Mass mortality among colony-breeding seabirds in the German Wadden Sea in 2022 due to distinct genotypes of HPAIV H5N1 clade 2.3.4.4b.

Mass mortality was observed among colony-breeding seabirds in the German Wadden Sea area of the North Sea during the summer months of 2022. Several species' colonies were affected, most notably sandwich terns (Thalasseus sandvicensis), common terns (Sterna hirundo) and Germany's only northern gannet (Morus bassanus) colony on the island of Heligoland. Mortality in some tern colonies reached 40%, while other colonies were almost spared. In all cases, infections with the high-pathogenicity avian influenza virus (HPAIV) subtype H5N1 of clade 2.3.4.4b were identified to have caused the epidemic. Phylogenetic analysis of whole-genome sequences revealed that the outbreaks were dominated by two genotypes, Ger-10-21 N1.2 and Ger-10-21 N1.5, previously identified in Germany. Spatiotemporal analyses of phylogenetic data suggested that these viruses could have entered the continental North Sea coastal region via the British Isles. A close linkage of viruses from tern colonies in the German Wadden Sea was evident with further connections to breeding colonies in Belgium and the Netherlands, and further spread to Denmark and Poland. Several of the affected species are endangered, such that negative effects of epizootic HPAIV infections on populations are feared, with uncertain long-term consequences.

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.

Immunosenescence in the wild? A longitudinal study in a long-lived seabird.

Longitudinal studies of various vertebrate populations have demonstrated senescent declines in reproductive performance and survival probability to be almost ubiquitous. Longitudinal studies of potential underlying proximate mechanisms, however, are still scarce. Due to its critical function in the maintenance of health and viability, the immune system is among the potential (mediators of) proximate mechanisms that could underlie senescence. Here, we studied three innate immune parameters-haemagglutination titre, haemolysis titre and haptoglobin concentration-in a population of common terns (Sterna hirundo) known to undergo actuarial senescence. We repeatedly sampled birds of known sex and age across 11 years and used random regression models to (a) quantify how immune parameters vary among individuals and (b) describe within-individual age-specific changes in, and potential trade-offs between, immune parameters. Our models revealed no differences between males and females in haemagglutination titre and haptoglobin concentration, and very low among-individual variation in these parameters in general. Within individuals, haemagglutination titre increased with age, while haptoglobin concentration did not change. We found no indication for selective (dis)appearance in relation to haemagglutination titre or haptoglobin concentration, nor for the existence of a trade-off between them. Haemolysis was absent in the majority (76%) of samples. Common terns do not exhibit clear senescence in haemagglutination titre and haptoglobin concentration and show very little among-individual variation in these parameters in general. This may be explained by canalisation of the immune parameters or by the colonial breeding behaviour of our study species, but more longitudinal studies are needed to facilitate investigation of links between species' characteristics and immunosenescence in wild animals.

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.

Contrasting haemoparasite prevalence in larid species with divergent ecological niches and migration patterns.

Haemoparasites represent a diverse group of vector-borne parasites that infect a wide range of vertebrate hosts. In birds, haemoparasite infection rates may be associated with various ecological and life history traits, including habitat choice, colony size and migration distance. Here, we molecularly assessed the prevalence of 3 main haemoparasite genera (Plasmodium, Haemoproteus and Leucocytozoon) in 2 bird species with different habitat preferences and migratory behaviour: black-headed gulls (Chroicocephalus ridibundus) and common terns (Sterna hirundo). We found that gulls showed a much higher prevalence and diversity of Plasmodium or Haemoproteus (ca. 60% of individuals infected) than terns (zero prevalence). The prevalence of Leucocytozoon was low in both species (<3%). The differences in haemoparasite prevalences may be primarily driven by varying vector encounter rate resulting from different habitat preferences, as black-headed gulls mainly use vector-rich vegetated freshwater habitats, whereas common terns often use vector-poor coastal and brackish habitats. Since common terns migrate further than black-headed gulls, our results did not provide support for an association between haemoparasite prevalence and migratory distance. In gulls, we found a negative association between colony size and infection rates, suggestive of an ideal despotic distribution, and phylogenetic analyses of detected haemoparasite lineages provided evidence for higher host specificity in Haemoproteus than Plasmodium. Our results suggest that the preference for coastal areas and less vegetated habitats in terns may reduce haemoparasite infection rates compared to other larids, regardless of their migratory distance, emphasizing the role of ecological niches in parasite exposure.

