Female Northern Elephant Seals Research Articles

Foraging Segregation Between Adult Female Northern Elephant Seals (Mirounga angustirostris) from Guadalupe Island and the San Benito Archipelago, Mexico

Female northern elephant seals (Mirounga angustirostris) are migratory animals that form colonies along the coasts of California and the Baja California Peninsula, Mexico. A recent decline in abundance has been recorded in this species Mexican distribution, which is an important reason to investigate the different ecological processes operating in these colonies. The aim of this study was to determine values of stable isotope ratios (δ13C and δ15N) in pup fur as foraging maternal indicators. During the same breeding season (2015), pup fur samples were collected to investigate these foraging variations between the two major Mexican colonies—Guadalupe Island (GI) and the San Benito Archipelago (SBA). Isotopic areas were built using the ‘SIBER’ package in R, and a custom hierarchical Bayesian model was used to compare the values from both localities. Mean (± standard deviation [SD]) δ13C values for individuals from GI and the SBA were -16.9 ± 0.8‰ and -17.3 ± 0.4‰, respectively, while δ15N values were 17.4 ± 1.1‰ and 16.7 ± 1.1‰, respectively. The difference between the posterior means indicated a high probability (P > 99%) of GI having higher stable isotope ratio values than the SBA. For the posterior SDs, there were highly probable differences (P = 100%) only for δ13C, where GI had a higher dispersion. Such differences explained why GI presented a wider isotopic niche area than the SBA, indicating more diverse foraging habits along GI’s offshore-inshore gradient. Additionally, GI showed higher δ15N values than the SBA. Although this could be related to a slightly higher trophic position for GI individuals, the latitudinal effects of foraging grounds with distinct isotopic baselines remain a plausible explanation for the variations in both isotope ratios, suggesting that individuals from the SBA foraged in a more northerly location than those from GI. This study provides valuable knowledge about how females from both colonies partition resources, especially regarding habitat use.

Coherent movement patterns of female northern elephant seals across the NE Pacific Ocean

Northern elephant seals engage in large-scale foraging migrations traveling up to 15,000 Km over 8 months in the northeast Pacific. While traditionally considered solitary migrants, we demonstrate here that female seals migrate in a surprisingly coherent manner, for individual northern elephant seals traveling in over such a large region of the ocean. Animal movement remained coherent, in terms of the direction of individual swimming relative to group movement, throughout much of their migrations. Movement coherence remained well above the value expected if the movement was independent until the migrating seals were further than 1,000 Km from the colony, beyond which movement coherence declined. Migrating seals presented regional aggregations consisting of female seals traveling within the center of the aggregation, closely following the main migration pathway, with individuals isolated on the extremes of the aggregation. These formations were preserved in the out-and-return migration trips. Animals at the edges of the group show an absence of correlation in their movement with the rest of animals. The observed movements exhibited a lag in the group movement patterns that was greater for female animals > 1,000 Km apart. A model that reproduced movement based on the average individual movement properties failed to reproduce the observed movement patterns. In turn, when a parameter was introduced that reflected group behavior, the resulting modelled movement conformed to the observed patterns, thereby demonstrating the presence of coherent, or synchronized, movement. Whereas the duration of female migration is ultimately constrained by reproductive biology, the coherent movement may involve both endogenous and exogenous cues determining the timing of the initiation of return across 25 million Km2 in the northeast Pacific.

Trans‐oceanic subsurface photovoltaic performance

AbstractUtilization of marine photovoltaic energy is primarily focused on surface harvesting with limited photovoltaic cell implementations in submarine environments. Potential applications include marine wildlife telemetry devices, autonomous underwater vehicles, or remote sensing assets. In these applications, understanding the power at depth is critical, but there has yet to be a long‐term study of cell performance in a realistic marine environment that spans time, geographic location, and depth. In this paper, we present photovoltaic assessments carried out by devices mounted to adult female northern elephant seals (Mirounga angustirostris) during their spring migrations in the Pacific Ocean with deployment times between 76 and 107 days. Encompassing a large geographic area between Santa Cruz, California, and the Aleutian Islands of Alaska during their migrations, elephant seal behavior allows for repeated depth profiles each day, making them an ideal host for subsurface power assessments. This paper presents the first longitudinal study of photovoltaic cell performance in the marine environment that spans location, time, and depth. This work discusses the calibration, data time alignment, and power calculations of these oceanic deployments. Deployment results, including power results and energy predictions from the data record, are presented up to 22 m in depth. We highlight how the recorded power data of these cells compares to previously published results and how depth impacts subsurface power and energy harvesting.

