Ecological implications of unprecedented warm water anomalies on interannual prey preferences and foraging areas of Guadalupe fur seals

The Guadalupe fur seal (GFS) currently is recovering from near extinction and prey availability is an important factor. Scat and stable isotope analyses (SIA) were used to assess GFS foraging on Guadalupe Island during 2013–2016. This period was characterized by normal (2013) ocean temperatures followed by warm conditions (2014–2016). Scat samples (~40/year) were collected for prey identification. Additionally, lanugo samples from 1-month-old pups (50/year) were processed for SIA (δ¹³C/δ¹⁵N). Interannual prey preferences were identified (ANOSIM, p < .05), including significant differences between 2013 and the anomalous years. The most important prey species among these years was the jumbo squid; followed by the neon flying squid (2014–2016). The GFS diet was more specialized in 2013–2015 and more generalized in 2016. Prey from higher trophic levels (determined by scat analysis) were consumed during 2014–2016, but with significantly lower δ¹³C/δ¹⁵N values than in 2013 (ANOVA, p < .05 for both isotope ratios). This pattern may indicate more northerly or offshore foraging areas, with the presence of oceanic prey (neon flying squid). The widest isotopic niche was observed in 2015 (2.2‰²), reflecting a broader foraging area. Our findings are an important step toward better understanding the impacts of climate change on the recovery of GFS.     

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.     

Niche overlap and habitat use at distinct temporal scales among the California sea lions (Zalophus californianus) and Guadalupe fur seals (Arctocephalus philippii townsendi)

The aim of this study was to determine the trophic level, trophic breadth, and dietary overlap of two species of otariids (Zalophus californianus and Arctocephalus philippii townsendi) at the San Benito Islands in Baja California, Mexico, using scat analysis, and stable isotope analyses (SIA) of carbon and nitrogen in pup hair and dental collagen. Scat samples were collected during summer and winter. The most important prey for both species during summer was squid, comprising 74% of the A. p. townsendi diet and 45% of that of Z. californianus. In winter, squid was 87% of the A. p. townsendi diet, whereas fish was the predominant food (76%) for Z. californianus. Both species were specialist feeders and reached maximum trophic overlap during the summer (C_H = 0.9). SIA of the hair of otariid pups showed significant differences in δ¹⁵N (P = 0.001), coinciding with A. p. townsendi's greater consumption of squid. The average δ¹³C value was significantly lower for A. p. townsendi (?16.3‰ ± 0.2‰), reflecting the species' consumption of squid from pelagic habitats, whereas that of Z. californianus (?15.9‰ ± 0.3‰) was significantly higher, reflecting their consumption of benthic fish. Difference in habitat use was confirmed in δ¹³C values of dental collagen.     

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.     

Incorporating uncertainty in spatial structure for viability predictions: a case study of California sea lions (Zalophus californianus californianus)

In recent years, population viability analysis has become a popular tool to assess the relative risk of extinction among populations. Viability estimates for spatially structured populations require movement data that are often unavailable. In this paper, a diffusion approximation model was used to explore the effects of different spatial scenarios resulting from assumptions about movement rates. Census data for 13 breeding islands occupied by California sea lions Zalophus californianus californianus in the Gulf of California were used to explore three potential scenarios: unlimited movement between sites (panmictic population), limited movement (several clusters of populations) and no movement between islands (isolated islands). Predicted viability estimates were different for each scenario, but contrary to expectations, the mean extinction risk estimates were generally lowest when movement was unlimited (panmictic scenario). However, despite an extensive dataset, the confidence of the viability predictions for each scenario was low. In some cases, uncertainty in predictions within a scenario was greater than differences between scenarios. Therefore, it is recommended that in situations where movement rates and spatial structure are unknown, extinction risk estimates should reflect both the confidence intervals for each risk estimate and the uncertainty resulting from different spatial scenarios. This study also provides the first estimate of population viability (considering spatial structure) for California sea lions in the Gulf of California and an evaluation of population status based on the IUCN criteria for species listing.     

Surface temperature patterns in seals and sea lions: A validation of temporal and spatial consistency

We assessed infrared thermography (IRT) as a tool for evaluating spatial and temporal surface temperature patterns in juvenile female harbor seals (Phoca vitulina, n=6) and adult female Steller sea lions (Eumetopias jubatus, n=2). Following a technical assessment of the influence of environmental parameters on the specific camera to be used, we identified regional and seasonal variability of surface temperatures. Variation was observed in several seasonal transitions (winter, reproductive, molt) in ten monitored body regions. Spatially and temporally consistent thermal patterns in the shoulder, axillae, foreflipper and hindflipper suggest thermal windows in both species.     

