Elephant seal foraging success is enhanced in Antarctic coastal polynyas.

Antarctic polynyas are persistent open water areas which enable early and large seasonal phytoplankton blooms. This high primary productivity, boosted by iron supply from coastal glaciers, attracts organisms from all trophic levels to form a rich and diverse community. How the ecological benefit of polynya productivity is translated to the highest trophic levels remains poorly resolved. We studied 119 southern elephant seals feeding over the Antarctic shelf and demonstrated that: (i) 96% of seals foraging here used polynyas, with individuals spending on average 62% of their time there; (ii) the seals exhibited more area-restricted search behaviour when in polynyas; and (iii) these seals gained more energy (indicated by increased buoyancy from greater fat stores) when inside polynyas. This higher-quality foraging existed even when ice was not present in the study area, indicating that these are important and predictable foraging grounds year-round. Despite these energetic advantages from using polynyas, not all the seals used them extensively. Factors other than food supply may influence an individual's choice in their use of feeding grounds, such as exposure to predation or the probability of being able to return to distant sub-Antarctic breeding sites.

Decadal changes in blood δ13C values, at-sea distribution, and weaning mass of southern elephant seals from Kerguelen Islands.

Changes in the foraging environment and at-sea distribution of southern elephant seals from Kerguelen Islands were investigated over a decade (2004-2018) using tracking, weaning mass, and blood δ13C values. Females showed either a sub-Antarctic or an Antarctic foraging strategy, and no significant shift in their at-sea distribution was detected between 2004 and 2017. The proportion of females foraging in sub-Antarctic versus Antarctic habitats did not change over the 2006-2018 period. Pup weaning mass varied according to the foraging habitat of their mothers. The weaning mass of sub-Antarctic foraging mothers' pups decreased by 11.7 kg over the study period, but they were on average 5.8 kg heavier than pups from Antarctic foraging mothers. Pup blood δ13C values decreased by 1.1‰ over the study period regardless of their sex and the presumed foraging habitat of their mothers. Together, these results suggest an ecological change is occurring within the Indian sector of the Southern Ocean with possible consequences on the foraging performance of southern elephant seals. We hypothesize that this shift in δ13C is related to a change in primary production and/or in the composition of phytoplankton communities, but this requires further multidisciplinary investigations.

Optimizing lifetime reproductive output: Intermittent breeding as a tactic for females in a long-lived, multiparous mammal.

In iteroparous species, intermittent breeding is an important life-history tactic that can greatly affect animal population growth and viability. Despite its importance, few studies have quantified the consequences of breeding pauses on lifetime reproductive output, principally because calculating lifetime reproductive output requires knowledge of each individual's entire reproductive history. This information is extremely difficult to obtain in wild populations. We applied novel statistical approaches that account for uncertainty in state assessment and individual heterogeneity to an 18-year capture-recapture dataset of 6,631 female southern elephant seals from Macquarie Island. We estimated survival and breeding probabilities, and investigated the consequences of intermittent breeding on lifetime reproductive output. We found consistent differences in females' demographic performance between two heterogeneity classes. In particular, breeding imbued a high cost on survival in the females from the heterogeneity class 2, assumed to be females of lower quality. Individual quality also appeared to play a major role in a female's decision to skip reproduction with females of poorer quality more likely to skip breeding events than females of higher quality. Skipping some breeding events allowed females from both heterogeneity classes to increase lifetime reproductive output over females that bred annually. However, females of lower quality produced less offspring over their lifetime. Intermittent breeding seems to be used by female southern elephant seals as a tactic to offset reproductive costs on survival and enhance lifetime reproductive output but remains unavoidable and driven by individual-specific constraints in some other females.

Decadal changes in habitat characteristics influence population trajectories of southern elephant seals.

Understanding divergent biological responses to climate change is important for predicting ecosystem level consequences. We use species habitat models to predict the winter foraging habitats of female southern elephant seals and investigate how changes in environmental variables within these habitats may be related to observed decreases in the Macquarie Island population. There were three main groups of seals that specialized in different ocean realms (the sub-Antarctic, the Ross Sea and the Victoria Land Coast). The physical and climate attributes (e.g. wind strength, sea surface height, ocean current strength) varied amongst the realms and also displayed different temporal trends over the last two to four decades. Most notably, sea ice extent increased on average in the Victoria Land realm while it decreased overall in the Ross Sea realm. Using a species distribution model relating mean residence times (time spent in each 50 × 50 km grid cell) to 9 climate and physical co-variates, we developed spatial predictions of residence time to identify the core regions used by the seals across the Southern Ocean from 120°E to 120°W. Population size at Macquarie Island was negatively correlated with ice concentration within the core habitat of seals using the Victoria Land Coast and the Ross Sea. Sea ice extent and concentration is predicted to continue to change in the Southern Ocean, having unknown consequences for the biota of the region. The proportion of Macquarie Island females (40%) utilizing the relatively stable sub-Antarctic region, may buffer this population against longer-term regional changes in habitat quality, but the Macquarie Island population has persistently decreased (-1.45% per annum) over seven decades indicating that environmental changes in the Antarctic are acting on the remaining 60% of the population to impose a long-term population decline in a top Southern Ocean predator.

