Conservation features of the terrestrial Antarctic Peninsula.

Conserving landscapes used by multiple stakeholder groups requires understanding of what each stakeholder values. Here we employed a semi-structured, participatory approach to identify features of value in the terrestrial Antarctic Peninsula related to biodiversity, science and tourism. Stakeholders identified 115 features, ranging from Adélie penguin colonies to sites suitable for snowshoeing tourists. We split the features into seven broad categories: science, tourism, historic, biodiversity, geographic, habitat, and intrinsic features, finding that the biodiversity category contained the most features of any one category, while science stakeholders identified the most features of any stakeholder group. Stakeholders have overlapping interests in some features, particularly for seals and seabirds, indicating that thoughtful consideration of their inclusion in future management is required. Acknowledging the importance of tourism and other social features in Antarctica and ensuring their integration into conservation planning and assessment will increase the likelihood of implementing successful environmental management strategies into the future.

TerrANTALife 1.0 Biodiversity data checklist of known Antarctic terrestrial and freshwater life forms.

Background: Incomplete species inventories for Antarctica represent a key challenge for comprehensive ecological research and conservation in the region. Additionally, data required to understand population dynamics, rates of evolution, spatial ranges, functional traits, physiological tolerances and species interactions, all of which are fundamental to disentangle the different functional elements of Antarctic biodiversity, are mostly missing. However, much of the fauna, flora and microbiota in the emerged ice-free land of the continent have an uncertain presence and/or unresolved status, with entire biodiversity compendia of prokaryotic groups (e.g. bacteria) being missing. All the available biodiversity information requires consolidation, cross-validation, re-assessment and steady systematic inclusion in order to create a robust catalogue of biodiversity for the continent. New information: We compiled, completed and revised eukaryotic species inventories present in terrestrial and freshwater ecosystems in Antarctica in a new living database: terrANTALife (version 1.0). The database includes the first integration in a compendium for many groups of eukaryotic microorganisms. We also introduce a first catalogue of amplicon sequence variants (ASVs) of prokaryotic biodiversity. Available compendia and literature to date were searched for Antarctic terrestrial and freshwater species, integrated, taxonomically harmonised and curated by experts to create comprehensive checklists of Antarctic organisms. The final inventories comprises 470 animal species (including vertebrates, free-living invertebrates and parasites), 306 plants (including all Viridiplantae: embryophytes and green algae), 997 fungal species and 434 protists (sensu lato). We also provide a first account for many groups of microorganisms, including non-lichenised fungi and multiple groups of eukaryotic unicellular species (Stramenophila, Alveolata and Rhizaria (SAR), Chromists and Amoeba), jointly referred to as "protists". In addition, we identify 1753 bacterial (obtained from 348117 ASVs) and 34 archaeal genera (from 1848 ASVs), as well as, at least, 14 virus families. We formulate a basic tree of life in Antarctica with the main lineages listed in the region and their "known-accepted-species" numbers.

Climate and human stressors on global penguin hotspots: Current assessments for future conservation.

As charismatic and iconic species, penguins can act as "ambassadors" or flagship species to promote the conservation of marine habitats in the Southern Hemisphere. Unfortunately, there is a lack of reliable, comprehensive, and systematic analysis aimed at compiling spatially explicit assessments of the multiple impacts that the world's 18 species of penguin are facing. We provide such an assessment by combining the available penguin occurrence information from Global Biodiversity Information Facility (>800,000 occurrences) with three main stressors: climate-driven environmental changes at sea, industrial fisheries, and human disturbances on land. Our analyses provide a quantitative assessment of how these impacts are unevenly distributed spatially within species' distribution ranges. Consequently, contrasting pressures are expected among species, and populations within species. The areas coinciding with the greatest impacts for penguins are the coast of Perú, the Patagonian Shelf, the Benguela upwelling region, and the Australian and New Zealand coasts. When weighting these potential stressors with species-specific vulnerabilities, Humboldt (Spheniscus humboldti), African (Spheniscus demersus), and Chinstrap penguin (Pygoscelis antarcticus) emerge as the species under the most pressure. Our approach explicitly differentiates between climate and human stressors, since the more achievable management of local anthropogenic stressors (e.g., fisheries and land-based threats) may provide a suitable means for facilitating cumulative impacts on penguins, especially where they may remain resilient to global processes such as climate change. Moreover, our study highlights some poorly represented species such as the Northern Rockhopper (Eudyptes moseleyi), Snares (Eudyptes robustus), and Erect-crested penguin (Eudyptes sclateri) that need internationally coordinated efforts for data acquisition and data sharing to understand their spatial distribution properly.

