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.

Supplemental structured surveys and pre-existing detection models improve fine-scale density and population estimation with opportunistic community science data.

Density and population estimates aid in conservation and stakeholder communication. While free and broadly available community science data can effectively inform species distribution models, they often lack the information necessary to estimate imperfect detection and area sampled, thus limiting their use in fine-scale density modeling. We used structured distance-sampling surveys to model detection probability and calculate survey-specific detection offsets in community science models. We estimated density and population for 16 songbird species under three frameworks: (1) a fixed framework that assumes perfect detection within a specified survey radius, (2) an independent framework that calculates offsets from an independent source, and (3) a calibration framework that calculates offsets from supplemental surveys. Within the calibration framework, we examined the effects of calibration dataset size and data pooling. Estimates of density and population size were consistently biased low in the fixed framework. The independent and calibration frameworks produced reliable estimates for some species, but biased estimates for others, indicating discrepancies in detection probability between structured and community science surveys. The calibration framework produced reliable population estimates with as few as 10 calibration surveys with positive detections. Data pooling dramatically decreased bias. This study provides conservationists and managers with a cost-effective method of estimating density and population.

Lesions in a songbird vocal circuit increase variability in song syntax.

Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC's recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by 'breaks' in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.

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.

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.

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.

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.

White-crested elaenias (Elaenia albiceps chilensis) breeding across Patagonia exhibit similar spatial and temporal movement patterns throughout the year.

For migratory birds, events happening during any period of their annual cycle can have strong carry-over effects on the subsequent periods. The strength of carry-over effects between non-breeding and breeding grounds can be shaped by the degree of migratory connectivity: whether or not individuals that breed together also migrate and/or spend the non-breeding season together. We assessed the annual cycle of the White-crested Elaenia (Elaenia albiceps chilensis), the longest-distance migrant flycatcher within South America, which breeds in Patagonia and spends the non-breeding season as far north as Amazonia. Using light-level geolocators, we tracked the annual movements of elaenias breeding on southern Patagonia and compared it with movements of elaenias breeding in northern Patagonia (1,365 km north) using Movebank Repository data. We found that elaenias breeding in southern Patagonia successively used two separate non-breeding regions while in their Brazilian non-breeding grounds, as already found for elaenias breeding in the northern Patagonia site. Elaenias breeding in both northern and southern Patagonia also showed high spread in their non-breeding grounds, high non-breeding overlap among individuals from both breeding sites, and similar migration phenology, all of which suggests weak migratory connectivity for this species. Elucidating the annual cycle of this species, with particular emphasis on females and juveniles, still requires further research across a wide expanse of South America. This information will be critical to understanding and possibly predicting this species' response to climate change and rapid land-use changes.

Seed preference is only weakly linked to seed-type-specific feeding performance in a songbird.

The dehusking of seeds by granivorous songbirds is a complex process that requires fast, coordinated and sensory-feedback-controlled movements of beak and tongue. Hence, efficient seed handling requires a high degree of sensorimotoric skill and behavioural flexibility, since seeds vary considerably in size, shape and husk structure. To deal with this variability, individuals might specialise on specific seed types, which could result in greater seed handling efficiency of the preferred seed type, but lower efficiency for other seed types. To test this, we assessed seed preferences of canaries (Serinus canaria) through food choice experiments and related these to data of feeding performance, seed-handling skills and beak kinematics during feeding on small, spindle-shaped canary seeds and larger, spheroid-shaped hemp seeds. We found great variety in seed preferences among individuals: some had no clear preference, while others almost exclusively fed on hemp seeds, or even prioritized novel seed types (millet seed). Surprisingly, we only observed few and weak effects of seed preference on feeding efficiency. This suggests either that the ability to handle seeds efficiently can be readily applied across various seed types, or alternatively, that achieving high levels of seed-specific handling skills does not require extensive practice.

Removal of older males increases extra-pair siring success of yearling males.

In animals, reproductive performance typically improves over time early in life. Several ultimate and proximate mechanisms may contribute to such an age-related improvement and these mechanisms can act in a relative or in an absolute sense. Low performance of young individuals may be the consequence of a comparison or competition with older individuals (relative), or it may be due to specific traits of young individuals and be unrelated to the presence of older competitors (absolute). Here, we perform a test to disentangle whether the effect of age class (yearling or older) on male extra-pair siring success is relative or absolute. Male age is the most consistent predictor of male extra-pair siring success across bird species, yet the mechanisms underlying this pattern are not well understood. Low extra-pair siring success of yearling males may be a consequence of the presence of older ("adult") males (hypothesis 1), because adult males are more successful in intra- and intersexual interactions or because females prefer to copulate with adult males when available (relative preference). Alternatively, low extra-pair siring success of yearlings may be independent of the presence of adult males (hypothesis 2), for example, if yearling males on average invest less in extra-pair behavior or if females avoid them as extra-pair mates, independent of the availability of older males (absolute preference). To distinguish between these 2 hypotheses, we experimentally manipulated the age structure of a nest-box-breeding population of blue tits (Cyanistes caeruleus) by removing almost all adult males, and compared patterns of extra-pair paternity in the experimental year with those from the preceding 15 "control" years. Removal of adult males resulted in a substantial increase in the extra-pair siring success of yearling males compared to the "control" years, but did not affect the population-level frequency of extra-pair paternity or its spatial patterns. Our results provide clear evidence that extra-pair siring success of yearlings can increase and that it depends on the presence of older males in the population, indicating a relative effect of age on reproductive performance. These results suggest that older males outcompete yearling males in direct or indirect interactions, in sperm competition or as a result of differences in attractiveness to females.

