Robustly estimating the demographic contribution of immigration: Simulation, sensitivity analysis and seals.

Identifying important demographic drivers of population dynamics is fundamental for understanding life-history evolution and implementing effective conservation measures. Integrated population models (IPMs) coupled with transient life table response experiments (tLTREs) allow ecologists to quantify the contributions of demographic parameters to observed population change. While IPMs can estimate parameters that are not estimable using any data source alone, for example, immigration, the estimated contribution of such parameters to population change is prone to bias. Currently, it is unclear when robust conclusions can be drawn from them. We sought to understand the drivers of a rebounding southern elephant seal population on Marion Island using the IPM-tLTRE framework, applied to count and mark-recapture data on 9500 female seals over nearly 40 years. Given the uncertainty around IPM-tLTRE estimates of immigration, we also aimed to investigate the utility of simulation and sensitivity analyses as general tools for evaluating the robustness of conclusions obtained in this framework. Using a Bayesian IPM and tLTRE analysis, we quantified the contributions of survival, immigration and population structure to population growth. We assessed the sensitivity of our estimates to choice of multivariate priors on immigration and other vital rates. To do so we make a novel application of Gaussian process priors, in comparison with commonly used shrinkage priors. Using simulation, we assessed our model's ability to estimate the demographic contribution of immigration under different levels of temporal variance in immigration. The tLTRE analysis suggested that adult survival and immigration were the most important drivers of recent population growth. While the contribution of immigration was sensitive to prior choices, the estimate was consistently large. Furthermore, our simulation study validated the importance of immigration by showing that our estimate of its demographic contribution is unlikely to result as a biased overestimate. Our results highlight the connectivity between distant populations of southern elephant seals, illustrating that female dispersal can be important in regulating the abundance of local populations even when natal site fidelity is high. More generally, we demonstrate how robust ecological conclusions may be obtained about immigration from the IPM-tLTRE framework, by combining sensitivity analysis and simulation.

Killer whale acoustic patterns respond to prey abundance and environmental variability around the Prince Edward Islands, Southern Ocean.

Killer whales are apex predators with temporally and spatially varying distributions throughout the world's oceans. Their ecology and behaviour are poorly understood in most regions due to limited research, often because of logistical challenges. Here, we used a passive acoustic monitoring device to investigate the seasonal acoustic occurrence and diel vocalizing behaviour of killer whales around the remote sub-Antarctic Prince Edward Islands (PEIs), Southern Ocean. Killer whales showed diel vocalizing patterns that varied seasonally in relation to their prey abundance and social activities. Killer whale calls were intermittently detected year-round with a high number of hours containing calls in October to December, and a secondary peak in February to May, corresponding to seal prey abundance. Random forest modelling identified wind speed as the primary predictor of the occurrence of killer whale calls (with a negative correlation) while sea surface height, chlorophyll-a and sea surface temperature were moderately important. We provide the first acoustic evidence that killer whale occurrence around the PEIs might coincide with variability in environmental conditions and prey abundance. Our results provide the first indication of diel vocalizing pattern of killer whales in the Southern Ocean. This knowledge is important for understanding killer whale ecology and adaptation to the changing oceans.

The effect of prey abundance and fisheries on the survival, reproduction, and social structure of killer whales (Orcinus orca) at subantarctic Marion Island.

Most marine apex predators are keystone species that fundamentally influence their ecosystems through cascading top-down processes. Reductions in worldwide predator abundances, attributed to environmental- and anthropogenic-induced changes to prey availability and negative interactions with fisheries, can have far-reaching ecosystem impacts. We tested whether the survival of killer whales (Orcinus orca) observed at Marion Island in the Southern Indian Ocean correlated with social structure and prey variables (direct measures of prey abundance, Patagonian toothfish fishery effort, and environmental proxies) using multistate models of capture-recapture data spanning 12 years (2006-2018). We also tested the effect of these same variables on killer whale social structure and reproduction measured over the same period. Indices of social structure had the strongest correlation with survival, with higher sociality associated with increased survival probability. Survival was also positively correlated with Patagonian toothfish fishing effort during the previous year, suggesting that fishery-linked resource availability is an important determinant of survival. No correlation between survival and environmental proxies of prey abundance was found. At-island prey availability influenced the social structure of Marion Island killer whales, but none of the variables explained variability in reproduction. Future increases in legal fishing activity may benefit this population of killer whales through the artificial provisioning of resources they provide.

