Parus Major Research Articles

Inhibitory control performance is repeatable over time and across contexts in a wild bird population

Inhibitory control is one of several cognitive mechanisms required for self-regulation, decision making and attention towards tasks. Inhibitory control is expected to influence behavioural plasticity in animals, for example in the context of foraging, social interaction or responses to sudden changes in the environment. One widely used inhibitory control assay is the ‘detour task’ where subjects must avoid impulsively touching transparent barriers positioned in front of food, and instead access the food by an alternative but known route. However, because the detour task has been reported to measure factors unrelated to inhibitory control, including motivation, previous experience and persistence, the task may be unreliable for making cross-species comparisons, estimating individual differences and linking performance with socioecological traits. To address these concerns, we designed a variant of the detour task for wild great tits, Parus major, and deployed it at the nesting site across two spring seasons. We compared task performance of the same individuals in the wild across 2 years, and with their performance in captivity when tested using the classical cylinder detour task during the nonbreeding season. Potential confounds of motivation, previous experience, body size, sex, age and personality did not significantly predict performance, and temporal and contextual repeatability were low but significant. These results support the hypothesis that our assays captured intrinsic differences in inhibitory control. Instead of dismissing detour tasks and ‘throwing the baby out with the bathwater’, we suggest confounds are likely system and experimental-design specific, and that assays for this potentially fundamental but largely overlooked source of behavioural plasticity in animal populations, should be validated and refined for each study system.

Dynamics of the Cavities of Grey-Headed Woodpeckers Picus canus Reveal Their Long- and Short-Term Ecological Roles in Boreal Forests

Cavities provide suitable microhabitats for various organisms. Therefore, cavity excavators are important species in forest environments. We observed large differences in both persistence and occupancy of the cavities of Grey-headed Woodpecker Picus canus monitored during the whole cavity lifespan in a 33-year study in southern Finland. Of a total of 80 cavities studied, the median persistence time was 17 years, but this varied from a median lifespan of 29 years for cavities in living trees to only 9 years for cavities in dead trees. The expected number of life-span nests of forest bird species per old cavity was 4.2 in living, and only 1.6 in dead trees. Ten bird species utilised the old cavities (most frequently Great Tit Parus major, Grey-headed Woodpecker and Pied Flycatcher Ficedula hypoleuca). The results show that both suitable living and dead trees should be available for cavity excavators such as the Grey-headed Woodpecker, and that living and dead trees may have different, but important ecological roles for cavity-nesting birds in boreal forests.

Which acoustic parameters modify the great tit’s response to conspecific combinatorial mobbing calls?

When responding to a conspecific call, especially when mobbing a predator, receivers rely on acoustic cues produced by callers. Variation in calls, either gradual or discrete, can inform potential mobbers about the situation. Great tits use a combinatorial call made of frequency-modulated elements (FMEs) and D notes. The gradual properties of the D notes change when facing different situations (e.g., different predators). We tested the relative effect of the number of D notes per call or the number of calls per minute on the behaviour of great tits with a playback experiment on free-ranging tits. Great tits did not change their approach behaviour depending on the treatments broadcast. However, they increased their vigilance level with an increased number of D notes in the total sequence. We propose that great tits can consider the overall amount of D notes as a form of information about the predator being mobbed. In addition, an increased number of D notes did not modify the approach behaviour but modified the vigilance behaviour, possibly indicating that great tits process the complete FME-D call as a whole mobbing unit rather than the simple sum of a vigilance call (FME) and a recruitment call (D notes). Our study sheds new light on the coding system of great tits when mobbing a predator and, more generally, how animals can combine simple syntactic rules and gradual variations when communicating. Information transfer when communicating about a predator is well described, particularly when mobbing a predator. However, it is unclear which specific variable(s) receivers rely on when adapting their response. Here, we test whether great tits adapt their response when the number of calls per minute and/or the number of notes per call is increased. Our results indicate that great tits rely on the overall number of notes in a calling sequence as a proxy for urgency. We also propose that the combinatorial call they use when mobbing is considered a whole rather than the simple sum of its constituents. Understanding how information transfer occurs in birds using combinatorial calls instead of simple note repetition adds to the current insights about compositional syntax in animals.

