Trade-off between aerobic performance and egg production in migratory macaroni penguins.

When successive stages of an organism's life-history overlap, conflicts and trade-offs can emerge due to competition among physiological pathways. For example, long periods of sustained locomotion in migrating birds are supported by the androgenic up-regulation of aerobic factors, such as new red blood cell production and hematocrit. However, towards the end of migration, many female birds begin up-regulating 17ß-estradiol (E2) to support vitellogenesis and egg production, but E2 secretion is known to have suppressive effects on red blood cell production (anti-erythropoiesis). We explored potential trade-offs between factors related to aerobic performance (hematocrit, reticulocyte index) and the expression of factors related to E2-mediated vitellogenesis (i.e. yolk precursor production) in female macaroni penguins (Eudyptes chrysolophus), a species in which the physiologies controlling egg production and migratory activity run simultaneously (e.g. females experience a migratory conflict). We collected blood samples from penguins immediately upon their return to the colony, prior to egg laying. Hematocrit was elevated when the penguins returned to the colony (50.05% ± 3.40 SD), which is similar to pre-laying values observed in other migratory bird species. Furthermore, mean reticulocyte levels were elevated (34.87% ± 2.34), which is the highest level yet recorded in birds. Similarly, both plasma vitellogenin and yolk-targeted very low density lipoprotein levels were upregulated (2.30 ± 0.06 µg Zn ml-1, and 9.70 ± 0.19 mmol l-1, respectively), indicating that penguins were reproductively active and producing eggs during migration and upon arrival on land. As predicted, a negative relationship between hematocrit and plasma vitellogenin was found, but we found no evidence to suggest that birds were experiencing reproductive anemia. Alternatively, we attribute the negative relationship to a hemodilution effect of yolk precursor secretion into circulation. It appears that female macaroni penguins are able to preserve hematocrit levels and new red blood cell production when migratory activity overlaps with reproductive processes.

Microplastics in gentoo penguins from the Antarctic region.

There is growing evidence that microplastic pollution (<5 mm in size) is now present in virtually all marine ecosystems, even in remote areas, such as the Arctic and the Antarctic. Microplastics have been found in water and sediments of the Antarctic but little is known of their ingestion by higher predators and mechanisms of their entry into Antarctic marine food webs. The goal of this study was to assess the occurrence of microplastics in a top predator, the gentoo penguin Pygoscelis papua from the Antarctic region (Bird Island, South Georgia and Signy Island, South Orkney Islands) and hence assess the potential for microplastic transfer through Antarctic marine food webs. To achieve this, the presence of microplastics in scats (as a proof of ingestion) was investigated to assess the viability of a non-invasive approach for microplastic analyses in Antarctic penguins. A total of 80 penguin scats were collected and any microplastics they contained were extracted. A total of 20% of penguin scats from both islands contained microplastics, consisting mainly of fibers and fragments with different sizes and polymer composition (mean abundance of microplastics: 0.23 ± 0.53 items individual-1 scat, comprising seven different polymers), which were lower values than those found for seabirds in other regions worldwide. No significant differences in microplastic numbers in penguin scats between the two regions were detected. These data highlight the need for further assessment of the levels of microplastics in this sensitive region of the planet, specifically studies on temporal trends and potential effects on penguins and other organisms in the Antarctic marine food web.

Full circumpolar migration ensures evolutionary unity in the Emperor penguin.

Defining reliable demographic models is essential to understand the threats of ongoing environmental change. Yet, in the most remote and threatened areas, models are often based on the survey of a single population, assuming stationarity and independence in population responses. This is the case for the Emperor penguin Aptenodytes forsteri, a flagship Antarctic species that may be at high risk continent-wide before 2100. Here, using genome-wide data from the whole Antarctic continent, we reveal that this top-predator is organized as one single global population with a shared demography since the late Quaternary. We refute the view of the local population as a relevant demographic unit, and highlight that (i) robust extinction risk estimations are only possible by including dispersal rates and (ii) colony-scaled population size is rather indicative of local stochastic events, whereas the species' response to global environmental change is likely to follow a shared evolutionary trajectory.

