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.

Genome-wide analyses reveal drivers of penguin diversification.

Penguins are the only extant family of flightless diving birds. They currently comprise at least 18 species, distributed from polar to tropical environments in the Southern Hemisphere. The history of their diversification and adaptation to these diverse environments remains controversial. We used 22 new genomes from 18 penguin species to reconstruct the order, timing, and location of their diversification, to track changes in their thermal niches through time, and to test for associated adaptation across the genome. Our results indicate that the penguin crown-group originated during the Miocene in New Zealand and Australia, not in Antarctica as previously thought, and that Aptenodytes is the sister group to all other extant penguin species. We show that lineage diversification in penguins was largely driven by changing climatic conditions and by the opening of the Drake Passage and associated intensification of the Antarctic Circumpolar Current (ACC). Penguin species have introgressed throughout much of their evolutionary history, following the direction of the ACC, which might have promoted dispersal and admixture. Changes in thermal niches were accompanied by adaptations in genes that govern thermoregulation and oxygen metabolism. Estimates of ancestral effective population sizes (Ne ) confirm that penguins are sensitive to climate shifts, as represented by three different demographic trajectories in deeper time, the most common (in 11 of 18 penguin species) being an increased Ne between 40 and 70 kya, followed by a precipitous decline during the Last Glacial Maximum. The latter effect is most likely a consequence of the overall decline in marine productivity following the last glaciation.

Selection-driven adaptation to the extreme Antarctic environment in the Emperor penguin.

The eco-evolutionary history of penguins is characterised by shifting from temperate to cold environments. Breeding in Antarctica, the Emperor penguin appears as an extreme outcome of this process, with unique features related to insulation, heat production and energy management. However, whether this species actually diverged from a less cold-adapted ancestor, more ecologically similar to its sister species, the King penguin, is still an open question. As the Antarctic colonisation likely resulted in vast changes in selective pressure experienced by the Emperor penguin, the relative quantification of the genomic signatures of selection, unique to each sister species, could answer this question. Applying phylogeny-based selection tests on 7651 orthologous genes, we identified a more pervasive selection shift in the Emperor penguin than in the King penguin, supporting the hypothesis that its extreme cold adaptation is a derived state. Furthermore, among candidate genes under selection, four (TRPM8, LEPR, CRB1, and SFI1) were identified before in other cold-adapted homeotherms, like the woolly Mammoth, while other 161 genes can be assigned to biological functions relevant to cold adaptation identified in previous studies. Location and structural effects of TRPM8 substitutions in Emperor and King penguin lineages support their functional role with putative divergent effects on thermal adaptation. We conclude that extreme cold adaptation in the Emperor penguin largely involved unique genetic options which, however, affect metabolic and physiological traits common to other cold-adapted homeotherms.

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

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

The early life of king penguins: ontogeny of dive capacity and foraging behaviour in an expert diver.

The period of emancipation in seabirds, when juveniles change from a terrestrial existence to a life at sea, is associated with many challenges. Apart from finding favourable foraging sites, they have to develop effective prey search patterns and physiological capacities that enable them to capture sufficient prey to meet their energetic needs. Animals that dive to forage, such as king penguins (Aptenodytes patagonicus), need to acquire an adequate breath-hold capacity, allowing them to locate and capture prey at depth. To investigate the ontogeny of their dive capacity and foraging performance, we implanted juvenile king penguins before their first departure to sea and also adult breeders with a data-logger recording pressure and temperature. We found that juvenile king penguins possess a remarkable dive capacity when leaving their natal colony, enabling them to conduct dives in excess of 100 m within their first week at sea. Despite this, juvenile dive/foraging performance, investigated in relation to dive depth, remained below the adult level throughout their first year at sea, probably reflecting physiological limitations as a result of incomplete maturation. A significantly shallower foraging depth of juveniles, particularly during their first 5 months at sea, could also indicate differences in foraging strategy and targeted prey. The initially greater wiggle rate suggests that juveniles fed opportunistically and also targeted different prey from adults and/or that many of the wiggles of juveniles reflect unsuccessful prey-capture attempts, indicating a lower foraging proficiency. After 5 months, this difference disappeared, suggesting sufficient physical maturation and improvement of juvenile foraging skills.

Vocal tract anatomy of king penguins: morphological traits of two-voiced sound production.