Seal mothers expend more on offspring under favourable conditions and less when resources are limited.

In mammals, maternal expenditure on offspring is a complex mix of several factors including the species' mating system, offspring sex and the condition and age of the mother. While theory suggests that in polygynous species mothers should wean larger male offspring than females when resources and maternal conditions allow, the evidence for this remains equivocal. Southern elephant seals are highly dimorphic, polygynous capital breeders existing in an environment with highly variable resources and should therefore provide clear evidence to support the theoretical expectations of differential maternal expenditure in male and female pups. We quantified maternal size (mass and length) and pup size at birth and weaning for 342 elephant seal mothers at Macquarie Island. The study was conducted over 11 years of contrasting sea-ice and Southern Annular Mode values, both indices of maternal prey resources. Overall, large females weaned male pups that weighed 17 kg (15·5%) more than female pups. Maternal condition varied by as much as 59 kg among years, and was positively related to Southern Annular Mode, and negatively to maximum sea-ice extent. Smaller mothers weaned relatively larger male pups under favourable conditions, this effect was less apparent for larger mothers. We developed a simple model linking environmental variation to maternal masses post-partum, followed by maternal masses post-partum to weaning masses and then weaning masses to pup survival and demonstrated that environmental conditions affected predicted survival so that the pups of small mothers had an estimated 7% increase in first year survival in 'good' vs. 'bad' years compared to 1% for female pups of large mothers. Co-occurrence of environmental quality and conservative reproductive tactics suggests that mothers retain substantial plasticity in maternal care, enhancing their lifetime reproductive success by adjusting reproductive expenditure relative to both prevailing environmental conditions and their own capabilities.

Bottom-up regulation of a pole-ward migratory predator population.

As the effects of regional climate change are most pronounced at polar latitudes, we might expect polar-ward migratory populations to respond as habitat suitability changes. The southern elephant seal (Mirounga leonina L.) is a pole-ward migratory species whose populations have mostly stabilized or increased in the past decade, the one exception being the Macquarie Island population which has decreased continuously over the past 50 years. To explore probable causes of this anomalous trend, we counted breeding female seals annually between 1988 and 2011 in order to relate annual rates of population change (r) to foraging habitat changes that have known connections with atmospheric variability. We found r (i) varied annually from -0.016 to 0.021 over the study period, (ii) was most effected by anomalous atmospheric variability after a 3 year time lag was introduced (R = 0.51) and (iii) was associated with sea-ice duration (SID) within the seals' foraging range at the same temporal lag. Negative r years may be extrapolated to explain, at least partially, the overall trend in seal abundance at Macquarie Island; specifically, increasing SID within the seals foraging range has a negative influence on their abundance at the island. Evidence is accruing that suggests southern elephant seal populations may respond positively to a reduced sea-ice field.

Age-specific cost of first reproduction in female southern elephant seals.

When to commence breeding is a crucial life-history decision that may be the most important determinant of an individual's lifetime reproductive output and can have major consequences on population dynamics. The age at which individuals first reproduce is an important factor influencing the intensity of potential costs (e.g. reduced survival) involved in the first breeding event. However, quantifying age-related variation in the cost of first reproduction in wild animals remains challenging because of the difficulty in reliably recording the first breeding event. Here, using a multi-event capture-recapture model that accounts for both imperfect detection and uncertainty in the breeding status on an 18-year dataset involving 6637 individuals, we estimated age and state-specific survival of female elephant seals (Mirounga leonina) in the declining Macquarie Island population. We detected a clear cost of first reproduction on survival. This cost was higher for both younger first-time breeders and older first-time breeders compared with females recruiting at age four, the overall mean age at first reproduction. Neither earlier primiparity nor delaying primiparity appear to confer any evolutionary advantage, rather the optimal strategy seems to be to start breeding at a single age, 4 years.

