Population links between an insectivorous bird and moths disentangled through national-scale monitoring data.

Insects are key components of food chains, and monitoring data provides new opportunities to identify trophic relationships at broad spatial and temporal scales. Here, combining two monitoring datasets from Great Britain, we reveal how the population dynamics of the blue tit Cyanistes caeruleus are influenced by the abundance of moths - a core component of their breeding diet. We find that years with increased population growth for blue tits correlate strongly with high moth abundance, but population growth in moths and birds is less well correlated; suggesting moth abundance directly affects bird population change. Next, we identify moths that are important components of blue tit diet, recovering associations to species previously identified as key food sources such as the winter moth Operoptera brumata. Our work provides new evidence that insect abundance impacts bird population dynamics in natural communities and provides insight into spatial diet turnover at a national-scale.

Spatial consistency in drivers of population dynamics of a declining migratory bird.

Many migratory species are in decline across their geographical ranges. Single-population studies can provide important insights into drivers at a local scale, but effective conservation requires multi-population perspectives. This is challenging because relevant data are often hard to consolidate, and state-of-the-art analytical tools are typically tailored to specific datasets. We capitalized on a recent data harmonization initiative (SPI-Birds) and linked it to a generalized modelling framework to identify the demographic and environmental drivers of large-scale population decline in migratory pied flycatchers (Ficedula hypoleuca) breeding across Britain. We implemented a generalized integrated population model (IPM) to estimate age-specific vital rates, including their dependency on environmental conditions, and total and breeding population size of pied flycatchers using long-term (34-64 years) monitoring data from seven locations representative of the British breeding range. We then quantified the relative contributions of different vital rates and population structure to changes in short- and long-term population growth rate using transient life table response experiments (LTREs). Substantial covariation in population sizes across breeding locations suggested that change was the result of large-scale drivers. This was supported by LTRE analyses, which attributed past changes in short-term population growth rates and long-term population trends primarily to variation in annual survival and dispersal dynamics, which largely act during migration and/or nonbreeding season. Contributions of variation in local reproductive parameters were small in comparison, despite sensitivity to local temperature and rainfall within the breeding period. We show that both short- and long-term population changes of British breeding pied flycatchers are likely linked to factors acting during migration and in nonbreeding areas, where future research should be prioritized. We illustrate the potential of multi-population analyses for informing management at (inter)national scales and highlight the importance of data standardization, generalized and accessible analytical tools, and reproducible workflows to achieve them.

Major population splits coincide with episodes of rapid climate change in a forest-dependent bird.

Climate change influences population demography by altering patterns of gene flow and reproductive isolation. Direct mutation rates offer the possibility for accurate dating on the within-species level but are currently only available for a handful of vertebrate species. Here, we use the first directly estimated mutation rate in birds to study the evolutionary history of pied flycatchers (Ficedula hypoleuca). Using a combination of demographic inference and species distribution modelling, we show that all major population splits in this forest-dependent system occurred during periods of increased climate instability and rapid global temperature change. We show that the divergent Spanish subspecies originated during the Eemian-Weichselian transition 115-104 thousand years ago (kya), and not during the last glacial maximum (26.5-19 kya), as previously suggested. The magnitude and rates of climate change during the glacial-interglacial transitions that preceded population splits in pied flycatchers were similar to, or exceeded, those predicted to occur in the course of the current, human-induced climate crisis. As such, our results provide a timely reminder of the strong impact that episodes of climate instability and rapid temperature changes can have on species' evolutionary trajectories, with important implications for the natural world in the Anthropocene.

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.

Gradients in richness and turnover of a forest passerine's diet prior to breeding: A mixed model approach applied to faecal metabarcoding data.

