Wayne Z. Trivelpiece

Variability in krill biomass links harvesting and climate warming to penguin population changes in Antarctica

The West Antarctic Peninsula (WAP) and adjacent Scotia Sea support abundant wildlife populations, many of which were nearly extirpated by humans. This region is also among the fastest-warming areas on the planet, with 5–6 °C increases in mean winter air temperatures and associated decreases in winter sea-ice cover. These biological and physical perturbations have affected the ecosystem profoundly. One hypothesis guiding ecological interpretations of changes in top predator populations in this region, the “sea-ice hypothesis,” proposes that reductions in winter sea ice have led directly to declines in “ice-loving” species by decreasing their winter habitat, while populations of “ice-avoiding” species have increased. However, 30 y of field studies and recent surveys of penguins throughout the WAP and Scotia Sea demonstrate this mechanism is not controlling penguin populations; populations of both ice-loving Adélie and ice-avoiding chinstrap penguins have declined significantly. We argue in favor of an alternative, more robust hypothesis that attributes both increases and decreases in penguin populations to changes in the abundance of their main prey, Antarctic krill. Unlike many other predators in this region, Adélie and chinstrap penguins were never directly harvested by man; thus, their population trajectories track the impacts of biological and environmental changes in this ecosystem. Linking trends in penguin abundance with trends in krill biomass explains why populations of Adélie and chinstrap penguins increased after competitors (fur seals, baleen whales, and some fishes) were nearly extirpated in the 19th to mid-20th centuries and currently are decreasing in response to climate change.

Ecological Segregation of Adelie, Gentoo, and Chinstrap Penguins at King George Island, Antarctica

Ecological segregation among Adelie, Gentoo, and Chinstrap penguins dur- ing summer results from differences in breeding chronology, foraging behaviors, and life history tactics. To determine the importance of these factors in segregating the niches of the three species, we collected data on their population size, breeding success, breeding chronology, feeding frequency, and foraging range. Gentoo Penguins feed inshore and are deep divers. Their small populations probably reflect the comparatively large amount of food they need to rear chicks and the small foraging range that is dictated by short nest relief schedules and nonfasting behaviors. Their deep diving ability enables them to exploit a niche that is unavailable to their more abundant congeners. Adelie and Chinstrap penguins are shallow-diving, offshore foragers that avoid competition by differences in breeding chronology, prebreeder behaviors, and molting strategies. Adelie chicks fledge just as Chinstrap chicks reach creche age. Different migration times and molting locations further reduce niche overlap. The ultimate factors responsible for this trophic segregation may be unrelated to these proximate factors, however. Nonmigratory behavior, short nest reliefs, nonfasting, and slow growth of chicks may be adaptations to the mild conditions experienced by Gentoo Penguins in their sub-Antarctic range. The differences in Adelie and Chinstrap breeding time may reflect adaptation of Adelies to early breeding in the harsh, short summer of the continental Antarctic, and adaptation of Chinstraps to later breeding in the milder Maritime Antarctic. We found no evidence to suggest that the niches of the Pygoscelis penguins were influenced by competition for food, and suggest that adaptation to conditions in the center of their respective distributions is the primary cause affecting ecological segregation in areas of sympatry.

Divergent responses of Pygoscelis penguins reveal a common environmental driver

The responses of predators to environmental variability in the Antarctic Peninsula region have exhibited divergent patterns owing to variation in the geographic settings of colonies and predator life-history strategies. Five breeding colonies of Pygoscelis penguins from King George Island and Livingston Island, South Shetland Islands, Antarctica, were examined to (1) compare the responses of sympatric congeners to recent changes in their Antarctic ecosystem and (2) assess underlying causes for such responses. We used linear regression and correlation analyses to compare indices of abundance, recruitment, and summer breeding performance of the Adélie (P. adeliae), gentoo (P. papua), and chinstrap penguins (P. antarctica). Breeding colonies of Adélie and chinstrap penguins have declined by roughly 50% since the mid-1970s, and recruitment indices of Adélie penguins have declined by roughly 80%, but no such patterns are evident for gentoo penguins. Fledging success, however, has remained stable at all breeding colonies. The different trends in abundance and recruitment indices for each species, despite generally similar indices of summer performance, suggest that winter conditions contribute to the divergent responses among the penguins. In particular, strong correlations between indices of penguin and krill recruitment suggest that penguins in the South Shetland Islands may live under an increasingly krill-limited system that has disproportionate effects on the survival of juvenile birds.

