Food, feeding ecology and ecological segregation of seabirds at South Georgia

At the sub-Antarctic island of South Georgia 25 of the 29 breeding species are seabirds. Fifteen of these have recently been studied in some detail. By examining the timing of their breeding seasons and their diet and feeding ecology (especially feeding techniques and potential foraging ranges), the nature of their ecological isolating mechanisms, and in particular the way in which they partition the resources of the marine environment, are reviewed.
Although breeding season adaptations occur (winter breeding in Wandering Albatross and King Penguin; out of phase breeding in two species-pairs of small petrels) these are less important than dillerences in food and feeding ecology. There is a fundamental distinction between the niche of pursuit-diving species (mainly penguins) and the remainder which are basically surface-feeders. The two abundant krill-eating penguins show clear differences in feeding zones. Three albatrosses and a petrel feed mainly on squid and there are differences in both the species and size of the prey of each. The remaining seabirds chiefly take krill (although the giant petrels are extensive scavengers and some smaller petrels specialize on copepods) and utilize different feeding methods and areas to do so.
Various adaptations related to inshore and offshore feeding zones are discussed. Although most species possess a combination of ecological isolating mechanisms additional evidence for the particular importance of dietary differences is presented.     

Ecological drivers of change at South Georgia: the krill surplus,or climate variability

Macaroni penguins Eudyptes chrysolophus are thought to be one of the most important mesopredators in the Southern Ocean having a greater impact on prey availability and abundance than any other seabird species. Their population centre has long been held to be South Georgia where populations were thought to comprise many million animals. Here we report the results of a recent census of the macaroni population at South Georgia undertaken using aerial survey methods. We report dramatic declines in numbers (～1.0 million breeding pairs) compared to numbers observed in the late 1970s (～5.4 million pairs), but show that these reductions have occurred principally at sites where numbers had previously been very large. During the breeding season, the main foraging grounds of birds from these sites overlap with the foraging grounds of Antarctic fur seals Arctocephalus gazella, a major competitor for their principal prey, Antarctic krill Euphausia superba. We suggest that the redistribution of the macaroni penguin population at South Georgia reflects the recent recovery of fur seal populations and thus the ongoing consequences of human intervention at South Georgia, a process which started more than 2 centuries previously. The implied resource competition and the observed population changes may also be exacerbated by recent reductions in Antarctic krill abundance which have been linked with reductions in seasonal sea ice following recent, rapid, regional warming in the Antarctic; however, the recovery of fur seal populations, and the ongoing recovery of krill‐eating whale populations argues that tropho‐dynamic interactions may be sufficient to explain the observed changes.     

Competition between the krill fishery and penguins in the South Shetland Islands

Among the South Shetland Islands, the potential competition for krill (Euphausia superba) between the Japanese fishery and krill-eating breeding penguins was assessed. A low level of competition was apparent due to several factors. Spatial overlap between the main fishing and foraging areas was insignificant. Firstly, the large colonies of the dominant penguin (chinstrap penguins,Pygoscelis antarctica) occurred where sea ice disappears early in spring, and not necessarily where krill are abundant in summer, i.e. the area of krill fishery. Secondly, overlap between trawling depth and foraging dive depth of penguins was marginal, with the latter depth being shallower. Moreover, overlap in the size-frequency of krill caught by trawlers and those captured by penguins was not complete; the penguins took larger krill on average. Finally, the present small fishery is unlikely to impact upon local krill biomass in the region. Krill biomass was estimated to be 250–1500 × 10³ tonnes within the preferred fishing areas during summer. The present catch rate by the fishery (≤13 × 10³ tonnes/half-month period) is smaller by an order of magnitude, and the fishing area does not include the main foraging areas of breeding penguins.     

