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.

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.

Gephyromycinifex aptenodytis gen. nov., sp. nov., isolated from gut of Antarctic emperor penguin Aptenodytes forsteri.

A novel actinobacterium NJES-13T was isolated from the gut of Antarctic emperor penguin Aptenodytes forsteri. The new isolate produces bioactive gephyromycin metabolites and exopolysaccharides (EPS). Cells were Gram-negative, motile with the peritrichous flagella, and with a faint layer of extracellular slime. Colonies were yellow when grown on marine agar, ISP1, 2, 4 and TSA media. The strain developed clusters of coccoid, and divided by binary fission in the early phase of growth. The cell clusters were gradually disrupted during the stationary phase and formed short rod-shape cells which were interconnected by viscous EPS showing a three-dimensional net-like morphology, and contained polyhydroxyalkanoates (PHA) granules inside the cells. Growth of strain NJES-13T was observed at 15-45 °C, at pH 6.0-9.0 with 0.5-9.0% (w/v) NaCl. The complete genomic size of strain NJES-13T was 3.45 Mb with a DNA G + C content of 67.0 mol%. The combined polyphasic taxonomic characterizations presented in this study unequivocally separated strain NJES-13T from all known genera in the family Dermatophilaceae. Thus, strain NJES-13T represents a novel species of a new genus, for which the name Gephyromycinifex aptenodytis gen. nov., and sp. nov. is proposed. The type strain is NJES-13T (= CCTCC 2019007T = KCTC 49281T). Genetic prediction of secondary metabolite biosynthesis revealed a 44.5 kb-long biosynthetic gene cluster (BGC) of type III polyketide synthase (PKS) as well as four other BGCs, indicating its great potential to produce novel bioactive metabolites derived from the gut microbiota of animals living in the extreme habitats in the Antarctica.

Isolation, Phylogenetic and Gephyromycin Metabolites Characterization of New Exopolysaccharides-Bearing Antarctic Actinobacterium from Feces of Emperor Penguin.

A new versatile actinobacterium designated as strain NJES-13 was isolated from the feces of the Antarctic emperor penguin. This new isolate was found to produce two active gephyromycin analogues and bioflocculanting exopolysaccharides (EPS) metabolites. Phylogenetic analysis based on pairwise comparison of 16S rRNA gene sequences showed that strain NJES-13 was closely related to Mobilicoccus pelagius Aji5-31T with a gene similarity of 95.9%, which was lower than the threshold value (98.65%) for novel species delineation. Additional phylogenomic calculations of the average nucleotide identity (ANI, 75.9-79.1%), average amino acid identity (AAI, 52.4-66.9%) and digital DNA-DNA hybridization (dDDH, 18.6-21.9%), along with the constructed phylogenomic tree based on the up-to-date bacterial core gene (UBCG) set from the bacterial genomes, unequivocally separated strain NJES-13 from its close relatives within the family Dermatophilaceae. Hence, it clearly indicated that strain NJES-13 represented a putative new actinobacterial species isolated from the gut microbiota of mammals inhabiting the Antarctic. The obtained complete genome of strain NJES-13 consisted of a circular 3.45 Mb chromosome with a DNA G+C content of 67.0 mol%. Furthering genome mining of strain NJES-13 showed the presence of five biosynthetic gene clusters (BGCs) including one type III PKS responsible for the biosynthesis of the core of gephyromycins, and a series of genes encoding for bacterial EPS biosynthesis. Thus, based on the combined phylogenetic and active metabolites characterization presented in this study, we confidently conclude that strain NJES-13 is a novel, fresh actinobacterial candidate to produce active gephyromycins and microbial bioflocculanting EPS, with potential pharmaceutical, environmental and biotechnological implications.

Population response of an apex Antarctic consumer to its prey and climate fluctuations.

A fundamental endeavor in population ecology is to identify the drivers of population dynamics. A few empirical studies included the effect of prey abundance when investigating simultaneously the effects of density-dependence and climate factors on marine top-predator population dynamics. Our aim was to unravel the mechanisms forcing population dynamics of an apex consumer seabird, the south polar skua, using long-term climatic and population time series of the consumer and its prey in Terre Adélie, Antarctica. Influences of density-dependence, climatic factors, and prey abundance with lag effects were tested on the breeding population dynamics with a Bayesian multi-model inference approach. We evidenced a negative trend in breeding population growth rate when density increased. Lagged effects of sea-ice concentration and air temperature in spring and a contemporary effect of prey resources were supported. Remarkably, results outline a reverse response of the south polar skua and one of its main preys to the same environmental factor (sea-ice concentration), suggesting a strong link between skua and penguin dynamics. The causal mechanisms may involve competition for food and space through territorial behavior as well as local climate and prey availability, which probably operate on breeding parameters (breeding propensity, breeding success, or recruitment) rather than on adult survival. Our results provide new insights on the relative importance of factors forcing the population dynamics of an apex consumer including density-dependence, local climate conditions, and direct and indirect effects of prey abundance.

Phase transitions in huddling emperor penguins.