Sleeping while diving: seals at sea drift in and out of sleep at depth

In mammals, sleep is critical and ubiquitous. However, in marine mammals that spend months or entire lifetimes at sea, sleep can limit access to air and foraging opportunities and leave animals vulnerable to predation. Large, deep-diving northern elephant seals (Mirounga angustirostris) travel thousands of kilometers and spend up to 7 months at sea in search of food. We posited that combined demands to feed and avoid predators would strongly restrict aquatic sleep in seals. We built a portable, non-invasive system to simultaneously monitor electroencephalogram (EEG), electrocardiogram (ECG), three-dimensional motion, and swimming behavior. EEG activity of 13 young (< 3-years-old) female northern elephant seals (N = 5 in the lab, N = 8 in the wild [N = 3 at sea]) revealed that total sleep time was indeed strongly restricted at sea compared to on land (> 6-fold difference; 10.8 ± 3.0 h/day on land, 1.7 ± 0.7 h/day at sea). Seals at sea slept during short naps (< 20 min) while resting on the ocean floor (64-249 m deep) or drifting through the water column (82-377 m deep). REM sleep in mammals co-occurs with sleep paralysis. Our data support the presence of sleep paralysis through a persistent supine inversion (belly-up posture) whenever the seal was in REM (100% of REM sleep in the open ocean). Unexpectedly, elephant seals at sea exhibited a large proportion of REM sleep (29.1 ± 4.3% of at-sea total sleep time), compared to aquatic sleep in captive Caspian seals, harp seals, walruses, and fur seals (11%, 6%, 5%, and 1% respectively). This suggests that sleep at depth allows seals to drift safely in and out of sleep paralysis. However, time for sleep is limited by near-constant foraging to support high energetic demands due to their large body size. The extreme flexibility in sleep duration exhibited by northern elephant seals is unprecedented among mammals – approaching that which is observed in migrating birds. These insights into sleep for a large, highly mobile marine mammal can contribute to our understanding of sleep’s function and pathology across mammals, including humans. Funding: NSF Graduate Resesarch Fellowship, Laurel Clark Sea to Space Physiology Research Grant, ARCS Fellowship, Sooy Graduate Fellowship, National Geographic Early Career Grant, Special Research Grant – UC Santa Cruz, Joint Industry Project (JIP2207-23) [DPC], Office of Naval Research (Grants # N00014-08-1-1195 [DPC], N00014-18-1-2822 [DPC], N00014-00-1-0880 [DPC], N00014-03-1-0651 [DPC], N00014-08-1-1195 [DPC], N00014-20-1-2762 [TMW], N00014-19-1-2178 [TMW]) This is the full abstract presented at the American Physiology Summit 2023 meeting and is only available in HTML format. There are no additional versions or additional content available for this abstract. Physiology was not involved in the peer review process.

Adrenal response to ACTH challenge alters thyroid and immune function and varies with body reserves in molting adult female northern elephant seals.

Intrinsic stressors associated with life-history stages may alter the responsiveness of the hypothalamic-pituitary-adrenal axis and responses to extrinsic stressors. We administered adrenocorticotropic hormone (ACTH) to 24 free-ranging adult female northern elephant seals (NESs) at two life-history stages: early and late in their molting period and measured a suite of endocrine, immune, and metabolite responses. Our objective was to evaluate the impact of extended, high-energy fasting on adrenal responsiveness. Animals were blood sampled every 30 min for 120 min post-ACTH injection, then blood was sampled 24 h later. In response to ACTH injection, cortisol levels increased 8- to 10-fold and remained highly elevated compared with baseline at 24 h. Aldosterone levels increased 6- to 9-fold before returning to baseline at 24 h. The magnitude of cortisol and aldosterone release were strongly associated, and both were greater after extended fasting. We observed an inverse relationship between fat mass and the magnitude of cortisol and aldosterone responses, suggesting that body reserves influenced adrenal responsiveness. Sustained elevation in cortisol was associated with alterations in thyroid hormones; both tT3 and tT4 concentrations were suppressed at 24 h, while rT3 increased. Immune cytokine IL-1β was also suppressed after 24 h of cortisol elevation, and numerous acute and sustained impacts on substrate metabolism were evident. Our data suggest that female NESs are more sensitive to stress after the molt fast and that acute stress events can have important impacts on metabolism and immune function. These findings highlight the importance of considering life-history context when assessing the impacts of anthropogenic stressors on wildlife.