Whisker isotopic signature depicts migration patterns and multi-year intra- and inter-individual foraging strategies in fur seals

The movement and dietary history of individuals can be studied using stable isotope records in archival keratinous tissues. Here, we present a chronology of temporally fine-scale data on the trophic niche of otariid seals by measuring the isotopic signature of serially sampled whiskers. Whiskers of male Antarctic fur seals breeding at the Crozet Islands showed synchronous and regular oscillations in both their δ¹³C and δ¹⁵N values that are likely to represent their annual migrations over the long term (mean 4.8 years). At the population level, male Antarctic fur seals showed substantial variation in both δ¹³C and δ¹⁵N values, occupying nearly all the ‘isotopic space’ created by the diversity of potential oceanic habitats (from high Antarctica to the subtropics) and prey (from Antarctic krill to subantarctic and subtropical mesopelagic fishes). At the individual level, whisker isotopic signatures depict a large diversity of foraging strategies. Some seals remained in either subantarctic or Antarctic waters, while the migratory cycle of most animals encompassed a wide latitudinal gradient where they fed on different prey. The isotopic signature of whiskers, therefore, revealed new multi-year foraging strategies of male Antarctic fur seals and is a powerful tool for investigating the ecological niche during cryptic stages of mammals'' life.     

USING CARBON AND NITROGEN ISOTOPE VALUES TO INVESTIGATE MATERNAL STRATEGIES IN NORTHEAST PACIFIC OTARIIDS

We examine the utility of stable carbon and nitrogen isotope variations to characterize the length of the nursing/lactation period and age at weaning for two northern Pacific otariid species, the northern fur seal (Callorhinus ursinus) and California sea lion (Zalophus californianus). We used two sampling strategies to measure ontogenetic trends in isotope value, and compared our results to observational data on the reproductive strategies used by these otariids. For Zalophus, we found evidence for ¹⁵N enrichment and ¹³C‐depletion in bone collagen representing the first and second year of growth, which is consistent with the ～12–14‐mo weaning age in this population after a suitable turnover rate for bone collagen is considered. Analysis of individual tooth annuli from a different suite of Zalophus specimens suggests that half of the individuals were weaned at ～12 mo of age, and half were dependent on milk for a portion of their second year. For Callorhinus, bone collagen for age classes that contain pre‐weaned individuals were ¹⁵N‐enriched, but values were significantly lower in specimens between 6 and 20 mo of age. These ¹⁵N‐enriched values, presumably acquired during nursing between 0 and 4 mo of age in Callorhinus, were not present in specimens older than 12 mo of age. Thus complete bone collagen turnover in young‐of‐the‐year occurs in 8–10 mo. ¹⁵N enrichment is evident in the first annulus of female Callorhinus individuals, but is not detectable in males. Analyses of Callorhinus tooth annuli show no ontogenetic trends in δ¹³C values. Our study indicates that nitrogen, and in some cases carbon, isotopes can be used to assess reproductive strategies in marine mammals. When coupled with accurate age estimates based on bone growth regressions, this isotopic technique can be applied to historical or fossil otariids to gain insight into the flexibility of maternal strategies within and across species.     

Accuracy and precision of age determination using growth layer groups for California sea lions (Zalophus californianus) with known ages

Age determination from counts of growth layer groups (GLGs) in tooth dentine is a common method for aging marine mammals. Using known‐aged animals, we validated this method for acid etched teeth of California sea lions (CSLs), Zalophus californianus. Between 1991 and 2013, the upper left canine (n = 33) was collected opportunistically during necropsy from animals tagged or branded as pups that later died. Overall, 55%–61% of age estimates by GLG counting were within 1 yr of the known‐age in the sample of 1–30‐yr‐old CSLs. Accuracy of age estimates was found to be dependent on age of the CSLs, however. 71%–79% of age estimates were within 1 yr of the known‐age in CSLs <10 yr old. These findings support the validity of counting GLGs to estimate age for CSLs <10 yr old to within 1 yr of accuracy.     

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.     

Movement, dive behavior, and survival of California sea lions (Zalophus californianus) posttreatment for domoic acid toxicosis

Domoic acid (DA) is a neuroexcitatory toxin increasingly causing strandings and mortality of marine mammals. The hippocampus of mammalian brains, associated with learning, memory, and spatial navigation, is one of the predominant regions affected by DA exposure. California sea lions stranding from 2003 to 2006 as a result of DA toxicosis were classified as having acute ( n = 12) or chronic neurologic ( n = 22) clinical signs. Chronic neurologic cases were examined by magnetic resonance imaging to determine the extent of brain damage related to DA exposure. Brain damage included hippocampal and parahippocampal atrophy, temporal horn enlargement, and pathological T2 hyperintensity. Posttreatment, animals were fitted with satellite transmitters and their movement and dive behaviors compared with those of a control group. The only significant difference between acute and chronic animals was distance traveled per day. There were, however, significant differences between chronic neurologic cases and controls: chronic neurologic cases dove shallower for shorter durations, traveled further from shore, and spent less time hauled out and more time surface swimming than control animals. There was no relationship between severity of brain damage and behavioral patterns for chronic neurologic cases. Sea lions with chronic neurologic changes had a poor prognosis for survival following release.     

