Antarctic Fur Seals Research Articles

Correction: Ecosystem shifts inferred from long-term stable isotope analysis of male Antarctic fur seal Arctocephalus gazella teeth

Correction: Ecosystem shifts inferred from long-term stable isotope analysis of male Antarctic fur seal Arctocephalus gazella teeth

Commercial krill fishing within a foraging supergroup of fin whales in the Southern Ocean.

Commercial krill fishing within a foraging supergroup of fin whales in the Southern Ocean.

Seasonal and interannual variability in the diet of young and subadult male Antarctic fur seals as revealed by stable C and N isotope ratios

Detailed knowledge of marine mammal diet is critical to understand their ecological roles and for the adequate management of marine resources. Antarctic fur seals ( Arctocephalus gazella) in the Southern Atlantic Ocean rely largely on Antarctic krill ( Euphausia superba) during the summer months, but their winter diet remains largely unknown. Here, stable carbon and nitrogen isotope ratios in whiskers and blood of young (2–3 years old) and subadult (4–7 years old) Antarctic fur seal males from the South Shetland Islands were used to assess the seasonal and interannual changes in the krill contribution to their diet. The stable isotope ratios revealed that krill dominated the diet of young and subadult male Antarctic fur seals year-round, with penguins, and not fish, as the second major prey, regardless of year and season. The year-round reliance of young and subadult male Antarctic fur seals on krill should be considered for ecosystem-based fisheries management, as they represent the bulk of the fur seal population remaining off Antarctica during the winter months.

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.

Viral metagenomics reveals persistent as well as dietary acquired viruses in Antarctic fur seals

Viruses linked to animals inhabiting Antarctic latitudes remain poorly studied. Remote environments hosting large pinniped populations may be prone to exposure of immunologically naïve animals to new infectious agents due to increasing human presence or introduction of new animal species. Antarctic fur seals (Arctocephalus gazella) inhabiting the Western Antarctic Peninsula and the South Shetland Islands are challenged because of climate change and increased anthropogenic activity. In the present study, the fecal and serum virome of A. gazella was characterized by applying target enrichment next generation sequencing. The resulting viromes were dominated by CRESS-DNA sequences. Viruses known to infect vertebrate and invertebrate hosts were also observed in fecal samples. Fur seal picornavirus was present in all the fecal pools studied suggesting it is a prevalent virus in these species. Six different viruses presenting similarities with previously described A. gazella viruses or other otariids and mammal viruses were identified as potential new A. gazella viruses. Also, diet-derived viruses such as crustacean viruses were present in fecal content. Penguin viruses, but not fish viruses, were also detected. Obtained results contribute to a better understanding of the viral community present in these species, which is relevant for its conservation.

Intronic primers reveal unexpectedly high major histocompatibility complex diversity in Antarctic fur seals

The major histocompatibility complex (MHC) is a group of genes comprising one of the most important components of the vertebrate immune system. Consequently, there has been much interest in characterising MHC variation and its relationship with fitness in a variety of species. Due to the exceptional polymorphism of MHC genes, careful PCR primer design is crucial for capturing all of the allelic variation present in a given species. We therefore developed intronic primers to amplify the full-length 267 bp protein-coding sequence of the MHC class II DQB exon 2 in the Antarctic fur seal. We then characterised patterns of MHC variation among mother–offspring pairs from two breeding colonies and detected 19 alleles among 771 clone sequences from 56 individuals. The distribution of alleles within and among individuals was consistent with a single-copy, classical DQB locus showing Mendelian inheritance. Amino acid similarity at the MHC was significantly associated with genome-wide relatedness, but no relationship was found between MHC heterozygosity and genome-wide heterozygosity. Finally, allelic diversity was several times higher than reported by a previous study based on partial exon sequences. This difference appears to be related to allele-specific amplification bias, implying that primer design can strongly impact the inference of MHC diversity.

Evaluating Thermal and Color Sensors for Automating Detection of Penguins and Pinnipeds in Images Collected with an Unoccupied Aerial System

Estimating seabird and pinniped abundance is central to wildlife management and ecosystem monitoring in Antarctica. Unoccupied aerial systems (UAS) can collect images to support monitoring, but manual image analysis is often impractical. Automating target detection using deep learning techniques may improve data acquisition, but different image sensors may affect target detectability and model performance. We compared the performance of automated detection models based on infrared (IR) or color (RGB) images and tested whether IR images, or training data that included annotations of non-target features, improved model performance. For this assessment, we collected paired IR and RGB images of nesting penguins (Pygoscelis spp.) and aggregations of Antarctic fur seals (Arctocephalus gazella) with a small UAS at Cape Shirreff, Livingston Island (60.79 °W, 62.46 °S). We trained seven independent classification models using the Video and Image Analytics for Marine Environments (VIAME) software and created an open-access R tool, vvipr, to standardize the assessment of VIAME-based model performance. We found that the IR images and the addition of non-target annotations had no clear benefits for model performance given the available data. Nonetheless, the generally high performance of the penguin models provided encouraging results for further improving automated image analysis from UAS surveys.

