Vultures of the seas: hyperacidic stomachs in wandering albatrosses as an adaptation to dispersed food resources, including fishery wastes

Animals are primarily limited by their capacity to acquire food, yet digestive performance also conditions energy acquisition, and ultimately fitness. Optimal foraging theory predicts that organisms feeding on patchy resources should maximize their food loads within each patch, and should digest these loads quickly to minimize travelling costs between food patches. We tested the prediction of high digestive performance in wandering albatrosses, which can ingest prey of up to 3 kg, and feed on highly dispersed food resources across the southern ocean. GPS-tracking of 40 wandering albatrosses from the Crozet archipelago during the incubation phase confirmed foraging movements of between 475-4705 km, which give birds access to a variety of prey, including fishery wastes. Moreover, using miniaturized, autonomous data recorders placed in the stomach of three birds, we performed the first-ever measurements of gastric pH and temperature in procellariformes. These revealed surprisingly low pH levels (average 1.50±0.13), markedly lower than in other seabirds, and comparable to those of vultures feeding on carrion. Such low stomach pH gives wandering albatrosses a strategic advantage since it allows them a rapid chemical breakdown of ingested food and therefore a rapid digestion. This is useful for feeding on patchy, natural prey, but also on fishery wastes, which might be an important additional food resource for wandering albatrosses.     

Breeding energetics and food requirements of gentoo penguins (Pygoscelis papua) at Heard and Macquarie Islands

The food and energy requirements of breeding gentoo penguins ( Pygoscelis papua ) were studied at Heard and Macquaric Islands by means of isotope turnover techniques.
The food consumption rates of chicks were measured at various stages of growth, providing estimates of the total food provided by adults to rear a chick to fledging.
The energy expenditures of attending adults were also measured at different stages of chick-rearing, allowing the total energy costs associated with breeding to be established for a pair of adults and at the population level on both islands. We estimate the total annual energy budget of a 6·2 kg breeding gentoo penguin to be 1517 MJ which is equivalent to the consumption of 292 kg prey.     

Modeling the marine resources consumed in raising a king penguin chick: an energetics approach

Accurate estimates of penguin energetics would represent an important contribution to our understanding of the trophodynamics of the Southern Ocean ecosystem and our ability to predict effects of environmental change on these species. We used the heart rate-rate of oxygen consumption technique to estimate rate of energy expenditure in adult king penguins raising a chick, in combination with data from the literature on changes in adult mass, chick energy requirements, and prey energy density. Our model estimated a variety of energetic costs and quantities of prey consumption related to raising a king penguin chick during the austral summer. The total energy requirements of a king penguin chick at the Crozet Archipelago from hatching until reaching a mass of 8 kg 90 d later is 271 MJ, representing the consumption of 38.4 kg of myctophid fish. A successfully breeding male requires 0.78 kg d(-1) of fish during the entirety of the incubation period and 1.14 kg d(-1) during the subsequent 90 d of chick rearing. Assuming the same energy requirements for females, the estimated 580,000 pairs of king penguins that breed successfully at Crozet each year, together with their chicks, consume a total of around 190,000 tons of fish during the incubation and summer rearing periods combined. If, due to depletion of fish stocks, the diet of breeders and chicks during the summer becomes identical to the typical diet of adults during the austral winter, the mass of prey required by both adults and chicks combined (where the chick still reaches 8 kg after 90 d) would increase by more than 25%.     

Comparative ecology of the six albatross species breeding on the Crozet Islands

Six species of albatrosses breed sympatrically at the Crozet Islands. The population size, masses and measurements of adults, nesting habitats and coloniality, laying, hatching and fledging dates, duration of incubation and brooding shifts are compared. The growth of chicks, diets and feeding methods of the six species are reviewed. Their distribution in the south Indian Ocean is described in relation to the feeding frequency of chicks. Various aspects of ecological isolation among the species are analysed. Overlaps exist in the timing of breeding in the small albatrosses and to a lesser extent in their diet. Differences in the foraging zones at sea appear to be the most important factor in reducing interspecific competition. It is shown that the effective division of resources results from a relative scarcity of resources around the Crozet Islands. Finally the close interrelationship between foraging strategy, breeding biology, diet, chick growth and breeding frequency in the small albatrosses is demonstrated.     

