Sexually Distinct Song Cultures Across a Songbird Metapopulation

Songbirds learn their songs culturally, through imitating tutors. The vocal culture of a songbird population changes as new song units (syllables) are introduced through immigration, copying errors, and innovation, while other syllables fall out of use. This leads to a diversification of the syllable pool across the species, much like the diversification and spatial patterns of human language. Vocal cultures have been well-studied in male songbirds but have been largely overlooked in females. Here we undertake one of the first comparisons of male and female song cultures across a songbird metapopulation—studying New Zealand bellbirds Anthornis melanura spanning a network of six islands. Having classified 20,700 syllables (702 types), we compare population syllable repertoire sizes and overlap between sites and sexes. We show that males and females—both with complex songs—have distinct song cultures, sharing only 6–26% of syllable types within each site. Furthermore, male and female syllable types can be statistically discriminated based on acoustic properties. Despite diverse syllable repertoires within sites, few syllable types were shared between sites (both sexes had highly distinct site-specific dialects). For the few types shared between sites, sharing decreased with distance only for males. Overall, there was no significant difference between sexes in degree of site–site repertoire overlap. These results suggest different cultural processes at play for the two sexes, underlining the inadequacy of male-centric song research and calling for comparisons of male and female song cultures in many more species.

Sexual and temporal variation in New Zealand bellbird song repertoires

How song repertoires vary within species and change over time is well studied in male songbirds. However, variation in female song repertoires remains largely unstudied despite female song being much more common and complex than once assumed. We investigated the song syllable repertoire of the New Zealand bellbird (Anthornis melanura), a species where both sexes have complex but sexually dimorphic song. We compared songs at individual and population levels to investigate sex and temporal variation of syllable repertoires. We detected 96 syllable types in the population over four years, of which 58% were unique to males, 32% unique to females and 9% were shared between the sexes. The population syllable repertoire of both sexes changed substantially across years with similar turnover rates (Jaccard’s similarity coefficients; female 52.9–69.0%; male 58.6–73.7%). Furthermore, many syllable types, unique to each sex, varied in prevalence within the population across years. The syllable repertoire sizes of individuals were higher for males than females (13-32, n = 7 and 6-16, n = 8, respectively). Although these sample sizes were low, the temporal variation in syllable prevalence and turnover for individuals were similar to patterns at the population level. Overall, male and female bellbirds exhibited similarities in temporal patterns of yearly repertoire composition, with rapid changes in syllable prevalence, but females had fewer syllable types than males. We suggest that these similarities and differences are consistent with male and female song repertoires being driven by similar but not identical selection pressures.

Perineuronal nets in HVC and plasticity in male canary song

Songbirds learn their vocalizations during developmental sensitive periods of song memorization and sensorimotor learning. Some seasonal songbirds, called open-ended learners, recapitulate transitions from sensorimotor learning and song crystallization on a seasonal basis during adulthood. In adult male canaries, sensorimotor learning occurs each year in autumn and leads to modifications of the syllable repertoire during successive breeding seasons. We previously showed that perineuronal nets (PNN) expression in song control nuclei decreases during this sensorimotor learning period. Here we explored the causal link between PNN expression in adult canaries and song modification by enzymatically degrading PNN in HVC, a key song control system nucleus. Three independent experiments identified limited effects of the PNN degradation in HVC on the song structure of male canaries. They clearly establish that presence of PNN in HVC is not required to maintain general features of crystallized song. Some suggestion was collected that PNN are implicated in the stability of song repertoires but this evidence is too preliminary to draw firm conclusions and additional investigations should consider producing PNN degradations at specified time points of the seasonal cycle. It also remains possible that once song has been crystallized at the beginning of the first breeding season, PNN no longer play a key role in determining song structure; this could be tested by treatments with chondroitinase ABC at key steps in ontogeny. It would in this context be important to develop multiple stereotaxic procedures allowing the simultaneous bilateral degradation of PNN in several song control nuclei for extended periods.

