Causes and consequences of pair-bond disruption in a sex-skewed population of a long-lived monogamous seabird.

Many animals form long-term monogamous pair bonds, and the disruption of a pair bond (through either divorce or widowhood) can have significant consequences for individual vital rates (survival, breeding, and breeding success probabilities) and life-history outcomes (lifetime reproductive success [LRS], life expectancy). Here, we investigated the causes and consequences of pair-bond disruption in wandering albatross (Diomedea exulans). State-of-the-art statistical and mathematical approaches were developed to estimate divorce and widowhood rates and their impacts on vital rates and life-history outcomes. In this population, females incur a higher mortality rate due to incidental fishery bycatch, so the population is male-skewed. Therefore, we first posited that males would show higher widowhood rates negatively correlated with fishing effort and females would have higher divorce rates because they have more mating opportunities. Furthermore, we expected that divorce could be an adaptive strategy, whereby individuals improved breeding success by breeding with a new partner of better quality. Finally, we posited that pair-bond disruptions could reduce survival and breeding probabilities owing to the cost of remating processes, with important consequences for life-history outcomes. As expected, we showed that males had higher widowhood rates than females and females had higher divorce rates in this male-skewed population. However, no correlation was found between fishing effort and male widowhood. Secondly, contrary to our expectation, we found that divorce was likely nonadaptive in this population. We propose that divorce in this population is caused by an intruder who outcompetes the original partner in line with the so-called forced divorce hypothesis. Furthermore, we found a 16.7% and 18.0% reduction in LRS only for divorced and widowed males, respectively, owing to missing breeding seasons after a pair-bond disruption. Finally, we found that divorced individuals were more likely to divorce again, but whether this is related to specific individual characteristics remains an important area of investigation.

Spatial segregation in a sexually dimorphic central place forager: Competitive exclusion or niche divergence?

Sexual competition is increasingly recognized as an important selective pressure driving species distributions. However, few studies have investigated the relative importance of interpopulation versus intrapopulation competition in relation to habitat availability and selection. To explain spatial segregation between sexes that often occurs in non-territorial and central place foragers, such as seabirds, two hypotheses are commonly used. The 'competitive exclusion' hypothesis states that dominant individuals should exclude subordinate individuals through direct competition, whereas the 'niche divergence' hypothesis states that segregation occurs due to past competition and habitat specialization. We tested these hypotheses in two populations of an extreme wide-ranging and sexually dimorphic seabird, investigating the relative role of intrapopulation and interpopulation competition in influencing sex-specific distribution and habitat preferences. Using GPS loggers, we tracked 192 wandering albatrosses Diomedea exulans during four consecutive years (2016-2019), from two neighbouring populations in the Southern Ocean (Prince Edward and Crozet archipelagos). We simulated pseudo-tracks to create a null spatial distribution and used Kernel Density Estimates (KDE) and Resource Selection Functions (RSF) to distinguish the relative importance of within- versus between-population competition. Kernel Density Estimates showed that only intrapopulation sexual segregation was significant for each monitoring year, and that tracks between the two colonies resulted in greater overlap than expected from the null distribution, especially for the females. RSF confirmed these results and highlighted key at-sea foraging areas, even if the estimated of at-sea densities were extremely low. These differences in selected areas between sites and sexes were, however, associated with high interannual variability in habitat preferences, with no clear specific preferences per site and sex. Our results suggest that even with low at-sea population densities, historic intrapopulation competition in wide-ranging seabirds may have led to sexual dimorphism and niche specialization, favouring the 'niche divergence' hypothesis. In this study, we provide a protocol to study competition within as well as between populations of central place foragers. This is relevant for understanding their distribution patterns and population regulation, which could potentially improve management of threatened populations.

Sex-specific effects of wind on the flight decisions of a sexually dimorphic soaring bird.