Are hippos Africa's most influential megaherbivore? A review of ecosystem engineering by the semi-aquatic common hippopotamus.

Megaherbivores perform vital ecosystem engineering roles, and have their last remaining stronghold in Africa. Of Africa's remaining megaherbivores, the common hippopotamus (Hippopotamus amphibius) has received the least scientific and conservation attention, despite how influential their ecosystem engineering activities appear to be. Given the potentially crucial ecosystem engineering influence of hippos, as well as mounting conservation concerns threatening their long-term persistence, a review of the evidence for hippos being ecosystem engineers, and the effects of their engineering, is both timely and necessary. In this review, we assess, (i) aspects of hippo biology that underlie their unique ecosystem engineering potential; (ii) evaluate hippo ecological impacts in terrestrial and aquatic environments; (iii) compare the ecosystem engineering influence of hippos to other extant African megaherbivores; (iv) evaluate factors most critical to hippo conservation and ecosystem engineering; and (v) highlight future research directions and challenges that may yield new insights into the ecological role of hippos, and of megaherbivores more broadly. We find that a variety of key life-history traits determine the hippo's unique influence, including their semi-aquatic lifestyle, large body size, specialised gut anatomy, muzzle structure, small and partially webbed feet, and highly gregarious nature. On land, hippos create grazing lawns that contain distinct plant communities and alter fire spatial extent, which shapes woody plant demographics and might assist in maintaining fire-sensitive riverine vegetation. In water, hippos deposit nutrient-rich dung, stimulating aquatic food chains and altering water chemistry and quality, impacting a host of different organisms. Hippo trampling and wallowing alters geomorphological processes, widening riverbanks, creating new river channels, and forming gullies along well-utilised hippo paths. Taken together, we propose that these myriad impacts combine to make hippos Africa's most influential megaherbivore, specifically because of the high diversity and intensity of their ecological impacts compared with other megaherbivores, and because of their unique capacity to transfer nutrients across ecosystem boundaries, enriching both terrestrial and aquatic ecosystems. Nonetheless, water pollution and extraction for agriculture and industry, erratic rainfall patterns and human-hippo conflict, threaten hippo ecosystem engineering and persistence. Therefore, we encourage greater consideration of the unique role of hippos as ecosystem engineers when considering the functional importance of megafauna in African ecosystems, and increased attention to declining hippo habitat and populations, which if unchecked could change the way in which many African ecosystems function.

Determinants of moult haulout phenology and duration in southern elephant seals.

Phenological shifts are among the most obvious biological responses to environmental change, yet documented responses for Southern Ocean marine mammals are extremely rare. Marine mammals can respond to environmental changes through phenological flexibility of their life-history events such as breeding and moulting. Southern elephant seals (Mirounga leonina) undergo an obligatory annual moult which involves the rapid shedding of epidermal skin and hair while seals fast ashore. We quantified the timing (phenology) and duration (the time from arrival ashore to departure) of the moult haulout of 4612 female elephant seals at Marion Island over 32 years. Using linear mixed-effects models, we investigated age, breeding state and environmental drivers of moult timing and haulout duration. We found no clear evidence for a temporal shift in moult phenology or its duration. Annual variation in moult arrival date and haulout duration was small relative to age and breeding effects, which explained more than 90% of the variance in moult arrival date and 25% in moult haulout duration. All environmental covariates we tested explained minimal variation in the data. Female elephant seals moulted progressively later as juveniles, but adults age 4 and older had similar moult start dates that depended on the breeding state of the female. In contrast, moult haulout duration was not constant with age among adults, but instead became shorter with increasing age. Moulting is energetically expensive and differences in the moult haulout duration are possibly due to individual variation in body mass and associated metabolizable energy reserves, although other drivers (e.g. hormones) may also be present. Individual-based data on moult arrival dates and haulout duration can be used as auxiliary data in demographic modelling and may be useful proxies of other important biological parameters such as body condition and breeding history.

