Spatially heterogeneous shifts in vegetation phenology induced by climate change threaten the integrity of the avian migration network.

Phenological responses to climate change frequently vary among trophic levels, which can result in increasing asynchrony between the peak energy requirements of consumers and the availability of resources. Migratory birds use multiple habitats with seasonal food resources along migration flyways. Spatially heterogeneous climate change could cause the phenology of food availability along the migration flyway to become desynchronized. Such heterogeneous shifts in food phenology could pose a challenge to migratory birds by reducing their opportunity for food availability along the migration path and consequently influencing their survival and reproduction. We develop a novel graph-based approach to quantify this problem and deploy it to evaluate the condition of the heterogeneous shifts in vegetation phenology for 16 migratory herbivorous waterfowl species in Asia. We show that climate change-induced heterogeneous shifts in vegetation phenology could cause a 12% loss of migration network integrity on average across all study species. Species that winter at relatively lower latitudes are subjected to a higher loss of integrity in their migration network. These findings highlight the susceptibility of migratory species to climate change. Our proposed methodological framework could be applied to migratory species in general to yield an accurate assessment of the exposure under climate change and help to identify actions for biodiversity conservation in the face of climate-related risks.

Heterogeneous selection on exploration behavior within and among West European populations of a passerine bird.

Heterogeneous selection is often proposed as a key mechanism maintaining repeatable behavioral variation ("animal personality") in wild populations. Previous studies largely focused on temporal variation in selection within single populations. The relative importance of spatial versus temporal variation remains unexplored, despite these processes having distinct effects on local adaptation. Using data from >3,500 great tits (Parus major) and 35 nest box plots situated within five West-European populations monitored over 4 to 18 y, we show that selection on exploration behavior varies primarily spatially, across populations, and study plots within populations. Exploration was, simultaneously, selectively neutral in the average population and year. These findings imply that spatial variation in selection may represent a primary mechanism maintaining animal personalities, likely promoting the evolution of local adaptation, phenotype-dependent dispersal, and nonrandom settlement. Selection also varied within populations among years, which may counteract local adaptation. Our study underlines the importance of combining multiple spatiotemporal scales in the study of behavioral adaptation.

Social Familiarity and Spatially Variable Environments Independently Determine Reproductive Fitness in a Wild Bird.

AbstractThe social interactions that an individual experiences are a key component of its environment and can have important consequences for reproductive success. The dear enemy effect posits that having familiar neighbors at a territory boundary can reduce the need for territory defense and competition and potentially increase cooperation. Although fitness benefits of reproducing among familiar individuals are documented in many species, it remains unclear to what extent these relationships are driven by direct benefits of familiarity itself versus other socioecological covariates of familiarity. We use 58 years of great tit (Parus major) breeding data to disentangle the relationship between neighbor familiarity, partner familiarity, and reproductive success while simultaneously considering individual and spatiotemporal effects. We find that neighbor familiarity was positively associated with reproductive success for females but not males, while an individual's familiarity with their breeding partner was associated with fitness benefits for both sexes. There was strong spatial heterogeneity in all investigated fitness components, but our findings were robust and significant over and above these effects. Our analyses are consistent with direct effects of familiarity on individuals' fitness outcomes. These results suggest that social familiarity can yield direct fitness benefits, potentially driving the maintenance of long-term bonds and evolution of stable social systems.

Disentangling the causes of age-assortative mating in bird populations with contrasting life-history strategies.

