Non-Vocal Shaping of Avian Song Development: Parallels to Human Speech Development

Vocal development in young male cowbirds (Molothrus ater) is sensitive to acoustical stimulation from males, but also to social feedback from female cowbirds, even though females do not sing. Juvenile males show different vocal trajectories if housed with local or distant population females. The major goal of the present study was to identify differences in the form and timing of non‐vocal cues from females during the period in early spring when juvenile males begin to sing stereotyped song and to finalize their repertoires. We housed juvenile males with either local or distant population females and no adult males. We found significant differences between the two groups of females in the use of wing stroking and in male reactions to wing strokes and gapes. There were also differences between the groups in male song performance. To understand further the potential consequences of these differences, we correlated measures of male and female responsiveness to results reported in Smith et al. (2000) on vocal ontogeny and song potency. We found that wing stroking by females was associated with a faster rate of song development and tended to relate to differences in song potency. The non‐vocal shaping seen here may represent a general mechanism for the development of vocal communication, as similar processes influence phonological development in human infants.     

The Development of Local Song Preferences in Female Cowbirds (Molothrus ater): Flock Living Stimulates Learning

We carried out two experiments across 2 yr on song perception in female cowbirds (Molothrus ater). In the first experiment, juvenile and adult female brown‐headed cowbirds, living in same‐sex flocks in outdoor aviaries, were periodically tutored with recordings of local male cowbirds’ songs. In the spring, four adult male cowbirds were placed with half of the females for a 12‐d period. We then tested song preferences of all females by measuring copulation solicitation displays during the breeding season. We found that the females exposed only to tape‐tutor songs preferred those songs to those of the unfamiliar males used as companions and that the females allowed to interact with males preferred their songs over the familiar tape‐tutor songs. These data establish the modifiability of female cowbirds’ song preferences at the level of local song. In a second experiment, we studied the playback responses of juvenile females, hand‐reared from the egg, who were tape‐tutored only in the spring in the presence or absence of adult females. There were no differences between the responses of juveniles housed with or without adult females and the hand‐reared juveniles were significantly less responsive to song than adult females. Adult females responded more to familiar songs than to the unfamiliar songs: juvenile females made no such distinction. Taken as a whole, these data are the first to document that female cowbirds’ song preferences for local song can be reshaped by post‐natal experience. These data complement recent study in cowbirds and other species showing that socially more complex contexts reveal plasticity in female song preferences that are not apparent when learning opportunities are constrained by impoverished laboratory settings.     

Acoustic mate copying: female cowbirds attend to other females' vocalizations to modify their song preferences

We conducted a tutoring experiment to determine whether female brown-headed cowbirds (Molothrus ater) would attend to vocalizations of other females and use those cues to influence their own preferences for male courtship songs. We collected recordings of male songs that were unfamiliar to the subject females and paired half of the songs with female chatter vocalizations—vocalizations that females give in response to songs sung by males that are courting the females effectively. Thus, chatter immediately following a song provided a cue indicating that the song was sung by a male who was of high-enough quality to court a female successfully. Using a cross-over design, we tutored two groups of females with song–chatter pairings prior to the breeding season. In the breeding season, we placed the tutored females into sound-attenuating chambers and played them the same songs without the chatter. Females produced significantly more copulation solicitation displays in response to the songs that they had heard paired with chatter than to songs that had not been paired with chatter. This experiment is the first demonstration that females can modify their song preferences by attending to the vocal behaviour of other females.     

A role of her own: female cowbirds, Molothrus ater, influence the development and outcome of song learning