Graded‐risk sensitivity in northern European mixed‐species flocks of tit and nuthatch species

AbstractAvian species often use anti‐predator calls such that the costs and benefits of vigilance are distributed within the group. Some species respond differentially to graded risk by attending to relevant predator cues, such as head orientation and gaze direction. One benefit of graded‐risk sensitivity is fewer missed foraging opportunities. It is not known how the makeup of risk response behaviors in mixed‐species flocks may relate to the relative nuclearity of each species in the flock. In the current study, predator models were presented to two nuclear and two satellite species of passerines that frequently occur in natural mixed flocks. Predator models either faced toward or away from a nearby stocked feeder to simulate high and low risk of predation, and calling and seed‐taking rates of the present flock were recorded. The nuclear species, great tits (Parus major) and crested tits (Lophophanes cristatus), took more seeds when the predator faced away from the feeder than toward it. The satellite species, Eurasian nuthatches (Sitta europaea) and willow tits (Poecile montanus), did not show an effect of predator orientation. No species showed consistent differences in calling behavior relative to predator orientation, although insufficient calling data for great tits prevented analysis for this species. The results of this study suggest that one aspect of nuclearity in mixed‐species flocks is a tendency for graded‐risk sensitivity, or alternatively, that satellite species are more sensitive to mere predator presence rather than to predator orientation cues.

Tree Species Diversity and Forest Edge Density Jointly Shape the Gut Microbiota Composition in Juvenile Great Tits (Parus major).

Despite the microbiome’s key role in health and fitness, little is known about the environmental factors shaping the gut microbiome of wild birds. With habitat fragmentation being recognised as a major threat to biological diversity, we here determined how forest structure influences the bacterial species richness and diversity of wild great tit nestlings (Parus major). Using an Illumina metabarcoding approach which amplifies the 16S bacterial ribosomal RNA gene, we measured gut microbiota diversity and composition from 49 great tit nestlings, originating from 23 different nests that were located in 22 different study plots across a gradient of forest fragmentation and tree species diversity. Per nest, an average microbiome was determined on which the influence of tree species (composition and richness) and forest fragmentation (fragment area and edge density) was examined and whether this was linked to host characteristics (body condition and fledging success). We found an interaction effect of edge density with tree species richness or composition on both the microbial richness (alpha diversity: Chao1 and Shannon) and community structure (beta diversity: weighted and unweighted UniFrac). No significant short-term impact was observed of the overall faecal microbiome on host characteristics, but rather an adverse effect of specific bacterial genera on fledging success. These results highlight the influence of environmental factors on the microbial richness as well as the phylogenetic diversity during a life stage where the birds’ microbiota is shaped, which could lead to long-term consequences for host fitness.

A longitudinal analysis of the growth rate and mass of tail feathers in a great tit population: ontogeny, genetic effects and relationship between both traits

Feathers have a diversity of functions in birds and are costly to produce, so their growth rate and mass can be reliable indicators of nutritional condition at the time of production. Despite the potential for feather metrics to advance our understanding of foraging, they are underused in avian ecology. One reason for this is the difficulty of interpreting whether individual variation is driven by ontogenetic, genetic or environmental effects, which is exacerbated by the fact that most analyses have been done on cross‐sectional data. We addressed this deficit using a longitudinal dataset of tail feathers collected from great titsParus majorto test for ontogenetic and genetic effects on growth rate, mass and length, while controlling for body/feather size differences and other confounding factors. First, we found that the type of moult episode and experimentally‐induced replacement differentially affected the length, mass and growth of feathers, providing evidence of an ontogenetic effect that should be considered when comparing these feather traits across individuals as a measure of condition. Second, we detected moderate to high repeatability and heritability values from parent–offspring regression for these three feather traits, which are suggestive of an underlying genetic component of variation. Third, we used a mean centring within‐individual approach to test whether feather growth rate and feather mass (length‐corrected) are indeed positively correlated with each other as overlapping indicators of body condition in birds, and found that this association, although positive, is weak and only significant between individuals. This suggests that both metrics are not so intimately linked as originally thought, and probably have different sensitivities to variation in foraging performance and ecological conditions. Together with the higher plasticity of feather growth rate compared to feather mass, our results support the idea that feather growth rate is better suited for examining short‐term responses to environmental variation.

