Clémentine Vignal

Audience drives male songbird response to partner's voice

According to the social intelligence hypothesis, social context represents an important force driving the selection of animal cognitive abilities such as the capacity to estimate the nature of the social relationships between other individuals. Despite this importance, the influence of this force has been assessed only in primates and never in other animals showing social interactions. In this way, avian communication generally takes place in a network of signallers and receivers, which represents an audience altering individual signalling behaviours. Indeed, vocal amplitude and repertoire are known to be socially regulated and the attitude towards the opposite sex may change depending on the audience. This ‘audience effect’ provides support for the reality of social awareness in some bird species. However no evidence has yet been found to suggest that birds are able to estimate the characteristics of the social relationships between group-mates. Here we show that the male of a gregarious songbird species—the zebra finch (Taeniopygia guttata)—pays attention to the mating status of conspecific pairs, and uses this information to control its behaviour towards its female partner.

Mate recognition by female zebra finch: Analysis of individuality in male call and first investigations on female decoding process

Zebra finches are monogamous birds living in large assemblies, which represent a source of confusion for recognition between mates. Because the members of a pair use distance calls to remain in contact, call-based mate recognition is highly probable in this species. Whereas it had been previously demonstrated in males [Vignal, C., Mathevon, N., Mottin, S., 2004. Audience drives male songbird response to mates voice. Nature 430, 448-451], call-based mate recognition remained to be shown in females. By analysing the acoustic structure of male calls, we investigated the existence of an individual signature and identified the involved acoustic cues. We tested to see if females can identify their mates on the basis of their calls alone, and performed preliminary experiments using modified signals to investigate the acoustic basis of this recognition. Playback tests carried on six individuals showed that a female zebra finch is able to perform the call-based recognition of its mate. Our experiments suggested that the female uses both the energy spectrum and the frequency modulation of the male signal. More experiments are now needed to decipher precisely which acoustic cues are used by females for recognition.

Vocal communication at the nest between mates in wild zebra finches: a private vocal duet?

Bird vocal duets are joint displays where two individuals, generally a mated pair, produce temporally coordinated vocalizations. Duets may contribute to pair bond maintenance, mate guarding or collaborative defence of resources. The degree of coordination between mates and the variety of vocalizations, however, vary considerably. Although only 3-4.3% of bird species have been reported to duet, this may be because studies have generally focused on conspicuous duets, and more private forms of duet might have been overlooked. We investigated private vocal communication between mates in wild zebra finches, Taeniopygia guttata, a gregarious Australian songbird that forms life-long pair bonds. The partners are inseparable unless nest building, incubating or brooding. Using microphones inside nestboxes, we monitored interactive communication between partners at the nest and its variation during different stages of breeding. After periods of separation, partners performed coordinated mutual vocal displays involving specific soft vocal elements that fulfilled all the criteria used to define duets. In addition, using playback experiments, we obtained preliminary results suggesting that these soft calls could allow mate recognition. Thus, we propose that mutual displays at the nest in zebra finches represent private vocal duets and may function to mediate pair bond maintenance.

Social context modulates behavioural and brain immediate early gene responses to sound in male songbird

Although it is well known that brain sensory information processing is a highly modulated phenomenon, how this brain function is shaped by experience and social context remains a question to explore. In this paper, we present the first attempt to investigate this problem using a songbird acoustic communication paradigm. Social context is well known to influence acoustic communicating behaviours in birds. The present paper investigates whether brain processing of auditory inputs can be modulated by this ‘audience effect’. Given that call‐based communication is known to be highly context‐dependent, we focused on the response of male zebra finches (Taeniopygia guttata) to female calls. We tested to see if the current social context surrounding the hearing bird can modify a sound‐induced immediate early gene (IEG) activation in the specific region of the caudomedial nidopallium (NCM), a songbird brain analogous to the superficial layers of the mammalian primary auditory cortex. Our results show that the expression of the sound‐induced immediate early gene ZENK in the NCM is considerably enhanced when the hearing bird is in the presence of conspecifics, compared to when he is alone. This context‐dependent increase of a sound‐induced immediate early gene expression can be correlated with the differential behavioural response of males to the playback of the same acoustic stimulus as a function of social context.

Differential responsiveness in brain and behavior to sexually dimorphic long calls in male and female zebra finches.

In zebra finches (Taeniopygia guttata), as in most other songbird species, there are robust sex differences in brain morphology and vocal behavior. First, male zebra finches have larger song system nuclei—involved in sensorimotor learning and production of song—than females. Second, male zebra finches learn their song from a tutor, whereas female zebra finches develop a learned preference for the song of their father but do not sing themselves. Third, female zebra finches produce an unlearned “long call,” while males learn their long call (which is different from that of females) from their song tutor. We investigated behavioral and molecular neuronal responsiveness to this sexually dimorphic communication signal. Behavioral responsiveness was quantified by measuring the number of calls and approaches in response to calls that were broadcast from a speaker. We quantified neuronal activation by measuring the number of neurons expressing Zenk, the protein product of the immediate early gene ZENK, in a number of different forebrain regions in response to male calls, to female calls, or to silence. In both sexes female calls evoked more calls and approaches than male calls. There was significantly greater Zenk expression in response to female calls compared to silence in the caudomedial nidopallium, caudomedial mesopallium, and the hippocampus in females, but not in males. Thus, male and female zebra finches both show a behavioral preference for female calls, but differential neuronal activation in response to sexually dimorphic calls. J. Comp. Neurol. 516:312–320, 2009.