A vision for incorporating human mobility in the study of human-wildlife interactions.

As human activities increasingly shape land- and seascapes, understanding human-wildlife interactions is imperative for preserving biodiversity. Habitats are impacted not only by static modifications, such as roads, buildings and other infrastructure, but also by the dynamic movement of people and their vehicles occurring over shorter time scales. Although there is increasing realization that both components of human activity substantially affect wildlife, capturing more dynamic processes in ecological studies has proved challenging. Here we propose a conceptual framework for developing a 'dynamic human footprint' that explicitly incorporates human mobility, providing a key link between anthropogenic stressors and ecological impacts across spatiotemporal scales. Specifically, the dynamic human footprint integrates a range of metrics to fully acknowledge the time-varying nature of human activities and to enable scale-appropriate assessments of their impacts on wildlife behaviour, demography and distributions. We review existing terrestrial and marine human-mobility data products and provide a roadmap for how these could be integrated and extended to enable more comprehensive analyses of human impacts on biodiversity in the Anthropocene.

Environmental Drivers of Growth and Oxidative Status during Early Life in a Long-Lived Antarctic Seabird, the Adélie Penguin.

AbstractIn vertebrates, developmental conditions can have long-term effects on individual performance. It is increasingly recognized that oxidative stress could be one physiological mechanism connecting early-life experience to adult phenotype. Accordingly, markers of oxidative status could be useful for assessing the developmental constraints encountered by offspring. Although some studies have demonstrated that developmental constraints are associated with high levels of oxidative stress in offspring, it remains unclear how growth, parental behavior, and brood competition may altogether affect oxidative stress in long-lived species in the wild. Here, we investigated this question in a long-lived Antarctic bird species by testing the impact of brood competition (e.g., brood size and hatching order) on body mass and on two markers of oxidative damage in Adélie penguin chicks. We also examined the influence of parental effort (i.e., foraging trip duration) and parental body condition on chick body mass and oxidative damage. First, we found that brood competition and parental traits had significant impacts on chick body mass. Second, we found that chick age and, to a lesser extent, chick body mass were two strong determinants of the levels of oxidative damage in Adélie penguin chicks. Finally, and importantly, we also found that brood competition significantly increased the levels of one marker of oxidative damage and was associated with a lower survival probability. However, parental effort and parental condition were not significantly linked to chick levels of oxidative damage. Overall, our study demonstrates that sibling competition can generate an oxidative cost even for this long-lived Antarctic species with a limited brood size (maximum of two chicks).

Holding time has limited impact on constitutive innate immune function in a long-lived Antarctic seabird, the Adélie penguin: implications for field studies.

There is great interest in measuring immune function in wild animals. Yet, field conditions often have methodological challenges related to handling stress, which can alter physiology. Despite general consensus that immune function is influenced by handling stress, previous studies have provided equivocal results. Furthermore, few studies have focused on long-lived species, which may have different stress-immune trade-offs compared to short-lived species that have primarily been tested. Here, we investigate whether capture and handling duration impacts innate immune function in a long-lived seabird, the Adélie penguin (Pygoscelis adeliae). We found no evidence for changes in three commonly used parameters of innate immune function upon holding time of up to 2 h, suggesting that immune function in this species is more robust against handling than in other species. This opens up exciting possibilities for measuring immune function in species with similar life-histories even if samples cannot be taken directly after capture.

Exposure, but not timing of exposure, to a sulfonylurea herbicide alters larval development and behaviour in an amphibian species.