Rather little is known about the dietary richness and variation of generalist insectivorous species, including birds, due primarily to difficulties in prey identification. Using faecal metabarcoding, we provide the most comprehensive analysis of a passerine's diet to date, identifying the relative magnitudes of biogeographic, habitat and temporal trends in the richness and turnover in diet of Cyanistes caeruleus (blue tit) along a 39 site and 2° latitudinal transect in Scotland. Faecal samples were collected in 2014-2015 from adult birds roosting in nestboxes prior to nest building. DNA was extracted from 793 samples and we amplified COI and 16S minibarcodes. We identified 432 molecular operational taxonomic units that correspond to putative dietary items. Most dietary items were rare, with Lepidoptera being the most abundant and taxon-rich prey order. Here, we present a statistical approach for estimation of gradients and intersample variation in taxonomic richness and turnover using a generalised linear mixed model. We discuss the merits of this approach over existing tools and present methods for model-based estimation of repeatability, taxon richness and Jaccard indices. We found that dietary richness increases significantly as spring advances, but changes little with elevation, latitude or local tree composition. In comparison, dietary composition exhibits significant turnover along temporal and spatial gradients and among sites. Our study shows the promise of faecal metabarcoding for inferring the macroecology of food webs, but we also highlight the challenge posed by contamination and make recommendations of laboratory and statistical practices to minimise its impact on inference.

A Spatial Perspective on the Phenological Distribution of the Spring Woodland Caterpillar Peak.

A classic system for studying trophic mismatch focuses on the timing of the spring caterpillar peak in relation to the breeding time and productivity of woodland passerine birds. Most work has been conducted in single-site oak woodlands, and little is known about how insights generalize to other woodland types or across space. Here we present the results of a 3-year study on the species composition and temporal distribution of the spring caterpillar peak on different tree taxa across 40 woodland sites spanning 2° of latitude in Scotland. We used molecular barcoding to identify 62 caterpillar species, with winter moth (Operophtera brumata) being the most abundant, comprising one-third of the sample. Oak (Quercus sp.) and willow (Salix sp.) hosted significantly higher caterpillar abundances than other tree taxa, with winter moth exhibiting similar trends and invariantly proportionate across tree taxa. Caterpillar peak phenology was broadly similar between tree taxa. While latitude had little effect, increasing elevation increased the height of the caterpillar peak and retarded timing by 3.7 days per 100 m. These findings extend our understanding of how mismatch may play out spatially, with caterpillar peak date varying with elevation and tree taxa varying in the caterpillar resource that they host.

The environmental predictors of spatio-temporal variation in the breeding phenology of a passerine bird.

Establishing the cues or constraints that influence avian timing of breeding is the key to accurate prediction of future phenology. This study aims to identify the aspects of the environment that predict the timing of two measures of breeding phenology (nest initiation and egg laying date) in an insectivorous woodland passerine, the blue tit (Cyanistes caeruleus). We analyse data collected from a 220 km, 40-site transect over 3 years and consider spring temperatures, tree leafing phenology, invertebrate availability and photoperiod as predictors of breeding phenology. We find that mean night-time temperature in early spring is the strongest predictor of both nest initiation and lay date and suggest this finding is most consistent with temperature acting as a constraint on breeding activity. Birch budburst phenology significantly predicts lay date additionally to temperature, either as a direct cue or indirectly via a correlated variable. We use cross-validation to show that our model accurately predicts lay date in two further years and find that similar variables predict lay date well across the UK national nest record scheme. This work refines our understanding of the principal factors influencing the timing of tit reproductive phenology and suggests that temperature may have both a direct and indirect effect.

Phenological sensitivity to climate change is higher in resident than in migrant bird populations among European cavity breeders.

Many organisms adjust their reproductive phenology in response to climate change, but phenological sensitivity to temperature may vary between species. For example, resident and migratory birds have vastly different annual cycles, which can cause differential temperature sensitivity at the breeding grounds, and may affect competitive dynamics. Currently, however, adjustment to climate change in resident and migratory birds have been studied separately or at relatively small geographical scales with varying time series durations and methodologies. Here, we studied differential effects of temperature on resident and migratory birds using the mean egg laying initiation dates from 10 European nest box schemes between 1991 and 2015 that had data on at least one resident tit species and at least one migratory flycatcher species. We found that both tits and flycatchers advanced laying in response to spring warming, but resident tit populations advanced more strongly in relation to temperature increases than migratory flycatchers. These different temperature responses have already led to a divergence in laying dates between tits and flycatchers of on average 0.94 days per decade over the current study period. Interestingly, this divergence was stronger at lower latitudes where the interval between tit and flycatcher phenology is smaller and winter conditions can be considered more favorable for resident birds. This could indicate that phenological adjustment to climate change by flycatchers is increasingly hampered by competition with resident species. Indeed, we found that tit laying date had an additional effect on flycatcher laying date after controlling for temperature, and this effect was strongest in areas with the shortest interval between both species groups. Combined, our results suggest that the differential effect of climate change on species groups with overlapping breeding ecology affects the phenological interval between them, potentially affecting interspecific interactions.

