The effect of climate change on avian offspring production: A global meta-analysis.

Climate change affects timing of reproduction in many bird species, but few studies have investigated its influence on annual reproductive output. Here, we assess changes in the annual production of young by female breeders in 201 populations of 104 bird species (N = 745,962 clutches) covering all continents between 1970 and 2019. Overall, average offspring production has declined in recent decades, but considerable differences were found among species and populations. A total of 56.7% of populations showed a declining trend in offspring production (significant in 17.4%), whereas 43.3% exhibited an increase (significant in 10.4%). The results show that climatic changes affect offspring production through compounded effects on ecological and life history traits of species. Migratory and larger-bodied species experienced reduced offspring production with increasing temperatures during the chick-rearing period, whereas smaller-bodied, sedentary species tended to produce more offspring. Likewise, multi-brooded species showed increased breeding success with increasing temperatures, whereas rising temperatures were unrelated to reproductive success in single-brooded species. Our study suggests that rapid declines in size of bird populations reported by many studies from different parts of the world are driven only to a small degree by changes in the production of young.

Telomere length is heritable and genetically correlated with lifespan in a wild bird.

Telomeres are protective caps at the end of eukaryotic chromosomes that shorten with age and in response to stressful or resource-demanding conditions. Their length predicts individual health and lifespan across a wide range of animals, but whether the observed positive association between telomere length and lifespan is environmentally induced, or set at conception due to a shared genetic basis, has not been tested in wild animals. We applied quantitative genetic "animal models" to longitudinal telomere measurements collected over a 10-year period from individuals of a wild seabird (common tern; Sterna hirundo) with known pedigree. We found no variation in telomere shortening with age among individuals at the phenotypic and genetic level, and only a small permanent environmental effect on adult telomere length. Instead, we found telomere length to be highly heritable and strongly positively genetically correlated with lifespan. Such heritable differences between individuals that are set at conception may present a hitherto underappreciated component of variation in somatic state.

Variation and correlation in the timing of breeding of North Atlantic seabirds across multiple scales.

Timing of breeding, an important driver of fitness in many populations, is widely studied in the context of global change, yet despite considerable efforts to identify environmental drivers of seabird nesting phenology, for most populations we lack evidence of strong drivers. Here we adopt an alternative approach, examining the degree to which different populations positively covary in their annual phenology to infer whether phenological responses to environmental drivers are likely to be (a) shared across species at a range of spatial scales, (b) shared across populations of a species or (c) idiosyncratic to populations. We combined 51 long-term datasets on breeding phenology spanning 50 years from nine seabird species across 29 North Atlantic sites and examined the extent to which different populations share early versus late breeding seasons depending on a hierarchy of spatial scales comprising breeding site, small-scale region, large-scale region and the whole North Atlantic. In about a third of cases, we found laying dates of populations of different species sharing the same breeding site or small-scale breeding region were positively correlated, which is consistent with the hypothesis that they share phenological responses to the same environmental conditions. In comparison, we found no evidence for positive phenological covariation among populations across species aggregated at larger spatial scales. In general, we found little evidence for positive phenological covariation between populations of a single species, and in many instances the inter-year variation specific to a population was substantial, consistent with each population responding idiosyncratically to local environmental conditions. Black-legged kittiwake Rissa tridactyla was the exception, with populations exhibiting positive covariation in laying dates that decayed with the distance between breeding sites, suggesting that populations may be responding to a similar driver. Our approach sheds light on the potential factors that may drive phenology in our study species, thus furthering our understanding of the scales at which different seabirds interact with interannual variation in their environment. We also identify additional systems and phenological questions to which our inferential approach could be applied.

Telomere length is repeatable, shortens with age and reproductive success, and predicts remaining lifespan in a long-lived seabird.

Telomeres are protective caps at the end of chromosomes, and their length is positively correlated with individual health and lifespan across taxa. Longitudinal studies have provided mixed results regarding the within-individual repeatability of telomere length. While some studies suggest telomere length to be highly dynamic and sensitive to resource-demanding or stressful conditions, others suggest that between-individual differences are mostly present from birth and relatively little affected by the later environment. This dichotomy could arise from differences between species, but also from methodological issues. In our study, we used the highly reliable Terminal Restriction Fragment analysis method to measure telomeres over a 10-year period in adults of a long-lived seabird, the common tern (Sterna hirundo). Telomeres shortened with age within individuals. The individual repeatability of age-dependent telomere length was high (>0.53), and independent of the measurement interval (i.e., one vs. six years). A small (R2  = .01), but significant part of the between-individual variation in telomere length was, however, explained by the number of fledglings produced in the previous year, while reproduction in years prior to the previous year had no effect. We confirmed that age-dependent telomere length predicted an individual's remaining lifespan. Overall, our study suggests that the majority of between-individual variation in adult telomere length is consistent across adult life, and that a smaller part of the variation can be explained by dynamic factors, such as reproduction.

