Male vocal imitation produces call convergence during pair bonding in budgerigars, Melopsittacus undulatus

The budgerigar, a small species of parrot, can learn new vocalizations throughout life and is therefore widely used as a model system for studying various aspects of vocal learning. It is not known, however, why parrots imitate sounds. To test the hypothesis that vocal imitation in budgerigars is related to pair bonding, we recorded approximately 100 contact calls from each of nine male and nine female adult budgerigars that were unfamiliar with one another and then placed them into pairs. We sampled their contact call repertoire weekly and conducted twice-weekly behavioural observation sessions. We compared contact calls by sonagram cross-correlation and classified them by means of a hierarchical clustering algorithm. This analysis showed that all pairs developed a shared call within an average of 2.1 weeks. Further analysis revealed that eight of the nine male budgerigars imitated the contact calls of their assigned mates, while none of the females imitated the calls of their males. We conclude that contact call imitation in adult budgerigars probably contributes to pair bond formation and maintenance. Prior studies on budgerigars were limited by the lack of a behavioural paradigm to elicit vocal imitation reliably. Our study remedies this and thereby serves as a foundation for future studies on vocal learning in adult animals. Copyright 2000 The Association for the Study of Animal Behaviour.     

Call Convergence within Groups of Female Budgerigars (Melopsittacus undulatus)

The budgerigar (Melopsittacus undulatus) is a promising model species for the study of adult vocal learning. To date, several studies have confirmed the existence of vocal plasticity and, more importantly, rapid imitation of contact calls by adult male budgerigars. Vocal learning has not been investigated in female budgerigars, however. Since one likely function of the contact call is to denote group affiliation, we tested the hypothesis that female budgerigars, when placed into groups, would develop a shared contact call. We recorded the contact call repertoires of eight adult female budgerigars that were unfamiliar with one another, then placed them into two groups. Each group was deprived of visual contact with other birds. Recording sessions continued for the subsequent 8 wks, and behavioral observations were also conducted during this time. Within 4–7 wks, females in both groups converged on a common call type. This rate of convergence is slower than that observed in prior experiments limited to male birds, and much slower than vocal imitation by male budgerigars paired with females. Therefore, while our study documents vocal plasticity in adult female budgerigars, it also suggests that female budgerigars learn new vocalizations more slowly than males do.     

Brain lesions that impair vocal imitation in adult budgerigars

Vocal imitation is a complex form of imitative learning that is well developed only in humans, dolphins, and birds. Among birds, only some species are able to imitate sounds in adulthood. Of these, the budgerigar (Melopsittacus undulatus) has been studied in most detail. Previous studies suggested that the vocal motor system in budgerigars receives auditory information from the lateral frontal neostriatum (NFl). In the present study, we confirm this hypothesis by showing that infusions of the GABA agonist muscimol into NFl reduce the strength of auditory responses in a telencephalic vocal motor nucleus, the central nucleus of the lateral neostriatum (NLc). To test whether the auditory information conveyed from NFl to NLc plays a role in vocal imitation, we lesioned parts of NFl and the overlying ventral hyperstriatum (HVl) in seven adult male budgerigars and then examined whether the lesioned males would imitate the calls of females with whom they were paired. We found that, compared to sham-lesioned controls, the lesioned birds were significantly impaired in their imitation of female calls. Yet, the lesioned males were clearly not deaf (e.g., their previously learned calls did not degrade as they do after deafening). Therefore, the data suggest that NFl/HVl lesions impair vocal imitation by reducing the amount of auditory information that reaches the vocal motor system. Interestingly, the females that were paired with lesioned males displayed more vocal plasticity than the females in the control group, and some even imitated their male's prepairing calls.     

Assortative Pairing Based on Contact Call Similarity in Budgerigars, Melopsittacus undulatus

