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.     

Postnatal dispersal of wandering albatrosses Diomedea exulans: implications for the conservation of the species

Many large marine vertebrates are today threatened by human activities and it is therefore crucial to obtain information on their distribution and behaviour at sea. In particular little is known about the time necessary for juveniles to acquire the foraging skills of adults. We tracked 13 juvenile wandering albatrosses Diomedea exulans by satellite telemetry during their first year at sea. They covered an average distance of 184,000 km during the first year and restricted their dispersal to the unproductive waters of the subtropical Indian Ocean and Tasman Sea. This region of low wind velocities does not overlap with the foraging areas used by adults. After an innate phase of rapid dispersal with a fixed flight direction, young birds progressively increased their daily flight distances and attained adult flight efficiency within their first six months at sea. The complete overlap of the juveniles’ foraging ranges with major long‐line fisheries in the subtropical waters constitutes a major threat that could jeopardize the long term recovery ability of populations of the endangered wandering albatross in the Indian Ocean.     

Postnatal dispersal of wandering albatrosses Diomedea exulans: implications for the conservation of the species

Many large marine vertebrates are today threatened by human activities and it is therefore crucial to obtain information on their distribution and behaviour at sea. In particular little is known about the time necessary for juveniles to acquire the foraging skills of adults. We tracked 13 juvenile wandering albatrosses Diomedea exulans by satellite telemetry during their first year at sea. They covered an average distance of 184,000 km during the first year and restricted their dispersal to the unproductive waters of the subtropical Indian Ocean and Tasman Sea. This region of low wind velocities does not overlap with the foraging areas used by adults. After an innate phase of rapid dispersal with a fixed flight direction, young birds progressively increased their daily flight distances and attained adult flight efficiency within their first six months at sea. The complete overlap of the juveniles' foraging ranges with major long-line fisheries in the subtropical waters constitutes a major threat that could jeopardize the long term recovery ability of populations of the endangered wandering albatross in the Indian Ocean.     

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.     

Do naive juvenile seabirds forage differently from adults?

Foraging skills of young individuals are assumed to be inferior to those of adults. The reduced efficiency of naive individuals may be the primary cause of the high juvenile mortality and explain the deferment of maturity in long-lived species. However, the study of juvenile and immature foraging behaviour has been limited so far. We used satellite telemetry to compare the foraging movements of juveniles, immatures and breeding adult wandering albatrosses Diomedea exulans, a species where foraging success is positively influenced by the distance covered daily. We showed that juveniles are able to use favourable winds as soon as the first month of independence, but cover shorter distances daily and spend more time sitting on water than adults during the first two months after fledging. These reduced movement capacities do not seem to be the cause of higher juvenile mortality. Moreover, juveniles almost never restrict their movement to specific areas, as adults and immatures frequently do over shelf edges or oceanic zones, which suggest that the location of appropriate areas is learned through experience. Immatures and adults have equivalent movement capacities, but when they are central place foragers, i.e. when adults breed or immatures come to the colony to display and pair, immatures make shorter trips than adults. The long duration of immaturity in this species seems to be related to a long period of learning to integrate the foraging constraints associated with reproduction and central place foraging. Our results indicate that foraging behaviour of young albatrosses is partly innate and partly learned progressively over immaturity. The first months of learning appear critical in terms of survival, whereas the long period of immaturity is necessary for young birds to attain the skills necessary for efficient breeding without fitness costs.     

Regulation of foraging trips and incubation routine in male and female wandering albatrosses

The resolution of the conflict between eggcare and foraging was studied in male and female wandering albatrosses. The foraging zone and range, duration of incubation shifts and foraging trips, and associated changes in body mass were studied. Costs during incubation, expressed as the time spent incubating and the proportional loss of body mass, were similar for both sexes. The mass gained at sea was related to the duration of foraging trips, but the relationship was much less significant in males, where foraging ranges, though similar on average to those of females, were very variable. Males foraged in more southerly waters than females, and gained mass more rapidly. Only females appeared to regulate the duration of foraging trips, and this compensated for the mass lost during the incubation fast. Previous breeding experience had no influence on foraging efficiency. Egg desertion because of depletion of body reserves was very rare because birds have a wide safety margin, i.e. the difference between the average body mass when relieved and that at nest desertion. This safety margin enables the birds to compensate for the high variability in the duration of foraging trips, and is probably a reason for the high breeding success of wandering albatrosses. Decisions to return from the sea to the nest or to desert the nest are probably related to the status of body reserves, and have been selected in the large wandering albatross so that both present and future reproductive success are maximised.     