Mercury Bioaccumulation and Cortisol Interact to Influence Endocrine and Immune Biomarkers in a Free-Ranging Marine Mammal

Mercury bioaccumulation from deep-ocean prey and the extreme life history strategies of adult female northern elephant seals (Mirounga angustirostris) provide a unique system to assess the interactive effects of mercury and stress on animal health by quantifying blood biomarkers in relation to mercury (skeletal muscle and blood mercury) and cortisol concentrations. The thyroid hormone thyroxine (tT4) and the antibody immunoglobulin E (IgE) were associated with mercury and cortisol concentrations interactively, where the magnitude and direction of the association of each biomarker with mercury or cortisol changed depending on the concentration of the other factor. For example, when cortisol concentrations were lowest, tT4 was positively related to muscle mercury, whereas tT4 had a negative relationship with muscle mercury in seals that had the highest cortisol concentrations. Additionally, we observed that two thyroid hormones, triiodothyronine (tT3) and reverse triiodothyronine (rT3), were negatively (tT3) and positively (rT3) associated with mercury concentrations and cortisol in an additive manner. As an example, tT3 concentrations in late breeding seals at the median cortisol concentration decreased by 14% across the range of observed muscle mercury concentrations. We also observed that immunoglobulin M (IgM), the pro-inflammatory cytokine IL-6 (IL-6), and a reproductive hormone, estradiol, were negatively related to muscle mercury concentrations but were not related to cortisol. Specifically, estradiol concentrations in late molting seals decreased by 50% across the range of muscle mercury concentrations. These results indicate important physiological effects of mercury on free-ranging apex marine predators and interactions between mercury bioaccumulation and extrinsic stressors. Deleterious effects on animals' abilities to maintain homeostasis (thyroid hormones), fight off pathogens and disease (innate and adaptive immune system), and successfully reproduce (endocrine system) can have significant individual- and population-level consequences.

Effects of disease on foraging behaviour and success in an individual free-ranging northern elephant seal.

Evaluating consequences of stressors on vital rates in marine mammals is of considerable interest to scientific and regulatory bodies. Many of these species face numerous anthropogenic and environmental disturbances. Despite its importance as a critical form of mortality, little is known about disease progression in air-breathing marine megafauna at sea. We examined the movement, diving, foraging behaviour and physiological state of an adult female northern elephant seal (Mirounga angustirostris) who suffered from an infection while at sea. Comparing her to healthy individuals, we identified abnormal behavioural patterns from high-resolution biologging instruments that are likely indicators of diseased and deteriorating condition. We observed continuous extended (3-30minutes) surface intervals coinciding with almost no foraging attempts (jaw motion) during 2weeks of acute illness early in her post-breeding foraging trip. Elephant seals typically spend ~ 2minutes at the surface. There were less frequent but highly extended (30-200minutes) surface periods across the remainder of the trip. Dive duration declined throughout the trip rather than increasing. This seal returned in the poorest body condition recorded for an adult female elephant seal (18.3% adipose tissue; post-breeding trip average is 30.4%). She was immunocompromised at the end of her foraging trip and has not been seen since that moulting season. The timing and severity of the illness, which began during the end of the energy-intensive lactation fast, forced this animal over a tipping point from which she could not recover. Additional physiological constraints to foraging, including thermoregulation and oxygen consumption, likely exacerbated her already poor condition. These findings improve our understanding of illness in free-ranging air-breathing marine megafauna, demonstrate the vulnerability of individuals at critical points in their life history, highlight the importance of considering individual health when interpreting biologging data and could help differentiate between malnutrition and other causes of at-sea mortality from transmitted data.

Foraging behavior of a mesopelagic predator, the northern elephant seal, in northeastern Pacific eddies

