Circumpolar assessment of mercury contamination: the Adélie penguin as a bioindicator of Antarctic marine ecosystems.

Due to its persistence and potential ecological and health impacts, mercury (Hg) is a global pollutant of major concern that may reach high concentrations even in remote polar oceans. In contrast to the Arctic Ocean, studies documenting Hg contamination in the Southern Ocean are spatially restricted and large-scale monitoring is needed. Here, we present the first circumpolar assessment of Hg contamination in Antarctic marine ecosystems. Specifically, the Adélie penguin (Pygoscelis adeliae) was used as a bioindicator species, to examine regional variation across 24 colonies distributed across the entire Antarctic continent. Mercury was measured on body feathers collected from both adults (n = 485) and chicks (n = 48) between 2005 and 2021. Because penguins' diet represents the dominant source of Hg, feather δ13C and δ15N values were measured as proxies of feeding habitat and trophic position. As expected, chicks had lower Hg concentrations (mean ± SD: 0.22 ± 0.08 µg·g‒1) than adults (0.49 ± 0.23 µg·g‒1), likely because of their shorter bioaccumulation period. In adults, spatial variation in feather Hg concentrations was driven by both trophic ecology and colony location. The highest Hg concentrations were observed in the Ross Sea, possibly because of a higher consumption of fish in the diet compared to other sites (krill-dominated diet). Such large-scale assessments are critical to assess the effectiveness of the Minamata Convention on Mercury. Owing to their circumpolar distribution and their ecological role in Antarctic marine ecosystems, Adélie penguins could be valuable bioindicators for tracking spatial and temporal trends of Hg across Antarctic waters in the future.

Investigating two consecutive catastrophic breeding seasons in a large king penguin colony.

Large-scale breeding failures, such as offspring die-offs, can disproportionately impact wildlife populations that are characterized by a few large colonies. However, breeding monitoring-and thus investigations of such die-offs-is especially challenging in species with long reproductive cycles. We investigate two unresolved dramatic breeding failures that occurred in consecutive years (2009 and 2010) in a large king penguin Aptenodytes patagonicus colony, a long-lived species with a breeding cycle lasting over a year. Here we found that a single period, winter 2009, was likely responsible for the occurrence of breeding anomalies during both breeding seasons, suggesting that adults experienced poor foraging conditions at sea at that time. Following that unfavorable winter, the 2009 breeding cohort-who were entering the late stage of chick-rearing-immediately experienced high chick mortality. Meanwhile, the 2010 breeding cohort greatly delayed their arrival and egg laying, which would have otherwise started not long after the winter. The 2010 breeding season continued to display anomalies during the incubation and chick-rearing period, such as high abandonment rate, long foraging trips and eventually the death of all chicks in winter 2010. These anomalies could have resulted from either a domino-effect caused by the delayed laying, the continuation of poor foraging conditions, or both. This study provides an example of a large-scale catastrophic breeding failure and highlights the importance of the winter period on phenology and reproduction success for wildlife that breed in few large colonies.

Foraging conditions for breeding penguins improve with distance from colony and progression of the breeding season at the South Orkney Islands.

BACKGROUND: According to central place foraging theory, animals will only increase the distance of their foraging trips if more distant prey patches offer better foraging opportunities. Thus, theory predicts that breeding seabirds in large colonies could create a zone of food depletion around the colony, known as "Ashmole's halo". However, seabirds' decisions to forage at a particular distance are likely also complicated by their breeding stage. After chicks hatch, parents must return frequently to feed their offspring, so may be less likely to visit distant foraging patches, even if their quality is higher. However, the interaction between prey availability, intra-specific competition, and breeding stage on the foraging decisions of seabirds is not well understood. The aim of this study was to address this question in chinstrap penguins Pygoscelis antarcticus breeding at a large colony. In particular, we aimed to investigate how breeding stage affects foraging strategy; whether birds foraging far from the colony visit higher quality patches than available locally; and whether there is evidence for intraspecific competition, indicated by prey depletions near the colony increasing over time, and longer foraging trips. METHODS: We used GPS and temperature-depth recorders to track the foraging movements of 221 chinstrap penguins from 4 sites at the South Orkney Islands during incubation and brood. We identified foraging dives and calculated the index of patch quality based on time allocation during the dive to assess the quality of the foraging patch. RESULTS: We found that chinstrap penguin foraging distance varied between stages, and that trips became shorter as incubation progressed. Although patch quality was lower near the colony than at more distant foraging patches, patch quality near the colony improved over the breeding season. CONCLUSIONS: These results suggest chinstrap penguin foraging strategies are influenced by both breeding stage and prey distribution, and the low patch quality near the colony may be due to a combination of depletion by intraspecific competition but compensated by natural variation in prey. Reduced trip durations towards the end of the incubation period may be due to an increase in food availability, as seabirds time their reproduction so that the period of maximum energy demand in late chick-rearing coincides with maximum resource availability in the environment. This may also explain why patch quality around the colony improved over the breeding season. Overall, our study sheds light on drivers of foraging decisions in colonial seabirds, an important question in foraging ecology.