Environmental contamination is one of the major causes of biodiversity loss. Wetlands are particularly susceptible to contamination and species inhabiting these habitats are subjected to pollutants during sensitive phases of their development. In this study, tadpoles of a widespread amphibian, the spined toad (Bufo spinosus), were exposed to environmental concentrations of nicosulfuron (0 µg/L; 0.15 ± 0.05 µg/L and 0.83 ± 0.04 µg/L), a sulfonylurea herbicide, during different phases of development. Tadpoles were exposed during embryonic (12.98 ± 0.90 days) or larval development (93.74± 0.85 days), or throughout both phases, and we quantified development duration, morphological traits and behavioural features as responses to exposure. Developing tadpoles exposed to nicosulfuron were larger, but with smaller body, and had shorter but wider tail muscles. They were also more active and swam faster than control tadpoles and showed diverging patterns of behavioural complexity. We showed that higher concentrations had greater effects on individuals than lower concentrations, but the timing of nicosulfuron exposure did not influence the metrics studied: Exposure to nicosulfuron triggered similar effects irrespective of the developmental stages at which exposure occurred. These results further indicate that transient exposure (e.g., during embryonic development) can induce long-lasting effects throughout larval development to metamorphosis. Our study confirms that contaminants at environmental concentrations can have strong consequences on non-target organisms. Our results emphasize the need for regulation agencies and policy makers to consider sublethal concentrations of sulfonulyrea herbicides, such as nicosulfuron, as a minimum threshold in their recommendations.

Threat management priorities for conserving Antarctic biodiversity.

Antarctic terrestrial biodiversity faces multiple threats, from invasive species to climate change. Yet no large-scale assessments of threat management strategies exist. Applying a structured participatory approach, we demonstrate that existing conservation efforts are insufficient in a changing world, estimating that 65% (at best 37%, at worst 97%) of native terrestrial taxa and land-associated seabirds are likely to decline by 2100 under current trajectories. Emperor penguins are identified as the most vulnerable taxon, followed by other seabirds and dry soil nematodes. We find that implementing 10 key threat management strategies in parallel, at an estimated present-day equivalent annual cost of US$23 million, could benefit up to 84% of Antarctic taxa. Climate change is identified as the most pervasive threat to Antarctic biodiversity and influencing global policy to effectively limit climate change is the most beneficial conservation strategy. However, minimising impacts of human activities and improved planning and management of new infrastructure projects are cost-effective and will help to minimise regional threats. Simultaneous global and regional efforts are critical to secure Antarctic biodiversity for future generations.

The role of individual variability on the predictive performance of machine learning applied to large bio-logging datasets.

Animal-borne tagging (bio-logging) generates large and complex datasets. In particular, accelerometer tags, which provide information on behaviour and energy expenditure of wild animals, produce high-resolution multi-dimensional data, and can be challenging to analyse. We tested the performance of commonly used artificial intelligence tools on datasets of increasing volume and dimensionality. By collecting bio-logging data across several sampling seasons, datasets are inherently characterized by inter-individual variability. Such information should be considered when predicting behaviour. We integrated both unsupervised and supervised machine learning approaches to predict behaviours in two penguin species. The classified behaviours obtained from the unsupervised approach Expectation Maximisation were used to train the supervised approach Random Forest. We assessed agreement between the approaches, the performance of Random Forest on unknown data and the implications for the calculation of energy expenditure. Consideration of behavioural variability resulted in high agreement (> 80%) in behavioural classifications and minimal differences in energy expenditure estimates. However, some outliers with < 70% of agreement, highlighted how behaviours characterized by signal similarity are confused. We advise the broad bio-logging community, approaching these large datasets, to be cautious when upscaling predictions, as this might lead to less accurate estimates of behaviour and energy expenditure.

Foraging range scales with colony size in high-latitude seabirds.

Density-dependent prey depletion around breeding colonies has long been considered an important factor controlling the population dynamics of colonial animals.1-4 Ashmole proposed that as seabird colony size increases, intraspecific competition leads to declines in reproductive success, as breeding adults must spend more time and energy to find prey farther from the colony.1 Seabird colony size often varies over several orders of magnitude within the same species and can include millions of individuals per colony.5,6 As such, colony size likely plays an important role in determining the individual behavior of its members and how the colony interacts with the surrounding environment.6 Using tracking data from murres (Uria spp.), the world's most densely breeding seabirds, we show that the distribution of foraging-trip distances scales to colony size0.33 during the chick-rearing stage, consistent with Ashmole's halo theory.1,2 This pattern occurred across colonies varying in size over three orders of magnitude and distributed throughout the North Atlantic region. The strong relationship between colony size and foraging range means that the foraging areas of some colonial species can be estimated from colony sizes, which is more practical to measure over a large geographic scale. Two-thirds of the North Atlantic murre population breed at the 16 largest colonies; by extrapolating the predicted foraging ranges to sites without tracking data, we show that only two of these large colonies have significant coverage as marine protected areas. Our results are an important example of how theoretical models, in this case, Ashmole's version of central-place-foraging theory, can be applied to inform conservation and management in colonial breeding species.

