Advances in remote sensing of emperor penguins: first multi-year time series documenting trends in the global population.

Like many polar animals, emperor penguin populations are challenging to monitor because of the species' life history and remoteness. Consequently, it has been difficult to establish its global status, a subject important to resolve as polar environments change. To advance our understanding of emperor penguins, we combined remote sensing, validation surveys and using Bayesian modelling, we estimated a comprehensive population trajectory over a recent 10-year period, encompassing the entirety of the species' range. Reported as indices of abundance, our study indicates with 81% probability that there were fewer adult emperor penguins in 2018 than in 2009, with a posterior median decrease of 9.6% (95% credible interval (CI) -26.4% to +9.4%). The global population trend was -1.3% per year over this period (95% CI = -3.3% to +1.0%) and declines probably occurred in four of eight fast ice regions, irrespective of habitat conditions. Thus far, explanations have yet to be identified regarding trends, especially as we observed an apparent population uptick toward the end of time series. Our work potentially establishes a framework for monitoring other Antarctic coastal species detectable by satellite, while promoting a need for research to better understand factors driving biotic changes in the Southern Ocean ecosystem.

Sex-specific recruitment rates contribute to male-biased sex ratio in Adélie penguins.

Sex-related differences in vital rates that drive population change reflect the basic life history of a species. However, for visually monomorphic bird species, determining the effect of sex on demographics can be a challenge. In this study, we investigated the effect of sex on apparent survival, recruitment, and breeding propensity in the Adélie penguin (Pygoscelis adeliae), a monochromatic, slightly size dimorphic species with known age, known sex, and known breeding history data collected during 1996-2019 (n = 2127 birds) from three breeding colonies on Ross Island, Antarctica. Using a multistate capture-mark-recapture maximum-likelihood model, we estimated apparent survival (S^), recapture (resighting) probability (p^), and the probability of transitioning among breeding states and moving between colonies (ψ^; colony-specific non-juvenile pre-breeders, breeders, and non-breeders). Survival rate varied by breeding status and colony, but not sex, and pre-breeders had higher survival rates than breeders and non-breeders. Females had a higher probability of recruiting into the breeding population each year and may enter the breeding pool at younger ages. In contrast, both sexes had the same probability of breeding from year to year once they had recruited. Although we detected no direct sex effects on survival, the variation in recruitment probability and age-at-first reproduction, along with lower survival rates of breeders compared to pre-breeders, likely leads to shorter lifespans for females. This is supported by our findings of a male-biased mean adult sex ratio (ASR) of 1.4 males for every female (x^ proportion of males = 0.57, SD = 0.07) across all colonies and years in this metapopulation. Our study illustrates how important it can be to disentangle sex-related variation in population vital rates, particularly for species with complex life histories and demographic dynamics.

Going with the floe: Sea-ice movement affects distance and destination during Adélie penguin winter movements.

Seasonal migration, driven by shifts in annual climate cycles and resources, is a key part of the life history and ecology of species across taxonomic groups. By influencing the amount of energy needed to move, external forces such as wind and ocean currents are often key drivers of migratory pathways exposing individuals to varying resources, environmental conditions, and competition pressures impacting individual fitness and population dynamics. Although wildlife movements in connection with wind and ocean currents are relatively well understood, movements within sea-ice fields have been much less studied, despite sea ice being an integral part of polar ecology. Adélie penguins (Pygoscelis adeliae) in the southern Ross Sea, Antarctica, currently exist at the southernmost edge of their range and undergo the longest (~12,000 km) winter migration known for the species. Within and north of the Ross Sea, the Ross Gyre drives ocean circulation and the large-scale movement of sea ice. We used remotely sensed sea-ice movement data together with geolocation-based penguin movement data to test the hypothesis that penguins use gyre-driven sea-ice movement to aid their migration. We found that penguins traveled greater distances when their movement vectors were aligned with those of sea ice (i.e., ice support) and the amount of ice support received depended on which route a penguin took. We also found that birds that took an eastern route traveled significantly further north in two of the 3 years we examined, coinciding with higher velocities of sea ice in those years. We compare our findings to patterns observed in migrating species that utilize air or water currents for their travel and with other studies showing the importance of ocean/sea-ice circulation patterns to wildlife movement and life history patterns within the Ross Sea. Changes in sea ice may have consequences not only for energy expenditure but, by altering migration and movement pathways, to the ecological interactions that exist in this region.