How fitness consequences of early-life conditions vary with age in a long-lived seabird: A Bayesian multivariate analysis of age-specific reproductive values.

Evolutionary theory suggests that individuals can benefit from deferring the fitness cost of developing under poor conditions to later in life. Although empirical evidence for delayed fitness costs of poor developmental conditions is abundant, individuals that die prematurely have not often been incorporated when estimating fitness, such that age-specific fitness costs, and therefore the relative importance of delayed fitness costs are actually unknown. We developed a Bayesian statistical framework to estimate age-specific reproductive values in relation to developmental conditions. We applied it to data obtained from a long-term longitudinal study of common terns Sterna hirundo, using sibling rank to describe variation in developmental conditions. Common terns have a maximum of three chicks, and later hatching chicks acquire less food, grow more slowly and have a lower fledging probability than their earlier hatched siblings. We estimated fitness costs in adulthood to constitute c. 45% and 70% of the total fitness costs of hatching third and second, respectively, compared to hatching first. This was due to third-ranked hatchlings experiencing especially high pre-fledging mortality, while second-ranked hatchlings had lower reproductive success in adulthood. Both groups had slightly lower adult survival. There was, however, no evidence for sibling rank-specific rates of senescence. We additionally found years with low fledgling production to be associated with particularly strong pre-fledging selection on sibling rank, and with increased adult survival to the next breeding season. This suggests that adults reduce parental allocation to reproduction in poor years, which disproportionately impacts low-ranked offspring. Interpreting these results, we suggest that selection at the level of the individual offspring for delaying fitness costs is counteracted by selection for parental reduction in brood size when resources are limiting.

Connecting the data landscape of long-term ecological studies: The SPI-Birds data hub.

The integration and synthesis of the data in different areas of science is drastically slowed and hindered by a lack of standards and networking programmes. Long-term studies of individually marked animals are not an exception. These studies are especially important as instrumental for understanding evolutionary and ecological processes in the wild. Furthermore, their number and global distribution provides a unique opportunity to assess the generality of patterns and to address broad-scale global issues (e.g. climate change). To solve data integration issues and enable a new scale of ecological and evolutionary research based on long-term studies of birds, we have created the SPI-Birds Network and Database (www.spibirds.org)-a large-scale initiative that connects data from, and researchers working on, studies of wild populations of individually recognizable (usually ringed) birds. Within year and a half since the establishment, SPI-Birds has recruited over 120 members, and currently hosts data on almost 1.5 million individual birds collected in 80 populations over 2,000 cumulative years, and counting. SPI-Birds acts as a data hub and a catalogue of studied populations. It prevents data loss, secures easy data finding, use and integration and thus facilitates collaboration and synthesis. We provide community-derived data and meta-data standards and improve data integrity guided by the principles of Findable, Accessible, Interoperable and Reusable (FAIR), and aligned with the existing metadata languages (e.g. ecological meta-data language). The encouraging community involvement stems from SPI-Bird's decentralized approach: research groups retain full control over data use and their way of data management, while SPI-Birds creates tailored pipelines to convert each unique data format into a standard format. We outline the lessons learned, so that other communities (e.g. those working on other taxa) can adapt our successful model. Creating community-specific hubs (such as ours, COMADRE for animal demography, etc.) will aid much-needed large-scale ecological data integration.

Understanding the Social Dynamics of Breeding Phenology: Indirect Genetic Effects and Assortative Mating in a Long-Distance Migrant.