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.

It's about Her: Male Within-Season Movements Are Related to Mate Searching in a Songbird.

AbstractIn species with resource-defense mating systems (such as most temperate-breeding songbirds), male dispersal is often considered to be limited in both frequency and spatial extent. When dispersal occurs within a breeding season, the favored explanation is ecological resource tracking. In contrast, movements of male birds associated with temporary emigration, such as polyterritoriality (i.e., defense of an additional location after attracting a female in the initial territory), are usually attributed to mate searching. We suggest that male dispersal and polyterritoriality are functionally related and that mate searching may be a unifying hypothesis for predicting the within-season movements of male songbirds. Here, we test three key predictions derived from this hypothesis in Wood Warblers (Phylloscopus sibilatrix). We collected data on the spatial behavior of 107 males between 2017 and 2019 and related male movements to a new territory (in both a dispersal and a polyterritorial context) to mating potential in the current territory. Most males dispersed from their territories within days or weeks after failing to attract a female, despite occupying territories in apparently suitable habitat. Probability of polyterritoriality by paired males increased after the peak fertile period of their mate. Males never dispersed following nest predation if the female remained to renest. Thus, our data are consistent with the hypothesis that both movement types are functionally related to mate searching.

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.

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.

Reduced hybrid survival in a migratory divide between songbirds.

Migratory divides, hybrid zones between populations that use different seasonal migration routes, are hypothesised to contribute to speciation. Specifically, relative to parental species, hybrids at divides are predicted to exhibit (1) intermediate migratory behaviour and (2) reduced fitness as a result. We provide the first direct test of the second prediction here with one of the largest existing avian tracking datasets, leveraging a divide between Swainson's thrushes where the first prediction is supported. Using detection rates as a proxy for survival, our results supported the migratory divide hypothesis with lower survival rates for hybrids than parental forms. This finding was juvenile-specific (vs. adults), suggesting selection against hybrids is stronger earlier in life. Reduced hybrid survival was not explained by selection against intermediate phenotypes or negative interactions among phenotypes. Additional work connecting specific features of migration is needed, but these patterns provide strong support for migration as an ecological driver of speciation.

The role of cerebellum in learned vocal communication in adult songbirds.

Injury, tumors, ischemia, and lesions in the cerebellum show the involvement of this region in human speech. The association of the cerebellum with learned birdsong has only been identified recently. Cerebellar dysfunction in young songbirds causes learning disabilities, but its role in adult songbirds has not been established. The aim of this study was to investigate the role of the deep cerebellar nuclei (DCN) in adult birdsong. We created bilateral excitotoxic lesions in the DCN of adult male zebra finches (Taeniopygia guttata) and recorded their songs for up to 4 months. Using magnetic resonance imaging (MRI) and immunohistochemistry, we validated the lesion efficacy. We found that the song duration significantly increased from 14 weeks post-op; the increase in duration was caused by a greater number of introductory notes as well as a greater number of syllables sung after the introductory notes. On the other hand, the motif duration decreased from 8 weeks after DCN lesions were induced, which was due to faster singing of syllables, not changes in inter-syllable interval length. DCN lesions also caused a decrease in the fundamental frequency of syllables. In summary, we showed that DCN lesions influence the temporal and acoustic features of birdsong. These results suggest that the cerebellum influences singing in adult songbirds.

Genome Assembly of Pyrocephalus nanus: A Step Toward the Genetic Conservation of the Endangered Little Vermilion Flycatcher of the Galapagos Islands.

Incredibly powerful whole genome studies of conservation genetics, evolution, and biogeography become possible for non-model organisms when reference genomes are available. Here, we report the sequence and assembly of the whole genome of the little vermilion flycatcher (Pyrocephalus nanus; family Tyrannidae), which is an endemic, endangered, and declining species of the Galapagos Islands. Using PacBio HiFi reads to assemble long contigs and Hi-C reads for scaffolding, we assembled a genome of 1.07 Gb comprising 267 contigs in 152 scaffolds, scaffold N50 74 M, contig N50 17.8 M, with 98.9% assigned to candidate chromosomal sequences and 99.72% of the BUSCO passeriformes 10,844 single-copy orthologs present. In addition, we used the novel HiFiMiTie pipeline to fully assemble and verify all portions of the mitochondrial genome from HiFi reads, obtaining a mitogenome of 17,151 bases, containing 13 protein-coding genes, 22 tRNAs, 2 rRNAs, two control regions, and a unique structure of control region duplication and repeats. These genomes will be a critical tool for much-needed studies of phylogenetics, population genetics, biogeography, and conservation genetics of Pyrocephalus and related genera. This genome and other studies that use it will be able to provide recommendations for conservation management, taxonomic improvement, and to understand the evolution and diversification of this genus within the Galapagos Islands.

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.