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1.  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.
PMCID: PMC4286031  PMID: 25473008
individual behavioural differences; boldness; ageing; foraging; life-history trade-offs; biologging
2.  Large-scale climatic anomalies affect marine predator foraging behaviour and demography 
Nature Communications  2015;6:8220.
Determining the links between the behavioural and population responses of wild species to environmental variations is critical for understanding the impact of climate variability on ecosystems. Using long-term data sets, we show how large-scale climatic anomalies in the Southern Hemisphere affect the foraging behaviour and population dynamics of a key marine predator, the king penguin. When large-scale subtropical dipole events occur simultaneously in both subtropical Southern Indian and Atlantic Oceans, they generate tropical anomalies that shift the foraging zone southward. Consequently the distances that penguins foraged from the colony and their feeding depths increased and the population size decreased. This represents an example of a robust and fast impact of large-scale climatic anomalies affecting a marine predator through changes in its at-sea behaviour and demography, despite lack of information on prey availability. Our results highlight a possible behavioural mechanism through which climate variability may affect population processes.
Understanding how organisms respond to short-term climate variations will help predict the impact of future global change. Here, Bost et al. show that large-scale climatic anomalies coincide with changes in the foraging behaviour and populations dynamics of king penguins in the Southern hemisphere.
PMCID: PMC4639794  PMID: 26506134
3.  Consistency pays: sex differences and fitness consequences of behavioural specialization in a wide-ranging seabird 
Biology Letters  2014;10(10):20140630.
Specialists and generalists often coexist within a single population, but the biological drivers of individual strategies are not fully resolved. When sexes differ in their foraging strategy, this can lead them to different environmental conditions and stability across their habitat range. As such, sexual segregation, combined with dominance, may lead to varying levels of specialization between the sexes. Here, we examine spatial and temporal niche width (intraindividual variability in aspects of foraging behaviour) of male and female black-browed albatrosses (Thalassarche melanophrys), and its consequences for fitness. We show that females, where maximum foraging range is under fluctuating selection, exhibit more variable behaviours and appear more generalist than males, who are under directional selection to forage close to the colony. However within each sex, successful birds had a much narrower niche width across most behaviours, suggesting some specialization is adaptive in both sexes. These results demonstrate that while there are sex differences in niche width, the fitness benefit of specialization in spatial distribution is strong in this wide-ranging seabird.
PMCID: PMC4272207  PMID: 25354918
intraindividual variability; seabirds; foraging; niche width; generalist
4.  Demographic Responses to Oxidative Stress and Inflammation in the Wandering Albatross (Diomedea exulans) 
PLoS ONE  2015;10(8):e0133967.
One of the major challenges in ecological research is the elucidation of physiological mechanisms that underlie the demographic traits of wild animals. We have assessed whether a marker of plasma oxidative stress (TBARS) and plasma haptoglobin (protein of the acute inflammatory phase response) measured at time t predict five demographic parameters (survival rate, return rate to the breeding colony, breeding probability, hatching and fledging success) in sexually mature wandering albatrosses over the next four years (Diomedea exulans) using a five-year individual-based dataset. Non-breeder males, but not females, having higher TBARS at time t had reduced future breeding probabilities; haptoglobin was not related to breeding probability. Neither TBARS nor haptoglobin predicted future hatching or fledging success. Haptoglobin had a marginally positive effect on female survival rate, while TBARS had a marginally negative effect on return rate. Our findings do not support the role for oxidative stress as a constraint of future reproductive success in the albatross. However, our data point to a potential mechanism underlying some aspects of reproductive senescence and survival. Our results also highlight that the study of the consequences of oxidative stress should consider the life-cycle stage of an individual and its reproductive history.
