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.

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 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.

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.

Plasticity results in delayed breeding in a long-distant migrant seabird.

A major question for conservationists and evolutionary biologists is whether natural populations can adapt to rapid environmental change through micro-evolution or phenotypic plasticity. Making use of 17 years of data from a colony of a long-distant migratory seabird, the common tern (Sterna hirundo), we examined phenotypic plasticity and the evolutionary potential of breeding phenology, a key reproductive trait. We found that laying date was strongly heritable (0.27 ± 0.09) and under significant fecundity selection for earlier laying. Paradoxically, and in contrast to patterns observed in most songbird populations, laying date became delayed over the study period, by about 5 days. The discrepancy between the observed changes and those predicted from selection on laying date was explained by substantial phenotypic plasticity. The plastic response in laying date did not vary significantly among individuals. Exploration of climatic factors showed individual responses to the mean sea surface temperature in Senegal in December prior to breeding: Common terns laid later following warmer winters in Senegal. For each 1°C of warming of the sea surface in Senegal, common terns delayed their laying date in northern Germany by 6.7 days. This suggests that warmer waters provide poorer wintering resources. We therefore found that substantial plastic response to wintering conditions can oppose natural selection, perhaps constraining adaptation.

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.

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.

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.

Feather mercury concentrations in Southern Ocean seabirds: Variation by species, site and time.

We studied mercury contamination in 25 seabird species breeding along a latitudinal gradient across the Southern Ocean, from Gough Island (40°S) through Marion Island (47°S) to Byers Peninsula (63°S). Total mercury concentrations in body feather samples of adults caught at breeding colonies from 2008 to 2011 were determined. Krill (Euphausia spp.) and other zooplankton consumers had low mercury concentrations (gentoo penguin Pygoscelis papua, chinstrap penguin Pseudomonas Antarctica, common diving petrel Pelecanoides urinatrix, broad-billed prion Pachyptila vittata; mean levels 308-753 ng g(-1)), whereas seabirds consuming squid or carrion had high mercury concentrations (ascending order: Kerguelen petrel Aphrodroma brevirostris, southern giant petrel Macronectes giganteus, soft-plumaged petrel Pterodroma mollis, sooty albatross Phoebetria fusca, Atlantic petrel Pterodroma incerta, northern giant petrel Macronectes halli, great-winged petrel Pterodroma macroptera; 10,720-28038 ng g(-1)). The two species with the highest mercury concentrations, northern giant petrels and great-winged petrels, bred at Marion Island. Among species investigated at multiple sites, southern giant petrels had higher mercury levels at Marion than at Gough Island and Byers Peninsula. Mercury levels among Byers Peninsula seabirds were low, in two species even lower than levels measured 10 years before at Bird Island, South Georgia. Replicate measurements after about 25 years at Gough Island showed much higher mercury levels in feathers of sooty albatrosses (by 187%), soft-plumaged petrels (53%) and Atlantic petrels (49%). Concentrations similar to the past were detected in southern giant petrels at Gough and Marion islands, and in northern giant petrels at Marion. There were no clear indications that timing of moult or migratory behavior affected mercury contamination patterns among species. Causes of inter-site or temporal differences in mercury contamination could not be verified due to a lack of long-term data related to species' diet and trophic levels, which should be collected in future together with data on mercury contamination.

Archiving Primary Data: Solutions for Long-Term Studies.

The recent trend for journals to require open access to primary data included in publications has been embraced by many biologists, but has caused apprehension amongst researchers engaged in long-term ecological and evolutionary studies. A worldwide survey of 73 principal investigators (Pls) with long-term studies revealed positive attitudes towards sharing data with the agreement or involvement of the PI, and 93% of PIs have historically shared data. Only 8% were in favor of uncontrolled, open access to primary data while 63% expressed serious concern. We present here their viewpoint on an issue that can have non-trivial scientific consequences. We discuss potential costs of public data archiving and provide possible solutions to meet the needs of journals and researchers.

Organochlorine and mercury residues in eggs of the lesser kestrel (Falco naumanni) from a long term study in the eastern Mediterranean.

Organochlorine and mercury residues were analyzed in unhatched eggs of the lesser kestrel (Falco naumanni) (2002-2012) in central Greece. Concentrations graded as ∑DDTs > ∑PCBs > HCB > ∑HCHs > ∑Chlordanes. Temporal declines were found in the concentrations of ∑DDTs, ∑HCHs and ∑Chlordanes but not in Hg, HCB and ∑PCBs. TEQs of PCBs and their degree of metabolisation showed no time trend. The reproductive parameters showed neither a temporal trend nor a significant year effect. No relationships occurred between the reproductive parameters per year and nest type (natural, artificial) with any of the contaminants analyzed except HCB influenced by year and clutch size. Low pollutant concentrations suggest that either lesser kestrels ranged across the year in unpolluted areas or may be caused by their short food chain. The low concentrations seem improbable to have affected the reproduction of these birds, although critical levels are still to be defined.

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.

Sex-specific pathways of parental age effects on offspring lifetime reproductive success in a long-lived seabird.

The conditions under which individuals are reared vary and sensitivity of offspring to such variation is often sex-dependent. Parental age is one important natal condition with consequences for aspects of offspring fitness, but reports are mostly limited to short-term fitness consequences and do not take into account offspring sex. Here we used individual-based data from a large colony of a long-lived seabird, the common tern Sterna hirundo, to investigate longitudinal long-term fitness consequences of parental age in relation to both offspring and parental sex. We found that recruited daughters from older mothers suffered from reduced annual reproductive success. Recruited sons from older fathers were found to suffer from reduced life span. Both effects translated to reductions in offspring lifetime reproductive success. Besides revealing novel sex-specific pathways of transgenerational parental age effects on offspring fitness, which inspire studies of potential underlying mechanisms, our analyses show that reproductive senescence is only observed in the common tern when including transgenerational age effects. In general, our study shows that estimates of selective pressures underlying the evolution of senescence, as well as processes such as age-dependent mate choice and sex allocation, will depend on whether causal transgenerational effects exist and are taken into account.

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.

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.