Early life conditions influence fledging success and subsequent local recruitment rates in a declining migratory songbird, the Whinchat Saxicola rubetra.

Life history traits and environmental conditions influence reproductive success in animals, and consequences of these can influence subsequent survival and recruitment into breeding populations. Understanding influences on demographic rates is required to determine the causes of decline. Migratory species experience spatially and temporally variable conditions across their annual cycle, making identifying where the factors influencing demographic rates operate challenging. Here, we use the Whinchat Saxicola rubetra as a model declining long-distance migrant bird. We analyse 10 years of data from 247 nesting attempts and 2519 post-fledging observations of 1193 uniquely marked nestlings to examine the influence of life history traits, habitat characteristics and weather on survival of young from the nestling stage to local recruitment into the natal population. We detected potential silver spoon effects where conditions during the breeding stage influence subsequent apparent local recruitment rates, with higher recruitment for fledglings from larger broods, and recruitment rate negatively related to rainfall that chicks experienced in-nest. Additionally, extreme temperatures experienced pre- and post-fledging increased fledging success and recruitment rate. However, we could not determine whether this was driven by temperature influencing mortality during the post-fledging period or later in the annual cycle. Brood size declined with hatching date. In-nest survival increased with brood size and was highest at local temperature extremes. Furthermore, nest survival was highest at nests surrounded with 40%-60% vegetation cover of Bracken Pteridium aquilinum within 50 m of the nest. Our results show that breeding phenology and environmental factors may influence fledging success and recruitment in songbird populations, with conditions experienced during the nestling stage influencing local recruitment rates in Whinchats (i.e. silver spoon effect). Recruitment rates are key drivers of songbird population dynamics. Our results help identify some of the likely breeding season mechanisms that could be important population drivers.

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.

Captive husbandry and socialization of the red-billed chough (Pyrrhocorax pyrrhocorax).

Since the 1970s, Paradise Park Wildlife Sanctuary in Cornwall, United Kingdom, has built up a captive flock of red-billed choughs Pyrrhocorax pyrrhocorax and over 30 years has developed successful methods of keeping, breeding, and appropriately socializing them in captivity. A total of 77 nests reached the egg stage with 27 nests producing at least one young and 48 young fledging in total. Several components are important in achieving successful breeding and socialization. Provision of live food, especially ant's eggs and small mealworms and crickets, in the first days after hatching is essential, improving the condition of adults and survival of nestlings. Situating aviaries in quiet areas, away from public view, is important. Socialization in family groups during the winter months and allowing choughs to choose partners induces better compatibility. Introduction of nest cameras greatly improved young survival through early identification of health problems enabling treatment of young between hatching and 10-days old, when mortality is otherwise highest, and enabling precautionary medication shortly after hatching. We show that clutch size increases significantly with female age and that direct intervention such as artificial egg incubation and hand rearing can be successful and worthwhile, but its requirement is reduced by closer monitoring. Red-billed choughs provide a good model species to further develop captive management and release techniques that can then be applied to critically endangered species that show similar social and long-learning behaviors. Captive breeding programs can play an important role in such work through provision of suitable birds and supporting avicultural expertise.

Accounting for predator species identity reveals variable relationships between nest predation rate and habitat in a temperate forest songbird.