In a highly dynamic airspace, flying animals are predicted to adjust foraging behaviour to variable wind conditions to minimize movement costs. Sexual size dimorphism is widespread in wild animal populations, and for large soaring birds which rely on favourable winds for energy-efficient flight, differences in morphology, wing loading and associated flight capabilities may lead males and females to respond differently to wind. However, the interaction between wind and sex has not been comprehensively tested. We investigated, in a large sexually dimorphic seabird which predominantly uses dynamic soaring flight, whether flight decisions are modulated to variation in winds over extended foraging trips, and whether males and females differ. Using GPS loggers we tracked 385 incubation foraging trips of wandering albatrosses Diomedea exulans, for which males are c. 20% larger than females, from two major populations (Crozet and South Georgia). Hidden Markov models were used to characterize behavioural states-directed flight, area-restricted search (ARS) and resting-and model the probability of transitioning between states in response to wind speed and relative direction, and sex. Wind speed and relative direction were important predictors of state transitioning. Birds were much more likely to take off (i.e. switch from rest to flight) in stronger headwinds, and as wind speeds increased, to be in directed flight rather than ARS. Males from Crozet but not South Georgia experienced stronger winds than females, and males from both populations were more likely to take-off in windier conditions. Albatrosses appear to deploy an energy-saving strategy by modulating taking-off, their most energetically expensive behaviour, to favourable wind conditions. The behaviour of males, which have higher wing loading requiring faster speeds for gliding flight, was influenced to a greater degree by wind than females. As such, our results indicate that variation in flight performance drives sex differences in time-activity budgets and may lead the sexes to exploit regions with different wind regimes.

From early life to senescence: individual heterogeneity in a long-lived seabird.

Although population studies have long assumed that all individuals of a given sex and age are identical, ignoring among-individual differences may strongly bias our perception of eco-evolutionary processes. Individual heterogeneity, often referred to as individual quality, has received increasing research attention in the last decades. However, there are still substantial gaps in our current knowledge. For example, there is little information on how individual heterogeneity influences various life-history traits simultaneously, and studies describing individual heterogeneity in wild populations are generally not able to jointly identify possible sources of this variation. Here, based on a mark-recapture data set of 9,685 known-aged Wandering Albatrosses (Diomedea exulans), we investigated the existence of individual quality over the entire life cycle of this species, from early life to senescence. Using finite mixture models, we investigated the expression of individual heterogeneity in various demographic traits, and examined the origin of these among-individual differences by considering the natal environmental conditions. We found that some individuals consistently outperformed others during most of their life. In old age, however, the senescence rate was stronger in males that showed high demographic performance at younger ages. Variation in individual quality seemed strongly affected by extrinsic factors experienced during the ontogenetic period. We found that individuals born in years with high population density tended to have lower performances during their lifespan, suggesting delayed density dependence effects through individual quality. Our study showed that among-individual differences could be important in structuring individual life history trajectories, with substantial consequences at higher ecological levels such as population dynamics.

Fathers matter: male body mass affects life-history traits in a size-dimorphic seabird.

One of the predicted consequences of climate change is a shift in body mass distributions within animal populations. Yet body mass, an important component of the physiological state of an organism, can affect key life-history traits and consequently population dynamics. Over the past decades, the wandering albatross-a pelagic seabird providing bi-parental care with marked sexual size dimorphism-has exhibited an increase in average body mass and breeding success in parallel with experiencing increasing wind speeds. To assess the impact of these changes, we examined how body mass affects five key life-history traits at the individual level: adult survival, breeding probability, breeding success, chick mass and juvenile survival. We found that male mass impacted all traits examined except breeding probability, whereas female mass affected none. Adult male survival increased with increasing mass. Increasing adult male mass increased breeding success and mass of sons but not of daughters. Juvenile male survival increased with their chick mass. These results suggest that a higher investment in sons by fathers can increase their inclusive fitness, which is not the case for daughters. Our study highlights sex-specific differences in the effect of body mass on the life history of a monogamous species with bi-parental care.