Genomes of Single-Stranded DNA Viruses in a Fecal Sample from South Polar Skua (Stercorarius maccormicki) on Ross Island, Antarctica.

South polar skuas migrate from subtropical regions to breed along coastal Antarctica. In a fecal sample collected on Ross Island, Antarctica, we identified 20 diverse microviruses (Microviridae) that share low levels of similarity to currently known microviruses; 6 appear to use a Mycoplasma/Spiroplasma codon translation table.

High-resolution recording of foraging behaviour over multiple annual cycles shows decline in old Adélie penguins' performance.

Age-related variation in foraging performance can result from both within-individual change and selection processes. These mechanisms can only be disentangled by using logistically challenging long-term, longitudinal studies. Coupling a long-term demographic data set with high-temporal-resolution tracking of 18 Adélie penguins (Pygoscelis adeliae, age 4-15 yrs old) over three consecutive annual cycles, we examined how foraging behaviour changed within individuals of different age classes. Evidence indicated within-individual improvement in young and middle-age classes, but a significant decrease in foraging dive frequency within old individuals, associated with a decrease in the dive descent rate. Decreases in foraging performance occurred at a later age (from 12-15 yrs old to 15-18 yrs old) than the onset of senescence predicted for this species (9-11 yrs old). Foraging dive frequency was most affected by the interaction between breeding status and annual life-cycle periods, with frequency being highest during returning migration and breeding season and was highest overall for successful breeders during the chick-rearing period. Females performed more foraging dives per hour than males. This longitudinal, full annual cycle study allowed us to shed light on the changes in foraging performance occurring among individuals of different age classes and highlighted the complex interactions among drivers of individual foraging behaviour.

Seasonal habitat preference and foraging behaviour of post-moult Weddell seals in the western Ross Sea.

Weddell seals (Leptonychotes weddellii) are important predators in the Southern Ocean and are among the best-studied pinnipeds on Earth, yet much still needs to be learned about their year-round movements and foraging behaviour. Using biologgers, we tagged 62 post-moult Weddell seals in McMurdo Sound and vicinity between 2010 and 2012. Generalized additive mixed models were used to (i) explain and predict the probability of seal presence and foraging behaviour from eight environmental variables, and (ii) examine foraging behaviour in relation to dive metrics. Foraging probability was highest in winter and lowest in summer, and foraging occurred mostly in the water column or just above the bottom; across all seasons, seals preferentially exploited the shallow banks and deeper troughs of the Ross Sea, the latter providing a pathway for Circumpolar Deep Water to flow onto the shelf. In addition, the probability of Weddell seal occurrence and foraging increased with increasing bathymetric slope and where water depth was typically less than 600 m. Although the probability of occurrence was higher closer to the shelf break, foraging was higher in areas closer to shore and over banks. This study highlights the importance of overwinter foraging for recouping body mass lost during the previous summer.

Protect global values of the Southern Ocean ecosystem.

Climate change and fishing present dual threats.

Foraging dive frequency predicts body mass gain in the Adélie penguin.

Quantifying food intake in wild animals is crucial to many ecological and evolutionary questions, yet it can be very challenging, especially in the marine environment. Because foraging behavior can be inferred from dive recordings in many marine creatures, we hypothesized that specific behavioral dive variables can indicate food intake. To test this hypothesis, we attached time-depth recorders to breeding Adélie penguins also implanted with RFID tags that crossed a weighbridge as they traveled to and from the ocean to feed their chicks. The weighbridge reported how much mass the penguin had gained during a foraging trip. The variables that explained a significant amount of the change in body mass while at sea were the number of foraging dives per hour (46%) and the number of undulations per hour (12%). Most importantly, every increment of 1 in the rate of foraging dives per hour equated to a penguin gaining an average 170 g of mass, over the course of a 6-60 h foraging trip. These results add to a growing understanding that different metrics of foraging success are likely appropriate for different species, and that assessing the types and frequencies of dives using time-depth recorders can yield valuable insights.

Circoviruses and cycloviruses identified in Weddell seal fecal samples from McMurdo Sound, Antarctica.