Age shapes fundamental processes related to behaviour, survival and reproduction, where age influences reproductive success, non-random mating with respect to age can magnify or mitigate such effects. Consequently, the correlation in partners' age across a population may influence its productivity. Despite widespread evidence for age-assortative mating, little is known about what drives this assortment and its variation. Specifically, the relative importance of active (same-age mate preference) and passive processes (assortment as a consequence of other spatial or temporal effects) in driving age assortment is not well understood. In this paper, we compare breeding data from a great tit and mute swan population (51- and 31-year datasets, respectively) to tease apart the contributions of pair retention, cohort age structure and active age-related mate selection to age assortment in species with contrasting life histories. Both species show age-assortative mating and variable assortment between years. However, we demonstrate that the drivers of age assortment differ between the species, as expected from their life histories and resultant demographic differences. In great tits, pair fidelity has a weak effect on age-assortative mating through pair retention; variation in age assortment is primarily driven by fluctuations in age structure from variable juvenile recruitment. Age-assortative mating is, therefore, largely passive, with no evidence consistent with active age-related mate selection. In mute swans, age assortment is partly explained by pair retention, but not population age structure, and evidence exists for active age-assortative pairing. This difference is likely to result from shorter life-spans in great tits compared with mute swans, leading to fundamental differences in their population age structure, whereby a larger proportion of great tit populations consist of a single age cohort. In mute swans, age-assortative pairing through mate selection may also be driven by greater age-dependent variation in fitness. The study highlights the importance of considering how different life histories and demographic differences arising from these affect population processes that appear congruent across species. We suggest that future research should focus on uncovering the proximate mechanisms that lead to variation in active age-assortative mate selection (as seen in mute swans); and the consequences of variation in age structure on the ecological and social functioning of wild populations.

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.

Phenological asynchrony: a ticking time-bomb for seemingly stable populations?

Climate change has been shown to induce shifts in the timing of life-history events. As a result, interactions between species can become disrupted, with potentially detrimental effects. Predicting these consequences has proven challenging. We apply structured population models to a well-characterised great tit-caterpillar model system and identify thresholds of temporal asynchrony, beyond which the predator population will rapidly go extinct. Our model suggests that phenotypic plasticity in predator breeding timing initially maintains temporal synchrony in the face of environmental change. However, under projections of climate change, predator plasticity was insufficient to keep pace with prey phenology. Directional evolution then accelerated, but could not prevent mismatch. Once predator phenology lagged behind prey by more than 24 days, rapid extinction was inevitable, despite previously stable population dynamics. Our projections suggest that current population stability could be masking a route to population collapse, if high greenhouse gas emissions continue.

Social learning of acoustic anti-predator cues occurs between wild bird species.

In many species, individuals gather information about their environment both through direct experience and through information obtained from others. Social learning, or the acquisition of information from others, can occur both within and between species and may facilitate the rapid spread of antipredator behaviour. Within birds, acoustic signals are frequently used to alert others to the presence of predators, and individuals can quickly learn to associate novel acoustic cues with predation risk. However, few studies have addressed whether such learning occurs only though direct experience or whether it has a social component, nor whether such learning can occur between species. We investigate these questions in two sympatric species of Parids: blue tits (Cyanistes caeruleus) and great tits (Parus major). Using playbacks of unfamiliar bird vocalizations paired with a predator model in a controlled aviary setting, we find that blue tits can learn to associate a novel sound with predation risk via direct experience, and that antipredator response to the sound can be socially transmitted to heterospecific observers, despite lack of first-hand experience. Our results suggest that social learning of acoustic cues can occur between species. Such interspecific social information transmission may help to mediate the formation of mixed-species aggregations.

Cue identification in phenology: A case study of the predictive performance of current statistical tools.