PMCID: PMC4537254  PMID: 26275171
5.  Demographic consequences of heavy metals and persistent organic pollutants in a vulnerable long-lived bird, the wandering albatross 
Seabirds are top predators of the marine environment that accumulate contaminants over a long life-span. Chronic exposure to pollutants is thought to compromise survival rate and long-term reproductive outputs in these long-lived organisms, thus inducing population decline. However, the demographic consequences of contaminant exposure are largely theoretical because of the dearth of long-term datasets. This study aims to test whether adult survival rate, return to the colony and long-term breeding performance were related to blood mercury (Hg), cadmium (Cd) and persistent organic pollutants (POPs), by using a capture–mark–recapture dataset on the vulnerable wandering albatross Diomedea exulans. We did not find evidence for any effect of contaminants on adult survival probability. However, blood Hg and POPs negatively impacted long-term breeding probability, hatching and fledging probabilities. The proximate mechanisms underlying these deleterious effects are likely multifaceted, through physiological perturbations and interactions with reproductive costs. Using matrix population models, we projected a demographic decline in response to an increase in Hg or POPs concentrations. This decline in population growth rate could be exacerbated by other anthropogenic perturbations, such as climate change, disease and fishery bycatch. This study gives a new dimension to the overall picture of environmental threats to wildlife populations.
PMCID: PMC4071534  PMID: 24920477
capture–recapture; Diomedea exulans; mercury; polybrominated diphenyl ethers (PBDE); polychlorinated biphenyl; pesticides
6.  Sex-Specific Habitat Utilization and Differential Breeding Investments in Christmas Island Frigatebirds throughout the Breeding Cycle 
PLoS ONE  2015;10(6):e0129437.
In seabirds, equal bi-parental care is the rule, as it is considered crucial for raising chicks successfully because seabirds forage in an environment with unpredictable and highly variable food supply. Frigatebirds forage in poor tropical waters, yet males reduce and even stop parental care soon after chick brooding, leaving the female to provision the chick alone for an extended fledging period. Using bird-borne tracking devices, male and female Christmas Island Frigatebirds (Fregata andrewsi) were investigated during the brooding, late chick rearing and post-fledging period to examine whether sexes exhibit foraging strategies that may be linked to differential breeding investments. During brooding, males and females showed similar foraging behaviour under average marine productivity of oceanic waters close to the colony, but males shifted to more distant and more productive habitats when conditions deteriorated to continue with reduced chick provisioning. During the late chick rearing period, females progressively increased their foraging range to the more distant but productive marine areas that only males had visited during brooding. Birds spent the non-breeding period roosting in highly productive waters of the Sunda Shelf. The sex-specific utilisation of three different foraging habitats with different primary productivity (oceanic, coastal, and shelf areas) allowed for temporal and spatial segregation in the exploitation of favourable habitats which seems to enable each sex to optimise its foraging profitability. In addition, post-fledging foraging movements of females suggest a biennial breeding cycle, while limited information on males suggests the possibility of an annual breeding cycle.
PMCID: PMC4476668  PMID: 26098941
7.  Half a World Apart? Overlap in Nonbreeding Distributions of Atlantic and Indian Ocean Thin-Billed Prions 
PLoS ONE  2015;10(5):e0125007.
Distant populations of animals may share their non-breeding grounds or migrate to distinct areas, and this may have important consequences for population differentiation and dynamics. Small burrow-nesting seabirds provide a suitable case study, as they are often restricted to safe breeding sites on islands, resulting in a patchy breeding distribution. For example, Thin-billed prions Pachyptila belcheri have two major breeding colonies more than 8,000 km apart, on the Falkland Islands in the south-western Atlantic and in the Kerguelen Archipelago in the Indian Ocean. We used geolocators and stable isotopes to compare at-sea movements and trophic levels of these two populations during their non-breeding season, and applied ecological niche models to compare environmental conditions in the habitat. Over three winters, birds breeding in the Atlantic showed a high consistency in their migration routes. Most individuals migrated more than 3000 km eastwards, while very few remained over the Patagonian Shelf. In contrast, all Indian Ocean birds migrated westwards, resulting in an overlapping nonbreeding area in the eastern Atlantic sector of the Southern Ocean. Geolocators and isotopic signature of feathers indicated that prions from the Falklands moulted at slightly higher latitudes than those from Kerguelen Islands. All birds fed on low trophic level prey, most probably crustaceans. The phenology differed notably between the two populations. Falkland birds returned to the Patagonian Shelf after 2-3 months, while Kerguelen birds remained in the nonbreeding area for seven months, before returning to nesting grounds highly synchronously and at high speed. Habitat models identified sea surface temperature and chlorophyll a concentration as important environmental parameters. In summary, we show that even though the two very distant populations migrate to roughly the same area to moult, they have distinct wintering strategies: They had significantly different realized niches and timing which may contribute to spatial niche partitioning.
