Use of acoustic signals in Cape fur seal mother-pup reunions: individual signature, signal propagation and pup home range.

The Cape fur seal (Arctocephalus pusillus pusillus) is one of the most colonial mammals, with colonies of up to hundreds of thousands of individuals during the breeding season. During the lactation period, mothers and pups are regularly separated as females undertake multi-day foraging trips at sea. Mothers and pups use a mutual vocal recognition system to reunite after separation. Such communication is highly constrained by both high background noise and risk of individual confusion owing to the density of seals. This study aimed to experimentally assess the acoustic features relevant for mother-pup vocal identification and the propagation properties of their calls. Playback experiments revealed that mother and pup individual vocal signatures rely on both temporal and frequency parameters: amplitude and frequency modulations, timbre and fundamental frequency (f0). This is more parameters than in any colonial species studied so far. The combinational use of acoustic features reinforces the concept that both environmental and social constraints may have acted as selective pressures on the individual vocal recognition systems. Theoretical propagation distances of mother and pup vocalisations were estimated to be below the range of distances at which mother-pup reunions can occur. This suggests that Cape fur seals may have strong abilities to extract vocal signals from the background noise, as previously demonstrated in the highly colonial king penguin. Investigating the transmission of information throughout the propagation of the signal as well as the ability of the receiving individual to decipher vocal signatures is crucial to understanding vocal recognition systems in the wild.

Life-history stage influences immune investment and oxidative stress in response to environmental heterogeneity in Antarctic fur seals.

Immune defenses are crucial for survival but costly to develop and maintain. Increased immune investment is therefore hypothesized to trade-off with other life-history traits. Here, we examined innate and adaptive immune responses to environmental heterogeneity in wild Antarctic fur seals. In a fully crossed, repeated measures design, we sampled 100 pups and their mothers from colonies of contrasting density during seasons of contrasting food availability. Biometric and cortisol data as well as blood for the analysis of 13 immune and oxidative status markers were collected at two key life-history stages. We show that immune responses of pups are more responsive than adults to variation in food availability, but not population density, and are modulated by cortisol and condition. Immune investment is associated with different oxidative status markers in pups and mothers. Our results suggest that early life stages show greater sensitivity to extrinsic and intrinsic effectors, and that immunity may be a strong target for natural selection even in low-pathogen environments such as Antarctica.

Little evidence of inbreeding depression for birth mass, survival and growth in Antarctic fur seal pups.

Inbreeding depression, the loss of offspring fitness due to consanguineous mating, is generally detrimental for individual performance and population viability. We investigated inbreeding effects in a declining population of Antarctic fur seals (Arctocephalus gazella) at Bird Island, South Georgia. Here, localised warming has reduced the availability of the seal's staple diet, Antarctic krill, leading to a temporal increase in the strength of selection against inbred offspring, which are increasingly failing to recruit into the adult breeding population. However, it remains unclear whether selection operates before or after nutritional independence at weaning. We therefore used microsatellite data from 885 pups and their mothers, and SNP array data from 98 mother-offspring pairs, to quantify the effects of individual and maternal inbreeding on three important neonatal fitness traits: birth mass, survival and growth. We did not find any clear or consistent effects of offspring or maternal inbreeding on any of these traits. This suggests that selection filters inbred individuals out of the population as juveniles during the time window between weaning and recruitment. Our study brings into focus a poorly understood life-history stage and emphasises the importance of understanding the ecology and threats facing juvenile pinnipeds.

Niche partitioning and individual specialisation in resources and space use of sympatric fur seals at their range margin.