BACKGROUND: The astonishing variety of sounds that birds can produce has been the subject of many studies aiming to identify the underlying anatomical and physical mechanisms of sound production. An interesting feature of some bird vocalisations is the simultaneous production of two different frequencies. While most work has been focusing on songbirds, much less is known about dual-sound production in non-passerines, although their sound production organ, the syrinx, would technically allow many of them to produce "two voices". Here, we focus on the king penguin, a colonial seabird whose calls consist of two fundamental frequency bands and their respective harmonics. The calls are produced during courtship and for partner and offspring reunions and encode the birds' identity. We dissected, µCT-scanned and analysed the vocal tracts of six adult king penguins from Possession Island, Crozet Archipelago. RESULTS: King penguins possess a bronchial type syrinx that, similarly to the songbird's tracheobronchial syrinx, has two sets of vibratory tissues, and thus two separate sound sources. Left and right medial labium differ consistently in diameter between 0.5 and 3.2%, with no laterality between left and right side. The trachea has a conical shape, increasing in diameter from caudal to cranial by 16%. About 80% of the king penguins' trachea is medially divided by a septum consisting of soft elastic tissue (septum trachealis medialis). CONCLUSIONS: The king penguins' vocal tract appears to be mainly adapted to the life in a noisy colony of a species that relies on individual vocal recognition. The extent between the two voices encoding for individuality seems morphologically dictated by the length difference between left and right medial labium. The septum trachealis medialis might support this extent and could therefore be an important anatomical feature that aids in the individual recognition process.

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.

The dive performance of immature king penguins following their annual molt suggests physiological constraints.

Like all birds, penguins undergo periodic molt, during which they replace old feathers. However, unlike other birds, penguins replace their entire plumage within a short period while fasting ashore. During molt, king penguins (Aptenodytes patagonicus) lose half of their initial body mass, most importantly their insulating subcutaneous fat and half of their pectoral muscle mass. The latter might challenge their capacity to generate and sustain a sufficient mechanical power output to swim to distant food sources and propel themselves to great depth for successful prey capture. To investigate the effects of the annual molt fast on their dive/foraging performance, we studied various dive/foraging parameters and peripheral temperature patterns in immature king penguins across two molt cycles, after birds had spent their first and second year at sea, using implanted data-loggers. We found that the dive/foraging performance of immature king penguins was significantly reduced during post-molt foraging trips. Dive and bottom duration for a given depth were shorter during post-molt and post-dive surface interval duration was longer, reducing overall dive efficiency and underwater foraging time. We attribute this decline to the severe physiological changes that birds undergo during their annual molt. Peripheral temperature patterns differed greatly between pre- and post-molt trips, indicating the loss of the insulating subcutaneous fat layer during molt. Peripheral perfusion, as inferred from peripheral temperature, was restricted to short periods at night during pre-molt but occurred throughout extended periods during post-molt, reflecting the need to rapidly deposit an insulating fat layer during the latter period.

Structural organisation and dynamics in king penguin colonies.

During breeding, king penguins do not build nests, however they show strong territorial behaviour and keep a pecking distance to neighbouring penguins. Penguin positions in breeding colonies are highly stable over weeks and appear regularly spaced, but thus far no quantitative analysis of the structural order inside a colony has been performed. In this study, we use the radial distribution function to analyse the spatial coordinates of penguin positions. Coordinates are obtained from aerial images of two colonies that were observed for several years. Our data demonstrate that the structural order in king penguin colonies resembles a 2-dimensional liquid of particles with a Lennard-Jones-type interaction potential. We verify this using a molecular dynamics simulation with thermally driven particles, whereby temperature corresponds to penguin movements, the energy well depth e of the attractive potential corresponds to the strength of the colony-forming behaviour, and the repulsive zone corresponds to the pecking radius. We can recapitulate the liquid disorder of the colony, as measured by the radial distribution function, when the particles have a temperature of several (1.4-10) ε/k B and a normally distributed repulsive radius. To account for the observation that penguin positions are stable over the entire breeding period, we hypothesize that the liquid disorder is quenched during the colony formation process. Quenching requires the temperature to fall considerably below 1 ε/k B, which corresponds to a glass transition, or the repulsion radius to exceed the distance between neighbouring penguins, which corresponds to a jamming transition. Video recordings of a breeding colony together with simulations suggest that quenching is achieved by a behavioural motility arrest akin to a glass transition. We suggest that a liquid disordered colony structure provides an ideal compromise between high density and high flexibility to respond to external disturbances that require a repositioning of penguins.

Rovers minimize human disturbance in research on wild animals.

Investigating wild animals while minimizing human disturbance remains an important methodological challenge. When approached by a remote-operated vehicle (rover) which can be equipped to make radio-frequency identifications, wild penguins had significantly lower and shorter stress responses (determined by heart rate and behavior) than when approached by humans. Upon immobilization, the rover-unlike humans-did not disorganize colony structure, and stress rapidly ceased. Thus, rovers can reduce human disturbance of wild animals and the resulting scientific bias.