Circoviridae is a family of circular single-stranded DNA viruses whose members infect a wide variety of hosts. While well characterized in avian and mammalian hosts, little is known about circoviruses associated with Antarctic animals. From 48 Weddell seal (Leptonychotes weddellii) fecal samples collected on the sea ice in McMurdo between Nov 2014 and Dec 2014, we identified and determined the genomes of novel viruses that fall within two genera of the family Circoviridae, i.e. Circovirus (n = 7) and Cyclovirus (n = 45). We named these viruses as werosea circovirus (WerCV) and werosea cyclovirus (WerCyV). The genomes of WerCV and WerCyV share ~63-64% genome-wide pairwise identity with classified circoviruses and cycloviruses, respectively. Based on the species demarcation threshold of 80% for members of the Circoviridae, the genomes of WerCV and WerCyV represent new species in their respective genera. Evidence indicated recombination in five of the 45 WerCyV genomes identified in this study. These are the first circoviruses found associated with Antarctic pinnipeds, adding to those recently identified associated with Adélie (Pygoscelis adeliae) and chinstrap penguins (P. antarcticus).

Insights from the first global population estimate of Weddell seals in Antarctica.

The Weddell seal is one of the best-studied marine mammals in the world, owing to a multidecadal demographic effort in the southernmost part of its range. Despite their occurrence around the Antarctic coastline, we know little about larger scale patterns in distribution, population size, or structure. We combined high-resolution satellite imagery from 2011, crowd-sourcing, and habitat modeling to report the first global population estimate for the species and environmental factors that influence its distribution. We estimated ~202,000 (95% confidence interval: 85,345 to 523,140) sub-adult and adult female seals, with proximate ocean depth and fast-ice variables as factors explaining spatial prevalence. Distances to penguin colonies were associated with seal presence, but only emperor penguin population size had a strong negative relationship. The small, estimated population size relative to previous estimates and the seals' nexus with trophic competitors indicates that a community ecology approach is required in efforts to monitor the Southern Ocean ecosystem.

The influence of subcolony-scale nesting habitat on the reproductive success of Adélie penguins.

Group-size variation is common in colonially breeding species, including seabirds, whose breeding colonies can vary in size by several orders of magnitude. Seabirds are some of the most threatened marine taxa and understanding the drivers of colony size variation is more important than ever. Reproductive success is an important demographic parameter that can impact colony size, and it varies in association with a number of factors, including nesting habitat quality. Within colonies, seabirds often aggregate into distinct groups or subcolonies that may vary in quality. We used data from two colonies of Adélie penguins 73 km apart on Ross Island, Antarctica, one large and one small to investigate (1) How subcolony habitat characteristics influence reproductive success and (2) How these relationships differ at a small (Cape Royds) and large (Cape Crozier) colony with different terrain characteristics. Subcolonies were characterized using terrain attributes (elevation, slope aspect, slope steepness, wind shelter, flow accumulation), as well group characteristics (area/size, perimeter-to-area ratio, and proximity to nest predators). Reproductive success was higher and less variable at the larger colony while subcolony characteristics explained more of the variance in reproductive success at the small colony. The most important variable influencing subcolony quality at both colonies was perimeter-to-area ratio, likely reflecting the importance of nest predation by south polar skuas along subcolony edges. The small colony contained a higher proportion of edge nests thus higher potential impact from skua nest predation. Stochastic environmental events may facilitate smaller colonies becoming "trapped" by nest predation: a rapid decline in the number of breeding individuals may increase the proportion of edge nests, leading to higher relative nest predation and hindering population recovery. Several terrain covariates were retained in the final models but which variables, the shapes of the relationships, and importance varied between colonies.

Age-related reproductive performance of the Adélie penguin, a long-lived seabird exhibiting similar outcomes regardless of individual life-history strategy.

Age-related variation in reproductive performance in long-lived iteroparous vertebrate species is common, with performance being influenced by within-individual processes, such as improvement and senescence, in combination with among-individual processes, such as selective appearance and disappearance. Few studies of age-related reproductive performance have compared the role of these drivers within a metapopulation, subject to varying degrees of resource competition. We accounted for within- and among-individual changes among known-aged Adélie penguins Pygoscelis adeliae during 17 years (1997-2013), at three clustered colonies of disparate size, to understand patterns in age-related reproductive success during early and late adulthood. Age at first reproduction (AFR) was lowest, and number of breeding attempts highest, at the largest colony. Regardless of AFR, success improved with early post-recruitment experience. For both oldest and youngest recruitment groups, peak performance occurred at the end of their reproductive life span indicating a possible cost of reproduction. Intermediate recruitment groups reached peak performance in their mid-reproductive life span and with intermediate breeding experience, before decreasing. Breeding success was lowest for the initial breeding attempt regardless of AFR, but we observed subsequent variation relative to recruitment age. Gaining experience by delaying recruitment positively influenced reproductive performance early in the reproductive life span and was most evident for the youngest breeders. Oldest recruits had the highest initial and peak breeding success. Differences in AFR resulted in trade-offs in reproductive life span or timing of senescence but not in the overall number of breeding attempts. Patterns differed as a function of colony size, and thus competition for resources. Early life improvement in performance at the larger colonies was primarily due to within-individual factors and at the largest colony, AFR. Regardless of colony size late-life performance was positively related to the age at last reproduction, indicating selective disappearance of lower performing individuals. These results highlight that different life-history strategies were equally successful, indicating that individuals can overcome potential trade-offs associated with early- and late-life performance. These results have important implications for understanding the evolution of life-history strategies responsible for driving population change.