Time and behavioral adjustments to lactation: Insights from a marine predator

AbstractThe energetic costs of lactation have been studied in many marine mammals, but little is known about the behavioral adjustments needed to cope with this event. By simultaneously measuring foraging behavior of lactating and nonlactating Antarctic fur seal females, we estimate the behavioral changes necessary to cope with the constraints of lactation and include the first comparative record of dive behavior between lactating and nonlactating female otariids. Nonlactating females exhibited highly variable foraging trip durations and spent long times onshore between trips. In contrast, lactating females exhibited consistently shorter trips and spent half the time hauled‐out compared to nonlactating females likely to maximize offspring provisioning. Lactating females show a reduced mean time per dive but greater percentage of time per trip spent diving compared to nonlactating animals. The reduction in time onshore and trip duration, together with modifications in dive performance suggests additional effort of lactating females to compensate for the constraints of rearing a pup, which has not been observed previously due to the lack of simultaneous comparison of lactating and nonlactating individuals. When possible, future studies of maternal investment should also include nonlactating individuals, since lactation may have a strong synergistic effect with other aspects shaping foraging behavior.

Signatures of Selection on Mitonuclear Integrated Genes Uncover Hidden Mitogenomic Variation in Fur Seals.

Nuclear copies of mitochondrial genes (numts) are commonplace in vertebrate genomes and have been characterized in many species. However, relatively little attention has been paid to understanding their evolutionary origins and to disentangling alternative sources of insertions. Numts containing genes with intact mitochondrial reading frames represent good candidates for this purpose. The sequences of the genes they contain can be compared with their mitochondrial homologs to characterize synonymous to nonsynonymous substitution rates, which can shed light on the selection pressures these genes have been subjected to. Here, we characterize 25 numts in the Antarctic fur seal (Arctocephalus gazella) genome. Among those containing genes with intact mitochondrial reading frames, three carry multiple substitutions in comparison to their mitochondrial homologs. Our analyses reveal that one represents a historic insertion subjected to strong purifying selection since it colonized the Otarioidea in a genomic region enriched in retrotransposons. By contrast, the other two numts appear to be more recent and their large number of substitutions can be attributed to noncanonical insertions, either the integration of heteroplasmic mtDNA or hybridization. Our study sheds new light on the evolutionary history of pinniped numts and uncovers the presence of hidden sources of mitonuclear variation.

Exploring fungal diversity in Antarctic wildlife: isolation and molecular identification of culturable fungi from penguins and pinnipeds

Aims: To survey the diversity of fungal species that may be cultured from Antarctic penguins and pinnipeds, and to test the in vitro susceptibility to triazole drugs of any medically important Aspergillus isolates. Methods: During an expedition to Argentinean Antarctic research stations at Potter Peninsula (South Shetland Islands) and Primavera Cape (Antarctic Peninsula) in February 2019, samples (n = 212) were collected from fur seals (Arctocephalus gazella), elephant seals (Mirounga leonine), leopard seals (Hydrurga leptonyx), Weddell seals (Leptonychotes weddellii) and crabeater seals (Lobodon carcinophaga) and gentoo penguins (Pygoscelis papua). Oral, nasal and rectal swabs and skin/hair brushings were collected from pinnipeds, and skin/feather brushings, cloacal swabs and moulted feathers from penguins. Samples were cultured on Sabouraud dextrose agar and/or potato dextrose agar plates and fungal isolates identified by morphological criteria followed by PCR amplification and DNA sequencing. Antifungal susceptibility of Aspergillus spp. isolates to triazoles was tested. Results: Fungi from 21 genera were isolated from 121/212 (57.1%) samples obtained from pinnipeds and penguins. Among pinnipeds from Potter Peninsula (fur seals and elephants seals), the most frequent fungal species were Debaryomyces hansenii and Rhodotorula mucilaginosa, isolated from the oral, nasal and/or rectal mucosa, and Antarctomyces psychrotrophicus isolated from the skin/hair of all sampled individuals. Among pinnipeds from Primavera Cape (leopard seals, Weddell seals and crabeater seals), the most frequent fungal species were Naganishia adeliensis and Cryptococcus neoformans var. uniguttulatus, isolated from the nasal/oral mucosa of 4/33 (15.2%) and 5/33 (12.1%) animals, respectively. The most frequently isolated fungal species from gentoo penguins (Potter Peninsula), were Pseudogymnoascus pannorum and A. pyschrotrophicus, which both were isolated from skin/feathers of 7/15 (46.7%) birds, and Thelebolus microsporus, isolated from the cloacal mucosa and skin/feathers of 5/15 (33.3%) and 2/15 (13.3%) birds, respectively. Fungi that are potentially pathogenic to both humans and animals, (Aspergillus fumigatus, Asp. flavus, Asp. versicolor, Candida parapsilosis and Microsporum canis) were isolated from 4/38 (10.5%), 1/38 (2.6%), 2/38 (5.3%), 4/38 (10.5%) and 2/38 (5.3%) sampled pinnipeds, respectively. Only non-azole-resistant isolates of Asp. fumigatus and Asp. flavus were identified. Conclusions: The fungal biodiversity in Antarctic pinnipeds and gentoo penguins was explored using standard mycological culture followed by PCR and DNA sequencing. The frequency of fungal carriage varied among animal species, sample type and location. This study constitutes an epidemiologic approach to monitoring of these marine animals for emerging fungal pathogens.