AbstractPhenological traits, such as the timing of reproduction, are often influenced by social interactions between paired individuals. Such partner effects may occur when pair members affect each other's prebreeding environment. Partner effects can be environmentally and/or genetically determined, and quantifying direct and indirect genetic effects is important for understanding the evolutionary dynamics of phenological traits. Here, using 26 years of data from a pedigreed population of a migratory seabird, the common tern (Sterna hirundo), we investigate male and female effects on female laying date. We find that female laying date harbors both genetic and environmental variation and is additionally influenced by the environmental and, to a lesser extent, genetic component of its mate. We demonstrate this partner effect to be largely explained by male arrival date. Interestingly, analyses of mating patterns with respect to arrival date show mating to be strongly assortative, and using simulations we show that assortative mating leads to overestimation of partner effects. Our study provides evidence for partner effects on breeding phenology in a long-distance migrant while uncovering the potential causal pathways underlying the observed effects and raising awareness for confounding effects resulting from assortative mating or other common environmental effects.

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.

Age-Specific Offspring Mortality Economically Tracks Food Abundance in a Piscivorous Seabird.

Earlier offspring mortality before independence saves resources for kin, which should be more beneficial when food is short. Using 24 years of data on age-specific common tern (Sterna hirundo) chick mortality, best described by the Gompertz function, and estimates of energy consumption per age of mortality, we investigated how energy wasted on nonfledged chicks depends on brood size, hatching order, and annual abundance of herring (Clupea harengus), the main food source. We found mortality directly after hatching (Gompertz baseline mortality) to be high and to increase with decreasing herring abundance. Mortality declined with age at a rate relatively insensitive to herring abundance. The sensitivity of baseline mortality to herring abundance reduced energy wasted on nonfledged chicks when herring was in short supply. Among chicks that did not fledge, last-hatched chicks were less costly than earlier-hatched chicks because of their earlier mortality. However, per hatchling produced, the least energy was wasted on chicks without siblings because their baseline mortality was most sensitive to herring abundance. We suggest that earlier mortality of offspring when food is short facilitates economic adjustment of posthatching parental investment to food abundance but that such economic brood reduction may be constrained by sibling competition.

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.

Live fast, don't die young: Survival-reproduction trade-offs in long-lived income breeders.

Trade-offs between survival and reproduction are at the core of life-history theory, and essential to understanding the evolution of reproductive tactics as well as population dynamics and stability. Factors influencing these trade-offs are multiple and often addressed in isolation. Further problems arise as reproductive states and survival in wild populations are estimated based on imperfect and potentially biased observation processes, which might lead to flawed conclusions. In this study, we aimed at elucidating trade-offs between current reproduction (both pregnancy and lactation), survival and future reproduction, including the specific costs of first reproduction, in long-lived, income breeding small mammals, an under-studied group. We developed a novel statistical framework that encapsulates the breeding life cycle of females, and accounts for incomplete information on female pregnancy and lactation and imperfect and biased recapture rates. We applied this framework to longitudinal data on two sympatric, closely related bat species (Myotis daubentonii and M. nattereri). We revealed the existence of several, to our knowledge previously unknown, trends in survival and breeding of these closely related, sympatric species and detected remarkable differences in their age and costs of first reproduction, as well as their survival-reproduction trade-offs. Our results indicate that species with this type of life history exhibit a mixture of patterns expected for long-lived and short-lived animals, and between income and capital breeders. Thus, we call for more studies to be conducted in similar study systems, increasing our ability to fully understand the evolutionary origin and fitness effects of trade-offs and senescence.

Embryonic growth rate affects telomere attrition: an experiment in a wild bird.

High growth rate is associated with a short lifespan, but the physiological basis for this trade-off is not well known. Telomere length predicts individual lifespan and in this study we investigated whether embryonic growth rate, manipulated using incubation temperature, affects erythrocyte telomere length in a wild bird species, the common tern (Sterna hirundo). A 1°C lower incubation temperature decreased growth rate by 5%, without affecting size at hatching. The slower growth was associated with an average telomere length that was 147 base pairs longer at hatching. If carried through to adulthood, this effect would correspond with an approximately 3 year longer lifespan. Our results thus suggest that an effect of growth rate on lifespan may be mediated by telomere dynamics or a physiological process reflected by telomere length.

