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

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

The impact of boldness on demographic rates and life-history outcomes in the wandering albatross.

Differences among individuals within a population are ubiquitous. Those differences are known to affect the entire life cycle with important consequences for all demographic rates and outcomes. One source of among-individual phenotypic variation that has received little attention from a demographic perspective is animal personality, which is defined as consistent and heritable behavioural differences between individuals. While many studies have shown that individual variation in individual personality can generate individual differences in survival and reproductive rates, the impact of personality on all demographic rates and outcomes remains to be assessed empirically. Here, we used a unique, long-term, dataset coupling demography and personality of wandering albatross (Diomedea exulans) in the Crozet Archipelago and a comprehensive analysis based on a suite of approaches (capture-mark-recapture statistical models, Markov chains models and structured matrix population models). We assessed the effect of boldness on annual demographic rates (survival, breeding probability, breeding success), life-history outcomes (life expectancy, lifetime reproductive outcome, occupancy times), and an integrative demographic outcome (population growth rate). We found that boldness had little impact on female demographic rates, but was very likely associated with lower breeding probabilities in males. By integrating the effects of boldness over the entire life cycle, we found that bolder males had slightly lower lifetime reproductive success compared to shyer males. Indeed, bolder males spent a greater proportion of their lifetime as non-breeders, which suggests longer inter-breeding intervals due to higher reproductive allocation. Our results reveal that the link between boldness and demography is more complex than anticipated by the pace-of-life literature and highlight the importance of considering the entire life cycle with a comprehensive approach when assessing the role of personality on individual performance and demography.

Where to live? Landfast sea ice shapes emperor penguin habitat around Antarctica.

Predicting species survival in the face of climate change requires understanding the drivers that influence their distribution. Emperor penguins (Aptenodytes forsteri) incubate and rear chicks on landfast sea ice, whose extent, dynamics, and quality are expected to vary substantially due to climate change. Until recently, this species' continent-wide observations were scarce, and knowledge on their distribution and habitat limited. Advances in satellite imagery now allow their observation and characterization of habitats across Antarctica at high resolution. Using circumpolar high-resolution satellite images, unique fast ice metrics, and geographic and biological factors, we identified diverse penguin habitats across the continent, with no significant difference between areas with penguins or not. There is a clear geographic partitioning of colonies with respect to their defining habitat characteristics, indicating possible behavioral plasticity among different metapopulations. This coincides with geographic structures found in previous genetic studies. Given projections of quasi-extinction for this species in 2100, this study provides essential information for conservation measures.

Individual life histories: neither slow nor fast, just diverse.

The slow-fast continuum is a commonly used framework to describe variation in life-history strategies across species. Individual life histories have also been assumed to follow a similar pattern, especially in the pace-of-life syndrome literature. However, whether a slow-fast continuum commonly explains life-history variation among individuals within a population remains unclear. Here, we formally tested for the presence of a slow-fast continuum of life histories both within populations and across species using detailed long-term individual-based demographic data for 17 bird and mammal species with markedly different life histories. We estimated adult lifespan, age at first reproduction, annual breeding frequency, and annual fecundity, and identified the main axes of life-history variation using principal component analyses. Across species, we retrieved the slow-fast continuum as the main axis of life-history variation. However, within populations, the patterns of individual life-history variation did not align with a slow-fast continuum in any species. Thus, a continuum ranking individuals from slow to fast living is unlikely to shape individual differences in life histories within populations. Rather, individual life-history variation is likely idiosyncratic across species, potentially because of processes such as stochasticity, density dependence, and individual differences in resource acquisition that affect species differently and generate non-generalizable patterns across species.

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.

Causes and consequences of pair-bond disruption in a sex-skewed population of a long-lived monogamous seabird.

Many animals form long-term monogamous pair bonds, and the disruption of a pair bond (through either divorce or widowhood) can have significant consequences for individual vital rates (survival, breeding, and breeding success probabilities) and life-history outcomes (lifetime reproductive success [LRS], life expectancy). Here, we investigated the causes and consequences of pair-bond disruption in wandering albatross (Diomedea exulans). State-of-the-art statistical and mathematical approaches were developed to estimate divorce and widowhood rates and their impacts on vital rates and life-history outcomes. In this population, females incur a higher mortality rate due to incidental fishery bycatch, so the population is male-skewed. Therefore, we first posited that males would show higher widowhood rates negatively correlated with fishing effort and females would have higher divorce rates because they have more mating opportunities. Furthermore, we expected that divorce could be an adaptive strategy, whereby individuals improved breeding success by breeding with a new partner of better quality. Finally, we posited that pair-bond disruptions could reduce survival and breeding probabilities owing to the cost of remating processes, with important consequences for life-history outcomes. As expected, we showed that males had higher widowhood rates than females and females had higher divorce rates in this male-skewed population. However, no correlation was found between fishing effort and male widowhood. Secondly, contrary to our expectation, we found that divorce was likely nonadaptive in this population. We propose that divorce in this population is caused by an intruder who outcompetes the original partner in line with the so-called forced divorce hypothesis. Furthermore, we found a 16.7% and 18.0% reduction in LRS only for divorced and widowed males, respectively, owing to missing breeding seasons after a pair-bond disruption. Finally, we found that divorced individuals were more likely to divorce again, but whether this is related to specific individual characteristics remains an important area of investigation.