Previous work has shown that captive female cowbirds, Molothrus ater, can influence the outcome of male song development by affecting retention or deletion of song elements and by stimulating improvization. Here we looked for evidence of female influence during the process of learning, as males progress from subsong to plastic song to stereotyped song. In a longitudinal study, we measured the rate and timing of vocal development in captive, juvenile male brown-headed cowbirds, M. a. artemisiae. Half the young males were housed with female cowbirds from their own population (South Dakota: SD) and half with female cowbirds from a M. a. ater population (Indiana: IN). Both populations of females prefer local songs and differ in the time of breeding, with SD females breeding 2 weeks later than IN females. The results showed significant effects of female presence on the age at which males advanced through stages of vocal development: the SD males with SD females, as opposed to SD males with IN females, developed stereotyped song earlier, reduced motor practise earlier, and produced more effective playback songs. Longitudinal observations of social interactions showed that the two groups of females reliably differed in social responses to males. Degree of social proximity of females to males in the winter predicted song maturity, rate of rehearsal and song potency. Thus, females can stimulate the progression of song learning, as well as prune song content. Copyright 2000 The Association for the Study of Animal Behaviour.     

Female Cowbird Song Perception: Evidence for Plasticity of Preference

The goal of the research reported here was to look for evidence of modifiability of preference for male song in female cowbirds, Molothrus ater. To this end, we investigated whether social experience affected the breadth and consistency of females’ playback preferences for geographic variants of male song. In three experiments, we varied female cowbirds’ exposure to males. Wild‐caught juvenile females showed a preference for local song in their first year when housed without males in sound‐attenuating chambers, as we had found previously with adult females. But we found that neither adult nor juvenile females showed a preference for local over distant song after they had been housed in large, outdoor aviaries with other females but without male residents. Aviary housing with local males did lead to preferences for local songs. These data represent the first unqualified evidence that adult and juvenile female cowbird preferences for song are modifiable. These data add to the growing body of literature suggesting that receivers, as well as signalers, rely on learning during development of their communication system.     

Watch Your Tone: Social Conditions Modulate Singing Strategies

Bird song is typically depicted as a male singing a long‐distance signal to potentially unknown receivers to (1) deter males and (2) attract females. Nevertheless, many songbirds sing from close distances to a known receiver; males of these species may be under more intense selective pressure to modify their songs depending on the sex of the receiver in order to convey different motivational states (aggression versus courtship) to the different sexes. In a laboratory setting, we examined how receiver sex affected within‐song variation of the close‐range singing behavior in the brown‐headed cowbird (Molothrus ater). Although we know that cowbird song is influenced by flock composition, it is still unclear as to how the cowbird modifies his song based on social context. Using a cross‐correlation analysis of each male's different song types, we found that pairs of songs were significantly more dissimilar if they were directed to females compared with songs directed to males. We subsequently tested whether there were any consistent spectral or temporal patterns in the songs males gave to females versus to males. Our results lend support for the Motivational Structural Rules Hypothesis as songs directed toward males had higher entropy (i.e., harshness) than the same song type directed toward females. Our results suggest that cowbirds may have evolved the ability to alter multiple dimensions of their singing behavior based on receiver sex.     

Sex and seasonal differences in neurogenesis and volume of the song‐control system are associated with song in brood‐parasitic and non‐brood‐parasitic icterid songbirds

The song‐control system in the brain of songbirds is important for the production and acquisition of song and exhibits both remarkable seasonal plasticity and some of the largest neural sex differences observed in vertebrates. We measured sex and seasonal differences in two nuclei of the song‐control system of brood‐parasitic brown‐headed cowbirds (Molothrus ater) and closely‐related non‐parasitic red‐winged blackbirds (Agelaius phoeniceus). These species differ in both the development and function of song. Brown‐headed cowbirds have a larger sex difference in song than red‐winged blackbirds. Female cowbirds never sing, whereas female blackbirds do though much less than males. In cowbirds, song primarily functions in mate choice and males modify their song as they approach sexual maturity and interact with females. In red‐winged blackbirds, song is used primarily in territorial defence and is crystalized earlier in life. We found that the HVC was more likely to be discernable in breeding female blackbirds than in breeding female cowbirds. Compared to males, females had a smaller HVC and a smaller robust nucleus of the arcopallium (RA). However, females had higher doublecortin immunoreactivity (DCX+) in HVC, a measure of neurogenesis. Consistent with sex differences in song, the sex difference in RA volume was greater in cowbirds than in blackbirds. Males of both species had a smaller HVC with higher DCX+ in post‐breeding condition than in breeding condition when song is more plastic. Sex and seasonal differences in the song‐control system were closely related to variation in song in these two icterid songbirds. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 76: 1226–1240, 2016     