Analysis of growth and stable isotopes in teeth of male Australian fur seals reveals interannual variability in prey resources

To detect and monitor long‐term ecosystem responses to environmental variability, managers must utilize reliable and quantitative techniques to predict future ecosystem responses. Canine teeth from 67 male Australian fur seals (aged 2–19 yr), collected at Seal Rocks, between 1967 and 1976, were measured for relative growth within the dentine growth layer groups (GLGs), as an index of body growth. Fluctuations in relative growth were apparent during 1956–1971, suggesting interannual variation in prey resources within Bass Strait. These were positively correlated with the Southern Oscillation Index and negatively with the Indian Ocean Subtropical Dipole, both on a 2 yr lag. The observed delay may reflect the time required for the nutrient cascade to filter through to the predominantly benthic prey of Australian fur seals. Stable isotope analysis (δ¹⁵N/δ¹³C) was also used to investigate whether fluctuations in growth were associated with differences in diet. Relative growth was found to be negatively correlated with δ¹⁵N, suggesting years of greater resource availability may be associated with individuals consuming proportionally more prey biomass of lower isotopic value. This study demonstrates that fluctuations in the dentine GLGs of male Australian fur seals are related to environmental parameters, suggesting variation in body growth is mediated by changes in prey resources.     

Visitor effects on a zoo population of California sea lions (Zalophus californianus) and harbor seals (Phoca vitulina)

The effects of visitor presence on zoo and aquarium animals have become increasingly well studied, using measures such as behavioral responses and exhibit usage. Many taxa remain underrepresented in this literature; this is the case for marine mammals, despite widespread public concern for their welfare in managed care settings. The current study therefore used behavioral activity budgets and exhibit usage to assess the responses of California sea lions (Zalophus californianus) and harbor seals (Phoca vitulina) to visitors at the Seal Cove exhibit at Six Flags Discovery Kingdom, Vallejo CA. Data was collected via focal follow video recordings over the summer season of 2016, and analyzed using MANCOVAs, discriminant analyses, and modified Spread of Participation Indices. The sea lions showed no significant changes in behavior when visitors were present, but did show greater preference for the water bordering visitor viewing areas during these times. Two sea lions gave birth during the study period, and showed greater preference for land areas both adjacent to and out of sight of visitors when nursing compared to while pregnant. In contrast, the harbor seals showed significant behavioral changes in the presence of visitors, including increased vigilance and feeding. This was associated with increased preferential use of water areas adjacent to the visitor viewing area. Visitors were able to purchase fish to throw to the animals, which likely contributed to the differences observed. Overall, this study found little evidence for negative visitor impacts on two pinniped species in a zoo setting.     

Influence of colony size on pup fitness and survival in South American sea lions

Increased terrestrial pup mortality in small colonies due to harassment by subadult males has been proposed as a mechanism to explain the stagnation of South American sea lion populations after sealing ended. To test this hypothesis, pup survival rate was assessed in five northern Patagonia colonies with different sizes. Female diet quality as well as pup growth rate and immune status from the largest and smallest of these colonies were also assessed. Results indicated that the pup survival rate increased with colony size and pup‐to‐subadult male ratio. Furthermore, pups grew faster in the smallest colony, although female diet composition and pup immune status did not differ between the two colonies. Inverse relationship between pup growth rate and survival rate indicated that mortality was independent of food supply. In absence of terrestrial predators, infanticide by subadult males is the only mortality source other than starvation and illness and the relationship between pup survival rate and pup‐to‐subadult male ratio approached a type II functional response curve. Thus, infanticide stands as the most likely reason for the observed positive relationship between colony size and pup survival rate, supporting the hypothesis that post‐sealing population stasis was caused by inverse density dependence.     

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.     

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.     

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.     

Temporal variability in stable isotope ratios of C and N in the vibrissa of captive and wild adult South American sea lions Otaria byronia: More than just diet shifts

We analyzed the δ¹³C and δ¹⁵N values in the vibrissae of captive adult breeding South American sea lions (Otaria byronia) fed at a constant diet and then used this information to analyze the change in stable isotope values along the vibrissae from wild individuals. The overall diet‐to‐vibrissa discrimination factor of the captive animals was 3.0‰ ± 0.1‰ for δ¹³C and 3.6‰ ± 0.1‰ for δ¹⁵N, but the stable isotope ratios fluctuated periodically despite constant diet. The δ¹³C and δ¹⁵N values of the captive male declined at the end of the breeding season, whereas the δ¹³C values of the female increased during the central part of pregnancy and the δ¹⁵N values peaked during lactation. The δ¹³C and δ¹⁵N values of adult wild specimens also fluctuated periodically and vibrissae growth rate (0.15 mm/d in both sexes) was slightly lower than in captivity (0.17 mm/d), assuming an annual periodicity for oscillations. Similarities in the amplitude of the cycles of captive and wild males suggested that fasting was probably the main source of periodic variability in the δ¹⁵N of wild males, whereas pregnancy and lactation were probably the main source of periodic variability for the δ¹³C of wild females.