Mixed-species flock sizes and compositions influence flock members' success in three field experiments with novel feeders.

Mixed-species groups and aggregations are quite common and may provide substantial fitness-related benefits to group members. Individuals may benefit from the overall size of the mixed-species group or from the diversity of species present, or both. Here we exposed mixed-species flocks of songbirds (Carolina chickadees, Poecile carolinensis, tufted titmice, Baeolophus bicolor, and the satellite species attracted to these two species) to three different novel feeder experiments to assess the influence of mixed-species flock size and composition on ability to solve the feeder tasks. We also assessed the potential role of habitat density and traffic noise on birds' ability to solve these tasks. We found that likelihood of solving a novel feeder task was associated with mixed-species flock size and composition, though the specific social factor involved depended on the particular species and on the novel feeder. We did not find an influence of habitat density or background traffic noise on likelihood of solving novel feeder tasks. Overall, our results reveal the importance of variation in mixed-species group size and diversity on foraging success in these songbirds.

A refined magnetic pulse treatment method for magnetic navigation experiments with adequate sham control: a case study on free-flying songbirds.

Migratory songbirds may navigate by extracting positional information from the geomagnetic field, potentially with a magnetic-particle-based receptor. Previous studies assessed this hypothesis experimentally by exposing birds to a strong but brief magnetic pulse aimed at remagnetizing the particles and evoking an altered behaviour. Critically, such studies were not ideally designed because they lacked an adequate sham treatment controlling for the induced electric field that is fundamentally associated with a magnetic pulse. Consequently, we designed a sham-controlled magnetic-pulse experiment, with sham and treatment pulse producing a similar induced electric field, while limiting the sham magnetic field to a value that is deemed insufficient to remagnetize particles. We tested this novel approach by pulsing more than 250 wild, migrating European robins (Erithacus rubecula) during two autumn seasons. After pulsing them, five traits of free-flight migratory behaviour were observed, but no effect of the pulse could be found. Notably, one of the traits, the migratory motivation of adults, was significantly affected in only one of the two study years. Considering the problem of reproducing experiments with wild animals, we recommend a multi-year approach encompassing large sample size, blinded design and built-in sham control to obtain future insights into the role of magnetic-particle-based magnetoreception in bird navigation.

Will a changing climate affect hatching success in cavity-nesting birds: A case study with Eastern Bluebirds (Sialia sialis)?

A significant body of evidence indicates that climate change is influencing many aspects of avian ecology. Yet, how climate change is affecting, and is expected to influence some aspects of the breeding ecology of cavity-nesting birds remains uncertain. To explore the potential linkage between timing of first clutch, and the influence of ambient temperature on hatching success, we used Eastern Bluebird (Sialia sialis) nest records over a nine-year period from Alabama, USA. We investigated changes to annual clutch initiation dates, as well as variability in hatching success associated with ambient air temperatures during the incubation period. Using a simple linear model, we observed earlier annual egg laying dates over the nine years of this study with a difference of 24 days between earliest egg-laying date of the season. Daily temperature minima increased 2 °C across the nine-year time frame of this study. These data also indicate that Eastern Bluebird hatching success was the highest when mean ambient air temperature during incubation was between 19 °C and 24 °C (78%, as opposed to 69% and 68% above and below this temperature range, respectively). Our findings of increasing maxima, earlier maxima each year, and the lower minima of temperatures within our study area could expand the breadth of temperatures experienced by nesting Eastern Bluebirds possibly exposing them to temperatures outside of what promotes nesting success. These findings with a cavity-nesting bird highlight an optimal range of ambient temperatures associated with highest hatching success, conditions likely to be affected by climate change.

Vocal convergence and social proximity shape the calls of the most basal Passeriformes, New Zealand Wrens.

Despite extensive research on avian vocal learning, we still lack a general understanding of how and when this ability evolved in birds. As the closest living relatives of the earliest Passeriformes, the New Zealand wrens (Acanthisitti) hold a key phylogenetic position for furthering our understanding of the evolution of vocal learning because they share a common ancestor with two vocal learners: oscines and parrots. However, the vocal learning abilities of New Zealand wrens remain unexplored. Here, we test for the presence of prerequisite behaviors for vocal learning in one of the two extant species of New Zealand wrens, the rifleman (Acanthisitta chloris). We detect the presence of unique individual vocal signatures and show how these signatures are shaped by social proximity, as demonstrated by group vocal signatures and strong acoustic similarities among distantly related individuals in close social proximity. Further, we reveal that rifleman calls share similar phenotypic variance ratios to those previously reported in the learned vocalizations of the zebra finch, Taeniopygia guttata. Together these findings provide strong evidence that riflemen vocally converge, and though the mechanism still remains to be determined, they may also suggest that this vocal convergence is the result of rudimentary vocal learning abilities.