Boldness predicts divorce rates in wandering albatrosses (Diomedea exulans).

Personality predicts divorce rates in humans, yet how personality traits affect divorce in wild animals remains largely unknown. In a male-skewed population of wandering albatross (Diomedea exulans), we showed that personality predicts divorce; shyer males exhibited higher divorce rates than bolder males but no such relationship was found in females. We propose that divorce may be caused by the intrusion of male competitors and shyer males divorce more often because of their avoidance of territorial aggression, while females have easier access to mates regardless of their personality. Thus, personality may have important implications for the dynamics of social relationships.

When the going gets tough, the tough get going: Effect of extreme climate on an Antarctic seabird's life history.

Individuals differ in many ways. Most produce few offspring; a handful produce many. Some die early; others live to old age. It is tempting to attribute these differences in outcomes to differences in individual traits, and thus in the demographic rates experienced. However, there is more to individual variation than meets the eye of the biologist. Even among individuals sharing identical traits, life history outcomes (life expectancy and lifetime reproduction) will vary due to individual stochasticity, that is to chance. Quantifying the contributions of heterogeneity and chance is essential to understand natural variability. Interindividual differences vary across environmental conditions, hence heterogeneity and stochasticity depend on environmental conditions. We show that favourable conditions increase the contributions of individual stochasticity, and reduce the contributions of heterogeneity, to variance in demographic outcomes in a seabird population. The opposite is true under poor conditions. This result has important consequence for understanding the ecology and evolution of life history strategies.

Temporal correlations among demographic parameters are ubiquitous but highly variable across species.

Temporal correlations among demographic parameters can strongly influence population dynamics. Our empirical knowledge, however, is very limited regarding the direction and the magnitude of these correlations and how they vary among demographic parameters and species' life histories. Here, we use long-term demographic data from 15 bird and mammal species with contrasting pace of life to quantify correlation patterns among five key demographic parameters: juvenile and adult survival, reproductive probability, reproductive success and productivity. Correlations among demographic parameters were ubiquitous, more frequently positive than negative, but strongly differed across species. Correlations did not markedly change along the slow-fast continuum of life histories, suggesting that they were more strongly driven by ecological than evolutionary factors. As positive temporal demographic correlations decrease the mean of the long-run population growth rate, the common practice of ignoring temporal correlations in population models could lead to the underestimation of extinction risks in most species.

Detecting climate signals in populations across life histories.

Climate impacts are not always easily discerned in wild populations as detecting climate change signals in populations is challenged by stochastic noise associated with natural climate variability, variability in biotic and abiotic processes, and observation error in demographic rates. Detection of the impact of climate change on populations requires making a formal distinction between signals in the population associated with long-term climate trends from those generated by stochastic noise. The time of emergence (ToE) identifies when the signal of anthropogenic climate change can be quantitatively distinguished from natural climate variability. This concept has been applied extensively in the climate sciences, but has not been explored in the context of population dynamics. Here, we outline an approach to detecting climate-driven signals in populations based on an assessment of when climate change drives population dynamics beyond the envelope characteristic of stochastic variations in an unperturbed state. Specifically, we present a theoretical assessment of the time of emergence of climate-driven signals in population dynamics ( ToE pop ). We identify the dependence of ToE pop on the magnitude of both trends and variability in climate and also explore the effect of intrinsic demographic controls on ToE pop . We demonstrate that different life histories (fast species vs. slow species), demographic processes (survival, reproduction), and the relationships between climate and demographic rates yield population dynamics that filter climate trends and variability differently. We illustrate empirically how to detect the point in time when anthropogenic signals in populations emerge from stochastic noise for a species threatened by climate change: the emperor penguin. Finally, we propose six testable hypotheses and a road map for future research.