The role of mesoscale features in structuring trophic transfer in the mesopelagic zone is poorly understood. Deploying sensors on marine animals, or “biologging,” is a powerful tool to infer the organism's behavior and simultaneously collect high-resolution oceanographic data to describe physical-biological interactions. We investigated whether mesoscale eddies are used by a mesopelagic predator, the northern elephant seal (Mirounga angustirostris), and if so, what mechanisms might create beneficial foraging conditions in association with eddies. We hypothesized seals would increase their foraging behavior in both cyclonic and anticyclonic eddies due to nutrient enhancement and physical aggregation of prey and that seals would dive deeper in anticyclonic eddies in response to a deeper prey field. We used tracking data and continuous in situ temperature measurements from 221 adult female northern elephant seals collected between 2004 and 2019. These predators primarily targeted myctophid fishes and squid throughout the northeast Pacific mesopelagic zone, foraging between approximately 400–800 m. Eddy encounters were identified using remotely sensed sea level anomaly data and confirmed visually with collocated sea level anomaly, in situ temperature, and in situ temperature anomaly. Over more than 30,000 days of data and >3 million temperature casts collected by seals, we found 129 high confidence encounters with anticyclonic eddies and 83 with cyclonic eddies. Overall, seals traveled more slowly and in a less directed manner while associated with eddies, particularly anticyclonic eddies, suggesting increased foraging behavior, especially in the California Current. Elephant seals spent more time at the edges of cyclonic eddies than their center. In contrast, they utilized both the interior and edge of anticyclonic eddies. This suggests that the aggregation of prey at the frontal region of an eddy is an important mechanism, whereas nutrient upwelling associated with an eddy play a more minor role in enhancing the seals' prey field. Seal foraging behavior was not influenced by eddy age, size, amplitude, or rotational speed. The large sample size in this study showed considerable variation between individual behavioral responses, suggesting caution when extrapolating individual behavior to a population level. Our data show that both cyclonic and anticyclonic eddies can affect the seals' prey field as demonstrated by enhanced foraging behavior. Still, the variation in behavioral responses resulting from individual foraging strategies, eddy histories, and possible spatiotemporal mismatches between eddy physics and biological responses relevant to mesopelagic predators merit further investigation.

Changes in serum adipokines during natural extended fasts in female northern elephant seals

Adipose tissue is essential to endotherms for thermoregulation and energy storage as well as functioning as an endocrine organ. Adipose derived hormones, or adipokines, regulate metabolism, energy expenditure, reproduction, and immune function in model systems but are less well studied in wildlife. Female northern elephant seals (NES) achieve high adiposity during foraging and then undergo natural fasts up to five weeks long during haul-outs associated with reproduction and molting, resulting in large changes in adipose reserves. We measured circulating levels of four adipokines: leptin, resistin, adiponectin, and kisspeptin-54, in 196 serum samples from female NES at the beginning and end of their breeding and molting fasts. We examined the relationships between these adipokines and life-history stage, adiposity, mass, cortisol, and an immune cytokine involved in the innate immune response interleukin 6 (IL-6). All four adipokines varied with life-history stage. Leptin concentrations were highest at the beginning of the breeding haul-out. Resistin concentrations were higher throughout the breeding haul-out compared to the molt haul-out. Adiponectin concentrations were highest at the beginning of both haul-outs. Kisspeptin-54 concentrations were highest at the end of the breeding haul-out. Leptin, resistin, and adiponectin were associated with measures of body condition, either adiposity, mass, or both. Resistin, adiponectin, and kisspeptin-54 were associated with circulating cortisol concentrations. Resistin was strongly associated with circulating IL-6, a multifunctional cytokine. Adiponectin was associated with glucose concentrations, suggesting a potential role in tissue-specific insulin sensitivity during life-history stages categorized by high adiposity. Increased cortisol concentrations late in lactation were associated with increased kisspeptin-54, suggesting a link to ovulation initiation in NES. This study suggests dramatic changes in circulating adipokines with life-history and body condition that may exert important regulatory roles in NES. The positive relationship between adiponectin and adiposity as well as the lack of a relationship between leptin and kisspeptin-54 differed from model systems. These differences from biomedical model systems suggest the potential for modifications of expression and function of adipose-derived hormones in species that undergo natural changes in adiposity as part of their life-history.

Acceleration-triggered animal-borne videos show a dominance of fish in the diet of female northern elephant seals.

Knowledge of the diet of marine mammals is fundamental to understanding their role in marine ecosystems and response to environmental change. Recently, animal-borne video cameras have revealed the diet of marine mammals that make short foraging trips. However, novel approaches that allocate video time to target prey capture events is required to obtain diet information for species that make long foraging trips over great distances. We combined satellite telemetry and depth recorders with newly developed date-/time-, depth- and acceleration-triggered animal-borne video cameras to examine the diet of female northern elephant seals during their foraging migrations across the eastern North Pacific. We obtained 48.2 h of underwater video, from cameras mounted on the head (n=12) and jaw (n=3) of seals. Fish dominated the diet (78% of 697 prey items recorded) across all foraging locations (range: 37-55°N, 122-152°W), diving depths (range: 238-1167 m) and water temperatures (range: 3.2-7.4°C), while squid comprised only 7% of the diet. Identified prey included fish such as myctophids, Merluccius sp. and Icosteus aenigmaticus, and squid such as Histioteuthis sp., Octopoteuthis sp. and Taningia danae Our results corroborate fatty acid analysis, which also found that fish are more important in the diet, and are in contrast to stomach content analyses that found cephalopods to be the most important component of the diet. Our work shows that in situ video observation is a useful method for studying the at-sea diet of long-ranging marine predators.