Integrating Stomach Content and Stable Isotope Analyses to Quantify the Diets of Pygoscelid Penguins

Stomach content analysis (SCA) and more recently stable isotope analysis (SIA) integrated with isotopic mixing models have become common methods for dietary studies and provide insight into the foraging ecology of seabirds. However, both methods have drawbacks and biases that may result in difficulties in quantifying inter-annual and species-specific differences in diets. We used these two methods to simultaneously quantify the chick-rearing diet of Chinstrap (Pygoscelis antarctica) and Gentoo (P. papua) penguins and highlight methods of integrating SCA data to increase accuracy of diet composition estimates using SIA. SCA biomass estimates were highly variable and underestimated the importance of soft-bodied prey such as fish. Two-source, isotopic mixing model predictions were less variable and identified inter-annual and species-specific differences in the relative amounts of fish and krill in penguin diets not readily apparent using SCA. In contrast, multi-source isotopic mixing models had difficulty estimating the dietary contribution of fish species occupying similar trophic levels without refinement using SCA-derived otolith data. Overall, our ability to track inter-annual and species-specific differences in penguin diets using SIA was enhanced by integrating SCA data to isotopic mixing modes in three ways: 1) selecting appropriate prey sources, 2) weighting combinations of isotopically similar prey in two-source mixing models and 3) refining predicted contributions of isotopically similar prey in multi-source models.

Pollution, habitat loss, fishing, and climate change as critical threats to penguins

Cumulative human impacts across the worlds 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.

Spatial and isotopic niche partitioning during winter in chinstrap and Adélie penguins from the South Shetland Islands

Closely related species with similar ecological requirements should exhibit segregation along spatial, temporal, or trophic niche axes to limit the degree of competitive overlap. For migratory marine organisms like seabirds, assessing such overlap during the non-breeding period is difficult because of long-distance dispersal to potentially diffuse foraging habitats. Miniaturization of geolocation devices and advances in stable isotope analysis (SIA), however, provide a robust toolset to quantitatively track the movements and foraging niches of wide ranging marine animals throughout much of their annual cycle. We used light-based geolocation tags and analyzed stable carbon and nitrogen isotopes from tail feathers to simultaneously characterize winter movements, habitat utilization, and overlap of spatial and isotopic niches of migratory chinstrap (Pygoscelis antarctica) and Adelie (P. adeliae) penguins during the austral winter of 2012. Chinstrap penguins exhibited a higher diversity of movements and occup...

Abundance and spatial distribution of sympatrically breeding Catharacta spp. (skuas) in Admiralty Bay, King George Island, Antarctica

We examined the abundance and spatial distribution of sympatrically breeding skuas (Catharacta spp.) within Admiralty Bay, King George Island, Antarctica, during the austral summer of 2004/2005 in relation to spatial variables, which correspond to access to resources and nesting site safety and quality. We also compared the distribution and abundance of skua pairs observed in 2004/2005 to published skua census data from 1978/1979. Similar to previous studies, we found that brown skua (C. antarctica lonnbergi) pairs often nested in close proximity to penguin colonies and actively excluded other pair types from having direct access to penguin resources. In areas directly around penguin colonies, brown skua displace south polar skua (C. maccormicki) and other pair types, indirectly forcing them to nest in possibly lower quality territories, which are farther away from the coastline and in areas with lower incident solar radiation. When examining skua population trends, we discovered that the total number of breeding skuas in Admiralty Bay had increased by 293%, from 128 to 468 pairs, since 1978/1979. This dramatic increase was driven primarily by a tenfold increase in south polar skua pairs, as well as smaller increases in mixed and hybrid pairs. In contrast, there has been an overall decline (by 40%) in brown skua pairs during this same time, driven primarily by a large decrease in the breeding density of brown skua pairs in areas without penguin colonies.

Identifying Risk: Concurrent Overlap of the Antarctic Krill Fishery with Krill-Dependent Predators in the Scotia Sea

Mitigating direct and indirect interactions between marine predators and fisheries is a motivating factor for ecosystem-based fisheries management (EBFM), especially where predators and fisheries compete for a shared resource. One difficulty in advancing EBFM is parameterizing clear functional responses of predators to indices of prey availability. Alternative characterizations of fishery-predator interactions may therefore benefit the implementation of EBFM. Telemetry data identify foraging areas used by predators and, therefore, represent critical information to mitigate potential competition between predators and fisheries. We analyzed six years (2009–2014) of telemetry data collected at Cape Shirreff, Livingston Island and Admiralty Bay, King George Island, Antarctica, on three species of Pygoscelid penguins and female Antarctic fur seals. In this region, all four species are primarily dependent on Antarctic krill. The tracking data demonstrate local movements near breeding colonies during the austral summer and dispersal from breeding colonies during the winter. We then assessed overlap between predators and the Antarctic krill fishery on a suite of spatiotemporal scales to examine how different data aggregations affect the extent and location of overlap. Concurrent overlap was observed on all spatiotemporal scales considered throughout the Antarctic Peninsula and South Orkney Islands region, including near tagging locations and in distant areas where recent fishing activity has concentrated. Overlap occurred at depths where mean krill densities were relatively high. Our results demonstrate that direct overlap of krill-dependent predators with the krill fishery on small spatiotemporal scales is relatively common throughout the Antarctic Peninsula region. As the krill fishery continues to develop and efforts to implement ecosystem-based management mature, indices of overlap may provide a useful metric for indicating where the risks of fishing are highest. A precautionary approach to allocating krill catches in space would be to avoid large increases in catch where overlap on small spatiotemporal scales is common.

