Whiskers as hydrodynamic prey sensors in foraging seals.

The darkness of the deep ocean limits the vision of diving predators, except when prey emit bioluminescence. It is hypothesized that deep-diving seals rely on highly developed whiskers to locate their prey. However, if and how seals use their whiskers while foraging in natural conditions remains unknown. We used animal-borne tags to show that free-ranging elephant seals use their whiskers for hydrodynamic prey sensing. Small, cheek-mounted video loggers documented seals actively protracting their whiskers in front of their mouths with rhythmic whisker movement, like terrestrial mammals exploring their environment. Seals focused their sensing effort at deep foraging depths, performing prolonged whisker protraction to detect, pursue, and capture prey. Feeding-event recorders with light sensors demonstrated that bioluminescence contributed to only about 20% of overall foraging success, confirming that whiskers play the primary role in sensing prey. Accordingly, visual prey detection complemented and enhanced prey capture. The whiskers' role highlights an evolutionary alternative to echolocation for adapting to the extreme dark of the deep ocean environment, revealing how sensory abilities shape foraging niche segregation in deep-diving mammals. Mammals typically have mobile facial whiskers, and our study reveals the significant function of whiskers in the natural foraging behavior of a marine predator. We demonstrate the importance of field-based sensory studies incorporating multimodality to better understand how multiple sensory systems are complementary in shaping the foraging success of predators.

Individual variation in life-history timing: synchronous presence, asynchronous events and phenological compensation in a wild mammal.

Many animals and plants have species-typical annual cycles, but individuals vary in their timing of life-history events. Individual variation in fur replacement (moult) timing is poorly understood in mammals due to the challenge of repeated observations and longitudinal sampling. We examined factors that influence variation in moult duration and timing among elephant seals (Mirounga angustirostris). We quantified the onset and progression of fur loss in 1178 individuals. We found that an exceptionally rapid visible moult (7 days, the shortest of any mammals or birds), and a wide range of moult start dates (spanning 6-10× the event duration) facilitated high asynchrony across individuals (only 20% of individuals in the population moulting at the same time). Some of the variation was due to reproductive state, as reproductively mature females that skipped a breeding season moulted a week earlier than reproductive females. Moreover, individual variation in timing and duration within age-sex categories far outweighed (76-80%) variation among age-sex categories. Individuals arriving at the end of the moult season spent 50% less time on the beach, which allowed them to catch up in their annual cycles and reduce population-level variance during breeding. These findings underscore the importance of individual variation in annual cycles.

Physiological tipping points in the relationship between foraging success and lifetime fitness of a long-lived mammal.

Although anthropogenic change is often gradual, the impacts on animal populations may be precipitous if physiological processes create tipping points between energy gain, reproduction or survival. We use 25 years of behavioural, diet and demographic data from elephant seals to characterise their relationships with lifetime fitness. Survival and reproduction increased with mass gain during long foraging trips preceding the pupping seasons, and there was a threshold where individuals that gained an additional 4.8% of their body mass (26 kg, from 206 to 232 kg) increased lifetime reproductive success three-fold (from 1.8 to 4.9 pups). This was due to a two-fold increase in pupping probability (30% to 76%) and a 7% increase in reproductive lifespan (6.0 to 6.4 years). The sharp threshold between mass gain and reproduction may explain reproductive failure observed in many species and demonstrates how small, gradual reductions in prey from anthropogenic disturbance could have profound implications for animal populations.

Density-dependent effects on reproductive output in a capital breeding carnivore, the northern elephant seal (Mirounga angustirostris).

All organisms face resource limitations that will ultimately restrict population growth, but the controlling mechanisms vary across ecosystems, taxa, and reproductive strategies. Using four decades of data, we examine how variation in the environment and population density affect reproductive outcomes in a capital-breeding carnivore, the northern elephant seal (Mirounga angustirostris). This species provides a unique opportunity to examine the relative importance of resource acquisition and density-dependence on breeding success. Capital breeders accrue resources over large temporal and spatial scales for use during an abbreviated reproductive period. This strategy may have evolved, in part, to confer resilience to short-term environmental variability. We observed density-dependent effects on weaning mass, and maternal age (experience) was more important than oceanographic conditions or maternal mass in determining offspring weaning mass. Together these findings show that the mechanisms controlling reproductive output are conserved across terrestrial and marine systems and vary with population dynamics, an important consideration when assessing the effect of extrinsic changes, such as climate change, on a population.

