid both larger predators; hyenas are expected to avoid lions. We deployed a grid of 225 camera traps across 1,125 km² in Serengeti National Park, Tanzania, to evaluate concurrent patterns of habitat use by lions, hyenas, cheetahs, and their primary prey. We used hurdle models to evaluate whether smaller species avoided areas preferred by larger species, and we used time‐to‐event models to evaluate fine‐scale temporal avoidance in the hours immediately surrounding top predator activity. We found no evidence of long‐term displacement of subordinate species, even at fine spatial scales. Instead, hyenas and cheetahs were positively associated with lions except in areas with exceptionally high lion use. Hyenas and lions appeared to actively track each, while cheetahs appear to maintain long‐term access to sites with high lion use by actively avoiding those areas just in the hours immediately following lion activity. Our results suggest that cheetahs are able to use patches of preferred habitat by avoiding lions on a moment‐to‐moment basis. Such fine‐scale temporal avoidance is likely to be less costly than long‐term avoidance of preferred areas: This may help explain why cheetahs are able to coexist with lions despite high rates of lion‐inflicted mortality, and highlights reactive avoidance as a general mechanism for predator coexistence.     

Isolation by distance among California sea lion populations in Mexico: redefining management stocks

Understanding the spatial structure of a population is critical for effective assessment and management. However, direct observation of spatial dynamics is generally difficult, particularly for marine mammals. California sea lions ( Zalophus californianus ) are polygynous pinnipeds distributed along the Pacific coast of North America. The species' range has been subdivided into three management stocks based on differences in mitochondrial DNA, but to date no studies have considered nuclear genetic variation, and thus we lack a comprehensive understanding of gene flow patterns among sea lion colonies. In light of recent population declines in the Gulf of California, Mexico, it is important to understand spatial structure to determine if declining sea lion colonies are genetically isolated from others. To define population subdivision and identify sex biases in gene flow, we analysed a 355-bp sequence of the mitochondrial DNA control region and 10 polymorphic microsatellite loci from 355 tissue samples collected from six colonies distributed along Mexican waters. Using a novel approach to estimate sex biases in gene flow, we found that male sea lions disperse on average 6.75 times more frequently than females. Analyses of population subdivision strongly suggest a pattern of isolation by distance among colonies and challenge current stock definitions. Based on these results, we propose an alternative classification that identifies three Mexican management units: Upper Gulf of California, Southern Baja Peninsula, and Upper Pacific Coast of Baja. This revised classification should be considered in future assessment and management of California sea lion populations in Mexican waters.     

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.     

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.     

Characterization of eight microsatellite loci in Steller sea lions (Eumetopias jubatus)

Steller sea lions (Eumetopias jubatus) are listed as an endangered species in western Alaska and have exhibited a significant population decline throughout their range. Eight microsatellite loci were isolated from genomic DNA libraries. In addition, all these markers were found to be variable in nine individuals of the California sea lion (Zalophus californicus). This panel of markers was developed to analyse population structure in Steller sea lions throughout their range.     

Linking seasonal distribution patterns with prey availability in a central-place forager, the Steller sea lion

Aim We used a novel approach to infer foraging areas of a central‐place forager, the Steller sea lion (Eumetopias jubatus), by assessing changes in the temporal and spatial distribution patterns of sea lions at terrestrial sites. Specifically, our objectives were (1) to classify seasonal distribution patterns of Steller sea lions and (2) to determine to what extent the seasonal distribution of Steller sea lions is explained by seasonal concentrations of prey. Location Southeast Alaska, USA. Methods Steller sea lions of all age classes were counted monthly (2001–04) by aerial surveys at 28 terrestrial sites. Hierarchical cluster analysis and principal components analysis were used to classify seasonal distribution patterns of Steller sea lions at these terrestrial sites. We estimated the proportion of sea lions in the study area that were associated with each seasonal distribution pattern. Results Multivariate ordination techniques revealed four distinct seasonal distributional patterns. During December, 55% of the sea lions in the study area were found at Type 1 sites, located near over‐wintering herring aggregations. During May, 56% of sea lions were found at Type 2 sites, near aggregations of spring‐spawning forage fish. In July, 78% of sea lions were found at Type 3 sites, near summer migratory corridors of salmon. During September, 44% of sea lions were found at Type 4 sites, near autumn migratory corridors of salmon. Main conclusions Seasonal attendance patterns of sea lions were commonly associated with the seasonal availability of prey species near terrestrial sites and reflected seasonal foraging patterns of Steller sea lions in Southeast Alaska. A reasonable annual foraging strategy for Steller sea lions is to forage on herring (Clupea pallasii) aggregations in winter, spawning aggregations of forage fish in spring, salmon (Oncorhynchus spp.) in summer and autumn, and pollock (Theragra chalcogramma) and Pacific hake (Merluccius productus) throughout the year. The seasonal use of haulouts by sea lions and ultimately haulout‐specific foraging patterns of Steller sea lions depend in part upon seasonally available prey species in each region.     