Trade-off between aerobic performance and egg production in migratory macaroni penguins.

When successive stages of an organism's life-history overlap, conflicts and trade-offs can emerge due to competition among physiological pathways. For example, long periods of sustained locomotion in migrating birds are supported by the androgenic up-regulation of aerobic factors, such as new red blood cell production and hematocrit. However, towards the end of migration, many female birds begin up-regulating 17ß-estradiol (E2) to support vitellogenesis and egg production, but E2 secretion is known to have suppressive effects on red blood cell production (anti-erythropoiesis). We explored potential trade-offs between factors related to aerobic performance (hematocrit, reticulocyte index) and the expression of factors related to E2-mediated vitellogenesis (i.e. yolk precursor production) in female macaroni penguins (Eudyptes chrysolophus), a species in which the physiologies controlling egg production and migratory activity run simultaneously (e.g. females experience a migratory conflict). We collected blood samples from penguins immediately upon their return to the colony, prior to egg laying. Hematocrit was elevated when the penguins returned to the colony (50.05% ± 3.40 SD), which is similar to pre-laying values observed in other migratory bird species. Furthermore, mean reticulocyte levels were elevated (34.87% ± 2.34), which is the highest level yet recorded in birds. Similarly, both plasma vitellogenin and yolk-targeted very low density lipoprotein levels were upregulated (2.30 ± 0.06 µg Zn ml-1, and 9.70 ± 0.19 mmol l-1, respectively), indicating that penguins were reproductively active and producing eggs during migration and upon arrival on land. As predicted, a negative relationship between hematocrit and plasma vitellogenin was found, but we found no evidence to suggest that birds were experiencing reproductive anemia. Alternatively, we attribute the negative relationship to a hemodilution effect of yolk precursor secretion into circulation. It appears that female macaroni penguins are able to preserve hematocrit levels and new red blood cell production when migratory activity overlaps with reproductive processes.

Evidence of Pathogen-Induced Immunogenetic Selection across the Large Geographic Range of a Wild Seabird.

Over evolutionary time, pathogen challenge shapes the immune phenotype of the host to better respond to an incipient threat. The extent and direction of this selection pressure depend on the local pathogen composition, which is in turn determined by biotic and abiotic features of the environment. However, little is known about adaptation to local pathogen threats in wild animals. The Gentoo penguin (Pygoscelis papua) is a species complex that lends itself to the study of immune adaptation because of its circumpolar distribution over a large latitudinal range, with little or no admixture between different clades. In this study, we examine the diversity in a key family of innate immune genes-the Toll-like receptors (TLRs)-across the range of the Gentoo penguin. The three TLRs that we investigated present varying levels of diversity, with TLR4 and TLR5 greatly exceeding the diversity of TLR7. We present evidence of positive selection in TLR4 and TLR5, which points to pathogen-driven adaptation to the local pathogen milieu. Finally, we demonstrate that two positively selected cosegregating sites in TLR5 are sufficient to alter the responsiveness of the receptor to its bacterial ligand, flagellin. Taken together, these results suggest that Gentoo penguins have experienced distinct pathogen-driven selection pressures in different environments, which may be important given the role of the Gentoo penguin as a sentinel species in some of the world's most rapidly changing environments.

Author Correction: Important At-Sea Areas of Colonial Breeding Marine Predators on the Southern Patagonian Shelf.

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

Microplastics in gentoo penguins from the Antarctic region.

