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.     

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.     

KNOWN SECONDARY CONTACT AND RAPID GENE FLOW AMONG SUBSPECIES AND DIALECTS IN THE BROWN-HEADED COWBIRD

We analyze geographic variation in morphology for Sierra Nevadan populations of Brown-headed Cowbirds (Molothrus ater) in relation to two levels of geographic structure of populations: 1) subspecies and 2) vocal dialects. Two morphologically distinct subspecies occupy opposite slopes of the Sierra Nevada: M. a artemisiae on the east slope is larger than M. a. obscurus on the west slope, and its juveniles have predominantly white versus yellow rictal (bill) flanges. Populations of obscurus moved into California from the lower Colorado River around 1900 and invaded the western Sierra during the 1930's. A relatively constant type of flight whistle occurs in obscurus populations up to 700 km apart, but east-slope artemisiae are divided into many distinct dialects. The means of seven morphological measurements and of principal component 1 (i.e., body size) for 2,287 individuals show similar clinal patterns for adult males, yearling males, and females over a 60-km north–south transect along the eastern Sierra Nevada: large sizes occur at the southernmost study site at Bishop, decrease clinally to the north to Mammoth Lakes, and then increase clinally to the north from Mammoth Lakes to the northernmost site at Lee Vining. This reversal in cline slope is reiterated for variation in the frequency of white-flanged juveniles. Our data do not support adaptive explanations for the clines. Rather, the most parsimonious explanation is that there has been flow of obscurus genes into artemisiae from the west slope across the crest of the Sierra Nevada into the Mammoth Lakes area. Concordantly, the Sierran crest at Mammoth Lakes is considerably lower than any other point within about 80 km to the north or 180 km to the south. Two other findings strongly support this interpretation. First, wing lengths of our longest-winged samples (at Bishop and Lee Vining) are significantly shorter than those of cowbirds collected in the same region between 1912 and 1922. Second, the wing lengths of Mammoth Lakes adult males and females during 1978–1981 are significantly larger than those of the 1982–1985 period. This putative hybridization must have been rapid, as there have been fewer than 50 years since secondary contact could have occurred. Calculation of the gene-flow parameter Ι of Endler (1977) indicates that the gene-flow rate reported here is higher than for nearly all of the species he surveyed. This gene flow occurs between two subspecies with different flight whistles and across several cowbird flight-whistle dialects within artemisiae. Therefore, vocal differences among these dialects do not appear to be a strong deterrent to gene flow.     

Patterns of courtship between cowbird subspecies: evidence for positive assortment

The courtship and mating behaviour of captive individuals from allopatric populations of two cowbird subspecies (Molothrus ater ater and Molothrus ater obscurus) were observed in a large indoor-outdoor aviary, using a multiple-choice design in order to assess whether they would selectively pair with members of their own subspecies. Twenty-nine of the 42 consortships observed were between consubspecifics, and 10 of the 15 copulating pairs were homogamic. Individuals tended to pair with consubspecifics whether or not they had had prior breeding experience with consubspecifics or winter contact with heterosubspecifics. This demonstration of selective courtship between individuals of widely separated populations is one of the first quantified examples, to our knowledge, of the development of assortative pairing in allopatry for a passerine species. These data place in perspective previous findings on the female cowbird's preferential response to playback of her own subspecies' song, thereby suggesting that song may be an important cue for selective mating between passerine populations.     

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.     

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.     

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.     

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.     

Male response to historical and geographical variation in bird song

In many species, individuals discriminate among sexual signals of conspecific populations in the contexts of mate choice and male–male competition. Differences in signals among populations (geographical variation) are in part the result of signal evolution within populations (temporal variation). Understanding the relative effect of temporal and geographical signal variation on signal salience may therefore provide insight into the evolution of behavioural discrimination. However, no study, to my knowledge, has compared behavioural response to historical signals with response to current signal variation among populations. Here, I measured the response of male white-crowned sparrows (Zonotrichia leucophrys) to historical songs compared with current songs from their local population, a nearby non-local population and a distant population. Males responded most strongly to current local songs, less, but equally, to historical local and current non-local songs, and least to songs of the distant population. Moreover, response to both temporal and geographical variation in song was proportional to how much songs differed acoustically from current local songs. Signal evolution on an ecological time scale appears to have an effect on signal salience comparable to differences found between current neighbouring populations, supporting the idea that behavioural discrimination among learned signals of conspecific populations can evolve relatively rapidly.     

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.     

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.     

A generalist brood parasite modifies use of a host in response to reproductive success

Avian obligate brood parasites, which rely solely on hosts to raise their young, should choose the highest quality hosts to maximize reproductive output. Brown-headed cowbirds (Molothrus ater) are extreme host generalists, yet female cowbirds could use information based on past reproductive outcomes to make egg-laying decisions thus minimizing fitness costs associated with parasitizing low-quality hosts. We use a long-term (21 years) nest-box study of a single host, the prothonotary warbler (Protonotaria citrea), to show that local cowbird reproductive success, but not host reproductive success, was positively correlated with the probability of parasitism the following year. Experimental manipulations of cowbird success corroborated that female cowbirds make future decisions about which hosts to use based on information pertaining to past cowbird success, both within and between years. The within-year pattern, in particular, points to local cowbird females selecting hosts based on past reproductive outcomes. This, coupled with high site fidelity of female cowbirds between years, points to information use, rather than cowbird natal returns alone, increasing parasitism rates on highly productive sites between years.     