Detection of clinically relevant antimicrobial resistance determinants in warm-blooded marine animals in Livingston Island (South Shetland Islands, Antarctica): A field-based molecular genetics study

Molecular genetic studies of stools were performed to assess the spread of some clinically relevant antimicrobial resistance determinants (ARD) in a gentoo penguin (Pygoscelis papua) and an Antarctic fur seal (Arctocephalus gazella) on Livingston Island. Glycopeptide resistance genes (vanA/vanD and vanB) were detected in both fecal samples, while the penguin's one was also mecA-positive and blaNDM-positive. Because of the remoteness and the isolation of the sampling locations, the carriage of vancomycin-resistant Enterococcus spp., methicillin-resistant Staphylococcus aureus, and NDM-producing Enterobacterales or other gram-negative bacilli suggested an ocean pollution with antibiotic resistant bacteria (ARB). Additionally, due to the type of ARD we detected, our results are alarming, and they cannot be explained only with agricultural and/or aquacultural pollution. Even though the current study is a preliminary one, it also demonstrates the potential of the field genetics analyses carried out with minimal equipment as a reliable monitoring tool for pollution with ARB.

Placenta of an antarctic fur seal, arctocephalusgazella (Peters, 1875) after spontaneous abortion

Placenta of an antarctic fur seal, arctocephalusgazella (Peters, 1875) after spontaneous abortion

Should I stay or should I go? Behavioral adjustments of fur seals related to foraging success

Abstract Understanding foraging strategies and decision-making processes of predators provide crucial insights into how they might respond to changes in prey availability and in their environment to maximize their net energy input. In this work, foraging strategies of Antarctic fur seals (Arctocephalus gazella, AFS) and Northern fur seals (Callorhinus ursinus, NFS) were studied to determine how they adjust their foraging behavior according to their past prey capture experiences. AFS on Kerguelen Islands are exclusively oceanic divers, while NFS population of St Paul Island shows both oceanic and neritic divers. We thus hypothesized that the two species would respond differently to a change in prey capture success depending on their foraging strategy. To test this, 40 females were equipped with tags that measured tri-axial acceleration, dive depth, and GPS coordinates, from which we derived prey capture attempts and behavioral metrics. Influence of prey capture success on horizontal and vertical movements of seals was investigated at different time scales: multi-dive, night, and trip. Both AFS and NFS traveled further during the day if they encountered low prey capture periods during the previous night. However, at the multi-dive scale, neritic NFS differed from oceanic NFS and AFS in terms of decision-making processes, e.g., both AFS and oceanic NFS dived deeper in response to low prey capture rate periods, while neritic NFS did not. Similarities in decision-making processes between NFS and AFS foraging on pelagic prey suggest that pelagic vs. neritic prey type is a key factor in defining foraging decisions of diving marine predators.

Demographic Reconstruction of Antarctic Fur Seals Supports the Krill Surplus Hypothesis.

