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.     

Female marsh wrens do not provide evidence of anatomical specializations of song nuclei for perception of male song

In songbirds the forebrain nuclei HVC (high vocal center) and RA (robust nucleus of the archistriatum) are larger in individuals or species that produce larger song repertoires, but the extent to which the size of these nuclei reflects a need for either producing or perceiving large repertoires is unknown. We, therefore, tested the hypothesis that species differences in the size of song nuclei reflect a commitment of “brain space” to the perceptual processing of conspecific song. The two species of marsh wren (Cistothorus palustris western and eastern) provide a good test case. Western males produce larger song repertoires, and have larger HVC and RA than do eastern males. Female marsh wrens do not sing, and if they use their song nuclei to assess conspecific male song repertoires, then we predicted that measurable cellular and nuclear parameters of HVC and RA would be greater in western than eastern female wrens. For males we confirmed that the volumes of HVC and RA, and cellular parameters of HVC, are greater in western than in eastern birds. These nuclei were also considerably larger in males than in conspecific females. Western and eastern female wrens, however, did not differ in any measured parameters of HVC or RA. Females of these wren species thus do not provide any direct evidence of anatomical specializations of song nuclei for the perceptual processing of conspecific male song. 1994 John Wiley & Sons, Inc.     

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.     

Monogamy and brood parasitism: an unlikely pair

Intensive observation of a population of brood parasitic brown-headed cowbirds (Molothrus ater), including 114 marked birds, demonstrated that monogamy is the prevalent mating system. Analysis of 1280 consort events and 73 copulations showed that nearly all copulations were between a female and the male most often seen with her, even though females had ample opportunities to mate with other males. Although monogamy prevails, some pair bonds do not endure throughout the breeding season. They are more unstable during the early season when resident cowbirds are establishing their social interrelations. This study provides strong evidence that the cowbird's mating system varies geographically, as the only previous study based on observed copulations demonstrated promiscuity. Current hypotheses for the evolution of avian mating systems, when considered in light of the field data presently available, do not fully explain the adaptive significance of monogamy in a parasitic bird.     

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.     

Searching for the functional origins of song in eastern brown-headed cowbirds,Molothrus ater ater

Three experiments were conducted to examine the functional properties of vocal precursors to stereotyped song in socially housed captive cowbirds. Previous studies had shown that eastern male cowbirds developed different song repertoires when housed in different social contexts. This paper reports on the acoustic origins of the different vocal outcomes. In addition, a winter roost of cowbirds was studied to investigate the setting in which males naturally develop song. Analyses of the vocalizations of laboratory-housed subjects revealed acoustic differences from the earliest stages of song ontogeny. The field data indicated that free-living and laboratory-housed males shared the same structural categories of song and that the winter roost provided males with opportunities to interact with females. Taken as a whole, the studies suggest that song ontogeny is a dynamic process involving social and vocal interactions between singers and listeners.     

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.     

The Functions of Song in the Serin

The function of song in the serin Serinus serinus was investigated by measuring variation in singing time and song flights by the male, and nest building by the female during the prelaying and laying period, and by correlating nest building, extra-pair copulation attempts and chasing of the female with male singing time and song flights between pairs. Both singing time and nest building varied in relation to the female fertile period, peaking at day −4. Moreover, nest-building activity correlated with singing time, but not song flights, between pairs. This suggests that song may have a function in stimulating the female to nest build or begin rapid yolk deposition. Pair copulations were not correlated with singing time or song flights either over days relative to laying or between pairs and pairs were not more likely to copulate in a given minute of observation when the male had sung in the previous minute than when he had not. However, extra-pair copulation attempts and chasing of the female showed a tendency to be negatively correlated with song flight but not singing time, between pairs. This suggests that song flight may have a function in discouraging sexual competition from other males.     

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     

Social Guidance of Vocal Learning by Female Cowbirds: Validating its Functional Significance

Juvenile male M. a. ater cowbirds, who have never heard other male cowbirds sing, develop distinctively different repertoires when housed with M. a. ater females from their own area versus M. a. obscurus females from a distant population. Because female cowbirds do not sing, the differences in the males' songs do not arise through vocal imitation. Here we provide data demonstrating that the songs of female-housed males are functionally, as well as acoustically, distinctive. The songs of 8 groups of males were tested where the groups differed by age of singer, acoustic experience, and identity of social companion. The playback results demonstrate that non-singing female cowbirds not only stimulate the male to modify song content, but song potency. As such, they demonstrate the critical role female cowbirds may assume in the proximate and ultimate regulation of vocal development.     

A test for repertoire matching in eastern song sparrows

Repertoire matching occurs when one songbird replies to another with a song type that the two birds share. Repertoire matching has previously been demonstrated to occur at well above chance levels in a western population of song sparrows, where it is hypothesized to serve as a low level threat in a hierarchy of aggressive signals. Here we test for repertoire matching in an eastern population of song sparrows. Previous work indicates that this eastern population differs from the western one in having lower levels of song sharing between neighboring males and in showing no association between song sharing and territory tenure. Here we confirm that males in this eastern population on average share few whole songs with their neighbors. The eastern males are familiar with their neighbors’ repertoires, as evidenced by a stronger singing response to stranger song than to neighbor song. Males in the eastern population did not repertoire match: when played an unshared song type from a specific neighbor, they did not reply with a song type shared with that neighbor more often than expected by chance or more often than in response to playback of a control song (an unshared stranger song). The results thus demonstrate a qualitative difference in vocal signaling strategies between two populations of the same species.     