The diversity of population responses to environmental change.

The current extinction and climate change crises pressure us to predict population dynamics with ever-greater accuracy. Although predictions rest on the well-advanced theory of age-structured populations, two key issues remain poorly explored. Specifically, how the age-dependency in demographic rates and the year-to-year interactions between survival and fecundity affect stochastic population growth rates. We use inference, simulations and mathematical derivations to explore how environmental perturbations determine population growth rates for populations with different age-specific demographic rates and when ages are reduced to stages. We find that stage- vs. age-based models can produce markedly divergent stochastic population growth rates. The differences are most pronounced when there are survival-fecundity-trade-offs, which reduce the variance in the population growth rate. Finally, the expected value and variance of the stochastic growth rates of populations with different age-specific demographic rates can diverge to the extent that, while some populations may thrive, others will inevitably go extinct.

Contrasting heterozygosity-fitness correlations across life in a long-lived seabird.

Selection is a central force underlying evolutionary change and can vary in strength and direction, for example across time and space. The fitness consequences of individual genetic diversity have often been investigated by testing for multilocus heterozygosity-fitness correlations (HFCs), but few studies have been able to assess HFCs across life stages and in both sexes. Here, we test for HFCs using a 26-year longitudinal individual-based data set from a large population of a long-lived seabird (the common tern, Sterna hirundo), where 7,974 chicks and breeders of known age were genotyped at 15 microsatellite loci and sampled for life-history traits over the complete life cycle. Heterozygosity was not correlated with fledging or post-fledging prospecting probabilities, but was positively correlated with recruitment probability. For breeders, annual survival was not correlated with heterozygosity, but annual fledgling production was negatively correlated with heterozygosity in males and highest in intermediately heterozygous females. The contrasting HFCs among life stages and sexes indicate differential selective processes and emphasize the importance of assessing fitness consequences of traits over complete life histories.

Better the devil you know: common terns stay with a previous partner although pair bond duration does not affect breeding output.

In a monogamous species two partners contribute to the breeding process. We study pair formation as well as the effect of pair bond length and age on breeding performance, incorporating individual heterogeneity, based on a high-quality dataset of a long-lived seabird, the common tern (Sterna hirundo). To handle missing information and model the complicated processes driving reproduction, we use a hierarchical Bayesian model of the steps that lead to the number of fledglings, including processes at the individual and the pair level. The results show that the age of both partners is important for reproductive performance, with similar patterns for both sexes and individual heterogeneity in reproductive performance, but pair bond length is not. The terns are more likely to choose a former partner independent of the previous breeding outcome with that partner, which suggests a tendency to retain the partner chosen at the beginning of the breeding career.

Telomere length reflects reproductive effort indicated by corticosterone levels in a long-lived seabird.

Telomere length (TL) is a candidate biomarker of ageing and phenotypic quality, but little is known of the (physiological) causes of TL variation. We previously showed that individual common terns Sterna hirundo with high reproductive success had short telomeres independent of age, and this pattern was particularly strong in the longer telomeres of the within-individual TL distribution. To test whether this relation can be attributed to effects of reproductive effort, we investigated baseline corticosterone in relation to reproductive success (number of fledglings) and TL. In this context, we assume that variation in baseline corticosterone can be interpreted as index of energy expenditure and allostatic load. Males with higher corticosterone levels during incubation, compared between and within individuals, achieved higher reproductive success and had shorter telomeres. The effect on telomeres was more pronounced in corticosterone measured later in incubation and in the longer telomeres of the within-individual TL distribution. Female corticosterone level during incubation was neither related to reproductive success nor to TL. That we observed these effects only in males mirrors different parental roles during reproduction in the common tern, where males do most of the chick provisioning. The negative association between reproductive success and TL suggests individual differences in reproductive effort as reflected in, or mediated by, baseline corticosterone. We see this result as a promising step towards unravelling the physiological causes of variation in TL and the costs of reproduction.

Male-biased sex allocation in ageing parents; a longitudinal study in a long-lived seabird.

