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.
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.
marine top predators; frigatebirds; (sub-)mesoscale; habitat choice; Lagrangian structures; remote sensing
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.
Animal model; Bayesian environment; individual behavioral differences; personality; quantitative genetics; wandering albatross
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.
habitat model; penguins; polar front; distribution shift; IPCC climate models
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.
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.
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.
intermittent breeding; age; GnRH challenge; luteinizing hormone; snow petrels
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.
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.
Measuring individual quality in vertebrates is difficult. Focusing on allostasis mechanisms may be useful because they are functionally involved in the ability of an individual to survive and reproduce in its environment. Thus, a rise in stress hormones levels (corticosterone) occurs when an organism has to cope with challenging environmental conditions. This has recently led to the proposal of the ‘cort–fitness hypothesis’, which suggests that elevated baseline corticosterone levels should be found in individuals of poor quality that have difficulty coping with their environment. We tested this hypothesis by comparing an integrative measure of individual quality to baseline corticosterone in black-browed albatrosses (Thalassarche melanophrys). We found that individual baseline corticosterone levels were related to individual quality and highly repeatable from one breeding season to the next. Importantly, this relationship was found in males, but not in females. Therefore, we suggest that the relationship between quality and baseline corticosterone levels may depend on the environmental and energetic constraints that individuals have to cope with.
corticosterone; fitness; quality; albatross
Sooty (Puffinus griseus) and short-tailed (P. tenuirostris) shearwaters are abundant seabirds that range widely across global oceans. Understanding the foraging ecology of these species in the Southern Ocean is important for monitoring and ecosystem conservation and management.
Tracking data from sooty and short-tailed shearwaters from three regions of New Zealand and Australia were combined with at-sea observations of shearwaters in the Southern Ocean, physical oceanography, near-surface copepod distributions, pelagic trawl data, and synoptic near-surface winds. Shearwaters from all three regions foraged in the Polar Front zone, and showed particular overlap in the region around 140°E. Short-tailed shearwaters from South Australia also foraged in Antarctic waters south of the Polar Front. The spatial distribution of shearwater foraging effort in the Polar Front zone was matched by patterns in large-scale upwelling, primary production, and abundances of copepods and myctophid fish. Oceanic winds were found to be broad determinants of foraging distribution, and of the flight paths taken by the birds on long foraging trips to Antarctic waters.
The shearwaters displayed foraging site fidelity and overlap of foraging habitat between species and populations that may enhance their utility as indicators of Southern Ocean ecosystems. The results highlight the importance of upwellings due to interactions of the Antarctic Circumpolar Current with large-scale bottom topography, and the corresponding localised increases in the productivity of the Polar Front ecosystem.
Ward and Zahavi suggested in 1973 that colonies could serve as information centres, through a transfer of information on the location of food resources between unrelated individuals (Information Centre Hypothesis). Using GPS tracking and observations on group movements, we studied the search strategy and information transfer in two of the most colonial seabirds, Guanay cormorants (Phalacrocorax bougainvillii) and Peruvian boobies (Sula variegata). Both species breed together and feed on the same prey. They do return to the same feeding zone from one trip to the next indicating high unpredictability in the location of food resources. We found that the Guanay cormorants use social information to select their bearing when departing the colony. They form a raft at the sea surface whose position is continuously adjusted to the bearing of the largest returning columns of cormorants. As such, the raft serves as a compass signal that gives an indication on the location of the food patches. Conversely, Peruvian boobies rely mainly on personal information based on memory to take heading at departure. They search for food patches solitarily or in small groups through network foraging by detecting the white plumage of congeners visible at long distance. Our results show that information transfer does occur and we propose a new mechanism of information transfer based on the use of rafts off colonies. The use of rafts for information transfer may be common in central place foraging colonial seabirds that exploit short lasting and/or unpredictably distributed food patches. Over the past decades Guanay cormorants have declined ten times whereas Peruvian boobies have remained relatively stable. We suggest that the decline of the cormorants could be related to reduced social information opportunities and that social behaviour and search strategies have the potential to play an important role in the population dynamics of colonial animals.