Delayed vocal ontogeny in songbirds: a laboratory study validates a model for delayed development derived from field studies

Based on field studies, we proposed a model that describes how vocal ontogeny proceeds over a 2-year period in wild brown-headed cowbirds (Molothrus ater). We tested this model in the laboratory by exposing yearling male cowbirds (n?=?7 tutees), trapped at the start of the breeding season in a southern California dialect, to adult tutors with unfamiliar song types from a different dialect. As adults at the start of their second season, the tutees all had enlarged repertoires based almost entirely on tutor song types. Thus, tutees dropped song types in their yearling repertoires that did not match tutor types and added tutor songs that they had heard for the first time as yearlings in captivity. We discuss these findings in the context of a previous captivity study in which tutees also changed their yearling repertoires but generally failed to copy their tutors’ songs. This is the first laboratory study to fully replicate the delayed ontogeny we have described for wild cowbirds, and validates the delayed vocal development model we proposed. This model is important in a more general context, because it explains how song dialects can remain temporally stable despite immigration by young males with non-local songs.     

Male and female rufous‐and‐white wrens do not match song types with same‐sex rivals during simulated territorial intrusions

In birds with song repertoires, song‐type matching occurs when an individual responds to another individual's song by producing the same song type. Song‐type matching has been described in multiple bird species and a growing body of evidence suggests that song‐type matching may serve as a conventional signal of aggression, particularly in male birds in the temperate zone. Few studies have investigated song‐type matching in tropical birds or female birds, in spite of the fact that avian biodiversity is highest in the tropics, that female song is widespread in the tropics, and that female song is the ancestral state among songbirds. In this study of rufous‐and‐white wrens Thryophilus rufalbus, a resident neotropical songbird where both sexes sing, we presented territorial males and females with playback that simulated a territorial rival producing shared and unshared songs. In response, both males and females sang matched song types at levels statistically equal to levels expected by chance. Furthermore, males and females exhibited similar levels of aggression and similar vocal behaviours in response to playback of both shared and unshared songs. These results indicate that rufous‐and‐white wrens do not use song‐type matching in territorial conflicts as a conventional signal of aggression. We discuss alternative hypotheses for the function of song‐type sharing in tropical birds. In particular, we point out that shared songs may play an important role in intra‐pair communication, especially for birds where males and females combine their songs in vocal duets, and this may supersede the function of song‐type matching in some tropical birds.     

Dual Signaling during Mating in Brown-headed Cowbirds (Molothrus ater,Family Emberizidae/Icterinae)

Male brown-headed cowbirds (Molothrus ater) vocalize to females during pair formation, a period usually lasting several days. Males also vocalize to females in the seconds immediately prior to females' adopting copulatory postures. The two major classes of male vocalizations occurring during courtship and copulation are songs and flight whistles. Observations across the species' North American range suggest that the function of these two courtship vocalizations may differ geographically. Aviary observations of eastern and midwestern populations suggested, furthermore, that the precise timing of song and whistle used during copulation sequences differs, with flight whistles occurring most often after a copulatory posture but before the male mounts and the pair copulates. Such timing of the two signals suggested different proximate functions. Here, we report three experiments that addressed the communicative properties of the two signals in two midwestern populations. First, we tested females of the two populations in two playback experiments to determine copulatory responsiveness and discrimination of the two signals. We asked whether females of the two populations gave more copulatory responses to the playbacks of songs and flight whistles of males of their own population than to those of males of the other population, and whether females responded differently to songs than to whistles. In the third experiment, we observed courtship interactions among males and females from one population in a large aviary to assess the use of flight whistles in relation to courtship success. Females of both populations responded more frequently to playbacks of songs than to playbacks of flight whistles and showed reliably more responsiveness to local song variants. Thus, information in male song can be used by females to discriminate the local population. The aviary data revealed that the rate of flight whistling correlated strongly with male courtship success. Thus, the vocal antecedents to mating in midwestern cowbirds include close-range signaling to females followed by longer range signaling, perhaps to other males and to females other than the mate. Acoustic and behavioral differences between these two signals in diverse parts of the cowbirds' range suggest that the function of ‘speciestypical’ signals such as songs or whistles may not be fixed, a conclusion in keeping with the growing evidence of vocal and social mallcability in these brood parasitic birds.     