PMCID: PMC4446212  PMID: 26018194
8.  Extreme ecological response of a seabird community to unprecedented sea ice cover 
Royal Society Open Science  2015;2(5):140456.
Climate change has been predicted to reduce Antarctic sea ice but, instead, sea ice surrounding Antarctica has expanded over the past 30 years, albeit with contrasted regional changes. Here we report a recent extreme event in sea ice conditions in East Antarctica and investigate its consequences on a seabird community. In early 2014, the Dumont d'Urville Sea experienced the highest magnitude sea ice cover (76.8%) event on record (1982–2013: range 11.3–65.3%; mean±95% confidence interval: 27.7% (23.1–32.2%)). Catastrophic effects were detected in the breeding output of all sympatric seabird species, with a total failure for two species. These results provide a new view crucial to predictive models of species abundance and distribution as to how extreme sea ice events might impact an entire community of top predators in polar marine ecosystems in a context of expanding sea ice in eastern Antarctica.
PMCID: PMC4453256  PMID: 26064653
Antarctic; breeding; sea ice; petrels; penguins; skuas
9.  Extreme variation in migration strategies between and within wandering albatross populations during their sabbatical year, and their fitness consequences 
Scientific Reports  2015;5:8853.
Migratory behavior, routes and zones used during the non-breeding season are assumed to have been selected to maximize fitness, and can lead to genetic differentiation. Yet, here we show that migration strategies differ markedly between and within two genetically similar populations of wandering albatross Diomedea exulans from the Crozet and Kerguelen archipelagos in the Indian Ocean. Wandering albatrosses usually breed biennially if successful, and during the sabbatical year, all birds from Kerguelen migrate to the Pacific Ocean, whereas most from Crozet are sedentary. Instead of taking the shortest routes, which would involve a return against headwinds, migratory birds fly with the westerly winds, requiring detours of 10,000 s km. In total, migrants circumnavigate Antarctica 2 to 3 times, covering more than 120,000 km in a single sabbatical year. Our results indicate strong links between migratory behavior and fitness; all birds from Kerguelen breed biennially, whereas a significant proportion of those from Crozet, especially females, are sedentary and breed in consecutive calendar years. To breed annually, these females temporarily change mate, but return to their original partner in the following year. This extreme variation in migratory behavior has important consequences in term of life history evolution and susceptibility to climate change and fisheries.
PMCID: PMC4352845  PMID: 25747757
10.  Poor Transferability of Species Distribution Models for a Pelagic Predator, the Grey Petrel, Indicates Contrasting Habitat Preferences across Ocean Basins 
PLoS ONE  2015;10(3):e0120014.
Species distribution models (SDMs) are increasingly applied in conservation management to predict suitable habitat for poorly known populations. High predictive performance of SDMs is evident in validations performed within the model calibration area (interpolation), but few studies have assessed SDM transferability to novel areas (extrapolation), particularly across large spatial scales or pelagic ecosystems. We performed rigorous SDM validation tests on distribution data from three populations of a long-ranging marine predator, the grey petrel Procellaria cinerea, to assess model transferability across the Southern Hemisphere (25-65°S). Oceanographic data were combined with tracks of grey petrels from two remote sub-Antarctic islands (Antipodes and Kerguelen) using boosted regression trees to generate three SDMs: one for each island population, and a combined model. The predictive performance of these models was assessed using withheld tracking data from within the model calibration areas (interpolation), and from a third population, Marion Island (extrapolation). Predictive performance was assessed using k-fold cross validation and point biserial correlation. The two population-specific SDMs included the same predictor variables and suggested birds responded to the same broad-scale oceanographic influences. However, all model validation tests, including of the combined model, determined strong interpolation but weak extrapolation capabilities. These results indicate that habitat use reflects both its availability and bird preferences, such that the realized distribution patterns differ for each population. The spatial predictions by the three SDMs were compared with tracking data and fishing effort to demonstrate the conservation pitfalls of extrapolating SDMs outside calibration regions. This exercise revealed that SDM predictions would have led to an underestimate of overlap with fishing effort and potentially misinformed bycatch mitigation efforts. Although SDMs can elucidate potential distribution patterns relative to large-scale climatic and oceanographic conditions, knowledge of local habitat availability and preferences is necessary to understand and successfully predict region-specific realized distribution patterns.