The significance of cephalopod beaks in marine ecology studies: Can we use beaks for DNA analyses and mercury contamination assessment?

Cephalopod beaks found in the diet of predators have been a major source of scientific information. In this study, we evaluated the usefulness of DNA and contaminants analysis (total mercury - T-Hg) in cephalopod beaks in order to assess their applicability as tools in marine ecology studies. We concluded that, when applying DNA techniques to cephalopod beaks from Antarctic squid species, when using flesh attached to those beaks, it was possible to obtain DNA and to successfully identify cephalopod species; DNA was not found on the beaks themselves. This study also showed that it is possible to obtain information on T-Hg concentrations in beaks: the T-Hg concentrations found in the beaks were 6 to 46 times lower than in the flesh of the same cephalopod species. More research on the relationships of mercury concentrations in cephalopod beaks (and other tissues), intra- and inter-specifically, are needed in the future.

Feathers as a Tool to Assess Mercury Contamination in Gentoo Penguins: Variations at the Individual Level.

Feathers have been widely used to assess mercury contamination in birds as they reflect metal concentrations accumulated between successive moult periods: they are also easy to sample and have minimum impact on the study birds. Moult is considered the major pathway for mercury excretion in seabirds. Penguins are widely believed to undergo a complete, annual moult during which they do not feed. As penguins lose all their feathers, they are expected to have a low individual-variability in feather mercury concentration as all feathers are formed simultaneously from the same somatic reserves. This assumption is central to penguin studies that use feathers to examine the annual or among-individual variation in mercury concentrations in penguins. To test this assumption, we measured the mercury concentrations in 3-5 body feathers of 52 gentoo penguins (Pygoscelis papua) breeding at Bird Island, South Georgia (54°S 38°W). Twenty-five percent of the penguins studied showed substantial within-individual variation in the amount of mercury in their feathers (Coefficient of Variation: 34.7-96.7%). This variation may be caused by differences in moult patterns among individuals within the population leading to different interpretations in the overall population. Further investigation is now needed to fully understand individual variation in penguins' moult.

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.

Emperors in hiding: when ice-breakers and satellites complement each other in Antarctic exploration.

Evaluating the demographic trends of marine top predators is critical to understanding the processes involved in the ongoing rapid changes in Antarctic ecosystems. However, the remoteness and logistical complexity of operating in Antarctica, especially during winter, make such an assessment difficult. Satellite imaging is increasingly recognised as a valuable method for remote animal population monitoring, yet its accuracy and reliability are still to be fully evaluated. We report here the first ground visit of an emperor penguin colony first discovered by satellite, but also the discovery of a second one not indicated by satellite survey at that time. Several successive remote surveys in this coastal region of East Antarctica, both before and after sudden local changes, had indeed only identified one colony. These two colonies (with a total of ca. 7,400 breeding pairs) are located near the Mertz Glacier in an area that underwent tremendous habitat change after the glacier tongue broke off in February 2010. Our findings therefore suggest that a satellite survey, although offering a major advance since it allows a global imaging of emperor penguin colonies, may miss certain colony locations when challenged by certain features of polar ecosystems, such as snow cover, evolving ice topology, and rapidly changing habitat. Moreover our survey shows that this large seabird has considerable potential for rapid adaptation to sudden habitat loss, as the colony detected in 2009 may have moved and settled on new breeding grounds. Overall, the ability of emperor penguin colonies to relocate following habitat modification underlines the continued need for a mix of remote sensing and field surveys (aerial photography and ground counts), especially in the less-frequented parts of Antarctica, to gain reliable knowledge about the population demography and dynamics of this flagship species of the Antarctic ecosystem.

Survival in macaroni penguins and the relative importance of different drivers: individual traits, predation pressure and environmental variability.