Winter-ground microhabitat use by differently coloured phenotypes affects return rate in a long-distance migratory bird.

Migratory bird populations are declining globally at alarming rates. Non-breeding site conditions affect breeding populations, but generalising non-breeding habitat conditions over large spatial regions cannot address potential fine-scale differences across landscapes or local populations. Plumage characteristics can mediate the effects of environmental conditions on individual fitness. However, whether different phenotypes use distinctive non-breeding sites, and whether they respond to non-breeding site conditions differently remains largely unknown. Stable isotopes (δ13C, δ15N, δ2H) of inert tissues are useful to infer habitat characteristics and geographic origins where those tissues were grown. We collected winter-grown feathers from pied flycatchers (Ficedula hypoleuca) on their breeding grounds over several years from males whose dorsal plumage colouration ranged continuously from brown to black and assessed their stable isotope values as proxies of local habitat conditions. Based on feather δ2H profiles we found that browner males spent their non-breeding season in drier habitats than black males. Assignment to origin analysis shows potential regional non-breeding ground separation between differently coloured males. High within-individual repeatability of both δ13C and δ15N indicate the pied flycatcher males return yearly to similar areas. Blacker males were more likely to return to the breeding grounds after dry years compared with brown males. The opposite was found in wet years. Our study demonstrates that different phenotypes are exposed to different non-breeding site conditions which can differentially affect individual survivorship. This has important ramifications for population dynamics under predicted climate change scenarios where especially brown phenotype pied flycatcher males may be under a risk of decreasing.

Call combination production is linked to the social environment in Western Australian magpies (Gymnorhina tibicen dorsalis).

It has recently become clear that some language-specific traits previously thought to be unique to humans (such as the capacity to combine sounds) are widespread in the animal kingdom. Despite the increase in studies documenting the presence of call combinations in non-human animals, factors promoting this vocal trait are unclear. One leading hypothesis proposes that communicative complexity co-evolved with social complexity owing to the need to transmit a diversity of information to a wider range of social partners. The Western Australian magpie (Gymnorhina tibicen dorsalis) provides a unique model to investigate this proposed link because it is a group-living, vocal learning species that is capable of multi-level combinatoriality (independently produced calls contain vocal segments and comprise combinations). Here, we compare variations in the production of call combinations across magpie groups ranging in size from 2 to 11 birds. We found that callers in larger groups give call combinations: (i) in greater diversity and (ii) more frequently than callers in smaller groups. Significantly, these observations support the hypothesis that combinatorial complexity may be related to social complexity in an open-ended vocal learner, providing an important step in understanding the role that sociality may have played in the development of vocal combinatorial complexity. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Translocated wild birds are predisposed to learn songs of their ancestral population.

Population differences in socially learned mating signals like oscine birdsong are particularly vulnerable to breakdown through dispersal.1 Despite this challenge, geographic variation in learned signals is ubiquitous.2 A proposed explanation for this pattern is that birds express predispositions to selectively learn and produce population-typical songs.3,4,5 While experimental studies on lab-reared birds have shown the existence of within-species learning predispositions,6,7,8,9,10 it remains unclear whether and how learning predispositions influence song acquisition in the wild. Here, we investigated innate song learning predispositions in wild pied flycatchers (Ficedula hypoleuca) by measuring the songs of individuals translocated as eggs from a Dutch population to a breeding population in Sweden. We compared the songs of the adult males hatched from these translocated eggs with those from the ancestral and receiving populations. Songs of translocated males closely resemble the local Swedish songs to which they were exposed during development, supporting the importance of social learning. However, translocated males selectively learned those local Swedish song elements that sound the most "Dutch-like." As a result, their songs are significantly shifted toward those of the ancestral Dutch population. This suggests that innate learning predispositions track ongoing song evolution in wild populations of pied flycatchers. We propose that as songs continue to diverge over time, this coevolutionary relationship between song and learning predispositions may contribute to the emergence of incipient pre-mating barriers.

A genomic basis of vocal rhythm in birds.