Positive early-late life-history trait correlations in elephant seals.

Correlations between early- and late-life performance are a major prediction of life-history theory. Negative early-late correlations can emerge because biological processes are optimized for early but not late life (e.g., rapid development may accelerate the onset of senescence; "developmental theory of aging") or because allocation to early-life performance comes at a cost in terms of late-life performance (as in the disposable soma theory). But variation in genetic and environmental challenges that each individual has to cope with during early life may also lead to positive early-late life-history trait correlations (the "fixed heterogeneity" or "individual quality" hypothesis). We analyzed individual life-history trajectories of 7,420 known-age female southern elephant seals (Mirounga leonina) monitored over 36 yr to determine how actuarial senescence (a proxy for late-life performance) correlate with age at first reproduction (a proxy for early-life performance). As some breeding events may not be detected in this field study, we used a custom "multievent" hierarchical model to estimate the age at first reproduction and correlate it to other life-history traits. The probability of first reproduction was 0.34 at age 3, with most females breeding for the first time at age 4, and comparatively few at older ages. Females with an early age of first reproduction outperformed delayed breeders in all aspects we considered (survival, rate of senescence, net reproductive output) but one: early breeders appeared to have an onset of actuarial senescence 1 yr earlier compared to late breeders. Genetics and environmental conditions during early life likely explain the positive correlation between early- and late-life performance. Our results provide the first evidence of actuarial senescence in female southern elephant seals.

Can the carbon and nitrogen isotope values of offspring be used as a proxy for their mother's diet? Using foetal physiology to interpret bulk tissue and amino acid δ15N values.

The measurement of bulk tissue nitrogen (δ15N) and carbon isotope values (δ13C) chronologically along biologically inert tissues sampled from offspring can provide a longitudinal record of their mothers' foraging habits. This study tested the important assumption that mother-offspring stable isotope values are positively and linearly correlated. In addition, any change in the mother-offspring bulk tissues and individual amino acids that occurred during gestation was investigated. Whiskers sampled from southern elephant seal pups (Mirounga leonina) and temporally overlapping whiskers from their mothers were analyzed. This included n = 1895 chronologically subsampled whisker segments for bulk tissue δ15N and δ13C in total and n = 20 whisker segments for amino acid δ15N values, sampled from recently weaned pups (n = 17), juvenile southern elephant seals (SES) < 2 years old (n = 23) and adult female SES (n = 17), which included nine mother-offspring pairs. In contrast to previous studies, the mother-offspring pairs were not in isotopic equilibrium or linearly correlated during gestation: the Δ15N and Δ13C mother-offspring offsets increased by 0.8 and 1.2‰, respectively, during gestation. The foetal bulk δ15N values were 1.7 ± 0.5‰ (0.9-2.7‰) higher than mothers' δ15N values before birth, while the foetal δ13C increased by ~1.7‰ during gestation and were 1.0 ± 0.5‰ (0.0-1.9‰) higher than their mothers' δ13C at the end of pregnancy. The mother-offspring serine and glycine Δ15N differed by ~4.3‰, while the foetal alanine δ15N values were 1.4‰ lower than that of their mothers during the third trimester of pregnancy. The observed mother-offspring δ15N differences are likely explained by shuttling of glutamate-glutamine and glycine-serine amongst skeletal muscle, liver, placenta and foetal tissue. Foetal development relies primarily on remobilized endogenous maternal proteinaceous sources. Researchers should consider foetal physiology when using offspring bulk tissue isotope values as biomarkers for the mother's isotopic composition as part of monitoring programmes.

Publisher Correction: The genetic legacy of extreme exploitation in a polar vertebrate.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Fasting affects amino acid nitrogen isotope values: a new tool for identifying nitrogen balance of free-ranging mammals.

