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.

Whole genome sequencing reveals stepping-stone dispersal buffered against founder effects in a range expanding seabird.

Many species are shifting their ranges in response to climate-driven environmental changes, particularly in high-latitude regions. However, the patterns of dispersal and colonization during range shifting events are not always clear. Understanding how populations are connected through space and time can reveal how species navigate a changing environment. Here, we present a fine-scale population genomics study of gentoo penguins (Pygoscelis papua), a presumed site-faithful colonial nesting species that has increased in population size and expanded its range south along the Western Antarctic Peninsula. Using whole genome sequencing, we analysed 129 gentoo penguin individuals across 12 colonies located at or near the southern range edge. Through a detailed examination of fine-scale population structure, admixture, and population divergence, we inferred that gentoo penguins historically dispersed rapidly in a stepping-stone pattern from the South Shetland Islands leading to the colonization of Anvers Island, and then the adjacent mainland Western Antarctica Peninsula. Recent southward expansion along the Western Antarctic Peninsula also followed a stepping-stone dispersal pattern coupled with limited post-divergence gene flow from colonies on Anvers Island. Genetic diversity appeared to be maintained across colonies during the historical dispersal process, and range-edge populations are still growing. This suggests large numbers of migrants may provide a buffer against founder effects at the beginning of colonization events to maintain genetic diversity similar to that of the source populations before migration ceases post-divergence. These results coupled with a continued increase in effective population size since approximately 500-800 years ago distinguish gentoo penguins as a robust species that is highly adaptable and resilient to changing climate.

Islands in the ice: Potential impacts of habitat transformation on Antarctic biodiversity.

Antarctic biodiversity faces an unknown future with a changing climate. Most terrestrial biota is restricted to limited patches of ice-free land in a sea of ice, where they are adapted to the continent's extreme cold and wind and exploit microhabitats of suitable conditions. As temperatures rise, ice-free areas are predicted to expand, more rapidly in some areas than others. There is high uncertainty as to how species' distributions, physiology, abundance, and survivorship will be affected as their habitats transform. Here we use current knowledge to propose hypotheses that ice-free area expansion (i) will increase habitat availability, though the quality of habitat will vary; (ii) will increase structural connectivity, although not necessarily increase opportunities for species establishment; (iii) combined with milder climates will increase likelihood of non-native species establishment, but may also lengthen activity windows for all species; and (iv) will benefit some species and not others, possibly resulting in increased homogeneity of biodiversity. We anticipate considerable spatial, temporal, and taxonomic variation in species responses, and a heightened need for interdisciplinary research to understand the factors associated with ecosystem resilience under future scenarios. Such research will help identify at-risk species or vulnerable localities and is crucial for informing environmental management and policymaking into the future.

Variability, skipped breeding and heavy-tailed dynamics in an Antarctic seabird.

The population dynamics of many colonially breeding seabirds are characterized by large interannual fluctuations that cannot be explained by environmental conditions alone. This variation may be particularly confounded by the use of skipped breeding by seabirds as a life-history strategy, which directly impacts the number of breeding pairs and may affect the accuracy of breeding abundance as a metric of population health. Additionally, large fluctuations in time series may suggest that the underlying population dynamics are heavy tailed, allowing for a higher likelihood of extreme events than expected under Gaussian dynamics. Here, we investigated the effect of demography on time series for abundance of the Adélie penguin Pygoscelis adeliae and explored the occurrence of heavy-tailed dynamics in observed Adélie time series. We focus this study on the Adélie penguin as it is an important bellwether species long used to track the impacts of climate change and fishing on the Southern Ocean ecosystem and shares life-history traits with many colonial seabirds. We quantified the impacts of demographic rates, including skipped breeding, on time series of Adélie abundance simulated using an age-structured model. We also used observed time series of Adélie breeding abundance at all known Antarctic colonies to classify distributions for abundance as Gaussian or non-Gaussian heavy tailed. We then identified the cause of such heavy-tailed dynamics in simulated time series and linked these to spatial patterns in Adélie food resource variability. We found that breeding propensity drives observed breeding fluctuations more than any other vital rate, with high variability in skipped breeding decoupling true abundance from observed breeding abundance. We also found several Antarctic regions characterized by heavy-tailed dynamics in abundance. These regions were often also characterized by high variability in zooplankton availability. In simulated time series, heavy-tailed dynamics were strongly linked to high variability in adult survival. Our results illustrate that stochastic variability in abundance dynamics, particularly the presence of variable rates of skipped breeding, can challenge our interpretation of fluctuations in abundance through time and obscure the relationship between key environmental drivers and population abundance.

Antarctica and the strategic plan for biodiversity.