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.

Growth in marine mammals: a review of growth patterns, composition and energy investment.

Growth of structural mass and energy reserves influences individual survival, reproductive success, population and species life history. Metrics of structural growth and energy storage of individuals are often used to assess population health and reproductive potential, which can inform conservation. However, the energetic costs of tissue deposition for structural growth and energy stores and their prioritization within bioenergetic budgets are poorly documented. This is particularly true across marine mammal species as resources are accumulated at sea, limiting the ability to measure energy allocation and prioritization. We reviewed the literature on marine mammal growth to summarize growth patterns, explore their tissue compositions, assess the energetic costs of depositing these tissues and explore the tradeoffs associated with growth. Generally, marine mammals exhibit logarithmic growth. This means that the energetic costs related to growth and tissue deposition are high for early postnatal animals, but small compared to the total energy budget as animals get older. Growth patterns can also change in response to resource availability, habitat and other energy demands, such that they can serve as an indicator of individual and population health. Composition of tissues remained consistent with respect to protein and water content across species; however, there was a high degree of variability in the lipid content of both muscle (0.1-74.3%) and blubber (0.4-97.9%) due to the use of lipids as energy storage. We found that relatively few well-studied species dominate the literature, leaving data gaps for entire taxa, such as beaked whales. The purpose of this review was to identify such gaps, to inform future research priorities and to improve our understanding of how marine mammals grow and the associated energetic costs.

Extreme polygyny results in intersex differences in age-dependent survival of a highly dimorphic marine mammal.

Developmental differences in vital rates are especially profound in polygamous mating systems. Southern elephant seals (Mirounga leonina) are highly dimorphic and extremely polygynous marine mammals. A demographic model, supported by long-term capture-mark-recapture records, investigated the influence of sex and age on survival in this species. The study revealed clear differences between female and male age-dependent survival rates. Overall juvenile survival estimates were stable around 80-85% for both sexes. However, male survival estimates were 5-10% lower than females in the same age classes until 8 years of age. At this point, male survival decreased rapidly to 50% ± 10% while female estimates remained constant at 80% ± 5%. Different energetic requirements could underpin intersex differences in adult survival. However, the species' strong sexual dimorphism diverges during early juvenile development when sex-specific survival rates were less distinct. Maximizing growth is especially advantageous for males, with size being a major determinant of breeding probability. Maturing males may employ a high-risk high-reward foraging strategy to compensate for extensive sexual selection pressures and sex-specific energetic needs. Our findings suggest sex-specific adult survival is a result of in situ ecological interactions and evolutionary specialization associated with being a highly polygynous marine predator.

Sex, body size, and boldness shape the seasonal foraging habitat selection in southern elephant seals.

Selecting foraging habitat is a fundamental behavior in the life of organisms as it directly links resource acquisition to fitness. Differences in habitat selection among individuals may arise from several intrinsic and extrinsic factors, and yet, their interaction has been given little attention in the study of wild populations. We combine sex, body size, and boldness to explain individual differences in the seasonal foraging habitat selection of southern elephant seals (Mirounga leonina) from the Kerguelen Archipelago. We hypothesize that habitat selection is linked to the trade-off between resource acquisition and risk, and that individuals differ in their position along this trade-off because of differences in reproductive strategies, life stages, and metabolic requirements. Before the post-molt foraging trip, we used a novel object approach test to quantify the boldness of 28 subadult and adult females and 42 subadult males and equipped them with data loggers to track their movements at sea. Subadult males selected neritic and oceanic habitats, whereas females mostly selected less productive oceanic habitats. Both sexes showed a seasonal shift from Antarctic habitats in the south in the summer to the free of ice subantarctic and subtropical habitats in the north in the winter. Males avoided oceanic habitats and selected more productive neritic and Antarctic habitats with body size mostly in the winter. Bolder males selected northern warmer waters in winter, while shyer ones selected the Kerguelen plateau and southern colder oceanic waters. Bolder females selected the Kerguelen plateau in the summer when prey profitability is assumed to be the highest. This study not only provides new insights into the spatiotemporal foraging ecology of elephant seals in relation to personality but also emphasizes the relevance of combining several intrinsic and extrinsic factors in understanding among-individual variation in space use essential in wildlife management and conservation.

Key questions in marine mammal bioenergetics.