Ecological theory predicts niche partitioning between high-level predators living in sympatry as a mechanism to minimise the selective pressure of competition. Accordingly, male Australian fur seals Arctocephalus pusillus doriferus and New Zealand fur seals A. forsteri that live in sympatry should exhibit partitioning in their broad niches (in habitat and trophic dimensions) in order to coexist. However, at the northern end of their distributions in Australia, both are recolonising their historic range after a long absence due to over-exploitation, and their small population sizes suggest competition should be weak and may allow overlap in niche space. We found some niche overlap, yet clear partitioning in diet trophic level (δ15N values from vibrissae), spatial niche space (horizontal and vertical telemetry data) and circadian activity patterns (timing of dives) between males of each species, suggesting competition may remain an active driver of niche partitioning amongst individuals even in small, peripheral populations. Consistent with individual specialisation theory, broad niches of populations were associated with high levels of individual specialisation for both species, despite putative low competition. Specialists in isotopic space were not necessarily specialists in spatial niche space, further emphasising their diverse individual strategies for niche partitioning. Males of each species displayed distinct foraging modes, with Australian fur seals primarily benthic and New Zealand fur seals primarily epipelagic, though unexpectedly high individual specialisation for New Zealand fur seals might suggest marginal populations provide exceptions to the pattern generally observed amongst other fur seals.

Sealing the deal - Antarctic fur seals' active hunting tactics to capture small evasive prey revealed by miniature sonar tags.

The ability of predators to adopt hunting tactics that minimise escape reactions from prey is crucial for efficient foraging, and depends on detection capabilities and locomotor performance of both predators and prey. Here, we investigated the efficiency of a small pinniped, the Antarctic fur seal (Arctocephalus gazella) at exploiting their small prey by describing for the first time their fine-scale predator-prey interactions. We compared these with those from another diving predator, the southern elephant seal (Mirounga leonina) that forage on the same prey type. We used data recorded by a newly developed sonar tag that combines active acoustics with ultrahigh-resolution movement sensors to study simultaneously the fine-scale behaviour of both Antarctic fur seals and prey during predator-prey interactions in more than 1200 prey capture events for eight female Antarctic fur seals. Our results showed that Antarctic fur seals and their prey detect each other at the same time, i.e. 1-2 s before the strike, forcing Antarctic fur seals to display reactive fast-moving chases to capture their prey. In contrast, southern elephant seals detect their prey up to 10 s before the strike, allowing them to approach their prey stealthily without triggering an escape reaction. The active hunting tactics used by Antarctic fur seals is probably very energy consuming compared with the stalking tactics used by southern elephant seals but might be compensated for by the consumption of faster-moving larger prey. We suggest that differences in manoeuvrability, locomotor performance and detection capacities and in pace of life between Antarctic fur seals and southern elephant seals might explain these differences in hunting styles.

The influence of prey availability on behavioral decisions and reproductive success of a central-place forager during lactation.

Marine central-place foragers are increasingly faced with altered prey landscapes, necessitating predictions of the impact of such changes on behavior, reproductive success, and population dynamics. We used state-dependent behavioral life history theory implemented via Stochastic Dynamic Programming (SDP) to explore the influence of changes in prey distribution and energy gain from foraging on the behavior and reproductive success of a central place forager during lactation. Our work is motivated by northern fur seals (Callorhinus ursinus) because of the ongoing population decline of the Eastern Pacific stock and projected declines in biomass of walleye pollock (Gadus chalcogrammus), a key fur seal prey species in the eastern Bering Sea. We also explored how changes in female and pup metabolic rates, body size, and lactation duration affected model output to provide insight into traits that might experience selective pressure in response to reductions in prey availability. Simulated females adopted a central-place foraging strategy after an initial extended period spent on land (4.7-8.3 days). Trip durations increased as the high energy prey patch moved farther from land or when the energy gain from foraging decreased. Increases in trip duration adversely affected pup growth rates and wean mass despite attempts to compensate by increasing land durations. Metabolic rate changes had the largest impacts on pup wean mass, with reductions in a pup's metabolic rate allowing females to successfully forage at distances of 600+ km from land for up to 15+ days. Our results indicate that without physiological adaptations, a rookery is unlikely to be viable if the primary foraging grounds are 400 km or farther from the rookery. To achieve pup growth rates characteristic of a population experiencing rapid growth, model results indicate the primary foraging grounds need to be <150 km from the rookery.

Sympatric otariids increase trophic segregation in response to warming ocean conditions in Peruvian Humboldt Current System.

