Long-lived Seabird Research Articles

Sex-Specific Variation in Foraging Behavior is Related to Telomere Length in a Long-Lived Seabird.

Foraging during breeding is a demanding activity linked to breeding investment and possibly constrained by individual quality. Telomere length, the protective nucleoproteins located at the ends of the chromosomes, is considered a trait reflecting somatic maintenance and individual quality. Therefore, foraging effort and parental investment may be positively related to telomere length, if individuals with longer telomeres are of better quality and thus able to maintain better body condition and allocate more resources to parental activities. In the brown booby (Sula leucogaster), we investigated if telomere length is related to body mass (a proxy of condition) and whether variation in foraging behavior and provisioning effort is related to telomere length or body mass. Then, we explored whether variation in foraging and provisioning influences the chick mass growth rate. In 34 pairs nesting in Isla de San Jorge, in the Gulf of California, México, we sampled their blood to estimate telomere length, measured their body mass, and for 10 days, recorded their foraging behavior via global positioning system (GPS) loggers and their chick provisioning rate and chicks' mass growth rate. We found a positive relationship between parents' body mass and telomere length. Body mass did not affect foraging behavior. Females with longer telomeres were more prone to travel longer distances toward offshore and deeper waters than females with shorter telomeres. In contrast, males with longer telomere lengths performed more nearshore foraging trips than males with shorter telomeres. The chick provisioning rate was unrelated to telomere length or body mass, but females fed the chick at a rate 2.4 times greater than males. Females' offshore foraging, but not males', was positively related to chick mass growth rate. Our results suggest that individual quality, indicated by telomere length, is an important driver of sex-specific, between-individual variation in foraging behavior, indirectly affecting offspring condition.

Longevity in Carnaby’s Cockatoo (Zanda latirostris) Carnaby, 1948

Context Carnaby’s Cockatoo Zanda latirostris is an endangered species endemic to south-western Australia. It has been the subject of long-term studies of its ecology from 1969 to the present. Aims This paper examines the maximum recorded life of the species in the wild. Methods The life spans of eight wild Carnaby’s Cockatoos that were more than 20 years old were compared with longevity records of long-lived birds recorded on the banding registers in Australia, USA, and UK. Key results Eight wild Carnaby’s Cockatoos were recorded living from 21 to 35 years, putting the species in the top 2% of all bird species in the wild for which there are longevity records. Conclusions The longevity of Carnaby’s Cockatoo is similar to that of long-lived seabirds. Implications Several years of immaturity and low reproductive output mean that Carnaby’s Cockatoos must be long-lived for the species to be sustainable. Conservation actions need to minimise threats to the lives of adult cockatoos.

Age-dependent shaping of the social environment in a long-lived seabird: a quantitative genetic approach.

Individual differences in social behaviour can result in fine-scale variation in spatial distribution and, hence, in the social environment experienced. Given the expected fitness consequences associated with differences in social environments, it is imperative to understand the factors that shape them. One potential such factor is age. Age-specific social behaviour-often referred to as 'social ageing'-has only recently attracted attention, requiring more empirical work across taxa. Here, we use 29 years of longitudinal data collected in a pedigreed population of long-lived, colonially breeding common terns (Sterna hirundo) to investigate sources of variation in, and quantitative genetic underpinnings of, an aspect of social ageing: the shaping of the social environment experienced, using the number of neighbours during breeding as a proxy. Our analyses reveal age-specific declines in the number of neighbours during breeding, as well as selective disappearance of individuals with a high number of neighbours. Moreover, we find this social trait, as well as individual variation in the slope of its age-specific decline, to be heritable. These results suggest that social ageing might underpin part of the variation in the overall multicausal ageing phenotype, as well as undergo microevolution, highlighting the potential role of social ageing as a facilitator for, or constraint of, the evolutionary potential of natural populations.This article is part of the discussion meeting issue 'Understanding age and society using natural populations'.