Seasonal resource pulses and the foraging depth of a Southern Ocean top predator.

Seasonal resource pulses can have enormous impacts on species interactions. In marine ecosystems, air-breathing predators often drive their prey to deeper waters. However, it is unclear how ephemeral resource pulses such as near-surface phytoplankton blooms alter the vertical trade-off between predation avoidance and resource availability in consumers, and how these changes cascade to the diving behaviour of top predators. We integrated data on Weddell seal diving behaviour, diet stable isotopes, feeding success and mass gain to examine shifts in vertical foraging throughout ice break-out and the resulting phytoplankton bloom each year. We also tested hypotheses about the likely location of phytoplankton bloom origination (advected or produced in situ where seals foraged) based on sea ice break-out phenology and advection rates from several locations within 150 km of the seal colony. In early summer, seals foraged at deeper depths resulting in lower feeding rates and mass gain. As sea ice extent decreased throughout the summer, seals foraged at shallower depths and benefited from more efficient energy intake. Changes in diving depth were not due to seasonal shifts in seal diets or horizontal space use and instead may reflect a change in the vertical distribution of prey. Correspondence between the timing of seal shallowing and the resource pulse was variable from year to year and could not be readily explained by our existing understanding of the ocean and ice dynamics. Phytoplankton advection occurred faster than ice break-out, and seal dive shallowing occurred substantially earlier than local break-out. While there remains much to be learned about the marine ecosystem, it appears that an increase in prey abundance and accessibility via shallower distributions during the resource pulse could synchronize life-history phenology across trophic levels in this high-latitude ecosystem.

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.

Climate mediates the success of migration strategies in a marine predator.

Individual behavioural specialisation has far-reaching effects on fitness and population persistence. Theory predicts that unconditional site fidelity, that is fidelity to a site independent of past outcome, provides a fitness advantage in unpredictable environments. However, the benefits of alternative site fidelity strategies driving intraspecific variation remain poorly understood and have not been evaluated in different environmental contexts. We show that contrary to expectation, strong and weak site fidelity strategies in migratory northern elephant seals performed similarly over 10 years, but the success of each strategy varied interannually and was strongly mediated by climate conditions. Strong fidelity facilitated stable energetic rewards and low risk, while weak fidelity facilitated high rewards and high risk. Weak fidelity outperformed strong fidelity in anomalous climate conditions, suggesting that the evolutionary benefits of site fidelity may be upended by increasing environmental variability. We highlight how individual behavioural specialisation may modulate the adaptive capacity of species to climate change.

Mesoscale activity facilitates energy gain in a top predator.

How animal movement decisions interact with the distribution of resources to shape individual performance is a key question in ecology. However, links between spatial and behavioural ecology and fitness consequences are poorly understood because the outcomes of individual resource selection decisions, such as energy intake, are rarely measured. In the open ocean, mesoscale features (approx. 10-100 km) such as fronts and eddies can aggregate prey and thereby drive the distribution of foraging vertebrates through bottom-up biophysical coupling. These productive features are known to attract predators, yet their role in facilitating energy transfer to top-level consumers is opaque. We investigated the use of mesoscale features by migrating northern elephant seals and quantified the corresponding energetic gains from the seals' foraging patterns at a daily resolution. Migrating elephant seals modified their diving behaviour and selected for mesoscale features when foraging. Daily energy gain increased significantly with increasing mesoscale activity, indicating that the physical environment can influence predator fitness at fine temporal scales. Results show that areas of high mesoscale activity not only attract top predators as foraging hotspots, but also lead to increased energy transfer across trophic levels. Our study provides evidence that the physical environment is an important factor in controlling energy flow to top predators by setting the stage for variation in resource availability. Such understanding is critical for assessing how changes in the environment and resource distribution will affect individual fitness and food web dynamics.

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.

Contrasting offspring dependence periods and diving development rates in two closely related marine mammal species.