Determining trophic habits of predator communities is essential to measure interspecific interactions and response to environmental fluctuations. South American fur seals, Arctocephalus australis (SAFS) and sea lions Otaria byronia (SASL), coexist along the coasts of Peru. Recently, ocean warming events (2014-2017) that can decrease and impoverish prey biomass have occurred in the Peruvian Humboldt Current System. In this context, our aim was to assess the effect of warming events on long-term inter- and intra-specific niche segregation. We collected whisker from SAFS (55 females and 21 males) and SASL (14 females and 22 males) in Punta San Juan, Peru. We used δ13C and δ15N values serially archived in otariid whiskers to construct a monthly time series for 2005-2019. From the same period we used sea level anomaly records to determine shifts in the predominant oceanographic conditions using a change point analysis. Ellipse areas (SIBER) estimated niche width of species-sex groups and their overlap. We detected a shift in the environmental conditions marking two distinct periods (P1: January 2005-October 2013; P2: November 2013-December 2019). Reduction in δ15N in all groups during P2 suggests impoverished baseline values with bottom-up effects, a shift towards consuming lower trophic level prey, or both. Reduced overlap between all groups in P2 lends support of a more redundant assemblage during the colder P1 to a more trophically segregated assemblage during warmer P2. SASL females show the largest variation in response to the warming scenario (P2), reducing both ellipse area and δ15N mean values. Plasticity to adapt to changing environments and feeding on a more available food source without fishing pressure can be more advantageous for female SASL, albeit temporary trophic bottom-up effects. This helps explain larger population size of SASL in Peru, in contrast to the smaller and declining SAFS population.

Shifts in maternal foraging strategies during pregnancy promote offspring health and survival in a marine top predator.

The success of maternal foraging strategies during the rearing period can greatly impact the physiology and survival of dependent offspring. Surprisingly though, little is known on the fitness consequences of foraging strategies during the foetal period. In this study, we characterized variation in maternal foraging strategy throughout pregnancy in a marine top predator (South American fur seal, Arctocephalus australis), and asked if these shifts predicted neonatal health and postnatal survival. We found that during early pregnancy all pregnant females belonged to a single, homogenized foraging niche without evident clusters. Intriguingly though, during late pregnancy, individual fur seal mothers diverged into two distinct foraging niches characterized by a benthic-nearshore and a pelagic-offshore strategy. Females that shifted towards the benthic-nearshore strategy gave birth to pups with greater body mass, higher plasmatic levels of glucose and lower levels of blood urea nitrogen. The pups born to these benthic females were eight times more likely to survive compared to females using the pelagic-offshore foraging strategy during late pregnancy. These survival effects were mediated primarily by the impact of foraging strategies on neonatal glucose independent of protein metabolic profile and body mass. Benthic-nearshore foraging strategies during late pregnancy potentially allow for the greater maternal transfer of glucose to the foetus, leading to higher chances of neonatal survival. These results call for a deeper understanding of the balance between resource acquisition and allocation provided by distinct foraging polymorphisms during critical life-history periods, and how this trade-off may be adaptive under certain environmental conditions.

Movement patterns and activity levels are shaped by the neonatal environment in Antarctic fur seal pups.

Tracking studies of juveniles are rare compared to those of adults, and consequently little is known about the influence of intrinsic and extrinsic factors on activity during this critical life stage. We used hourly GPS data, collected from 66 Antarctic fur seal pups from birth until moulting, to investigate the explanatory power of multiple individual-based and environmental variables on activity levels. Pups were sampled from two nearby breeding colonies of contrasting density during two subsequent years, and a two-state hidden Markov model was used to identify modalities in their movement behaviour, specifically 'active' and 'inactive' states. We found that movement was typified by central place exploration, with active movement away from and subsequent return to a location of inactivity. The probability of such directed exploration was unaffected by several factors known to influence marine mammal movement including sex, body condition, and temperature. Compared to pups born at the high-density colony, pups at low-density were more active, increased their activity with age, and transitioned earlier into the tussock grass, which offers protection from predators and extreme weather. Our study illustrates the importance of extrinsic factors, such as colony of birth, to early-life activity patterns and highlights the adaptive potential of movement.