There is growing evidence that microplastic pollution (<5 mm in size) is now present in virtually all marine ecosystems, even in remote areas, such as the Arctic and the Antarctic. Microplastics have been found in water and sediments of the Antarctic but little is known of their ingestion by higher predators and mechanisms of their entry into Antarctic marine food webs. The goal of this study was to assess the occurrence of microplastics in a top predator, the gentoo penguin Pygoscelis papua from the Antarctic region (Bird Island, South Georgia and Signy Island, South Orkney Islands) and hence assess the potential for microplastic transfer through Antarctic marine food webs. To achieve this, the presence of microplastics in scats (as a proof of ingestion) was investigated to assess the viability of a non-invasive approach for microplastic analyses in Antarctic penguins. A total of 80 penguin scats were collected and any microplastics they contained were extracted. A total of 20% of penguin scats from both islands contained microplastics, consisting mainly of fibers and fragments with different sizes and polymer composition (mean abundance of microplastics: 0.23 ± 0.53 items individual-1 scat, comprising seven different polymers), which were lower values than those found for seabirds in other regions worldwide. No significant differences in microplastic numbers in penguin scats between the two regions were detected. These data highlight the need for further assessment of the levels of microplastics in this sensitive region of the planet, specifically studies on temporal trends and potential effects on penguins and other organisms in the Antarctic marine food web.

More than the eye can see: Genomic insights into the drivers of genetic differentiation in Royal/Macaroni penguins across the Southern Ocean.

The study of systematics in wide-ranging seabirds can be challenging due to the vast geographic scales involved, as well as the possible discordance between molecular, morphological and behavioral data. In the Southern Ocean, macaroni penguins (Eudyptes chrysolophus) are distributed over a circumpolar range including populations in Antarctic and sub-Antarctic areas. Macquarie Island, in its relative isolation, is home to a closely related endemic taxon - the royal penguin (Eudyptes schlegeli), which is distinguishable from E. chrysolophus mainly by facial coloration. Although these sister taxa are widely accepted as representing distinct species based on morphological grounds, the extent of their genome-wide differentiation remains uncertain. In this study, we use genome-wide Single Nucleotide Polymorphisms to test genetic differentiation between these geographically isolated taxa and evaluate the main drivers of population structure among breeding colonies of macaroni/royal penguins. Genetic similarity observed between macaroni and royal penguins suggests they constitute a single evolutionary unit. Nevertheless, royal penguins exhibited a tendency to cluster only with macaroni individuals from Kerguelen Island, suggesting that dispersal occurs mainly between these neighboring colonies. A stepping stone model of differentiation of macaroni/royal populations was further supported by a strong pattern of isolation by distance detected across its whole distribution range, possibly driven by large geographic distances between colonies as well as natal philopatry. However, we also detected intraspecific genomic differentiation between Antarctic and sub-Antarctic populations of macaroni penguins, highlighting the role of environmental factors together with geographic distance in the processes of genetic differentiation between Antarctic and sub-Antarctic waters.

Important At-Sea Areas of Colonial Breeding Marine Predators on the Southern Patagonian Shelf.

The Patagonian Shelf Large Marine Ecosystem supports high levels of biodiversity and endemism and is one of the most productive marine ecosystems in the world. Despite the important role marine predators play in structuring the ecosystems, areas of high diversity where multiple predators congregate remains poorly known on the Patagonian Shelf. Here, we used biotelemetry and biologging tags to track the movements of six seabird species and three pinniped species breeding at the Falkland Islands. Using Generalized Additive Models, we then modelled these animals' use of space as functions of dynamic and static environmental indices that described their habitat. Based on these models, we mapped the predicted distribution of animals from both sampled and unsampled colonies and thereby identified areas where multiple species were likely to overlap at sea. Maximum foraging trip distance ranged from 79 to 1,325 km. However, most of the 1,891 foraging trips by 686 animals were restricted to the Patagonian Shelf and shelf slope, which highlighted a preference for these habitats. Of the seven candidate explanatory covariates used to predict distribution, distance from the colony was retained in models for all species and negatively affected the probability of occurrence. Predicted overlap among species was highest on the Patagonian Shelf around the Falkland Islands and the Burdwood Bank. The predicted area of overlap is consistent with areas that are also important habitat for marine predators migrating from distant breeding locations. Our findings provide comprehensive multi-species predictions for some of the largest marine predator populations on the Patagonian Shelf, which will contribute to future marine spatial planning initiatives. Crucially, our findings highlight that spatially explicit conservation measures are likely to benefit multiple species, while threats are likely to impact multiple species.