Understanding the ontogeny of diving behaviour in marine megafauna is crucial owing to its influence on foraging success, energy budgets, and mortality. We compared the ontogeny of diving behaviour in two closely related species-northern elephant seals (Mirounga angustirostris, n = 4) and southern elephant seals (Mirounga leonina, n = 9)-to shed light on the ecological processes underlying migration. Although both species have similar sizes and behaviours as adults, we discovered that juvenile northern elephant seals have superior diving development, reaching 260 m diving depth in just 30 days, while southern elephant seals require 160 days. Similarly, northern elephant seals achieve dive durations of approximately 11 min on their first day of migration, while southern elephant seals take 125 days. The faster physiological maturation of northern elephant seals could be related to longer offspring dependency and post-weaning fast durations, allowing them to develop their endogenous oxygen stores. Comparison across both species suggests that weaned seal pups face a trade-off between leaving early with higher energy stores but poorer physiological abilities or leaving later with improved physiology but reduced fat stores. This trade-off might be influenced by their evolutionary history, which shapes their migration behaviours in changing environments over time.

Genomics of post-bottleneck recovery in the northern elephant seal.

Populations and species are threatened by human pressure, but their fate is variable. Some depleted populations, such as that of the northern elephant seal (Mirounga angustirostris), recover rapidly even when the surviving population was small. The northern elephant seal was hunted extensively and taken by collectors between the early 1800s and 1892, suffering an extreme population bottleneck as a consequence. Recovery was rapid and now there are over 200,000 individuals. We sequenced 260 modern and 8 historical northern elephant seal nuclear genomes to assess the impact of the population bottleneck on individual northern elephant seals and to better understand their recovery. Here we show that inbreeding, an increase in the frequency of alleles compromised by lost function, and allele frequency distortion, reduced the fitness of breeding males and females, as well as the performance of adult females on foraging migrations. We provide a detailed investigation of the impact of a severe bottleneck on fitness at the genomic level and report on the role of specific gene systems.

Estimating resource acquisition and at-sea body condition of a marine predator.

1. Body condition plays a fundamental role in many ecological and evolutionary processes at a variety of scales and across a broad range of animal taxa. An understanding of how body condition changes at fine spatial and temporal scales as a result of interaction with the environment provides necessary information about how animals acquire resources. 2. However, comparatively little is known about intra- and interindividual variation of condition in marine systems. Where condition has been studied, changes typically are recorded at relatively coarse time-scales. By quantifying how fine-scale interaction with the environment influences condition, we can broaden our understanding of how animals acquire resources and allocate them to body stores. 3. Here we used a hierarchical Bayesian state-space model to estimate the body condition as measured by the size of an animal's lipid store in two closely related species of marine predator that occupy different hemispheres: northern elephant seals (Mirounga angustirostris) and southern elephant seals (Mirounga leonina). The observation model linked drift dives to lipid stores. The process model quantified daily changes in lipid stores as a function of the physiological condition of the seal (lipid:lean tissue ratio, departure lipid and departure mass), its foraging location, two measures of behaviour and environmental covariates. 4. We found that physiological condition significantly impacted lipid gain at two time-scales - daily and at departure from the colony - that foraging location was significantly associated with lipid gain in both species of elephant seals and that long-term behavioural phase was associated with positive lipid gain in northern and southern elephant seals. In northern elephant seals, the occurrence of short-term behavioural states assumed to represent foraging were correlated with lipid gain. Lipid gain was a function of covariates in both species. Southern elephant seals performed fewer drift dives than northern elephant seals and gained lipids at a lower rate. 5. We have demonstrated a new way to obtain time series of body condition estimates for a marine predator at fine spatial and temporal scales. This modelling approach accounts for uncertainty at many levels and has the potential to integrate physiological and movement ecology of top predators. The observation model we used was specific to elephant seals, but the process model can readily be applied to other species, providing an opportunity to understand how animals respond to their environment at a fine spatial scale.

Seasonal habitat preference and foraging behaviour of post-moult Weddell seals in the western Ross Sea.