A trait typical of parrots, but rare in other groups of birds, is the acquisition of new learned calls (acquired by copying conspecifics) throughout an individual's lifetime. The significance of this distinctive psittacid trait is not understood. In budgerigars, females preferentially affiliate with unfamiliar males whose contact calls resemble their own during brief dyadic choice trials; also, in forced‐pair situations, contact call similarity of members of pairs increases as a result of a male tendency to imitate his mate's call type. The functions of budgerigar call imitation and preference for pre‐pairing similarity are currently unknown. Moreover, as budgerigar pair formation occurs over a span of days or weeks, it is important to determine whether birds in breeding colonies assort and proceed to breed on the basis of pre‐pairing contact call similarity, and whether high levels of call similarity are maintained after pair formation is complete. To explore these questions, we recorded contact calls of male and female budgerigars before and after they were placed into an aviary equipped for breeding. As predicted, birds paired assortatively based on pre‐pairing call similarity. Once birds had paired, their calls converged further in acoustic structure, as previous work had led us to expect. However, after eggs were laid and the males began to feed their mates, the calls of mated birds diverged, suggesting that there might be some cost to maintenance of shared calls. Male care‐giving correlated with the degree to which his pre‐pairing calls resembled those of his mate, but not with the similarity achieved through convergence. These results suggest that female budgerigars may use a male's pre‐pairing call similarity as a predictor of paternal investment. The questions of why such similarity predicts male care‐giving, and why calls converge following initial pairing activities, require further work.     

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.     

‘Virtual Parrots’ Confirm Mating Preferences of Female Budgerigars

Parrots comprise one of the several taxa in which life‐long learning of new vocal signals used in intraspecific communication is known to occur routinely. The functions and evolutionary bases of this ability are largely unknown. In the budgerigar (Melopsittacus undulatus), males typically imitate their partner’s contact call type during pair formation. However, a female’s initial choice among unfamiliar males is not based on their production of her call type, because birds without prior social contact rarely produce the same call type. Here, we demonstrate that female budgerigars prefer unfamiliar males with calls that are similar to their own, as measured by spectrogram cross‐correlation, but which are not imitations. This was shown by training females via operant conditioning to control access to movies of courting males and by systematically varying the audio tracks of these movies. Females learned this task easily and interacted with virtual males as if they were real. This methodology will be useful for exploring functions and mechanisms of social communication, because it eliminates the confounding impact of short‐term changes in a stimulus individual’s behavior on a test individual’s response. Our results suggest that the neuroplastic vocal abilities of budgerigars, and perhaps other parrots, have been shaped by sexual selection.     

For whom the male calls: an effect of audience on contact call rate and repertoire in budgerigars, Melopsittacus undulatus

Budgerigars are well known for their ability to imitate sounds, but little is known about the functional contexts in which they use these imitations. Recently, we have shown that male budgerigars consistently imitate the contact calls of the females with whom they are paired. Here we investigate whether males produce these imitations more frequently when they are with their mates than when they are with other females. In one experiment, we established seven budgerigar pairs and then tested each male with his mate and with an unfamiliar female. In the second experiment, we allowed pairs to form freely in an aviary and then tested the males with their mate and with a familiar mated female. In both experiments, the males produced significantly more imitations of their mate's call (defined as calls that were more than 75% similar to the mate's predominant contact call) when they were with their mate than when they were recorded with another female. Under aviary conditions, this difference was due to both a general increase in the males' rate of calling and to an increase in the percentage of the males' calls that were imitations. These data show that male budgerigars modify their contact call rates and repertoires in an audience-specific manner. This audience effect is unusual because it involves a learned vocalization and is extremely specific to a particular audience, namely the mate. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Function of male song in the greater white-lined bat, Saccopteryx bilineata

The use of vocalizations by males to attract mates and defend territories is widespread in birds but uncommon in mammals. In the greater white-lined bat, males defend small territories in tree buttresses and produce complex audible vocalizations. During the day, females roost within these territories, and males with females in their territories have higher reproductive success than males without females. To determine call function, we recorded male vocalizations on the island of Trinidad and made behavioural observations of the focal male and nearby bats at the time the calls were given. Noisy broadband calls were directed mainly at other males whereas tonal calls were used primarily in interactions with females. Two other types of calls were given independently of any observable context and may be involved in territorial defence or conspecific notification. Poisson regression showed that males with song repertoires that contained more unique types of composite syllables had more females in their territories. In addition, several acoustic features of one common call type significantly correlated with the number of females on a territory. Male vocalizations may, therefore, transfer information to colony members about male quality or fighting ability.     