Bioenergetic approaches are increasingly used to understand how marine mammal populations could be affected by a changing and disturbed aquatic environment. There remain considerable gaps in our knowledge of marine mammal bioenergetics, which hinder the application of bioenergetic studies to inform policy decisions. We conducted a priority-setting exercise to identify high-priority unanswered questions in marine mammal bioenergetics, with an emphasis on questions relevant to conservation and management. Electronic communication and a virtual workshop were used to solicit and collate potential research questions from the marine mammal bioenergetic community. From a final list of 39 questions, 11 were identified as 'key' questions because they received votes from at least 50% of survey participants. Key questions included those related to energy intake (prey landscapes, exposure to human activities) and expenditure (field metabolic rate, exposure to human activities, lactation, time-activity budgets), energy allocation priorities, metrics of body condition and relationships with survival and reproductive success and extrapolation of data from one species to another. Existing tools to address key questions include labelled water, animal-borne sensors, mark-resight data from long-term research programs, environmental DNA and unmanned vehicles. Further validation of existing approaches and development of new methodologies are needed to comprehensively address some key questions, particularly for cetaceans. The identification of these key questions can provide a guiding framework to set research priorities, which ultimately may yield more accurate information to inform policies and better conserve marine mammal populations.

N-dimensional animal energetic niches clarify behavioural options in a variable marine environment.

Animals respond to environmental variation by exhibiting a number of different behaviours and/or rates of activity, which result in corresponding variation in energy expenditure. Successful animals generally maximize efficiency or rate of energy gain through foraging. Quantification of all features that modulate energy expenditure can theoretically be modelled as an animal energetic niche or power envelope; with total power being represented by the vertical axis and n-dimensional horizontal axes representing extents of processes that affect energy expenditure. Such an energetic niche could be used to assess the energetic consequences of animals adopting particular behaviours under various environmental conditions. This value of this approach was tested by constructing a simple mechanistic energetics model based on data collected from recording devices deployed on 41 free-living Magellanic penguins (Spheniscus magellanicus), foraging from four different colonies in Argentina and consequently catching four different types of prey. Energy expenditure was calculated as a function of total distance swum underwater (horizontal axis 1) and maximum depth reached (horizontal axis 2). The resultant power envelope was invariant, irrespective of colony location, but penguins from the different colonies tended to use different areas of the envelope. The different colony solutions appeared to represent particular behavioural options for exploiting the available prey and demonstrate how penguins respond to environmental circumstance (prey distribution), the energetic consequences that this has for them, and how this affects the balance of energy acquisition through foraging and expenditure strategy.

Climate influences on female survival in a declining population of southern elephant seals (Mirounga leonina).

The Southern Ocean has been disproportionately affected by climate change and is therefore an ideal place to study the influence of changing environmental conditions on ecosystems. Changes in the demography of predator populations are indicators of broader shifts in food web structure, but long-term data are required to study these effects. Southern elephant seals (Mirounga leonina) from Macquarie Island have consistently decreased in population size while all other major populations across the Southern Ocean have recently stabilized or are increasing. Two long-term mark-recapture studies (1956-1967 and 1993-2009) have monitored this population, which provides an opportunity to investigate demographic performance over a range of climatic conditions. Using a 9-state matrix population model, we estimated climate influences on female survival by incorporating two major climatic indices into our model: The Southern Annular Mode (SAM) and the Southern Oscillation Index (SOI). Our best model included a 1 year lagged effect of SAM and an unlagged SOI as covariates. A positive relationship with SAM1 (lagged) related the previous year's SAM with juvenile survival, potentially due to changes in local prey availability surrounding Macquarie Island. The unlagged SOI had a negative effect on both juvenile and adult seals, indicating that sea ice dynamics and access to foraging grounds on the East Antarctic continental shelf could explain the different contributions of ENSO events on the survival of females in this population.

Inter- and intrasex habitat partitioning in the highly dimorphic southern elephant seal.