Mercury concentrations in blood and back feathers are repeatable, heritable and correlated in a long-lived seabird

Mercury pollution is increasing both in the environment and in various organisms, especially top-predators. If variation in individual mercury concentrations is underpinned by genetic among-individual differences in traits related to mercury uptake, storage or excretion, and results in variation in fitness, populations may have the potential to evolve in response to this development. Few studies, however, have been able to collect sufficient information to investigate the genetic basis of pollution levels. We ran Bayesian quantitative genetic analyses, combining pedigree information obtained from a marine top-predator, the common tern (Sterna hirundo), with total mercury concentrations (THg) measured in 1364 blood and 1560 back feather samples obtained from >600 individual birds across seven years. Blood and back feather THg concentrations differed in repeatability (19 vs. 64 %, respectively), but showed similar levels of heritability (c. 9 %) and evolvability (c. 2 %). Blood and back feather THg concentrations were positively correlated at the phenotypic, but not genetic, level. Although further work is needed to elucidate the uptake, storage or excretion pathways underlying these patterns, our study provides pioneering insights into the architecture of THg concentrations, and suggests that adaptation to environmental pollution may to some extent be possible.

A novel technique for estimating age and demography of long-lived seabirds (genus Pterodroma) using an epigenetic clock for Gould's petrel (Pterodroma leucoptera).

Understanding the demography of wildlife populations is a key component for ecological research, and where necessary, supporting the conservation and management of long-lived animals. However, many animals lack phenological changes with which to determine individual age; therefore, gathering this fundamental information presents difficulties. More so for species that are rare, highly mobile, migratory and those that reside in inaccessible habitats. Until recently, the primary method to measure demography is through labour intensive mark-recapture approaches, necessitating decades of effort for long-lived species. Gadfly petrels (genus: Pterodroma) are one such taxa that are overrepresented with threatened and declining species, and for which numerous aspects of their ecology present challenges for research, monitoring and recovery efforts. To overcome some of these challenges, we developed the first DNA methylation (DNAm) demography technique to estimate the age of petrels, using the epigenetic clock of Gould's petrels (Pterodroma leucoptera). We collected reference blood samples from known-aged Gould's petrels at a long-term monitored population on Cabbage Tree Island, Australia. Epigenetic ages were successfully estimated for 121 individuals ranging in age from zero (fledgling) to 30 years of age, showing a mean error of 2.24 ± 0.17 years between the estimated and real age across the population. This is the first development of an epigenetic clock using multiplex PCR sequencing in a bird. This method enables demography to be measured with relative accuracy in a single sampling trip. This technique can provide information for emerging demographic risks that can mask declines in long-lived seabird populations and be applied to other Pterodroma populations.

Leach’s storm-petrel (Hydrobates leucorhous), a long-lived seabird shows flexible, condition-dependent, feeding strategies in response to poor chick condition

BackgroundParent-offspring conflict represents the sensitive balance of resource allocation between self-maintenance and reproduction. Two strategies have been proposed to better understand how species manage this conflict. In fixed-level feeding behavior, parents feed offspring consistent quantities of food; while flexible feeding shows plasticity in parental allocation based on offspring need. Life-history theory predicts that parents of long-lived species prioritize their survival and may favor the fixed-level hypothesis to maximize lifetime reproductive success. In this study, we highlight the natural variation of parent-offspring allocation strategies within a unique population of Leach’s storm-petrels (Hydrobates leucorhous), and through month-long food supplementation and restriction manipulations, we investigate how chick condition affects parental provisioning during the chick-rearing period of reproduction.ResultsWe show that the parents upregulated chick feeding frequency of nutritionally deprived chicks, resulting in a larger total amount of food delivered during the study period. Additionally, the proportion of nights when both parents fed was highest in restricted chicks, and the proportion of nights when neither parents fed was lowest in restricted chicks, suggesting that storm-petrel parents shorten their foraging bouts to deliver food more often when their chicks are in relatively poor condition.ConclusionsOur results support that Leach’s storm-petrels use a flexible-level feeding strategy, suggesting that parents can assess offspring condition, and respond by feeding chicks at higher frequencies. These data provide insight on how a long-lived seabird balances its own energetic demands with that of their offspring during the reproductive period.

Diversity of major histocompatibility complex of II B gene and mate choice in a monogamous and long-lived seabird, the Little Auk (Alle alle).