Changes in the nutritional status of free-ranging animals have a strong influence on individual fitness, yet it remains challenging to monitor longitudinally. Nitrogen (δ15N) and carbon (δ13C) isotope values measured chronologically along the length of metabolically inert keratinous tissues can be used as a nutritional biomarker to retrospectively reconstruct the foraging ecology and eco-physiology of consumers. We quantitatively describe the physiological effects of fasting on amino acid metabolism using sequentially measured bulk tissue and amino acid δ15N values along the length of whiskers sampled from free-ranging juvenile, subadults, adult female, and male southern elephant seals (SES; Mirounga leonina) on Marion Island in the Southern Ocean. For both juveniles and adult females, whisker segments representing fasting had significantly higher bulk tissue δ15N values of 0.6 ± 0.5‰ and 1.3-1.8‰, respectively, in comparison to segments unaffected by fasting. We also found a large increase (2-6‰) in δ15N values for most glucogenic amino acids and a simultaneous depletion (2-3‰) of alanine in segments reflecting fasting, which enabled us to accurately predict (74%) the nutritional status of our model species. We hypothesize that the glucose-alanine cycle is the mechanism driving the observed depletion of alanine δ15N values during fasting. We demonstrated that keratinaceous tissues can be used as a longitudinal nutritional biomarker to detect changes in the nitrogen balance of an individual. Moreover, it is evident that physiological factors have an important influence on tissue δ15N values and can lead to erroneous bulk tissue or amino acid isotope-based reconstructions of foraging habits.

Tracking of marine predators to protect Southern Ocean ecosystems.

Southern Ocean ecosystems are under pressure from resource exploitation and climate change1,2. Mitigation requires the identification and protection of Areas of Ecological Significance (AESs), which have so far not been determined at the ocean-basin scale. Here, using assemblage-level tracking of marine predators, we identify AESs for this globally important region and assess current threats and protection levels. Integration of more than 4,000 tracks from 17 bird and mammal species reveals AESs around sub-Antarctic islands in the Atlantic and Indian Oceans and over the Antarctic continental shelf. Fishing pressure is disproportionately concentrated inside AESs, and climate change over the next century is predicted to impose pressure on these areas, particularly around the Antarctic continent. At present, 7.1% of the ocean south of 40°S is under formal protection, including 29% of the total AESs. The establishment and regular revision of networks of protection that encompass AESs are needed to provide long-term mitigation of growing pressures on Southern Ocean ecosystems.

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.

What's in a whisker? High-throughput analysis of twenty-eight C19 and C21 steroids in mammalian whiskers by ultra-performance convergence chromatography-tandem mass spectrometry.

Obtaining longitudinal endocrinological data from free-ranging animals remains challenging. Steroid hormones can be extracted sequentially from non-invasively sampled biologically inert keratinous tissues, such as feathers, nails, hair and whiskers. However, uncertainty regarding the type and levels of steroids incorporated into such tissues complicates their utility in wildlife studies. Here, we developed a novel, comprehensive method to analyze fourteen C19 and fourteen C21 steroids deposited chronologically along the length of seal whiskers in a single, 6-minute chromatographic step, using ultra-performance convergence chromatography-tandem mass spectrometry. The limits of detection and quantification ranged from 0.01 to 2 ng/mL and from 0.1 to 10 ng/mL, respectively. The accuracy and precision were within acceptable limits for steroids at concentrations ≥2 ng/mL. The recovery (mean = 107.5% at 200 ng/mL), matrix effect and process efficiency of steroids evaluated, using blanked whisker matrix samples, were acceptable. The method was applied to the analysis of steroid hormone levels in adult female whisker segments obtained from southern elephant seals (Mirounga leonina), n = 10, and two fur seal species, Antarctic fur seals (Arctocephalus gazella; n = 5) and subantarctic fur seals (Arctocephalus tropicalis; n = 5), sampled between 2012 and 2017. In the whisker subsamples analyzed (n = 71), the median concentration of steroid hormones detected above the LOQ ranged from 2.0 to 273.7 pg/mg. This was the first extraction of multiple C19 and C21 steroids, including their C11-oxy metabolites, from the whiskers of mammals. Measuring hormones sequentially along the whisker lengths can contribute to our understanding of the impact of stress associated with environmental/climate changes that affect the health, survival of organisms, as well as to delineate the reproductive cycles of free-living mammals with cryptic life stages.