Weddell seals (Leptonychotes weddellii) are important predators in the Southern Ocean and are among the best-studied pinnipeds on Earth, yet much still needs to be learned about their year-round movements and foraging behaviour. Using biologgers, we tagged 62 post-moult Weddell seals in McMurdo Sound and vicinity between 2010 and 2012. Generalized additive mixed models were used to (i) explain and predict the probability of seal presence and foraging behaviour from eight environmental variables, and (ii) examine foraging behaviour in relation to dive metrics. Foraging probability was highest in winter and lowest in summer, and foraging occurred mostly in the water column or just above the bottom; across all seasons, seals preferentially exploited the shallow banks and deeper troughs of the Ross Sea, the latter providing a pathway for Circumpolar Deep Water to flow onto the shelf. In addition, the probability of Weddell seal occurrence and foraging increased with increasing bathymetric slope and where water depth was typically less than 600 m. Although the probability of occurrence was higher closer to the shelf break, foraging was higher in areas closer to shore and over banks. This study highlights the importance of overwinter foraging for recouping body mass lost during the previous summer.

Brain activity of diving seals reveals short sleep cycles at depth.

Sleep is a crucial part of the daily activity patterns of mammals. However, in marine species that spend months or entire lifetimes at sea, the location, timing, and duration of sleep may be constrained. To understand how marine mammals satisfy their daily sleep requirements while at sea, we monitored electroencephalographic activity in wild northern elephant seals (Mirounga angustirostris) diving in Monterey Bay, California. Brain-wave patterns showed that seals took short (less than 20 minutes) naps while diving (maximum depth 377 meters; 104 sleeping dives). Linking these patterns to accelerometry and the time-depth profiles of 334 free-ranging seals (514,406 sleeping dives) revealed a North Pacific sleepscape in which seals averaged only 2 hours of sleep per day for 7 months, rivaling the record for the least sleep among all mammals, which is currently held by the African elephant (about 2 hours per day).

Elephant seals time their long-distance migrations using a map sense.

Many marine animals migrate between foraging areas and reproductive sites, often timing the return migration with extreme precision. In theory, the decision to return should reflect energy acquisition at foraging areas, energetic costs associated with transit, and timing arrival for successful reproduction. For long-distance migrations to be successful, animals must integrate 'map' information to assess where they are relative to their reproductive site as well as 'calendar' information to know when to initiate the return migration given their distance from home1. Elephant seals, Mirounga angustirostris, migrate thousands of kilometers from reproductive sites to open ocean foraging areas (Figure 1A), yet return within a narrow window of time to specific beaches2. Each year, pregnant female elephant seals undertake a ∼240-day, 10,000 km foraging migration across the Northeast Pacific Ocean before returning to their breeding beaches, where they give birth 5 days after arriving2. We found that the seals' abilities to adjust the timing of their return migration is based on the perception of space and time, which further elucidates the mechanisms behind their astonishing navigational feats3.

Underwater and surface behavior of homing juvenile northern elephant seals.

Northern elephant seals, Mirounga angustirostris, travel between colonies along the west coast of North America and foraging areas in the North Pacific. They also have the ability to return to their home colony after being experimentally translocated. However, the mechanisms of this navigation are not known. Visual information could serve an important role in navigation, either primary or supplementary. We examined the role of visual cues in elephant seal navigation by translocating three seals and recording their heading direction continuously using GPS, and acceleration and geomagnetic data loggers while they returned to the colony. The seals first reached the coast and then proceeded to the colony by swimming along the coast. While underwater the animals exhibited a horizontally straight course (mean net-to-gross displacement ratio=0.94±0.02). In contrast, while at the surface they changed their headings up to 360 deg. These results are consistent with the use of visual cues for navigation to the colony. The seals may visually orient by using landmarks as they swim along the coast. We further assessed whether the seals could maintain a consistent heading while underwater during drift dives where one might expect that passive spiraling during drift dives could cause disorientation. However, seals were able to maintain the initial course heading even while underwater during drift dives where there was spiral motion (to within 20 deg). This behavior may imply the use of non-visual cues such as acoustic signals or magnetic fields for underwater orientation.

Northern elephant seals adjust gliding and stroking patterns with changes in buoyancy: validation of at-sea metrics of body density.