Begging calls support offspring individual identity and recognition by zebra finch parents

In colonial birds, the recognition between parents and their offspring is essential to ensure the exclusivity of parental care. Although individual vocal recognition seems to be a key component of parent-chicks recognition, few studies assessed the period when the emergence of the vocal signature takes place. The present study investigated the acoustic cues of signaler identity carried in the begging calls at three stages of development in zebra finches (Taeniopygia guttata castanotis), a colonial species which experiences food-dependence after fledging. Testing parents with playback of begging calls recorded the day before fledging, we found that the offspring recognition was based on acoustic cues. Begging calls showed a highly individualized vocal signature well before fledging. The individual identity coding was multi-parametric and encoded in both spectral and temporal domains. These results suggest that the successful recognition process of offspring might be strongly dependent on the receivers abilities to use multi-parametric acoustic cues. The precocity of the vocal signature in chicks could enable parents to familiarize with the call features of their offspring at the pre-fledging period through a learning process.

Same-sex pair-bonds are equivalent to male–female bonds in a life-long socially monogamous songbird

Same-sex sexual behaviors are well documented in both captive and wild animals. In monogamous species, these behaviors are often exclusive, each individual having only one same-sex partner. A bias in sex ratio has been proposed as a social context yielding same-sex pair-bonding, but this hypothesis has rarely been tested. Focusing on a life-long pair-bonding songbird, the zebra finch Taeniopygia guttata, we tested whether same-sex pairing results from a shortage of individuals of the opposite sex. By experimentally skewing the sex ratio towards members of one sex, we observed a greater proportion of same-sex pair-bonds of that sex. Moreover, we assessed whether the quality and stability of social interactions were equivalent in same-sex and male–female pairs. Male–male and female–female same-sex bonds display the same behavioral characteristics as male–female ones: they are intense, highly selective, and stable affinitive relationships involving the same behavioral displays already described in wild birds. Moreover, same-sex male bonds were sufficiently strong not to split up when individuals were given the opportunity to reproduce with females. Because the pair-bond in socially monogamous species represents a partnership that may give advantages for survival (e.g., resources defense, fighting against predators, etc.), we propose that same-sex pairing in the zebra finch may result from the pressure to find a social partner.

Dynamics of communal vocalizations in a social songbird, the zebra finch (Taeniopygia guttata)

Colonies or communities of animals such as fishes, frogs, seabirds, or marine mammals can be noisy. Although vocal communication between clearly identified sender(s) and receiver(s) has been well studied, the properties of the noisy sound that results from the acoustic network of a colony of gregarious animals have received less attention. The resulting sound could nonetheless convey some information about the emitting group. Using custom-written software for automatic detection of vocalizations occurring over many hours of recordings, this study reports acoustic features of communal vocal activities in a gregarious species, the zebra finch (Taeniopygia guttata). By biasing the sex ratio and using two different housing conditions (individual versus communal housing), six groups of zebra finches were generated, with six different social structures that varied both in terms of sex-composition and proportion of paired individuals. The results showed that the rate of emission and the acoustic dynamic both depended on the social structure. In particular, the vocal activity of a group of zebra finches depended mainly on the number of unpaired birds, i.e., individuals not part of a stably bonded pair.

Measuring brain hemodynamic changes in a songbird: responses to hypercapnia measured with functional MRI and near-infrared spectroscopy

Songbirds have been evolved into models of choice for the study of the cerebral underpinnings of vocal communication. Nevertheless, there is still a need for in vivo methods allowing the real-time monitoring of brain activity. Functional Magnetic Resonance Imaging (fMRI) has been applied in anesthetized intact songbirds. It relies on blood oxygen level-dependent (BOLD) contrast revealing hemodynamic changes. Non-invasive near-infrared spectroscopy (NIRS) is based on the weak absorption of near-infrared light by biological tissues. Time-resolved femtosecond white laser NIRS is a new probing method using real-time spectral measurements which give access to the local variation of absorbing chromophores such as hemoglobins. In this study, we test the efficiency of our time-resolved NIRS device in monitoring physiological hemodynamic brain responses in a songbird, the zebra finch (Taeniopygia guttata), using a hypercapnia event (7% inhaled CO(2)). The results are compared to those obtained using BOLD fMRI. The NIRS measurements clearly demonstrate that during hypercapnia the blood oxygen saturation level increases (increase in local concentration of oxyhemoglobin, decrease in deoxyhemoglobin concentration and total hemoglobin concentration). Our results provide the first correlation in songbirds of the variations in total hemoglobin and oxygen saturation level obtained from NIRS with local BOLD signal variations.

Juvenile social experience affects pairing success at adulthood: congruence with the loser effect?

Social interactions with adults are often critical for the development of mating behaviours. However, the potential role of other primary social partners such as juvenile counterparts is rarely considered. Most interestingly, it is not known whether interactions with juvenile females improve males’ courtship and whether, similar to the winner and loser effects in a fighting context—outcome of these interactions shapes males’ behaviour in future encounters. We investigated the combined effects of male quality and juvenile social experience on pairing success at adulthood in zebra finches (Taeniopygia guttata). We manipulated brood size to alter male quality and then placed males in either same- or mixed-sex juvenile dyads until adulthood. We found that males from reduced broods obtained more copulations and males from mixed-sex dyads had more complete courtships. Furthermore, independent of their quality, males that failed to pair with juvenile females, but not juvenile males, had a lower pairing success at adulthood. Our study shows that negative social experience with peers during adolescence may be a potent determinant of pairing success that can override the effects of early environmental conditions on male attractiveness and thereby supports the occurrence of an analogous process to the loser effect in a mating context.