Partitioning resources is a key mechanism for avoiding intraspecific competition and maximizing individual energy gain. However, in sexually dimorphic species it is difficult to discern if partitioning is due to competition or the different resource needs of morphologically distinct individuals. In the highly dimorphic southern elephant seal, there are intersexual differences in habitat use; at Iles Kerguelen, males predominantly use shelf waters, while females use deeper oceanic waters. There are equally marked intrasexual differences, with some males using the nearby Kerguelen Plateau, and others using the much more distant Antarctic continental shelf (~2,000 km away). We used this combination of inter and intrasexual behavior to test two hypotheses regarding habitat partitioning in highly dimorphic species. (a) that intersexual differences in habitat use will not appear until the seals diverge in body size and (b) that some habitats have higher rates of energy return than others. In particular, that the Antarctic shelf would provide higher energy returns than the Kerguelen Shelf, to offset the greater cost of travel. We quantified the habitat use of 187 southern elephant seals (102 adult females and 85 subadult males). The seals in the two groups were the same size (~2.4 m) removing the confounding effect of body size. We found that the intersexual differences in habitat use existed before the divergence in body size. Also, we found that the amount of energy gained was the same in all of the major habitats. This suggests that the use of shelf habitats by males is innate, and a trade-off between the need to access the large benthic prey available on shelf waters, against the higher risk of predation there. Intrasexual differences in habitat use are another trade-off; although there are fewer predators on the Antarctic shelf, it is subject to considerable interannual fluctuations in sea-ice extent. In contrast, the Kerguelen Plateau presents more consistent foraging opportunities, but contains higher levels of predation. Habitat partitioning in this highly dimorphic species is therefore the result of complex interplay of life history strategies, environmental conditions and predation pressure.

Risk assessment of SARS-CoV-2 in Antarctic wildlife.

The coronavirus disease 2019 (COVID-19) pandemic is caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). This pathogen has spread rapidly across the world, causing high numbers of deaths and significant social and economic impacts. SARS-CoV-2 is a novel coronavirus with a suggested zoonotic origin with the potential for cross-species transmission among animals. Antarctica can be considered the only continent free of SARS-CoV-2. Therefore, concerns have been expressed regarding the potential human introduction of this virus to the continent through the activities of research or tourism to minimise the effects on human health, and the potential for virus transmission to Antarctic wildlife. We assess the reverse-zoonotic transmission risk to Antarctic wildlife by considering the available information on host susceptibility, dynamics of the infection in humans, and contact interactions between humans and Antarctic wildlife. The environmental conditions in Antarctica seem to be favourable for the virus stability. Indoor spaces such as those at research stations, research vessels or tourist cruise ships could allow for more transmission among humans and depending on their movements between different locations the virus could be spread across the continent. Among Antarctic wildlife previous in silico analyses suggested that cetaceans are at greater risk of infection whereas seals and birds appear to be at a low infection risk. However, caution needed until further research is carried out and consequently, the precautionary principle should be applied. Field researchers handling animals are identified as the human group posing the highest risk of transmission to animals while tourists and other personnel pose a significant risk only when in close proximity (< 5 m) to Antarctic fauna. We highlight measures to reduce the risk as well as identify of knowledge gaps related to this issue.

Complete tag loss in capture-recapture studies affects abundance estimates: An elephant seal case study.

In capture-recapture studies, recycled individuals occur when individuals lose all of their tags and are recaptured as though they were new individuals. Typically, the effect of these recycled individuals is assumed negligible.Through a simulation-based study of double-tagging experiments, we examined the effect of recycled individuals on parameter estimates in the Jolly-Seber model with tag loss (Cowen & Schwarz, 2006). We validated the simulation framework using long-term census data of elephant seals.Including recycled individuals did not affect estimates of capture, survival, and tag-retention probabilities. However, with low tag-retention rates, high capture rates, and high survival rates, recycled individuals produced overestimates of population size. For the elephant seal case study, we found population size estimates to be between 8% and 53% larger when recycled individuals were ignored.Ignoring the effects of recycled individuals can cause large biases in population size estimates. These results are particularly noticeable in longer studies.

A baseline for POPs contamination in Australian seabirds: little penguins vs. short-tailed shearwaters.

While globally distributed throughout the world's ecosystems, there is little baseline information on persistent organic pollutants (POPs) in marine environments in Australia and, more broadly, the Southern Hemisphere. To fill this knowledge gap, we collected baseline information on POPs in migratory short-tailed shearwaters (Ardenna tenuirostris) from Fisher Island, Tasmania, and resident little penguins (Eudyptula minor) from Phillip Island, Victoria. Levels of polychlorinated biphenyls (PCBs), organochlorine pesticides (OCPs) and brominated flame retardants (BFRs) were determined from blood samples, with total contamination ranging 7.6-47.7 ng/g ww for short-tailed shearwaters and 0.12-46.9 ng/g ww for little penguins. In both species contamination followed the same pattern where PCBs>OCPs>BFRs. BFR levels included the presence of the novel flame retardant hexabromobenzene (HBB). These novel results of POPs in seabirds in southeast Australia provide important information on the local (penguins) and global (shearwaters) distribution of POPs in the marine environment.