The major histocompatibility complex (MHC) plays a key role in the adaptive immune system of vertebrates, and is known to influence mate choice in many species. In birds, the MHC has been extensively examined but mainly in galliforms and passerines while other taxa that represent specific ecological and evolutionary life-histories, like seabirds, are underexamined. Here, we characterized diversity of MHC Class II B exon 2 in a colonial pelagic seabird, the Little Auk (or Dovekie Alle alle). We further examined whether MHC variation could be maintained through balancing selection and disassortative mating. We found high polymorphism at the genotyped MHC fragment, characterizing 99 distinct alleles across 140 individuals from three populations. The alleles frequencies exhibited a similar skewed distribution in both sexes, with the four most commonly occurring alleles representing approximately 35% of allelic variation. The results of a Bayesian site-by-site selection analysis suggest evidence of balancing selection and no direct evidence for MHC-dependent disassortative mating preferences in the Little Auk. The latter result might be attributed to the high overall polymorphism of the examined fragment, which itself may be maintained by the large population size of the species.

Sex- and age-specific mercury accumulation in a long-lived seabird

Mercury levels in the environment are increasing, such that they are also expected to accumulate in top-predators, but individual-based longitudinal studies required to investigate this are rare. Between 2017 and 2023, we therefore collected 1314 blood samples from 588 individual common terns (Sterna hirundo) to examine how total blood mercury concentration changed with age, and whether this differed between the sexes. Blood mercury concentrations were highly variable, but all exceeded toxicity thresholds above which adverse health effects were previously observed. A global model showed blood mercury to be higher in older birds of both sexes. Subsequent models partitioning the age effect into within- and among-individual components revealed a linear within-individual accumulation with age in females, and a decelerating within-individual accumulation with age in males. Time spent at the (particularly contaminated) breeding grounds prior to sampling, as well as egg laying in females, were also found to affect mercury concentrations. As such, our study provides evidence that male and female common terns differentially accumulate mercury in their blood as they grow older and calls for further studies of the underlying mechanisms as well as its consequences for fitness components, such as reproductive performance and survival.

The challenges of independence: ontogeny of at-sea behaviour in a long-lived seabird

The challenges of independence: ontogeny of at-sea behaviour in a long-lived seabird

Telomere length links with physiological phenotype and breeding patterns in a long-lived seabird

Abstract Telomere length (TL) is known to covary with a suite of physiological traits involved in energy balances that may influence breeding success. Thus, TL may be an indicator of individual quality, influencing mate choice and breeding strategies. In the Brown Booby (Sula leucogaster), a long-lived seabird, we investigated in a total of 72 pairs whether TL may indicate the individual physiological phenotype by examining how it relates to mitochondrial DNA copy number (mtDNAcn) and corticosterone (CORT) levels. Then, we tested if TL is associated with mating patterns by looking for covariation with skin coloration (a condition-dependent sexual trait), whether there is assortative mating by TL, and if the degree of TL similarity between partners influences an individual’s likelihood of changing mates between reproductive seasons. Because environmental conditions can have important effects on the condition and reproductive strategies of individuals, the study was performed in 2 colonies with contrasting breeding conditions. We found that TL was positively related to mtDNAcn (but not CORT levels), suggesting that individuals with shorter telomeres may have a reduced mitochondrial density. TL was reflected in sexual coloration, but only in the colony with good breeding conditions. There was positive assortative mating by TL; however, the degree of assortative mating was unrelated to the probability of mate change, which greatly varied between the 2 colonies. Our results suggest that TL is associated with the physiological phenotype of individuals and their breeding patterns. Importantly, contrasting environmental conditions influenced the link between TL and sexual coloration and the propensity of individuals to change mate, highlighting the importance of environmental variation on mating patterns.

Sex-specific foraging behaviour in a long-lived seabird

Sex-specific foraging behaviour may lead to differences between the sexes in both resource acquisition and exposure to threats and thereby contribute to sex-specific reproductive roles or mortality. As such, it is important to identify in which species sex-specific foraging behaviour occurs. We deployed GPS devices to incubating common terns (Sterna hirundo) from a German breeding population to study how sex and spatial or temporal extrinsic factors influence the daily activity budget, foraging distribution, and trip characteristics of this slightly sexually size dimorphic seabird. Birds of both sexes only foraged during the day, showing peaks of activity after sunrise and before sunset, perhaps in response to temporal variation in prey availability and/or as a strategy to overcome or prepare for nocturnal fasting. Furthermore, foraging was more frequent around low tide and at the beginning of the flood tide and mainly occurred in shallow (< 5 m depth) and coastal waters (< 2 km from coastline) up to 20 km from the colony. Females rested less, foraged closer to the colony in more coastal waters, and showed a lower maximum flight speed than males. Males foraged more outside protected areas than females and showed higher variability in their foraging distribution throughout the tide cycle. As such, our study provides evidence for sex-specific aspects of foraging behaviour in common terns and underlines the importance of considering sex-specific foraging distributions when assessing the impact of at-sea threats on seabirds, knowledge of which should be incorporated when developing conservation management strategies.