Fur seals do, but sea lions don't - cross taxa insights into exhalation during ascent from dives.

Management of gases during diving is not well understood across marine mammal species. Prior to diving, phocid (true) seals generally exhale, a behaviour thought to assist with the prevention of decompression sickness. Otariid seals (fur seals and sea lions) have a greater reliance on their lung oxygen stores, and inhale prior to diving. One otariid, the Antarctic fur seal (Arctocephalus gazella), then exhales during the final 50-85% of the return to the surface, which may prevent another gas management issue: shallow-water blackout. Here, we compare data collected from animal-attached tags (video cameras, hydrophones and conductivity sensors) deployed on a suite of otariid seal species to examine the ubiquity of ascent exhalations for this group. We find evidence for ascent exhalations across four fur seal species, but that such exhalations are absent for three sea lion species. Fur seals and sea lions are no longer genetically separated into distinct subfamilies, but are morphologically distinguished by the thick underfur layer of fur seals. Together with their smaller size and energetic dives, we suggest their air-filled fur might underlie the need to perform these exhalations, although whether to reduce buoyancy and ascent speed, for the avoidance of shallow-water blackout or to prevent other cardiovascular management issues in their diving remains unclear. This article is part of the theme issue 'Measuring physiology in free-living animals (Part I)'.

Wintertime overlaps between female Antarctic fur seals (Arctocephalus gazella) and the krill fishery at South Georgia, South Atlantic.

The diet of Antarctic fur seals (Arctocephalus gazella) at South Georgia is dominated by Antarctic krill (Euphausia superba). During the breeding season, foraging trips by lactating female fur seals are constrained by their need to return to land to provision their pups. Post-breeding, seals disperse in order to feed and recover condition; estimates indicate c.70% of females remain near to South Georgia, whilst others head west towards the Patagonian Shelf or south to the ice-edge. The krill fishery at South Georgia operates only during the winter, providing the potential for fur seal: fishery interaction during these months. Here we use available winter (May to September) tracking data from Platform Terminal Transmitter (PTT) tags deployed on female fur seals at Bird Island, South Georgia. We develop habitat models describing their distribution during the winters of 1999 and 2003 with the aim of visualising and quantifying the degree of spatial overlap between female fur seals and krill harvesting in South Georgia waters. We show that spatial distribution of fur seals around South Georgia is extensive, and that the krill fishery overlaps with small, highly localised areas of available fur seal habitat. From these findings we discuss the implications for management, and future work.

The northernmost haulout site of South American sea lions and fur seals in the western South Atlantic.

We present estimates of the seasonal and spatial occupation by pinnipeds of the Wildlife Refuge of Ilha dos Lobos (WRIL), based on aerial photographic censuses. Twenty aerial photographic censuses were analysed between July 2010 and November 2018. To assess monthly differences in the numbers of pinnipeds in the WRIL we used a Generalized Linear Mixed Model. Spatial analysis was carried out using Kernel density analysis of the pinnipeds on a grid plotted along the WRIL. Subadult male South American sea lions (Otaria flavescens) were the most abundant pinniped in the WRIL. Potential females of this species were also recorded during half of the census. The maximum number of pinnipeds observed in the WRIL was 304 in September 2018, including an unexpected individual southern elephant seal (Mirounga leonina), and a high number of South American fur seal yearlings (Arctocephalus australis). However, there was no statistically significant difference in counts between months. In all months analysed, pinnipeds were most often found concentrated in the northern portion of the island, with the highest abundances reported in September. This study confirms the importance of the WRIL as a haulout site for pinnipeds in Brazil, recommends that land research and recreational activities occur in months when no pinnipeds are present, and encourages a regulated marine mammal-based tourism during winter and spring months.

Environmental influences on foraging effort, success and efficiency in female Australian fur seals.