EpiGBS2: Improvements and evaluation of highly multiplexed, epiGBS-based reduced representation bisulfite sequencing.

Several reduced‐representation bisulfite sequencing methods have been developed in recent years to determine cytosine methylation de novo in nonmodel species. Here, we present epiGBS2, a laboratory protocol based on epiGBS with a revised and user‐friendly bioinformatics pipeline for a wide range of species with or without a reference genome. epiGBS2 is cost‐ and time‐efficient and the computational workflow is designed in a user‐friendly and reproducible manner. The library protocol allows a flexible choice of restriction enzymes and a double digest. The bioinformatics pipeline was integrated in the snakemake workflow management system, which makes the pipeline easy to execute and modular, and parameter settings for important computational steps flexible. We implemented bismark for alignment and methylation analysis and we preprocessed alignment files by double masking to enable single nucleotide polymorphism calling with freebayes (epifreebayes). The performance of several critical steps in epiGBS2 was evaluated against baseline data sets from Arabidopsis thaliana and great tit (Parus major), which confirmed its overall good performance. We provide a detailed description of the laboratory protocol and an extensive manual of the bioinformatics pipeline, which is publicly accessible on github (https://github.com/nioo‐knaw/epiGBS2) and zenodo (https://doi.org/10.5281/zenodo.4764652).

Prior territorial responses and home range size predict territory defense in radio-tagged great tits

Territorial animals often use signals to advertise territorial occupancy within their larger home ranges. Songbirds are among the best-studied territorial signaling taxa, and when competitors start singing during a territorial intrusion, residents usually show elevated spatial and vocal responses. These responses could be used by intruders and distant eavesdroppers to predict future responses or to compare responses across competitors. Yet, the extent to which responses of a resident to a territorial intrusion predict its future responses and its overall spatial behavior (home range) within a neighborhood is less well understood. We used wild great tits (Parus major) as a model species in repeated song playback trials, simulating territorial intrusions combined with radio-tracking before and during playback trials. The time spent close to the loudspeaker in response to an initial simulated intrusion predicted the same response variable during a second simulated intrusion on the next day, whereas singing activity during the first simulated intrusion did not predict singing during the second simulated intrusion. We also show that more explorative males (as determined by a novel environment test) and males with smaller home ranges sang more and spent more time near the loudspeaker in response to both simulated intrusions. Thus, by probing residents, intruders can obtain reliable information about subsequent response probabilities, while eavesdroppers from a distance, who can use auditory information only, would not receive sufficient predictive information. Our findings also suggest that males with larger home ranges are more tolerant toward intruders, which could reflect a trade-off between tendencies to respond strongly and to range widely. The lack of predictability of singing activity with regard to responses to future intrusions might explain why territorial animals continuously exchange vocal signals and regularly foray into neighboring territories, as a way to obtain regular information updates.Significance StatementAnimals use experience from interactions with conspecifics in their future decision making, such as mate choice and strategies for conflict resolution. The value of such information depends in part on the predictability of the future behavior of that conspecific. In songbirds, territorial individuals respond to intruders by approach and signaling. Here, we tested in radio-tagged great tits (Parus major) if territorial responses are predictable and are affected by individual and environmental factors. We show that the time spent near the simulated intruder was more predictable than singing activity and that birds with larger home ranges showed weaker responses. These findings suggest that information based on such spatial responses is more useful for future decision making, as compared to vocal information, and that distant eavesdroppers will thus receive less reliable information. Limited predictability may explain why territorial animals continuously exchange vocal signals and foray into neighboring territories, providing opportunities for regular information updates.