Sex‐specific responses to territorial intrusions in a communication network: Evidence from radio‐tagged great tits

Signals play a key role in the ecology and evolution of animal populations, influencing processes such as sexual selection and conflict resolution. In many species, sexually selected signals have a dual function: attracting mates and repelling rivals. Yet, to what extent males and females under natural conditions differentially respond to such signals remains poorly understood, due to a lack of field studies that simultaneously track both sexes. Using a novel spatial tracking system, we tested whether or not the spatial behavior of male and female great tits (Parus major) changes in relation to the vocal response of a territorial male neighbor to an intruder. We tracked the spatial behavior of male and female great tits (N = 44), 1 hr before and 1 hr after simulating territory intrusions, employing automatized Encounternet radio‐tracking technology. We recorded the spatial and vocal response of the challenged males and quantified attraction and repulsion of neighboring males and females to the intrusion site. We additionally quantified the direct proximity network of the challenged male. The strength of a male's vocal response to an intruder induced sex‐dependent movements in the neighborhood, via female attraction and male repulsion. Stronger vocal responders were older and in better body condition. The proximity networks of the male vocal responders, including the number of sex‐dependent connections and average time spent with connections, however, did not change directly following the intrusion. The effects on neighbor movements suggest that the strength of a male's vocal response can provide relevant social information to both the males and the females in the neighborhood, resulting in both sexes adjusting their spatial behavior in contrasting ways, while the social proximity network remained stable. This study underlines the importance of “silent” eavesdroppers within communication networks for studying the dual functioning and evolution of sexually selected signals.     

Auditory responses in the vocal motor system of budgerigars

Budgerigars (Melopsittacus undulatus) are small Australian parrots that can imitate novel sounds in adulthood and therefore serve as a convenient model system for the study of vocal learning in adult animals. Previous anatomical studies had indicated that known auditory regions in the telencephalon of budgerigars are connected, albeit indirectly and rather sparsely, to vocal motor nuclei. Physiological evidence for connections between the auditory and vocal motor systems in budgerigars had been lacking, however. Here, we show that neurons in a telencephalic vocal motor region, i.e., the central nucleus of the lateral neostriatum (NLc), are responsive to auditory stimuli in isoflurane-anesthetized budgerigars. These responses are highly variable from trial to trial and frequently have latencies in excess of 100 ms. Neurons in NLc generally respond better to a budgerigar's own contact call than to a white noise stimulus, but the response preferences of NLc neurons in budgerigars are generally weaker and more diverse than the response preferences of neurons in the high vocal center of songbirds, which is probably analogous to NLc. These data indicate that parrots and songbirds, which have evolved the ability to learn vocalizations independently of one another, have both evolved physiologically effective connections between their auditory and vocal motor systems. Interestingly, however, the anatomical pathways by which the auditory and vocal motor systems interact, and the physiological details of how they communicate, appear to be significantly different between the two taxa.     

Behavioral responses of males to estradiol-treated females in the budgerigar (<Emphasis Type="Italic">Melopsittacus undulatus</Emphasis>)

We investigated the effects of estradiol-treated females on the behavior of male budgerigars. In comparison to control females, females given implants of estradiol showed elevated nest behavior and darker cere color, which are characteristics of breeding females. After we confirmed the efficacy of estradiol treatment on behavior and morphology, each female was paired with a male mate. Males paired with estradiol-treated females showed more courtship behavior (auditory and visual display, and courtship feeding) to their mates than males paired with control females. These data indicate that budgerigar females with a high estrogen level enhance males' courtship behavior. Since males did not show response to estradiol-treated females soon after females were introduced, effects of estradiol-treated female budgerigars may be mediated by the endocrine system, rather than wholly by the nervous system, of males. Electronic Publication     

Vocal imitation in blindfolded zebra finches (<Emphasis Type="Italic">Taeniopygia guttata</Emphasis>) is facilitated in the presence of a non-singing conspecific female

Song acquisition in young male zebra finches, Taeniopygia guttata, is viewed as a learning process by imitation from a visible conspecific male acting as a song tutor. The role played by non-singing conspecific females in this process has been poorly documented. The influence of social contact on the song learning of blindfolded young males was investigated in both female-raised and pair-raised birds. Pupils with both eyes occluded from about 35 to 65 days post-hatch, the sensitive phase for song learning, copied significantly more from an adult male sharing their cage when tutored in the presence of a female sibling than in her absence. Interestingly, the effect was more pronounced in female-raised birds compared to pair-raised birds. I conclude that physical contact in the absence of visual cues is sufficient for song imitation to occur. The results demonstrate an instance of social stimulation by non-singing females in the song acquisition of male songbirds.     

Vocal learning by greater spear-nosed bats.