Nest predation is the primary cause of nest failure in most ground-nesting bird species. Investigations of relationships between nest predation rate and habitat usually pool different predator species. However, such relationships likely depend on the specific predator involved, partly because habitat requirements vary among predator species. Pooling may therefore impair our ability to identify conservation-relevant relationships between nest predation rate and habitat. We investigated predator-specific nest predation rates in the forest-dependent, ground-nesting wood warbler Phylloscopus sibilatrix in relation to forest area and forest edge complexity at two spatial scales and to the composition of the adjacent habitat matrix. We used camera traps at 559 nests to identify nest predators in five study regions across Europe. When analyzing predation data pooled across predator species, nest predation rate was positively related to forest area at the local scale (1000 m around nest), and higher where proportion of grassland in the adjacent habitat matrix was high but arable land low. Analyses by each predator species revealed variable relationships between nest predation rates and habitat. At the local scale, nest predation by most predators was higher where forest area was large. At the landscape scale (10,000 m around nest), nest predation by buzzards Buteo buteo was high where forest area was small. Predation by pine martens Martes martes was high where edge complexity at the landscape scale was high. Predation by badgers Meles meles was high where the matrix had much grassland but little arable land. Our results suggest that relationships between nest predation rates and habitat can depend on the predator species involved and may differ from analyses disregarding predator identity. Predator-specific nest predation rates, and their relationships to habitat at different spatial scales, should be considered when assessing the impact of habitat change on avian nesting success.

Species-specific song responses emerge as a by-product of tuning to the local dialect.

Oscine birds preferentially respond to certain sounds over others from an early age, which focuses subsequent learning onto sexually relevant songs.1,2,3 Songs vary both across species and, due to cultural evolution, among populations of the same species. As a result, early song responses are expected to be shaped by selection both to avoid the fitness costs of cross-species learning4 and to promote learning of population-typical songs.5 These sources of selection are not mutually exclusive but can result in distinct geographic patterns of song responses in juvenile birds: if the risks of interspecific mating are the main driver of early song discrimination, then discrimination should be strongest where closely related species co-occur.4 In contrast, if early discrimination primarily facilitates learning local songs, then it should be tuned to songs typical of the local dialect.5,6,7 Here, we experimentally assess the drivers of song discrimination in nestling pied flycatchers (Ficedula hypoleuca). We first demonstrate that early discrimination against the songs of the closely related collared flycatcher (F. albicollis) is not strongly affected by co-occurrence. Second, across six European populations, we show that nestlings' early song responses are tuned to their local song dialect and that responses to the songs of collared flycatchers are similarly weak as to those of other conspecific dialects. Taken together, these findings provide clear experimental support for the hypothesis that cultural evolution, in conjunction with associated learning predispositions, drives the emergence of pre-mating reproductive barriers.

Bird populations most exposed to climate change are less sensitive to climatic variation.

The phenology of many species shows strong sensitivity to climate change; however, with few large scale intra-specific studies it is unclear how such sensitivity varies over a species' range. We document large intra-specific variation in phenological sensitivity to temperature using laying date information from 67 populations of two co-familial European songbirds, the great tit (Parus major) and blue tit (Cyanistes caeruleus), covering a large part of their breeding range. Populations inhabiting deciduous habitats showed stronger phenological sensitivity than those in evergreen and mixed habitats. However, populations with higher sensitivity tended to have experienced less rapid change in climate over the past decades, such that populations with high phenological sensitivity will not necessarily exhibit the strongest phenological advancement. Our results show that to effectively assess the impact of climate change on phenology across a species' range it will be necessary to account for intra-specific variation in phenological sensitivity, climate change exposure, and the ecological characteristics of a population.

Multiple environmental gradients affect spatial variation in the productivity of a tropical bird population.

1. Spatial variation in habitat quality and its demographic consequences have important implications for the regulation of animal populations. Theoretically, habitat quality is typically viewed as a single gradient from 'poor' to 'good', but in wild populations it is possible that there are multiple environmental gradients that determine spatial variation in demography. 2. Understanding environmental gradients is important to gain mechanistic insights into important population processes, but also to understand how populations might respond to environmental change. Here, we explore habitat and elevation gradients and their implications for population persistence using detailed long-term data on 600 individuals of the Mauritius kestrel. These data allow us to statistically separate spatial variation in demography from variation arising out of individual or environmental quality and explore its relationships with habitat and topography. 3. Birds that breed earlier in the season have higher reproductive success, and we found that the timing of breeding varies significantly between territories. This variation is primarily driven by elevation, with birds breeding progressively later as elevation increases. 4. Pre-fledging survival from the egg to fledgling stage (independently of timing), and recruitment, also varied significantly between territories. This variation is driven by the habitat surrounding breeding sites with increasing agricultural encroachment causing survival and recruitment to decline. 5. Taken together, our results suggest that there are likely to be multiple environmental gradients affecting spatial variation in productivity in wild populations, and hence multiple and different routes through which environmental change might have consequences for population dynamics by modifying spatial 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.