Emperor penguins (Aptenodytes forsteri) are highly adapted to the harsh conditions of the Antarctic winter: they are able to fast for up to 134 days during breeding. To conserve energy, emperor penguins form tight groups (huddles), which is key for their reproductive success. The effect of different meteorological factors on the huddling behaviour, however, is not well understood. Using time-lapse image recordings of an emperor penguin colony, we show that huddling can be described as a phase transition from a fluid to a solid state. We use the colony density as order parameter, and an apparent temperature that is perceived by the penguins as the thermodynamic variable. We approximate the apparent temperature as a linear combination of four meteorological parameters: ambient temperature, wind speed, global radiation and relative humidity. We find a wind chill factor of -2.9 °C/(ms -1), a humidity chill factor of -0.5°C/% rel. humidity, and a solar radiation heating factor of 0.3 °C//(Wm 2). In the absence of wind, humidity and solar radiation, the phase transition temperature (50% huddling probability) is -48.2°C for the investigated time period (May 2014). We propose that higher phase transition temperatures indicate a shrinking thermal insulation and thus can serve as a proxy for lower energy reserves of the colony, integrating pre-breeding foraging success at sea and energy expenditure at land due to environmental conditions. As current global change is predicted to have strong detrimental effects on emperor penguins within the next decades, our approach may thus contribute towards an urgently needed long-term monitoring system for assessing colony health.

Hidden keys to survival: the type, density, pattern and functional role of emperor penguin body feathers.

Antarctic penguins survive some of the harshest conditions on the planet. Emperor penguins breed on the sea ice where temperatures drop below -40°C and forage in -1.8°C waters. Their ability to maintain 38°C body temperature in these conditions is due in large part to their feathered coat. Penguins have been reported to have the highest contour feather density of any bird, and both filoplumes and plumules (downy feathers) are reported absent in penguins. In studies modelling the heat transfer properties and the potential biomimetic applications of penguin plumage design, the insulative properties of penguin plumage have been attributed to the single afterfeather attached to contour feathers. This attribution of the afterfeather as the sole insulation component has been repeated in subsequent studies. Our results demonstrate the presence of both plumules and filoplumes in the penguin body plumage. The downy plumules are four times denser than afterfeathers and play a key, previously overlooked role in penguin survival. Our study also does not support the report that emperor penguins have the highest contour feather density.

Bottom-up effects drive the dynamic of an Antarctic seabird predator-prey system.

Understanding how populations respond to variability in environmental conditions and interspecific interactions is one of the biggest challenges of population ecology, particularly in the context of global change. Although many studies have investigated population responses to climate change, very few have explicitly integrated interspecific relationships when studying these responses. In this study, we aimed to understand the combined effects of interspecific interactions and environmental conditions on the demographic parameters of a prey-predator system of three sympatric seabird populations breeding in Antarctica: the south polar skua (Catharacta maccormicki) and its two main preys during the breeding season, the Adélie penguin (Pygoscelis adeliae) and the emperor penguin (Aptenodytes forsteri). We built a two-species integrated population model (IPM) with 31 years of capture-recapture and count data and provided a framework that made it possible to estimate the demographic parameters and abundance of a predator-prey system in a context where capture-recapture data were not available for one species. Our results showed that predator-prey interactions and local environmental conditions differentially affected south polar skuas depending on their breeding state of the previous year. Concerning prey-predator relationships, the number of Adélie penguin breeding pairs showed a positive effect on south polar skua survival and breeding probability, and the number of emperor penguin dead chicks showed a positive effect on the breeding success of south polar skuas. In contrast, there was no evidence for an effect of the number of south polar skuas on the demography of Adélie penguins. We also found an important impact of sea ice conditions on both the dynamics of south polar skuas and Adélie penguins. Our results suggest that this prey-predator system is mostly driven by bottom-up processes and local environmental conditions.

Regional Differences in the Diets of Adélie and Emperor Penguins in the Ross Sea, Antarctica.

To identify the dietary composition and characteristics of both Adélie (Pygoscelis adeliae) and Emperor (Aptenodytes forsteri) penguins at four breeding sites, we performed stable carbon (δ13C) and nitrogen (δ15N) isotope analysis of down samples taken from penguin chicks. Adélie Penguin chicks at Cape Hallett mostly fed on Antarctic krill (Euphausia superba; 65.5 ± 3.5%), a reflection of the prevalence of that species near Cape Hallett, and no significant differences were noted between 2017 and 2018. However, Adélie Penguin chicks at Inexpressible Island, located near Terra Nova Bay, fed on both Antarctic silverfish (Pleuragramma antarctica; 42.5%) and ice krill (Euphausia crystallorophias; 47%), reflecting the high biomass observed in Terra Nova Bay. Meanwhile, no significant difference was noted between the two breeding sites of the Emperor Penguin. Emperor Penguin chicks predominantly fed on Antarctic silverfish (74.5 ± 2.1%) at both breeding sites (Cape Washington and Coulman Island), suggesting that diet preference represents the main factor influencing Emperor Penguin foraging. In contrast, the diet of the Adélie Penguin reflects presumed regional differences in prey prevalence, as inferred from available survey data.