Origin, age, sex and breeding status of wandering albatrosses (Diomedea exulans), northern (Macronectes halli) and southern giant petrels (Macronectes giganteus) attending demersal longliners in Falkland Islands and Scotia Ridge waters, 2001–2005

A total of 547 sightings of 291 banded wandering albatrosses Diomedea exulans and 21 sightings of 14 banded giant petrels Macronectes spp. were made from toothfish longliners operating on the southern Patagonian Shelf during 2001–2005. This included 25% of the wandering albatrosses with Darvic bands that bred at Bird Island (South Georgia) during this period. Thirteen of the northern Macronectes halli and southern giant petrels Macronectes giganteus had been banded at South Georgia, and there was one sighting of a southern giant petrel from Argentina. Male and female wandering albatrosses of all age classes except young birds (<15 years old) were equally likely to attend longline vessels. Most sightings of all age classes were made during the incubation period and fewest during the brood period. Eighty-six percent of birds sighted had bred at least once before, with half currently breeding and half on sabbatical (i.e. between breeding attempts). Almost half of the wandering albatrosses were sighted on more than one occasion. The data confirms that the southern Patagonian shelf is an important foraging area for wandering albatrosses and northern and southern giant petrels, and that some individuals show consistent associations in multiple years with longline vessels fishing in the region.     

Extrapair paternities in black-browed Thalassarche melanophris, grey-headed T. chrysostoma and wandering albatrosses Diomedea exulans at South Georgia

Extrapair paternities (EPP) are relatively common in passerines, but rare in seabirds. Like most seabirds, albatrosses are long lived, form long-term pair bonds and require biparental care for chick-rearing. Microsatellite analyses of 327 chicks from black-browed Thalassarche melanophris , grey-headed T. chrysostoma and wandering albatrosses Diomedea exulans over two breeding seasons revealed the presence of EPP in all three species. Though EPP rates varied between species and years, up to 21% of offspring were the result of extrapair matings. Rates were highest in wandering albatrosses (6–21%) followed by grey-headed (3–10%) and black-browed (0–9%) albatrosses. EPP rates were lower in 1998 compared to 1999 in both black-browed and grey-headed albatrosses, whereas the reverse was true for wandering albatrosses. Interspecific differences in EPP rates may reflect differences in breeding phenology and sexual size dimorphism. Differences in timing and frequency of breeding may promote different opportunities for interactions with birds other than their normal partner. The different breeding habitat, dispersion and mate-attraction rituals in wandering albatross, together with the disparity in size between the sexes may also offer more scope for higher rates of EPP. Despite extensive sampling within each colony, we were unable to identify sires for many of the extrapair young; however males from other colonies were involved, raising interesting questions regarding the timing and nature of such events.     

Giant petrels as predators of albatross chicks

Giant petrels Macronectes spp. are not thought to be important predators of albatross chicks, although they are known to kill pre-fledging Thalassarche and Phoebetria albatrosses. We report the first records of predation of healthy great albatross Diomedea spp. chicks, killing wandering albatrosses D. exulans at night on sub-Antarctic Marion Island. Breeding success of this species has decreased markedly in the area where attacks occurred, suggesting that giant petrel predation events are a recent phenomenon. Mouse attacks on wandering albatross chicks may have contributed to the development of this hunting technique. We also report the first observations of giant petrel predation on pre-fledging grey-headed albatross T. chrysostoma chicks as well as additional records of sooty albatross P. fusca chicks being targeted. Only adult northern giant petrels M. halli have been confirmed to kill albatross chicks on Marion Island. Given the threatened status of wandering albatrosses, and the importance of Marion Island for this species, monitoring of their breeding success is necessary to assess whether the predation of chicks by giant petrels spreads around the island.     