Trade-offs between age-related breeding improvement and survival senescence in highly polygynous elephant seals: Dominant males always do better.

Life history trade-off theory predicts that current reproduction can negatively affect survival and future reproduction. Few studies have assessed breeding costs for males of polygynous species compared to females, despite substantial variation in breeding success among individual males (e.g. subordinate cf. dominant breeders). Specifically, differentiating between the cost of attending breeding seasons, and the additional cost of successfully securing and mating females is lacking. We investigated whether trade-offs are present in the highly polygynous male southern elephant seal (Mirounga leonina) using 34-years of individual-level data. We compare age-specific survival, recruitment and future breeding success probabilities of pre-breeders (males yet to recruit) and breeders (subordinate and dominant social ranks) using multievent models. Pre-breeders and breeders of overlapping ages had similar survival probabilities, suggesting that there was no attendance cost for early recruits. In addition, the probability of recruiting as a dominant breeder never exceeded recruitment probability as a subordinate breeder of the same age. Therefore, older pre-breeders that delayed attendance costs generally did not improve their breeding success (probability of being dominant) at recruitment more than younger recruits. Rather, recruitment age may be a function of individual quality, with lower quality individuals requiring more time to socially mature. When comparing subordinate and dominant breeders, we found clear evidence for survival senescence, with subordinate breeders having a higher baseline mortality. In contrast, age-specific future breeding success (probability of being dominant at t + 1) increased with age, with dominant breeders maintaining higher subsequent breeding success than subordinate breeders. The opposite trends in survival and future breeding success for both subordinate and dominant breeders may indicate a lifetime, population-level trade-off. However, we found no evidence to suggest that being a dominant breeder consecutively (and having a higher accumulated breeding cost) accelerated the rate of senescence when compared to individuals that were previously subordinate. Thus, males experienced actuarial senescence regardless of social rank, with dominant (and possibly high quality) breeders showing a reduced trade-off between survival and future breeding success. We make several novel contributions to understanding polygynous male life histories and southern elephant seal demography.

Pinniped entanglement in oceanic plastic pollution: A global review.

Oceanic plastic pollution is a growing worldwide environmental concern, endangering numerous marine species. Pinnipeds are particularly susceptible to entanglement, especially in abandoned, lost or discarded fishing gear and packaging straps. We searched three international databases to compile a comprehensive review of all reported pinniped entanglements over the last 40 years, with the aim to identify areas of concern and foci for mitigation. The majority of published records of entanglement emanate from North America and Oceania and are focused on a few populous species (notably, Zalophus californianus and Arctocephalus gazella). Reporting bias, skewed research effort and incomplete understanding of plastic pollution and pinniped abundance overlap, combine to cloud our understanding of the entanglement problem. Broader geographical effort in entanglement data collection, reporting of such data, and improved quantification of the proportions of populations, sexes and ages that are most susceptible, will aid our efforts to pinpoint priority mitigation measures.

Preferred, small-scale foraging areas of two Southern Ocean fur seal species are not determined by habitat characteristics.

BACKGROUND: To understand and predict the distribution of foragers, it is crucial to identify the factors that affect individual movement decisions at different scales. Individuals are expected to adjust their foraging movements to the hierarchical spatial distribution of resources. At a small local scale, spatial segregation in foraging habitat happens among individuals of closely situated colonies. If foraging segregation is due to differences in distribution of resources, we would expect segregated foraging areas to have divergent habitat characteristics. RESULTS: We investigated how environmental characteristics of preferred foraging areas differ between two closely situated Subantarctic fur seal (Arctocephalus tropicalis) colonies and a single Antarctic fur seal (A. gazella) colony that forage in different pelagic areas even though they are located well within each other's foraging range. We further investigated the influence of the seasonal cycle on those environmental factors. This study used tracking data from 121 adult female Subantarctic and Antarctic fur seals, collected during summer and winter (2009-2015), from three different colonies. Boosted Regression Tree species distribution models were used to determine key environmental variables associated with areas of fur seal restricted search behaviour. There were no differences in the relative influence of key environmental variables between colonies and seasons. The variables with the most influence for each colony and season were latitude, longitude and magnitude of sea-currents. The influence of latitude and longitude is a by-product of the species' distinct foraging areas, despite the close proximity (< 25 km) of the colonies. The predicted potential foraging areas for each colony changed from summer to winter, reflecting the seasonal cycle of the Southern Ocean. The model predicted that the potential foraging areas of females from the three colonies should overlap, and the fact they do not in reality indicates that factors other than environmental are influencing the location of each colony's foraging area. CONCLUSIONS: The results indicated that small scale spatial segregation of foraging habitats is not driven by bottom-up processes. It is therefore important to also consider other potential drivers, e.g. competition, information transfer, and memory, to understand animal foraging decisions and movements.