A GENETIC AND BEHAVIORAL ANALYSIS OF MATE CHOICE AND SONG NEIGHBORHOODS IN INDIGO BUNTINGS

Neighboring males of indigo buntings (Passerina cyanea) share songs in southern Michigan. We sampled polymorphic enzymes to compare the genetic variation between mates and the variation among contiguous song neighborhoods. Mate choice was independent of the genetic and morphometric similarity of female and male, and these measures were independent of each other. The incidence of extrapair copulations and fertilizations was independent of the song of cuckolding males. Breeding success of the mated pairs was independent of their genetic or morphological similarity. Males characterized by different song dialects did not differ in mean lifetime reproductive success. We found no significant genetic differences among the neighborhoods. Most birds that bred in one song neighborhood were born in another, and neighborhoods were not isolated demes. Bunting songs may provide no information to a female about genetic quality of males. The results are consistent with a neutral model of no mate choice for genes.     

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.     

Evolution of nocturnal flight calls in migrating wood-warblers: apparent lack of morphological constraints

Many migratory songbirds produce flight calls that vary, sometimes strikingly, among species in duration, frequency, modulation, and pattern, and little is known about what factors are responsible for this variation. Negative correlations between body mass or bill length and song frequencies are well documented in birds, but no studies have examined these associations for flight calls. We explored relationships between flight call and song frequencies and body mass or bill length in 33 species of wood-warblers. Phylogenetically controlled and uncontrolled analyses showed no significant relationship between body mass or bill length and flight call frequency; however, we found significant differences between flight call and song frequencies and a significant relationship between maximum frequencies of flight calls and songs. Our findings suggest that factors other than body mass and bill length are responsible for variation in flight call frequencies in wood-warblers. We suggest that different ecological and atmospheric properties might play important roles in selection for flight call frequencies.     

Facultative development of courtship and communication in juvenile male cowbirds (Molothrus ater)

We investigated effects of naturally occurring variation inexperience with adult males on development of song and courtshipcompetence in captive juvenile cowbirds. We studied birds ingroups housed in large outdoor aviaries that allowed birdsto regulate access to social stimulation. In two aviaries, we housed juvenile males and females either with or withoutadult males. Birds remained in these conditions from September1999 through their breeding season. We documented social andvocal development of juvenile males in the two aviaries bymeasuring social assortment and patterns and frequencies of their song interactions. We then brought the juveniles fromthe two aviaries together to compete against each other foraccess to females. In addition, we recorded juveniles' songsfour times over the study and played back their breeding seasonsongs to females in sound-attenuating chambers to measure the effectiveness of songs in eliciting copulatory responses fromthe females. Compared to juvenile males housed with adult males,juvenile males housed without adult males developed atypicalbehavior patterns. They (1) displayed little intrasexual aggressionor near-neighbor associations and (2) exhibited different patternsof courtship and copulation, but (3) were as successful at competing for copulations. Furthermore, they developed stereotypedsongs sooner and developed more potent breeding season songs.These different outcomes could not be traced to one variablebut to a cascade of effects involving diverging patterns ofsong acquisition and social interaction. The patterns of socialskills that emerged indicate considerable plasticity in the mechanisms underlying acquisition of courtship competence.     

Undirected Song in Wild Zebra Finch Flocks: Contexts and Effects of Mate Removal

Wild zebra finches, Taeniopygia guttata, sing frequently throughout the year but the function of undirected song, the most prevalent type, is unknown. Paired males commonly sang undirected song in feeding flocks where it occurred more frequently in the non-breeding season than in the breeding season. Song rate varied greatly among males. The context of the singer and the absence of any overt responses from flock members excludes direct aggressive and mate-attracting functions. Performance of undirected song may have energetic costs and predatory risks. The finding that singers are active individuals with ‘spare time’, that are neither hungry, nor tired, nor sexually motivated, suggests that singers are advertising their ‘quality’ as potential mates and/or participants for extra-pair copulations. When the female partner in non-breeding pairs was experimentally removed, the rate of undirected song of the ‘widower’ increased significantly. Males quickly re-paired. This experiment supports the hypothesis that singing in the flock has a mate-attracting role.     

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.     

Population density and the intensity of paternity assurance behaviour in a monogamous wader: the Curlew Numenius arquata

We compared paternity assurance behaviour and related displays in high (1.6 pairs perkm²) and low (6.7 pairs per km²) density populations of the Curlew Numenius arquata breeding on arable farmland in western Finland. There was little evidence of individuals pursuing extra-pair copulations or males exhibiting paternity assurance behaviour. Furthermore, there was no variation in the frequency of intrusions or in the intensity of paternity assurance behaviour relative to lay date. However, intrusions and approaches to the pair female by extra-pair males were more frequent at high breeding density, and pair males remained closer to their female, followed her more and exhibited a higher frequency of copulatory behaviours in the high-density population. Therefore, high breeding density appeared to increase opportunities for individuals to copulate outside the pair-bond and resulted in more intense male paternity guards. Male song flight displays were also more frequent in the high-density population. Territorial absences by males were infrequent in both areas. The increased frequency of intrusions and interactions between non-pair individuals (male-male and male-female) at high density were probably the major factors in explaining area differences in the intensity of paternity assurance and territorial behaviour.     

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.