Influence of adult breeding experience on growth and provisioning of Wandering Albatross Diomedea exulans chicks at South Georgia

For most seabirds, reproductive performance improves with age; in albatrosses this is thought not to be so (experience being acquired before starting breeding) but only one study (of chick growth in a single season at one site) has specifically addressed this. We compared the provisioning performance and growth rates of chicks of Wandering Albatrosses Diomedea exulans breeding for the first (IN), second and third (LE) and fourth or more times (EE) on Bird Island, South Georgia in the austral winters of 1996 and 1997. Eggs from EE adults were significantly heavier than the other two categories and these chicks had a greater mass and longer wings up to 160 days of age and longer culmen and tarsus up to 115 days old. However chicks from all categories fledged at the same average mass, size and age. No significant differences between categories in feeding frequency or meal size were detected but experienced adults made shorter long foraging trips and spent more time at the nest than less experienced birds. Adults that remained at the nest gave chicks smaller meals than those that left immediately after feeding the chick. Although provision of smaller but more frequent meals by experienced adults promotes more rapid chick growth, the resulting differences do not persist into the late chick-rearing period. Our results were very similar to those from Iles Crozet in the Indian Ocean, supporting the hypothesis that when Wandering Albatrosses start to breed they are fully competent foragers but that it takes a while, during early chick-rearing, for birds breeding for the first time to adapt to the additional demands of provisioning a chick.     

Effects of Climate Change and Fisheries Bycatch on Shy Albatross (Thalassarche cauta) in Southern Australia

The impacts of climate change on marine species are often compounded by other stressors that make direct attribution and prediction difficult. Shy albatrosses (Thalassarche cauta) breeding on Albatross Island, Tasmania, show an unusually restricted foraging range, allowing easier discrimination between the influence of non-climate stressors (fisheries bycatch) and environmental variation. Local environmental conditions (rainfall, air temperature, and sea-surface height, an indicator of upwelling) during the vulnerable chick-rearing stage, have been correlated with breeding success of shy albatrosses. We use an age-, stage- and sex-structured population model to explore potential relationships between local environmental factors and albatross breeding success while accounting for fisheries bycatch by trawl and longline fisheries. The model uses time-series of observed breeding population counts, breeding success, adult and juvenile survival rates and a bycatch mortality observation for trawl fishing to estimate fisheries catchability, environmental influence, natural mortality rate, density dependence, and productivity. Observed at-sea distributions for adult and juvenile birds were coupled with reported fishing effort to estimate vulnerability to incidental bycatch. The inclusion of rainfall, temperature and sea-surface height as explanatory variables for annual chick mortality rate was statistically significant. Global climate models predict little change in future local average rainfall, however, increases are forecast in both temperatures and upwelling, which are predicted to have detrimental and beneficial effects, respectively, on breeding success. The model shows that mitigation of at least 50% of present bycatch is required to offset losses due to future temperature changes, even if upwelling increases substantially. Our results highlight the benefits of using an integrated modeling approach, which uses available demographic as well as environmental data within a single estimation framework, to provide future predictions. Such predictions inform the development of management options in the face of climate change.     

Predator–prey interactions: why do larger albatrosses eat bigger squid?

The relationship between predator sizes and prey sizes is well documented for terrestrial but rarely for marine ecosystems. We show that wandering albatrosses, the biggest albatross species, feed on larger cephalopod prey than those consumed by smaller albatrosses (grey-headed and black-browed albatrosses). This reflects differences in timing of breeding, foraging ecology and their feeding methods. Wandering albatrosses breed later in the year, during the austral winter, than smaller albatrosses (therefore catching older squid) and forage most of the year in Antarctic open waters, sub-Antarctic, subtropical and tropical waters, overlapping minimally with the smaller albatrosses' foraging range while breeding. Also, wandering albatrosses mostly scavenge whereas smaller albatrosses feed more on live prey. Prey ecology may also play a key role because many squid species might experience post-spawning mortality during the austral winter, becoming easily available to wandering albatrosses. Spawning in winter can be linked to predator avoidance (i.e. reduction in mortality in winter by avoiding pelagic predators) and would allow squid larvae to develop and take advantage of the high productivity (i.e. Antarctic phytoplankton bloom) in spring and at the beginning of summer. Thus, aspects of prey and predator ecology may combine to generate observed differences in prey size.     