Marked phylogeographic structure of Gentoo penguin reveals an ongoing diversification process along the Southern Ocean.

Two main hypotheses have been debated about the biogeography of the Southern Ocean: (1) the Antarctic Polar Front (APF), acting as a barrier between Antarctic and sub-Antarctic provinces, and (2) the Antarctic Circumpolar Current (ACC), promoting gene flow among sub-Antarctic areas. The Gentoo penguin is distributed throughout these two provinces, separated by the APF. We analyzed mtDNA (HVR1) and 12 microsatellite loci of 264 Gentoo penguins, Pygoscelis papua, from 12 colonies spanning from the Western Antarctic Peninsula and the South Shetland Islands (WAP) to the sub-Antarctic Islands (SAI). While low genetic structure was detected among WAP colonies (mtDNA ФST=0.037-0.133; microsatellite FST=0.009-0.063), high differentiation was found between all SAI and WAP populations (mtDNA ФST=0.678-0.930; microsatellite FST=0.110-0.290). These results suggest that contemporary dispersal around the Southern Ocean is very limited or absent. As predicted, the APF appears to be a significant biogeographical boundary for Gentoo penguin populations; however, the ACC does not promote connectivity in this species. Our data suggest demographic expansion in the WAP during the last glacial maximum (LGM, about 20kya), but stability in SAI. Phylogenetic analyses showed a deep divergence between populations from the WAP and those from the SAI. Therefore, taxonomy should be further revised. The Crozet Islands resulted as a basal clade (3.57Mya), followed by the Kerguelen Islands (2.32Mya) as well as a more recent divergence between the Falkland/Malvinas Islands and the WAP (1.27Mya). Historical isolation, local adaptation, and past climate scenarios of those Evolutionarily Significant Units may have led to different potentials to respond to climate changes.

Apparent changes in body insulation of juvenile king penguins suggest an energetic challenge during their early life at sea.

Little is known about the early life at sea of marine top predators, like deep-diving king penguins (Aptenodytes patagonicus), although this dispersal phase is probably a critical phase in their life. Apart from finding favourable foraging sites, they have to develop effective prey search patterns as well as physiological capacities that enable them to capture sufficient prey to meet their energetic needs. To investigate the ontogeny of their thermoregulatory responses at sea, we implanted 30 juvenile king penguins and 8 adult breeders with a small data logger that recorded pressure and subcutaneous temperature continuously for up to 2.5 years. We found important changes in the development of peripheral temperature patterns of foraging juvenile king penguins throughout their first year at sea. Peripheral temperature during foraging bouts fell to increasingly lower levels during the first 6 months at sea, after which it stabilized. Most importantly, these changes re-occurred during their second year at sea, after birds had fasted for ∼4 weeks on land during their second moult. Furthermore, similar peripheral temperature patterns were also present in adult birds during foraging trips throughout their breeding cycle. We suggest that rather than being a simple consequence of concurrent changes in dive effort or an indication of a physiological maturation process, these seasonal temperature changes mainly reflect differences in thermal insulation. Heat loss estimates for juveniles at sea were initially high but declined to approximately half after ∼6 months at sea, suggesting that juvenile king penguins face a strong energetic challenge during their early oceanic existence.

Reliability of flipper-banded penguins as indicators of climate change.

In 2007, the Intergovernmental Panel on Climate Change highlighted an urgent need to assess the responses of marine ecosystems to climate change. Because they lie in a high-latitude region, the Southern Ocean ecosystems are expected to be strongly affected by global warming. Using top predators of this highly productive ocean (such as penguins) as integrative indicators may help us assess the impacts of climate change on marine ecosystems. Yet most available information on penguin population dynamics is based on the controversial use of flipper banding. Although some reports have found the effects of flipper bands to be deleterious, some short-term (one-year) studies have concluded otherwise, resulting in the continuation of extensive banding schemes and the use of data sets thus collected to predict climate impact on natural populations. Here we show that banding of free-ranging king penguins (Aptenodytes patagonicus) impairs both survival and reproduction, ultimately affecting population growth rate. Over the course of a 10-year longitudinal study, banded birds produced 41% [corrected] fewer chicks and had a survival rate 16 percentage points [corrected] lower than non-banded birds, demonstrating a massive long-term impact of banding and thus refuting the assumption that birds will ultimately adapt to being banded. Indeed, banded birds still arrived later for breeding at the study site and had longer foraging trips even after 10 years. One of our major findings is that responses of flipper-banded penguins to climate variability (that is, changes in sea surface temperature and in the Southern Oscillation index) differ from those of non-banded birds. We show that only long-term investigations may allow an evaluation of the impact of flipper bands and that every major life-history trait can be affected, calling into question the banding schemes still going on. In addition, our understanding of the effects of climate change on marine ecosystems based on flipper-band data should be reconsidered.