The consequences of chaos: Foraging activity of a marine predator remains impacted several days after the end of a storm.

As extreme weather is expected to become more frequent with global climate change, it is crucial to evaluate the capacity of species to respond to short-term and unpredictable events. Here, we examined the effect of a strong storm event during the chick-rearing stage of little penguins (Eudyptula minor) from a mega colony in southern Australia. We investigated how a 3-day storm affected the foraging behaviour of little penguins by comparing their foraging activities and body mass change before, during and after the storm event. As strong winds deepened the mixed layer in the birds' foraging zone during the storm, penguins increased their foraging trip duration, had a lower prey encounter rate and a lower body mass gain. The adverse effects on the foraging efficiency of little penguins continued several days after the storm ceased; even though the water column stratification had returned as before the storm, suggesting a prolonged effect of the storm event on the prey availability. Thus, short-term stochastic events can have an extended impact on the foraging efficiency of penguins. When occurring at a crucial stage of breeding, this may affect breeding success.

One hundred research questions in conservation physiology for generating actionable evidence to inform conservation policy and practice.

Environmental change and biodiversity loss are but two of the complex challenges facing conservation practitioners and policy makers. Relevant and robust scientific knowledge is critical for providing decision-makers with the actionable evidence needed to inform conservation decisions. In the Anthropocene, science that leads to meaningful improvements in biodiversity conservation, restoration and management is desperately needed. Conservation Physiology has emerged as a discipline that is well-positioned to identify the mechanisms underpinning population declines, predict responses to environmental change and test different in situ and ex situ conservation interventions for diverse taxa and ecosystems. Here we present a consensus list of 10 priority research themes. Within each theme we identify specific research questions (100 in total), answers to which will address conservation problems and should improve the management of biological resources. The themes frame a set of research questions related to the following: (i) adaptation and phenotypic plasticity; (ii) human-induced environmental change; (iii) human-wildlife interactions; (iv) invasive species; (v) methods, biomarkers and monitoring; (vi) policy, engagement and communication; (vii) pollution; (viii) restoration actions; (ix) threatened species; and (x) urban systems. The themes and questions will hopefully guide and inspire researchers while also helping to demonstrate to practitioners and policy makers the many ways in which physiology can help to support their decisions.

Adélie penguins foraging consistency and site fidelity are conditioned by breeding status and environmental conditions.

There is a growing interest in studying consistency and site fidelity of individuals to assess, respectively, how individual behaviour shapes the population response to environmental changes, and to highlight the critical habitats needed by species. In Antarctica, the foraging activity of central place foragers like Adélie penguins (Pygoscelis adeliae) is constrained by the sea-ice cover during the breeding season. We estimated the population-level repeatability in foraging trip parameters and sea-ice conditions encountered by birds across successive trips over several years, and we examined their foraging site fidelity linked to sea-ice concentrations throughout the chick-rearing season. Penguins' foraging activity was repeatable despite varying annual sea-ice conditions. Birds' site fidelity is constrained by both sea-ice conditions around the colony that limit movements and resources availability, and also behavioural repeatability of individuals driven by phenological constraints. Adélie penguins favoured sea-ice concentrations between 20-30%, as these facilitate access to open water while opening multiple patches for exploration in restricted areas in case of prey depletion. When the sea-ice concentration became greater than 30%, foraging site fidelity decreased and showed higher variability, while it increased again after 60%. Between two trips, the foraging site fidelity remained high when sea-ice concentration changed by ± 10% but showed greater variability when sea-ice concentrations differed on a larger range. In summary, Adélie penguins specialize their foraging behaviour during chick-rearing according to sea-ice conditions to enhance their reproductive success. The balance between being consistent under favourable environmental conditions vs. being flexible under more challenging conditions may be key to improving foraging efficiency and reproductive success to face fast environmental changes.

Acceleration predicts energy expenditure in a fat, flightless, diving bird.