Flexibility in foraging strategies of Brown Skuas in response to local and seasonal dietary constraints

AbstractThe Brown Skua Stercorarius antarcticus lonnbergi is an opportunistic species that displays a high degree of flexibility in foraging tactics. We deployed global positioning system (GPS) and immersion (activity) loggers on breeding Brown Skuas of known sex, body size and condition at Admiralty Bay, King George Island with the aim to examine the impacts of spatial and seasonal fluctuations in prey availability on movement and foraging behavior. We also investigated whether reversed sexual size dimorphism (females larger than males) in this species leads to differences between sexes in foraging behavior and whether this or other factors contribute to variation in breeding success. Analysis of the GPS data highlighted the high degree of plasticity in foraging behavior among individuals. Although most Brown Skuas were flexible in their feeding tactics, this was not enough to ensure a successful breeding season, as few pairs fledged chicks. During early chick rearing, Brown Skuas spent most of their time on land, feeding almost exclusively on penguin chicks. By late chick rearing, when the availability of penguins had diminished, Brown Skuas supplemented the food obtained on land by traveling to the ocean. All foraging trips to sea occurred during daylight, mostly during the early morning. Despite marked sexual size dimorphism, we failed to find any difference in foraging tactics between males and females. Furthermore, although laying date affected the number of chicks hatched (earlier pairs were more successful), no relationship was found between breeding success and male or female body size, condition or degree of dimorphism within pairs.ZusammenfassungFlexible Nahrungsstrategien von Skuas als Reaktion auf lokale und saisonale Nahrungsengpässe Skuas Stercorarius antarcticus lonnbergi sind Opportunisten, die hoch flexibel sind in ihren Nahrungsstrategien. In der vorliegenden Studie, durchgeführt in der Admiralty Bay auf King George Island, wurden brütende Skuas mit bekanntem Geschlecht, Körpergröße und Kondition mit GPS- und Immersions- (Aktivitäts-) Datenloggern ausgestattet, um die Auswirkungen von räumlichen und saisonalen Fluktuationen in der Nahrungsverfügbarkeit auf das Bewegungs-und Nahrungssucheverhalten zu untersuchen. Außerdem wurde untersucht, ob der umgekehrte Sexualdimorphismus bezüglich der Körpergröße (Weibchen größer als Männchen) bei dieser Art zu Unterschieden zwischen den Geschlechtern im Nahrungssucheverhalten führt und ob dieser oder andere Faktoren zu Variationen im Bruterfolg beitragen. Die Analyse der GPS-Daten stellte einen hohen Grad an Plastizität im Nahrungssuchverhalten zwischen den Individuen heraus. Obwohl die meisten Skuas flexibel in ihren Fresstaktiken waren, sicherte dies nicht automatisch eine erfolgreiche Brutsaison, da nur wenige Paare Küken aufzogen. Während der frühen Phase der Kükenaufzucht verbrachten die Skuas die meiste Zeit an Land und erbeuteten nahezu ausnahmslos Pinguinküken. In der späten Phase der Kükenaufzucht, als die Verfügbarkeit von Pinguinen vermindert war, ergänzten die Skuas ihre Landnahrung durch Nahrungsflüge auf dem Ozean. Alle Nahrungsflüge auf dem Meer waren tagsüber, meistens am frühen Morgen. Trotz des ausgeprägten Geschlechtsdimorphismus in der Körpergröße konnten keine Unterschiede im Nahrungssuchverhalten zwischen Männchen und Weibchen gefunden werden. Und obwohl das Legedatum die Anzahl der geschlüpften Küken beeinflusste (frühe Paare waren erfolgreicher), konnte keine Abhängigkeit zwischen dem Bruterfolg und der Körpergröße und Kondition von Männchen und Weibchen oder dem Grad des Dimorphismus innerhalb der Paare nachgewiesen werden.

Differing foraging strategies influence mercury (Hg) exposure in an Antarctic penguin community

Seabirds are ideal model organisms to track mercury (Hg) through marine food webs as they are long-lived, broadly distributed, and are susceptible to biomagnification due to foraging at relatively high trophic levels. However, using these species as biomonitors requires a solid understanding of the degree of species, sexual and age-specific variation in foraging behaviors which act to mediate their dietary exposure to Hg. We combined stomach content analysis along with Hg and stable isotope analyses of blood, feathers and common prey items to help explain inter and intra-specific patterns of dietary Hg exposure across three sympatric Pygoscelis penguin species commonly used as biomonitors of Hg availability in the Antarctic marine ecosystem. We found that penguin tissue Hg concentrations differed across species, between adults and juveniles, but not between sexes. While all three penguins species diets were dominated by Antarctic krill (Euphausia superba) and to a lesser extent fish, stable isotope based proxies of relative trophic level and krill consumption could not by itself sufficiently explain the observed patterns of inter and intra-specific variation in Hg. However, integrating isotopic approaches with stomach content analysis allowed us to identify the relatively higher risk of Hg exposure for penguins foraging on mesopelagic prey relative to congeners targeting epipelagic or benthic prey species. When possible, future seabird biomonitoring studies should seek to combine isotopic approaches with other, independent measures of foraging behavior to better account for the confounding effects of inter and intra-specific variation on dietary Hg exposure.