A Physio-Logging Journey: Heart Rates of the Emperor Penguin and Blue Whale.

Physio-logging has the potential to explore the processes that underlie the dive behavior and ecology of marine mammals and seabirds, as well as evaluate their adaptability to environmental change and other stressors. Regulation of heart rate lies at the core of the physiological processes that determine dive capacity and performance. The bio-logging of heart rate in unrestrained animals diving at sea was infeasible, even unimaginable in the mid-1970s. To provide a historical perspective, I review my 40-year experience in the development of heart rate physio-loggers and the evolution of a digital electrocardiogram (ECG) recorder that is still in use today. I highlight documentation of the ECG and the interpretation of heart rate profiles in the largest of avian and mammalian divers, the emperor penguin and blue whale.

Crozier's penguin: An object history of maritime and museum science.

In November 1843 John Cassidy, curator in the Belfast Museum received, perhaps rather dolefully, a collection of bird skins. The Museum was barely managing to cope with the constant flow of donations from the 'four quarters of the globe'. But the gift of bird skins could not be ignored. Sent by Captain Francis Crozier, recently returned from the British Antarctic Expedition, the bequest contained 150 species of Southern Ocean birds, including the remains of two immature 'great penguins'. Taking the one surviving specimen as a focal point, this paper compares and contrasts the ways in which Aptenodytes forsteri, or the emperor penguin, was differently scripted on board ship and in the museum. The lively interpretations and close encounters with emperor penguins on the ice and on board the two naval bomb vessels are set alongside the more constrained meanings and fleeting attention given to them in a metropolitan and a provincial museum.

The complete mitochondrial genome sequence of Emperor Penguins (Aptenodytes forsteri).

The emperor penguin (Aptenodytes forsteri) is the largest living species of penguin. Herein, we first reported the complete mitochondrial genome of emperor penguin. The mitochondrial genome is a circular molecule of 17 301 bp in length, consisting of 13 protein-coding genes, 22 tRNA genes, two rRNA, and one control region. To verify the accuracy and the utility of new determined mitogenome sequences, we constructed the species phylogenetic tree of emperor penguin together with 10 other closely species. This is the second complete mitochondrial genome of penguin, and this is going to be an important data to study mitochondrial evolution of birds.

Geochemical record of high emperor penguin populations during the Little Ice Age at Amanda Bay, Antarctica.

Emperor penguins (Aptenodytes forsteri) are sensitive to the Antarctic climate change because they breed on the fast sea ice. Studies of paleohistory for the emperor penguin are rare, due to the lack of archives on land. In this study, we obtained an emperor penguin ornithogenic sediment profile (PI) and performed geochronological, geochemical and stable isotope analyses on the sediments and feather remains. Two radiocarbon dates of penguin feathers in PI indicate that emperor penguins colonized Amanda Bay as early as CE 1540. By using the bio-elements (P, Se, Hg, Zn and Cd) in sediments and stable isotope values (δ(15)N and δ(13)C) in feathers, we inferred relative population size and dietary change of emperor penguins during the period of CE 1540-2008, respectively. An increase in population size with depleted N isotope ratios for emperor penguins on N island at Amanda Bay during the Little Ice Age (CE 1540-1866) was observed, suggesting that cold climate affected the penguin's breeding habitat, prey availability and thus their population and dietary composition.

Transport of nutrients and contaminants from ocean to island by emperor penguins from Amanda Bay, East Antarctic.

Penguins play important roles in the biogeochemical cycle between Antarctic Ocean and land ecosystems. The roles of emperor penguin Aptenodytes forsteri, however, are usually ignored because emperor penguin breeds in fast sea ice. In this study, we collected two sediment profiles (EPI and PI) from the N island near a large emperor penguin colony at Amanda Bay, East Antarctic and performed stable isotope and element analyses. The organic C/N ratios and carbon and nitrogen isotopes suggested an autochthonous source of organic materials for the sediments of EPI (C/N = 10.21 ± 0.28, n = 17; δ(13)C = -13.48 ± 0.50‰, δ(15)N = 8.35 ± 0.55‰, n = 4) and an allochthonous source of marine-derived organic materials for the sediments of PI (C/N = 6.15 ± 0.08, δ(13)C = -26.85 ± 0.11‰, δ(15)N = 21.21 ± 2.02‰, n = 20). The concentrations of total phosphorus (TP), selenium (Se), mercury (Hg) and zinc (Zn) in PI sediments were much higher than those in EPI, the concentration of copper (Cu) in PI was a little lower, and the concentration of element lead (Pb) showed no difference. As measured by the geoaccumulation indexes, Zn, TP, Hg and Se were from moderately to very strongly enriched in PI, relative to local mother rock, due to the guano input from juvenile emperor penguins. Because of its high trophic level and transfer efficiency, emperor penguin can transport a large amount of nutrients and contaminants from ocean to land even with a relatively small population, and its roles in the biogeochemical cycle between ocean and terrestrial environment should not be ignored.