Vocal learning is well known among passerine and psittacine birds, but most data on mammals are equivocal. Specific benefits of vocal learning are poorly understood for most species. One case where vocal learning should be favoured by selection is where calls indicate group membership and group mates are unrelated. Female greater spear-nosed bats, Phyllostomus hastatus, live in stable groups of unrelated bats and use loud, broadband calls to coordinate foraging movements of social group mates. Bats benefit from group foraging. Calls differ between female social groups and cave colonies, and playback experiments demonstrate that bats perceive these acoustic differences. Here I show that the group distinctive structure of calls arises through vocal learning. Females change call structure when group composition changes, resulting in increased similarity among new social group mates. Comparisons of transfers with age-matched half-sibs indicate that call changes are not simply due to maturation, the physical environment or heredity. These results suggest that studies testing vocal learning in mammals could profit by focusing on vocalizations that signify group membership.     

Significance of temporal and spectral acoustic cues for sexual recognition in Xenopus laevis

As in many anurans, males of the totally aquatic species, Xenopus laevis, advertise their sexual receptivity using vocalizations. Unusually for anurans, X. laevis females also advertise producing a fertility call that results in courtship duets between partners. Although all X. laevis calls consist of repetitive click trains, male and female calls exhibit sex-specific acoustic features that might convey sexual identity. We tested the significance of the carrier frequency and the temporal pattern of calls using underwater playback experiments in which modified calls were used to evoke vocal responses in males. Since males respond differently to male and female calls, the modification of a key component of sexual identity in calls should change the male's response. We found that a female-like slow call rhythm triggers more vocal activity than a male-like fast rhythm. A call containing both a female-like temporal pattern and a female-like carrier frequency elicits higher levels of courtship display than either feature alone. In contrast, a male-like temporal pattern is sufficient to trigger typical male-male encounter vocalizations regardless of spectral cues. Thus, our evidence supports a role for temporal acoustic cues in sexual identity recognition and for spectral acoustic cues in conveying female attractiveness in X. laevis.     

Seasonal Changes of Vocal Rates and Their Relation to Territorial Status in Male Galápagos Sea Lions (Zalophus wollebaeki)

Male vocal displays play an important role in sexual selection through both male–male competition and female choice. While this is supported by numerous studies in birds, much less attention has been paid to the role of such displays in mammals. We investigated the function of vocal displays in a polygynous mammal, the Galápagos sea lion (Zalophus wollebaeki). In our study population a large proportion of mature males are unable to establish a territory, providing the opportunity to compare the vocal behaviour between territorial and non‐territorial males. We examined how seasonal patterns of vocalizations differed between territorial and non‐territorial males and how the number of females present in a territory influenced behaviour of territorial males. We found that territorial males vocalized at higher rates than non‐territorial males, and territorial males vocalized more at the onset than towards the end of territory tenure. During the onset of territory‐tenure vocalizations of territorial males were directed more often towards other males than females. Furthermore, we found that vocalizations of territorial males were not only given in male–male interactions, but were also actively directed towards females. Territorial males vocalized at higher rates when more females were present in their territory. Our results suggest that vocalizations are important in male–male interactions, are relevant in territorial disputes and are used as a proxy for females to assess a male’s quality.     

The relationship between perception and production in songbird vocal imitation: what learned calls can teach us

Songbirds produce calls as well as song. This paper summarizes four studies of the zebra finch long call, used by both sexes in similar behavioral contexts. Female long calls are acoustically simpler than male long calls, which include acoustic features learned during development. Production of these male-typical features requires an intact nucleus robustus archistriatalis, the sexually-dimorphic source of the telencephalic projection to brainstem vocal effectors. In experiments that quantified the long calls produced in response to long call playbacks, intact adult zebra finch males, but not females, show a categorical preference for the long calls of females over those of males. Experiments with synthetic stimuli showed that males classify long call stimuli that they hear by gender, using both spectral and temporal information, but that females use only temporal information. Juvenile males (<45 days) did not show the categorical preference, but it emerged during the same period when the robustus archistriatalis matures anatomically and the first male-typical vocalizations are produced. Adult males with robustus archistriatalis lesions lost the categorical preference for female long calls, suggesting that the robustus archistriatalis plays a role in long call discrimination. These results demonstrate that calls complement song as a potent tool for studying the neurobiology of vocal communication.     