Much debate surrounds the importance of top-down and bottom-up effects in the Southern Ocean, where the harvesting of over two million whales in the mid twentieth century is thought to have produced a massive surplus of Antarctic krill. This excess of krill may have allowed populations of other predators, such as seals and penguins, to increase, a top-down hypothesis known as the ‘krill surplus hypothesis’. However, a lack of pre-whaling population baselines has made it challenging to investigate historical changes in the abundance of the major krill predators in relation to whaling. Therefore, we used reduced representation sequencing and a coalescent-based maximum composite likelihood approach to reconstruct the recent demographic history of the Antarctic fur seal, a pinniped that was hunted to the brink of extinction by 18th and 19th century sealers. In line with the known history of this species, we found support for a demographic model that included a substantial reduction in population size around the time period of sealing. Furthermore, maximum likelihood estimates from this model suggest that the recovered, post-sealing population at South Georgia may have been around two times larger than the pre-sealing population. Our findings lend support to the krill surplus hypothesis and illustrate the potential of genomic approaches to shed light on long-standing questions in population biology.

The Rapid Population Collapse of a Key Marine Predator in the Northern Antarctic Peninsula Endangers Genetic Diversity and Resilience to Climate Change

Antarctic fur seals (AFS) are an ecologically important predator and a focal indicator species for ecosystem-based Antarctic fisheries management. This species suffered intensive anthropogenic exploitation until the early 1900s, but recolonized most of its former distribution, including the southern-most colony at Cape Shirreff, South Shetland Islands (SSI). The IUCN describes a single, global AFS population of least concern; however, extensive genetic analyses clearly identify four distinct breeding stocks, including one in the SSI. To update the population status of SSI AFS, we analyzed 20 years of field-based data including population counts, body size and condition, natality, recruitment, foraging behaviors, return rates, and pup mortality at the largest SSI colony. Our findings show a precipitous decline in AFS abundance (86% decrease since 2007), likely driven by leopard seal predation (increasing since 2001, p << 0.001) and potentially worsening summer foraging conditions. We estimated that leopard seals consumed an average of 69.3% (range: 50.3–80.9%) of all AFS pups born each year since 2010. AFS foraging-trip durations, an index of their foraging habitat quality, were consistent with decreasing krill and fish availability. Significant improvement in the age-specific over-winter body condition of AFS indicates that observed population declines are driven by processes local to the northern Antarctic Peninsula. The loss of SSI AFS would substantially reduce the genetic diversity of the species, and decrease its resilience to climate change. There is an urgent need to reevaluate the conservation status of Antarctic fur seals, particularly for the rapidly declining SSI population.

Ecosystem shifts inferred from long-term stable isotope analysis of male Antarctic fur seal Arctocephalus gazella teeth

The Atlantic sector of the Southern Ocean has been rapidly changing over the last century. Many of those changes are driven by climate anomalies such as the El Niño-Southern Oscillation and the Southern Annular Mode, which affect biological processes that scale up the food web. We used δ13C and δ15N time series of dentine growth layer groups (as a proxy of individual foraging history from multiple years, n = 41 teeth) to assess temporal shifts in foraging habits of subadult/adult male Antarctic fur seals Arctocephalus gazella (AFSs) in 2 areas of high concentration of Antarctic krill Euphausia superba: the South Shetland Islands and the South Orkney Islands. Our analyses, which represent the first long-term isotopic assessment of male AFS sampled in Antarctic waters, revealed a significant decrease of δ13C (0.04‰ yr-1) from 1974 to 2015 and a decrease of δ15N after the late 1990s. The observed changes are likely driven by shifts in latitudinal and longitudinal distribution of krill and increased incorporation of 15N-enriched sources (higher trophic level prey and/or feeding in different areas) in the most recent period for reasons that are not yet clear. We were able to trace ecosystem changes through isotopic bio-archives of Antarctic fur seals, highlighting the role of this species as an ecosystem indicator of the trophic cascade effects caused by climate change in the Southern Ocean.

Environmental drivers of foraging behaviour during long-distance foraging trips of male Antarctic fur seals

Animals may use long-distance foraging trips to capitalize on spatiotemporal variation in food availability, allowing individuals to maximize resource gain from foraging effort. This is particularly important for dimorphic species with polygynous mating where males face strong selection pressures to attain large size and access to reproductive females. We tracked 17 male Antarctic fur seals, Arctocephalus gazella , during their prolonged postbreeding trips and assessed links between their movements and environmental predictors of profitable feeding areas. Males made one of two types of trips: a long trip to the Antarctic ice edge or shorter trips to areas where the southern Antarctic Circumpolar Current fronts generate high biological activity. The trip type was not determined by body size but was related to departure date from the breeding area, suggesting that males must trade off opportunities at the breeding area (reproductive, social interactions) and foraging opportunities between breeding seasons. Regardless of trip structure, males focused search effort far from foraging areas of central-place foraging seabirds and seals including female Antarctic fur seals provisioning offspring. Males showed clear spatiotemporal patterns in dive behaviour, with deep dives in shelf waters during the day and predominantly shallower dives in pelagic waters at night. Diel dive patterns showed monthly changes in photoperiod and lunar phase, consistent with feeding on vertically migrating prey. However, males did not use area-restricted search to focus dive effort, instead performing a mix of foraging and nonforaging behaviour within and between restricted search areas. We discuss the scale and type of inference that can be made from movement models, given the behavioural constraints that govern long-distance trips in vast, heterogeneous environments like the Southern Ocean. • Males made two types of long-distance trip, related to departure date not body size. • Foraging and nonforaging behaviour occurred throughout these trips. • Males foraged mostly away from breeding seals, in areas of high biological activity. • Diel dive behaviour aligned with changes in solar and lunar light.