Vocal rhythm plays a fundamental role in sexual selection and species recognition in birds, but little is known of its genetic basis due to the confounding effect of vocal learning in model systems. Uncovering its genetic basis could facilitate identifying genes potentially important in speciation. Here we investigate the genomic underpinnings of rhythm in vocal non-learning Pogoniulus tinkerbirds using 135 individual whole genomes distributed across a southern African hybrid zone. We find rhythm speed is associated with two genes that are also known to affect human speech, Neurexin-1 and Coenzyme Q8A. Models leveraging ancestry reveal these candidate loci also impact rhythmic stability, a trait linked with motor performance which is an indicator of quality. Character displacement in rhythmic stability suggests possible reinforcement against hybridization, supported by evidence of asymmetric assortative mating in the species producing faster, more stable rhythms. Because rhythm is omnipresent in animal communication, candidate genes identified here may shape vocal rhythm across birds and other vertebrates.

Social restructuring during harsh environmental conditions promotes cooperative behaviour in a songbird.

Cooperation may emerge from intrinsic factors such as social structure and extrinsic factors such as environmental conditions. Although these factors might reinforce or counteract each other, their interaction remains unexplored in animal populations. Studies on multilevel societies suggest a link between social structure, environmental conditions and individual investment in cooperative behaviours. These societies exhibit flexible social configurations, with stable groups that overlap and associate hierarchically. Structure can be seasonal, with upper-level units appearing only during specific seasons, and lower-level units persisting year-round. This offers an opportunity to investigate how cooperation relates to social structure and environmental conditions. Here, we study the seasonal multilevel society of superb fairy-wrens (Malurus cyaneus), observing individual responses to experimental playback of conspecific distress calls. Individuals engaged more in helping behaviour and less in aggressive/territorial song during the harsher non-breeding season compared to the breeding season. The increase in cooperation was greater for breeding group members than for members of the same community, the upper social unit, comprised of distinct breeding groups in association. Results suggest that the interaction between social structure and environmental conditions drives the seasonal switch in cooperation, supporting the hypothesis that multilevel societies can emerge to increase cooperation during harsh environmental conditions.

Body size shapes song in honeyeaters.

Birdsongs are among the most distinctive animal signals. Their evolution is thought to be shaped simultaneously by habitat structure and by the constraints of morphology. Habitat structure affects song transmission and detectability, thus influencing song (the acoustic adaptation hypothesis), while body size and beak size and shape necessarily constrain song characteristics (the morphological constraint hypothesis). Yet, support for the acoustic adaptation and morphological constraint hypotheses remains equivocal, and their simultaneous examination is infrequent. Using a phenotypically diverse Australasian bird clade, the honeyeaters (Aves: Meliphagidae), we compile a dataset consisting of song, environmental, and morphological variables for 163 species and jointly examine predictions of these two hypotheses. Overall, we find that body size constrains song frequency and pace in honeyeaters. Although habitat type and environmental temperature influence aspects of song, that influence is indirect, likely via effects of environmental variation on body size, with some evidence that elevation constrains the evolution of song peak frequency. Our results demonstrate that morphology has an overwhelming influence on birdsong, in support of the morphological constraint hypothesis, with the environment playing a secondary role generally via body size rather than habitat structure. These results suggest that changing body size (a consequence of both global effects such as climate change and local effects such as habitat transformation) will substantially influence the nature of birdsong.

Diet of moulting Swainson's Thrushes (Catharus ustulatus) and Tennessee Warblers (Leiothlypis peregrina) at a stopover site during fall migration measured with fecal DNA metabarcoding.

Moult and migration are energetically demanding and require adequate nutrition. In some species, individuals may interrupt their fall migration to moult at discrete stopover locations outside of their breeding grounds (i.e., moult-migration) leading to competing nutritional demands for moult and migration. Here, we use DNA barcoding of fecal samples to compare the diet of moulting and actively migrating (post-moult) Swainson's Thrushes (Catharus ustulatus) and Tennessee Warblers (Leiothlypis peregrina) during their fall migration stopover at a large urban greenspace in Montreal, Canada. Diet differed according to moult status, species, and seasonality. Swainson's Thrushes had a broad diet with frequent detections of both insects and berry-producing shrubs; while detections in Tennessee Warblers' diets were mainly arthropods. For both species, more actively migrating individuals consumed fleshy-fruiting plants than moulting individuals. A higher proportion of moulting birds consumed arthropods compared to active migrants, due to either arthropod availability or a dietary preference for proteinaceous foods to grow feathers. Both species and moult classes consumed more native plants than non-native plants later in the season. We show the importance of managing urban greenspaces with native plants and diverse food sources that can provide for the different dietary needs of migratory birds.