PMCID: PMC4352036  PMID: 25748948
11.  Combining Methods to Describe Important Marine Habitats for Top Predators: Application to Identify Biological Hotspots in Tropical Waters 
PLoS ONE  2014;9(12):e115057.
In tropical waters resources are usually scarce and patchy, and predatory species generally show specific adaptations for foraging. Tropical seabirds often forage in association with sub-surface predators that create feeding opportunities by bringing prey close to the surface, and the birds often aggregate in large multispecific flocks. Here we hypothesize that frigatebirds, a tropical seabird adapted to foraging with low energetic costs, could be a good predictor of the distribution of their associated predatory species, including other seabirds (e.g. boobies, terns) and subsurface predators (e.g., dolphins, tunas). To test this hypothesis, we compared distribution patterns of marine predators in the Mozambique Channel based on a long-term dataset of both vessel- and aerial surveys, as well as tracking data of frigatebirds. By developing species distribution models (SDMs), we identified key marine areas for tropical predators in relation to contemporaneous oceanographic features to investigate multi-species spatial overlap areas and identify predator hotspots in the Mozambique Channel. SDMs reasonably matched observed patterns and both static (e.g. bathymetry) and dynamic (e.g. Chlorophyll a concentration and sea surface temperature) factors were important explaining predator distribution patterns. We found that the distribution of frigatebirds included the distributions of the associated species. The central part of the channel appeared to be the best habitat for the four groups of species considered in this study (frigatebirds, brown terns, boobies and sub-surface predators).
PMCID: PMC4262456  PMID: 25494047
12.  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.
PMCID: PMC3757974  PMID: 23926153
albatross; learning; movement; immaturity; telemetry
13.  Age-Related Mercury Contamination and Relationship with Luteinizing Hormone in a Long-Lived Antarctic Bird 
PLoS ONE  2014;9(7):e103642.
Seabirds, as long-lived top predators, accumulate contaminants such as mercury (Hg), an established endocrine disruptor. In long lived species hormonal secretion varies with age; therefore, Hg-induced endocrine disruption may be exacerbated in some age classes. Here we investigated relationships between blood total Hg and luteinizing hormone (LH, a key pituitary hormone for the onset of breeding), in pre-laying known-age (11–45 years old) snow petrels (Pagodroma nivea) from Adélie Land, Antarctica. We predicted that 1) blood Hg would increase with advancing age as a consequence of bio-accumulation; and that 2) increasing blood Hg would be related to decreased concentrations of LH in the most Hg-contaminated individuals. Hg concentrations were higher in females than in males (p<0.001), and contrary to our prediction, decreased with advancing age in males (p = 0.009) and tended to do so in females (p = 0.06). The analysis of stable isotopes (δ13C and δ15N) suggested that this unexpected pattern could originate from age and sex-related variations in trophic niche, and hence Hg exposure. Regarding LH, our prediction was only supported in young birds (≤23 years) where baseline LH was inversely correlated with Hg concentrations (p = 0.04). Hg burden did not predict baseline LH or GnRH-induced LH in birds that were more than 23 years old. These results show that age and contaminants may interfere with major endocrine mechanisms and, together with other recent studies, support the view that Hg could be connected to LH secretion and could then impair the fitness of long-lived birds.
PMCID: PMC4114970  PMID: 25072936
14.  Coupling instantaneous energy-budget models and behavioural mode analysis to estimate optimal foraging strategy: an example with wandering albatrosses 
Movement Ecology  2014;2(1):8.
