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.

Foraging behavior and age affect maternal transfer of mercury to northern elephant seal pups.

Deep ocean foraging northern elephant seals (Mirounga angustirostris) consume fish and squid in remote depths of the North Pacific Ocean. Contaminants bioaccumulated from prey are subsequently transferred by adult females to pups during gestation and lactation, linking pups to mercury contamination in mesopelagic food webs (200-1000 m depths). Maternal transfer of mercury to developing seal pups was related to maternal mercury contamination and was strongly correlated with maternal foraging behavior (biotelemetry and isotopes). Mercury concentrations in lanugo (hair grown in utero) were among the highest observed worldwide for young pinnipeds (geometric mean 23.01 µg/g dw, range 8.03-63.09 µg/g dw; n = 373); thus, some pups may be at an elevated risk of sub-lethal adverse health effects. Fetal mercury exposure was affected by maternal foraging geographic location and depth; mercury concentrations were highest in pups of the deepest diving, pelagic females. Moreover, pup lanugo mercury concentrations were strongly repeatable among successive pups of individual females, demonstrating relative consistency in pup mercury exposure based on maternal foraging strategies. Northern elephant seals are biosentinels of a remote deep-sea ecosystem. Our results suggest that mercury within North Pacific mesopelagic food webs may also pose an elevated risk to other mesopelagic-foraging predators and their offspring.

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 (3-30 minutes) surface intervals coinciding with almost no foraging attempts (jaw motion) during 2 weeks of acute illness early in her post-breeding foraging trip. Elephant seals typically spend ~ 2 minutes at the surface. There were less frequent but highly extended (30-200 minutes) 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.

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.

Large-scale molecular diet analysis in a generalist marine mammal reveals male preference for prey of conservation concern.

Sex-specific diet information is important in the determination of predator impacts on prey populations. Unfortunately, the diet of males and females can be difficult to describe, particularly when they are marine predators. We combined two molecular techniques to describe haul-out use and prey preferences of male and female harbor seals (Phoca vitulina) from Comox and Cowichan Bay (Canada) during 2012-2013. DNA metabarcoding quantified the diet proportions comprised of prey species in harbor seal scat, and qPCR determined the sex of the individual that deposited each scat. Using 287 female and 260 male samples, we compared the monthly sex ratio with GLMs and analyzed prey consumption relative to sex, season, site, and year with PERMANOVA. The sex ratio between monthly samples differed widely in both years (range = 12%-79% males) and showed different patterns at each haul-out site. Male and female diet differed across both years and sites: Females consumed a high proportion of demersal fish species while males consumed more salmonid species. Diet composition was related to both sex and season (PERMANOVA: R 2 = 27%, p < 0.001; R 2 = 24%, p < 0.001, respectively) and their interaction (PERMANOVA: R 2 = 11%, p < 0.001). Diet differences between males and females were consistent across site and year, suggesting fundamental foraging differences, including that males may have a larger impact on salmonids than females. Our novel combination of techniques allowed for both prey taxonomic and spatiotemporal resolution unprecedented in marine predators.