Understanding the demographic response of free-living animal populations to different drivers is the first step towards reliable prediction of population trends. Penguins have exhibited dramatic declines in population size, and many studies have linked this to bottom-up processes altering the abundance of prey species. The effects of individual traits have been considered to a lesser extent, and top-down regulation through predation has been largely overlooked due to the difficulties in empirically measuring this at sea where it usually occurs. For 10 years (2003-2012), macaroni penguins (Eudyptes chrysolophus) were marked with subcutaneous electronic transponder tags and re-encountered using an automated gateway system fitted at the entrance to the colony. We used multistate mark-recapture modelling to identify the different drivers influencing survival rates and a sensitivity analysis to assess their relative importance across different life stages. Survival rates were low and variable during the fledging year (mean = 0·33), increasing to much higher levels from age 1 onwards (mean = 0·89). We show that survival of macaroni penguins is driven by a combination of individual quality, top-down predation pressure and bottom-up environmental forces. The relative importance of these covariates was age specific. During the fledging year, survival rates were most sensitive to top-down predation pressure, followed by individual fledging mass, and finally bottom-up environmental effects. In contrast, birds older than 1 year showed a similar response to bottom-up environmental effects and top-down predation pressure. We infer from our results that macaroni penguins will most likely be negatively impacted by an increase in the local population size of giant petrels. Furthermore, this population is, at least in the short term, likely to be positively influenced by local warming. More broadly, our results highlight the importance of considering multiple causal effects across different life stages when examining the survival rates of seabirds.

Climate change and Southern Ocean ecosystems I: how changes in physical habitats directly affect marine biota.

Antarctic and Southern Ocean (ASO) marine ecosystems have been changing for at least the last 30 years, including in response to increasing ocean temperatures and changes in the extent and seasonality of sea ice; the magnitude and direction of these changes differ between regions around Antarctica that could see populations of the same species changing differently in different regions. This article reviews current and expected changes in ASO physical habitats in response to climate change. It then reviews how these changes may impact the autecology of marine biota of this polar region: microbes, zooplankton, salps, Antarctic krill, fish, cephalopods, marine mammals, seabirds, and benthos. The general prognosis for ASO marine habitats is for an overall warming and freshening, strengthening of westerly winds, with a potential pole-ward movement of those winds and the frontal systems, and an increase in ocean eddy activity. Many habitat parameters will have regionally specific changes, particularly relating to sea ice characteristics and seasonal dynamics. Lower trophic levels are expected to move south as the ocean conditions in which they are currently found move pole-ward. For Antarctic krill and finfish, the latitudinal breadth of their range will depend on their tolerance of warming oceans and changes to productivity. Ocean acidification is a concern not only for calcifying organisms but also for crustaceans such as Antarctic krill; it is also likely to be the most important change in benthic habitats over the coming century. For marine mammals and birds, the expected changes primarily relate to their flexibility in moving to alternative locations for food and the energetic cost of longer or more complex foraging trips for those that are bound to breeding colonies. Few species are sufficiently well studied to make comprehensive species-specific vulnerability assessments possible. Priorities for future work are discussed.

Post-fledging dispersal of king penguins (Aptenodytes patagonicus) from two breeding sites in the South Atlantic.

Most studies concerning the foraging ecology of marine vertebrates are limited to breeding adults, although other life history stages might comprise half the total population. For penguins, little is known about juvenile dispersal, a period when individuals may be susceptible to increased mortality given their naïve foraging behaviour. Therefore, we used satellite telemetry to study king penguin fledglings (n = 18) from two sites in the Southwest Atlantic in December 2007. The two sites differed with respect to climate and proximity to the Antarctic Polar Front (APF), a key oceanographic feature generally thought to be important for king penguin foraging success. Accordingly, birds from both sites foraged predominantly in the vicinity of the APF. Eight king penguins were tracked for periods greater than 120 days; seven of these (three from the Falkland Islands and four from South Georgia) migrated into the Pacific. Only one bird from the Falkland Islands moved into the Indian Ocean, visiting the northern limit of the winter pack-ice. Three others from the Falkland Islands migrated to the eastern coast of Tierra del Fuego before travelling south. Derived tracking parameters describing their migratory behaviour showed no significant differences between sites. Nevertheless, generalized linear habitat modelling revealed that juveniles from the Falkland Islands spent more time in comparatively shallow waters with low sea surface temperature, sea surface height and chlorophyll variability. Birds from South Georgia spent more time in deeper waters with low sea surface temperature and sea surface height, but high concentrations of chlorophyll. Our results indicate that inexperienced king penguins, irrespective of the location of their natal site in relation to the position of the APF, develop their foraging skills progressively over time, including specific adaptations to the environment around their prospective breeding site.