Validating the female bioassay of cowbird song: Relating differences in song potency to mating success

Female cowbirds (Molothrus ater), maintained in isolation from males during the breeding season, respond to the playback of male song with copulatory postures. They respond more often to some songs than others. Song potency can thus be operationally defined by the number of copulatory responses a song elicits. The purpose of the present study was to validate this measure of song potency by investigating its relationship to mating success. We observed two colonies of cowbirds during the breeding season and recorded details of their courtship. In addition, song potency of the males was tested by playback with a different group of captive females. The results indicate a relationship between maximum song potency and mating success: the males that obtained the most copulations had songs of higher maximum potency and were also observed to have been more dominant during the winter and early spring.     

Ecological effects on song learning: delayed development is widespread in wild populations of brown-headed cowbirds

The timing and extent of early exposure to conspecific song can have critical influence on subsequent male vocal development in songbirds. Opportunities to memorize local song models may vary among populations depending on local ecological conditions that determine the length of the breeding season. In populations with comparatively short breeding seasons, such as northern or high-elevation populations, restricted access to local songs may delay development in a large proportion of juveniles. Previous studies have described extreme examples of delayed development in high-elevation populations of brown-headed cowbirds, Molothrus ater, in the Sierra Nevada of California, U.S.A. In the current study, we determined that delayed development also occurs in a low-elevation population located at a more northerly latitude than those in the Sierra. We recorded two kinds of songs from yearling and adult males who had been given testosterone (testosterone increased song output but did not change the nature of songs in males' repertoires) soon after being trapped at two adjacent sites in New York state, U.S.A. The average size of ‘perched’ song repertoires of 17 yearlings was significantly smaller than that of 20 local adults (2.8 versus 4.6 types, respectively) and yearlings generally lacked the shared songs typically found in adult repertoires. Only 40% of yearlings trapped at one site produced the correct local dialect ‘flight whistle’ compared with 91.7% of adults. These results strongly suggest that juvenile access to local songs is also restricted in this population and that delayed vocal development is widespread in cowbirds. In addition, these findings indicate that reliance on field recordings may underestimate adult-yearling differences in vocal competency in cowbirds because yearlings that sing readily in nature may not be representative of yearlings in general, a result that may also apply to other songbird species.     

East and west coast female brown-headed cowbirds agree: both categories of male song are sexy

Some prior studies of brown-headed cowbirds, Molothrus ater, suggest geographical variation in female copulatory responsiveness to the two categories of male courtship songs, flight whistles (FWs) and perched songs (PSs). Females from the eastern M. ater ater subspecies and midwestern populations of the M. a. artemisiae and M. a. obscurus subspecies were reported to give copulation solicitation responses only to playback of PSs. But females from far western populations of M. a. artemisiae and M. a. obscurus responded to both PSs and FWs. An east-west difference in the social salience of FWs could have an ecological basis. FWs are used mostly for long-distance signalling and because western birds have larger home ranges they may use FWs more often. However, the disparate FW findings may result from different procedures used to assess female responsiveness to playbacks. Determining whether the disparate findings are due to geographical variation or to methodological differences is important because many potentially significant insights into song development and female preferences in oscines are based on cowbirds. Furthermore, either explanation would elucidate important links between female choice and male sexual displays. To resolve this issue, we tested M. a. ater females from New York using identical procedures to those we used in the far west and found that they were highly responsive to both FWs and PSs. This does not support the hypothesis that there is pronounced geographical variation in the courtship salience of FWs. Rather, it suggests that different procedures used by researchers in different areas of the cowbird’s range are responsible for the disparate findings. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

The song structure and seasonal patterns of vocal behavior of male and female bellbirds (Anthornis melanura)