南极Gerlache海峡海鸟的取食集群及食性

1997年12月至1998年2月,我们对南极半岛席尔瓦角善于飞翔海鸟与企鹅的取食关联性进行了研究,同时调查了取食集团中主要鸟种的食性.发现每个取食集团中有35.6-37.0只善于飞翔的海鸟,其中几乎都有纹颊企鹅群 (Pygoscelis antarctica),黑背鸥(Larus dominicanus)、灰贼鸥(Catharacta maccormicki)、花斑鹱(Daption capensis)和巨鹱(Macronectes giganteus)是各集团中最常见的鸟类.各取样单元内有相关性的种数随季节变化而减少,一些种类的减少与特定的物候期有关.南极磷虾(Euphausia superba)是绝大部分飞翔海鸟的主要食物,研究发现黑背鸥与纹颊企鹅所捕食的南极磷虾的大小最为接近.飞翔海鸟的觅食行为表明:在海面上短时停留的飞翔海鸟也能够成功捕捉到磷虾,这可能与磷虾躲避企鹅的捕食有关[动物学报 53(3):425-430,2007].     

Diet and reproductive success of Adélie and chinstrap penguins: linking response of predators to prey population dynamics

The diet and reproductive performance of two sympatric penguin species were studied at Signy Island, South Orkney Islands between 1997 and 2001. Each year, Adélie (Pygoscelis adeliae) and chinstrap (P. antarctica) penguins fed almost exclusively (>99% by mass) on Antarctic krill; however, there was considerable inter-annual variation in reproductive output. In 1998, chinstrap penguins were adversely affected by extensive sea-ice in the vicinity of the colony, whereas Adélie penguins were unaffected by this. However, in 2000, both species suffered reduced reproductive output. Detailed analysis of the population-size structure of krill in the diet indicated a lack of recruitment of small krill into the population since 1996. A simple model of krill growth and mortality indicated that the biomass represented by the last recruiting cohort would decline dramatically between 1999 and 2000. Thus, despite the lack of a change in the proportion of krill in the diet, the population demographics of the krill population suggested that the abundance of krill may have fallen below the level required to support normal breeding success of penguins sometime before or during the 2000 breeding season. The role of marine predators as indicator species is greatly enhanced when studies provide data reflecting not only the consequences of changes in the ecosystem but also those data that elucidate the causes of such changes.     

The fish diet of black-browed albatrossDiomedea melanophris and grey-headed albatrossD. Chrysostoma at South Georgia

 The fish component of the diet of black-browed and grey-headed albatrosses at South Georgia was investigated by intercepting 155 meals from adults arriving to feed chicks during February 1986 and 1994. Fish represented 30% and 72% by mass of the diet of black-browed albatrosses and 14% and 60% by mass of the diet of grey-headed albatrosses in 1986 and 1994 respectively. We determined the identity and quantified the contribution (by numbers, size and mass) of fish species mainly by using otoliths (54 representing 9 taxa and 57 representing 17 taxa in black-browed and grey-headed albatross samples respectively). For black-browed albatrosses in 1986 the main fish prey was Patagonotothen guntheri (77% of otoliths, 51% of estimated fish biomass) and a single large specimen of Icichthys australis (40% estimated biomass), whereas in 1994 Pseudochaenichthys georgianus was the main fish prey (57% of estimated biomass) with Magnisudis prionosa (30%) and Champsocephalus gunnari (12%) also making substantial contributions. Grey-headed albatross samples from 1986 were dominated by southern lampreys (40% by number, 79% of estimated biomass), lanternfish (32% of numbers, 9% by mass) and Patagonotothen guntheri (11% by mass); in 1994 Champsocephalus gunnari (42% by numbers, 24% by mass), Magnisudis prionosa (13% by number, 36% by mass), Muraenolepis microps (90% by number), Pseudochaenichthys georgianus (15% by mass) and lanternfish (18% by number but only 1% by mass) were the main prey. The importance of Patagonotothen guntheri to both species in 1986 and its absence in 1994 probably reflect albatrosses obtaining it from the commercial fishery, which was active in 1986 but closed in 1994. Otherwise the fish diet of black-browed albatrosses is dominated by krill-feeding fish, characteristic of the waters of the South Georgia shelf. In contrast, the grey-headed albatross diet comprises deeper water mesopelagic species, especially lanternfish, which reflect its affinity for the Antarctic Polar Frontal Zone and associated oceanic upwellings. Received: 28 June 1995 / Accepted: 8 October 1995     