Emperor penguins breeding on iceshelves.

We describe a new breeding behaviour discovered in emperor penguins; utilizing satellite and aerial-survey observations four emperor penguin breeding colonies have been recorded as existing on ice-shelves. Emperors have previously been considered as a sea-ice obligate species, with 44 of the 46 colonies located on sea-ice (the other two small colonies are on land). Of the colonies found on ice-shelves, two are newly discovered, and these have been recorded on shelves every season that they have been observed, the other two have been recorded both on ice-shelves and sea-ice in different breeding seasons. We conduct two analyses; the first using synthetic aperture radar data to assess why the largest of the four colonies, for which we have most data, locates sometimes on the shelf and sometimes on the sea-ice, and find that in years where the sea-ice forms late, the colony relocates onto the ice-shelf. The second analysis uses a number of environmental variables to test the habitat marginality of all emperor penguin breeding sites. We find that three of the four colonies reported in this study are in the most northerly, warmest conditions where sea-ice is often sub-optimal. The emperor penguin's reliance on sea-ice as a breeding platform coupled with recent concerns over changed sea-ice patterns consequent on regional warming, has led to their designation as "near threatened" in the IUCN red list. Current climate models predict that future loss of sea-ice around the Antarctic coastline will negatively impact emperor numbers; recent estimates suggest a halving of the population by 2052. The discovery of this new breeding behaviour at marginal sites could mitigate some of the consequences of sea-ice loss; potential benefits and whether these are permanent or temporary need to be considered and understood before further attempts are made to predict the population trajectory of this iconic species.

Corticosterone predicts foraging behavior and parental care in macaroni penguins.

Corticosterone has received considerable attention as the principal hormonal mediator of allostasis or physiological stress in wild animals. More recently, it has also been implicated in the regulation of parental care in breeding birds, particularly with respect to individual variation in foraging behavior and provisioning effort. There is also evidence that prolactin can work either inversely or additively with corticosterone to achieve this. Here we test the hypothesis that endogenous corticosterone plays a key physiological role in the control of foraging behavior and parental care, using a combination of exogenous corticosterone treatment, time-depth telemetry, and physiological sampling of female macaroni penguins (Eudyptes chrysolophus) during the brood-guard period of chick rearing, while simultaneously monitoring patterns of prolactin secretion. Plasma corticosterone levels were significantly higher in females given exogenous implants relative to those receiving sham implants. Increased corticosterone levels were associated with significantly higher levels of foraging and diving activity and greater mass gain in implanted females. Elevated plasma corticosterone was also associated with an apparent fitness benefit in the form of increased chick mass. Plasma prolactin levels did not correlate with corticosterone levels at any time, nor was prolactin correlated with any measure of foraging behavior or parental care. Our results provide support for the corticosterone-adaptation hypothesis, which predicts that higher corticosterone levels support increased foraging activity and parental effort.

An emperor penguin population estimate: the first global, synoptic survey of a species from space.