Optimal sex allocation is frequency-dependent, but senescence may cause behaviour at old age to be suboptimal. We investigated whether sex allocation changes with parental age, using 16 years of data comprising more than 2500 molecularly sexed offspring of more than 600 known-age parents in common terns (Sterna hirundo), slightly sexually size-dimorphic seabirds. We decomposed parental age effects into within-individual change and sex allocation-associated selective (dis)appearance. Individual parents did not differ consistently in sex allocation, but offspring sex ratios at fledging changed from female- to male-biased as parents aged. Sex ratios at hatching were not related to parental age, suggesting sons to outperform daughters after hatching in broods of old parents. Our results call for the integration of sex allocation theory with theory on ageing and demography, as a change in sex allocation with age per se will cause the age structure of a population to affect the frequency-dependent benefits and the age-specific strength of selection on sex allocation.

Seabird diversity hotspot linked to ocean productivity in the Canary Current Large Marine Ecosystem.

Upwelling regions are highly productive habitats targeted by wide-ranging marine predators and industrial fisheries. In this study, we track the migratory movements of eight seabird species from across the Atlantic; quantify overlap with the Canary Current Large Marine Ecosystem (CCLME) and determine the habitat characteristics that drive this association. Our results indicate the CCLME is a biodiversity hotspot for migratory seabirds; all tracked species and more than 70% of individuals used this upwelling region. Relative species richness peaked in areas where sea surface temperature averaged between 15 and 20°C, and correlated positively with chlorophyll a, revealing the optimum conditions driving bottom-up trophic effects for seabirds. Marine vertebrates are not confined by international boundaries, making conservation challenging. However, by linking diversity to ocean productivity, our research reveals the significance of the CCLME for seabird populations from across the Atlantic, making it a priority for conservation action.

Contrasting between- and within-individual trait effects on mortality risk in a long-lived seabird.

Individual life span is the most important determinant of lifetime reproductive success and fitness across taxa. Identifying the relationships between life-history traits and survival therefore is fundamental to understanding the evolution of a species' traits. Especially important in this respect is to separate the contributions of between- and within-individual trait effects, because only such an approach can identify markers of individual quality and expose within-individual processes such as aging or the occurrence of costs of reproduction. Here we report a rigorous cross-trait comparison in which we quantify effects of between- and within- individual variation in phenology, body mass, and reproductive performance on mortality risk in a long-lived seabird, the Common Tern Sterna hirundo. Between individuals, earlier arrival at the breeding colony, earlier egg-laying, greater body mass, and more successful reproduction are associated with a lower mortality risk, and are markers of individual quality. The standardized between-individual effects of arrival and laying date especially stand out, suggesting that phenology represents the best proxy for life span. In contrast, within individuals, earlier phenology, greater body mass, and more successful reproduction are associated with a higher mortality risk, as is a reduced probability of breeding. After correcting for changes in traits with age, within-individual effects of phenology, breeding probability, clutch size, and egg volume remain significantly associated with mortality risk, which reveals survival costs of early arrival and initial investment in reproduction, but suggests terminal effects in breeding probability. Overall, our study illustrates the usefulness of separating between- and within-individual trait effects on fitness measures to identify markers of individual quality and life-history trade-offs in natural populations.

Age-dependent trait variation: the relative contribution of within-individual change, selective appearance and disappearance in a long-lived seabird.

Within populations, the expression of phenotypic traits typically varies with age. Such age-dependent trait variation can be caused by within-individual change (improvement, senescence, terminal effects) and/or selective (dis)appearance of certain phenotypes among older age classes. In this study, we applied two methods (decomposition and mixed modelling) to attribute age-dependent variation in seven phenological and reproductive traits to within-individual change and selective (dis)appearance, in a long-lived seabird, the common tern (Sterna hirundo). At the population level, all traits, except the probability to breed, improved with age (i.e. phenology advanced and reproductive output increased). Both methods identified within-individual change as the main responsible process, and, within individuals, performance improved until age 6-13, before levelling off. In contrast, within individuals, breeding probability decreased to age 10, then levelled off. Effects of selective appearance and disappearance were small, but showed that longer-lived individuals had a higher breeding probability and bred earlier and that younger recruits performed better throughout life than older recruits in terms of both phenology and reproductive performance. In the year prior to death, individuals advanced reproduction, suggesting terminal investment. The decomposition method attributed more age-dependent trait variation to selective disappearance than the mixed-modelling method: 14-36% versus 0-8%, respectively, which we identify to be due to covariance between rates of within-individual change and selective (dis)appearance leading to biased results from the decomposition method. We conclude that the decomposition method is ideal for visualizing processes underlying population change in performance from one age class to the next, but that a mixed-modelling method is required to investigate the significance and relative contribution of age effects. Considerable variation in the contribution of the different age processes between the seven phenotypic traits studied, as well as notable differences between species in patterns of age-dependent trait expression, calls for better predictions regarding optimal allocation strategies with age.

Fitness prospects: effects of age, sex and recruitment age on reproductive value in a long-lived seabird.