Lifetime reproductive success of northern elephant seals (Mirounga angustirostris)

Lifetime reproductive success of individuals in a natural population provides an estimate of Darwinian fitness. We calculated lifetime reproductive success in a colony of female northern elephant seals (Mirounga angustirostris (Gill, 1866)) by monitoring annual breeding throughout life of 7735 female weanlings marked individually at Año Nuevo, California, USA, from 1963 to 2005. Great variation in lifetime reproductive success was evident in three aspects of life history: (1) 75% of the females died before reaching breeding age and produced no pups; (2) nearly half of the survivors bred for only a few years before dying, and young females had low weaning success; (3) less than 1% of the females in the sample were exceptionally successful producing up to 20 pups in life. Many females that bred early, while still growing, had decreased lifespan, low weaning success, and lower lifetime reproductive success than females that postponed first breeding. Exceptional reproductive success was associated with giving birth annually, living long (up to age 23), and weaning large pups that were more likely to survive and breed. We conclude that there is strong selection for increased lifespan and multiparous supermoms that contribute significantly to pup production in the next generation.

Use of 15N-enriched glycine to estimate vibrissa growth in free-ranging northern elephant seals Mirounga angustirostris

MEPS Marine Ecology Progress Series Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections MEPS 614:199-207 (2019) - DOI: https://doi.org/10.3354/meps12913 Use of 15N-enriched glycine to estimate vibrissa growth in free-ranging northern elephant seals Mirounga angustirostris David Aurioles-Gamboa1,*, Seth D. Newsome2, Jason L. Hassrick3, Tatiana Acosta-Pachón4, Félix Aurioles-Rodríguez5, Daniel P. Costa6 1Facultad de Ingeniería Ambiental, Universidad Popular Autónoma del Estado de Puebla, Puebla 72410, México 2Biology Department, University of New Mexico, Albuquerque, New Mexico 87131, USA 3ICF Fish and Aquatic Science, 201 Mission Street, Suite 1500, San Francisco, California 94105, USA 4Departamento Académico de Ciencias Marinas y Costeras. Universidad Autónoma de Baja California Sur, La Paz, Baja California Sur 23080, México 5División de Ciencias Naturales y Exactas, Universidad de Guanajuato, 36050 Guanajuato, México 6Ecology and Evolutionary Biology Department, University of California Santa Cruz, Santa Cruz, California 95064, USA *Corresponding author: daurioles@gmail.com ABSTRACT: The stable isotope composition of continuously growing but metabolically inert tissues remains unaltered after they are synthesized, providing insights on seasonal and inter-annual variation in the ecology of individuals. In pinnipeds, isotope analysis of sub-sampled vibrissae can provide a longitudinal record of movement, diet, and even physiological state at the individual level. To reliably apply this approach, however, taxon-specific vibrissa growth needs to be estimated, especially for species with complicated annual life cycles that undergo periods of active foraging interspersed with reproduction and/or molting associated with fasting. Here, we intravenously injected 15N-enriched glycine to estimate vibrissa growth in 8 free-ranging adult female northern elephant seals during their (shorter) post-breeding and (longer) post-molting foraging trips; all animals were instrumented with satellite tags to track movements and vibrissae were collected when the animals returned to land. We found a significant positive relationship between the maximum δ15N values, representing 15N-glycine injections, and the distance between the origin of the spike and the root of the vibrissa. The δ15N spikes that occurred closest to the root were narrower and had lower δ15N values than those that occurred closer to the tip of the vibrissa, suggesting differential velocities of 15N-glycine absorption and vibrissa growth. A derived von Bertalanffy model yielded mean (±SD) growth of 0.015 ± 0.006 d-1, similar to that previously reported for a single captive northern elephant seal. Vibrissa length is an important consideration for accurately interpreting isotope-based ecological and physiological histories given the non-continuous growth observed in our study. KEY WORDS: Northern elephant seal · Vibrissae growth · 15N-enriched glycine Full text in pdf format PreviousNextCite this article as: Aurioles-Gamboa D, Newsome SD, Hassrick JL, Acosta-Pachón T, Aurioles-Rodríguez F, Costa DP (2019) Use of 15N-enriched glycine to estimate vibrissa growth in free-ranging northern elephant seals Mirounga angustirostris. Mar Ecol Prog Ser 614:199-207. https://doi.org/10.3354/meps12913 Export citation RSS - Facebook - Tweet - linkedIn Cited by Published in MEPS Vol. 614. Online publication date: April 04, 2019 Print ISSN: 0171-8630; Online ISSN: 1616-1599 Copyright © 2019 Inter-Research.