Understanding the factors which influence foraging behaviour and success in marine mammals is crucial to predicting how their populations may respond to environmental change. The Australian fur seal (Arctocephalus pusillus doriferus, AUFS) is a predominantly benthic forager on the shallow continental shelf of Bass Strait, and represents the greatest biomass of marine predators in south-eastern Australia. The south-east Australian region is experiencing rapid oceanic warming, predicted to lead to substantial alterations in prey diversity, distribution and abundance. In the present study, foraging effort and indices of foraging success and efficiency were investigated in 138 adult female AUFS (970 foraging trips) during the winters of 1998-2019. Large scale climate conditions had a strong influence on foraging effort, foraging success and efficiency. Foraging effort and foraging success were also strongly influenced by winter chlorophyll-a concentrations and sea-surface height anomalies in Bass Strait. The results suggest increasing foraging effort and decreasing foraging success and efficiency under anticipated environmental conditions, which may have population-level impacts.

Drivers of concentrated predation in an Antarctic marginal-ice-zone food web.

Predators impact preyscapes (3-D distribution of forage species) by consuming prey according to their abilities or by altering prey behavior as they avoid being consumed. We elucidate prey (Antarctic silverfish[Pleuragramma antarctica] and crystal krill[Euphausia chrystallorophias]) responses to predation associated with the marginal ice zone (MIZ) of the McMurdo Sound, Antarctica, polynya. Prey abundance and habitat was sampled across a 30 × 15 km area by remotely-operated vehicle, and included locations that were accessible (ice edge) or inaccessible (solid fast ice) to air-breathing predators. Prey and habitat sampling coincided with bio-logging of Adélie penguins and observations of other air-breathing predators (penguins, seals, and whales), all of which were competing for the same prey. Adélie penguins dived deeper, and more frequently, near the ice edge. Lowered abundance of krill at the ice edge indicated they were depleted or were responding to increased predation and/or higher light levels along the ice edge. Penguin diet shifted increasingly to silverfish from krill during sampling, and was correlated with the arrival of krill-eating whales. Behaviorally-mediated, high trophic transfer characterizes the McMurdo Sound MIZ, and likely other MIZs, warranting more specific consideration in food web models and conservation efforts.

The genetic legacy of extreme exploitation in a polar vertebrate.

Understanding the effects of human exploitation on the genetic composition of wild populations is important for predicting species persistence and adaptive potential. We therefore investigated the genetic legacy of large-scale commercial harvesting by reconstructing, on a global scale, the recent demographic history of the Antarctic fur seal (Arctocephalus gazella), a species that was hunted to the brink of extinction by 18th and 19th century sealers. Molecular genetic data from over 2,000 individuals sampled from all eight major breeding locations across the species' circumpolar geographic distribution, show that at least four relict populations around Antarctica survived commercial hunting. Coalescent simulations suggest that all of these populations experienced severe bottlenecks down to effective population sizes of around 150-200. Nevertheless, comparably high levels of neutral genetic variability were retained as these declines are unlikely to have been strong enough to deplete allelic richness by more than around 15%. These findings suggest that even dramatic short-term declines need not necessarily result in major losses of diversity, and explain the apparent contradiction between the high genetic diversity of this species and its extreme exploitation history.

Intra-specific Niche Partitioning in Antarctic Fur Seals, Arctocephalus gazella.

Competition for resources within a population can lead to niche partitioning between sexes, throughout ontogeny and among individuals, allowing con-specifics to co-exist. We aimed to quantify such partitioning in Antarctic fur seals, Arctocephalus gazella, breeding at South Georgia, which hosts ~95% of the world's population. Whiskers were collected from 20 adult males and 20 adult females and stable isotope ratios were quantified every 5 mm along the length of each whisker. Nitrogen isotope ratios (δ15N) were used as proxies for trophic position and carbon isotope ratios (δ13C) indicated foraging habitat. Sexual segregation was evident: δ13C values were significantly lower in males than females, indicating males spent more time foraging south of the Polar Front in maritime Antarctica. In males δ13C values declined with age, suggesting males spent more time foraging south throughout ontogeny. In females δ13C values revealed two main foraging strategies: 70% of females spent most time foraging south of the Polar Front and had similar δ15N values to males, while 30% of females spent most time foraging north of the Polar Front and had significantly higher δ15N values. This niche partitioning may relax competition and ultimately elevate population carrying capacity with implications for ecology, evolution and conservation.