Piecing together the global population puzzle of wandering albatrosses: genetic analysis of the Amsterdam albatross Diomedea amsterdamensis

Wandering albatrosses have been subjected to numerous taxonomic revisions due to discoveries of new species, analyses of morphological data and, more recently, the inclusion of genetic data. The small population of albatrosses (170 individuals including 26 pairs breeding annually) on Amsterdam Island in the Indian Ocean, Diomedea amsterdamensis, has been given species status based on plumage and morphometrics, but genetic data published to date provide weak support and its specific status remains controversial for some authors. We used mitochondrial control region sequence data to elucidate the relationship of the Amsterdam albatross within the wandering albatross complex (Diomedea amsterdamensis, D. antipodensis, D. dabbenena and D. exulans). Three novel haplotypes were present in 35 individuals from Amsterdam Island, and were highly divergent (3.6–7.3%) from haplotypes found in the other three members of the wandering albatross complex. Low levels of genetic variation in Amsterdam albatross likely resulted, at least in part, from a population bottleneck. Geographic isolation in the wandering albatross complex is maintained by high natal philopatry. As Amsterdam Island is the only breeding ground for this critically endangered species, we strongly urge conservation efforts in the area, especially in relation to long line fisheries and other threats such as disease and introduced predators, and it be listed as a distinct species.     

Quantitative analysis of the use of discards from squid trawlers by Black-browed Albatrosses Diomedea melanophris in the vicinity of the Falkland Islands

In the past decade, a major trawl fishery for the squid Loligo gahi has developed in the vicinity of Beauchêne Island, an internationally important breeding site for the Black-browed Albatross Diomedea melanophris. The breeding season diet of this albatross in the Falklands and its use of discards generated by the Loligo fishery were investigated. Albatross chicks are fed extensively on commercially exploited species of squid and fish including Loligo gahi and southern blue whiting Micromesistius australis. The quantity of waste generated by the Loligo fishery amounts to c. 5% of the reported catch and just over 50% of this waste, mainly Loligo and nototheniid fish, is scavenged by adult Black-browed Albatrosses. The total quantity scavenged during the chick rearing period amounts to 1000–2000 tonnes per year. This is equivalent to 10–15% of the total food requirement of the breeding Black-browed Albatross population on Beauchene Island during the period when the fishery is operating. Although the Loligo fishery currently provides a significant quantity of food to these albatrosses, its net effect may be detrimental to them, as it is a much greater predator of Loligo stocks than the albatrosses are estimated to have been prior to the fishery's development.     

The breeding biology and population dynamics of King Penguins Aptenodytes patagonica on the Crozet Islands

Among King Penguins Aptenodytes patagonica at Possession Island, one of the Crozet Islands, the length of the moult period, pre-laying period, incubating and brooding shifts were highly variable according to the year and to the stage of the breeding season. The moulting period was shorter in late breeders than in early breeders. Only half of the birds which successfully reared a chick bred the following cycle, but late in the season. Almost all these late breeders were unsuccessful. The reasons for the high variability in the breeding pattern observed in this species between years, as well as between colonies and between individuals are discussed. Breeding success was on average 30.6% and survival during the first year at sea could reach 50%. The survival of adult birds has increased during the past 10 years from 90.7% to 95.2% per annum. Despite an almost biennial breeding frequency and a very high rate of chick loss during the winter fast, the King Penguin population of Possession Island has doubled between 1966 and 1985 due to a high survival rate of adult and immature birds. The increase during the last decade in adult survival and in adult and chick condition suggests that the population increase could be the result of an improvement in food availability.     

Effect of breeding performance on the distribution and activity budgets of a predominantly resident population of black‐browed albatrosses