Oxygen minimum zone: An important oceanographic habitat for deep-diving northern elephant seals, Mirounga angustirostris.

Little is known about the foraging behavior of top predators in the deep mesopelagic ocean. Elephant seals dive to the deep biota‐poor oxygen minimum zone (OMZ) (>800 m depth) despite high diving costs in terms of energy and time, but how they successfully forage in the OMZ remains largely unknown. Assessment of their feeding rate is the key to understanding their foraging behavior, but this has been challenging. Here, we assessed the feeding rate of 14 female northern elephant seals determined by jaw motion events (JME) and dive cycle time to examine how feeding rates varied with dive depth, particularly in the OMZ. We also obtained video footage from seal‐mounted videos to understand their feeding in the OMZ. While the diel vertical migration pattern was apparent for most depths of the JME, some very deep dives, beyond the normal diel depth ranges, occurred episodically during daylight hours. The midmesopelagic zone was the main foraging zone for all seals. Larger seals tended to show smaller numbers of JME and lower feeding rates than smaller seals during migration, suggesting that larger seals tended to feed on larger prey to satisfy their metabolic needs. Larger seals also dived frequently to the deep OMZ, possibly because of a greater diving ability than smaller seals, suggesting their dependency on food in the deeper depth zones. Video observations showed that seals encountered the rarely reported ragfish (Icosteus aenigmaticus) in the depths of the OMZ, which failed to show an escape response from the seals, suggesting that low oxygen concentrations might reduce prey mobility. Less mobile prey in OMZ would enhance the efficiency of foraging in this zone, especially for large seals that can dive deeper and longer. We suggest that the OMZ plays an important role in structuring the mesopelagic ecosystem and for the survival and evolution of elephant seals.

Evaluating gain functions in foraging bouts using vertical excursions in northern elephant seals

The marginal value theorem models patch departure decisions for foraging animals when resources are unevenly distributed. A key component of these models is the decelerating energy gain function used to represent patch depletion. However, the within-patch gain function has rarely been assessed in marine predators. We evaluated the gain functions in foraging bouts of northern elephant seals, Mirounga angustirostris, using a long-term data set (2004–2012) that included complete foraging trips from 205 individual female northern elephant seals on 303 migrations as revealed by time–depth recorders and satellite tags (Argos System Inc.). Since the majority of putative prey capture attempts are associated with vertical excursions at the bottom of dives, we used vertical excursions to evaluate patch depletion across foraging bouts as defined using dive shapes. Rates of energy gain were measured using changes in mass and body composition across trips. Decelerating gain functions occurred in 83% of 77 820 foraging bouts, with the remainder showing accelerating functions. Rates of patch depletion strongly influenced patch residence times. Despite wide variation between individual patches, mean deceleration exponents did not vary with year or season, suggesting that average rates of patch depletion were relatively stable across the study period. The mean duration and number of dives in foraging bouts showed little annual or seasonal variation; however, the mean rate of vertical excursions during foraging dives varied and predicted rates of energy gain across migrations. The relative mean consistency of individual diving behaviour despite wide variation in geoposition supports the idea that northern elephant seals have evolved a foraging strategy that buffers against short-term variation in prey abundance and optimizes energy acquisition across the duration of the migration.