Our aim was to estimate the population of emperor penguins (Aptenodytes fosteri) using a single synoptic survey. We examined the whole continental coastline of Antarctica using a combination of medium resolution and Very High Resolution (VHR) satellite imagery to identify emperor penguin colony locations. Where colonies were identified, VHR imagery was obtained in the 2009 breeding season. The remotely-sensed images were then analysed using a supervised classification method to separate penguins from snow, shadow and guano. Actual counts of penguins from eleven ground truthing sites were used to convert these classified areas into numbers of penguins using a robust regression algorithm.We found four new colonies and confirmed the location of three previously suspected sites giving a total number of emperor penguin breeding colonies of 46. We estimated the breeding population of emperor penguins at each colony during 2009 and provide a population estimate of ~238,000 breeding pairs (compared with the last previously published count of 135,000-175,000 pairs). Based on published values of the relationship between breeders and non-breeders, this translates to a total population of ~595,000 adult birds.There is a growing consensus in the literature that global and regional emperor penguin populations will be affected by changing climate, a driver thought to be critical to their future survival. However, a complete understanding is severely limited by the lack of detailed knowledge about much of their ecology, and importantly a poor understanding of their total breeding population. To address the second of these issues, our work now provides a comprehensive estimate of the total breeding population that can be used in future population models and will provide a baseline for long-term research.

Migratory carryover effects and endocrinological correlates of reproductive decisions and reproductive success in female albatrosses.

Physiological mechanisms mediating carryover effects, wherein events or activities occurring in one season, habitat, or life-history stage affect important processes in subsequent life-history stages, are largely unknown. The mechanism most commonly invoked to explain carryover effects from migration centres on the acquisition and utilization of resources (e.g. body mass, or individual 'condition'). However, other mechanisms are plausible, e.g. trade-offs reflecting conflict or incompatibility between physiological regulatory systems required for different activities or life-history stages (migration vs. reproduction). Here we show that in female black-browed albatrosses (Thalassarche melanophris) the decision to reproduce or to defer reproduction, made prior to their arrival at breeding colonies after long-distance migration, is associated with condition-related (body mass, hematocrit, hemoglobin concentrations) and hormonal (progesterone, testosterone, estrogen-dependent yolk precursors) traits. In contrast, reproductive success showed little association with condition but showed significant associations with the steroidogenic processes underlying follicle development. Specifically, success was determined by reproductive readiness via differences in steroid hormones and hormone-dependent traits. Successful albatrosses were characterized by high progesterone and high estradiol-dependent yolk precursor levels, whereas failed albatrosses had high testosterone and low yolk precursor levels. Results are discussed with reference to migratory carryover effects and how these can differentially affect the physiologies influencing reproductive decisions and reproductive success.

Seasonal patterns of prolactin and corticosterone secretion in an Antarctic seabird that moults during reproduction.

In avian species that have evolved life-history strategies wherein molt and breeding overlap, there are potential conflicts between the regulatory roles of baseline prolactin and corticosterone in parental care (positive) and moult (negative). We describe seasonal patterns of hormonal secretion, moult, and parental behaviour in sibling species of giant petrels (Macronectes spp.) which begin moult during the incubation/early chick-rearing stage of reproduction. With the exception of male Southern giant petrels (Macronectes giganteus), prolactin secretion and moult in Northern (Macronectes halli) and female Southern giant petrels conformed to those observed in all other avian species, with the initiation of moult coincident with decreases from peak prolactin levels. However, male Southern giant petrels began moulting early in incubation when prolactin was increasing and had not yet peaked, which suggests a requirement of prolactin for incubation behaviour and a dissociation of prolactin from moult. Corticosterone showed little seasonal variation and no relationship with moult. When comparing prolactin, corticosterone, and moult in failed vs. active breeders, we found that failed breeding enabled a more rapid down-regulation of prolactin, thus facilitating a more rapid moult. We present specific examples of the behavioural ecology of giant petrels which we conclude help mediate any potential hormonal conflicts between parental care and moult.

Responding to climate change: Adélie Penguins confront astronomical and ocean boundaries.

