Krill body size drives particulate organic carbon export in West Antarctica.

The export of carbon from the ocean surface and storage in the ocean interior is important in the modulation of global climate1-4. The West Antarctic Peninsula experiences some of the largest summer particulate organic carbon (POC) export rates, and one of the fastest warming rates, in the world5,6. To understand how warming may alter carbon storage, it is necessary to first determine the patterns and ecological drivers of POC export7,8. Here we show that Antarctic krill (Euphausia superba) body size and life-history cycle, as opposed to their overall biomass or regional environmental factors, exert the dominant control on the POC flux. We measured POC fluxes over 21 years, the longest record in the Southern Ocean, and found a significant 5-year periodicity in the annual POC flux, which oscillated in synchrony with krill body size, peaking when the krill population was composed predominately of large individuals. Krill body size alters the POC flux through the production and export of size-varying faecal pellets9, which dominate the total flux. Decreases in winter sea ice10, an essential habitat for krill, are causing shifts in the krill population11, which may alter these export patterns of faecal pellets, leading to changes in ocean carbon storage.

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

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

Influence of migration range and foraging ecology on mercury accumulation in Southern Ocean penguins.

In order to evaluate mercury (Hg) accumulation patterns in Southern Ocean penguins, we measured Hg concentrations and carbon (δ13C) and nitrogen (δ15N) stable isotope ratios in body feathers of adult Adélie (Pygoscelis adeliae), gentoo (Pygoscelis papua), and chinstrap (Pygoscelis antarctica) penguins living near Anvers Island, West Antarctic Peninsula (WAP) collected in the 2010/2011 austral summer. With these and data from Pygoscelis and other penguin genera (Eudyptes and Aptenodytes) throughout the Southern Ocean, we modelled Hg variation using δ13C and δ15N values. Mean concentrations of Hg in feathers of Adélie (0.09 ± 0.05 µg g-1) and gentoo (0.16 ± 0.08 µg g-1) penguins from Anvers Island were among the lowest ever reported for the Southern Ocean. However, Hg concentrations in chinstrap penguins (0.80 ± 0.20 µg g-1), which undertake relatively broad longitudinal winter migrations north of expanding sea ice, were significantly higher (P < 0.001) than those in gentoo or Adélie penguins. δ13C and δ15N values for feathers from all three Anvers Island populations were also the lowest among those previously reported for Southern Ocean penguins foraging within Antarctic and subantarctic waters. These observations, along with size distributions of WAP krill, suggest foraging during non-breeding seasons as a primary contributor to higher Hg accumulation in chinstraps relative to other sympatric Pygoscelis along the WAP. δ13C values for all Southern Ocean penguin populations, alone best explained feather Hg concentrations among possible generalized linear models (GLMs) for populations grouped by either breeding site (AICc = 36.9, wi = 0.0590) or Antarctic Frontal Zone (AICc = 36.9, wi = 0.0537). Although Hg feather concentrations can vary locally by species, there was an insignificant species-level effect (wi < 0.001) across the full latitudinal range examined. Therefore, feeding ecology at breeding locations, as tracked by δ13C, control Hg accumulation in penguin populations across the Southern Ocean.

The interaction between island geomorphology and environmental parameters drives Adélie penguin breeding phenology on neighboring islands near Palmer Station, Antarctica.