Unveiling Crucivirus Diversity by Mining Metagenomic Data.

The discovery of cruciviruses revealed the most explicit example of a common protein homologue between DNA and RNA viruses to date. Cruciviruses are a novel group of circular Rep-encoding single-stranded DNA (ssDNA) (CRESS-DNA) viruses that encode capsid proteins that are most closely related to those encoded by RNA viruses in the family Tombusviridae The apparent chimeric nature of the two core proteins encoded by crucivirus genomes suggests horizontal gene transfer of capsid genes between DNA and RNA viruses. Here, we identified and characterized 451 new crucivirus genomes and 10 capsid-encoding circular genetic elements through de novo assembly and mining of metagenomic data. These genomes are highly diverse, as demonstrated by sequence comparisons and phylogenetic analysis of subsets of the protein sequences they encode. Most of the variation is reflected in the replication-associated protein (Rep) sequences, and much of the sequence diversity appears to be due to recombination. Our results suggest that recombination tends to occur more frequently among groups of cruciviruses with relatively similar capsid proteins and that the exchange of Rep protein domains between cruciviruses is rarer than intergenic recombination. Additionally, we suggest members of the stramenopiles/alveolates/Rhizaria supergroup as possible crucivirus hosts. Altogether, we provide a comprehensive and descriptive characterization of cruciviruses.IMPORTANCE Viruses are the most abundant biological entities on Earth. In addition to their impact on animal and plant health, viruses have important roles in ecosystem dynamics as well as in the evolution of the biosphere. Circular Rep-encoding single-stranded (CRESS) DNA viruses are ubiquitous in nature, many are agriculturally important, and they appear to have multiple origins from prokaryotic plasmids. A subset of CRESS-DNA viruses, the cruciviruses, have homologues of capsid proteins encoded by RNA viruses. The genetic structure of cruciviruses attests to the transfer of capsid genes between disparate groups of viruses. However, the evolutionary history of cruciviruses is still unclear. By collecting and analyzing cruciviral sequence data, we provide a deeper insight into the evolutionary intricacies of cruciviruses. Our results reveal an unexpected diversity of this virus group, with frequent recombination as an important determinant of variability.

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

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

The 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.

Identification of a Novel Adélie Penguin Circovirus at Cape Crozier (Ross Island, Antarctica).

Understanding the causes of disease in Antarctic wildlife is crucial, as many of these species are already threatened by environmental changes brought about by climate change. In recent years, Antarctic penguins have been showing signs of an unknown pathology: a feather disorder characterised by missing feathers, resulting in exposed skin. During the 2018-2019 austral summer breeding season at Cape Crozier colony on Ross Island, Antarctica, we observed for the first time an Adélie penguin chick missing down over most of its body. A guano sample was collected from the nest of the featherless chick, and using high-throughput sequencing, we identified a novel circovirus. Using abutting primers, we amplified the full genome, which we cloned and Sanger-sequenced to determine the complete genome of the circovirus. The Adélie penguin guano-associated circovirus genome shares <67% genome-wide nucleotide identity with other circoviruses, representing a new species of circovirus; therefore, we named it penguin circovirus (PenCV). Using the same primer pair, we screened 25 previously collected cloacal swabs taken at Cape Crozier from known-age adult Adélie penguins during the 2014-2015 season, displaying no clinical signs of feather-loss disorder. Three of the 25 samples (12%) were positive for a PenCV, whose genome shared >99% pairwise identity with the one identified in 2018-2019. This is the first report of a circovirus associated with a penguin species. This circovirus could be an etiological agent of the feather-loss disorder in Antarctic penguins.