Contrasting drivers of reproductive ageing in albatrosses.

Age-related variation in reproductive performance is ubiquitous in wild vertebrate populations and has important consequences for population and evolutionary dynamics. The ageing trajectory is shaped by both within-individual processes, such as improvement and senescence, and the among-individual effects of selective appearance and disappearance. To date, few studies have compared the role of these different drivers among species or populations. In this study, we use nearly 40 years of longitudinal monitoring data to contrast the within- and among-individual processes contributing to the reproductive ageing patterns in three albatross species (two biennial and one annual breeder) and test whether these can be explained by differences in life histories. Early-life performance in all species increased with age and was predominantly influenced by within-individual improvements. However, reproductive senescence was detected in only two of the species. In the species exhibiting senescent declines, we also detected a terminal improvement in breeding success. This is suggestive of a trade-off between reproduction and survival, which was supported by evidence of selective disappearance of good breeders. We demonstrate that comparisons of closely related species which differ in specific aspects of their life history can shed light on the ecological and evolutionary forces shaping variation in ageing patterns.

Telomere length measurement by qPCR in birds is affected by storage method of blood samples.

Given the potential role of telomeres as biomarkers of individual health and ageing, there is an increasing interest in studying telomere dynamics in a wider range of taxa in the fields of ecology and evolutionary biology. Measuring telomere length across the lifespan in wild animal systems is essential for testing these hypotheses, and may be aided by archived blood samples collected as part of longitudinal field studies. However, sample collection, storage, and DNA extraction methods may influence telomere length measurement, and it may, therefore, be difficult to balance consistency in sampling protocol with making the most of available samples. We used two complementary approaches to examine the impacts of sample storage method on measurements of relative telomere length (RTL) by qPCR, particularly focusing on FTA (Flinders Technology Associates) cards as a long-term storage solution. We used blood samples from wandering albatrosses collected over 14 years and stored in three different ways (n = 179), and also blood samples from captive zebra finches (n = 30) that were each stored using three different methods. Sample storage method influenced RTL in both studies, and samples on FTA cards had significantly shorter RTL measurements. There was no significant correlation between RTL measured in zebra finch blood on FTA cards and the same samples stored either as frozen whole blood or as extracted DNA. These results highlight the importance of consistency of sampling protocol, particularly in the context of long-term field studies, and suggest that FTA cards should not be used as a long-term storage solution to measure RTL without validation.

Variation in the age of first reproduction: different strategies or individual quality?

Although age at first reproduction is a key demographic parameter that is probably under high selective pressure, it is highly variable and the cause of this variability is not well understood. Two non-exclusive hypotheses may explain such variability. It could be the expression of different individual strategies, i.e., different allocation strategies in fitness components, or the consequences of individual difference in intrinsic quality, i.e., some individuals always doing better than others in all fitness components. We tested these hypotheses in the Wandering Albatross investigating relationships between the age at first reproduction and subsequent adult demographic traits. Using finite mixture capture recapture modeling, we demonstrate that the age at first reproduction is negatively related to both reproductive performances and adult survival, suggesting that individual quality was an important factor explaining variation in the age at first reproduction. Our results suggest that age at first breeding is a good predictor of quality in this long-lived seabird species.

Population density and climate shape early-life survival and recruitment in a long-lived pelagic seabird.