Despite many studies on Adélie penguin breeding phenology, understanding the drivers of clutch initiation dates (CIDs, egg 1 lay date) is limited or lacks consensus. Here, we investigated Adélie penguin CIDs over 25 years (1991-2016) on two neighboring islands, Torgersen and Humble (<1 km apart), in a rapidly warming region near Palmer Station, Antarctica. We found that sea ice was the primary large-scale driver of CIDs and precipitation was a secondary small-scale driver that fine-tunes CID to island-specific nesting habitat geomorphology. In general, CIDs were earlier (later) when the spring sea ice retreat was earlier (later) and when the preceding annual ice season was shorter (longer). Island-specific effects related to precipitation and island geomorphology caused greater snow accumulation and delayed CIDs by ~2 days on Torgersen compared to Humble Island. When CIDs on the islands were similar, conditions were mild with less snow across breeding sites. At Torgersen Island, the negative relationship between CID and breeding success highlights detrimental effects of delayed breeding and/or snow on penguin fitness. Past phenological studies reported a relationship between air temperature and CID, assumed to be related to precipitation, but we found air temperature was more highly correlated to sea ice, revealing a misinterpretation of temperature effects. Finally, contrasting trends in CIDs based on temporal shifts in regional sea ice patterns revealed trends toward earlier CIDs (4-6 day advance) from 1979 to 2009 as the annual ice season shortened, and later CIDs (7-10 day delay) from 2010 to 2016 as the annual ice season lengthened. Adélie penguins tracked environmental conditions with flexible breeding phenology, but their life history remains vulnerable to subpolar weather conditions that can delay CIDs and decrease breeding success, especially on landscapes where geomorphology facilitates snow accumulation.

High latitude changes in ice dynamics and their impact on polar marine ecosystems.

Polar regions have experienced significant warming in recent decades. Warming has been most pronounced across the Arctic Ocean Basin and along the Antarctic Peninsula, with significant decreases in the extent and seasonal duration of sea ice. Rapid retreat of glaciers and disintegration of ice sheets have also been documented. The rate of warming is increasing and is predicted to continue well into the current century, with continued impacts on ice dynamics. Climate-mediated changes in ice dynamics are a concern as ice serves as primary habitat for marine organisms central to the food webs of these regions. Changes in the timing and extent of sea ice impose temporal asynchronies and spatial separations between energy requirements and food availability for many higher trophic levels. These mismatches lead to decreased reproductive success, lower abundances, and changes in distribution. In addition to these direct impacts of ice loss, climate-induced changes also facilitate indirect effects through changes in hydrography, which include introduction of species from lower latitudes and altered assemblages of primary producers. Here, we review recent changes and trends in ice dynamics and the responses of marine ecosystems. Specifically, we provide examples of ice-dependent organisms and associated species from the Arctic and Antarctic to illustrate the impacts of the temporal and spatial changes in ice dynamics.

Spatial niche partitioning may promote coexistence of Pygoscelis penguins as climate-induced sympatry occurs.

Climate-induced range overlap can result in novel interactions between similar species and potentially lead to competitive exclusion. The West Antarctic Peninsula (WAP) is one of the most rapidly warming regions on Earth and is experiencing a poleward climate migration from a polar to subpolar environment. This has resulted in a range expansion of the ice-intolerant gentoo penguins (Pygoscelis papua) and a coincident decrease in ice-obligate Adélie penguins (P. adeliae) near Palmer Station, Anvers Island, WAP. Ecologically similar species that share a limited prey resource must occupy disparate foraging niches in order to co-exist. Therefore, we determined the extent of foraging and dietary niche segregation between Adélie and gentoo penguins during the austral breeding season near Palmer Station. This research was conducted across six breeding seasons, from 2009 to 2014, which allowed us to investigate niche overlap in the context of interannual resource variability. Using biotelemetry and diet sampling, we found substantial overlap in the diets of Adélie and gentoo penguins, who primarily consumed Antarctic krill (Euphausia superba); however, our results showed that Adélie and gentoo penguins partitioned this shared prey resource through horizontal segregation of their core foraging areas. We did not find evidence that Antarctic krill were a limiting resource during the breeding season or that climate-induced sympatry of Adélie and gentoo penguins resulted in competition for prey or caused the subsequent differing population trajectories. This apparent absence of resource competition between Adélie and gentoo penguins throughout this study implies that current population trends in this region are governed by other biological and physical factors. Our results highlight the importance of understanding the mechanistic processes that influence top predator populations in the context of climate-driven ecosystem shifts.

Climate-driven sympatry may not lead to foraging competition between congeneric top-predators.