Sexually distinct song cultures in a songbird metapopulation

Songbirds learn their songs culturally, through imitating tutors. The vocal culture of a songbird population changes as new song units (syllables) are introduced through immigration, copying errors, and innovation, while other syllables fall out of use. This leads to a diversification of the syllable pool across the species, much like the diversification and spatial patterns of human language. Vocal cultures have been well studied in male songbirds but have been largely overlooked in females. In particular, few studies compare spatial variation of male and female song cultures. Here we undertake one of the first comparisons of male and female song culture in birds, analysing song data from a metapopulation of New Zealand bellbirds Anthornis melanura, spanning an archipelago of six islands. Having classified 20,700 syllables, we compare population syllable repertoire sizes and overlap between sites and sexes. We show that males and females - both with complex songs - have distinct song cultures, sharing only 6-26% of syllable types within each site. Furthermore, male and female syllable types can be statistically discriminated based on acoustic properties. Despite diverse syllable repertoires within sites, very few syllable types were shared between sites (both sexes had highly distinct site-specific dialects). For the few types shared between sites, sharing decreased with distance only for males. Overall, there was no significant difference between sexes in degree of site-site repertoire overlap. These results show different cultural processes at play for the two sexes. We discuss the implications for future research on female culture.

Perineuronal nets in HVC and plasticity in male canary song

Songbirds learn their vocalizations during sensitive periods of song memorization and sensorimotor learning during development. Some seasonal songbirds, called open-ended learners, recapitulate transitions from sensorimotor learning and song crystallization on a seasonal basis during adulthood. In adult male canaries, sensorimotor learning occurs each year in autumn and leads to modifications of the syllable repertoire during successive breeding seasons. We previously showed that perineuronal nets (PNN) expression in song control nuclei decreases during this sensorimotor learning period. Here we explored the causal link between PNN expression in adult canaries and song modification by enzymatically degrading PNN in HVC, a key song control system nucleus. Three independent experiments identified limited effects of the PNN degradation in HVC on the song structure of male canaries. They clearly establish that presence of PNN in HVC is not required to maintain general features of crystallized song. Some suggestion was collected that PNN are implicated in the stability of song repertoires but this evidence is too preliminary to draw firm conclusions and additional investigations should consider producing PNN degradations at specified time points of the seasonal cycle. It also remains possible that once song has been crystallized at the beginning of the first breeding season, PNN no longer play a key role in determining song structure which could be tested by treatments with ChABC at key step in ontogeny. It would in this context be important to develop multiple stereotaxic procedures allowing the simultaneous bilateral degradation of PNN in several song control nuclei for extended periods.

Habitat-related differences in song structure and complexity in a songbird with a large repertoire

Background Urbanisation has been shown to influence many aspects of animal vocal communication. Much attention has been paid to anthropogenic noise, which is often described as one of the most challenging disturbances for urban dwellers. While a large body of literature describes associations between vocal behavior of avian populations and background noise level, most of these studies were conducted on species with relatively simple songs and small repertoire sizes. This study focuses on the song thrush, Turdus philomelos, a common Eurasian songbird with a complex singing style and large syllable repertoire. Our objective was to determine whether frequency, repertoire and temporal organisation of song parameters vary between birds inhabiting urban and adjacent forest habitats in which ambient noise levels differ. Results Songs of urban males were found to be more complex than in conspecifics from natural forest populations. Urban dwellers possessed greater syllable repertoires and repeated syllable sequences more often. In addition, they used a smaller proportion of whistles and a higher proportion of twitter syllables when singing compared to the nonurban males. Moreover, we found significant differences in the minimum and peak frequency of the whistle syllable between studied populations. Conclusions These findings may be an example of adaptation of acoustic communication in noisy urban environments, but we also discuss other possible explanations. We emphasize the need for further investigation into the relationships between birdsong and habitat characteristics, male quality, population density and ambient noise level in populations occupying urban and nonurban habitats.