Linking mesopelagic prey abundance and distribution to the foraging behavior of a deep-diving predator, the northern elephant seal

The Transition Zone in the eastern North Pacific is important foraging habitat for many marine predators. Further, the mesopelagic depths (200–1000m) host an abundant prey resource known as the deep scattering layer that supports deep diving predators, such as northern elephant seals, beaked whales, and sperm whales. Female northern elephant seals (Mirounga angustirostris) undertake biannual foraging migrations to this region where they feed on mesopelagic fish and squid; however, in situ measurements of prey distribution and abundance, as well as the subsurface oceanographic features in the mesopelagic Transition Zone are limited. While concurrently tracking female elephant seals during their post-molt migration, we conducted a ship-based oceanographic and hydroacoustic survey and used mesopelagic mid-water trawls to sample the deep scattering layer. We found that the abundance of mesopelagic fish at 400–600m depth zone was the highest in the 43°N zone, the primary foraging area of female seals. We identified twenty-nine families of fishes from the mid-water trawls, with energy-rich myctophid fishes dominating by species number, individual number, and wet weight. Biomass of mesopelagic fishes is positively correlated to annual net primary productivity; however, at the temporal and spatial scale of our study, we found no relationship between satellite derived surface primary production and prey density. Instead, we found that the subsurface chlorophyll maximum correlated with the primary elephant seal foraging regions, indicating a stronger linkage between mesopelagic ecosystem dynamics and subsurface features rather than the surface features measured with satellites. Our study not only provides insights on prey distribution in a little-studied deep ocean ecosystem, but shows that northern elephant seals are targeting the dense, species-diverse mesopelagic ecosystem at the gyre-gyre boundary that was previously inferred from their diving behavior.

Effects of environmental variables on surface temperature of breeding adult female northern elephant seals, Mirounga angustirostris, and pups

Pinnipeds spend extended periods of time on shore during breeding, and some temperate species retreat to the water if exposed to high ambient temperatures. However, female northern elephant seals (Mirounga angustirostris) with pups generally avoid the water, presumably to minimize risks to pups or male harassment. Little is known about how ambient temperature affects thermoregulation of well insulated females while on shore. We used a thermographic camera to measure surface temperature (Ts) of 100 adult female elephant seals and their pups during the breeding season at Point Reyes National Seashore, yielding 782 thermograms. Environmental variables were measured by an onsite weather station. Environmental variables, especially solar radiation and ambient temperature, were the main determinants of mean and maximum Ts of both females and pups. An average of 16% of the visible surface of both females and pups was used as thermal windows to facilitate heat loss and, for pups, this area increased with solar radiation. Thermal window area of females increased with mean Ts until approximately 26°C and then declined. The Ts of both age classes were warmer than ambient temperature and had a large thermal gradient with the environment (female mean 11.2±0.2°C; pup mean 14.2±0.2°C). This large gradient suggests that circulatory adjustments to bypass blubber layers were sufficient to allow seals to dissipate heat under most environmental conditions. We observed the previously undescribed behavior of females and pups in the water and determined that solar radiation affected this behavior. This may have been possible due to the calm waters at the study site, which reduced the risk of neonates drowning. These results may predict important breeding habitat features for elephant seals as solar radiation and ambient temperatures change in response to changing climate.

Summing the strokes: energy economy in northern elephant seals during large-scale foraging migrations.

BackgroundThe energy requirements of free-ranging marine mammals are challenging to measure due to cryptic and far-ranging feeding habits, but are important to quantify given the potential impacts of high-level predators on ecosystems. Given their large body size and carnivorous lifestyle, we would predict that northern elephant seals (Mirounga angustirostris) have elevated field metabolic rates (FMRs) that require high prey intake rates, especially during pregnancy. Disturbance associated with climate change or human activity is predicted to further elevate energy requirements due to an increase in locomotor costs required to accommodate a reduction in prey or time available to forage. In this study, we determined the FMRs, total energy requirements, and energy budgets of adult, female northern elephant seals. We also examined the impact of increased locomotor costs on foraging success in this species.ResultsBody size, time spent at sea and reproductive status strongly influenced FMR. During the short foraging migration, FMR averaged 90.1 (SE = 1.7) kJ kg−1d−1 – only 36 % greater than predicted basal metabolic rate. During the long migration, when seals were pregnant, FMRs averaged 69.4 (±3.0) kJ kg−1d−1 – values approaching those predicted to be necessary to support basal metabolism in mammals of this size. Low FMRs in pregnant seals were driven by hypometabolism coupled with a positive feedback loop between improving body condition and reduced flipper stroking frequency. In contrast, three additional seals carrying large, non-streamlined instrumentation saw a four-fold increase in energy partitioned toward locomotion, resulting in elevated FMRs and only half the mass gain of normally-swimming study animals.ConclusionsThese results highlight the importance of keeping locomotion costs low for successful foraging in this species. In preparation for lactation and two fasting periods with high demands on energy reserves, migrating elephant seals utilize an economical foraging strategy whereby energy savings from reduced locomotion costs are shuttled towards somatic growth and fetal gestation. Remarkably, the energy requirements of this species, particularly during pregnancy, are 70–80 % lower than expected for mammalian carnivores, approaching or even falling below values predicted to be necessary to support basal metabolism in mammals of this size.Electronic supplementary materialThe online version of this article (doi:10.1186/s40462-015-0049-2) contains supplementary material, which is available to authorized users.