The skin structures and their role in the thermoregulation of the South American fur seal (Arctocephalus australis).

The skin of the South American fur seal (Arctocephalus australis) is important for animal thermoregulation in both terrestrial and aquatic environments. Skin tissue samples were collected from A. australis for microscopic analysis and were related to anatomical references. The aim of this study was to describe the skin morphology, as well as to suggest the major anatomical regions and skin components involved in the thermoregulation of this species. Using light microscopy, the skin of six animals was examined based on histological, morphometric, and immunohistochemical criteria. Hair follicle morphology was examined using scanning electron microscopy. The skin was classified as either thick or thin based on its epidermal thickness. The thin epidermis regions had more abundant hair follicles, as well as high pigmentation, whereas the thick epidermis regions had very pigmented epidermal layers. Pigmentation of hair and skin is fundamental for protection against ultraviolet rays; moreover, hair is important in preventing abrasion, and provides an insulating layer against the external environment, which can be much colder than body temperature. Furthermore, the dermis is well vascularized, especially the superficial dermis. All regions of the skin have adaptations for maintaining the animal's condition in both terrestrial and aquatic environments. Among the studied regions, the interdigital region from hindflipper showed important morphological characteristics related to thermoregulation, such as having an epidermis of intermediate thickness, a dermis with a small number of hairs, a large amount of blood vessels, and sweat glands with large lumens, indicating that heat exchange in this region may be faster.

Isotopic variation in blood components based on their biochemistry and physiology: A comparison between sharks and fur seals.

Research using stable isotopes analysis (SIA) of carbon (δ13 C) and nitrogen (δ15 N) in blood components is lacking, because of the challenge of sample collection, processing, and storage in remote areas. There also is a paucity of information regarding the effect of tissue biochemical composition on isotopic ratios with few comparisons among taxa. We collected blood samples from shortfin mako sharks (n = 70; 2016) and Guadalupe fur seals (n = 25; 2017). All samples were centrifuged to obtain plasma from sharks and serum from the Guadalupe fur seals, and all the samples were prepared for SIA and analyzed using a Costech 4010 elemental analyzer interfaced with a Delta V Plus isotope ratio mass spectrometer. We found significant differences between plasma δ13 C values of shortfin mako sharks (-17.6 ± 0.9‰) and serum of Guadalupe fur seals (-20.3 ± 1.2‰), but we did not find any differences for δ15 N values between the two species. The differences in δ13 C values between species are probably due to the specific blood composition and to the different biochemical characteristics and different adaptations within taxa. These findings highlight the importance of further research on the influence of biochemistry features on isotopic results, in this way a more accurate assessment will be possible for this factor, separating it from the dietary influences on stable isotopic values.

Migratory strategies of juvenile northern fur seals (Callorhinus ursinus): bridging the gap between pups and adults.

In species exhibiting differential migration by sex and age, understanding what differences exist, and the adaptive reasons for these differences is critical for determining how demographic groups will respond to environmental variability and anthropogenic perturbations. We used satellite-telemetered movement and diving data to investigate differential migration and its ontogeny in a highly migratory North Pacific Ocean predator, the northern fur seal (Callorhinus ursinus; NFS), with a focus on understudied juvenile (1- to 2-year-old) animals. We instrumented 71 juvenile NFS in two years (2006-07 and 2007-08) at three major North American breeding sites and compared their migratory strategies with pups and adults. Although sexual dimorphism is strong in adult NFS, only weak differences in body mass between sexes were found in juveniles, which had similar body mass to pups (~3-4 months). However, unlike widely-dispersed pups, juvenile male and female NFS dispersed in different directions, and used different habitats characterized by distinct hydrography and prey assemblages during migration, similar to breeding adults. Juvenile diving behavior differed only modestly among habitats and between sexes, consistent with weak differences in body mass. Evidence of habitat sexual segregation by juvenile NFS contradicts previous hypotheses that physiological differences predominantly drive the ontogeny of differential migration.