Prehatching temperatures drive inter-annual cohort differences in great tit metabolism

Basal metabolic rate (BMR) constitutes the lowest metabolic rate in a resting animal and is, therefore, considered to reflect the energetic cost of maintenance in endotherms. BMR is a reversible plastic trait that changes with environmental and ecological circumstances, albeit being heritable and susceptible to selection. Inter-individual variation within populations of small birds is substantial, and while many of the drivers of such variation have been identified, many remain unexplained. We studied winter BMR variation of juveniles over a 15-year period in a wild population of great tits Parus major at the northern border of their distribution. BMR during winter consistently changed between years, even after controlling for environmental factors, suggestive of a non-reversible developmental plasticity shaping the adult metabolic phenotype. BMR in cohorts of wintering great tits varied among winters as a response to minimum ambient temperatures experienced early in life, during the prehatching period. This developmental plasticity might be adaptive if temperatures experienced by growing embryos would metabolically prime them to an environment that they will likely encounter in future life. However, in line with a more unpredictable future climate, the risk of phenotype-environment mismatch is likely to lead to certain cohorts being poorly adapted to prevailing winter conditions, resulting in wider annual fluctuations in population size.

Differences in feather structure between urban and forest great tits: constraint or adaptation?

Urbanization is one of the strongest habitat transforming processes today that has resulted in changes in the ecological conditions for wild populations. In birds, the limitation of natural food sources and a warmer microclimate in cities can potentially influence the development and functioning of the plumage that may have important fitness consequences. Despite its potential significance, the plumage structure of urban birds are largely unexplored and it is unclear whether and how they respond to urban ecological processes such as different constraints and selection pressures. In this study, we compared several structural properties of contour, primary and tail feathers between two forest and two urban great tit Parus major populations. Our results show that the urban environment affects only a few structural properties of feathers and only in the plumage of first‐year birds. We found that both the plumulaceous and the pennaceous parts of their contour feathers are longer and have lower barb density in the urban than in the forest habitat. We also found that the primaries of first‐year birds have narrower rachis and higher barbule density in the cities than in the forests, but there were no differences in other wing feather traits and in any tail feather traits between habitats. We did not find differences in the feather structure of urban versus forest adult birds. The habitat differences in first‐year birds may indicate nutritional constraints or the effects of the warmer microclimate of the urban environment. These differences seem to disappear completely in adulthood that can be explained by the selective mortality of first‐year birds, or by adults being less sensitive than first‐year birds to environmental effects during their moult.

Biomarkers of oxidative stress, metabolic processes, and lysosomal activity in the muscle tissue of the great tit (Parus major) living in sodium industry and agricultural areas in Inowrocław region (central part of northern Poland)

An region of ecological hazard (EHR) is an area where, as a result of intensive human economic activity, degradation of components of the natural environment has taken place, leading to the deterioration of the ecological balance. EHR management is a globalised ever-increasing challenge. To eliminate the hazardous effect of these pollutants, research has been accelerated worldwide. The current study analyzed the specific biomarkers of the lipid and protein oxidation, total antioxidative status, activities of antioxidant enzymes (superoxide dismutase, catalase, glutathione reductase and peroxidase), lysosomal enzymes (alanyl aminopeptidase, leucyl aminopeptidase, acid phosphatase), and biomarkers of aerobic and anaerobic metabolic pathways (activities of alanine and aspartate aminotransferases, succinate dehydrogenase, lactate dehydrogenase, lactate and pyruvate levels) in skeletal muscle tissue of wild great tit nestlings in environments with different levels of anthropogenic pressure such as sodium industry and agriculture in the central part of northern Poland (Inowrocław EHR). Control samples were collected from Tuchola Forest and Borkowo village, where no direct sources of contamination were found. The relevance of the study was to assess the changes in lysosomal functioning caused by pollution-induced oxidative stress that may indicate multidirectional adaptative mechanisms of metabolic processes occurring in the wild birds to compensate for the negative effects of contamination. It was shown that the initiation of oxidative stress caused by anthropogenic pollution shifted the balance of the normal functioning of lysosomal enzymes towards their increased activity. A general tendency towards an increase in the intensity of lipid peroxidation processes with an increasing level of oxidatively modified proteins (aldehydic and ketonic derivatives) and a simultaneous reduction in the TAS was observed in the muscle tissue of great tits living in the anthropogenically modified areas. The intensity of lipid peroxidation and protein damage caused changes and reorganization of the energy-related metabolic pathways in the muscle tissue of wild great tits living in the sodium industry and agricultural areas of the EHR.