Winter distribution of juvenile and sub-adult male Antarctic fur seals (Arctocephalus gazella) along the western Antarctic Peninsula

Detailed knowledge of habitat use by marine megafauna is critical to understand their ecological roles and for the adequate management of marine resources. Antarctic fur seals (Arctocephalus gazella) inhabiting the Atlantic sector of the Southern Ocean prey largely on Antarctic krill (Euphausia superba) and play a central role in managing the krill fishery. Here, we assessed the demographic structure of three post-mating, early moult male haul-outs in the South Shetland Islands in early March and calculated the relative contribution of juveniles (1–4 years old) and sub-adult males (5–6 years) to the population remaining in maritime Antarctica after the breeding season. We also satellite tagged 11 juvenile males and four sub-adult males to analyze their movements and develop a species distribution model including both age classes. Our results highlighted the dominance of young individuals in the male population, revealed that they do not behave as central place foragers and identified key environmental drivers that affected their distribution at-sea throughout winter. Predicted potential foraging habitat overlapped highly with the known distribution of Antarctic krill, and identified the waters off the western Antarctic Peninsula and the Scotia Sea as the core of the distribution area of juvenile and sub-adult male Antarctic fur seals in winter. This pattern is similar to that of adult males but totally different from that of adult females, as the latter overwinter in areas at latitude 45–55° S. This segregation has implications for the ecology and management of the krill fishery.

Mercury and stable carbon and nitrogen isotopes in the natal Fur of two Antarctic pinniped species

Southern elephant seal (SES) and Antarctic fur seal (AFS) are short Southern Ocean food web top predators and are spatial and temporal trend bioindicators of Antarctic Hg bioavailability. Hg, stable isotope composition (δ13C and δ15N) and trophic position (TP) regarding sex were determined using lanugo samples from Antarctic pinnipeds pups (SES n = 35 and AFS n = 11). Hg concentrations in over 50% of the SES pups (mean 5.9 ± 3.1 mg kg−1 dry wt.) are compatible with those found to cause neurologic damage to polar bears in the Arctic. No significant differences regarding sexes for SES or AFS are found based on mean Hg concentrations normalized by body weight. δ15N values and TPs are similar among both species, indicating that gestating SES and AFS mothers feed at the same trophic level. Significantly different δ13C values were found, indicating distinct feeding grounds for mothers belonging to both species when pup lanugo is formed in utero; while SES females like to feed in Antarctic waters, AFS females remain in sub-Antarctic waters. The differences in Hg and δ13C observed for both species reflect not only contrasting feeding habits and anthropogenic Hg inputs, but also maternal foraging strategies.

50,000 years of ice and seals: Impacts of the Last Glacial Maximum on Antarctic fur seals.

Ice is one of the most important drivers of population dynamics in polar organisms, influencing the locations, sizes, and connectivity of populations. Antarctic fur seals, Arctocephalus gazella, are particularly interesting in this regard, as they are concomitantly reliant on both ice‐associated prey and ice‐free coastal breeding areas. We reconstructed the history of this species through the Last Glacial Maximum (LGM) using genomic sequence data from seals across their range. Population size trends and divergence events were investigated using continuous‐time size estimation analysis and divergence time estimation models. The combined results indicated that a panmictic population present prior to the LGM split into two small refugial populations during peak ice extent. Following ice decline, the western refugial population founded colonies at the South Shetlands, South Georgia, and Bouvetøya, while the eastern refugial population founded the colony on Iles Kerguelen. Postglacial population divergence times closely match geological estimates of when these coastal breeding areas became ice free. Given the predictions regarding continued future warming in polar oceans, these responses of Antarctic fur seals to past climate variation suggest it may be worthwhile giving conservation consideration to potential future breeding locations, such as areas further south along the Antarctic Peninsula, in addition to present colony areas.