Mapping seasonal migration in a songbird hybrid zone -- heritability, genetic correlations, and genomic patterns linked to speciation.

Seasonal migration is a widespread behavior relevant for adaptation and speciation, yet knowledge of its genetic basis is limited. We leveraged advances in tracking and sequencing technologies to bridge this gap in a well-characterized hybrid zone between songbirds that differ in migratory behavior. Migration requires the coordinated action of many traits, including orientation, timing, and wing morphology. We used genetic mapping to show these traits are highly heritable and genetically correlated, explaining how migration has evolved so rapidly in the past and suggesting future responses to climate change may be possible. Many of these traits mapped to the same genomic regions and small structural variants indicating the same, or tightly linked, genes underlie them. Analyses integrating transcriptomic data indicate cholinergic receptors could control multiple traits. Furthermore, analyses integrating genomic differentiation further suggested genes underlying migratory traits help maintain reproductive isolation in this hybrid zone.

The effect of environmental variation on the relationship between survival and risk-taking behaviour in a migratory songbird.

Temporal changes in environmental conditions may play a major role in the year-to-year variation in fitness consequences of behaviours. Identifying environmental drivers of such variation is crucial to understand the evolutionary trajectories of behaviours in natural contexts. However, our understanding of how environmental variation influences behaviours in the wild remains limited. Using data collected over 14 breeding seasons from a collared flycatcher (Ficedula albicollis) population, we examined the effect of environmental variation on the relationship between survival and risk-taking behaviour, a highly variable behavioural trait with great evolutionary and ecological significance. Specifically, using annual recapture probability as a proxy of survival, we evaluated the specific effect of predation pressure, food availability, and mean temperature on the relationship between annual recapture probability and risk-taking behaviour (measured as flight initiation distance [FID]). We found a negative trend, as the relationship between annual recapture probability and FID decreased over the study years and changed from positive to negative. Specifically, in the early years of the study, risk-avoiding individuals exhibited a higher annual recapture probability, whereas in the later years, risk-avoiders had a lower annual recapture probability. However, we did not find evidence that any of the considered environmental factors mediated the variation in the relationship between survival and risk-taking behaviour.

Synchrony in adult survival is remarkably strong among common temperate songbirds across France.

Synchronous variation in demographic parameters across species increases the risk of simultaneous local extinction, which lowers the probability of subsequent recolonization. Synchrony therefore tends to destabilize meta-populations and meta-communities. Quantifying interspecific synchrony in demographic parameters, like abundance, survival, or reproduction, is thus a way to indirectly assess the stability of meta-populations and meta-communities. Moreover, it is particularly informative to identify environmental drivers of interspecific synchrony because those drivers are important across species. Using a Bayesian hierarchical multisite multispecies mark-recapture model, we investigated temporal interspecific synchrony in annual adult apparent survival for 16 common songbird species across France for the period 2001-2016. Annual adult survival was largely synchronous among species (73%, 95% credible interval [47%-94%] of the variation among years was common to all species), despite species differing in ecological niche and life history. This result was robust to different model formulations, uneven species sample sizes, and removing the long-term trend in survival. Synchrony was also shared across migratory strategies, which suggests that environmental forcing during the 4-month temperate breeding season has a large-scale, interspecific impact on songbird survival. However, the strong interspecific synchrony was not easily explained by a set of candidate weather variables we defined a priori. Spring weather variables explained only 1.4% [0.01%-5.5%] of synchrony, while the contribution of large-scale winter weather indices may have been stronger but uncertain, accounting for 12% [0.3%-37%] of synchrony. Future research could jointly model interspecific variation and covariation in breeding success, age-dependent survival, and age-dependent dispersal to understand when interspecific synchrony in abundance emerges and destabilizes meta-communities.

Hearing and vocalizations in a small songbird, the red-cheeked cordon bleu (Uraeginthus bengalus) (L).

The auditory sensitivity of a small songbird, the red-cheeked cordon bleu, was measured using the standard methods of animal psychophysics. Hearing in cordon bleus is similar to other small passerines with best hearing in the frequency region from 2 to 4 kHz and sensitivity declining at the rate of about 10 dB/octave below 2 kHz and about 35 dB/octave as frequency increases from 4 to 9 kHz. While critical ratios are similar to other songbirds, the long-term average power spectrum of cordon bleu song falls above the frequency of best hearing in this species.

