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.

Canine morphometrics as a tool for distinguishing species, sex, and age class in Southern Ocean fur seals.

Carcasses resulting from natural mortalities are invaluable for use in scientific studies, provided species, sex, and age class are known. When such data are unavailable, identifying skeletal remains is necessary if one is to use the information contained within samples. Teeth are amongst the best preserved skeletal remains owing to the durability of enamel and dentine. Here, we tested whether external measurements of canines could be used to distinguish two partially sympatric species of Southern Ocean fur seals, the Antarctic Arctocephalus gazella and Sub-Antarctic A. tropicalis fur seals. We also investigated whether the external measurements of canines could be used to determine the age, sex, as well as island of origin of the animals. Eight morphological variables (crown length, root length, crown width, root width, crown thickness, root thickness, total canine length, and count of external surface annular ridges) were recorded from canines of 340 individuals of known species, sex, and island of origin. The count of external annular ridges provided a good estimate of age, which was confirmed by counting the growth layer groups of sectioned teeth, especially for older animals (> 9 years old). External canine measurements proved useful in distinguishing species, as well as sex within and between species, particularly in adult animals. Species were more difficult to distinguish in females than in males. The islands of origin could only be inferred in male Antarctic fur seals. This study indicates that fur seal teeth of unknown provenance, found either in breeding colonies or as vagrants, provide evidence on species, sex, and age of the animal, which increases the value of associated samples. It further highlights the importance of external measurements of skeletal remains such as canine teeth in separating closely related species.

Focal Palatitis (Previously Focal Palatine Erosions) in Captive Cheetahs (Acinonyx jubatus).

Focal palatine erosion (FPE) is a misleading term that is used in the literature to describe inflammatory lesions associated with depressions of the palatal mucosa in cheetah. Cheetahs have large cheek teeth and these depressions are formed to accommodate them. Previously FPE was only described as a mandibular molar tooth malocclusion on the hard palate due to suspected rotation and super eruption of the mandibular molar teeth of cheetahs aged 18 months and older. Two hundred and fifty six cheetahs (135 male, 121 female), originating from two independent facilities, had their oral cavities evaluated as part of an annual health visit over a decade. Ninety-nine cheetahs were seen once, 59 cheetahs were seen twice, 33 were seen three times, 43 on four occasions, 16 on five occasions, 5 on six occasions, and 1 cheetah was seen seven times. Apart from these clinical cases a prospective study on 5 cheetah cubs (3 male and 2 female) was conducted to document their skull development and mandibular molar tooth eruption over a period of 25 months. Of the 261 cheetahs observed none developed rotation or super eruption of their mandibular molar teeth. The term FPE is a misnomer as these inflammatory lesions were found in palatal depressions opposing any of the cusps of all of the cheetah mandibular cheek teeth. It consisted mainly of deep ulcerations, inflammation and oedema and also micro abscess formation. In severe cases oro-nasal fistulas were present. Of all the depressions present on the cheetah's palate, the large one palatal to the 4th maxillary premolar tooth was most commonly affected. In the five cubs evaluated prospectively, focal palatitis was evident from the 7 month evaluation, before all the permanent teeth erupted. Conservative treatment of the inflamed depressions by removing the foreign material through curettage and copious flushing reduced the grade of the inflammation when observed on follow-up. Focal palatine erosion is an incorrect term used to describe focal palatitis that occurs randomly in cheetahs. This focal palatitis is often associated with foreign material trapped in the palatal depressions. Conservative management is sufficient to treat these animals without odontoplasties.

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)'.

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.

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.

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.

Seal bites at sub-Antarctic Marion Island: Incidence, outcomes and treatment recommendations.

Seal biologists at Marion Island (Southern Ocean) are in frequent contact with seals. During research activities, biologists may be bitten by seals, yet no standardised protocol for treating such bites is in place. Information on 22 seal bite cases at Marion Island was collected. Treatment of these bites varied, reflecting a need for standardised protocols for the treatment of bites. Recommendations for the in-field treatment of bites are presented. Five of the 22 cases had some symptoms which resembled 'seal finger' - a zoonotic infection, usually of the hands, that is contracted after a person comes into contact with tissues of seals or is bitten by one. However, in four of these cases, symptoms subsided within 4 days without antibiotic treatment; in the fifth case antibiotics were administered and symptoms subsided in 4 days. There is little evidence of the occurrence of seal finger at Marion Island, but this deserves further investigation.

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.

The retrospective analysis of Antarctic tracking data project.

The Retrospective Analysis of Antarctic Tracking Data (RAATD) is a Scientific Committee for Antarctic Research project led jointly by the Expert Groups on Birds and Marine Mammals and Antarctic Biodiversity Informatics, and endorsed by the Commission for the Conservation of Antarctic Marine Living Resources. RAATD consolidated tracking data for multiple species of Antarctic meso- and top-predators to identify Areas of Ecological Significance. These datasets and accompanying syntheses provide a greater understanding of fundamental ecosystem processes in the Southern Ocean, support modelling of predator distributions under future climate scenarios and create inputs that can be incorporated into decision making processes by management authorities. In this data paper, we present the compiled tracking data from research groups that have worked in the Antarctic since the 1990s. The data are publicly available through biodiversity.aq and the Ocean Biogeographic Information System. The archive includes tracking data from over 70 contributors across 12 national Antarctic programs, and includes data from 17 predator species, 4060 individual animals, and over 2.9 million observed locations.