Correction: Return Customers: Foraging Site Fidelity and the Effect of Environmental Variability in Wide-Ranging Antarctic Fur Seals.

[This corrects the article DOI: 10.1371/journal.pone.0120888.].

Full circumpolar migration ensures evolutionary unity in the Emperor penguin.

Defining reliable demographic models is essential to understand the threats of ongoing environmental change. Yet, in the most remote and threatened areas, models are often based on the survey of a single population, assuming stationarity and independence in population responses. This is the case for the Emperor penguin Aptenodytes forsteri, a flagship Antarctic species that may be at high risk continent-wide before 2100. Here, using genome-wide data from the whole Antarctic continent, we reveal that this top-predator is organized as one single global population with a shared demography since the late Quaternary. We refute the view of the local population as a relevant demographic unit, and highlight that (i) robust extinction risk estimations are only possible by including dispersal rates and (ii) colony-scaled population size is rather indicative of local stochastic events, whereas the species' response to global environmental change is likely to follow a shared evolutionary trajectory.

The significance of cephalopod beaks in marine ecology studies: Can we use beaks for DNA analyses and mercury contamination assessment?

Cephalopod beaks found in the diet of predators have been a major source of scientific information. In this study, we evaluated the usefulness of DNA and contaminants analysis (total mercury - T-Hg) in cephalopod beaks in order to assess their applicability as tools in marine ecology studies. We concluded that, when applying DNA techniques to cephalopod beaks from Antarctic squid species, when using flesh attached to those beaks, it was possible to obtain DNA and to successfully identify cephalopod species; DNA was not found on the beaks themselves. This study also showed that it is possible to obtain information on T-Hg concentrations in beaks: the T-Hg concentrations found in the beaks were 6 to 46 times lower than in the flesh of the same cephalopod species. More research on the relationships of mercury concentrations in cephalopod beaks (and other tissues), intra- and inter-specifically, are needed in the future.

Feathers as a Tool to Assess Mercury Contamination in Gentoo Penguins: Variations at the Individual Level.

Feathers have been widely used to assess mercury contamination in birds as they reflect metal concentrations accumulated between successive moult periods: they are also easy to sample and have minimum impact on the study birds. Moult is considered the major pathway for mercury excretion in seabirds. Penguins are widely believed to undergo a complete, annual moult during which they do not feed. As penguins lose all their feathers, they are expected to have a low individual-variability in feather mercury concentration as all feathers are formed simultaneously from the same somatic reserves. This assumption is central to penguin studies that use feathers to examine the annual or among-individual variation in mercury concentrations in penguins. To test this assumption, we measured the mercury concentrations in 3-5 body feathers of 52 gentoo penguins (Pygoscelis papua) breeding at Bird Island, South Georgia (54°S 38°W). Twenty-five percent of the penguins studied showed substantial within-individual variation in the amount of mercury in their feathers (Coefficient of Variation: 34.7-96.7%). This variation may be caused by differences in moult patterns among individuals within the population leading to different interpretations in the overall population. Further investigation is now needed to fully understand individual variation in penguins' moult.

Return customers: foraging site fidelity and the effect of environmental variability in wide-ranging antarctic fur seals.

Strategies employed by wide-ranging foraging animals involve consideration of habitat quality and predictability and should maximise net energy gain. Fidelity to foraging sites is common in areas of high resource availability or where predictable changes in resource availability occur. However, if resource availability is heterogeneous or unpredictable, as it often is in marine environments, then habitat familiarity may also present ecological benefits to individuals. We examined the winter foraging distribution of female Antarctic fur seals, Arctocephalus gazelle, over four years to assess the degree of foraging site fidelity at two scales; within and between years. On average, between-year fidelity was strong, with most individuals utilising more than half of their annual foraging home range over multiple years. However, fidelity was a bimodal strategy among individuals, with five out of eight animals recording between-year overlap values of greater than 50%, while three animals recorded values of less than 5%. High long-term variance in sea surface temperature, a potential proxy for elevated long-term productivity and prey availability, typified areas of overlap. Within-year foraging site fidelity was weak, indicating that successive trips over the winter target different geographic areas. We suggest that over a season, changes in prey availability are predictable enough for individuals to shift foraging area in response, with limited associated energetic costs. Conversely, over multiple years, the availability of prey resources is less spatially and temporally predictable, increasing the potential costs of shifting foraging area and favouring long-term site fidelity. In a dynamic and patchy environment, multi-year foraging site fidelity may confer a long-term energetic advantage to the individual. Such behaviours that operate at the individual level have evolutionary and ecological implications and are potential drivers of niche specialization and modifiers of intra-specific competition.