Body reserves influence allocation to immune responses in capital breeding female northern elephant seals

Summary Mounting an immune response requires substantial energy. Ecological immunology theory predicts allocation trade‐offs between reproductive effort and immune responses under conditions of energy limitation. Little is known about the impact of capital breeding strategies on energy allocation to immune function in mammals. Northern elephant seals (NES) forage in the marine environment, breed in dense terrestrial colonies and exhibit high rates of energy expenditure for lactation while fasting. Body reserves strongly influence reproductive effort and lactation requires elevation of plasma cortisol for energy mobilization. We characterized immune response by measuring a suite of immune markers including cytokines, an acute phase protein, and immunoglobulins early and late in breeding and moult haul‐outs in 197 samples from 129 female NES. We explored potential impacts of breeding, body condition and plasma cortisol on immune function. Immune responses were greater and more varied during breeding. Adiposity had positive associations with innate immune responses across all life‐history stages. Body mass had positive associations with both adaptive and innate immune responses early in fasts. Females with lower fat reserves showed reduced innate immune responses at the end of lactation. Immunoglobulin E, a marker of immune response to parasitic infection, exhibited a significant negative association with cortisol across all life‐history stages. These data suggest that breeding carries an immune cost and provide evidence for allocation trade‐offs between immune function and breeding effort. These trade‐offs may reflect a compromise between immune costs inherent in colonial breeding and energetic limitations that arise in use of capital breeding strategies. Variation in evidence for immunosuppressive effects of cortisol suggests that decoupling of these effects may be limited to specific aspects of the immune response during terrestrial fasting. Immune responses that are required for survival may be modulated relative to the energetic demands required for successful reproduction.

Fine-scale whisker growth measurements can reveal temporal foraging patterns from stable isotope signatures

Stable isotope analysis of slow-growing, metabolically inert tissues is a common method for investigating foraging ecology in migratory animals, as direct observations of feeding are often not possible. Using tissue growth dynamics to interpret foraging timelines can maximize the utility of foraging data; however, applying inappropriate growth models is problematic, and high-resolution growth measurements are seldom made. We used photogrammetry to repeatedly measure the length of whiskers in 93 follicles over 670 d in a trained, captive northern elephant seal Mirounga angustirostris. We developed and optimized a follicle-specific growth model to describe the 18 000 whisker length measurements. Whiskers from the captive seal exhibited asymptotic growth that was described by the von Bertalanffy growth function. Applying the growth model to serially sampled whiskers from 4 free-ranging adult female northern elephant seals resulted in alignment of peaks in δ 15 N along the length of whiskers with the breeding haul- out period, when seals are not feeding. Our study provides a high-resolution whisker growth model and is the first to use whisker growth dynamics to improve temporal interpretation of iso- topic ratios.

The foraging benefits of being fat in a highly migratory marine mammal.

Foraging theory predicts that breath-hold divers adjust the time spent foraging at depth relative to the energetic cost of swimming, which varies with buoyancy (body density). However, the buoyancy of diving animals varies as a function of their body condition, and the effects of these changes on swimming costs and foraging behaviour have been poorly examined. A novel animal-borne accelerometer was developed that recorded the number of flipper strokes, which allowed us to monitor the number of strokes per metre swam (hereafter, referred to as strokes-per-metre) by female northern elephant seals over their months-long, oceanic foraging migrations. As negatively buoyant seals increased their fat stores and buoyancy, the strokes-per-metre increased slightly in the buoyancy-aided direction (descending), but decreased significantly in the buoyancy-hindered direction (ascending), with associated changes in swim speed and gliding duration. Overall, the round-trip strokes-per-metre decreased and reached a minimum value when seals achieved neutral buoyancy. Consistent with foraging theory, seals stayed longer at foraging depths when their round-trip strokes-per-metre was less. Therefore, neutrally buoyant divers gained an energetic advantage via reduced swimming costs, which resulted in an increase in time spent foraging at depth, suggesting a foraging benefit of being fat.