Circulating corticosterone predicts near-term, while H/L ratio predicts long-term, survival in a long-lived seabird

Assessing stress in wild populations is important in many ecological and conservation contexts because the physiological responses of individuals to stressors can be used to identify at-risk populations and the ability to respond appropriately to stressors is related to individual quality and fitness. Yet, one of the great challenges in ecophysiology is linking physiological measures in wild animal populations with changes in individual fitness. Here, we examined two indices of stress, namely, circulating baseline corticosterone concentration ([Cort]) and the heterophil:lymphocyte (H/L) ratio, in a long-lived seabird, the Nazca booby (Sula granti) and their relationship with current individual state and subsequent survival and residual and lifetime reproductive success. [Cort] was related to sex, age, and current reproductive effort in in that males, older birds, and birds currently engaged in a breeding attempt birds had higher [Cort]. [Cort] was negatively associated with survival to the next breeding season. The H/L ratio was not associated with the current state of birds but predicted cohort-specific long-term survival. Lifespan and reproductive performance are correlated in Nazca boobies; therefore, our results suggest that the H/L ratio may be useful as an indicator of overall fitness, while [Cort] can be used to predict current or near-term fitness in this species. We further propose the H/L [or neutrophil/lymphocyte (N/L)] Ratio-Fitness Hypothesis, which posits that this ratio is repeatable within individuals and are negatively associated with fitness. This hypothesis needs to be tested in Nazca boobies and other species, and when supported by empirical evidence, then these ratios could be a powerful monitoring tool for assessing population health or identifying at-risk populations.

Compensatory Growth Is Accompanied by Changes in Insulin-Like Growth Factor 1 but Not Markers of Cellular Aging in a Long-Lived Seabird.

AbstractDeveloping organisms often plastically modify growth in response to environmental circumstances, which may be adaptive but is expected to entail long-term costs. However, the mechanisms that mediate these growth adjustments and any associated costs are less well understood. In vertebrates, one mechanism that may be important in this context is the highly conserved signaling factor insulin-like growth factor 1 (IGF-1), which is frequently positively related to postnatal growth and negatively related to longevity. To test this idea, we exposed captive Franklin's gulls (Leucophaeus pipixcan) to a physiologically relevant nutritional stressor by restricting food availability during postnatal development and examined the effects on growth, IGF-1, and two potential biomarkers of cellular and organismal aging (oxidative stress and telomeres). During food restriction, experimental chicks gained body mass more slowly and had lower IGF-1 levels than controls. Following food restriction, experimental chicks underwent compensatory growth, which was accompanied by an increase in IGF-1 levels. Interestingly, however, there were no significant effects of the experimental treatment or of variation in IGF-1 levels on oxidative stress or telomeres. These findings suggest that IGF-1 is responsive to changes in resource availability but is not associated with increased markers of cellular aging during development in this relatively long-lived species.

Holding time has limited impact on constitutive innate immune function in a long-lived Antarctic seabird, the Adélie penguin: implications for field studies.

There is great interest in measuring immune function in wild animals. Yet, field conditions often have methodological challenges related to handling stress, which can alter physiology. Despite general consensus that immune function is influenced by handling stress, previous studies have provided equivocal results. Furthermore, few studies have focused on long-lived species, which may have different stress-immune trade-offs compared to short-lived species that have primarily been tested. Here, we investigate whether capture and handling duration impacts innate immune function in a long-lived seabird, the Adélie penguin (Pygoscelis adeliae). We found no evidence for changes in three commonly used parameters of innate immune function upon holding time of up to 2h, suggesting that immune function in this species is more robust against handling than in other species. This opens up exciting possibilities for measuring immune function in species with similar life-histories even if samples cannot be taken directly after capture.

