Additive effects of climate and fisheries drive ongoing declines in multiple albatross species.

Environmental and anthropogenic factors often drive population declines in top predators, but how their influences may combine remains unclear. Albatrosses are particularly threatened. They breed in fast-changing environments, and their extensive foraging ranges expose them to incidental mortality (bycatch) in multiple fisheries. The albatross community at South Georgia includes globally important populations of three species that have declined by 40-60% over the last 35 years. We used three steps to deeply understand the drivers of such dramatic changes: (i) describe fundamental demographic rates using multievent models, (ii) determine demographic drivers of population growth using matrix models, and (iii) identify environmental and anthropogenic drivers using ANOVAs. Each species was affected by different processes and threats in their foraging areas during the breeding and nonbreeding seasons. There was evidence for two kinds of combined environmental and anthropogenic effects. The first was sequential; in wandering and black-browed albatrosses, high levels of bycatch have reduced juvenile and adult survival, then increased temperature, reduced sea-ice cover, and stronger winds are affecting the population recovery potential. The second was additive; in gray-headed albatrosses, not only did bycatch impact adult survival but also this impact was exacerbated by lower food availability in years following El Niño events. This emphasizes the need for much improved implementation of mitigation measures in fisheries and better enforcement of compliance. We hope our results not only help focus future management actions for these populations but also demonstrate the power of the modelling approach for assessing impacts of environmental and anthropogenic drivers in wild animal populations.

Proximate drivers of spatial segregation in non-breeding albatrosses.

Many animals partition resources to avoid competition, and in colonially-breeding species this often leads to divergent space or habitat use. During the non-breeding season, foraging constraints are relaxed, yet the patterns and drivers of segregation both between and within populations are poorly understood. We modelled habitat preference to examine how extrinsic (habitat availability and intra-specific competition) and intrinsic factors (population, sex and breeding outcome) influence the distributions of non-breeding grey-headed albatrosses Thalassarche chrysostoma tracked from two major populations, South Georgia (Atlantic Ocean) and the Prince Edward Islands (Indian Ocean). Spatial segregation was greater than expected, reflecting distinct seasonal differences in habitat selection and accessibility, and avoidance of intra-specific competition with local breeders. Previously failed birds segregated spatially from successful birds during summer, when they used less productive waters, suggesting a link between breeding outcome and subsequent habitat selection. In contrast, we found weak evidence of sexual segregation, which did not reflect a difference in habitat use. Our results indicate that the large-scale spatial structuring of albatross distributions results from interactions between extrinsic and intrinsic factors, with important implications for population dynamics. As habitat preferences differed substantially between colonies, populations should be considered independently when identifying critical areas for protection.

Understanding oceanic migrations with intrinsic biogeochemical markers.

Migratory marine vertebrates move annually across remote oceanic water masses crossing international borders. Many anthropogenic threats such as overfishing, bycatch, pollution or global warming put millions of marine migrants at risk especially during their long-distance movements. Therefore, precise knowledge about these migratory movements to understand where and when these animals are more exposed to human impacts is vital for addressing marine conservation issues. Because electronic tracking devices suffer from several constraints, mainly logistical and financial, there is emerging interest in finding appropriate intrinsic markers, such as the chemical composition of inert tissues, to study long-distance migrations and identify wintering sites. Here, using tracked pelagic seabirds and some of their own feathers which were known to be grown at different places and times within the annual cycle, we proved the value of biogeochemical analyses of inert tissue as tracers of marine movements and habitat use. Analyses of feathers grown in summer showed that both stable isotope signatures and element concentrations can signal the origin of breeding birds feeding in distinct water masses. However, only stable isotopes signalled water masses used during winter because elements mainly accumulated during the long breeding period are incorporated into feathers grown in both summer and winter. Our findings shed new light on the simple and effective assignment of marine organisms to distinct oceanic areas, providing new opportunities to study unknown migration patterns of secretive species, including in relation to human-induced mortality on specific populations in the marine environment.

Differences in metabolic costs of terrestrial mobility in two closely related species of albatross.

Black-browed albatrosses Thalassarche melanophrys typically colonise steeper habitats than grey-headed albatrosses T. chrysostoma. The present study investigated the effect of colony philopatry on terrestrial locomotory ability in these two species, to determine: (1) if there is a difference in terrestrial locomotory ability between these two closely related species, and (2) what physiological or behavioural adaptations may account for any differences identified. We examined the metabolic cost, mechanical efficiency on an incline, and gait characteristics of terrestrial locomotion of these two species on both level and inclined planes. T. chrysostoma were able to perform at a significantly greater speed than T. melanophrys without reaching a significantly different maximal rate of oxygen consumption (V(O(2))). Conversely, T. melanophrys were able to move up a significantly steeper incline than T. chrysostoma while maintaining a similar maximal V(O(2)). Each species demonstrates stride length, force production (behavioural) and leg length (morphological) adaptations that minimise the cost of traversing their chosen colonies, indicating a clear relationship between terrestrial performance and local topography. However, it is not possible to determine if the difference in locomotory ability results from differences in colony topography, or if choice of colony site is dictated by the ability of the species to traverse different terrain.