Pelagic seabirds breeding at high latitudes generally split their annual cycle between reproduction, migration, and wintering. During the breeding season, they are constrained in their foraging range due to reproduction while during winter months, and they often undertake long‐distance migrations. Black‐browed albatrosses (Thalassarche melanophris) nesting in the Falkland archipelago remain within 700 km from their breeding colonies all year‐round and can therefore be considered as resident. Accordingly, at‐sea activity patterns are expected to be adjusted to the absence of migration. Likewise, breeding performance is expected to affect foraging, flying, and floating activities, as failed individuals are relieved from reproduction earlier than successful ones. Using geolocators coupled with a saltwater immersion sensor, we detailed the spatial distribution and temporal dynamics of at‐sea activity budgets of successful and failed breeding black‐browed albatrosses nesting in New Island, Falklands archipelago, over the breeding and subsequent nonbreeding season. The 90% monthly kernel distribution of failed and successful breeders suggested no spatial segregation. Both groups followed the same dynamics of foraging effort both during daylight and darkness all year, except during chick‐rearing, when successful breeders foraged more intensively. Failed and successful breeders started decreasing flying activities during daylight at the same time, 2–3 weeks after hatching period, but failed breeders reached their maximum floating activity during late chick‐rearing, 2 months before successful breeders. Moon cycle had a significant effect on activity budgets during darkness, with individuals generally more active during full moon. Our results highlight that successful breeders buffer potential reproductive costs during the nonbreeding season, and this provides a better understanding of how individuals adjust their spatial distribution and activity budgets according to their breeding performance in absence of migration.     

Age‐related variation in reproductive traits in the wandering albatross: evidence for terminal improvement following senescence

The processes driving age‐related variation in demographic rates are central to understanding population and evolutionary ecology. An increasing number of studies in wild vertebrates find evidence for improvements in reproductive performance traits in early adulthood, followed by senescent declines in later life. However, life history theory predicts that reproductive investment should increase with age as future survival prospects diminish, and that raised reproductive investment may have associated survival costs. These non‐mutually exclusive processes both predict an increase in breeding performance at the terminal breeding attempt. Here, we use a 30‐year study of wandering albatrosses (Diomedea exulans) to disentangle the processes underpinning age‐related variation in reproduction. Whilst highlighting the importance of breeding experience, we reveal senescent declines in performance are followed by a striking increase in breeding success and a key parental investment trait at the final breeding attempt.     

Breeding biology of the Light-mantled sooty albatross (Phoebetria palpebrata) at South Georgia

Aspects of the breeding biology of the Light-mantled sooty albatross Phoebetria palpebrata were studied at South Georgia. Its breeding distribution there is summarized and an annual breeding population of c. 5000 breeding pairs estiamted. Laying, hatching and fledgine dates are given, together with egg measurements and data on the duration of incubation and brooding shift. Chick growth in weight and wing length from hatching to fledging was followed in detail.
Breeding season adaptations of P. palpebrata are compared with those of the other three albatrosses at South Georgia. The slow chick growth of P. palpebrata results in a nestling period even longer than those of the two larger mollymawks and is attributable mainly to the lower frequency of feeding resulting from the highly pelagic existence of adult P. palpebrata .
Comparisons are made with other breeding populations and especially with that on Marion Island. This is basically very similar and differences in chick growth patters are suggested to relate to differences in diet and particulartly to the frequency with which chicks receive food.     

Comparison of methods for evaluating energy expenditure of incubating wandering albatrosses.

Measurements of incubation energetics can vary depending on the method used to measure metabolism of an incubating bird. Therefore, we evaluated the energy expenditure of six male and four female wandering albatrosses (Diomedea exulans Linnaeus) using doubly labeled water (DLW), the rate of mass loss, and estimates of metabolic water production derived from water influx rate (WIR). Incubation metabolic rates (IMR) determined with DLW (169+/-21 kJ x kg(-1) x d(-1) SD) were significantly lower than estimates derived from mass loss (277+/-46 kJ x kg(-1) x d(-1) SD) and WIR (males=289+/-60 kJ x kg(-1) x d(-1) vs. females=400+/-69 kJ x kg(-1) x d(-1) SD). Estimates of IMR from mass loss and WIR were similar to IMR (305+/-39 kJ x kg(-1) x d(-1) SD) determined by respirometry in a previous study, and IMR from DLW was similar to estimates based on heart rate (HR; 147+/-26 kJ x kg(-1) x d(-1) SD) determined in another study. Applying the different measurements of IMR to construct an energy budget, we estimate that a breeding pair of wandering albatrosses spends 124-234 MJ to incubate the egg for 78 d. Finally, IMRs determined with DLW and HR were similar to estimated basal metabolic rates derived from six different allometric equations, suggesting that heat production from adult maintenance metabolism is sufficient to incubate the egg.     