Making use of multiple surveys: Estimating breeding probability using a multievent-robust design capture-recapture model.

Increased environmental stochasticity due to climate change will intensify temporal variance in the life-history traits, and especially breeding probabilities, of long-lived iteroparous species. These changes may decrease individual fitness and population viability and is therefore important to monitor. In wild animal populations with imperfect individual detection, breeding probabilities are best estimated using capture-recapture methods. However, in many vertebrate species (e.g., amphibians, turtles, seabirds), nonbreeders are unobservable because they are not tied to a territory or breeding location. Although unobservable states can be used to model temporary emigration of nonbreeders, there are disadvantages to having unobservable states in capture-recapture models. The best solution to deal with unobservable life-history states is therefore to eliminate them altogether. Here, we achieve this objective by fitting novel multievent-robust design models which utilize information obtained from multiple surveys conducted throughout the year. We use this approach to estimate annual breeding probabilities of capital breeding female elephant seals (Mirounga leonina). Conceptually, our approach parallels a multistate version of the Barker/robust design in that it combines robust design capture data collected during discrete breeding seasons with observations made at other times of the year. A substantial advantage of our approach is that the nonbreeder state became "observable" when multiple data sources were analyzed together. This allowed us to test for the existence of state-dependent survival (with some support found for lower survival in breeders compared to nonbreeders), and to estimate annual breeding transitions to and from the nonbreeder state with greater precision (where current breeders tended to have higher future breeding probabilities than nonbreeders). We used program E-SURGE (2.1.2) to fit the multievent-robust design models, with uncertainty in breeding state assignment (breeder, nonbreeder) being incorporated via a hidden Markov process. This flexible modeling approach can easily be adapted to suit sampling designs from numerous species which may be encountered during and outside of discrete breeding seasons.

Moving in the Anthropocene: Global reductions in terrestrial mammalian movements.

Animal movement is fundamental for ecosystem functioning and species survival, yet the effects of the anthropogenic footprint on animal movements have not been estimated across species. Using a unique GPS-tracking database of 803 individuals across 57 species, we found that movements of mammals in areas with a comparatively high human footprint were on average one-half to one-third the extent of their movements in areas with a low human footprint. We attribute this reduction to behavioral changes of individual animals and to the exclusion of species with long-range movements from areas with higher human impact. Global loss of vagility alters a key ecological trait of animals that affects not only population persistence but also ecosystem processes such as predator-prey interactions, nutrient cycling, and disease transmission.

Regional differences in plastic ingestion among Southern Ocean fur seals and albatrosses.

We provide data on regional differences in plastic ingestion for two Southern Ocean top predators: Arctocephalus fur seals and albatrosses (Diomedeidae). Fur seals breeding on Macquarie Island in the 1990s excreted small (mainly 2-5 mm) plastic fragments, probably derived secondarily from myctophid fish. No plastic was found in the scats of these seals breeding on three islands in the southwest Indian and central South Atlantic Oceans, despite myctophids dominating their diets at these locations. Compared to recent reports of plastic ingestion by albatrosses off the east coast of South America, we confirm that plastic is seldom found in the stomachs of Thalassarche albatrosses off South Africa, but found no Diomedea albatrosses to contain plastic, compared to 26% off South America. The reasons for such regional differences are unclear, but emphasize the importance of reporting negative as well as positive records of plastic ingestion by marine biota.