SEASONAL DISTRIBUTION OF STELLER'S SEA LIONS AT ROOKERIES AND HAUL-OUT SITES IN ALASKA

The Steller's sea lion population has declined by 60%-70% over much of Alaska since the late 1970s. Overlap in species composition and sizes of fishes consumed by sea lions and harvested by commercial fisheries, particularly during winter, has led to examination of potential interaction between commercial fisheries and Steller's sea lions. Abundance and distribution data for Steller's sea lions in Alaska were derived from aerial surveys conducted during the breeding season, mid-June to early July 1992, 1994, and 1996. To study winter distribution of sea lions, we conducted aerial surveys during March 1993, November-December 1994, and March 1999. We counted about one-half as many sea lions during winter surveys compared to the breeding-season surveys. Numbers of sea lions at rookery sites dropped off considerably during winter, whereas numbers at haul-out sites did not. We found little evidence of large-scale, seasonal movement, at least for the western stock of sea lions. Rather, differences between summer and winter distribution were primarily a function of sea lions dispersing to local haul-out sites during the winter. Terrestrial sites, both rookeries and haul-outs, clearly are important to Steller's sea lions during the entire year. Individual sites may be occupied year-round or only during particular times of year.     

Olfactory Enrichment in California Sea Lions (Zalophus californianus): An Effective Tool for Captive Welfare?

In the wild, California sea lions (Zalophus californianus) are exposed to a wide variety of sensory information, which cannot be replicated in captive environments. Therefore, unique procedures are necessary for maintaining physiological and psychological health in nonhuman animals in captivity. The effects of introducing natural scents to captive enclosures have been investigated in a variety of species, yet they have not been examined in marine mammals. This project explored the behavioral effect of scent added to the environment, with the goal of improving the welfare of sea lions in captivity. Two scent types were introduced: (a) natural scents, found in their native environment, and (b) non-natural scents, not found in their native environment. This study examined not only scent enrichment but also the possible evolutionary underpinnings of pinniped olfaction. Scent enrichment was found to significantly impact sea lion behavior as demonstrated by a reduction in pattern swimming, an increase in habitat utilization, and a reduction in stereotypical behavior. However, there were no differences in behavior between natural and non-natural scent conditions.     

Spatial patterns and scaling behaviors of Steller sea lion (Eumetopias jubatus) distributions and their environment

Fractal geometry and other multi-scale analyses have become popular tools for investigating spatial patterns of animal distributions in heterogeneous environments. In theory, changes in patterns of animal distributions with changes in scale reflect transitions between the controlling influences of one environmental factor or process over another. In an effort to find linkages between Steller sea lions (Eumetopias jubatus) and their environment, the objective of this study was to determine if the spatial distribution of Steller sea lions at sea displayed similar scaling properties to the variation of two environmental features, including bathymetry and sea surface temperature (SST). Additionally, distributions of Steller sea lion point patterns were examined with respect to measurements of bathymetric complexity. From February 2000 to May 2004, satellite transmitters were deployed on 10 groups of juvenile Steller sea lions (n=52) at eight different locations within the Aleutian Islands and Gulf of Alaska. Indices of fractal dimension were calculated for each group of sea lions using a unit square box-counting method, whereas indices of bathymetry and SST patchiness were derived by conducting a variance ratio analysis over the same scales. Distributions of Steller sea lions at sea displayed self-similar fractal patterns, suggesting that individuals were distributed in a continuous hierarchical set of clumps within clumps across scales, and foraging behavior was likely influenced by a scale invariant mechanism. Patterns of bathymetric variability also were self-similar, whereas patterns of SST variability were scale dependent and failed to retain self-similar spatial structure at larger scales. These results indicate that the distributions of Steller sea lions at sea were more influenced by bathymetry than SST at the scales examined, but scale-dependent patterns in the distribution of Steller sea lions at sea or linkages with SST may have been apparent if analyses were conducted at finer spatial scales.