How foragers move across the landscape to search for resources and obtain energy is a central issue in ecology. Direct energetic quantification of animal movements allows for testing optimal foraging theory predictions which assumes that animals forage so as to maximise net energy gain. Thanks to biologging advances, we coupled instantaneous energy-budget models and behavioural mode analysis to test optimal foraging theory predictions on wandering albatross Diomedea exulans during the brooding period. Specifically, the instantaneous energy-budget model considered the energetic balance (i.e., the difference between empirical energy gain data and modelled energy expenditure via heart rate values) along the trajectory of a given individual. Four stereotypic instantaneous behavioural modes were identified based on trajectory properties (e.g., speed and turning angle) by applying a new algorithm called Expectation Maximization Binary Clustering. Previous studies on this species have shown that foraging-in-flight is the optimal foraging strategy during the incubation period when albatrosses undertake long-distance movements but no specific foraging strategy has been determined for shorter foraging movements (e.g., brooding period).
The output of our energy-budget model (measured as net energy gain) highlighted the potential optimality of alternative search strategies (e.g., sit-and-wait) during brooding, when birds may be subjected to specific energetic trade-offs and have to adapt their foraging strategies accordingly. However, not all birds showed this pattern, revealing the importance of considering individual variability in foraging strategies, as well as any switching among strategies, before drawing population-level generalizations. Finally, our study unveils the importance of considering fine scale activities to make realistic estimates of trip energy expenditure for flying birds at sea.
The up-scaling of accurately measured fine-scale energy patterns is essential to quantify energy balances, and their fluctuations by season of different activities among individuals or populations. In particular, we offer new insights for the energetic quantification of the effect of changing oceanic winds on the biology of pelagic predators in the southern oceans.
Electronic supplementary material
The online version of this article (doi:10.1186/2051-3933-2-8) contains supplementary material, which is available to authorized users.
PMCID: PMC4267543  PMID: 25520818
Optimal foraging theory; Energy-budget model; Behavioural clustering; Oceanic winds; Oceanic predator
15.  Evidence for Sex-Segregated Ocean Distributions of First-Winter Wandering Albatrosses at Crozet Islands 
PLoS ONE  2014;9(2):e86779.
The highly mobile wandering albatrosses (Diomedea exulans) are adapted to navigate the extreme environment of the Southern Ocean and return to isolated islands to breed. Each year they cover several hundreds of thousands of kilometers during travels across the sea. Little is known about the dispersal flights and migration of young albatrosses. We tracked, by satellite telemetry, the departure dispersal of 13 juvenile wandering albatrosses from the Crozet Islands and compared them with tracks of 7 unrelated adults during the interbreeding season. We used the satellite tracks to identify different behavioural steps of the inherited migration program used by juvenile wandering albatrosses during their first solo-migration. Our results show that the juvenile wandering albatrosses from Crozet Islands moved to sex-specific foraging zones of the ocean using at departures selectively the wind. The results suggest that the inherited migration program used by the juvenile wandering albatrosses encode several distinct steps, based on inherited preferred departure routes, differences in migration distance between sexes, and selective use of winds. During long transportation flights the albatrosses were influenced by winds and both adult and juveniles followed approximate loxodrome (rhumbline) routes coinciding with the foraging zone and the specific latitudes of their destination areas. During the long segments of transportation flights across open seas the juveniles selected routes at more northerly latitudes than adults.
PMCID: PMC3937278  PMID: 24586254
16.  Personality, Foraging and Fitness Consequences in a Long Lived Seabird 
PLoS ONE  2014;9(2):e87269.
While personality differences in animals are defined as consistent behavioural variation between individuals, the widely studied field of foraging specialisation in marine vertebrates has rarely been addressed within this framework. However there is much overlap between the two fields, both aiming to measure the causes and consequences of consistent individual behaviour. Here for the first time we use both a classic measure of personality, the response to a novel object, and an estimate of foraging strategy, derived from GPS data, to examine individual personality differences in black browed albatross and their consequences for fitness. First, we examine the repeatability of personality scores and link these to variation in foraging habitat. Bolder individuals forage nearer the colony, in shallower regions, whereas shyer birds travel further from the colony, and fed in deeper oceanic waters. Interestingly, neither personality score predicted a bird’s overlap with fisheries. Second, we show that both personality scores are correlated with fitness consequences, dependent on sex and year quality. Our data suggest that shyer males and bolder females have higher fitness, but the strength of this relationship depends on year quality. Females who forage further from the colony have higher breeding success in poor quality years, whereas males foraging close to the colony always have higher fitness. Together these results highlight the potential importance of personality variation in seabirds and that the fitness consequences of boldness and foraging strategy may be highly sex dependent.