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.     

Behavioral responses to encounter of fishing boats in wandering albatrosses

Animals are attracted to human food subsidies worldwide. The behavioral response of individuals to these resources is rarely described in detail, beyond chances of encounters. Seabirds for instance scavenge in large numbers at fishing boats, triggering crucial conservation issues, but how the response to boats varies across encounters is poorly known. Here we examine the behavioral response of wandering albatrosses (Diomedea exulans), equipped with GPS tags, to longline fishing boats operating near their colony for which we had access to vessel monitoring system data. We distinguish between encounters (flying within 30 km of a boat) and attendance behavior (sitting on the sea within 3 km of a boat), and examine factors affecting each. In particular, we test hypotheses that the response to encountered boats should vary with sex and age in this long‐lived dimorphic species. Among the 60% trips that encountered boats at least once, 80% of them contained attendance (but attendance followed only 60% of each single encounter). Birds were more attracted and remained attending longer when boats were hauling lines, despite the measures enforced by this fleet to limit food availability during operations. Sex and age of birds had low influence on the response to boats, except the year when fewer boats came fishing in the area, and younger birds were attending further from boats compared to older birds. Net mass gain of birds was similar across sex and not affected by time spent attending boats. Our results indicate albatrosses extensively attend this fishery, with no clear advantages, questioning impacts on foraging time budgets. Factors responsible for sex foraging segregation at larger scale seem not to operate at this fleet near the colony and are not consistent with predictions of optimal foraging theory on potential individual dominance asymmetries. This approach complements studies of large‐scale overlap of animals with human subsidies.     

Senescence rates and late adulthood reproductive success are strongly influenced by personality in a long-lived seabird

Studies are increasingly demonstrating that individuals differ in their rate of ageing, and this is postulated to emerge from a trade-off between current and future reproduction. Recent theory predicts a correlation between individual personality and life-history strategy, and from this comes the prediction that personality may predict the intensity of senescence. Here we show that boldness correlates with reproductive success and foraging behaviour in wandering albatrosses, with strong sex-specific differences. Shy males show a strong decline in reproductive performance with age, and bold females have lower reproductive success in later adulthood. In both sexes, bolder birds have longer foraging trips and gain more mass per trip as they get older. However, the benefit of this behaviour appears to differ between the sexes, such that it is only matched by high reproductive success in males. Together our results suggest that personality linked foraging adaptations with age are strongly sex-specific in their fitness benefits and that the impact of boldness on senescence is linked to ecological parameters.     

Fast and fuel efficient? Optimal use of wind by flying albatrosses

The influence of wind patterns on behaviour and effort of free-ranging male wandering albatrosses (Diomedea exulans) was studied with miniaturized external heart-rate recorders in conjunction with satellite transmitters and activity recorders. Heart rate was used as an instantaneous index of energy expenditure. When cruising with favourable tail or side winds, wandering albatrosses can achieve high flight speeds while expending little more energy than birds resting on land. In contrast, heart rate increases concomitantly with increasing head winds, and flight speeds decrease. Our results show that effort is greatest when albatrosses take off from or land on the water. On a larger scale, we show that in order for birds to have the highest probability of experiencing favourable winds, wandering albatrosses use predictable weather systems to engage in a stereotypical flight pattern of large looping tracks. When heading north, albatrosses fly in anticlockwise loops, and to the south, movements are in a clockwise direction. Thus, the capacity to integrate instantaneous eco-physiological measures with records of large-scale flight and wind patterns allows us to understand better the complex interplay between the evolution of morphological, physiological and behavioural adaptations of albatrosses in the windiest place on earth.     