Senescence effects in an extremely long-lived bird: the grey-headed albatross Thalassarche chrysostoma.

Studies attempting to document reproductive or other pre-lethal senescence effects in wild birds typically face an array of problems, including flaws in statistical analyses, non-adaptive philopatry to deteriorating environments, confounding effects arising from cohort heterogeneity and differential death rates of phenotypes and the frequent pairing of old birds to younger mates. Furthermore, recent studies suggest that birds could maintain a high level of physical fitness until old age, before being struck by a catastrophic illness leading quickly to their demise. The presence of terminally ill individuals in most datasets (and their greater incidence in older age categories) may therefore provide a false impression of progressive senescence in cross-sectional analyses. This study was designed explicitly to avoid all the known pitfalls linked to the demonstration of progressive senescence in wild populations, and involved one of the very longest-lived bird species. We show that, during incubation, old (aged 35 years and over) male grey-headed albatrosses Thalassarche chrysostoma make longer foraging trips, and have lower daily mass gains, than experienced mid-aged individuals (aged up to 28 years). This is, to our knowledge, the first report documenting reduced foraging performance with old age. Hatching and breeding success of pairs composed of two old individuals were reduced in comparison to mid-aged pairs. Overall results were very similar when analyses were repeated using only individuals known to have survived 1 or 2 years beyond field measurements (hence probably not suffering from the effects of an advanced terminal illness). We conclude that extremely long-lived individuals usually experience some degree of general physical deterioration, leading to reduced foraging and breeding performance, long before their final demise.

Albatross populations in peril: a population trajectory for black-browed albatrosses at south Georgia.

Simulation modeling was used to reconstruct Black-browed Albatross (Diomedea melanophris) population trends. Close approximations to observed data were accomplished by annually varying survival rates, reproductive success, and probabilities of returning to breed given success in previous years. The temporal shift in annual values coincided with the start of longline fishing at South Georgia and potential changes in krill abundance. We used 23 years of demographic data from long-term studies of a breeding colony of this species at Bird Island, South Georgia, to validate our model. When we used annual parameter estimates for survival, reproductive success, and probabilities of returning to breed given success in previous years, our model trajectory closely followed the observed changes in breeding population size over time. Population growth rate was below replacement (lambda < 1) in most years and was most sensitive to changes in adult survival. This supports the recent IUCN uplisting of this species from "Vulnerable" to "Endangered." Comparison of pre-1988 and post-1988 demography (before and after the inception of a longline fishery in the breeding area) reveals a decrease in lambda from 0.963 to 0.910. A life table response experiment (LTRE) showed that this decline in lambda was caused mostly by declines in survival of adults. If 1988-1998 demographic rates are maintained, the model predicts a 98% chance of a population of fewer than 25 pairs within 78 years. For this population to recover to a status under which it could be "delisted," a 10% increase in survival of all age classes would be needed.

Global circumnavigations: tracking year-round ranges of nonbreeding albatrosses.

Although albatrosses are paradigms of oceanic specialization, their foraging areas and migration routes when not breeding remain essentially unknown. Our continuous remote tracking of 22 adult gray-headed albatrosses for over 30 bird-years reveals three distinct strategies: (i) Stay in breeding home range; (ii) make return migrations to a specific area of the southwest Indian Ocean; and (iii) make one or more global circumnavigations (the fastest in just 46 days). The consistencies in patterns, routes, and timings offer the first hope of identifying areas of critical habitat for nonbreeding albatrosses, wherein appropriate management of longline fisheries might alleviate the plight of the world's most threatened family of birds.

Telomere loss in relation to age and early environment in long-lived birds.

Shortening of telomeres, specific nucleotide repeats that cap eukaryotic chromosomes, is thought to play an important role in cellular and organismal senescence. We examined telomere dynamics in two long-lived seabirds, the European shag and the wandering albatross. Telomere length in blood cells declines between the chick stage and adulthood in both species. However, among adults, telomere length is not related to age. This is consistent with reports of most telomere loss occurring early in life in other vertebrates. Thus, caution must be used in estimating annual rates of telomere loss, as these are probably not constant with age. We also measured changes within individuals in the wild, using repeat samples taken from individual shags as chicks and adults. We found high inter-individual variation in the magnitude of telomere loss, much of which was explained by circumstances during growth. Individuals laying down high tissue mass for their size showed greater telomere shortening. Independently of this, individuals born late in the season showed more telomere loss. Early conditions, possibly through their effects on oxidative stress, appear to play an important role in telomere attrition and thus potentially in the longevity of individuals.