Environmental response of upper trophic-level predators reveals a system change in an Antarctic marine ecosystem

Long-term changes in the physical environment in the Antarctic Peninsula region have significant potential for affecting populations of Antarctic krill (Euphausia superba), a keystone food web species. In order to investigate this, we analysed data on krill-eating predators at South Georgia from 1980 to 2000. Indices of population size and reproductive performance showed declines in all species and an increase in the frequency of years of low reproductive output. Changes in the population structure of krill and its relationship with reproductive performance suggested that the biomass of krill within the largest size class was sufficient to support predator demand in the 1980s but not in the 1990s. We suggest that the effects of underlying changes in the system on the krill population structure have been amplified by predator-induced mortality, resulting in breeding predators now regularly operating close to the limit of krill availability. Understanding how krill demography is affected by changes in physical environmental factors and by predator consumption and how, in turn, this influences predator performance and survival, is one of the keys to predicting future change in Antarctic marine ecosystems.     

The effects of prey demography on humpback whale (Megaptera novaeangliae) abundance around Anvers Island, Antarctica

Baleen whales and Adelie penguins in the near-shore waters around the Antarctic Peninsula forage principally on Antarctic krill. Given the spatial overlap in the distribution of these krill predators (particularly humpback whales) and their dependence on krill, the goals of this paper are to determine if the inter-annual community structure and relative abundance of baleen whales around Anvers Island is related to krill demography and abundance, and if the potential exists for inter-specific interactions between Adelie penguins and baleen. We use whale sightings and prey data from both net tows and Adelie penguin stomach samples to correlate the abundance of humpback whales with krill demography and abundance from 1993 to 2001. We find significant relationships between whale abundance and the size–frequency distribution of krill targeted by Adelie penguins, as well as the foraging success of Adelie penguins. These findings suggest both krill predators share common prey preferences in the upper portions of the water column around Anvers Island. These findings highlight the need for better knowledge of baleen whale foraging ecology and inter-specific interactions with penguins, as sea ice and krill populations around the Antarctic Peninsula are affected by rapid changes in climate.     

Proximity of krill and salps in an Antarctic coastal ecosystem: evidence from penguin-mounted cameras

Antarctic krill (Euphausia superba) and salps (mainly Salpa thompsoni) are main components of Southern Ocean ecosystem, but little is known about their coastal distribution at a fine scale (<1 km). We deployed miniaturised cameras on breeding chinstrap (n = 9 birds) and gentoo penguins (n = 9 birds) in the Antarctic Peninsula region and obtained 2,333 krill images, 93 salp images and 609 sea floor images from 1,843 dives. 51.2 % of penguin dives that had salps present in the images occurred near the dives with krill images (within 5 min). The vertical distribution of salp images showed overlap with the upper depth zone of krill images. While 16.3 % of dives with krill images were associated in time with the sea floor, only 1.2 % of dives with salp images did. These results revealed close proximity between krill and salps within the penguin’s foraging range in an Antarctic coastal ecosystem. These results also imply that krill patches were common in both pelagic and benthic habitat, whereas salps were common mainly in pelagic habitat. If the effects of deployments are similar between the years or regions, inter-annual or regional comparison using the penguin-mounted camera will be valid for characterising prey environment in the penguin foraging area.     