Foraging and provisioning strategies of black-browed albatrosses in relation to the requirements of the chick: natural variation and experimental study

We studied regulation of the food supply to black-browed albatrosschicks at Kerguelen by simultaneously recording the provisioningrates achieved by individual parents and satellite trackingforaging birds during two seasons, by studying changes in adultmass, and by experimentally manipulating the food requirementof chicks. In 1994 black-browed albatrosses had a higher breedingsuccess and produced heavier chicks that grew faster than in1995. They spent a similar time foraging but brought heaviermeals to their chick in 1994. Satellite tracking indicated thatin both seasons birds foraged in the same oceanographic area,250 km from the colony. Travel times to and from this area remainedunchanged, and similar times were spent foraging there. In ourstudy area, black-browed albatrosses appear to rely on a foodresource that is predictable in location, but whose availabilityvaries from one year to the next. The principal difference betweenyears of differing food availability was that birds broughtlarger meals when food was more abundant Costs of commutingto nearby feeding areas are probably low and allow the deliveryof energy to the chick at a high rate. A study carried out in1991 indicated that there was no relationship between the changesin adult mass from one trip to the next and the duration offoraging trips or feed mass, suggesting that adult body conditionhad little influence on the provisioning strategy of this species.An experiment whereby some chicks were deprived of food andothers received supplementary food showed that parents of underfedchicks spent the same time foraging and brought slightly largeramounts of food to their chicks as control parents. We suggestthat parents are searching for food to the maximum limits oftheir ability and thus cannot reduce further foraging time,but underfed chicks can swallow more food. Parents of overfedchicks delivered less food and increased the time between feeds.The reduction in provisioning frequency is interpreted as thecapacity of parents to modify their foraging behavior accordingto the nutritional status of the chick, but the reduction offeed mass is probably the result of chicks being close to theirmaximum assimilatory capacity. Comparison between Procellariiformspecies indicates extensive differences in the degree to whichparents can regulate the supply of food to their chicks. Neriticspecies like black-browed albatrosses appear to have a reducedability to regulate, and especially to increase provisioningrates, whereas more pelagic species may have a greater regulationability     

Environmental heterogeneity and the evolution of foraging behaviour in long ranging greater albatrosses

Habitat selection in heterogeneous environments is assumed to allow diversification. Wide‐ranging species like pelagic seabirds present a paradox, in that their diversity appears difficult to reconcile with a frequent lack of geographical isolation between populations. We studied the foraging strategies of three closely related species of greater albatrosses, wandering albatross, Diomedea exulans, Amsterdam albatrosses D. amsterdamensis and royal albatross, D. epomophora, in relation to environmental heterogeneity at coarse‐grained and fine‐grained scales. During the incubation period the three species foraged at long distances from their colonies. We observed significant differences between the species in the duration of foraging trips and the distance travelled per day. There were significant differences in preference for habitat types in relation to bathymetric features, and in chlorophyll a concentrations in the waters traversed. Royal albatross preferred shallower waters (<1500 m depth), which were rich in chlorophyll (>0.5 mg/m³), while the other species spent on average 80% of their time in waters deeper than this, where chlorophyll levels were lower. Wandering albatrosses foraged in colder waters than Amsterdam albatrosses. Patterns of activity divided the species into two groups: those exploiting oceanic habitats (wandering and Amsterdam albatrosses) spent high proportions of time on the water (49%), and had on average 1.35 takeoffs and landings per hour, while royal albatross, which foraged mainly over neritic waters spent only 35% of their time sitting on the water, and made on average 2.6 takeoff per hour. Further, royal albatross showed a similar pattern of activity during all periods of the day, while wandering and Amsterdam albatrosses were mostly inactive during the night. We link these differences in activity to prey patch availability in two contrasting habitats – continental shelf areas compared to open ocean habitats. The divergent styles of foraging observed in this study suggest that these closely‐related and wide‐ranging species could effectively co‐exist by dividing the resources available to them by different modes of exploitation.     