Reproductive value is an integrated measure of survival and reproduction fundamental to understanding life-history evolution and population dynamics, but little is known about intraspecific variation in reproductive value and factors explaining such variation, if any. By applying generalized additive mixed models to longitudinal individual-based data of the common tern Sterna hirundo, we estimated age-specific annual survival probability, breeding probability and reproductive performance, based on which we calculated age-specific reproductive values. We investigated effects of sex and recruitment age (RA) on each trait. We found age effects on all traits, with survival and breeding probability declining with age, while reproductive performance first improved with age before levelling off. We only found a very small, marginally significant, sex effect on survival probability, but evidence for decreasing age-specific breeding probability and reproductive performance with RA. As a result, males had slightly lower age-specific reproductive values than females, while birds of both sexes that recruited at the earliest ages of 2 and 3 years (i.e. 54% of the tern population) had somewhat higher fitness prospects than birds recruiting at later ages. While the RA effects on breeding probability and reproductive performance were statistically significant, these effects were not large enough to translate to significant effects on reproductive value. Age-specific reproductive values provided evidence for senescence, which came with fitness costs in a range of 17-21% for the sex-RA groups. Our study suggests that intraspecific variation in reproductive value may exist, but that, in the common tern, the differences are small.

Survival and local recruitment are driven by environmental carry-over effects from the wintering area in a migratory seabird.

We estimated annual apparent survival rates, as well as local recruitment rates in different age groups and for different breeding status in the common tern Sterna hirundo using mark-recapture analysis on a long-term individual-based dataset from a breeding colony in Germany. Strong inter-annual variability in survival rates became apparent, especially in prospectors. Local recruitment also varied strongly between years and age groups. To explain these fluctuations, we linked survival and recruitment estimates to several environmental covariates expected to be limiting during the wintering period and migration, including the global climate indices of North Atlantic Oscillation and Southern Oscillation, fish abundance indices, and marine primary productivity in the West African wintering area. Contrary to expectations, global indices did not seem to be linked strongly to vital rates. Results showed that primary productivity had the strongest effect on annual survival, especially in young and inexperienced individuals. Primary productivity in the wintering area was also strongly associated with the probability of recruitment in the following breeding season, indicating that conditions during winter can have carry-over effects on the life cycle of individuals.

Within the genome, long telomeres are more informative than short telomeres with respect to fitness components in a long-lived seabird.

Telomeres, DNA-protein structures at chromosome ends, shorten with age, and telomere length has been linked to age-related diseases and survival. In vitro studies revealed that the shortest telomeres trigger cell senescence, but whether the shortest telomeres are also the best biomarker of ageing is not known. We measured telomeres in erythrocytes of wild common terns Sterna hirundo using terminal restriction fragment analysis. This yields a distribution of telomere lengths for each sample, and we investigated how different telomere subpopulations (percentiles) varied in their relation to age and fitness proxies. Longer telomeres within a genome lost more base pairs with age and were better predictors of survival than shorter telomeres. Likewise, fitness proxies such as arrival date at the breeding grounds and reproductive success were best predicted by telomere length at the higher percentiles. Our finding that longer telomeres within a genome predict fitness components better than the shorter telomeres indicates that they are a more informative ageing biomarker. This finding contrasts with the fact that cell senescence is triggered by the shortest telomeres. We suggest that this paradox arises, because longer telomeres lose more base pairs per unit time and thus better reflect the various forms of stress that accelerate telomere shortening, and that telomeres primarily function as biomarker because their shortening reflects cumulative effects of various stressors rather than reflecting telomere-induced cell senescence.

Immigrants are attracted by local pre-breeders and recruits in a seabird colony.

Immigration is a major demographic factor shaping population dynamics. However, due to methodological difficulties, the extent of immigration and factors affecting immigration are insufficiently studied. This is also true for seabird colonies. We estimated annual immigration based on a long-term study of a colony of common terns Sterna hirundo marked with transponders, using a Bayesian integrated population model that links colony size and productivity with individual life histories. Strong annual fluctuations in the number of immigrants were found. To identify whether colony-specific covariates influenced immigration, we related the number of immigrants to various proxy variables for breeding site quality, specifically colony size, productivity, number of local subadults and local recruits. Numbers of local recruits and local subadults showed strong positive correlations with number of immigrants. We found that variation in immigration rate had strongly contributed to variation in colony growth rate, more so than variation in local recruitment or adult survival. Collectively, results suggest that immigration strongly affects colony growth rate, that the driving force behind immigration is natal dispersal and that immigrants were attracted by local recruits.