Recent natural variability in global warming weakened phenological mismatch and selection on seasonal timing in great tits (Parus major).

Climate change has led to phenological shifts in many species, but with large variation in magnitude among species and trophic levels. The poster child example of the resulting phenological mismatches between the phenology of predators and their prey is the great tit (Parus major), where this mismatch led to directional selection for earlier seasonal breeding. Natural climate variability can obscure the impacts of climate change over certain periods, weakening phenological mismatching and selection. Here, we show that selection on seasonal timing indeed weakened significantly over the past two decades as increases in late spring temperatures have slowed down. Consequently, there has been no further advancement in the date of peak caterpillar food abundance, while great tit phenology has continued to advance, thereby weakening the phenological mismatch. We thus show that the relationships between temperature, phenologies of prey and predator, and selection on predator phenology are robust, also in times of a slowdown of warming. Using projected temperatures from a large ensemble of climate simulations that take natural climate variability into account, we show that prey phenology is again projected to advance faster than great tit phenology in the coming decades, and therefore that long-term global warming will intensify phenological mismatches.

The interplay between hunting rate, hunting selectivity, and reproductive strategies shapes population dynamics of a large carnivore.

Harvest, through its intensity and regulation, often results in selection on female reproductive traits. Changes in female traits can have demographic consequences, as they are fundamental in shaping population dynamics. It is thus imperative to understand and quantify the demographic consequences of changes in female reproductive traits to better understand and anticipate population trajectories under different harvest intensities and regulations. Here, using a dynamic, frequency-dependent, population model of the intensively hunted brown bear (Ursus arctos) population in Sweden, we quantify and compare population responses to changes in four reproductive traits susceptible to harvest-induced selection: litter size, weaning age, age at first reproduction, and annual probability to reproduce. We did so for different hunting quotas and under four possible hunting regulations: (i) no individuals are protected, (ii) mothers but not dependent offspring are protected, (iii) mothers and dependent offspring of the year (cubs) are protected, and (iv) entire family groups are protected (i.e., mothers and dependent offspring of any age). We found that population growth rate declines sharply with increasing hunting quotas. Increases in litter size and the probability to reproduce have the greatest potential to affect population growth rate. Population growth rate increases the most when mothers are protected. Adding protection on offspring (of any age), however, reduces the availability of bears for hunting, which feeds back to increase hunting pressure on the nonprotected categories of individuals, leading to reduced population growth. Finally, we found that changes in reproductive traits can dampen population declines at very high hunting quotas, but only when protecting mothers. Our results illustrate that changes in female reproductive traits may have context-dependent consequences for demography. Thus, to predict population consequences of harvest-induced selection in wild populations, it is critical to integrate both hunting intensity and regulation, especially if hunting selectivity targets female reproductive strategies.

Extreme climate events limit northern range expansion of wild turkeys.

For species inhabiting areas at the limit of their environmental tolerance, extreme events often drive population persistence. However, because extreme events are uncommon, their effects on population dynamics of expanding species are poorly known. We examined how extreme climate events in winter and summer affected three populations of wild turkeys occupying a natural climate gradient at the northern edge of their range. First, we examined the mechanism by which vital rates affect the population growth rate. Second, we developed a climate-dependent structured population model. Finally, by linking this population model to IPCC-class climate projections, we projected wild turkey population abundance in response to the frequency of extreme snow events by 2100 for the northernmost population. We showed that the population dynamics of the three populations is driven through different pathways expected from the theory of invading population dynamics; that those populations were mainly limited by heavy snow that decreases winter survival by restraining food access; and that a population of immigrant is projected to decline at the northern species range. This study exemplifies how extreme events affect population dynamics and range expansion of temperate species at the northern edge of the distribution.

The call of the emperor penguin: Legal responses to species threatened by climate change.

Species extinction risk is accelerating due to anthropogenic climate change, making it urgent to protect vulnerable species through legal frameworks in order to facilitate conservation actions that help mitigate risk. Here, we discuss fundamental concepts for assessing climate change risks to species using the example of the emperor penguin (Aptenodytes forsteri), currently being considered for protection under the US Endangered Species Act (ESA). This species forms colonies on Antarctic sea ice, which is projected to significantly decline due to ongoing greenhouse gas (GHG) emissions. We project the dynamics of all known emperor penguin colonies under different GHG emission scenarios using a climate-dependent meta-population model including the effects of extreme climate events based on the observational satellite record of colonies. Assessments for listing species under the ESA require information about how species resiliency, redundancy and representation (3Rs) will be affected by threats within the foreseeable future. Our results show that if sea ice declines at the rate projected by climate models under current energy system trends and policies, the 3Rs would be dramatically reduced and almost all colonies would become quasi-extinct by 2100. We conclude that the species should be listed as threatened under the ESA.