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.

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.

Longitudinal Radiographic Study of Cranial Bone Growth in Young Cheetah.

Focal palatitis (also known as focal palatine erosion) is thought to be a developmental disease, specifically of cheetah in captivity raised on a commercial diet. The lack of chewing is thought to cause the mandibular molar to change angulation, contacting the palate and causing the lesions. We followed the development of five captive cheetah cubs, born within 2 weeks of each other, at the same facility. This longitudinal study followed the cubs cephalometrically from 7-months-old to 25-months-old. Of each cub we made a lateral and dorsoventral radiograph at 7, 13, 20, and 25-months-old. For each radiograph at each age, a predefined series of measurements were made including the angle of the molar. The latter was measured as the angle of the bisecting line running through the apex of the caudal molar root intersecting with a line drawn at the ventral margin of the mandible. The results confirmed that the cheetah skull and neurocranium follows the same neural growth pattern as has been described for other mammalians. Similarly the maxillofacial component follows the same somatic growth as seen in all mammalians excluding humans and non-human primates, where a pubertal growth spurt is present. Finally the angle of the mandibular molar at 7 months differed significantly from the angle at the other ages, however there were no statistical difference in the angulation of the molar after eruption (13 months and older ages). In these five cheetah the lack of chewing (as seen in captivity with a commercial or meat only based diet) did not alter the angulation of the mandibular molar, nor did the mandibular molars super erupt in these patients at 25-months-of-age.

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.

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.

Accuracy of using visual identification of white sharks to estimate residency patterns.

Determining the residency of an aquatic species is important but challenging and it remains unclear what is the best sampling methodology. Photo-identification has been used extensively to estimate patterns of animals' residency and is arguably the most common approach, but it may not be the most effective approach in marine environments. To examine this, in 2005, we deployed acoustic transmitters on 22 white sharks (Carcharodon carcharias) in Mossel Bay, South Africa to quantify the probability of detecting these tagged sharks by photo-identification and different deployment strategies of acoustic telemetry equipment. Using the data collected by the different sampling approaches (detections from an acoustic listening station deployed under a chumming vessel versus those from visual sightings and photo-identification), we quantified the methodologies' probability of detection and determined if the sampling approaches, also including an acoustic telemetry array, produce comparable results for patterns of residency. Photo-identification had the lowest probability of detection and underestimated residency. The underestimation is driven by various factors primarily that acoustic telemetry monitors a large area and this reduces the occurrence of false negatives. Therefore, we propose that researchers need to use acoustic telemetry and also continue to develop new sampling approaches as photo-identification techniques are inadequate to determine residency. Using the methods presented in this paper will allow researchers to further refine sampling approaches that enable them to collect more accurate data that will result in better research and more informed management efforts and policy decisions.

Effects of Smart Position Only (SPOT) tag deployment on white sharks Carcharodon carcharias in South Africa.

We present 15 individual cases of sub-adult white sharks that were SPOT tagged in South Africa from 2003-2004 and have been re-sighted as recently as 2011. Our observations suggest SPOT tags can cause permanent cosmetic and structural damage to white shark dorsal fins depending on the duration of tag attachment. SPOT tags that detached within 12-24 months did not cause long term damage to the dorsal fin other than pigmentation scarring. Within 12 months of deployment, tag fouling can occur. After 24 months of deployment permanent damage to the dorsal fin occurred. A shark survived this prolonged attachment and there seems little compromise on the animal's long term survival and resultant body growth. This is the first investigation detailing the long term effects of SPOT deployment on the dorsal fin of white sharks.

Shifting trends: detecting environmentally mediated regulation in long-lived marine vertebrates using time-series data.

Assessing the status and trends in animal populations is essential for effective species conservation and management practices. However, unless time-series abundance data demonstrate rapid and reliable fluctuations, objective appraisal of directionality of trends is problematic. We adopted a multiple-working hypotheses approach based on information-theoretic and Bayesian multi-model inference to examine the population trends and form of intrinsic regulation demonstrated by a long-lived species, the southern elephant seal. We also determined the evidence for density dependence in 11 other well-studied marine mammal species. (1) We tested the type of population regulation for elephant seals from Marion Island (1986-2004) and from 11 other marine mammal species, and (2) we described the trends and behavior of the 19-year population time series at Marion Island to identify changes in population trends. We contrasted five plausible trend models using information-theoretic and Bayesian-inference estimates of model parsimony. Our analyses identified two distinct phases of population growth for this population with the inflexion occurring in 1998. Thus, the population decreased between 1986 and 1997 (-3.7% per annum) and increased between 1997 and 2004 (1.9% per annum). An index of environmental stochasticity, the Southern Oscillation Index, explained some of the variance in r and N. We determined analytically that there was good evidence for density dependence in the Marion Island population and that density dependence was widespread among marine mammal species (67% of species showed evidence for population regulation). This approach demonstrates the potential functionality of a relatively simple technique that can be applied to short time series to identify the type of regulation, and the uncertainty associated with the phenomenon, operating in populations of large mammals.