Adélie penguin survival: age structure,temporal variability and environmental influences

The driving factors of survival, a key demographic process, have been particularly challenging to study, especially for winter migratory species such as the Adélie penguin (Pygoscelis adeliae). While winter environmental conditions clearly influence Antarctic seabird survival, it has been unclear to which environmental features they are most likely to respond. Here, we examine the influence of environmental fluctuations, broad climatic conditions and the success of the breeding season prior to winter on annual survival of an Adélie penguin population using mark–recapture models based on penguin tag and resight data over a 16-year period. This analysis required an extension to the basic Cormack–Jolly–Seber model by incorporating age structure in recapture and survival sub-models. By including model covariates, we show that survival of older penguins is primarily related to the amount and concentration of ice present in their winter foraging grounds. In contrast, fledgling and yearling survival depended on other factors in addition to the physical marine environment and outcomes of the previous breeding season, but we were unable to determine what these were. The relationship between sea-ice and survival differed with penguin age: extensive ice during the return journey to breeding colonies was detrimental to survival for the younger penguins, whereas either too little or too much ice (between 15 and 80% cover) in the winter foraging grounds was detrimental for adults. Our results demonstrate that predictions of Adélie penguin survival can be improved by taking into account penguin age, prior breeding conditions and environmental features.     

Distribution and abundance of the tick Ixodes uriae in a diverse subantarctic seabird community

At Bird Island, South Georgia, we surveyed the distribution and abundance of ticks on the vertebrate fauna and found only 1 species Ixodes uriae. We classified all seabird species into 3 groups: (1) seabirds nesting on the surface of the ground solitarily, in dispersed groups of a few nests, or in colonies with well-spaced nests; (2) seabirds nesting on the surface of the ground in dense colonies; and (3) seabirds nesting in dense colonies in burrows or rock crevices. We detected I. uriae only on 3 species of the second group that nested in large, dense, persistent colonies, i.e., black-browed albatross (Diomedea melanophrys), gray-headed albatross (Diomedea chrysostoma), and macaroni penguin (Eudyptes chrysolophus). Ticks were found on the undersides of the feet on albatrosses but not on the undersides of the feet on penguins. We hypothesize that the coarse pebble nests of penguins, combined with the fact that their young walk around more than albatross young, make the environment on the underside of penguin feet more harsh and hostile for ticks than the underside of albatross feet. Despite the great abundance of Antarctic fur seals (Arctocephalus gazella) on the island, we found no ticks on them.     

Penguins, fur seals, and fishing: prey requirements and potential competition in the South Shetland Islands, Antarctica

Antarctic and sub-Antarctic seabirds, marine mammals, and human fisheries concentrate their foraging efforts on a single species, Antarctic krill (Euphausiasuperba). Because these predators may have a significant effect on krill abundance, we estimated the energy and prey requirements of Adelie (Pygoscelisadeliae), chinstrap (Pygoscelisantarctica), and gentoo (Pygoscelispapua) penguins and female Antarctic fur seals (Arctocephalusgazella) breeding on the South Shetland Islands, Antarctica and compared these estimates with catch statistics from the Antarctic krill fishery. Published data on field metabolic rate, population size, diet, prey energy content, and metabolic efficiency were used to estimate prey requirements of these breeding, adult, land-based predators and their dependent offspring. Due to their large population size, chinstrap penguins were the most significant krill predators during the period examined, consuming an estimated 7.8 × 10⁸ kg krill, followed by Adelie penguins (3.1 × 10⁷ kg), gentoo penguins (1.2 × 10⁷ kg), and Antarctic fur seals (3.6 × 10⁶ kg). Total consumption of all land-based predators on the South Shetland Islands was estimated at 8.3 × 10⁸ kg krill. The commercial krill fishery harvest in the South Shetland Island region (1.0 × 10⁸ kg) was approximately 12% of this. Commercial harvest coincides seasonally and spatially with peak penguin and fur seal prey demands, and may affect prey availability to penguins and fur seals. This differs from the conclusions of Ichii et al. who asserted that the potential for competition between South Shetland predators and the commercial krill fishery is low. Received: 26 August 1997 / Accepted: 16 December 1997     

Warming effects in the western Antarctic Peninsula ecosystem: the role of population dynamic models for explaining and predicting penguin trends

