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.     

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.     

Effects of Male Vocal Learning on Female Behavior in the Budgerigar, Melopsittacus undulatus

Parrots are unusual among birds and animals in general in the extent of their ability to learn new vocalizations throughout life and irrespective of season. The budgerigar (Melopsittacus undulatus), a small parrot that is well suited for laboratory studies, has been the subject of numerous studies investigating the neurobiology of vocal learning. To date, few studies have focused on the function of vocal imitation by parrots. Previous work from our research group has shown that vocal imitation in budgerigars is sex‐biased, as males paired with females learn vocalizations from their new mates, but not vice versa. This bias led us to hypothesize that vocal learning has a reproductive function. To test this hypothesis, we conducted two experiments. In the first experiment, we tutored males so that they could produce a call similar to one shared by a group of experimental females. The experimental females were then presented with one of the tutored males and another, equally unfamiliar, male that had not been tutored. We found that the females spent a greater proportion of time in proximity of, and made more affiliative displays toward, the tutored males. In the second experiment, seven males received small bilateral brain lesions that disrupt vocal learning. These males and an equal number of control males were then released into an aviary containing females and reproductive resources. We found that lesioned and control males were equally successful in obtaining social mates, but females mated to lesioned males were more likely to engage in extra‐pair activities. These experiments indicate that a male's ability to imitate a female's call can influence the sexual behavior of the female even though lack of imitation ability does not appear to influence social pairing. We hypothesize that mate choice in budgerigars has multiple stages. Upon meeting a strange male, a female quickly assesses its ability for social acquisition of calls by the presence or absence of a call type similar to its own in its repertoire. As courtship proceeds into pair formation, the female assesses the ability of male to learn more directly by the extent of the male's perfection of imitation.     

DETECTION OF SPECIES-SPECIFIC CALLS IN NOISE BY ZEBRA FINCHES POEPHILA GUTTATA AND BUDGERIGARS MELOPSITTACUS UNDULATUS: TIME OF FREQUENCY DOMAIN?

ABSTRACT

Two zebra finches and two budgerigars were trained, by operant conditioning, to detect autogenous (self-generated) distance calls in the presence of masking noise. For both species, there were no differences in detection thresholds for normal calls compared to time- reversed calls. Thresholds for autogenous calls were also compared with thresholds of the other species of birds listening to the same call. When detecting a zebra finch call, budgerigars had slightly lower thresholds than that of the zebra finch. On the other hand, when detecting a budgerigar call, zebra finches showed significantly higher thresholds than the budgerigar. From these results, and from what is known about basic hearing capabilities in these species, we conclude that these birds are not using a mechanism which utilizes “matched” or cross-correlational filtering. It is more likely that they are using “frequency-based” filtering in detecting calls in noise.     

‘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.      

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.     

Lifetime patterns of pairing success in male Ortolan Buntings Emberiza hortulana

Analyses of lifetime fitness in birds are typically based on estimates of breeding success, in particular the number of offspring fledged. Small and isolated bird populations often have a male‐skewed adult sex ratio, so that male lifetime productivity depends to a large degree on pairing success, but few studies have focused on patterns of lifetime pairing success. The Norwegian population of Ortolan Buntings Emberiza hortulana is strongly male‐skewed, such that in any year about half of all males are unpaired. Pairing success of first‐year males (16–44%) was significantly lower than for older males (52–89%). Lifetime pairing success was correlated with lifespan and was strongly skewed, with a majority of males being paired only once or never, and only 11% paired three or more times despite a stable lifetime annual survival rate of 63%. Males that were paired in one year were more likely to be paired the next year than males that were unpaired in the previous year. The shortage of females caused even the older males to have a substantial probability of becoming unpaired, and 49% of long‐lived males (known as adults for at least 4 years) were unpaired after years in which they were paired. Pairing success in the Ortolan Bunting therefore follows similar age‐related and lifetime patterns in breeding success documented in other species. However, even the older males ran a high risk of not being paired, contrasting with earlier distinctions between pre‐breeding and breeding lifespans. I discuss the importance of knowledge of pairing success for the management of endangered and declining populations.     