1. Our understanding of demographic processes is mainly based on analyses of traits from the adult component of populations. Early-life demographic traits are poorly known mainly for methodological reasons. Yet, survival of juvenile and immature individuals is critical for the recruitment into the population and thus for the whole population dynamic, especially for long-lived species. This bias currently restrains our ability to fully understand population dynamics of long-lived species and life-history theory. 2. The goal of this study was to estimate the early-life demographic parameters of a long-lived species with a long immature period (9-10 years), to test for sex and age effects on these parameters and to identify the environmental factors encountered during the period of immaturity that may influence survival and recruitment. 3. Using capture-mark-recapture multievent models allowing us to deal with uncertain and unobservable individual states, we analysed a long-term data set of wandering albatrosses to estimate both age- and sex-specific early-life survival and recruitment. We investigated environmental factors potentially driving these demographic traits using climatic and fisheries covariates and tested for density dependence. 4. Our study provides for the first time an estimate of annual survival during the first 2 years at sea for an albatross species (0·801 ± 0·014). Both age and sex affected early-life survival and recruitment processes of this long-lived seabird species. Early-life survival and recruitment were highly variable across years although the sensitivity of young birds to environmental variability decreased with age. Early-life survival was negatively associated with sea surface temperature, and recruitment rate was positively related to both Southern Annular Mode and sea surface temperature. We found strong evidence for density-dependent mortality of juveniles. Population size explained 41% of the variation of this parameter over the study period. 5. These results indicate that early-life survival and recruitment were strongly age and sex dependent in a dimorphic long-lived species. In addition, early-life demographic parameters were affected by natal environmental conditions and by environmental conditions faced during the period of immaturity. Finally, our results constitute one of the first demonstrations of density dependence on juvenile survival in seabirds, with major consequences for our understanding of population dynamics in seabirds.

Wandering albatrosses exert high take-off effort only when both wind and waves are gentle.

The relationship between the environment and marine animal small-scale behavior is not fully understood. This is largely due to the difficulty in obtaining environmental datasets with a high spatiotemporal precision. The problem is particularly pertinent in assessing the influence of environmental factors in rapid, high energy-consuming behavior such as seabird take-off. To fill the gaps in the existing environmental datasets, we employed novel techniques using animal-borne sensors with motion records to estimate wind and ocean wave parameters and evaluated their influence on wandering albatross take-off patterns. Measurements revealed that wind speed and wave heights experienced by wandering albatrosses during take-off ranged from 0.7 to 15.4 m/s and 1.6 to 6.4 m, respectively. The four indices measured (flapping number, frequency, sea surface running speed, and duration) also varied with the environmental conditions (e.g., flapping number varied from 0 to over 20). Importantly, take-off was easier under higher wave conditions than under lower wave conditions at a constant wind speed, and take-off effort increased only when both wind and waves were gentle. Our data suggest that both ocean waves and winds play important roles for albatross take-off and advances our current understanding of albatross flight mechanisms.

Wandering albatrosses are large seabirds with one of the most impressive wingspans found in the animal kingdom. While they spend most of their time efficiently gliding above the waves, they do have to regularly land on sea to snatch their prey. To resume flight, the birds turn into the wind and flap their wings as they run on the surface of the ocean; this causes their heart to beat three to four times faster than normal. In contrast, flying barely leads to a change in pulse rate compared to rest. As for many other marine birds, sea take-offs therefore represent one of the major energy costs that albatrosses face when out foraging. Scientists have long assumed that the amount of effort required for this manoeuvre depends on factors such as wind speed and, potentially, the height of the waves. However, this is difficult to establish for sure because direct information about the environment that a bird faces as it takes off is rarely available. Often, the best that researchers can do is to reconstruct this data based on global weather patterns, ocean climatic models or evidence collected from nearby locations. To address this problem, Uesaka et al. devised innovative ways to use data from animal-borne sensors. They equipped 44 albatrosses with these instruments and recorded over 1,500 hours of foraging sea trips. Wind parameters such as speed and direction were estimated based on the animals' flying paths, and wave height calculated from their floating motion. Sensor data also gave an insight into the energy cost of each take-off, which was estimated based on four parameters (running duration, running speed, number of wing flaps, and flapping frequency). The analyses confirmed that albatrosses take off into a headwind, with stronger winds reducing the amount of effort required. However, wave height also had a profound impact, suggesting that this parameter should be included in future studies. Overall, the birds flapped their wings less and ran on the surface of the water for shorter amounts of time when the wind was strong, or the waves were high. Even with weak winds, take offs were easier when waves were taller, and they were most costly when both the sea and wind were calm. The work by Uesaka et al. helps to capture how environmental factors influence the energy balance of albatrosses and other marine birds. As ocean weather patterns become more volatile and extreme climate events more frequent, such knowledge is acutely needed to understand how these creatures may respond to their changing world.