Climate-driven sympatry may lead to competition for food resources between species. Rapid warming in the West Antarctic Peninsula (WAP) is coincident with increasing gentoo penguin and decreasing Adélie penguin populations, suggesting that competition for food may exacerbate the Adélie penguin decline. On fine scales, we tested for foraging competition between these species during the chick-rearing period by comparing their foraging behaviors with the distribution of their prey, Antarctic krill. We detected krill aggregations within the horizontal and vertical foraging ranges of Adélie and gentoo penguins, and found that krill selected for habitats that balance the need to consume food and avoid predation. In overlapping Adélie and gentoo penguin foraging areas, four gentoo penguins switched foraging behavior by foraging at deeper depths, a strategy which limits competition with Adélie penguins. This suggests that climate-driven sympatry does not necessarily result in competitive exclusion of Adélie penguins by gentoo penguins. Contrary to a recent theory, which suggests that increased competition for krill is one of the major drivers of Adélie penguin population declines, we suggest that declines in Adélie penguins along the WAP are more likely due to direct and indirect climate impacts on their life histories.

Ecological sexual dimorphism and environmental variability within a community of antarctic penguins (Genus Pygoscelis).

BACKGROUND: Sexual segregation in vertebrate foraging niche is often associated with sexual size dimorphism (SSD), i.e., ecological sexual dimorphism. Although foraging behavior of male and female seabirds can vary markedly, differences in isotopic (carbon, δ13C and nitrogen, δ15N) foraging niche are generally more pronounced within sexually dimorphic species and during phases when competition for food is greater. We examined ecological sexual dimorphism among sympatric nesting Pygoscelis penguins asking whether environmental variability is associated with differences in male and female pre-breeding foraging niche. We predicted that all Pygoscelis species would forage sex-specifically, and that higher quality winter habitat, i.e., higher or lower sea ice coverage for a given species, would be associated with a more similar foraging niche among the sexes. RESULTS: P2/P8 primers reliably amplified DNA of all species. On average, male Pygoscelis penguins are structurally larger than female conspecifics. However, chinstrap penguins were more sexually dimorphic in culmen and flipper features than Adélie and gentoo penguins. Adélies and gentoos were more sexually dimorphic in body mass than chinstraps. Only male and female chinstraps and gentoos occupied separate δ15N foraging niches. Strong year effects in δ15N signatures were documented for all three species, however, only for Adélies, did yearly variation in δ15N signatures tightly correlate with winter sea ice conditions. There was no evidence that variation in sex-specific foraging niche interacted with yearly winter habitat quality. CONCLUSION: Chinstraps were most sexually size dimorphic followed by gentoos and Adélies. Pre-breeding sex-specific foraging niche was associated with overall SSD indices across species; male chinstrap and gentoo penguins were enriched in δ15N relative to females. Our results highlight previously unknown trophic pathways that link Pygoscelis penguins with variation in Southern Ocean sea ice suggesting that each sex within a species should respond similarly in pre-breeding trophic foraging to changes in future winter habitat.

Winter and spring controls on the summer food web of the coastal West Antarctic Peninsula.

Understanding the mechanisms by which climate variability affects multiple trophic levels in food webs is essential for determining ecosystem responses to climate change. Here we use over two decades of data collected by the Palmer Long Term Ecological Research program (PAL-LTER) to determine how large-scale climate and local physical forcing affect phytoplankton, zooplankton and an apex predator along the West Antarctic Peninsula (WAP). We show that positive anomalies in chlorophyll-a (chl-a) at Palmer Station, occurring every 4-6 years, are constrained by physical processes in the preceding winter/spring and a negative phase of the Southern Annular Mode (SAM). Favorable conditions for phytoplankton included increased winter ice extent and duration, reduced spring/summer winds, and increased water column stability via enhanced salinity-driven density gradients. Years of positive chl-a anomalies are associated with the initiation of a robust krill cohort the following summer, which is evident in Adélie penguin diets, thus demonstrating tight trophic coupling. Projected climate change in this region may have a significant, negative impact on phytoplankton biomass, krill recruitment and upper trophic level predators in this coastal Antarctic ecosystem.

Satellite data identify decadal trends in the quality of Pygoscelis penguin chick-rearing habitat.