The impact of predation by marine mammals on patagonian toothfish longline fisheries.

Predatory interaction of marine mammals with longline fisheries is observed globally, leading to partial or complete loss of the catch and in some parts of the world to considerable financial loss. Depredation can also create additional unrecorded fishing mortality of a stock and has the potential to introduce bias to stock assessments. Here we aim to characterise depredation in the Patagonian toothfish (Dissostichus eleginoides) fishery around South Georgia focusing on the spatio-temporal component of these interactions. Antarctic fur seals (Arctocephalus gazella), sperm whales (Physeter macrocephalus), and orcas (Orcinus orca) frequently feed on fish hooked on longlines around South Georgia. A third of longlines encounter sperm whales, but loss of catch due to sperm whales is insignificant when compared to that due to orcas, which interact with only 5% of longlines but can take more than half of the catch in some cases. Orca depredation around South Georgia is spatially limited and focused in areas of putative migration routes, and the impact is compounded as a result of the fishery also concentrating in those areas at those times. Understanding the seasonal behaviour of orcas and the spatial and temporal distribution of "depredation hot spots" can reduce marine mammal interactions, will improve assessment and management of the stock and contribute to increased operational efficiency of the fishery. Such information is valuable in the effort to resolve the human-mammal conflict for resources.

Pollution, habitat loss, fishing, and climate change as critical threats to penguins.

Cumulative human impacts across the world's oceans are considerable. We therefore examined a single model taxonomic group, the penguins (Spheniscidae), to explore how marine species and communities might be at risk of decline or extinction in the southern hemisphere. We sought to determine the most important threats to penguins and to suggest means to mitigate these threats. Our review has relevance to other taxonomic groups in the southern hemisphere and in northern latitudes, where human impacts are greater. Our review was based on an expert assessment and literature review of all 18 penguin species; 49 scientists contributed to the process. For each penguin species, we considered their range and distribution, population trends, and main anthropogenic threats over the past approximately 250 years. These threats were harvesting adults for oil, skin, and feathers and as bait for crab and rock lobster fisheries; harvesting of eggs; terrestrial habitat degradation; marine pollution; fisheries bycatch and resource competition; environmental variability and climate change; and toxic algal poisoning and disease. Habitat loss, pollution, and fishing, all factors humans can readily mitigate, remain the primary threats for penguin species. Their future resilience to further climate change impacts will almost certainly depend on addressing current threats to existing habitat degradation on land and at sea. We suggest protection of breeding habitat, linked to the designation of appropriately scaled marine reserves, including in the High Seas, will be critical for the future conservation of penguins. However, large-scale conservation zones are not always practical or politically feasible and other ecosystem-based management methods that include spatial zoning, bycatch mitigation, and robust harvest control must be developed to maintain marine biodiversity and ensure that ecosystem functioning is maintained across a variety of scales.

Influence of fasting during moult on the faecal microbiota of penguins.

Many seabirds including penguins are adapted to long periods of fasting, particularly during parts of the reproductive cycle and during moult. However, the influence of fasting on the gastrointestinal (GI) microbiota has not been investigated in seabirds. Therefore, the present study aimed to examine the microbial composition and diversity of the GI microbiota of fasting little (Eudyptula minor) and king penguins (Aptenodytes patagonicus) penguins during early and late moult. The results from this study indicated that there was little change in the abundance of the major phyla during moult, except for a significant increase in the level of Proteobacteria in king penguins. In king penguins the abundance of Fusobacteria increases from 1.73% during early moult to 33.6% by late moult, whilst the abundance of Proteobacteria (35.7% to 17.2%) and Bacteroidetes (19.5% to 11%) decrease from early to late moult. In little penguins, a decrease in the abundances of Firmicutes (44% to 29%) and an increase in the abundance of Bacteroidetes (11% to 20%) were observed from early to late moult respectively. The results from this study indicate that the microbial composition of both king and little penguins alters during fasting. However, it appears that the microbial composition of king penguins is more affected by fasting than little penguins with the length of fast the most probable cause for this difference.