Comparison between short-term stress and long-term adaptive responses reveal common paths to molecular adaptation

SummaryThe phenotypic plasticity in responses to short-term stress can provide clues for understanding the adaptive fixation mechanism of genetic variation during long-term exposure to extreme environments. However, few studies have compared short-term stress responses with long-term evolutionary patterns; in particular, no interactions between the two processes have been evaluated in high-altitude environment. We performed RNA sequencing in embryo fibroblasts derived from great tits and mice to explore transcriptional responses after exposure to simulated high-altitude environmental stresses. Transcriptional changes of genes associated with metabolic pathways were identified in both bird and mice cells after short-term stress responses. Genomic comparisons among long-term highland tits and mammals and their lowland relatives revealed similar pathways (e.g., metabolic pathways) with that initiated under short-term stress transcriptional responses in vitro. These findings highlight the indicative roles of short-term stress in the long-term adaptation, and adopt common paths to molecular adaptation in mouse and bird cells.

Does the Urban Environment Act as a Filter on the Individual Quality of Birds?

Phenotypic divergences of birds are common between urban and natural habitats and can result from different selective pressures between habitats or maladaptation to the city. No uniform patterns were observed, especially concerning markers of bird health, such as, for example, telomere length. Telomeres are involved in maintaining genome integrity and naturally shorten with age, but environmental stressors can accelerate their attrition. Thus, telomere length can be an indicator of individual quality. Some studies showed that urban breeders had longer telomeres than forest individuals. Two hypotheses can explain this result: (1) urban breeders are younger than forests breeders, and (2) cities act as a filter on individuals and only high-quality birds can successfully reproduce. In this context, we compared the age category (molting pattern) and morphological and physiological characteristics of urban and forest Great Tits before and during breeding. No differences in age or body condition were observed. However, urban breeders were smaller and had shorter telomeres than birds captured in winter. Urban birds had longer telomeres than forest birds, only in winter. These results highlight that urban habitats potentially favor smaller birds. However, the decrease in telomere length between winter and reproduction only in the city suggest a higher cost of reproduction in the city compared to the forest.

An Experimental Approach to Investigating Effects of Artificial Light at Night on Free-Ranging Animals: Implementation, Results, and Directions for Future Research.

Animals have evolved with natural patterns of light and darkness. However, artificial light is being increasingly introduced into the environment from human infrastructure and recreational activity. Artificial light at night (ALAN) has the potential to have widespread effects on animal behavior, physiology, and fitness, which can translate into broader-scale effects on populations and communities. Understanding the effects of ALAN on free-ranging animals is non-trivial due to challenges such as measuring levels of light encountered by mobile organisms and separating the effects of ALAN from those of other anthropogenic disturbance factors. Here we describe an approach that allows us to isolate the effects of artificial light exposure on individual animals by experimentally manipulating light levels inside nest boxes. To this end, a system can be used consisting of light-emitting diode (LED) light(s) adhered to a plate and connected to a battery and timer system. The setup allows exposure of individuals inside nest boxes to varying intensities and durations of ALAN while simultaneously obtaining video recordings, which also include audio. The system has been used in studies on free-ranging great tits (Parus major) and blue tits (Cyanistes caeruleus) to gain insight into how ALAN affects sleep and activity patterns in adults and physiology and telomere dynamics in developing nestlings. The system, or an adaptation thereof, could be used to answer many other intriguing research questions, such as how ALAN interacts with other disturbance factors and affects bioenergetic balance. Furthermore, similar systems could be installed in or near the nest boxes, nests or burrows of a variety of species to manipulate levels of ALAN, evaluate biological responses, and work towards building an interspecific perspective. Especially when combined with other advanced approaches for monitoring the behavior and movement of free-living animals, this approach promises to yield ongoing contributions to our understanding of the biological implications of ALAN.