Observations and models of across-wind flight speed of the wandering albatross.

Wandering albatrosses exploit wind shear by dynamic soaring (DS), enabling rapid, efficient, long-range flight. We compared the ability of a theoretical nonlinear DS model and a linear empirical model to explain the observed variation of mean across-wind airspeeds of GPS-tracked wandering albatrosses. Assuming a flight trajectory of linked, 137° turns, a DS cycle of 10 s and a cruise airspeed of 16 m s-1, the theoretical model predicted that the minimum wind speed necessary to support DS is greater than 3 m s-1. Despite this, tracked albatrosses were observed in flight at wind speeds as low as 2 m s-1. We hypothesize at these very low wind speeds, wandering albatrosses fly by obtaining additional energy from updrafts over water waves. In fast winds (greater than 8 m s-1), assuming the same 10 s cycle period and a turn angle (TA) of 90°, the DS model predicts mean across-wind airspeeds of up to around 50 m s-1. In contrast, the maximum observed across-wind mean airspeed of our tracked albatrosses reached an asymptote at approximately 20 m s-1. We hypothesize that this is due to birds actively limiting airspeed by making fine-scale adjustments to TAs and soaring heights in order to limit aerodynamic force on their wings.

Protein Deimination and Extracellular Vesicle Profiles in Antarctic Seabirds.

Pelagic seabirds are amongst the most threatened of all avian groups. They face a range of immunological challenges which seem destined to increase due to environmental changes in their breeding and foraging habitats, affecting prey resources and exposure to pollution and pathogens. Therefore, the identification of biomarkers for the assessment of their health status is of considerable importance. Peptidylarginine deiminases (PADs) post-translationally convert arginine into citrulline in target proteins in an irreversible manner. PAD-mediated deimination can cause structural and functional changes in target proteins, allowing for protein moonlighting in physiological and pathophysiological processes. PADs furthermore contribute to the release of extracellular vesicles (EVs), which play important roles in cellular communication. In the present study, post-translationally deiminated protein and EV profiles of plasma were assessed in eight seabird species from the Antarctic, representing two avian orders: Procellariiformes (albatrosses and petrels) and Charadriiformes (waders, auks, gulls and skuas). We report some differences between the species assessed, with the narrowest EV profiles of 50-200 nm in the northern giant petrel Macronectes halli, and the highest abundance of larger 250-500 nm EVs in the brown skua Stercorarius antarcticus. The seabird EVs were positive for phylogenetically conserved EV markers and showed characteristic EV morphology. Post-translational deimination was identified in a range of key plasma proteins critical for immune response and metabolic pathways in three of the bird species under study; the wandering albatross Diomedea exulans, south polar skua Stercorarius maccormicki and northern giant petrel. Some differences in Gene Ontology (GO) biological and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways for deiminated proteins were observed between these three species. This indicates that target proteins for deimination may differ, potentially contributing to a range of physiological functions relating to metabolism and immune response, as well as to key defence mechanisms. PAD protein homologues were identified in the seabird plasma by Western blotting via cross-reaction with human PAD antibodies, at an expected 75 kDa size. This is the first study to profile EVs and to identify deiminated proteins as putative novel plasma biomarkers in Antarctic seabirds. These biomarkers may be further refined to become useful indicators of physiological and immunological status in seabirds-many of which are globally threatened.

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.

Differences in boldness are repeatable and heritable in a long-lived marine predator.

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.