Migration increases mitochondrial oxidative capacity without increasing reactive oxygen species emission in a songbird.

Birds remodel their flight muscle metabolism prior to migration to meet the physiological demands of migratory flight, including increases in both oxidative capacity and defence against reactive oxygen species. The degree of plasticity mediated by changes in these mitochondrial properties is poorly understood but may be explained by two non-mutually exclusive hypotheses: variation in mitochondrial quantity or in individual mitochondrial function. We tested these hypotheses using yellow-rumped warblers (Setophaga coronata), a Nearctic songbird which biannually migrates 2000-5000 km. We predicted higher flight muscle mitochondrial abundance and substrate oxidative capacity, and decreased reactive oxygen species emission in migratory warblers captured during autumn migration compared with a short-day photoperiod-induced non-migratory phenotype. We assessed mitochondrial abundance via citrate synthase activity and assessed isolated mitochondrial function using high-resolution fluororespirometry. We found 60% higher tissue citrate synthase activity in the migratory phenotype, indicating higher mitochondrial abundance. We also found 70% higher State 3 respiration (expressed per unit citrate synthase) in mitochondria from migratory warblers when oxidizing palmitoylcarnitine, but similar H2O2 emission rates between phenotypes. By contrast, non-phosphorylating respiration was higher and H2O2 emission rates were lower in the migratory phenotype. However, flux through electron transport system complexes I-IV, II-IV and IV was similar between phenotypes. In support of our hypotheses, these data suggest that flight muscle mitochondrial abundance and function are seasonally remodelled in migratory songbirds to increase tissue oxidative capacity without increasing reactive oxygen species formation.

Genes and gene networks underlying spatial cognition in food-caching chickadees.

Substantial progress has been made in understanding the genetic architecture of phenotypes involved in a variety of evolutionary processes. Behavioral genetics remains, however, among the least understood. We explore the genetic architecture of spatial cognitive abilities in a wild passerine bird, the mountain chickadee (Poecile gambeli). Mountain chickadees cache thousands of seeds in the fall and require specialized spatial memory to recover these caches throughout the winter. We previously showed that variation in spatial cognition has a direct effect on fitness and has a genetic basis. It remains unknown which specific genes and developmental pathways are particularly important for shaping spatial cognition. To further dissect the genetic basis of spatial cognitive abilities, we combine experimental quantification of spatial cognition in wild chickadees with whole-genome sequencing of 162 individuals, a new chromosome-scale reference genome, and species-specific gene annotation. We have identified a set of genes and developmental pathways that play a key role in creating variation in spatial cognition and found that the mechanism shaping cognitive variation is consistent with selection against mildly deleterious non-coding mutations. Although some candidate genes were organized into connected gene networks, about half do not have shared regulation, highlighting that multiple independent developmental or physiological mechanisms contribute to variation in spatial cognitive abilities. A large proportion of the candidate genes we found are associated with synaptic plasticity, an intriguing result that leads to the hypothesis that certain genetic variants create antagonism between behavioral plasticity and long-term memory, each providing distinct benefits depending on ecological context.

Goal-directed and flexible modulation of syllable sequence within birdsong.

Songs constitute a complex system of vocal signals for inter-individual communication in songbirds. Here, we elucidate the flexibility which songbirds exhibit in the organizing and sequencing of syllables within their songs. Utilizing a newly devised song decoder for quasi-real-time annotation, we execute an operant conditioning paradigm, with rewards contingent upon specific syllable syntax. Our analysis reveals that birds possess the capacity to modify the contents of their songs, adjust the repetition length of particular syllables and employing specific motifs. Notably, birds altered their syllable sequence in a goal-directed manner to obtain rewards. We demonstrate that such modulation occurs within a distinct song segment, with adjustments made within 10 minutes after cue presentation. Additionally, we identify the involvement of the parietal-basal ganglia pathway in orchestrating these flexible modulations of syllable sequences. Our findings unveil an unappreciated aspect of songbird communication, drawing parallels with human speech.

Window into the songbird brain reveals superdiffusive migration of adult-born neurons.

In a recent study, Shvedov and colleagues used live two-photon imaging in transgenic zebra finches to reveal migration patterns of neuroblasts through the complex environment of the postembryonic brain. This study highlights the value of ubiquitin C/green fluorescent protein (UBC-GFP) transgenic zebra finches in studying adult neurogenesis and advances our understanding of dispersed long-distance neuronal migration in the adult brain, shedding light on this understudied phenomenon.