Summary 1.To gain insight into the foraging behaviour of deep diving seals, we developed a long-term jaw-motion recorder, which successfully measured the feeding attempts of four post-breeding female northern elephant seals for 55-68 days during migration in the north-east Pacific Ocean. 2. Using the jaw-motion recorders in conjunction with satellite tracking data, we first reveal the three-dimensional fine-scale distribution of deep foraging activity in the north-east Pacific Ocean. 3. A large number of jaw-motion events (23 817-58 766 during 2925-4178 dives, per seal) were observed with diel patterns suggesting their dependency on small mesopelagic prey. Calculations using at-sea field metabolic-rate and the photographs concurrently obtained by the headmounted camera indicated feeding on small mesopelagic prey (10-20 g) including lantern fish (F. Myctophidae). 4. The foraging behaviour of the northern elephant seal contrasts with echolocating toothed whales, which make fewer feeding attempts, suggesting the whales forage more selectively. We hypothesize that the continuous diving mode exhibited by this seal could be attributed to their reliance on small prey and their less efficient 'passive sensors' for prey search, that is, their vision or whiskers to detect prey.

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 animalborne 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.

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.

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 hours 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, 122–150°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 fishes such as myctophids, Merluccius sp., and Icosteus aenigmaticus, and squids 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 contrasts 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.

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.

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.

Summary Foraging theory predicts that predators adjust their movements according to the spatial distribution of prey. Since prey is often patchily distributed, area‐restricted search (ARS) behaviour, characterized by sinuous search paths of predators with increased turning frequency, should be effective in foraging. However, it remains unclear whether ARS behaviour actually enhances foraging success in free‐ranging animals, especially in marine animals that forage in a three‐dimensional (3D) environment. Here, we reconstructed 3D dive paths of a highly pelagic marine predator, the northern elephant seal (n = 3), with multisensor data loggers that recorded depth, tri‐axis acceleration, tri‐axis magnetism and swim speed. We identified spatial scales of volume‐restricted search (VRS, termed for 3D ARS) behaviour using spherical first‐passage time analysis on 3D dive paths, accompanied with quantifying feeding rates in VRS by using mandible accelerometers that recorded feeding events. Seals exhibited VRS behaviour at two spatial scales (radius of spheres): small‐VRS (8–10 m) and large‐VRS (17–19 m). Most feeding events occurred in VRS zones (78 and 86% for small and large‐VRS, respectively), although VRS accounted for a small proportion of bottom phase of dives in distance travelled. This suggests a strong link between VRS behaviour and foraging success. There was a hierarchical structure to the VRS; most small‐VRS (95%) were nested within large‐VRS (i.e. nested VRS). Importantly, nested VRS had significantly higher feeding rates than non‐nested VRS, because nested VRS contained small‐ and large‐VRS with higher and lower feeding rates, respectively. These results suggest that seals forage on mesopelagic prey in a hierarchical patch system where high‐density patches at small scales are nested within low‐density patches at larger scales. We demonstrated that seals employed scale‐dependent, hierarchical 3D movements and that underwater fine‐scale sinuous movements (i.e. VRS) were strongly linked to higher foraging success, particularly within nested VRS zones. We suggest that seals enhanced foraging success by employing hierarchical movements that possibly reflect the hierarchical property of prey distribution. Although recent studies advocate that optimal searching behaviour would be scale‐independent (e.g. Lévy walk), our study suggests that scale‐dependent processes are important components of successful foraging behaviour.

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.