The bellbird (Anthornis melanura) is a honeyeater endemic to New Zealand, which uses song to defend breeding territories and/or food resources year round. Both sexes sing and the song structure and singing behavior have not yet been quantified. The number of song types, spectral structure, repertoire size, and singing behavior of male and female bellbirds was investigated for a large island population. Song types differed between the sexes with males singing a number of structurally distinct song types and females producing song types that overlapped in structure. Singing behavior also differed between the sexes; males often sung long series of songs while females sung each song at relatively long and variable intervals. Singing by both sexes occurred year round but the frequency of male and female singing bouts showed contrasting seasonal patterns. The frequency of female singing bouts increased as the breeding season progressed, whereas male singing bouts decreased. In contrast to almost all studied passerines, female bellbirds exhibited significant singing behavior and sung songs of complex structure and variety that parallel male song. These results provide a quantitative foundation for further research of song in bellbirds and in particular the function of female vocal behavior.     

The agonistic and sexual functions of vocalizations of male brown-headed cowbirds,Molothrus ater

Functional analyses of three vocalizations of male brown-headed cowbirds, Molothrus ater, are presented and it is shown that two of these function as songs. Perched song (PS) is given by stationary birds and is used over short distances in male-male aggression and female courtship. The ‘flight whistle’ (FW) is a multisyllabic, usually pure tone, vocalization and the ‘single syllable flight call’ (SS) a monosyllabic pure tone. FWs and SSs are given occasionally by perched males and repetitively by flying males. Field playbacks of FWs showed that male cowbirds responded in the agonistic way most passerines respond to playback of conspecific song. Playbacks of the female's chatter call demonstrated that males of all three subspecies use FWs and SSs, but almost never PSs, to communicate with a female as they approach her. Thus FWs and SSs are used to communicate over long distances with both males and females. FWs are also used in one critical short-distance context as they are significantly more likely than PSs to be given just before copulations in nature, at least in our western study area. By contrast, studies of captive eastern cowbirds showed that PSs regularly precede copulations whereas FWs rarely do so. These different results for western and eastern birds may be an artefact of captivity and/or a result of geographical variation in behaviour.     

Testosterone Induces Sexual Release Quality in the Song of Female Canaries

We tested the sexual responsiveness of female canaries, Serinus canaria, to two sets of different types of female conspecific songs versus an adult male conspecific song. Female songs were either spontaneously emitted (‘S-songs’) or were testosterone-induced (‘T-songs’). Copulation-solicitation displays (CSD) were used as an index of female sexual response. Playbacks were performed several days before and during egg laying, a period of natural sexual responsiveness of the females to song. We demonstrated that the weaker sexual displays of female canaries were recorded to S-songs, thus suggesting that these types of female songs do not contain fully functional sexual releasers. Three T-songs elicited high levels of sexual displays, thus demonstrating that testosterone treatment may induce sexual release quality in the female songs. Study of the phonology of these three T-songs strongly suggested that special song phrases may be good candidates as powerful sexual releasers. To test the sexual value of these female song phrases, we carried out a third experiment, using hybrid songs where each of these special T-song phrase types was included in a well-known heterospecific context. Two phrases elicited high levels of sexual responses in females. Essential features of the male full song, such as broadband rapid frequency modulations and high repetition rate, are retrieved in both female song phrases. Taken together, these data demonstrate that testosterone treatment not only induces a male-like structure in the songs of females, but also induces functionally ‘male-like’ songs. This result allows features of the vocal control network of testosterone-treated females to be compared with those of adult males singing full songs, to distinguish neural correlates of testosterone-dependent full songs. However, because testosterone does not induce functionally male-like songs in all the females, neuroanatomical structure-function correlations need detailed behavioural analysis.     