Restricted dispersal reduces the strength of spatial density dependence in a tropical bird population.

Spatial processes could play an important role in density-dependent population regulation because the disproportionate use of poor quality habitats as population size increases is widespread in animal populations-the so-called buffer effect. While the buffer effect patterns and their demographic consequences have been described in a number of wild populations, much less is known about how dispersal affects distribution patterns and ultimately density dependence. Here, we investigated the role of dispersal in spatial density dependence using an extraordinarily detailed dataset from a reintroduced Mauritius kestrel (Falco punctatus) population with a territorial (despotic) breeding system. We show that recruitment rates varied significantly between territories, and that territory occupancy was related to its recruitment rate, both of which are consistent with the buffer effect theory. However, we also show that restricted dispersal affects the patterns of territory occupancy with the territories close to release sites being occupied sooner and for longer as the population has grown than the territories further away. As a result of these dispersal patterns, the strength of spatial density dependence is significantly reduced. We conclude that restricted dispersal can modify spatial density dependence in the wild, which has implications for the way population dynamics are likely to be impacted by environmental change.

Tritrophic phenological match-mismatch in space and time.

Increasing temperatures associated with climate change may generate phenological mismatches that disrupt previously synchronous trophic interactions. Most work on mismatch has focused on temporal trends, whereas spatial variation in the degree of trophic synchrony has largely been neglected, even though the degree to which mismatch varies in space has implications for meso-scale population dynamics and evolution. Here we quantify latitudinal trends in phenological mismatch, using phenological data on an oak-caterpillar-bird system from across the UK. Increasing latitude delays phenology of all species, but more so for oak, resulting in a shorter interval between leaf emergence and peak caterpillar biomass at northern locations. Asynchrony found between peak caterpillar biomass and peak nestling demand of blue tits, great tits and pied flycatchers increases in earlier (warm) springs. There is no evidence of spatial variation in the timing of peak nestling demand relative to peak caterpillar biomass for any species. Phenological mismatch alone is thus unlikely to explain spatial variation in population trends. Given projections of continued spring warming, we predict that temperate forest birds will become increasingly mismatched with peak caterpillar timing. Latitudinal invariance in the direction of mismatch may act as a double-edged sword that presents no opportunities for spatial buffering from the effects of mismatch on population size, but generates spatially consistent directional selection on timing, which could facilitate rapid evolutionary change.

Direct versus indirect sexual selection: genetic basis of colour, size and recruitment in a wild bird.

Indirect and direct models of sexual selection make different predictions regarding the quantitative genetic relationships between sexual ornaments and fitness. Indirect models predict that ornaments should have a high heritability and that strong positive genetic covariance should exist between fitness and the ornament. Direct models, on the other hand, make no such assumptions about the level of genetic variance in fitness and the ornament, and are therefore likely to be more important when environmental sources of variation are large. Here we test these predictions in a wild population of the blue tit (Parus caeruleus), a species in which plumage coloration has been shown to be under sexual selection. Using 3 years of cross-fostering data from over 250 breeding attempts, we partition the covariance between parental coloration and aspects of nestling fitness into a genetic and environmental component. Contrary to indirect models of sexual selection, but in agreement with direct models, we show that variation in coloration is only weakly heritable h2<0.11, and that two components of offspring fitness-nestling size and fledgling recruitment-are strongly dependent on parental effects, rather than genetic effects. Furthermore, there was no evidence of significant positive genetic covariation between parental colour and offspring traits. Contrary to direct benefit models, however, we find little evidence that variation in colour reliably indicates the level of parental care provided by either males or females. Taken together, these results indicate that the assumptions of indirect models of sexual selection are not supported by the genetic basis of the traits reported on here.