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     

Operant conditioning of small birds for acoustic discrimination

Standard operant conditioning techniques have been successfully applied to the problem of call discrimination in small birds. Budgerigars (Melopsittacus undulatus) and canaries (Serinus canarius) were trained with a GO/NOGO procedure using positive reinforcement to discriminate between both conspecific contact calls and contact calls of the other species. Budgerigars showed equal facility at each task. By contrast, canaries learned the task involving conspecific contact calls but failed, as a group, to discriminate between budgerigar contact calls. These results show that conditioning techniques can be used to study perceptual learning of species typical calls in small birds.     

Vocal cooperation between the sexes in Little Spotted Kiwi Apteryx owenii

Sexual call dimorphism in birds is usually associated with sexual size dimorphism. Departures from this relationship can be used to infer call function, but research into inter‐sexual call differences, as with song function in general, has been restricted by a bias towards male passerines. The nocturnal and flightless New Zealand kiwi (Apterygidae) are acoustically similar but taxonomically and ecologically very different from other birds, so provide a contrast in exploring avian call function and evolution. However, kiwi acoustic ecology is poorly understood, with the calls of only one of the five kiwi species spectrally described, and acoustic differences between the sexes virtually unknown. We conducted the first bioacoustic study of Little Spotted Kiwi Apteryx owenii, and assessed sexual call dimorphism in this species. There were significant inter‐sexual differences in call temporal and frequency characteristics that were not related to size dimorphism. Contribution to duets and variation in temporal structure with call context also differed between the sexes. We suggest that these differences indicate divergent call function, with male calls more suited for territory defence, and female calls for pair contact. There was a striking lack of overlap in the frequency spectrum distributions of male and female calls, which was also unrelated to size and was further emphasized by the presence of formants in female calls. We propose that this provides evidence for inter‐sexual acoustic cooperation in call frequency, of a type which to our knowledge has not previously been described in birds. This may result from selection for enhanced joint resource defence in kiwi.     

Individuality,kin similarity and experimental playback of contact calls in cooperatively breeding riflemen

Riflemen/tītipounamu (Acanthisitta chloris) are kin-based cooperatively breeding birds, which appear able to recognise their relatives. Here, we investigate the potential for vocalisations to act as recognition cues in riflemen. We identified an appropriate contact call and recorded it at the nest from 19 adult riflemen. Measurements of call characteristics were individually repeatable. In addition, call similarity was significantly correlated with relatedness among all birds and among males. Thus, in principle, these contact calls contain sufficient information for individual recognition of familiar kin, and some assessment of relatedness between unfamiliar birds. To test whether riflemen responded differently to calls of kin, we broadcast calls of relatives and non-relatives as separate treatments in a playback experiment. Focal birds rarely responded aggressively or affiliatively, and their tendency to do so was unrelated to treatment. We conclude that zip calls are suitable kin recognition cues, but whether they are used as such remains unknown.     

First pairing in Snow Geese Anser caerulescens: at what age and at what time of year does it occur?

In migratory birds, the place and time of pair formation are important parameters for population structure and dynamics. Geese are not only migratory but also exhibit long-term monogamy, and therefore the first pairing event in a bird's lifetime is of particular importance. Through behavioural observations of young, known-age, marked birds conducted on the wintering grounds during three winter seasons we investigated two aspects of the timing of first pair formation in the Wrangel Island population of Snow Geese Anser caerulescens : (1) the age at which birds first form pair bonds, and (2) the seasonal pattern of first pair formation. Wrangel Island Snow Geese paired considerably later in life than Snow Geese from a low-Arctic population: almost none of the birds formed pairs in their second winter, and many were still in sibling groups for at least part of that season. The proportion of birds in pairs continued to increase until at least 5 years of age. Most pairing took place during the observation periods, and in general the proportion of birds in pair bonds increased gradually throughout the winter season. The amount of pairing during spring migration or summer varied annually and among cohorts, indicating that even very young birds may be able to form pair bonds quickly if conditions on the breeding grounds are unusually favourable. Pairing later and remaining in family groups longer may be a response to breeding conditions in this high-Arctic colony. Here, productivity is typically low due to harsh weather and predation, whereas Snow Geese breeding in the low Arctic are less restricted and form pairs and start to breed when younger. The fact that most, but not all, pairing takes place on the wintering grounds helps explain why a previous study found a certain amount of gene flow between the two Wrangel Island subpopulations with separate wintering grounds.     