Inter-sexual multimodal communication during mating in wild geladas: the leading role of females

Female primates can emit vocalizations associated with mating that can function as honest signals of fertility. Here, we investigated the role of mating calls and visual signals in female geladas (Theropithecus gelada). Because females have a central role in the gelada society and seem to solicit sexual interactions, we answered whether they emit vocalizations in conjunction with gazing to increase mating success probability. Before and during copulations, females can emit pre-copulation calls and copulation calls. For the first time, we identified a new female vocalization emitted at the final stage of copulations (end-copulation call), possibly marking the occurrence of ejaculation. We found that longer pre-copulation call sequences were followed by both prolonged copulations and the presence of end-copulation calls, thus suggesting that females use pre-copulation calls to ensure successful copula completion. Moreover, we found that different combinations of female vocal types and gazing had different effects on male vocal behavior and motivation to complete the copula. The analysis of the vocal and visual signals revealed a complex inter-sexual multimodal chattering with the leading role of females in the signal exchange. Such chattering, led by females, modulates male sexual arousal, thus increasing the probability of the copula success.     

An Automated Procedure for Evaluating Song Imitation

Songbirds have emerged as an excellent model system to understand the neural basis of vocal and motor learning. Like humans, songbirds learn to imitate the vocalizations of their parents or other conspecific “tutors.” Young songbirds learn by comparing their own vocalizations to the memory of their tutor song, slowly improving until over the course of several weeks they can achieve an excellent imitation of the tutor. Because of the slow progression of vocal learning, and the large amounts of singing generated, automated algorithms for quantifying vocal imitation have become increasingly important for studying the mechanisms underlying this process. However, methodologies for quantifying song imitation are complicated by the highly variable songs of either juvenile birds or those that learn poorly because of experimental manipulations. Here we present a method for the evaluation of song imitation that incorporates two innovations: First, an automated procedure for selecting pupil song segments, and, second, a new algorithm, implemented in Matlab, for computing both song acoustic and sequence similarity. We tested our procedure using zebra finch song and determined a set of acoustic features for which the algorithm optimally differentiates between similar and non-similar songs.     

Interactive vocal communication at the nest by parent Great Tits Parus major

Although most bird species show monogamous pair bonds and bi‐parental care, little is known of how mated birds coordinate their activities. Whether or not partners communicate with each other to adjust their behaviour remains an open question. During incubation and the first days after hatching, one parent – generally the female – stays in the nest for extended periods, and might depend on acoustic communication to exchange information with its mate outside. The Great Tit Parus major is an interesting study system to investigate intra‐pair communication at the nest because males address songs to their mate while she is in the nest cavity, and females answer the male from the cavity with calls. However, the function of this communication remains unknown. In this study, we recorded the vocalizations and observed the resulting behaviour of Great Tit pairs around the nest at different breeding stages (laying, incubation and chick‐rearing). We observed vocal exchanges (vocalization bouts, alternated on the same tempo, between the female inside the nest and her male outside) in three contexts with different outcomes: (1) the female left the nest, (2) the male entered the box with food, and the female then used specific call types, (3) mates stopped calling but did not leave or enter the nest. The structure of vocal exchanges was globally stable between contexts, but females used calls with an up‐shifted spectrum during exchanges, at the end of which they left the nest or the male entered the nest. Birds vocalized more and at higher tempo during exchanges that ended up in feeding inside the nest. Birds also vocalized more during exchanges taking place during laying – a period of active mate guarding – than during incubation. We conclude that vocal exchanges could signal the females’ need for food and the males’ mate guarding behaviour, and discuss other possible functions of this communication.     

Graded Aggressive Calls in the African Painted Reed Frog Hyperolius marmoratus (Hyperoliidae)

The African painted reed frog, Hyperolius marmoratus, has a potentially complex communication system. Advertisement calls and aggressive calls, although distinct from each other, are in fact two ends of a continuum of graded calls. Playback experiments using standard advertisement calls showed that males increased the proportion of aggressive calls as the stimulus intensity was increased. In addition, three characteristics of the aggressive calls changed in response to higher playback levels. Males increased the number of pulses/call, increased call duration, and decreased dominant frequency. Aggressive calling occurred primarily during the early hours of the night, with considerable overlap with times when females were searching for mates in the chorus. Females tested in two-choice arena trials discriminated against aggressive calls in favor of advertisement calls. It is suggested that aggressive calls reduce a male's ability to attract a female and that a graded signalling system may enable males to escalate agonistic encounters with other males without rendering calls completely unattractive to females.