King penguin demography since the last glaciation inferred from genome-wide data.

How natural climate cycles, such as past glacial/interglacial patterns, have shaped species distributions at the high-latitude regions of the Southern Hemisphere is still largely unclear. Here, we show how the post-glacial warming following the Last Glacial Maximum (ca 18 000 years ago), allowed the (re)colonization of the fragmented sub-Antarctic habitat by an upper-level marine predator, the king penguin Aptenodytes patagonicus. Using restriction site-associated DNA sequencing and standard mitochondrial data, we tested the behaviour of subsets of anonymous nuclear loci in inferring past demography through coalescent-based and allele frequency spectrum analyses. Our results show that the king penguin population breeding on Crozet archipelago steeply increased in size, closely following the Holocene warming recorded in the Epica Dome C ice core. The following population growth can be explained by a threshold model in which the ecological requirements of this species (year-round ice-free habitat for breeding and access to a major source of food such as the Antarctic Polar Front) were met on Crozet soon after the Pleistocene/Holocene climatic transition.

Remote sensing of emperor penguin abundance and breeding success.

Emperor penguins (Aptenodytes forsteri) are under increasing environmental pressure. Monitoring colony size and population trends of this Antarctic seabird relies primarily on satellite imagery recorded near the end of the breeding season, when light conditions levels are sufficient to capture images, but colony occupancy is highly variable. To correct population estimates for this variability, we develop a phenological model that can predict the number of breeding pairs and fledging chicks, as well as key phenological events such as arrival, hatching and foraging times, from as few as six data points from a single season. The ability to extrapolate occupancy from sparse data makes the model particularly useful for monitoring remotely sensed animal colonies where ground-based population estimates are rare or unavailable.

King penguins adjust their diving behaviour with age.

Increasing experience in long-lived species is fundamental to improving breeding success and ultimately individual fitness. Diving efficiency of marine animals is primarily determined by their physiological and mechanical characteristics. This efficiency may be apparent via examination of biomechanical performance (e.g. stroke frequency and amplitude, change in buoyancy or body angle, etc.), which itself may be modulated according to resource availability, particularly as a function of depth. We investigated how foraging and diving abilities vary with age in a long-lived seabird. During two breeding seasons, small accelerometers were deployed on young (5 year old) and older (8/9 year old) brooding king penguins (Aptenodytes patagonicus) at the Crozet Archipelago, Indian Ocean. We used partial dynamic body acceleration (PDBA) to quantify body movement during dive and estimate diving cost. During the initial part of the descent, older birds exerted more effort for a given speed but younger penguins worked harder in relation to performance at greater depths. Younger birds also worked harder per unit speed for virtually the whole of the ascent. We interpret these differences using a model that takes into account the upthrust and drag to which the birds are subjected during the dive. From this, we suggest that older birds inhale more at the surface but that an increase in the drag coefficient is the factor leading to the increased effort to swim at a given speed by the younger birds at greater depths. We propose that this higher drag may be the result of young birds adopting less hydrodynamic postures or less direct trajectories when swimming or even having a plumage in poorer condition.

No evidence of microplastic ingestion in emperor penguin chicks (Aptenodytes forsteri) from the Atka Bay colony (Dronning Maud Land, Antarctica).

Microplastic (<5 mm; MP) pollution has been an emerging threat for marine ecosystems around the globe with increasing evidence that even the world's most remote areas, including Antarctica, are no longer unaffected. Few studies however, have examined MP in Antarctic biota, and especially those from Antarctic regions with low human activity, meaning little is known about the extent to which biota are affected. The aim of this study was to investigate, for the first time, the occurrence of MP in the emperor penguin (Aptenodytes forsteri), the only penguin species breeding around Antarctica during the austral winter, and an endemic apex predator in the Southern Ocean. To assess MP ingestion, the gizzards of 41 emperor penguin chicks from Atka Bay colony (Dronning Maud Land, Antarctica), were dissected and analyzed for MP >500 µm using Attenuated Total Reflection Fourier-transform Infrared (ATR-FTIR) spectroscopy. A total of 85 putative particles, mostly in the shape of fibers (65.9 %), were sorted. However, none of the particles were identified as MP applying state-of-the-art methodology. Sorted fibers were further evidenced to originate from contamination during sample processing and analyses. We find that MP concentrations in the local food web of the Weddell Sea and Dronning Maud Land coastal and marginal sea-ice regions; the feeding grounds to chick-rearing emperor penguin adults, are currently at such low levels that no detectable biomagnification is occurring via trophic transfer. Being in contrast to MP studies on other Antarctic and sub-Antarctic penguin species, our comparative discussion including these studies, highlights the importance for standardized procedures for sampling, sample processing and analyses to obtain comparable results. We further discuss other stomach contents and their potential role for MP detection, as well as providing a baseline for the long-term monitoring of MP in apex predator species from this region.