Early‐life foraging: Behavioral responses of newly fledged albatrosses to environmental conditions

In order to survive and later recruit into a population, juvenile animals need to acquire resources through the use of innate and/or learnt behaviors in an environment new to them. For far‐ranging marine species, such as the wandering albatross Diomedea exulans, this is particularly challenging as individuals need to be able to rapidly adapt and optimize their movement strategies in response to the highly dynamic and heterogeneous nature of their open‐ocean pelagic habitats. Critical to this is the development and flexibility of dispersal and exploratory behaviors. Here, we examine the movements of eight juvenile wandering albatrosses, tracked using GPS/Argos satellite transmitters for eight months following fledging, and compare these to the trajectories of 17 adults to assess differences and similarities in behavioral strategies through time. Behavioral clustering algorithms (Expectation Maximization binary Clustering) were combined with multinomial regression analyses to investigate changes in behavioral mode probabilities over time, and how these may be influenced by variations in day duration and in biophysical oceanographic conditions. We found that juveniles appeared to quickly acquire the same large‐scale behavioral strategies as those employed by adults, although generally more time was spent resting at night. Moreover, individuals were able to detect and exploit specific oceanographic features in a manner similar to that observed in adults. Together, the results of this study suggest that while shortly after fledging juvenile wandering albatrosses are able to employ similar foraging strategies to those observed in adults, additional skills need to be acquired during the immature period before the efficiency of these behaviors matches that of adults.     

From the Eye of the Albatrosses: A Bird-Borne Camera Shows an Association between Albatrosses and a Killer Whale in the Southern Ocean

Albatrosses fly many hundreds of kilometers across the open ocean to find and feed upon their prey. Despite the growing number of studies concerning their foraging behaviour, relatively little is known about how albatrosses actually locate their prey. Here, we present our results from the first deployments of a combined animal-borne camera and depth data logger on free-ranging black-browed albatrosses (Thalassarche melanophrys). The still images recorded from these cameras showed that some albatrosses actively followed a killer whale (Orcinus orca), possibly to feed on food scraps left by this diving predator. The camera images together with the depth profiles showed that the birds dived only occasionally, but that they actively dived when other birds or the killer whale were present. This association with diving predators or other birds may partially explain how albatrosses find their prey more efficiently in the apparently ‘featureless’ ocean, with a minimal requirement for energetically costly diving or landing activities.     

Satellite tracking of light-mantled sooty albatrosses

Five light-mantled sooty albatrosses (Phoebetria palpebrata) breeding at Macquarie Island were tracked with miniaturised satellite transmitters during foraging trips of the incubation period. Birds moved rapidly to specific sectors of the Southern Ocean, where they spent several days foraging before returning to their nests. These specific sectors were at an average distance of 1516 km from Macquarie Island and located in pelagic Antarctic waters, mostly along the Antarctic continent. The maximum foraging range was in average 1721 km and the total distance covered by two birds for which there were complete tracks was 6463 and 6975 km. This study confirms previous suggestions that light-mantled sooty albatrosses are able to forage in the waters of the high Antarctic while breeding in the sub-Antarctic. The implications of the extreme separation of feeding zones from nesting grounds, in terms of conservation and life-history strategies, are discussed.     

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.     

Corticosterone and foraging behavior in a pelagic seabird

Because endocrine mechanisms are thought to mediate behavioral responses to changes in the environment, examining these mechanisms is essential for understanding how long-lived seabirds adjust their foraging decisions to contrasting environmental conditions in order to maximize their fitness. In this context, the hormone corticosterone (CORT) deserves specific attention because of its major connections with locomotor activities. We examined for the first time the relationships between individual CORT levels and measurements of foraging success and behavior using satellite tracking and blood sampling from wandering albatrosses (Diomedea exulans) before (pretrip CORT levels) and after (posttrip CORT levels) foraging trips during the incubation period. Plasma CORT levels decreased after a foraging trip, and the level of posttrip CORT was negatively correlated with individual foraging success, calculated as total mass gain over a foraging trip. Pretrip CORT levels were not linked to time spent at sea but were positively correlated with daily distance traveled and maximum range at sea. In this study, we were able to highlight the sensitivity of CORT levels to variation in energy intake, and we showed for the first time that individual CORT levels can be explained by variation in foraging success. Relationships between pretrip CORT levels and daily distance traveled and maximum range were independent of pretrip body mass, suggesting that slight elevations in pretrip CORT levels might facilitate locomotor activity. However, because both foraging behavior and pretrip CORT levels could be affected by individual quality, future experimental studies including manipulation of CORT levels are needed to test whether CORT can mediate foraging decisions according to foraging conditions.     