The flight ability of animals is restricted by the scaling effects imposed by physical and physiological factors. In comparisons of the power available from muscle and the mechanical power required to fly, it is predicted that the margin between the powers should decrease with body size and that flying animals have a maximum body size. However, predicting the absolute value of this upper limit has proven difficult because wing morphology and flight styles varies among species. Albatrosses and petrels have long, narrow, aerodynamically efficient wings and are considered soaring birds. Here, using animal-borne accelerometers, we show that soaring seabirds have two modes of flapping frequencies under natural conditions: vigorous flapping during takeoff and sporadic flapping during cruising flight. In these species, high and low flapping frequencies were found to scale with body mass (mass−0.30 and mass−0.18) in a manner similar to the predictions from biomechanical flight models (mass−1/3 and mass−1/6). These scaling relationships predicted that the maximum limits on the body size of soaring animals are a body mass of 41 kg and a wingspan of 5.1 m. Albatross-like animals larger than the limit will not be able to flap fast enough to stay aloft under unfavourable wind conditions. Our result therefore casts doubt on the flying ability of large, extinct pterosaurs. The largest extant soarer, the wandering albatross, weighs about 12 kg, which might be a pragmatic limit to maintain a safety margin for sustainable flight and to survive in a variable environment.
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.
genetic diversity; life-history traits; albatrosses; AFLP
Ecosystems and populations are known to be influenced not only by long-term climatic trends, but also by other short-term climatic modes, such as interannual and decadal-scale variabilities. Because interactions between climatic forcing, biotic and abiotic components of ecosystems are subtle and complex, analysis of long-term series of both biological and physical factors is essential to understanding these interactions. Here, we apply a wavelet analysis simultaneously to long-term datasets on the environment and on the populations and breeding success of three Antarctic seabirds (southern fulmar, snow petrel, emperor penguin) breeding in Terre Adélie, to study the effects of climate fluctuations on Antarctic marine ecosystems. We show that over the past 40 years, populations and demographic parameters of the three species fluctuate with a periodicity of 3–5 years that was also detected in sea-ice extent and the Southern Oscillation Index. Although the major periodicity of these interannual fluctuations is not common to different species and environmental variables, their cyclic characteristics reveal a significant change since 1980. Moreover, sliding-correlation analysis highlighted the relationships between environmental variables and the demography of the three species, with important change of correlation occurring between the end of the 1970s and the beginning of the 1980s. These results suggest that a regime shift has probably occurred during this period, significantly affecting the Antarctic ecosystem, but with contrasted effects on the three species.
climate change; cyclic variability; regime shift; Antarctic marine predators; time-series analysis
Long-term studies have documented that climate fluctuations affect the dynamics of populations, but the relative influence of stochastic and density-dependent processes is still poorly understood and debated. Most studies have been conducted on terrestrial systems, and lacking are studies on marine systems explicitly integrating the fact that most populations live in seasonal environments and respond to regular or systematic environmental changes. We separated winter from summer mortality in a seabird population, the blue petrel Halobaena caerulea, in the southern Indian Ocean where the El Niño/Southern Oscillation effects occur with a 3-4-year lag. Seventy per cent of the mortality occurred in winter and was linked to climatic factors, being lower during anomalous warm events. The strength of density dependence was affected by climate, with population crashes occurring when poor conditions occurred at high densities. We found that an exceptionally long-lasting warming caused a ca. 40% decline of the population, suggesting that chronic climate change will strongly affect this top predator. These findings demonstrate that populations in marine systems are particularly susceptible to climate variation through complex interactions between seasonal mortality and density-dependent effects.
Foraging animals are expected to adjust their path according to the hierarchical spatial distribution of food resources and environmental factors. Studying such behaviour requires methods that allow for the detection of changes in pathways' characteristics across scales, i.e. a definition of scale boundaries and techniques to continuously monitor the precise movement of the animal over a sufficiently long period. We used a recently developed application of fractals, the changes in fractal dimension within a path and applied it to foraging trips over scales ranging across five orders of magnitude (10 m to 1000 km), using locations of wandering albatrosses (Diomedea exulans) recorded at 1 s intervals with a miniaturized global positioning system. Remarkably, all animals consistently showed the same pattern: the use of three scale-dependent nested domains where they adjust tortuosity to different environmental and behavioural constraints. At a small scale (ca. 100 m) they use a zigzag movement as they continuously adjust for optimal use of wind; at a medium scale (1-10 km), the movement shows changes in tortuosity consistent with food-searching behaviour; and at a large scale (greater than 10 km) the movement corresponds to commuting between patches and is probably influenced by large-scale weather systems. Our results demonstrate the possibility of identifying the hierarchical spatial scales at which long-ranging animals adjust their foraging behaviour, even in featureless environments such as oceans, and hence how to relate their movement patterns to environmental factors using an objective mathematical approach.