Landfast ice: a major driver of reproductive success in a polar seabird.

In a fast-changing world, polar ecosystems are threatened by climate variability. Understanding the roles of fine-scale processes, and linear and nonlinear effects of climate factors on the demography of polar species is crucial for anticipating the future state of these fragile ecosystems. While the effects of sea ice on polar marine top predators are increasingly being studied, little is known about the impacts of landfast ice (LFI) on this species community. Based on a unique 39-year time series of satellite imagery and in situ meteorological conditions and on the world's longest dataset of emperor penguin (Aptenodytes forsteri) breeding parameters, we studied the effects of fine-scale variability of LFI and weather conditions on this species' reproductive success. We found that longer distances to the LFI edge (i.e. foraging areas) negatively affected the overall breeding success but also the fledging success. Climate window analyses suggested that chick mortality was particularly sensitive to LFI variability between August and November. Snowfall in May also affected hatching success. Given the sensitivity of LFI to storms and changes in wind direction, important future repercussions on the breeding habitat of emperor penguins are to be expected in the context of climate change.

Sea ice predicts long-term trends in Adélie penguin population growth, but not annual fluctuations: Results from a range-wide multiscale analysis.

Understanding the scales at which environmental variability affects populations is critical for projecting population dynamics and species distributions in rapidly changing environments. Here we used a multilevel Bayesian analysis of range-wide survey data for Adélie penguins to characterize multidecadal and annual effects of sea ice on population growth. We found that mean sea ice concentration at breeding colonies (i.e., "prevailing" environmental conditions) had robust nonlinear effects on multidecadal population trends and explained over 85% of the variance in mean population growth rates among sites. In contrast, despite considerable year-to-year fluctuations in abundance at most breeding colonies, annual sea ice fluctuations often explained less than 10% of the temporal variance in population growth rates. Our study provides an understanding of the spatially and temporally dynamic environmental factors that define the range limits of Adélie penguins, further establishing this iconic marine predator as a true sea ice obligate and providing a firm basis for projection under scenarios of future climate change. Yet, given the weak effects of annual sea ice relative to the large unexplained variance in year-to-year growth rates, the ability to generate useful short-term forecasts of Adélie penguin breeding abundance will be extremely limited. Our approach provides a powerful framework for linking short- and longer term population processes to environmental conditions that can be applied to any species, facilitating a richer understanding of ecological predictability and sensitivity to global change.

The Paris Agreement objectives will likely halt future declines of emperor penguins.

The Paris Agreement is a multinational initiative to combat climate change by keeping a global temperature increase in this century to 2°C above preindustrial levels while pursuing efforts to limit the increase to 1.5°C. Until recently, ensembles of coupled climate simulations producing temporal dynamics of climate en route to stable global mean temperature at 1.5 and 2°C above preindustrial levels were not available. Hence, the few studies that have assessed the ecological impact of the Paris Agreement used ad-hoc approaches. The development of new specific mitigation climate simulations now provides an unprecedented opportunity to inform ecological impact assessments. Here we project the dynamics of all known emperor penguin (Aptenodytes forsteri) colonies under new climate change scenarios meeting the Paris Agreement objectives using a climate-dependent-metapopulation model. Our model includes various dispersal behaviors so that penguins could modulate climate effects through movement and habitat selection. Under business-as-usual greenhouse gas emissions, we show that 80% of the colonies are projected to be quasiextinct by 2100, thus the total abundance of emperor penguins is projected to decline by at least 81% relative to its initial size, regardless of dispersal abilities. In contrast, if the Paris Agreement objectives are met, viable emperor penguin refuges will exist in Antarctica, and only 19% and 31% colonies are projected to be quasiextinct by 2100 under the Paris 1.5 and 2 climate scenarios respectively. As a result, the global population is projected to decline by at least by 31% under Paris 1.5 and 44% under Paris 2. However, population growth rates stabilize in 2060 such that the global population will be only declining at 0.07% under Paris 1.5 and 0.34% under Paris 2, thereby halting the global population decline. Hence, global climate policy has a larger capacity to safeguard the future of emperor penguins than their intrinsic dispersal abilities.

Climate change and functional traits affect population dynamics of a long-lived seabird.