Biologging of emperor penguins-Attachment techniques and associated deployment performance.

An increasing number of marine animals are equipped with biologgers, to study their physiology, behaviour and ecology, often for conservation purposes. To minimise the impacts of biologgers on the animals' welfare, the Refinement principle from the Three Rs framework (Replacement, Reduction, Refinement) urges to continuously test and evaluate new and updated biologging protocols. Here, we propose alternative and promising techniques for emperor penguin (Aptenodytes forsteri) capture and on-site logger deployment that aim to mitigate the potential negative impacts of logger deployment on these birds. We equipped adult emperor penguins for short-term (GPS, Time-Depth Recorder (TDR)) and long-term (i.e. planned for one year) deployments (ARGOS platforms, TDR), as well as juvenile emperor penguins for long-term deployments (ARGOS platforms) in the Weddell Sea area where they had not yet been studied. We describe and qualitatively evaluate our protocols for the attachment of biologgers on-site at the colony, the capture of the animals and the recovery of the devices after deployment. We report unprecedented recaptures of long-term equipped adult emperor penguins (50% of equipped individuals recaptured after 290 days). Our data demonstrate that the traditional technique of long-term attachment by gluing the biologgers directly to the back feathers causes excessive feather breakage and the loss of the devices after a few months. We therefore propose an alternative method of attachment for back-mounted devices. This technique led to successful year-round deployments on 37.5% of the equipped juveniles. Finally, we also disclose the first deployments of leg-bracelet mounted TDRs on emperor penguins. Our findings highlight the importance of monitoring potential impacts of biologger deployments on the animals and the need to continue to improve methods to minimize disturbance and enhance performance and results.

Juvenile emperor penguin range calls for extended conservation measures in the Southern Ocean.

To protect the unique and rich biodiversity of the Southern Ocean, conservation measures such as marine protected areas (MPAs) have been implemented. Currently, the establishment of several additional protection zones is being considered based on the known habitat distributions of key species of the ecosystems including emperor penguins and other marine top predators. However, the distribution of such species at sea is often insufficiently sampled. Specifically, current distribution models focus on the habitat range of adult animals and neglect that immatures and juveniles can inhabit different areas. By tracking eight juvenile emperor penguins in the Weddell Sea over 1 year and performing a meta-analysis including previously known data from other colonies, we show that conservation efforts in the Southern Ocean are insufficient for protecting this highly mobile species, and particularly its juveniles. We find that juveniles spend approximately 90% of their time outside the boundaries of proposed and existing MPAs, and that their distribution extends beyond (greater than 1500 km) the species' extent of occurrence as defined by the International Union for Conservation of Nature. Our data exemplify that strategic conservation plans for the emperor penguin and other long-lived ecologically important species should consider the dynamic habitat range of all age classes.

King penguin population threatened by Southern Ocean warming.

Seabirds are sensitive indicators of changes in marine ecosystems and might integrate and/or amplify the effects of climate forcing on lower levels in food chains. Current knowledge on the impact of climate changes on penguins is primarily based on Antarctic birds identified by using flipper bands. Although flipper bands have helped to answer many questions about penguin biology, they were shown in some penguin species to have a detrimental effect. Here, we present for a Subantarctic species, king penguin (Aptenodytes patagonicus), reliable results on the effect of climate on survival and breeding based on unbanded birds but instead marked by subcutaneous electronic tags. We show that warm events negatively affect both breeding success and adult survival of this seabird. However, the observed effect is complex because it affects penguins at several spatio/temporal levels. Breeding reveals an immediate response to forcing during warm phases of El Niño Southern Oscillation affecting food availability close to the colony. Conversely, adult survival decreases with a remote sea-surface temperature forcing (i.e., a 2-year lag warming taking place at the northern boundary of pack ice, their winter foraging place). We suggest that this time lag may be explained by the delay between the recruitment and abundance of their prey, adjusted to the particular 1-year breeding cycle of the king penguin. The derived population dynamic model suggests a 9% decline in adult survival for a 0.26 degrees C warming. Our findings suggest that king penguin populations are at heavy extinction risk under the current global warming predictions.