Energy drives behaviour and life history decisions, yet it can be hard to measure at fine scales in free-moving animals. Accelerometry has proven a powerful tool to estimate energy expenditure, but requires calibration in the wild. This can be difficult in some environments, or for particular behaviours, and validations have produced equivocal results in some species, particularly air-breathing divers. It is, therefore, important to calibrate accelerometry across different behaviours to understand the most parsimonious way to estimate energy expenditure in free-living conditions. Here, we combine data from miniaturised acceleration loggers on 58 free-living Adélie penguins with doubly labelled water (DLW) measurements of their energy expenditure over several days. Across different behaviours, both in water and on land, dynamic body acceleration was a good predictor of independently measured DLW-derived energy expenditure (R2 = 0.72). The most parsimonious model suggested different calibration coefficients are required to predict behaviours on land versus foraging behaviour in water (R2 = 0.75). Our results show that accelerometry can be used to reliably estimate energy expenditure in penguins, and we provide calibration equations for estimating metabolic rate across several behaviours in the wild.

Oceanic thermal structure mediates dive sequences in a foraging seabird.

Changes in marine ecosystems are easier to detect in upper-level predators, like seabirds, which integrate trophic interactions throughout the food web.Here, we examined whether diving parameters and complexity in the temporal organization of diving behavior of little penguins (Eudyptula minor) are influenced by sea surface temperature (SST), water stratification, and wind speed-three oceanographic features influencing prey abundance and distribution in the water column.Using fractal time series analysis, we found that foraging complexity, expressed as the degree of long-range correlations or memory in the dive series, was associated with SST and water stratification throughout the breeding season, but not with wind speed. Little penguins foraging in warmer/more-stratified waters exhibited greater determinism (memory) in foraging sequences, likely as a response to prey aggregations near the thermocline. They also showed higher foraging efficiency, performed more dives and dove to shallower depths than those foraging in colder/less-stratified waters.Reductions in the long-term memory of dive sequences, or in other words increases in behavioral stochasticity, may suggest different strategies concerning the exploration-exploitation trade-off under contrasting environmental conditions.

Reframing conservation physiology to be more inclusive, integrative, relevant and forward-looking: reflections and a horizon scan.

Applying physiological tools, knowledge and concepts to understand conservation problems (i.e. conservation physiology) has become commonplace and confers an ability to understand mechanistic processes, develop predictive models and identify cause-and-effect relationships. Conservation physiology is making contributions to conservation solutions; the number of 'success stories' is growing, but there remain unexplored opportunities for which conservation physiology shows immense promise and has the potential to contribute to major advances in protecting and restoring biodiversity. Here, we consider how conservation physiology has evolved with a focus on reframing the discipline to be more inclusive and integrative. Using a 'horizon scan', we further explore ways in which conservation physiology can be more relevant to pressing conservation issues of today (e.g. addressing the Sustainable Development Goals; delivering science to support the UN Decade on Ecosystem Restoration), as well as more forward-looking to inform emerging issues and policies for tomorrow. Our horizon scan provides evidence that, as the discipline of conservation physiology continues to mature, it provides a wealth of opportunities to promote integration, inclusivity and forward-thinking goals that contribute to achieving conservation gains. To advance environmental management and ecosystem restoration, we need to ensure that the underlying science (such as that generated by conservation physiology) is relevant with accompanying messaging that is straightforward and accessible to end users.

Tracking of marine predators to protect Southern Ocean ecosystems.

Southern Ocean ecosystems are under pressure from resource exploitation and climate change1,2. Mitigation requires the identification and protection of Areas of Ecological Significance (AESs), which have so far not been determined at the ocean-basin scale. Here, using assemblage-level tracking of marine predators, we identify AESs for this globally important region and assess current threats and protection levels. Integration of more than 4,000 tracks from 17 bird and mammal species reveals AESs around sub-Antarctic islands in the Atlantic and Indian Oceans and over the Antarctic continental shelf. Fishing pressure is disproportionately concentrated inside AESs, and climate change over the next century is predicted to impose pressure on these areas, particularly around the Antarctic continent. At present, 7.1% of the ocean south of 40°S is under formal protection, including 29% of the total AESs. The establishment and regular revision of networks of protection that encompass AESs are needed to provide long-term mitigation of growing pressures on Southern Ocean ecosystems.

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.