PMCID: PMC3913606  PMID: 24504180
17.  What shall I do now? State-dependent variations of life-history traits with aging in Wandering Albatrosses 
Ecology and Evolution  2014;4(4):474-487.
Allocation decisions depend on an organism's condition which can change with age. Two opposite changes in life-history traits are predicted in the presence of senescence: either an increase in breeding performance in late age associated with terminal investment or a decrease due to either life-history trade-offs between current breeding and future survival or decreased efficiency at old age. Age variation in several life-history traits has been detected in a number of species, and demographic performances of individuals in a given year are influenced by their reproductive state the previous year. Few studies have, however, examined state-dependent variation in life-history traits with aging, and they focused mainly on a dichotomy of successful versus failed breeding and non-breeding birds. Using a 50-year dataset on the long-lived quasi-biennial breeding wandering albatross, we investigated variations in life-history traits with aging according to a gradient of states corresponding to potential costs of reproduction the previous year (in ascending order): non-breeding birds staying at sea or present at breeding grounds, breeding birds that failed early, late or were successful. We used multistate models to study survival and decompose reproduction into four components (probabilities of return, breeding, hatching, and fledging), while accounting for imperfect detection. Our results suggest the possible existence of two strategies in the population: strict biennial breeders that exhibited almost no reproductive senescence and quasi-biennial breeders that showed an increased breeding frequency with a strong and moderate senescence on hatching and fledging probabilities, respectively. The patterns observed on survival were contrary to our predictions, suggesting an influence of individual quality rather than trade-offs between reproduction and survival at late ages. This work represents a step further into understanding the evolutionary ecology of senescence and its relationship with costs of reproduction at the population level. It paves the way for individual-based studies that could show the importance of intra-population heterogeneity in those processes.
PMCID: PMC3936393  PMID: 24634731
Bienniality; breeding probability and success; capture–mark–recapture; cost of reproduction; Diomedea exulans; failure; survival.
18.  Frigatebird behaviour at the ocean–atmosphere interface: integrating animal behaviour with multi-satellite data 
Marine top predators such as seabirds are useful indicators of the integrated response of the marine ecosystem to environmental variability at different scales. Large-scale physical gradients constrain seabird habitat. Birds however respond behaviourally to physical heterogeneity at much smaller scales. Here, we use, for the first time, three-dimensional GPS tracking of a seabird, the great frigatebird (Fregata minor), in the Mozambique Channel. These data, which provide at the same time high-resolution vertical and horizontal positions, allow us to relate the behaviour of frigatebirds to the physical environment at the (sub-)mesoscale (10–100 km, days–weeks). Behavioural patterns are classified based on the birds’ vertical displacement (e.g. fast/slow ascents and descents), and are overlaid on maps of physical properties of the ocean–atmosphere interface, obtained by a nonlinear analysis of multi-satellite data. We find that frigatebirds modify their behaviours concurrently to transport and thermal fronts. Our results suggest that the birds’ co-occurrence with these structures is a consequence of their search not only for food (preferentially searched over thermal fronts) but also for upward vertical wind. This is also supported by their relationship with mesoscale patterns of wind divergence. Our multi-disciplinary method can be applied to forthcoming high-resolution animal tracking data, and aims to provide a mechanistic understanding of animals' habitat choice and of marine ecosystem responses to environmental change.
PMCID: PMC3481590  PMID: 22951344
marine top predators; frigatebirds; (sub-)mesoscale; habitat choice; Lagrangian structures; remote sensing
19.  Differences in boldness are repeatable and heritable in a long-lived marine predator 
Ecology and Evolution  2013;3(13):4291-4299.