The western Antarctica Peninsula and Scotia Sea ecosystems appear to be driven by complex links between climatic variables, primary productivity, krill and Avian predators. There are several studies reporting statistical relationships between climate, krill and Penguin population size. The Adélie (Pygoscelis adeliae), Chinstrap (P. antarctica) and Gentoo (P. papua) penguins appear to be influenced by interannual variability in sea-ice extent and krill biomass. In this paper we developed simple conceptual models to decipher the role of climate and krill fluctuations on the population dynamics of these three Pygoscelis penguin species inhabiting the Antarctic Peninsula region. Our results suggest that the relevant processes underlying the population dynamics of these penguin species at King George Island (South Shetland Islands) are intra-specific competition and the combined effects of krill abundance and sea-ice cover. Our results using population theoretical models appear to support that climate change, specifically regional warming on the western Antarctic Peninsula, represents a major driver. At our study site, penguins showed species-specific responses to climate change. While Chinstrap penguins were only influenced by krill abundance, the contrasting population trends of Adélie and Gentoo penguins appear to be better explained by the “sea-ice hypothesis”. We think that proper population dynamic modeling and theory are essential for deciphering and proposing the ecological mechanisms underlying dynamics of these penguin populations.     

Comparative study of the effects of the late pack-ice break-off on chinstrap and Adélie penguins' diet and reproductive success at Laurie Island,South Orkney Islands,Antarctica

The effects of ice cover on diet and breeding chronology of Adélie (Pygoscelis adeliae) and chinstrap penguins (P. antarctica) were studied in the colonies located at Point Martin, South Orkney Islands. Reproductive success and diet parameters were measured as described in the CCAMLR Environmental Monitoring Program protocols. It was found that late pack-ice break-off in 1998 resulted in lower reproductive success than in 1999 for chinstrap penguins, while Adélie penguin parameters were rather insensitive. This species has shown to be able to cope with this environmental factor, as suggested by its circumpolar and more southerly range. Significant differences in stomach contents' weights and in the proportion of whole krill were found between ice-covered and open-sea periods within and between years. Foraging trips of both species became longer, resulting in underfeeding of chicks and nest desertion by chinstrap-penguin parents. Simultaneous analysis of reproductive parameters of both species and their diets have proven to be useful in discriminating between variation in reproductive success parameters due to prey accessibility and prey abundance.     

Food and feeding ecology of emperor penguins in the eastern Weddell Sea

Summary The diet of the emperor penguin Aptenodytes forsteri in the eastern Weddell Sea, Antarctica was studied during October and November 1986 by stomach content analysis. Emperor penguins fed mainly on Antarctic krill Euphausia superba, Antarctic silverfish Pleuragramma antarcticum and squid Psychroteuthis glacialis. Benthic prey was not found. The prey composition suggests two different feeding strategies, shallow dives exploring the rugged underside of sea ice where krill is taken, and deep dives when mesopelagic fish and squid are consumed. Chicks were fed on average every 1.44 days.     

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.     

Annual variation in breeding biology of macaroni penguins, Eudyptes chvysolophus, at Bird Island, South Georgia

The breeding biology of the macaroni penguin, Eudyptes chrysolophus , was studied over four years, 1976 and 1986–88, at Bird Island, South Georgia. Birds were migratory, being absent during winter (May to September). Arrival at the colony was highly synchronous between years: 14–23 October, over a 7-year period. The pre-breeding, incubation and chick-brooding period was characterized by long fasts ashore, for 36 and 39 days in males and 41 days in females, alternating with long periods at sea. Within years egg-laying was highly synchronous: 95% of clutches initiated within 4–6 days. Arrival date and mean egg-laying date were later (by 3 days), and breeding population size lower (by 20%) in 1987, compared to other years. The incubation period was 35 days and comprised three long shifts, the first shared by the male and female, the second by the female and the third by the male. In 1986 and 1988 these were of 12, 12 and 9 days' duration, but in 1987 the first shift was significantly shorter: 9 days. Chicks creched at 23–25 days of age and fledged at 60 days of age. Neither chick age nor weight at creching or fledging varied between the years 1986–88. The breeding biology of macaroni penguins at Bird Island is compared with that of other Eudyptes penguins, and with the sympatric gentoo penguin, Pygoscelispupuu. There is little variation in breeding biology within the genus Eudyptes , except in the length of time spent at sea prior to the annual moult. This is much shorter at Bird Island, probably reflecting a greater food availability compared to other localities. Inter-annual variation in certain breeding parameters, e.g. laying date, breeding population size, is much greater in the gentoo penguin than in the macaroni penguin. The shorter breeding season, rearing of only one chick and proportionately lower chick fledging weight in macaroni penguins, may be linked to this species' migratory strategy.     