The Strategic Plan for Biodiversity, adopted under the auspices of the Convention on Biological Diversity, provides the basis for taking effective action to curb biodiversity loss across the planet by 2020-an urgent imperative. Yet, Antarctica and the Southern Ocean, which encompass 10% of the planet's surface, are excluded from assessments of progress against the Strategic Plan. The situation is a lost opportunity for biodiversity conservation globally. We provide such an assessment. Our evidence suggests, surprisingly, that for a region so remote and apparently pristine as the Antarctic, the biodiversity outlook is similar to that for the rest of the planet. Promisingly, however, much scope for remedial action exists.

A method to estimate pre-exploitation population size.

Antarctic fur seals (Arctocephalus gazella) were commercially exploited on the subantarctic island of South Georgia for over 100 years and nearly driven to extinction. Since the cessation of harvesting, however, their populations have rebounded, and they are now often considered a nuisance species whose impact on the terrestrial landscape should be mitigated. Any evaluation of their current population requires the context provided by their historic, pre-exploitation abundance, lest ecologists fall prey to shifting baseline syndrome in which their perspective on current abundance is compared only with an altered state resulting from past anthropogenic disturbance. Estimating pre-exploitation abundance is critical to defining species recovery and setting recovery targets, both of which are needed for the International Union for the Conservation of Nature's recent efforts to develop a green list of recovering species. To address this issue, we reconstructed the South Georgia fur seal harvest from 1786 to 1908 from ship logbooks and other historical records and interpolated missing harvest data as necessary with a generalized linear model fit to the historical record. Using an approximate Bayesian computation framework, harvest data, and a stochastic age-structured population model, we estimated the pre-exploitation abundance of Antarctic fur seals on South Georgia was 2.5 million females (95% CI 1.5-3.5 million). This estimate is similar to recent abundance estimates, and suggests current populations, and the ecological consequences of so many fur seals on the island, may be similar to conditions prior to human harvest. Although the historic archive on the fur sealing era is unavoidably patchy, the use of archival records is essential for reconstructing the past and, correspondingly, to understanding the present. Article impact statement: Defining species recovery requires an understanding of baseline population state, which can be estimated through statistical methods.

Un Método para Estimar el Tamaño Poblacional Previo a la Explotación Resumen La foca antártica (Arctocephalus gazella) fue explotada comercialmente en la isla subantártica de Georgia del Sur durante más de 100 años y esto casi la llevó a la extinción. Sin embargo, desde que se detuvo la captura de esta especie, su población se ha recuperado y actualmente se le considera con frecuencia una especie molesta cuyo impacto sobre el paisaje terrestre debería ser mitigado. Cualquier evaluación de la población actual requiere del contexto proporcionado por su abundancia histórica previa a la explotación para así evitar que los ecólogos sufran del síndrome de la línea base cambiante, en el cual la perspectiva de la abundancia contemporánea se compara solamente con un estado alterado resultante de perturbaciones antropogénicas pasadas. La estimación de la abundancia previa a la explotación es sumamente importante para definir la recuperación de una especie y para establecer los objetivos de recuperación, ambos requisitos necesarios para los esfuerzos recientes de la Unión Internacional para la Conservación de la Naturaleza (UICN) por desarrollar una lista verde de especies en recuperación. Para tratar este tema reconstruimos la captura de la foca antártica en la isla de Georgia del Sur desde 1786 hasta 1908 a partir de bitácoras de navíos y otros registros históricos e interpolamos los datos faltantes de las capturas conforme fuera necesario con un modelo lineal generalizado que se ajustara al registro histórico. Con un marco de trabajo de cómputo bayesiano aproximado, los datos de las capturas y un modelo poblacional estocástico estructurado por edades estimamos que la abundancia previa a la explotación de la foca antártica en la isla de Georgia del Sur era de 2.5 millones de hembras (95% IC1.5 - 3.5 millones). Este estimado es similar a las estimaciones recientes de abundancia y sugiere que las poblaciones actuales y las consecuencias ecológicas de la presencia de tantas focas en la isla podría ser similar a las condiciones previas a la captura. Aunque el archivo histórico sobre la era de la caza de focas antárticas presenta vacíos inevitablemente, el uso de registros archivados es esencial para la reconstrucción del pasado y, correspondientemente, para entender el presente.

Rethinking "normal": The role of stochasticity in the phenology of a synchronously breeding seabird.