Changes in the timing of life-history events (phenology) are a widespread consequence of climate change. Predicting population resilience requires knowledge of how phenology is likely to change over time, which can be gained by identifying the specific environmental cues that drive phenological events. Cue identification is often achieved with statistical testing of candidate cues. As the number of methods used to generate predictions increases, assessing the predictive accuracy of different approaches has become necessary. This study aims to (a) provide an empirical illustration of the predictive ability of five commonly applied statistical methods for cue identification (absolute and relative sliding time window analyses, penalized signal regression, climate sensitivity profiles and a growing degree-day model) and (b) discuss approaches for implementing cue identification methods in different systems. Using a dataset of mean clutch initiation timing in wild great tits (Parus major), we explored how the days of the year identified as most important, and the aggregate statistic identified as a cue, differed between statistical methods and with respect to the time span of data used. Each method's predictive capacity was tested using cross-validation and assessed for robustness to varying sample size. We show that the identified critical time window of cue sensitivity was consistent across four of the five methods. The accuracy and precision of predictions differed by method with penalized signal regression resulting in the most accurate and most precise predictions in our case. Accuracy was maximal for near-future predictions and showed a relationship with time. The difference between predictions and observations systematically shifted across the study from preceding observations to lagging. This temporal trend in prediction error suggests that the current statistical tools either fail to capture a key component of the cue-phenology relationship, or the relationship itself is changing through time in our system. These two influences need to be teased apart if we are to generate realistic predictions of phenological change. We recommend future phenological studies to challenge the idea of a static cue-phenology relationship and should cross-validate results across multiple time periods.

To graze or gorge: consistency and flexibility of individual foraging tactics in tits.

An individual's foraging behaviour and time allocated to feeding have direct consequences for its fitness. Despite much research on population-level foraging decisions, few studies have investigated individual differences in fine-scale daily foraging patterns among wild animals. Here, we explore the consistency and plasticity of feeding tactics of individual great tits (Parus major) and blue tits (Cyanistes caeruleus), using a grid of 65 automated feeding stations in a 385-ha woodland, during three winters. We use a principal component analysis to describe individual variation in six feeding parameters and examine how these differences covary with dominance-linked attributes (species, age and sex), the personality trait 'exploration behaviour', distance to territory and local competition intensity. Analysis of 933 086 feeder visits by 3134 individuals revealed that the majority of variation in the timing of feeding was explained by two principal components. PC1 ('binge-eating'), accounting for 38% of variation, captured temporal clustering of feeding, with high repeatability both within and between years (r range: 0·42-0·55). PC2 ('transience'), accounting for 27% of variance, described how much individuals used feeders and was also repeatable (r: 0·34-0·62). While exhibiting consistent individual differences, birds also showed flexibility in foraging patterns, binge-eating less and using feeders more when they experienced greater local competition. Individuals in behaviourally dominant states (great tits, males and adults) binged more than subordinate birds (blue tits, females and juveniles) when their territories were distant from feeding stations. Moreover, great tits and males used feeders more than blue tits and females respectively, while birds feeding further from their territory used feeders less than those feeding closer. 'Exploration behaviour' was unrelated to both measures of daily foraging behaviour. This study presents some of the first evidence that birds use consistent alternative foraging tactics at a fine temporal scale. Individuals are consistent in their tactics, and also adjust their foraging behaviour with changes in local competition. Hence, studies of foraging behaviour should consider the extent to which such individual-level variability in foraging behaviour is under selection.

Scale-dependent phenological synchrony between songbirds and their caterpillar food source.

In seasonal environments, the timing of reproduction has important fitness consequences. Our current understanding of the determinants of reproductive phenology in natural systems is limited because studies often ignore the spatial scale on which animals interact with their environment. When animals use a restricted amount of space and the phenology of resources is spatially variable, selection may favor sensitivity to small-scale environmental variation. Population-level studies of how songbirds track the changing phenology of their food source have been influential in explaining how populations adjust to changing climates but have largely ignored the spatial scale at which phenology varies. We explored whether individual great tits (Parus major) synchronize their breeding with phenological events in their local environment and investigated the spatial scale at which this occurs. We demonstrate marked variation in the timing of food availability, at a spatial scale relevant to individual birds, and that such local variation predicts the breeding phenology of individuals. Using a 45-year data set, we show that measures of vegetation phenology at very local scales are the most important predictors of timing of breeding within years, suggesting that birds can fine-tune their phenology to that of other trophic levels. Knowledge of the determinants of variation in reproductive behavior at different spatial scales is likely to be critical in understanding how selection operates on breeding phenology in natural populations.

Who escapes detection? Quantifying the causes and consequences of sampling biases in a long-term field study.