First documentation of leopard seal predation of South Georgia pintail duck

Leopard seals are regular winter visitors to Bird Island, South Georgia, where they mostly prey on fur seals and penguins, and to a lesser extent on Antarctic krill and fish. Leopard seals can exploit many different species, but there are no records of predation on flying shorebirds in the wild. On 4 October 2008, an individually identified juvenile leopard seal female was observed killing and eating a South Georgia Pintail duck. It also preyed on Antarctic fur seals and gentoo and macaroni penguins during its 2-month temporary residency around the island. The varied diet of this seal exemplifies the generalist prey utilization typical of its species. Long-term diet studies at Bird Island and the published record suggest that predation on ducks is a rather exceptional finding; individual ducks are more likely to escape leopard seal attacks than penguins and provide a far less substantial ration. This note documents the first observation of this species of duck in the diet of leopard seals.     

Cycles of <Emphasis Type="Italic">Euphausia superba</Emphasis> recruitment evident in the diet of Pygoscelid penguins and net trawls in the South Shetland Islands,Antarctica

Size and sex of Antarctic krill taken from chinstrap and gentoo penguin diet were compared to those from scientific net surveys in the South Shetland Islands from 1998 to 2006 in order to evaluate penguin diet as a sampling mechanism and to look at trends in krill populations. Both penguin diet and net samples revealed a 4–5 year cycle in krill recruitment with one or two strong cohorts sustaining the population during each cycle. Penguin diet samples contained adult krill of similar lengths to those caught in nets; however, penguins rarely took juvenile krill. Penguin diet samples contained proportionately more females when the krill population was dominated by large adults at the end of the cycles; net samples showed greater proportions of males in these years. These patterns are comparable to those reported elsewhere in the region and are likely driven by the availability of different sizes and sexes of krill in relation to the colony.     

Long-term population trends in seven Antarctic seabirds at Pointe Géologie (Terre Adélie) Human impact compared with environmental change

Antarctic seabird populations have been much studied over the last decades as bioindicators of the nature of variability in the Southern Ocean marine ecosystem, and most attention has been focused on the role of food supply and the extent of sea ice. In addition, the rapid spread of tourism and the activities of researchers since the early 1960s have raised questions related to their real and potential impact on bird populations. Our data sets start in 1952 for several species of Antarctic seabirds and this study documents the trends over a 14-year period (1985–1999) in seven species breeding on Pointe Géologie archipelago (Terre Adélie, Antarctica). This is the first study where the direct impact of destruction of breeding sites (for building of an airstrip) is examined and where such long-term populations trends have been assessed in such a number of Antarctic species at one site. Trends from 1985 show that for the whole archipelago and when excluding islands destroyed, Adélie penguins and south polar skuas were the only species to show a significant increase (>3.5% annual change). The others species showed opposite trends, three increasing slightly (southern fulmars +0.4%, cape petrels +2.3%, snow petrels +0.9%) and two decreasing (emperor penguin −0.9%, southern giant petrel −3.9%). Three species particularly affected by the destruction of their breeding habitat (Adélie penguin, cape petrel, snow petrel) showed the capability to restore their populations. The availability of food and nesting sites is discussed in relation to environmental change. Species feeding on krill (Adélie penguins and cape petrels) increased more than other species; however, decrease of ice cover can increase availability of nesting sites. The importance of long-term studies is shown when assessing the role of human activities in Antarctica compared to larger-scale changes. Accepted: 18 September 2000