Animal personalities, composed of axes of consistent individual behaviors, are widely reported and can have important fitness consequences. However, despite theoretical predictions that life-history trade-offs may cause and maintain personality differences, our understanding of the evolutionary ecology of personality remains poor, especially in long-lived species where trade-offs and senescence have been shown to be stronger. Furthermore, although much theoretical and empirical work assumes selection shapes variation in personalities, studies exploring the genetic underpinnings of personality traits are rare. Here we study one standard axis of personality, the shy–bold continuum, in a long-lived marine species, the wandering albatross from Possession Island, Crozet, by measuring the behavioral response to a human approach. Using generalized linear mixed models in a Bayesian framework, we show that boldness is highly repeatable and heritable. We also find strong differences in boldness between breeding colonies, which vary in size and density, suggesting birds are shyer in more dense colonies. These results demonstrate that in this seabird population, boldness is both heritable and repeatable and highlights the potential for ecological and evolutionary processes to shape personality traits in species with varying life-history strategies.
PMCID: PMC3856731  PMID: 24340172
Animal model; Bayesian environment; individual behavioral differences; personality; quantitative genetics; wandering albatross
20.  Projected poleward shift of king penguins' (Aptenodytes patagonicus) foraging range at the Crozet Islands, southern Indian Ocean 
Seabird populations of the Southern Ocean have been responding to climate change for the last three decades and demographic models suggest that projected warming will cause dramatic population changes over the next century. Shift in species distribution is likely to be one of the major possible adaptations to changing environmental conditions. Habitat models based on a unique long-term tracking dataset of king penguin (Aptenodytes patagonicus) breeding on the Crozet Islands (southern Indian Ocean) revealed that despite a significant influence of primary productivity and mesoscale activity, sea surface temperature consistently drove penguins' foraging distribution. According to climate models of the Intergovernmental Panel on Climate Change (IPCC), the projected warming of surface waters would lead to a gradual southward shift of the more profitable foraging zones, ranging from 25 km per decade for the B1 IPCC scenario to 40 km per decade for the A1B and A2 scenarios. As a consequence, distances travelled by incubating and brooding birds to reach optimal foraging zones associated with the polar front would double by 2100. Such a shift is far beyond the usual foraging range of king penguins breeding and would negatively affect the Crozet population on the long term, unless penguins develop alternative foraging strategies.
PMCID: PMC3350699  PMID: 22378808
habitat model; penguins; polar front; distribution shift; IPCC climate models
21.  Fisheries Bycatch as an Inadvertent Human-Induced Evolutionary Mechanism 
PLoS ONE  2013;8(4):e60353.
Selective harvesting of animals by humans can affect the sustainability and genetics of their wild populations. Bycatch - the accidental catch of non-target species - spans the spectrum of marine fauna and constitutes a harvesting pressure. Individual differences in attraction to fishing vessels and consequent susceptibility to bycatch exist, but few studies integrate this individual heterogeneity with demography. Here, we tested for the evidence and consequences of individual heterogeneity on the demography of the wandering albatross, a seabird heavily affected by fisheries bycatch. We found strong evidence for heterogeneity in survival with one group of individuals having a 5.2% lower annual survival probability than another group, and a decrease in the proportion of those individuals with the lowest survival in the population coinciding with a 7.5 fold increase in fishing effort in the foraging areas. Potential causes for the heterogeneity in survival are discussed and we suggest that bycatch removed a large proportion of individuals attracted by fishing vessels and had significant phenotypic and population consequences.
PMCID: PMC3622665  PMID: 23593199
22.  When Celibacy Matters: Incorporating Non-Breeders Improves Demographic Parameter Estimates 
PLoS ONE  2013;8(3):e60389.
In long-lived species only a fraction of a population breeds at a given time. Non-breeders can represent more than half of adult individuals, calling in doubt the relevance of estimating demographic parameters from the sole breeders. Here we demonstrate the importance of considering observable non-breeders to estimate reliable demographic traits: survival, return, breeding, hatching and fledging probabilities. We study the long-lived quasi-biennial breeding wandering albatross (Diomedea exulans). In this species, the breeding cycle lasts almost a year and birds that succeed a given year tend to skip the next breeding occasion while birds that fail tend to breed again the following year. Most non-breeders remain unobservable at sea, but still a substantial number of observable non-breeders (ONB) was identified on breeding sites. Using multi-state capture-mark-recapture analyses, we used several measures to compare the performance of demographic estimates between models incorporating or ignoring ONB: bias (difference in mean), precision (difference is standard deviation) and accuracy (both differences in mean and standard deviation). Our results highlight that ignoring ONB leads to bias and loss of accuracy on breeding probability and survival estimates. These effects are even stronger when studied in an age-dependent framework. Biases on breeding probabilities and survival increased with age leading to overestimation of survival at old age and thus actuarial senescence and underestimation of reproductive senescence. We believe our study sheds new light on the difficulties of estimating demographic parameters in species/taxa where a significant part of the population does not breed every year. Taking into account ONB appeared important to improve demographic parameter estimates, models of population dynamics and evolutionary conclusions regarding senescence within and across taxa.