Inferences drawn from long-term field studies are vulnerable to biases in observability of different classes of individuals, which may lead to biases in the estimates of selection, or fitness. Population surveys that monitor breeding individuals can introduce such biases by not identifying individuals that fail early in their reproductive attempts. Here, we quantify how the standard protocol for detecting breeding females introduces bias in a long-term population study of the great tit, Parus major. We do so by identifying females whose breeding attempts fail before they would normally be censused and explore whether this early failure can be predicted by a number of intrinsic and extrinsic factors. We investigate the effect of these biases on estimates of reproductive performance and selection. We show that females that go undetected by standard censusing because they fail early in their breeding attempt were less likely to have been previously trapped within our study site and were more likely to breed in poor-quality habitats. Furthermore, we demonstrate that this bias sampling had lead previous studies on this population to overestimate the reproductive performance of unringed females, which are likely to be immigrants to the population. Finally, we show that these biases in detectability influence estimates of selection on a key life-history trait. While these conclusions are specific to this study, we suggest that such effects are likely to be widespread and that more attention should be given to whether or not methods for surveying natural populations introduce systematic bias that will influence conclusions about ecological and evolutionary processes.

Shy birds play it safe: personality in captivity predicts risk responsiveness during reproduction in the wild.

Despite a growing body of evidence linking personality to life-history variation and fitness, the behavioural mechanisms underlying these relationships remain poorly understood. One mechanism thought to play a key role is how individuals respond to risk. Relatively reactive and proactive (or shy and bold) personality types are expected to differ in how they manage the inherent trade-off between productivity and survival, with bold individuals being more risk-prone with lower survival probability, and shy individuals adopting a more risk-averse strategy. In the great tit (Parus major), the shy-bold personality axis has been well characterized in captivity and linked to fitness. Here, we tested whether 'exploration behaviour', a captive assay of the shy-bold axis, can predict risk responsiveness during reproduction in wild great tits. Relatively slow-exploring (shy) females took longer than fast-exploring (bold) birds to resume incubation after a novel object, representing an unknown threat, was attached to their nest-box, with some shy individuals not returning within the 40 min trial period. Risk responsiveness was consistent within individuals over days. These findings provide rare, field-based experimental evidence that shy individuals prioritize survival over reproductive investment, supporting the hypothesis that personality reflects life-history variation through links with risk responsiveness.

Temperature synchronizes temporal variation in laying dates across European hole-nesting passerines.

Identifying the environmental drivers of variation in fitness-related traits is a central objective in ecology and evolutionary biology. Temporal fluctuations of these environmental drivers are often synchronized at large spatial scales. Yet, whether synchronous environmental conditions can generate spatial synchrony in fitness-related trait values (i.e., correlated temporal trait fluctuations across populations) is poorly understood. Using data from long-term monitored populations of blue tits (Cyanistes caeruleus, n = 31), great tits (Parus major, n = 35), and pied flycatchers (Ficedula hypoleuca, n = 20) across Europe, we assessed the influence of two local climatic variables (mean temperature and mean precipitation in February-May) on spatial synchrony in three fitness-related traits: laying date, clutch size, and fledgling number. We found a high degree of spatial synchrony in laying date but a lower degree in clutch size and fledgling number for each species. Temperature strongly influenced spatial synchrony in laying date for resident blue tits and great tits but not for migratory pied flycatchers. This is a relevant finding in the context of environmental impacts on populations because spatial synchrony in fitness-related trait values among populations may influence fluctuations in vital rates or population abundances. If environmentally induced spatial synchrony in fitness-related traits increases the spatial synchrony in vital rates or population abundances, this will ultimately increase the risk of extinction for populations and species. Assessing how environmental conditions influence spatiotemporal variation in trait values improves our mechanistic understanding of environmental impacts on populations.

Personality and problem-solving performance explain competitive ability in the wild.