Sex-specific responses to vocal convergence and divergence of contact calls in orange-fronted conures (Aratinga canicularis)

We investigated the signal function of vocal imitation of contact calls in orange-fronted conures (OFCs; Aratinga canicularis) in Costa Rica. OFCs live in dynamic social systems with frequent flock fusions and fissions. Exchanges of contact calls precede these flock changes. During call exchanges, the similarity between the contact calls of different individuals may either increase (converge) or decrease (diverge). We conducted a playback experiment on wild-caught captive birds in which we simulated convergent, divergent and no-change interaction series with male and female contact calls. OFCs responded differently to convergent and divergent series of contact calls, but only when we considered the sex of the test birds. Males called most in response to convergent series, whereas females demonstrated high calling rates in response to both convergent and divergent interactions. Both sexes responded most to contact calls from the opposite sex, but overall females produced more calls and had shorter latencies to calling than males. These results demonstrate that OFCs can discriminate between male and female contact calls and that subtle changes in contact call structure during interactions have signal function. The stronger overall response to convergent series suggests that convergence of contact calls is an affiliative signal.     

Social influences on foraging behaviour of the Red-cheeked Cordon Bleu Uraeginthus bengalus Estrildidae

Red-cheeked Cordon Bleus U. bengalus forage on bare patches of ground for fallen grass seeds and termites in particular home ranges. Foraging is confined to shaded areas in the middle parts of the day but birds exploit places exposed to the full sun in the early mornings and late afternoons. They mostly occur in pairs but often aggregate to form temporary foraging groups. Although birds in groups spend less time vigilant than those foraging alone, they react sooner than them to approaching danger. Birds foraging in pairs peck more rapidly than those in other situations and it is suggested that one advantage of forming permanent pair bonds is that paired birds forage more efficiently than unpaired ones in preparation for the coming breeding season. Flight calls, contact calls and alarm calls are given in specific behavioural contexts. Birds make contact calls when they become separated from their mates and evidently use them to re-locate one another. It is shown experimentally that members of pairs can recognize one another's contact calls.     

Abundance,territory sizes,and pairing success of male Henslow's Sparrows in restored warm‐ and cool‐season grasslands

Henslow's Sparrows (Ammodramus henslowii) are known to breed in restored grasslands consisting of either warm‐ or cool‐season grasses, but additional information is needed concerning their breeding biology in these two types of grasslands. We compared the abundance, territory sizes, and pairing success of male Henslow's Sparrows in grasslands in west‐central Missouri in 2010 and 2011 using a paired‐treatment design, where warm‐ and cool‐season grasslands were located in close proximity. Selection indices indicated no apparent preference by male Henslow's Sparrows for either type of grassland, and the territory sizes and pairing success of males in cool‐ and warm‐season grasslands did not differ. In addition, we found no significant differences in habitat structure between these grassland types. Thus, our results suggest that the warm‐ and cool‐season grasslands in our study provided suitable habitat for Henslow's Sparrows. Other investigators have drawn similar conclusions for Henslow's Sparrows and for grassland birds in general, with the structural characteristics and, for some species, the size of grasslands being more important for grassland birds than plant species composition.     

Males’ calls carry information about individual identity and morphological characteristics of the caller in burrowing petrels

Acoustic communication in burrowing petrels has been poorly studied. However, as for many other bird species, acoustic communication seems to play an essential role in social interactions during the breeding season of these seabirds. Bachelor males call from their burrow, likely to attract females, but also when vocally challenged by other males. Calling in the breeding colony exposes petrels to high predation risks and thus it should provide an important benefit. The present study focuses on the informative content of males’ calls in the blue petrel Halobaena caerulea and the Antarctic prion Pachyptila desolata, two monogamous petrel species producing a single egg per year. We tested the hypotheses that acoustic parameters of a male's calls 1) reflect phenotypic characteristics, and 2) bear an individual vocal signature. To do so, we first tested on both species the relationships between seven morphometric measurements and 11 acoustic parameters using multivariate analyses. Second, we performed a between‐class analysis and calculated the potential of individuality coding (i.e. the ratio between intra‐ and inter‐individual variabilities) for acoustic parameters in both spectral and temporal domains. Results show acoustic parameters (especially energy quartiles, call duration, and syllable or phrase rate) reflect the caller's body size, bill morphology and wing morphology in both species. Considering the seeming pertinence of wing morphology, we suggest wing area may be a more relevant trait to consider than wing length when studying soaring birds. The results support the idea that energy quartiles, phrase rate and call duration also code for individual identity. Information carried by males’ calls might play a role in social interactions, such as burrow defence (e.g. male‐male competition, neighbour‐stranger discrimination) and/or female mate choice.     