Rufous‐capped Warblers Basileuterus rufifrons show seasonal,temporal and annual variation in song use

In the majority of songbird species, males have repertoires of multiple song types used for mate attraction and territory defence. The wood‐warblers (family Parulidae) are a diverse family of songbirds in which males of many migratory species use different song types or patterns of song delivery (known as ‘singing modes’) depending on context. The vocal behaviour of most tropical resident warblers remains undescribed, although these species differ ecologically and behaviourally from migratory species, and may therefore differ in their vocal behaviour. We test whether male Rufous‐capped Warblers Basileuterus rufifrons use distinct singing modes by examining song structure and context‐dependent variation in their songs. We recorded multiple song bouts from 50 male Warblers in a Costa Rican population over 3 years to describe seasonal, diel and annual variation in song structure and vocal behaviour. We found that Rufous‐capped Warbler songs are complex, with many syllable types shared both within and between males’ repertoires. Males varied their song output depending on context: they sang long songs at a high rate at dawn and during the breeding season, and shortened songs in the presence of a vocalizing female mate. Unlike many migratory species, Rufous‐capped Warblers do not appear to have different singing modes; they did not change the song variants used or the pattern of song delivery according to time of day, season or female vocal activity. Our research provides the first detailed vocal analysis of any Basileuterus warbler species, and enhances our understanding of the evolution of repertoire specialization in tropical resident songbirds.     

Testosterone-induced Singing in Female European Starlings (Sturnus vulgaris)

Adult female starlings (Sturnus vulgaris) were injected with testosterone in order to determine the song structures they had in memory. Those females had been caught in the wild in different geographical areas and had different ages. This hormone treatment clearly stimulated singing behaviour of females in isolation and revealed their ability to sing quite complex songs. Both categories of songs observed in males (warbling and whistles) were demonstrated and large repertoires were observed. Although the testosterone treatment may have altered the female song system and induced male-like vocalizations, it is interesting that none of the species-typic elements of male starlings was produced by the experimental females. Large changes were found in both repertoire size and composition over a year, revealing a high plasticity, even in older birds. We also found evidence that even under testosterone treatment, females do not necessarily sing all the songs they may have in memory.     

Is Female Visual Signaling to Male Song Socially Regulated in Brown‐headed Cowbirds?

This research focused on how adult female brown‐headed cowbirds, Molothrus ater, regulate social feedback on a group level to shape the development of male song. Specifically, females produce rapid wing movements in response to male song, termed ‘wing strokes,’ which have been shown to shape male song and predict song quality. These effects have been documented in captive dyads and triads, but not in more naturalistic flocks, where song development actually occurs. Here, we studied wing stroking in small seminatural flocks of differing female‐to‐male ratios. Despite differences in the number of females and their social selectivity, the same pattern of female feedback emerged in seven of eight flocks: One female produced the majority of wing strokes to male song, making her the primary wing stroker in her flock. Previous studies on large flocks have demonstrated females to facilitate male song improvisation and development if they exhibited higher social selectivity by approaching immature males less. Here, we found that primary wing strokers were indeed more socially selective than non‐primary wing strokers. This research is the first to document social stimulation being facilitated at the group level to ensure that more highly selective females deliver the most feedback.     

Male singing behaviour and female presence in the territory in whitethroats Sylvia communis

Unmated male songbirds usually change their vocal behaviour when females enter their territories. Either the males court the females by changing the rate or pattern with which their normal long-ranging full songs are emitted, or they shift to special displays and long- or short-ranging vocalisations. In this study we quantified how female presence and behaviour affect the singing behaviour of male whitethroats. In the presence of a female the male frequently performed song flights, maybe to locate the female before it was courted, with sequences of diving-song displays. The courtship was interrupted by periods of perch songs. Female dscharp calls and short movements made the males initiate or resume courtship, whereas short horizontal jumps made the males intensify their courtship. Overall, the males changed their dual-function song activity in females' presence by emitting fewer perch songs and more flight songs. The quiet diving songs were only emitted during direct courtship of a female. The song types emitted immediately before, during, and after courtship are all highly variable, thus allowing for a quick assessment of the male's song repertoire. The courtship was also interrupted by periods of male woid calling, a call that is known to have a deterring effect on rival males. Bouts of woid calls were usually followed by song flights, again probably to locate the female that might have moved out of sight, or maybe to locate potential rival intruders. The latter was supported by an increased intrusion rate during female presence. Communicated by P. McGregor