Predicting reproductive success from hormone concentrations in the common tern (Sterna hirundo) while considering food abundance.

In birds, reproductive success is mainly a function of skill or environmental conditions, but it can also be linked to hormone concentrations due to their effect on behavior and individual decisions made during reproduction. For example, a high prolactin concentration is required to express parental behaviors such as incubation or guarding and feeding the young. Corticosterone level, on the other hand, is related to energy allocation or stress and foraging or provisioning effort. In this study, we measured individual baseline prolactin and corticosterone between 2006 and 2012 in breeding common terns (Sterna hirundo) using blood-sucking bugs. Reproductive parameters as well as prey abundance on a local and a wider scale were also determined during this period. Baseline prolactin and corticosterone varied significantly between years, as did breeding success. At the individual level, prolactin was positively and corticosterone was negatively linked to herring and sprat abundance. At the population level, we also found a negative link between corticosterone and prey abundance, probably reflecting overall foraging conditions. High prolactin during incubation was mainly predictive of increased hatching success, potentially by supporting more constant incubation and nest-guarding behavior. It was also positively linked to a lesser extent with fledging success, which could indicate a high feeding rate of young. Corticosterone concentration was positively related to high breeding success, which may be due to increased foraging activity and feeding of young. In general, our study shows that baseline prolactin and corticosterone levels during incubation can predict reproductive success, despite the presence of an interval between sampling and hatching or fledging of young.

Response of testosterone and corticosterone plasma levels to the challenge of sibling competition: a study in common terns.

The hormonal response to social challenges has been widely studied, however, most work focused on adult behavior in a reproductive context although developing animals also encounter important social challenges early in life. We studied the relationship between acute sibling competition and plasma corticosterone (CORT) and testosterone (T) in common tern (Sterna hirundo) chicks, a species whose young compete for access to food by scramble interactions. Blood samples were taken in nests with two and only one single chick both immediately after a feeding bout and in non-challenged controls. We found that T levels were lower in siblings challenged by a feeding bout as compared to controls, which may be explained by the fact that T suppresses begging behavior and is only elevated in response to territorial intrusion but not sibling competition in a related species. Singletons had, corrected for body condition, generally lower CORT levels than siblings suggesting that growing up with siblings creates a competitive environment in which high CORT levels are sustained irrespective of a social challenge. CORT levels were also negatively correlated with body condition and were higher in males than in females. The latter may be related to sex-specific food requirements and susceptibility to stress. Our results suggest a possible suppressive effect of acute sibling competition on T secretion, and a positive effect on CORT levels by longer term sibling competition. The degree to which these dynamics are related to begging or aggression, or both, needs further experimental work.

How life history influences population dynamics in fluctuating environments.

A major question in ecology is how age-specific variation in demographic parameters influences population dynamics. Based on long-term studies of growing populations of birds and mammals, we analyze population dynamics by using fluctuations in the total reproductive value of the population. This enables us to account for random fluctuations in age distribution. The influence of demographic and environmental stochasticity on the population dynamics of a species decreased with generation time. Variation in age-specific contributions to total reproductive value and to stochastic components of population dynamics was correlated with the position of the species along the slow-fast continuum of life-history variation. Younger age classes relative to the generation time accounted for larger contributions to the total reproductive value and to demographic stochasticity in "slow" than in "fast" species, in which many age classes contributed more equally. In contrast, fluctuations in population growth rate attributable to stochastic environmental variation involved a larger proportion of all age classes independent of life history. Thus, changes in population growth rates can be surprisingly well explained by basic species-specific life-history characteristics.

Telomere length reflects phenotypic quality and costs of reproduction in a long-lived seabird.

Telomere length is associated with cellular senescence, lifestyle and ageing. Short telomeres indicate poor health in humans and reduced life expectancy in several bird species, but little is known about telomeres in relation to phenotypic quality in wild animals. We investigated telomere lengths in erythrocytes of known-age common terns (Sterna hirundo), a migratory seabird, in relation to arrival date and reproductive performance. Cross-sectional data revealed that, independent of age, individuals with short telomeres performed better: they arrived and reproduced earlier in the season and had more chicks in the nest. The latter effect was stronger the older the brood and stronger in males, which do most of the chick provisioning. Longitudinal data confirmed this pattern: compared with birds that lost their brood, birds that raised chicks beyond the 10th nestling day experienced higher telomere attrition from one year to the next. However, more detailed analysis revealed that the least and most successful individuals lost the fewest base pairs compared with birds with intermediate success. Our results suggest that reproductive success is achieved at the expense of telomeres, but that individual heterogeneity in susceptibility to such detrimental effects is important, as indicated by low telomere loss in the most successful birds.