The use of trail cameras to monitor species inhabiting artificial nest boxes.

Artificial boxes are commonly used in studies of cavity‐dwelling animals of various taxa. One advantage of nest boxes is that cameras can be used to monitor animals inside the cavity, however, most cameras used today have to be built de novo or modified or are expensive.Here, we describe a method for monitoring nest boxes using off‐the‐shelf models of trail cameras that can record photographs and videos in daylight and darkness (TCM; Trail Camera Method). The cameras can record sequentially within a given time lapse or an infra‐red motion sensor can be triggered by activity in the nest box.Using TCM in a Great Tit (Parus major) nest box population, we studied the hourly pattern of the first egg laying and the first egg hatching. We found that Great Tits laid eggs within 2 h of the sunrise while the timing of hatching spanned the 24‐h day. Moreover, we found that the hour of hatching affects the nestlings’ mass on the 2nd day of life, but not on the 12th day of life.Comparing to traditional nest box checks, TMC requires about 75% less time to obtain data on the timing of egg laying and hatching. Moreover, the hour estimation error was several orders of magnitude greater with the traditional method.Our data demonstrate that commercially available trail cameras are an affordable and convenient method of monitoring artificial cavities. Trail cameras are small, standalone, weather‐proof devices with integrated powering, memory storage, lighting, and recording systems. They could be easily swapped between boxes or removed. After small modifications of the box, they could be used to monitor a wide variety of behaviors of many animal taxa.

Integrated molecular and behavioural data reveal deep circadian disruption in response to artificial light at night in male Great tits (Parus major)

Globally increasing levels of artificial light at night (ALAN) are associated with shifting rhythms of behaviour in many wild species. However, it is unclear whether changes in behavioural timing are paralleled by consistent shifts in the molecular clock and its associated physiological pathways. Inconsistent shifts between behavioural and molecular rhythms, and between different tissues and physiological systems, disrupt the circadian system, which coordinates all major body functions. We therefore compared behavioural, transcriptional and metabolomic responses of captive great tits (Parus major) to three ALAN intensities or to dark nights, recording activity and sampling brain, liver, spleen and blood at mid-day and midnight. ALAN advanced wake-up time, and this shift was paralleled by advanced expression of the clock gene BMAL1 in all tissues, suggesting close links between behaviour and clock gene expression across tissues. However, further analysis of gene expression and metabolites revealed that clock shifts were inconsistent across physiological systems. Untargeted metabolomic profiling showed that only 9.7% of the 755 analysed metabolites followed the behavioural shift. This high level of desynchronization indicates that ALAN disrupted the circadian system on a deep, easily overlooked level. Thus, circadian disruption could be a key mediator of health impacts of ALAN on wild animals.

A contribution to avian ectoparasite fauna of Turkey: the reports of feather mites and tick on the Great tit (Parus major L.)

Birds have a symbiotic relationship with many ectoparasite groups such as chewing lice (Mallophaga: Amblycera, Ischnocera), fleas (Siphonaptera), keds (Diptera: Hippoboscidae), mites (Acari: Sarcoptiformes, Trombidiformes) and ticks (Acari: Ixodidae, Argasidae). In fact, this relationship is mainly based on parasitism, but feather mites are mostly classified as commensal ectosymbionts, compared to other parasitic insects and arachnids. This study reports tick and feather mite species detected on a dead specimen of the Great Tit (Parus major L.) that was brought to the Department of Parasitology, Faculty of Veterinary Medicine, Ondokuz Mayıs University, Samsun, Turkey. As a result of the parasitological examination, the tick samples were identified as Ixodes frontalis (Panzer) and feather mites were identified as Analges mucronatus (Buchholz) and Proctophyllodes stylifer (Buchholz). With this study, A. mucronatus and P. stylifer have been reported for the first time from Turkey, and the feather mite fauna of Turkey has reached 42 identified species.