Increased foraging effort and reduced chick condition of razorbills under lower prey biomass in coastal Newfoundland, Canada

When resources are finite, individuals optimize energy allocation between survival and reproduction to maximize fitness. As food becomes more limited within foraging ranges of breeding colonies, long-lived seabirds are predicted to increase time spent foraging, and chick growth, breeding success and ultimately adult survival, will be reduced. Across 3 years (2017, 2019, 2020), we investigated responses of breeding razorbills Alca torda in coastal Newfoundland, Canada, to inter- and intra-annual variation in biomass of the primary forage fish, capelin Mallotus villosus, which migrate from offshore into coastal regions during the summer to spawn. We combined capelin biomass (hydroacoustic surveys) with chick-rearing razorbill foraging effort (GPS, temperature-depth recorders), dietary proportions (blood δ15N and δ13C) and adult/chick body condition. Peak capelin biomass was near the long-term average for the study area in 2017 (0.109 g m-2) and 2019 (0.098 g m-2) and the lowest on record in 2020 (0.002 g m-2). In 2017 and 2019, razorbill foraging effort decreased after spawning capelin arrived inshore, but this decrease was not observed in 2020 (mean ± SE trip distance: 12.8 ± 2.8 km in 2017, 14.3 ± 1.7 km in 2019, 150.4 ± 25.2 km in 2020; number of dives per trip: 48.4 ± 11.8 in 2017, 385.8 ± 67.4 in 2020). Increased foraging effort during 2020 was associated with lower chick and adult body condition, likely due to parental birds flying farther and diving more to capture capelin. Findings suggest that lower capelin biomass observed in recent years may have long-term population-level consequences for razorbills and other seabirds in this region.

Climate change and commercial fishing practices codetermine survival of a long-lived seabird.

Understanding the environmental mechanisms that govern population change is a fundamental objective in ecology. Although the determination of how top-down and bottom-up drivers affect demography is important, it is often equally critical to understand the extent to which, environmental conditions that underpin these drivers fluctuate across time. For example, associations between climate and both food availability and predation risk may suggest the presence of trophic interactions that may influence inferences made from patterns in ecological data. Analytical tools have been developed to account for these correlations, while providing opportunities to ask novel questions regarding how populations change across space and time. Here, we combine two modeling disciplines-path analysis and mark-recapture-recovery models-to explore whether shifts in sea-surface temperatures (SSTs) influenced top-down (entanglement in fishing equipment) or bottom-up (forage fish production) population constraints over 60 years, and the extent to which these covarying processes shaped the survival of a long-lived seabird, the Royal tern. We found that hemispheric trends in SST were associated with variation in the amount of fish harvested along the Atlantic coast of North America and in the Caribbean, whereas reductions in forage fish production were mostly driven by shifts in the amount of fish harvested by commercial fisheries throughout the North Atlantic the year prior. Although the indirect (i.e., stock depletion) and direct (i.e., entanglement) impacts of commercial fishing on Royal tern mortality has declined over the last 60 years, increased SSTs during this time period has resulted in a comparable increase in mortality risk, which disproportionately impacted the survival of the youngest age-classes of Royal terns. Given climate projections for the North Atlantic, our results indicate that threats to Royal tern population persistence in the Mid-Atlantic will most likely be driven by failures to recruit juveniles into the breeding population.

Age-Related Interactions with Wind During Migration Support the Hypothesis of Developmental Learning in a Migrating Long-Lived Seabird

Wind patterns shape migratory pathways and detours of many procellariiform bird species that seasonally migrate between hemispheres. These seabirds are long-lived, and the period of immaturity is presumed to be a time of development and learning the environment, specifically how to use wind to their advantage. We assess how wind encountered by individual Great Shearwaters (Ardenna gravis) varies along the migration journey and compare responses between presumed mature and immature birds (early and late, respectively) in southbound migration and mature birds in northbound migration. We analyze modeled Argos locations from 71 individual tracks of migratory Great Shearwaters with concurrent U (East/West) and V (North/South) wind components. Migration in seabirds is well studied, but there is limited quantitative work measuring individual birds directly interacting with wind and their associated changes in flight behavior during migration. We show that Great Shearwaters made optimal use of winds, and that different age groups made decisions that exposed them to different wind constraints. Overall, Great Shearwaters derived positive responses from wind under most conditions and did not rely on a drifting strategy, which would be suggested if wind effect (difference between ground and airspeed) was predominantly positive during migrations. Instead, they appeared to use a compensating strategy to achieve an acceptable course and speed. The difference we observed in migration phenologies suggests that by migrating later, immature birds might travel the path of least resistance and experience flight conditions that are less risky furthering their ability to withstand a variety of wind conditions encountered later in life as done by adults, which migrate earlier and are subject to more variable flight conditions. We conclude that like other procellariiforms, a longer period of sexual maturity is required to enhance flight performance and mediate energy expenditure through experiential learning and increased fitness.