Competitive ability is a major determinant of fitness, but why individuals vary so much in their competitiveness remains only partially understood. One increasingly prevalent view is that realized competitive ability varies because it represents alternative strategies that arise because of the costs associated with competitiveness. Here we use a population of great tits (Parus major) to explore whether individual differences in competitive ability when foraging can be explained by two traits that have previously been linked to alternative behavioural strategies: the personality trait 'exploration behaviour' and a simple cognitive trait, 'innovative problem-solving performance'. We assayed these traits under standardized conditions in captivity and then measured competitive ability at feeders with restricted access in the wild. Competitive ability was repeatable within individual males across days and correlated positively with exploration behaviour, representing the first such demonstration of a link between a personality trait and both competitive ability and food intake in the wild. Competitive ability was also simultaneously negatively correlated with problem-solving performance; individuals who were poor competitors were good at problem-solving. Rather than being the result of variation in 'individual quality', our results support the hypothesis that individual variation in competitive ability can be explained by alternative behavioural strategies.

Scale and state dependence of the relationship between personality and dispersal in a great tit population.

1. Dispersal is a key process in population biology and ecology. Although the general ecological conditions that lead to dispersal have been well studied, the causes of individual variation in dispersal are less well understood. A number of recent studies suggest that heritable temperament - or personality - traits are correlated with dispersal in the wild but the extent to which these 'personality-dispersal syndromes' are general, how they depend on an individual's state and on spatial scale and whether they are temporally stable, both within and across individuals, remains unclear. 2. Here, we examine the relationship between exploration behaviour - an axis of personality that appears to be important in animals generally - and a variety of dispersal processes over 6 years in a population of the great tit Parus major. 3. Exploration behaviour was higher in immigrant than in locally born juveniles, but the difference was much larger for individuals with a small body mass, though independent of sex, representing one of the first examples of a state-dependent effect in a personality-dispersal syndrome. 4. Despite a temporal trend in exploration behaviour at the population level, the difference between immigrants and locally born birds remained stable over time, both across and within individuals. This suggests that the personality difference between immigrants and locally born birds is established early in development, but that the process of immigration interacts with both personality and state. 5. We found that the number of immigrant parents a locally born bird had did not influence exploration behaviour, suggesting either the difference between immigrants and residents was environmental or that the effect is overridden by local environmental sources of variation. 6. In contrast to previous work, we found no evidence for links between personality and natal dispersal distance within the population, either in terms of an individual's own exploration behaviour or that of its parents. 7. Our results suggest that there are links between individual differences in personality and dispersal, but that these can be dependent on differences in state among individuals and on the scale over which dispersal is measured. Future work should aim to understand the differences between dispersal within and between populations and the ways in which personality and state interact to determine the outcome of these processes.

Exploring the causes and consequences of cooperative behaviour in wild animal populations using a social network approach.

Understanding why individuals carry out behaviours that benefit others, especially genetically unrelated others, has been a major undertaking in many fields and particularly in biology. Here, we focus on the cooperation literature from natural populations and present the benefits of a social network approach in terms of how it can help to identify and understand factors that influence the maintenance and spread of cooperation, but are not easily captured when solely considering independent dyadic interactions. We describe how various routes to cooperation can be tested within the social network framework. Applying the social network approach to data from natural populations can help to uncover the evolutionary and ecological pressures that lead to differences in cooperation and other social processes.

Strengthening the evidence base for temperature-mediated phenological asynchrony and its impacts.

Climate warming has caused the seasonal timing of many components of ecological food chains to advance. In the context of trophic interactions, the match-mismatch hypothesis postulates that differential shifts can lead to phenological asynchrony with negative impacts for consumers. However, at present there has been no consistent analysis of the links between temperature change, phenological asynchrony and individual-to-population-level impacts across taxa, trophic levels and biomes at a global scale. Here, we propose five criteria that all need to be met to demonstrate that temperature-mediated trophic asynchrony poses a growing risk to consumers. We conduct a literature review of 109 papers studying 129 taxa, and find that all five criteria are assessed for only two taxa, with the majority of taxa only having one or two criteria assessed. Crucially, nearly every study was conducted in Europe or North America, and most studies were on terrestrial secondary consumers. We thus lack a robust evidence base from which to draw general conclusions about the risk that climate-mediated trophic asynchrony may pose to populations worldwide.

