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.

Sea ice concentration decline in an important Adélie penguin molt area.

Unlike in many polar regions, the spatial extent and duration of the sea ice season have increased in the Ross Sea sector of the Southern Ocean during the satellite era. Simultaneously, populations of Adélie penguins, a sea ice obligate, have been stable or increasing in the region. Relationships between Adélie penguin population growth and sea ice concentration (SIC) are complex, with sea ice driving different, sometimes contrasting, demographic patterns. Adélie penguins undergo a complete molt annually, replacing all their feathers while fasting shortly after the breeding season. Unlike most penguin species, a majority of Adélies are thought to molt on sea ice, away from the breeding colonies, which makes this period particularly difficult to study. Here, we evaluate the hypothesis that persistent areas of high SIC provide an important molting habitat for Adélie penguins. We analyzed data from geolocating dive recorders deployed year-round on 195 adult penguins at two colonies in the Ross Sea from 2017 to 2019. We identified molt by detecting extended gaps in postbreeding diving activity and used associated locations to define two key molting areas. Remotely sensed data indicated that SIC during molt was anomalously low during the study and has declined in the primary molt area since 1980. Further, annual return rates of penguins to breeding colonies were positively correlated with SIC in the molt areas over 20 y. Together these results suggest that sea ice conditions during Adélie penguin molt may represent a previously underappreciated annual bottleneck for adult survival.

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.

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.

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.

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.

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.

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.