Recent studies unravelled the effect of climate changes on populations through their impact on functional traits and demographic rates in terrestrial and freshwater ecosystems, but such understanding in marine ecosystems remains incomplete. Here, we evaluate the impact of the combined effects of climate and functional traits on population dynamics of a long-lived migratory seabird breeding in the southern ocean: the black-browed albatross (Thalassarche melanophris, BBA). We address the following prospective question: "Of all the changes in the climate and functional traits, which would produce the biggest impact on the BBA population growth rate?" We develop a structured matrix population model that includes the effect of climate and functional traits on the complete BBA life cycle. A detailed sensitivity analysis is conducted to understand the main pathway by which climate and functional trait changes affect the population growth rate. The population growth rate of BBA is driven by the combined effects of climate over various seasons and multiple functional traits with carry-over effects across seasons on demographic processes. Changes in sea surface temperature (SST) during late winter cause the biggest changes in the population growth rate, through their effect on juvenile survival. Adults appeared to respond to changes in winter climate conditions by adapting their migratory schedule rather than by modifying their at-sea foraging activity. However, the sensitivity of the population growth rate to SST affecting BBA migratory schedule is small. BBA foraging activity during the pre-breeding period has the biggest impact on population growth rate among functional traits. Finally, changes in SST during the breeding season have little effect on the population growth rate. These results highlight the importance of early life histories and carry-over effects of climate and functional traits on demographic rates across multiple seasons in population response to climate change. Robust conclusions about the roles of various phases of the life cycle and functional traits in population response to climate change rely on an understanding of the relationships of traits to demographic rates across the complete life cycle.

Multi-modal survey of Adélie penguin mega-colonies reveals the Danger Islands as a seabird hotspot.

Despite concerted international effort to track and interpret shifts in the abundance and distribution of Adélie penguins, large populations continue to be identified. Here we report on a major hotspot of Adélie penguin abundance identified in the Danger Islands off the northern tip of the Antarctic Peninsula (AP). We present the first complete census of Pygoscelis spp. penguins in the Danger Islands, estimated from a multi-modal survey consisting of direct ground counts and computer-automated counts of unmanned aerial vehicle (UAV) imagery. Our survey reveals that the Danger Islands host 751,527 pairs of Adélie penguins, more than the rest of AP region combined, and include the third and fourth largest Adélie penguin colonies in the world. Our results validate the use of Landsat medium-resolution satellite imagery for the detection of new or unknown penguin colonies and highlight the utility of combining satellite imagery with ground and UAV surveys. The Danger Islands appear to have avoided recent declines documented on the Western AP and, because they are large and likely to remain an important hotspot for avian abundance under projected climate change, deserve special consideration in the negotiation and design of Marine Protected Areas in the region.

Interacting effects of unobserved heterogeneity and individual stochasticity in the life history of the southern fulmar.

Individuals are heterogeneous in many ways. Some of these differences are incorporated as individual states (e.g. age, size, breeding status) in population models. However, substantial amounts of heterogeneity may remain unaccounted for, due to unmeasurable genetic, maternal or environmental factors. Such unobserved heterogeneity (UH) affects the behaviour of heterogeneous cohorts via intra-cohort selection and contributes to inter-individual variance in demographic outcomes such as longevity and lifetime reproduction. Variance is also produced by individual stochasticity, due to random events in the life cycle of wild organisms, yet no study thus far has attempted to decompose the variance in demographic outcomes into contributions from UH and individual stochasticity for an animal population in the wild. We developed a stage-classified matrix population model for the southern fulmar breeding on Ile des Pétrels, Antarctica. We applied multievent, multistate mark-recapture methods to estimate a finite mixture model accounting for UH in all vital rates and Markov chain methods to calculate demographic outcomes. Finally, we partitioned the variance in demographic outcomes into contributions from UH and individual stochasticity. We identify three UH groups, differing substantially in longevity, lifetime reproductive output, age at first reproduction and in the proportion of the life spent in each reproductive state. -14% of individuals at fledging have a delayed but high probability of recruitment and extended reproductive life span. -67% of individuals are less likely to reach adulthood, recruit late and skip breeding often but have the highest adult survival rate. -19% of individuals recruit early and attempt to breed often. They are likely to raise their offspring successfully, but experience a relatively short life span. Unobserved heterogeneity only explains a small fraction of the variances in longevity (5.9%), age at first reproduction (3.7%) and lifetime reproduction (22%). UH can affect the entire life cycle, including survival, development and reproductive rates, with consequences over the lifetime of individuals and impacts on cohort dynamics. The respective role of UH vs. individual stochasticity varies greatly among demographic outcomes. We discuss the implication of our finding for the gradient of life-history strategies observed among species and argue that individual differences should be accounted for in demographic studies of wild populations.