Phenological changes have been observed in a variety of systems over the past century. There is concern that, as a consequence, ecological interactions are becoming increasingly mismatched in time, with negative consequences for ecological function. Significant spatial heterogeneity (inter-site) and temporal variability (inter-annual) can make it difficult to separate intrinsic, extrinsic and stochastic drivers of phenological variability. The goal of this study was to understand the timing and variability in breeding phenology of Adélie penguins under fixed environmental conditions and to use those data to identify a "null model" appropriate for disentangling the sources of variation in wild populations. Data on clutch initiation were collected from both wild and captive populations of Adélie penguins. Clutch initiation in the captive population was modelled as a function of year, individual and age to better understand phenological patterns observed in the wild population. Captive populations displayed as much inter-annual variability in breeding phenology as wild populations, suggesting that variability in breeding phenology is the norm and thus may be an unreliable indicator of environmental forcing. The distribution of clutch initiation dates was found to be moderately asymmetric (right skewed) both in the wild and in captivity, consistent with the pattern expected under social facilitation. The role of stochasticity in phenological processes has heretofore been largely ignored. However, these results suggest that inter-annual variability in breeding phenology can arise independent of any environmental or demographic drivers and that synchronous breeding can enhance inherent stochasticity. This complicates efforts to relate phenological variation to environmental variability in the wild. Accordingly, we must be careful to consider random forcing in phenological processes, lest we fit models to data dominated by random noise. This is particularly true for colonial species where breeding synchrony may outweigh each individual's effort to time breeding with optimal environmental conditions. Our study highlights the importance of identifying appropriate null models for studying phenology.

The importance of topographically corrected null models for analyzing ecological point processes.

Analyses of point process patterns and related techniques (e.g., MaxEnt) make use of the expected number of occurrences per unit area and second-order statistics based on the distance between occurrences. Ecologists working with point process data often assume that points exist on a two-dimensional x-y plane or within a three-dimensional volume, when in fact many observed point patterns are generated on a two-dimensional surface existing within three-dimensional space. For many surfaces, however, such as the topography of landscapes, the projection from the surface to the x-y plane preserves neither area nor distance. As such, when these point patterns are implicitly projected to and analyzed in the x-y plane, our expectations of the point pattern's statistical properties may not be met. When used in hypothesis testing, we find that the failure to account for the topography of the generating surface may bias statistical tests that incorrectly identify clustering and, furthermore, may bias coefficients in inhomogeneous point process models that incorporate slope as a covariate. We demonstrate the circumstances under which this bias is significant, and present simple methods that allow point processes to be simulated with corrections for topography. These point patterns can then be used to generate "topographically corrected" null models against which observed point processes can be compared.

Circumpolar analysis of the Adélie Penguin reveals the importance of environmental variability in phenological mismatch.

Evidence of climate-change-driven shifts in plant and animal phenology have raised concerns that certain trophic interactions may be increasingly mismatched in time, resulting in declines in reproductive success. Given the constraints imposed by extreme seasonality at high latitudes and the rapid shifts in phenology seen in the Arctic, we would also expect Antarctic species to be highly vulnerable to climate-change-driven phenological mismatches with their environment. However, few studies have assessed the impacts of phenological change in Antarctica. Using the largest database of phytoplankton phenology, sea-ice phenology, and Adélie Penguin breeding phenology and breeding success assembled to date, we find that, while a temporal match between Penguin breeding phenology and optimal environmental conditions sets an upper limit on breeding success, only a weak relationship to the mean exists. Despite previous work suggesting that divergent trends in Adélie Penguin breeding phenology are apparent across the Antarctic continent, we find no such trends. Furthermore, we find no trend in the magnitude of phenological mismatch, suggesting that mismatch is driven by interannual variability in environmental conditions rather than climate-change-driven trends, as observed in other systems. We propose several criteria necessary for a species to experience a strong climate-change-driven phenological mismatch, of which several may be violated by this system.

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.

Modeling structured population dynamics using data from unmarked individuals.

The study of population dynamics requires unbiased, precise estimates of abundance and vital rates that account for the demographic structure inherent in all wildlife and plant populations. Traditionally, these estimates have only been available through approaches that rely on intensive mark-recapture data. We extended recently developed N-mixture models to demonstrate how demographic parameters and abundance can be estimated for structured populations using only stage-structured count data. Our modeling framework can be used to make reliable inferences on abundance as well as recruitment, immigration, stage-specific survival, and detection rates during sampling. We present a range of simulations to illustrate the data requirements, including the number of years and locations necessary for accurate and precise parameter estimates. We apply our modeling framework to a population of northern dusky salamanders (Desmognathus fuscus) in the mid-Atlantic region (USA) and find that the population is unexpectedly declining. Our approach represents a valuable advance in the estimation of population dynamics using multistate data from unmarked individuals and should additionally be useful in the development of integrated models that combine data from intensive (e.g., mark-recapture) and extensive (e.g., counts) data sources.