Long-distance migration enables many organisms to take advantage of lucrative breeding and feeding opportunities during summer at high latitudes and then to move to lower, more temperate latitudes for the remainder of the year. The latitudinal range of the Adélie Penguin (Pygoscelis adeliae) spans approximately 22 degrees. Penguins from northern colonies may not migrate, but due to the high latitude of Ross Island colonies, these penguins almost certainly undertake the longest migrations for the species. Previous work has suggested that Adélies require both pack ice and some ambient light at all times of year. Over a three-year period, which included winters of both extensive and reduced sea ice, we investigated characteristics of migratory routes and wintering locations of Adélie Penguins from two colonies of very different size on Ross Island, Ross Sea, the southernmost colonies for any penguin. We acquired data from 3-16 geolocation sensor tags (GLS) affixed to penguins each year at both Cape Royds and Cape Crozier in 2003-2005. Migrations averaged 12760 km, with the longest being 17 600 km, and were in part facilitated by pack ice movement. Trip distances varied annually, but not by colony. Penguins rarely traveled north of the main sea-ice pack, and used areas with high sea-ice concentration, ranging from 75% to 85%, about 500 km inward from the ice edge. They also used locations where there was some twilight (2-7 h with sun < 6 degrees below the horizon). We report the present Adélie Penguin migration pattern and conjecture on how it probably has changed over the past approximately 12000 years, as the West Antarctic Ice Sheet withdrew southward across the Ross Sea, a situation that no other Adélie Penguin population has had to confront. As sea ice extent in the Ross Sea sector decreases in the near future, as predicted by climate models, we can expect further changes in the migration patterns of the Ross Sea penguins.

A carryover effect of migration underlies individual variation in reproductive readiness and extreme egg size dimorphism in macaroni penguins.

Where life-history stages overlap, there is the potential for physiological conflicts that might be important in mediating carryover effects. However, our knowledge of the specific physiological mechanisms underlying carryover effects remains rudimentary, and specific examples remain rare. Here we show that female macaroni penguins (Eudyptes chrysolophus) initiate vitellogenesis and yolk formation while at sea during return migrations to breeding colonies; yolk formation takes approximately 16 days, but females lay only 7-14 days after their return. Once on land, Eudyptes penguins show a unique reproductive pattern of extreme egg size dimorphism in which the smaller, first-laid A-egg is 55%-75% of the size of the larger B-egg. We show that the degree of egg size dimorphism is inversely correlated with time between arrival and laying; that is, females that begin reproductive development well in advance of their return produce more dimorphic eggs. Furthermore, late-arriving females that produce the most dimorphic eggs have lower plasma levels of the yolk precursor vitellogenin on arrival; that is, they show lower reproductive "readiness." These data support the hypothesis that extreme egg size dimorphism in Eudyptes penguins is due to a physiological constraint imposed by a migratory carryover effect and argue against small A-eggs having a specific, adaptive function.

Getting long in the tooth: a strong positive correlation between canine size and heterozygosity in Antarctic fur seals Arctocephalus gazella.

Most studies of heterozygosity-fitness correlations (HFCs) in natural populations relate to fitness traits expressed early in life, whereas traits that are often more difficult to measure such as longevity and adult body size remain elusive. Teeth provide a window on an individual's life history, allowing the reliable estimation of both age and body size. Consequently, we collected paired upper canine teeth and tissue samples from 84 adult male Antarctic fur seals Arctocephalus gazella that died of natural causes at Bird Island, South Georgia. Tooth size is a good predictor of skull and body size both within and across taxa, and we similarly find a strong relationship with skull size in our species. In turn, tooth size is itself predicted strongly by genetic heterozygosity estimated using 9 microsatellites. With only 9 loci, the exact mechanisms involved remain unclear, although the observed pattern appears largely attributable to a small subset of loci, suggesting that associative overdominance rather than inbreeding depression provides the proximate mechanism. In addition, locating these markers in the dog genome reveals proximity to genes involved with fat metabolism and growth. Our study illustrates how canine teeth, and potentially other structures such as tympano-periotic bone, waxy inner earplugs, or otoliths, may be used to explore links between genetic variation and important life-history traits in free-ranging vertebrate populations.