Response of brown-headed cowbirds to simulated conspecific intruders

The response of brown-headed cowbirds (Molothrus ater) to simulated intruders was examined using playbacks of cowbird vocalizations in conjunction with a model of a male or female cowbird. Females reacted aggressively to female vocalizations but not to male vocalizations. Solitary males approached and often courted the female model but did not approach the male model. Males accompanying females showed little reaction to either model, although some evidence suggests that proximity to the male model may influence their response. These data support the hypothesis that female cowbirds are territorial and that males guard females from the solications of other males. The ecological pressures which may have influenced the development of this social system are discussed.     

Referential alarm calling elicits future vigilance in a host of an avian brood parasite

Yellow warblers (Setophaga petechia) use referential ‘seet’ calls to warn mates of brood parasitic brown-headed cowbirds (Molothrus ater). In response to seet calls during the day, female warblers swiftly move to sit tightly on their nests, which may prevent parasitism by physically blocking female cowbirds from inspecting and laying in the nest. However, cowbirds lay their eggs just prior to sunrise, not during daytime. We experimentally tested whether female warblers, warned by seet calls on one day, extend their anti-parasitic responses into the future by engaging in vigilance at sunrise on the next day, when parasitism may occur. As predicted, daytime seet call playbacks caused female warblers to leave their nests less often on the following morning, relative to playbacks of both their generic anti-predator calls and silent controls. Thus, referential calls do not only convey the identity or the type of threat at present but also elicit vigilance in the future to provide protection from threats during periods of heightened vulnerability.     

Atypical Song Reveals Spontaneously Developing Coordination between Multi-Modal Signals in Brown-Headed Cowbirds (Molothrus ater)

The courtship and dominance behavior of brown-headed cowbirds (Molothrus ater) consists of a multi-modal display, including song as well as postural and wing movements. The temporal sequences of the acoustic and the visual display are coordinated. In adult male cowbirds the largest wing movements of the display are synchronized with silent periods of song, but it is unknown how this coordination emerges during song development. Here we investigate how visual display features are coordinated with song by using atypical song sequence structure of isolation-reared male cowbirds. In birds with atypical song, all components of the visual display were highly similar to those of “normal” song displays, but their timing was slightly different. The number of maximal wing movement cycles of isolation-reared males was linked to the number of sound units in the song, and was therefore reduced during the abbreviated song types of isolates. These data indicate that young cowbirds do not need to be exposed to a model of the visual display during ontogeny and that there is synchronization with the temporal structure of song. A physiological link between respiratory and syringeal control of silent periods between sound units and wing movement cycles may be driving this synchronization.     

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.     

Winter dialects in the bronzed cowbird and their relationship to breeding-season dialects

Studies of geographical variation in animal signals generally focus on breeding-season behaviour but, in many species, signalling persists throughout the year. In passerine birds, patterns of variation in the nonbreeding season might provide opportunities for vocal learning that have been neglected by a historic focus on breeding-season behaviour. This study provides the first example of dialect variation outside of the breeding season. Quantitative analysis of acoustic similarity showed discrete differences between the songs of bronzed cowbirds, Molothrus aeneus, in four winter flocks. Most songs produced by members of a given flock were classified as belonging to the same dialect. Songs from one of the four winter dialects were indistinguishable from songs recorded in the breeding season in the same region. Depending on migratory patterns, dialects in one season may be a consequence of dialects in the other season, or the two seasonal patterns may be the result of independent social or evolutionary forces. Because the nonbreeding season is an important period of vocal learning in some bird species, winter dialects might limit the range of signals available for individuals to learn to produce. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Macrogeographical variation in the song of a widely distributed African warbler

The songs of oscine passerine birds vary on many spatial scales, reflecting the actions of diverse evolutionary pressures. Here we examine the songs of Cisticola erythrops, which effectively signal species identity across a geographical area spanning 6500 km in sub-Saharan Africa. Selection for species identification should promote stability in song traits, while sexual selection and geographical segregation should promote diversity. Cisticola erythrops share syllable types across the entire range of species and structure songs similarly, but individuals sing highly variable songs through improvisational recombination of syllables. Patterns of syllable use change gradually across the range of the species and do not show distinct breaks at subspecies boundaries. The acoustic properties of the most common syllable type also change gradually with distance. The results illustrate how songs can be simultaneously species-specific and highly variable at an individual level. At a larger level, patterns of variation indicate that cultural drift has generated song diversity through an isolation by distance mechanism.     

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.     

Courtship in two species of periodical cicadas, Magicicada septendecim and Magicicada cassini

Courtship behaviour of two species of periodical cicadas, Magicicada septendecim and M. cassini, was studied in the field during the 1970, 1973, and 1974 emergences of these insects. In areas where both species were courting there were differences in both male and female courtship patterns, both in acoustic and behavioural components. Experiments with models showed that male M. septendecim were more likely to court crude models of females than were M. cassini males. When females were ‘courted’ with models that could imitate some of male courtship, they were more receptive when the models' ‘songs’ were those of conspecific males. Acoustic differences between species are probably used by females in mate selection, maintaining species separation even in areas where the two species overlap in both space and time.