Great Tits Learn Odors and Colors Equally Well, and Show No Predisposition for Herbivore-Induced Plant Volatiles

Ability to efficiently localize productive foraging habitat is crucial for nesting success of insectivorous birds. Some bird species can use olfaction to identify caterpillar-infested trees by detection of herbivore induced plant volatiles (HIPVs), but these cues probably need to be learned. So far, we know very little about the process of olfactory learning in birds, whether insectivorous species have a predisposition for detecting and learning HIPVs, due to the high ecological significance of these odors, and how olfaction is integrated with vision in making foraging decisions. In a standardized setup, we tested whether 35 wild-caught great tits (Parus major) show any preference for widely abundant HIPVs compared to neutral (non-induced) plant odors, how fast they learn to associate olfactory, visual and multimodal foraging cues with food, and whether the olfactory preferences and learning speed were influenced by bird sex or habitat (urban or rural). We also tested how fast birds switch to a new cue of the same modality. Great tits showed no initial preference for HIPVs compared to neutral odors, and they learned all olfactory cues at a similar pace, except for methyl salicylate (MeSA), which they learned more slowly. We also found no differences in learning speeds between visual, olfactory and multimodal foraging cues, but birds learned the second cue they were offered faster than the first one. Bird sex or habitat had no effect on learning speed or olfactory preference, but urban birds tended to learn visual cues more slowly. We conclude that insectivorous birds utilize olfactory and visual cues with similar efficiency in foraging, and that they probably don‘t have any special predisposition toward the tested HIPVs. These results confirm that great tits are flexible foragers with good learning abilities.

Cognitive flexibility in the wild: Individual differences in reversal learning are explained primarily by proactive interference, not by sampling strategies, in two passerine bird species.

Behavioural flexibility allows animals to adjust to changes in their environment. Although the cognitive processes that explain flexibility have been relatively well studied in psychology, this is less true for animals in the wild. Here we use data collected automatically during self-administered discrimination-learning trialsfor two passerine species, and during four phases (habituation, initial learning, first reversal and second reversal) in orderto decompose sources of consistent among-individual differences in reversal learning, a commonly used measure for cognitive flexibility. First, we found that, as expected, proactive interference was significantly repeatable and had a negative effect on reversal learning, confirming that individuals with poor ability to inhibit returning to a previously rewarded feeder were also slower toreversal learn. Second, to our knowledge for the first time in a natural population, we examined how sampling of non-rewarding options post-learning affected reversal-learning performance. Sampling quantity was moderately repeatable in blue tits but not great tits; sampling bias, the variance in the proportion of visits to each non-rewarded feeder, was not repeatable for either species. Sampling behaviour did not predict variation in reversal-learning speed to any significant extent. Finally, the repeatability of reversal learning was explained almost entirely by proactive interference for blue tits; in great tits, the effects of proactive interference and sampling bias on the repeatability of reversal learning were indistinguishable. Our results highlight the value of proactive interference as a more direct measurement of cognitive flexibility and shed light on how animals respond to changes in their environment.

Resident bird species track inter-annual variation in spring phenology better than long-distance migrants in a subalpine habitat

The ability to track variation in climate is important for species to persist in a given environment. Lack of responses to both long-term changes and inter-annual variation in climate parameters can result in reduced fitness and population decline. Furthermore, migration strategy can influence the ability to track climatic variation due to the potential to use reliable environmental cues. Here, we studied the temporal relationship between birch leafing and onset of breeding for three bird species with contrasting migration strategies over a 20-year period in a subalpine habitat in Central Norway. We found no temporal change in birch leafing date or breeding onset for the three bird species over the study period. However, we found a statistically significant difference in the ability to track inter-annual variation in birch leafing date between the resident and two long-distance migratory species. The resident great tit Parus major was more capable of initiating egg laying in closer association to variation in birch leafing in early springs, than the long-distance migratory European pied flycatcher Ficedula hypoleuca and common redstart Phoenicurus phoenicurus. Long-distance migrants seem to have been constrained by arrival date or time from arrival to entering the breeding areas, in contrast to resident birds, which might be better able track early initiation of spring in breeding areas by adjusting egg laying date. Our findings highlight the importance of not solely studying directional long-term climatic change, but also pay attention to inter-annual variation.