Pygoscelis penguins are experiencing general population declines in their northernmost range whereas there are reported increases in their southernmost range. These changes are coincident with decadal-scale trends in remote sensed observations of sea ice concentrations (SIC) and sea surface temperatures (SST) during the chick-rearing season (austral summer). Using SIC, SST, and bathymetry, we identified separate chick-rearing niche spaces for the three Pygoscelis penguin species and used a maximum entropy approach (MaxEnt) to spatially and temporally model suitable chick-rearing habitats in the Southern Ocean. For all Pygoscelis penguin species, the MaxEnt models predict significant changes in the locations of suitable chick-rearing habitats over the period of 1982-2010. In general, chick-rearing habitat suitability at specific colony locations agreed with the corresponding increases or decreases in documented population trends over the same time period. These changes were the most pronounced along the West Antarctic Peninsula where there has been a rapid warming event during at least the last 50 years.

Autonomous gliders reveal features of the water column associated with foraging by adelie penguins.

Despite their strong dependence on the pelagic environment, seabirds and other top predators in polar marine ecosystems are generally studied during their reproductive phases in terrestrial environments. As a result, a significant portion of their life history is understudied which in turn has led to limited understanding. Recent advances in autonomous underwater vehicle (AUV) technologies have allowed satellite-tagged Adélie penguins to guide AUV surveys of the marine environment at the Palmer Long-Term Ecological Research (LTER) site on the western Antarctic Peninsula. Near real-time data sent via Iridium satellites from the AUVs to a centralized control center thousands of miles away allowed scientists to adapt AUV sampling strategies to meet the changing conditions of the subsurface. Such AUV data revealed the water masses and fine-scale features associated with Adélie penguin foraging trips. During this study, the maximum concentration of chlorophyll was between 30 and 50 m deep. Encompassing this peak in the chlorophyll concentration, within the water-column, was a mixture of nutrient-laden Upper Circumpolar Deep (UCDW) and western Antarctic Peninsula winter water (WW). Together, data from the AUV survey and penguin dives reveal that 54% of foraging by Adélie penguins occurs immediately below the chlorophyll maximum. These data demonstrate how bringing together emerging technologies, such as AUVs, with established methods such as the radio-tagging of penguins can provide powerful tools for monitoring and hypothesis testing of previously inaccessible ecological processes. Ocean and atmosphere temperatures are expected to continue increasing along the western Antarctic Peninsula, which will undoubtedly affect regional marine ecosystems. New and emerging technologies such as unmanned underwater vehicles and individually mounted satellite tracking devices will provide the tools critical to documenting and understanding the widespread ecological change expected in polar regions.

How do polar marine ecosystems respond to rapid climate change?

Climate change will alter marine ecosystems; however, the complexity of the food webs, combined with chronic undersampling, constrains efforts to predict their future and to optimally manage and protect marine resources. Sustained observations at the West Antarctic Peninsula show that in this region, rapid environmental change has coincided with shifts in the food web, from its base up to apex predators. New strategies will be required to gain further insight into how the marine climate system has influenced such changes and how it will do so in the future. Robotic networks, satellites, ships, and instruments mounted on animals and ice will collect data needed to improve numerical models that can then be used to study the future of polar ecosystems as climate change progresses.

Melting glaciers: a probable source of DDT to the Antarctic marine ecosystem.

Persistent organic pollutants reach polar regions by long-range atmospheric transport and biomagnify through the food web accumulating in higher trophic level predators. We analyzed Adélie penguin (Pygoscelis adeliae) samples collected from 2004 to 2006 to evaluate current levels of sigmaDDT (p,p'-DDT + p,p'-DDE) in these birds, which are confined to Antarctica. Ratios of p,p'-DDT to p,p'-DDE in Adélie penguins have declined significantly since 1964 indicating current exposure to old rather than new sources of sigmaDDT. However, sigmaDDT has not declined in Adélie penguins from the Western Antarctic Peninsula for more than 30 years and the presence of p,p'-DDT in these birds indicates that there is a current source of DDT to the Antarctic marine food web. DDT has been banned or severely restricted since peak use in the 1970s, implicating glacier meltwater as a likely source for DDT contamination in coastal Antarctic seas. Our estimates indicate that 1-4 kg x y(-1) sigmaDDT are currently being released into coastal waters along the Western Antarctic Ice Sheet due to glacier ablation.