Neutral metacommunity models predict fish diversity patterns in Mississippi-Missouri basin.

River networks, seen as ecological corridors featuring connected and hierarchical dendritic landscapes for animals and plants, present unique challenges and opportunities for testing biogeographical theories and macroecological laws. Although local and basin-scale differences in riverine fish diversity have been analysed as functions of energy availability and habitat heterogeneity, scale-dependent environmental conditions and river discharge, a model that predicts a comprehensive set of system-wide diversity patterns has been hard to find. Here we show that fish diversity patterns throughout the Mississippi-Missouri River System are well described by a neutral metacommunity model coupled with an appropriate habitat capacity distribution and dispersal kernel. River network structure acts as an effective template for characterizing spatial attributes of fish biodiversity. We show that estimates of average dispersal behaviour and habitat capacities, objectively calculated from average runoff production, yield reliable predictions of large-scale spatial biodiversity patterns in riverine systems. The success of the neutral theory in two-dimensional forest ecosystems and here in dendritic riverine ecosystems suggests the possible application of neutral metacommunity models in a diverse suite of ecosystems. This framework offers direct linkage from large-scale forcing, such as global climate change, to biodiversity patterns.

Quantifying potential marine debris sources and potential threats to penguins on the West Antarctic Peninsula.

Marine pollution is becoming ubiquitous in the environment. Observations of pollution on beaches, in the coastal ocean, and in organisms in the Antarctic are becoming distressingly common. Increasing human activity, growing tourism, and an expanding krill fishing industry along the West Antarctic Peninsula all represent potential sources of plastic pollution and other debris (collectively referred to as debris) to the region. However, the sources of these pollutants from point (pollutants released from discrete sources) versus non-point (pollutants from a large area rather than a specific source) sources are poorly understood. We used buoyant simulated particles released in a high-resolution physical ocean model to quantify pollutant loads throughout the region. We considered non-point sources of debris from the Antarctic Circumpolar Current, Bellingshausen Sea, Weddell Sea, and point source pollution from human activities including tourism, research, and fishing. We also determined possible origins for observed debris based on data from the Southern Ocean Observing System and Palmer Long-Term Ecological Research program. Our results indicate that point source pollution released in the coastal Antarctic is more likely to serve as a source for observed debris than non-point sources, and that the dominant source of pollution is region-specific. Penguin colonies in the South Shetland and Elephant Islands had the greatest debris load from point sources whereas loads from non-point sources were greatest around the southernmost colonies. Penguin colonies at Cornwallis Island and Fort Point were exposed to the highest theoretical debris loads. While these results do not include physical processes such as windage and Stokes Drift that are known to impact debris distributions and transport in the coastal ocean, these results provide critical insights to building an effective stratified sampling and monitoring effort to better understand debris distributions, concentrations, and origins throughout the West Antarctic Peninsula.

The influence of biotic and abiotic factors on the bacterial microbiome of gentoo penguins (Pygoscelis papua) in their natural environment.

The microbiome is a key factor in the health, well-being, and success of vertebrates, contributing to the adaptive capacity of the host. However, the impact of geographic and biotic factors that may affect the microbiome of wild birds in polar environments is not well defined. To address this, we determined the bacterial 16S rRNA gene sequence profiles in faecal samples from pygoscelid penguin populations in the Scotia Arc, focusing on gentoo penguins. This mesopredatory group breeds in defined colonies across a wide geographic range. Since diet could influence microbiome structure, we extracted dietary profiles from a eukaryotic 18S rRNA gene sequence profile. The bacterial microbiome profiles were considered in the context of a diverse set of environmental and ecological measures. Integrating wide geographic sampling with bacterial 16S and eukaryotic 18S rRNA gene sequencing of over 350 faecal samples identified associations between the microbiome profile and a suite of geographic and ecological factors. Microbiome profiles differed according to host species, colony identity, distance between colonies, and diet. Interestingly there was also a relationship between the proportion of host DNA (in relation to total 18S rRNA gene signal) and the microbiome, which may reflect gut passage time. Colony identity provided the strongest association with differences in microbiome profiles indicating that local factors play a key role in the microbiome structure of these polar seabirds. This may reflect the influence of local transfer of microbes either via faecal-oral routes, during chick feeding or other close contact events. Other factors including diet and host species also associate with variation in microbiome profile, and in at least some locations, the microbiome composition varies considerably between individuals. Given the variation in penguin microbiomes associated with diverse factors there is potential for disruption of microbiome associations at a local scale that could influence host health, productivity, and immunological competence. The microbiome represents a sensitive indicator of changing conditions, and the implications of any changes need to be considered in the wider context of environmental change and other stressors.