Telomere length correlates with physiological and behavioural responses of a long-lived seabird to an ecologically relevant challenge.

Determinants of individual variation in reallocation of limited resources towards self-maintenance versus reproduction are not well known. We tested the hypothesis that individual heterogeneity in long-term ‘somatic state’ (i) explains variation in endocrine and behavioural responses to environmental challenges, and (ii) is associated with variation in strategies for allocating to self-maintenance versus reproduction. We used relative telomere length as an indicator of somatic state and experimentally generated an abrupt short-term reduction of food availability (withdrawal of food supplementation) for free-living seabirds (black-legged kittiwakes, Rissa tridactyla). Incubating male kittiwakes responded to withdrawal by increasing circulating corticosterone and losing more weight compared to continuously supplemented controls. Males with longer telomeres increased time in directed travel regardless of treatment, while experiencing smaller increases in corticosterone. Males with longer telomeres fledged more chicks in the control group and tended to be more likely to return regardless of treatment. This study supports the hypothesis that somatic state can explain variation in short-term physiological and behavioural responses to challenges, and longer-term consequences for fitness. Male kittiwakes with longer telomeres appear to have prioritized investment in self over investment in offspring under challenging conditions.

Higher mercury contamination is associated with shorter telomeres in a long-lived seabird – A direct effect or a consequence of among-individual variation in phenotypic quality?

Mercury is a heavy metal, which is pervasive and persistent in the marine environment. It bioaccumulates within organisms and biomagnifies in the marine food chain. Due to its high toxicity, mercury contamination is a major concern for wildlife and human health. Telomere length is a biomarker of aging and health, because it predicts survival, making it a potential tool to investigate sublethal effects of mercury contamination. However, the relationship between telomeres and mercury contamination is unclear. We measured feather mercury concentration in Cory's Shearwaters Calonectris borealis, long-lived seabirds and top predators, between 9 and 35 years of age and related it to telomere length in erythrocytes. Cory's Shearwaters with higher mercury concentrations had shorter telomeres and the effect was sex-dependent, reaching significance in males only. This may be explained by the fact that males have longer telomeres and higher and more variable mercury concentrations than females in this population. The mercury effect on telomere length was stronger on longer telomeres in the genome within individuals. We discuss the hypotheses that the negative correlation could either be a direct effect of mercury on telomere shortening and/or a consequence of variation in phenotypic quality among individuals that results in a covariation between mercury contamination and telomere length.

Episodes of high recruitment buffer against climate-driven mass mortality events in a North Pacific seabird population.

Longitudinal studies of marked animals provide an opportunity to assess the relative contributions of survival and reproductive output to population dynamics and change. Cassin's auklets are a long-lived seabird that maximizes annual reproductive effort in resource-rich years through a behaviour called double brooding, the initiation of a second breeding attempt following the success of the first during the same season. Our objective was to explore whether double brooding influenced population change by contributing a greater number of future recruits. We fit temporal symmetry models to 32 years of mark-recapture data of Cassin's auklets to infer the mechanisms underlying the observed variability in per capita recruitment rates. We found that periodic peaks in recruitment were explained by an increase in available nest sites, the proportion of the population double brooding 4years prior, and spring upwelling conditions. Estimates of population change suggests a relatively stable population throughout the time series, attributable to a 'floating' demographic class of sexually mature individuals excluded from breeding by competition which quickly fill vacant sites following periods of low adult survival. Our results highlight the importance of recruitment in maintaining the population of a long-lived seabird periodically impacted by adverse environmental conditions.