Personality shapes pair bonding in a wild bird social system.

Mated pair bonds are integral to many animal societies, yet how individual variation in behaviour influences their formation remains largely unknown. In a population of wild great tits (Parus major), we show that personality shapes pair bonding: proactive males formed stronger pre-breeding pair bonds by meeting their future partners sooner and increasing their relationship strength at a faster rate. As a result, proactive males sampled fewer potential mates. Thus, personality may have important implications for social relationship dynamics and emergent social structure.

The shifting phenological landscape: Within- and between-species variation in leaf emergence in a mixed-deciduous woodland.

Many organisms rely on synchronizing the timing of their life-history events with those of other trophic levels-known as phenological matching-for survival or successful reproduction. In temperate deciduous forests, the extent of matching with the budburst date of key tree species is of particular relevance for many herbivorous insects and, in turn, insectivorous birds. In order to understand the ecological and evolutionary forces operating in these systems, we require knowledge of the factors influencing leaf emergence of tree communities. However, little is known about how phenology at the level of individual trees varies across landscapes, or how consistent this spatial variation is between different tree species. Here, we use field observations, collected over 2 years, to characterize within- and between-species differences in spring phenology for 825 trees of six species (Quercus robur, Fraxinus excelsior, Fagus sylvatica, Betula pendula, Corylus avellana, and Acer pseudoplatanus) in a 385-ha woodland. We explore environmental predictors of individual variation in budburst date and bud development rate and establish how these phenological traits vary over space. Trees of all species showed markedly consistent individual differences in their budburst timing. Bud development rate also varied considerably between individuals and was repeatable in oak, beech, and sycamore. We identified multiple predictors of budburst date including altitude, local temperature, and soil type, but none were universal across species. Furthermore, we found no evidence for interspecific covariance of phenology over space within the woodland. These analyses suggest that phenological landscapes are highly complex, varying over small spatial scales both within and between species. Such spatial variation in vegetation phenology is likely to influence patterns of selection on phenology within populations of consumers. Knowledge of the factors shaping the phenological environments experienced by animals is therefore likely to be key in understanding how these evolutionary processes operate.

Incubation behavior adjustments, driven by ambient temperature variation, improve synchrony between hatch dates and caterpillar peak in a wild bird population.

For organisms living in seasonal environments, synchronizing the peak energetic demands of reproduction with peak food availability is a key challenge. Understanding the extent to which animals can adjust behavior to optimize reproductive timing, and the cues they use to do this, is essential for predicting how they will respond to future climate change. In birds, the timing of peak energetic demand is largely determined by the timing of clutch initiation; however, considerable alterations can still occur once egg laying has begun. Here, we use a wild population of great tits (Parus major) to quantify individual variation in different aspects of incubation behavior (onset, duration, and daily intensity) and conduct a comprehensive assessment of the causes and consequences of this variation. Using a 54-year dataset, we demonstrate that timing of hatching relative to peak prey abundance (synchrony) is a better predictor of reproductive success than clutch initiation or clutch completion timing, suggesting adjustments to reproductive timing via incubation are adaptive in this species. Using detailed in-nest temperature recordings, we found that postlaying, birds improved their synchrony with the food peak primarily by varying the onset of incubation, with duration changes playing a lesser role. We then used a sliding time window approach to explore which spring temperature cues best predict variance in each aspect of incubation behavior. Variation in the onset of incubation correlated with mean temperatures just prior to laying; however, incubation duration could not be explained by any of our temperature variables. Daily incubation intensity varied in response to daily maximum temperatures throughout incubation, suggesting female great tits respond to temperature cues even in late stages of incubation. Our results suggest that multiple aspects of the breeding cycle influence the final timing of peak energetic demand. Such adjustments could compensate, in part, for poor initial timing, which has significant fitness impacts.