Sensitivity to dimethyl sulphide suggests a mechanism for olfactory navigation by seabirds

Petrels, albatrosses and other procellariiform seabirds have an excellent sense of smell, and routinely navigate over the world's oceans by mechanisms that are not well understood. These birds travel thousands of kilometres to forage on ephemeral prey patches at variable locations, yet they can quickly and efficiently find their way back to their nests on remote islands to provision chicks, even with magnetic senses experimentally disrupted. Over the seemingly featureless ocean environment, local emissions of scents released by phytoplankton reflect bathymetric features such as shelf breaks and seamounts. These features suggest an odour landscape that may provide birds with orientation cues. We have previously shown that concentrated experimental deployments of one such compound, dimethyl sulphide (DMS), attracts procellariiforms at sea, suggesting that some species can use it as a foraging cue. Here we present the first physiological demonstration that an Antarctic seabird can detect DMS at biogenic levels. We further show that birds can use DMS as an orientation cue in a non-foraging context within a concentration range that they might naturally encounter over the ocean.     

Surviving with low genetic diversity: the case of albatrosses

Low genetic diversity is predicted to negatively impact species viability and has been a central concern for conservation. In contrast, the possibility that some species may thrive in spite of a relatively poor diversity has received little attention. The wandering and Amsterdam albatrosses (Diomedea exulans and Diomedea amsterdamensis) are long-lived seabirds standing at an extreme along the gradient of life strategies, having traits that may favour inbreeding and low genetic diversity. Divergence time of the two species is estimated at 0.84 Myr ago from cytochrome b data. We tested the hypothesis that both albatrosses inherited poor genetic diversity from their common ancestor. Within the wandering albatross, per cent polymorphic loci and expected heterozygosity at amplified fragment length polymorphisms were approximately one-third of the minimal values reported in other vertebrates. Genetic diversity in the Amsterdam albatross, which is recovering from a severe bottleneck, was about twice as low as in the wandering albatross. Simulations supported the hypothesis that genetic diversity in albatrosses was already depleted prior to their divergence. Given the generally high breeding success of these species, it is likely that they are not suffering much from their impoverished diversity. Whether albatrosses are unique in this regard is unknown, but they appear to challenge the classical view about the negative consequences of genetic depletion on species survival.     

Annual energy budget and food requirements of breeding wandering albatrosses (<Emphasis Type="Italic">Diomedea exulans</Emphasis>)

Energy budgets form an integral part of our understanding of animal energetics, particularly when presented in the context of reproduction. In this paper, I created a time-energy budget for a breeding pair of wandering albatrosses (Diomedea exulans) to estimate the annual breeding costs and food requirements of the population at Possession Island, Crozet Archipelago. For a breeding cycle that lasts 356 days on average, a pair uses 2,733 MJ to raise a single chick to fledging. This estimate is 1.21 times higher than previously calculated for wandering albatrosses breeding at Marion Island. Unlike the current analysis, the previous study assumed that foraging costs were constant across all stages of the breeding cycle. Recent evidence shows that foraging costs vary during breeding for wandering albatrosses at Crozet and this is probably true for all populations. Incubation costs have also been shown to be substantially lower than previously determined. Therefore, if a wandering albatross pair at Crozet uses a total of 2,733 MJ to breed, they would need to consume at least 1.7 kg bird^–1 day^–1 of fresh food, on average, to balance their own energy requirements and to provision a single chick for approximately 278 days. At this rate of food consumption, the breeding population at Crozet would consume approximately 340 tonnes of fresh food per breeding season.