Seasonal changes in the provisioning behaviour and mass of male and female wandering albatrosses in relation to the growth of their chick

Procellariiform seabirds have a number of extreme life-history characteristics in common, in particular low reproductive rates and slow postnatal development, which are generally assumed to reflect the difficulty in acquiring energy in the marine environment. The wandering albatross (Diomedea exulans) is a sexually dimorphic species with the longest postnatal growth found in any bird, suggesting severe constraints on provisioning and possible sex-specific strategies of provisioning. We studied the provisioning behaviour and mass changes of male and female parent wandering albatross throughout the 9-months rearing period to examine how each sex adjusts its foraging effort in relation to the needs of the chicks and the seasonal changes in food availability. The study was carried out on the Crozet Islands, using an automated system recording continuously the attendance pattern of parents between March and December 1994. During the brooding period when energy requirements are highest, parents only perform trips of short duration to sea, and their body condition deteriorates. When the chick is old enough to be left alone, the parents mix short and long foraging trips. The proportion of short trips is very high until July, allowing high rate of food delivery and rapid growth, and at the same time the body condition of adults improves. From August this proportion declines until fledging in December. As a result, the feeding rate decreases from August and adult condition declines, suggesting that feeding conditions at sea are better during the first part of the chick-rearing period, i.e. in autumn and winter. Male parents perform more short trips of shorter duration and provide larger meals than females, delivering an estimated total after brooding of 110 kg of food, compared to 70–80 kg delivered by females. Meal size is inversely related to the body condition of male chicks but not to that of female chicks, suggesting that food delivery is regulated by the adults in response to the condition of the male chick. Male chicks received larger meals and more food every month than female chicks, and overall it was estimated that they receive, after brooding, 195 kg of food compared to 180 kg for the female. As a result, male chicks have a higher growth rate, attain a higher asymptotic mass, and are larger and heavier at fledging than female chicks. However, the differences are relatively small between the chicks of each sex and suggest that energy may be used differently between the sexes to maximise fitness. The results of the study suggest that provisioning effort of wandering albatrosses is adjusted by parents in relation to the availability of food, to the energetic needs of the chick and to the sex of the chick. The adult body mass is likely to play an important role in the long term for the regulation of provisioning, deficits in body mass probably providing the buffer in high power-requirement periods. Accepted: 20 March 2000     

The effect of parental age,experience and historical reproductive success on wandering albatross (Diomedea exulans) chick growth and survival

Growth and survival of altricial young are influenced by their parents’ abilities to invest in a breeding attempt. As a result, chick growth and survival in one breeding season may be indicative of their parents’ long-term reproductive potential. To determine whether variation in long-term reproductive success is driven by differential breeding investment, parental care and chick growth in wandering albatrosses (Diomedea exulans) were correlated with parental historical reproductive success. Effects of age and breeding experience (determined from past breeding attempts) and pre-laying body condition (mass–size indices) on chick growth and survival also were tested. Longer brooding of chicks increased their survival, but length of chick brooding did not differ between historically unproductive and successful breeders. Past reproductive success also was not correlated with chick growth rates or fledging mass or size. Chick brooding period, chick growth rates, final mass and size were independent of parental body condition. Older and more experienced parents brooded chicks for longer and their chicks grew faster, supporting previous findings that breeding competence is a learnt skill. Chick care and growth characteristics differed more between than within pairs, suggesting that differences in these characteristics are driven by variation among pairs.     

Population dynamics of the wandering albatross (Diomedea exulans) on Macquarie Island and the effects of mortality from longline fishing

The estimated breeding population of wandering albatrosses on Macquarie Island increased from 17 in 1956 to a maximum of 97 in 1966, and then declined at an average rate of 8.1% per year. Mark-recapture analysis shows that the population is not closed (i.e., subject to immigration and emigration). The decline is correlated with the onset of large-scale fishing for tuna in the southern hemisphere using longlines. The effect of longline mortality on the population dynamics of the wandering albatross is estimated. An annual number of longline hooks in the southern hemisphere tuna fishery of 41.6 million is calculated as the ceiling below which the population would begin to recover.