Many diving animals undergo substantial changes in their body density that are the result of changes in lipid content over their annual fasting cycle. Because the size of the lipid stores reflects an integration of foraging effort (energy expenditure) and foraging success (energy assimilation), measuring body density is a good way to track net resource acquisition of free-ranging animals while at sea. Here, we experimentally altered the body density and mass of three free-ranging elephant seals by remotely detaching weights and floats while monitoring their swimming speed, depth and three-axis acceleration with a high-resolution data logger. Cross-validation of three methods for estimating body density from hydrodynamic gliding performance of freely diving animals showed strong positive correlation with body density estimates obtained from isotope dilution body composition analysis over density ranges of 1015 to 1060 kg m(-3). All three hydrodynamic models were within 1% of, but slightly greater than, body density measurements determined by isotope dilution, and therefore have the potential to track changes in body condition of a wide range of freely diving animals. Gliding during ascent and descent clearly increased and stroke rate decreased when buoyancy manipulations aided the direction of vertical transit, but ascent and descent speed were largely unchanged. The seals adjusted stroking intensity to maintain swim speed within a narrow range, despite changes in buoyancy. During active swimming, all three seals increased the amplitude of lateral body accelerations and two of the seals altered stroke frequency in response to the need to produce thrust required to overcome combined drag and buoyancy forces.

Accuracy and precision of citizen scientist animal counts from drone imagery.

Repeated counts of animal abundance can reveal changes in local ecosystem health and inform conservation strategies. Unmanned aircraft systems (UAS), also known as drones, are commonly used to photograph animals in remote locations; however, counting animals in images is a laborious task. Crowd-sourcing can reduce the time required to conduct these censuses considerably, but must first be validated against expert counts to measure sources of error. Our objectives were to assess the accuracy and precision of citizen science counts and make recommendations for future citizen science projects. We uploaded drone imagery from Año Nuevo Island (California, USA) to a curated Zooniverse website that instructed citizen scientists to count seals and sea lions. Across 212 days, over 1,500 volunteers counted animals in 90,000 photographs. We quantified the error associated with several descriptive statistics to extract a single citizen science count per photograph from the 15 repeat counts and then compared the resulting citizen science counts to expert counts. Although proportional error was relatively low (9% for sea lions and 5% for seals during the breeding seasons) and improved with repeat sampling, the 12+ volunteers required to reduce error was prohibitively slow, taking on average 6 weeks to estimate animals from a single drone flight covering 25 acres, despite strong public outreach efforts. The single best algorithm was 'Median without the lowest two values', demonstrating that citizen scientists tended to under-estimate the number of animals present. Citizen scientists accurately counted adult seals, but accuracy was lower when sea lions were present during the summer and could be confused for seals. We underscore the importance of validation efforts and careful project design for researchers hoping to combine citizen science with imagery from drones, occupied aircraft, and/or remote cameras.

Forced into an ecological corner: Round-the-clock deep foraging on small prey by elephant seals.

Small mesopelagic fishes dominate the world's total fish biomass, yet their ecological importance as prey for large marine animals is poorly understood. To reveal the little-known ecosystem dynamics, we identified prey, measured feeding events, and quantified the daily energy balance of 48 deep-diving elephant seals throughout their oceanic migrations by leveraging innovative technologies: animal-borne smart accelerometers and video cameras. Seals only attained positive energy balance after feeding 1000 to 2000 times per day on small fishes, which required continuous deep diving (80 to 100% of each day). Interspecies allometry suggests that female elephant seals have exceptional diving abilities relative to their body size, enabling them to exploit a unique foraging niche on small but abundant mesopelagic fish. This unique foraging niche requires extreme round-the-clock deep diving, limiting the behavioral plasticity of elephant seals to a changing mesopelagic ecosystem.

Lightscapes of fear: How mesopredators balance starvation and predation in the open ocean.

Like landscapes of fear, animals are hypothesized to strategically use lightscapes based on intrinsic motivations. However, longitudinal evidence of state-dependent risk aversion has been difficult to obtain in wild animals. Using high-resolution biologgers, we continuously measured body condition, time partitioning, three-dimensional movement, and risk exposure of 71 elephant seals throughout their 7-month foraging migrations (N = 16,000 seal days). As body condition improved from 21 to 32% fat and daylength declined from 16 to 10 hours, seals rested progressively earlier with respect to sunrise, sacrificing valuable nocturnal foraging hours to rest in the safety of darkness. Seals in superior body condition prioritized safety over energy conservation by resting >100 meters deeper where it was 300× darker. Together, these results provide empirical evidence that marine mammals actively use the three-dimensional lightscape to optimize risk-reward trade-offs based on ecological and physiological factors.