On the ecological insights provided by a long-term study on an even longer-lived bird.

In Focus: Weimerskirch, H. (2018). Linking demographic processes and foraging ecology in wandering albatross-Conservation implications. Journal of Animal Ecology, 87, 945-955. https://doi.org/10.1111/1365-2656.12817 Long-term individual-based studies are extremely valuable resources to study how life histories are shaped by selection on between-individual variation in the acquisition and allocation of resources. In this issue, Weimerskirch (2018) synthesises a 50-year study, uniquely including 20 years of individual-based movement tracking, of the majestic wandering albatross. The synthesis shows how variation in foraging distribution and efficiency in relation to sex and age is reflected in physiology, fitness and population dynamics, and how understanding of such patterns and processes can aid conservation efforts. It thereby exemplifies why long-term individual-based studies are especially productive and informative and require maintenance and safeguarding.

Reduced telomere length in offspring of old fathers in a long-lived seabird.

Evidence for transgenerational effects of senescence, whereby offspring from older parents have a reduced lifetime reproductive success, is increasing. Such effects could arise from compromised germline maintenance in old parents, potentially reflected in reduced telomere length in their offspring. We test the relationship between parental age and offspring early-life telomere length in a natural population of common terns and find a significant negative correlation between paternal age and offspring telomere length. Offspring telomere length is reduced by 35 base pairs for each additional year of paternal age. We find no correlation with maternal age. These results fit with the idea of compromised germline maintenance in males, whose germline stem cells require continued division.

Early mortality saves energy: estimating the energetic cost of excess offspring in a seabird.

Offspring are often produced in excess as insurance against stochastic events or unpredictable resources. This strategy may result in high early-life mortality, yet age-specific mortality before offspring independence and its associated costs have rarely been quantified. In this study, we modelled age-specific survival from hatching to fledging using 24 years of data on hatching order (HO), growth and age of mortality of more than 15 000 common tern (Sterna hirundo) chicks. We found that mortality peaked directly after hatching, after which it declined rapidly. Mortality hazard was best described with the Gompertz function, and was higher with later HO, mainly due to differences in baseline mortality hazard, rather than age-dependent mortality. Based on allometric mass-metabolism relationships and detailed growth curves of starving chicks, we estimated that the average metabolizable energy intake of non-fledged chicks was only 8.7% of the metabolizable energy intake of successful chicks during the nestling phase. Although 54% of hatchlings did not fledge, our estimates suggest them to have consumed only 9.3% of the total energy consumption of all hatched chicks in the population before fledging. We suggest that rapid mortality of excess offspring is part of an adaptive brood reduction strategy to the benefit of the parents.

Quantitative assessment of the importance of phenotypic plasticity in adaptation to climate change in wild bird populations.

Predictions about the fate of species or populations under climate change scenarios typically neglect adaptive evolution and phenotypic plasticity, the two major mechanisms by which organisms can adapt to changing local conditions. As a consequence, we have little understanding of the scope for organisms to track changing environments by in situ adaptation. Here, we use a detailed individual-specific long-term population study of great tits (Parus major) breeding in Wytham Woods, Oxford, UK to parameterise a mechanistic model and thus directly estimate the rate of environmental change to which in situ adaptation is possible. Using the effect of changes in early spring temperature on temporal synchrony between birds and a critical food resource, we focus in particular on the contribution of phenotypic plasticity to population persistence. Despite using conservative estimates for evolutionary and reproductive potential, our results suggest little risk of population extinction under projected local temperature change; however, this conclusion relies heavily on the extent to which phenotypic plasticity tracks the changing environment. Extrapolating the model to a broad range of life histories in birds suggests that the importance of phenotypic plasticity for adjustment to projected rates of temperature change increases with slower life histories, owing to lower evolutionary potential. Understanding the determinants and constraints on phenotypic plasticity in natural populations is thus crucial for characterising the risks that rapidly changing environments pose for the persistence of such populations.

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.

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.