Increased extra‐pair paternity in broods of aging males and enhanced recruitment of extra‐pair young in a migratory bird

Despite keen interest in extra‐pair mating in birds, its adaptive significance remains unresolved. Here, we use a multi‐year dataset to test whether traits of a female's social mate influence her propensity to produce extra‐pair offspring in a population of house wrens, and whether producing extra‐pair young has consequences for a female's fitness through effects on offspring survival. Females were most likely to produce extra‐pair offspring when paired with old males and when paired with males on poor‐quality territories, although this latter effect was marginally nonsignificant. Among offspring, the cutaneous immunity of within‐pair young decreased as the age of their sires increased, but cutaneous immunity of extra‐pair young was not affected by the age of their extra‐pair sires or by the age of the males rearing them. Extra‐pair offspring were more likely than within‐pair offspring to return as breeding adults to the local population, with extra‐pair sons being more likely to return as a breeder for multiple years. Our findings support the hypothesis that females produce extra‐pair offspring to enhance their inclusive fitness beyond what they are capable of given the male with which they are socially paired.     

Female Attraction to Higher Pitched Male Enticement Calls in Barn Swallows

Current sexual selection studies demonstrate that female mate preference almost always favors exaggerated male traits, such as colorful plumage and elongated tails. However, such studies focused mainly on secondary sexual characteristics, i.e., traits that are fully developed at maturation, while ignoring others, which precludes generalization of the findings. We studied the expression of the male enticement call, a nestling‐like courtship trait, in relation to female attraction and to the expression of secondary sexual ornaments in the Japanese barn swallow Hirundo rustica gutturalis. First, we showed that the peak amplitude frequency of male enticement calls was, on average, lower than that of nestling food‐begging calls, indicating that higher pitched calls are more similar to nestling food‐begging calls than are lower pitched calls. Second, we conducted an experimental playback of male enticement calls during the courtship period with the female's mate removed, and found that females were more attracted to heightened‐pitch calls than to control calls. Lastly, the peak amplitude frequency of male enticement calls was negatively related to the ornamentation, as measured by throat coloration. Taken together, these findings suggest the following: (1) females are attracted to a more nestling‐like trait, and (2) similarity to nestling food‐begging calls increases with decreasing secondary sexual ornaments. Nestling‐like male traits that are not secondary sexual characteristics should be considered when studying the general pattern of female attraction to male traits.     

Context and sex differences exist in the acoustic structure of phee calls by newly–paired common marmosets (Callithrix jacchus)

Captive common marmosets of all ages robustly produce a “separation” phee call during brief separations from their group. In contrast, a second structural variant, which may function as an intergroup call, is produced in the home cage primarily by the reproductive adults. A previous study found that postpubertal but nonreproductive offspring rarely produce phee calls when in the home cage with the natal group, yet these marmosets call frequently after pairing with an opposite‐sex partner. The sudden increase in home cage phee calls may indicate the rapid onset of intergroup calling. Alternatively, marmosets may be producing the separation phee variant as a result of separation from the natal group. The present study investigated whether phee calls produced by recently paired individuals in the home cage were structurally distinguishable from their calls recorded in a separation paradigm. We also tested whether sex differences, known to exist in the calls of mature adults, could be found in calls recorded from younger, nonreproductive animals separated from their natal groups. We analyzed 18 acoustic parameters of phee calls produced in the home cage after pairing and of calls produced during separation both from the natal group and from a new mate. Discriminant function analyses found that home cage calls were clearly discriminable from separation calls (average 91.7% correctly classified), indicating that the rapid increase in home cage phee call production shortly after pairing is not a consequence of separation from the family group. Postpubertal marmosets appear to show a rapid behavioral adjustment to separation from their natal groups. Additionally, sex was clearly discriminable in calls recorded both before and after pairing (average 86.8% correctly classified). Like calls recorded from well‐established paired marmosets, phee calls produced by recently paired, postpubertal marmosets are discriminable by context and sex. Am. J. Primatol. 49:165–181, 1999. Published 1999 Wiley‐Liss, Inc.