PMCID: PMC3612038  PMID: 23555965
23.  Why do some adult birds skip breeding? A hormonal investigation in a long-lived bird 
Biology Letters  2011;7(5):790-792.
Skipping reproduction is often observed in long-lived organisms, but proximate mechanisms remain poorly understood. Since young and/or very old snow petrels (Pagodroma nivea) commonly skip breeding, we tested whether they are physiologically able to breed during the pre-laying stage. To do so, we measured the ability of known-age (11–45 years old) petrels to release luteinizing hormone (LH, a crucial driver for breeding), by injecting exogenous gonadotropin-releasing hormone (GnRH). Although young petrels exhibited low baseline LH levels, they were able to elevate LH levels after a GnRH challenge. Moreover, young and very old petrels showed a stronger decrease in LH levels after the 10 min post-GnRH injection compared with middle-aged petrels. Birds that skipped breeding were as able as breeders to release LH after a GnRH challenge, indicating that they had functional pituitaries. However, the decision to skip reproduction was linked to a strong LH decrease after the 10 min post-GnRH injection. Our result suggests that the youngest and the oldest petrels fail to maintain elevated baseline LH levels, thereby do not initiate reproductive activities. Skipping reproduction in long-lived birds probably results from age-related changes in the dynamics of the hypothalamic–pituitary–gonadal (HPG) axis function.
PMCID: PMC3169054  PMID: 21508027
intermittent breeding; age; GnRH challenge; luteinizing hormone; snow petrels
24.  Vultures of the Seas: Hyperacidic Stomachs in Wandering Albatrosses as an Adaptation to Dispersed Food Resources, including Fishery Wastes 
PLoS ONE  2012;7(6):e37834.
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.
PMCID: PMC3368928  PMID: 22701581
25.  Protecting Persistent Dynamic Oceanographic Features: Transboundary Conservation Efforts Are Needed for the Critically Endangered Balearic Shearwater 
PLoS ONE  2012;7(5):e35728.
The protection of key areas for biodiversity at sea is not as widespread as on land and research investment is necessary to identify biodiversity hotspots in the open ocean. Spatially explicit conservation measures such as the creation of representative networks of marine protected areas (MPAs) is a critical step towards the conservation and management of marine ecosystems, as well as to improve public awareness. Conservation efforts in ecologically rich and threatened ecosystems are specially needed. This is particularly urgent for the Mediterranean marine biodiversity, which includes highly mobile marine vertebrates. Here, we studied the at sea distribution of one of the most endangered Mediterranean seabird, the critically endangered Balearic shearwater Puffinus mauretanicus. Present knowledge, from vessel-based surveys, suggests that this species has a coastal distribution over the productive Iberian shelf in relation to the distribution of their main prey, small pelagic fish. We used miniaturised satellite transmitters to determine the key marine areas of the southern population of Balearic shearwaters breeding on Eivissa and spot the spatial connections between breeding and key marine areas. Our tracking study indicates that Balearic shearwaters do not only forage along the Iberian continental shelf but also in more distant marine areas along the North African coast, in particular W of Algeria, but also NE coast of Morocco. Birds recurrently visit these shelf areas at the end of the breeding season. Species distribution modelling identified chlorophyll a as the most important environmental variable in defining those oceanographic features characterizing their key habitats in the western Mediterranean. We identified persistent oceanographic features across time series available in the study area and discuss our results within the current conservation scenario in relation to the ecology of the species.
PMCID: PMC3349676  PMID: 22590510

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