Phylogenetic prediction of the maximum per capita rate of population growth.

The maximum per capita rate of population growth, r, is a central measure of population biology. However, researchers can only directly calculate r when adequate time series, life tables and similar datasets are available. We instead view r as an evolvable, synthetic life-history trait and use comparative phylogenetic approaches to predict r for poorly known species. Combining molecular phylogenies, life-history trait data and stochastic macroevolutionary models, we predicted r for mammals of the Caniformia and Cervidae. Cross-validation analyses demonstrated that, even with sparse life-history data, comparative methods estimated r well and outperformed models based on body mass. Values of r predicted via comparative methods were in strong rank agreement with observed values and reduced mean prediction errors by approximately 68 per cent compared with two null models. We demonstrate the utility of our method by estimating r for 102 extant species in these mammal groups with unknown life-history traits.

Adélie penguins north and east of the 'Adélie gap' continue to thrive in the face of dramatic declines elsewhere in the Antarctic Peninsula region.

While population declines among Adélie penguins and population increases among gentoo penguins on the Western Antarctic Peninsula are well established, the logistical challenges of operating in the sea ice-heavy northern tip of the Antarctic Peninsula have prohibited reliable monitoring of seabirds in this region. Here we describe the findings of an expedition to the northern and eastern sides of the Antarctic Peninsula-a region at the nexus of two proposed Marine Protected Areas-to investigate the distribution and abundance of penguins in this region. We discovered several previously undocumented penguin colonies, completed direct surveys of three colonies initially discovered in satellite imagery, and re-surveyed several colonies last surveyed more than a decade ago. Whereas our expectation had been that the Peninsula itself would divide the areas undergoing ecological transition and the apparently more stable Weddell Sea region, our findings suggest that the actual transition zone lies in the so-called "Adélie gap," a 400-km stretch of coastline in which Adélies are notably absent. Our findings suggest that the region north and east of this gap represents a distinct ecoregion whose dynamics stand in sharp contrast to surrounding areas and is likely to be impacted by future conservation measures.

Difficulties in summing log-normal distributions for abundance and potential solutions.

The log-normal distribution, often used to model animal abundance and its uncertainty, is central to ecological modeling and conservation but its statistical properties are less intuitive than those of the normal distribution. The right skew of the log-normal distribution can be considerable for highly uncertain estimates and the median is often chosen as a point estimate. However, the use of the median can become complicated when summing across populations since the median of the sum of log-normal distributions is not the sum of the constituent medians. Such estimates become sensitive to the spatial or taxonomic scale over which abundance is being summarized and the naive estimate (the median of the distribution representing the sum across populations) can become grossly inflated. Here we review the statistical issues involved and some alternative formulations that might be considered by ecologists interested in modeling abundance. Using a recent estimate of global avian abundance as a case study (Callaghan et al. 2021), we investigate the properties of several alternative methods of summing across species' abundance, including the sorted summing used in the original study (Callaghan et al. 2021) and the use of shifted log-normal distributions, truncated normal distributions, and rectified normal distributions. The appropriate method of summing across distributions was intimately tied to the use of the mean or median as the measure of central tendency used as the point estimate. Use of the shifted log-normal distribution, however, generated scale-consistent estimates for global abundance across a spectrum of contexts. Our paper highlights how seemingly inconsequential decisions regarding the estimation of abundance yield radically different estimates of global abundance and its uncertainty, with conservation consequences that are underappreciated and require careful consideration.

Quantifying Antarctic krill connectivity across the West Antarctic Peninsula and its role in large-scale Pygoscelis penguin population dynamics.

Antarctic krill (Euphausia superba) are considered a keystone species for higher trophic level predators along the West Antarctic Peninsula (WAP) during the austral summer. The connectivity of krill may play a critical role in predator biogeography, especially for central-place foragers such as the Pygoscelis spp. penguins that breed along the WAP during the austral summer. Antarctic krill are also heavily fished commercially; therefore, understanding population connectivity of krill is critical to effective management. Here, we used a physical ocean model to examine adult krill connectivity in this region using simulated krill with realistic diel vertical migration behaviors across four austral summers. Our results indicate that krill north and south of Low Island and the southern Bransfield Strait are nearly isolated from each other and that persistent current features play a role in this lack of inter-region connectivity. Transit and entrainment times were not correlated with penguin populations at the large spatial scales examined. However, long transit times and reduced entrainment correlate spatially with the areas where krill fishing is most intense, which heightens the risk that krill fishing may lead to limited krill availability for predators.