Evidence of age-related improvement in the foraging efficiency of Adélie penguins.

Age variation in reproductive performance is well-documented but the mechanisms underlying this variation remain unclear. Foraging efficiency is likely to be a key source of demographic variation as it determines the amount of energy that can be invested in fitness-related activities. Evidence of age-related changes in the foraging efficiency of adult seabirds is scarce and inconsistent. We investigated the effects of age on the foraging efficiency of breeding Adélie penguins, a relatively short-lived seabird species, in order to gain a broader perspective on the processes driving variation in ageing rates. We found support for a positive effect of age, either linear or levelling off at old ages, on both our proxies for daily catch rate and catch per unit effort. Across all age classes, males were more performant foragers than females. We found no strong evidence for differing ageing patterns between sexes or individual quality levels, and no evidence for senescence. We infer that continuous individual improvement could be responsible for a larger amount of the variation in foraging efficiency with age at our study site, compared with selective disappearance of underperforming phenotypes. The different results reported by other studies highlight the need to conduct longitudinal studies across a range of species in different environments.

Viruses associated with Antarctic wildlife: From serology based detection to identification of genomes using high throughput sequencing.

The Antarctic, sub-Antarctic islands and surrounding sea-ice provide a unique environment for the existence of organisms. Nonetheless, birds and seals of a variety of species inhabit them, particularly during their breeding seasons. Early research on Antarctic wildlife health, using serology-based assays, showed exposure to viruses in the families Birnaviridae, Flaviviridae, Herpesviridae, Orthomyxoviridae and Paramyxoviridae circulating in seals (Phocidae), penguins (Spheniscidae), petrels (Procellariidae) and skuas (Stercorariidae). It is only during the last decade or so that polymerase chain reaction-based assays have been used to characterize viruses associated with Antarctic animals. Furthermore, it is only during the last five years that full/whole genomes of viruses (adenoviruses, anelloviruses, orthomyxoviruses, a papillomavirus, paramyoviruses, polyomaviruses and a togavirus) have been sequenced using Sanger sequencing or high throughput sequencing (HTS) approaches. This review summaries the knowledge of animal Antarctic virology and discusses potential future directions with the advent of HTS in virus discovery and ecology.

Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins.

The family Papillomaviridae contains more than 320 papillomavirus types, with most having been identified as infecting skin and mucosal epithelium in mammalian hosts. To date, only nine non-mammalian papillomaviruses have been described from birds (n = 5), a fish (n = 1), a snake (n = 1), and turtles (n = 2). The identification of papillomaviruses in sauropsids and a sparid fish suggests that early ancestors of papillomaviruses were already infecting the earliest Euteleostomi. The Euteleostomi clade includes more than 90 per cent of the living vertebrate species, and progeny virus could have been passed on to all members of this clade, inhabiting virtually every habitat on the planet. As part of this study, we isolated a novel papillomavirus from a 16-year-old female Adélie penguin (Pygoscelis adeliae) from Cape Crozier, Ross Island (Antarctica). The new papillomavirus shares ∼64 per cent genome-wide identity to a previously described Adélie penguin papillomavirus. Phylogenetic analyses show that the non-mammalian viruses (expect the python, Morelia spilota, associated papillomavirus) cluster near the base of the papillomavirus evolutionary tree. A papillomavirus isolated from an avian host (Northern fulmar; Fulmarus glacialis), like the two turtle papillomaviruses, lacks a putative E9 protein that is found in all other avian papillomaviruses. Furthermore, the Northern fulmar papillomavirus has an E7 more similar to the mammalian viruses than the other avian papillomaviruses. Typical E6 proteins of mammalian papillomaviruses have two Zinc finger motifs, whereas the sauropsid papillomaviruses only have one such motif. Furthermore, this motif is absent in the fish papillomavirus. Thus, it is highly likely that the most recent common ancestor of the mammalian and sauropsid papillomaviruses had a single motif E6. It appears that a motif duplication resulted in mammalian papillomaviruses having a double Zinc finger motif in E6. We estimated the divergence time between Northern fulmar-associated papillomavirus and the other Sauropsid papillomaviruses be to around 250 million years ago, during the Paleozoic-Mesozoic transition and our analysis dates the root of the papillomavirus tree between 400 and 600 million years ago. Our analysis shows evidence for niche adaptation and that these non-mammalian viruses have highly divergent E6 and E7 proteins, providing insights into the evolution of the early viral (onco-)proteins.