Song acquisition and control in the chaffinch 'Fringilla coelebs' : the organisation of a behavioural repertoire

Bird song provides us with one of the best models with which to investigate learning, communication and the organisation of behavioural repertoires. This study describes temporal organisation and song pattern choice in the chaffinch in order to develop hypotheses for possible song control mechanisms. Influences of the song learning process and motivation on performance are tested in experiments. The role of nature and nurture in shaping females' song preferences is investigated by using operant tasks. A first quantitative assessment of temporal organisation within songs is provided in Chapter 2. Chaffinches sing with eventual variety, each song type in a male's repertoire is repeated a few times before a switch to the next type occurs. Chapter 3 tests two hypotheses for mechanisms controlling song type switching: that a maximum number of repetitions or that a maximum duration (time window) sets the upper limit. Clear evidence for a time window as an upper constraint was found in wild birds as song type bouts with many repetitions were sung at fast rates only, whereas those with few repetitions could be sung at either fast or slow rates. However, the mean number of song type repetitions depended strongly both on the subject and the song type. No evidence could be found that number of repetitions per song type were influenced by the tutor's singing style in hand-reared chaffinches (Chapter 4). Playbacks of single songs to wild males revealed the motivation dependent flexibility of the system as the birds reacted with distinct increases in bout duration (Chapter 5) but showed a different response to playbacks of songs that were the same or different from that being performed by the subject. Song was used as a positive reinforcer in an operant conditioning task with female chaffinches (Chapter 6). The influence of early exposure to song on later preferences and the relative importance of the trill and flourish sections of the song were tested this way. Females showed no preference for familiar over unfamiliar songs, but preferred songs with flourishes over those without

An Experimental Test of Condition-Dependent Male and Female Mate Choice in Zebra Finches

In mating systems with social monogamy and obligatory bi-parental care, such as found in many songbird species, male and female fitness depends on the combined parental investment. Hence, both sexes should gain from choosing mates in high rather than low condition. However, theory also predicts that an individual's phenotypic quality can constrain choice, if low condition individuals cannot afford prolonged search efforts and/or face higher risk of rejection. In systems with mutual mate choice, the interaction between male and female condition should thus be a better predictor of choice than either factor in isolation. To address this prediction experimentally, we manipulated male and female condition and subsequently tested male and female mating preferences in zebra finches Taeniopygia guttata, a songbird species with mutual mate choice and obligatory bi-parental care. We experimentally altered phenotypic quality by manipulating the brood size in which the birds were reared. Patterns of association for high- or low-condition individuals of the opposite sex differed for male and female focal birds when tested in an 8-way choice arena. Females showed repeatable condition-assortative preferences for males matching their own rearing background. Male preferences were also repeatable, but not predicted by their own or females' rearing background. In combination with a brief review of the literature on condition-dependent mate choice in the zebra finch we discuss whether the observed sex differences and between-studies differences arise because males and females differ in context sensitivity (e.g. male-male competition suppressing male mating preferences), sampling strategies or susceptibility to rearing conditions (e.g. sex-specific effect on physiology). While a picture emerges that juvenile and current state indeed affect preferences, the development and context-dependency of mutual state-dependent mate choice warrants further study

Effects of Cortical FoxP1 Knockdowns on Learned Song Preference in Female Zebra Finches

The search for molecular underpinnings of human vocal communication has focused on genes encoding forkhead-box transcription factors, as rare disruptions of FOXP1, FOXP2, and FOXP4 have been linked to disorders involving speech and language deficits. In male songbirds, an animal model for vocal learning, experimentally altered expression levels of these transcription factors impair song production learning. The relative contributions of auditory processing, motor function or auditory-motor integration to the deficits observed after different FoxP manipulations in songbirds are unknown. To examine the potential effects on auditory learning and development, we focused on female zebra finches (Taeniopygia guttata) that do not sing but develop song memories, which can be assayed in operant preference tests. We tested whether the relatively high levels of FoxP1 expression in forebrain areas implicated in female song preference learning are crucial for the development and/or maintenance of this behavior. Juvenile and adult female zebra finches received FoxP1 knockdowns targeted to HVC (proper name) or to the caudomedial mesopallium (CMM). Irrespective of target site and whether the knockdown took place before (juveniles) or after (adults) the sensitive phase for song memorization, all groups preferred their tutor’s song. However, adult females with FoxP1 knockdowns targeted at HVC showed weaker motivation to hear song and weaker song preferences than sham-treated controls, while no such differences were observed after knockdowns in CMM or in juveniles. In summary, FoxP1 knockdowns in the cortical song nucleus HVC were not associated with impaired tutor song memory but reduced motivation to actively request tutor songs

Personality assortative female mating preferences in a songbird

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Toward Testing for Multimodal Perception of Mating Signals

Many mating signals consist of multimodal components that need decoding by several sensory modalities on the receiver's side. For methodological and conceptual reasons, the communicative functions of these signals are often investigated only one at a time. Likewise, variation of single signal traits are frequently correlated by researchers with senders' quality or receivers' behavioral responses. Consequently, the two classic and still dominating hypotheses regarding the communicative meaning of multimodal mating signals postulate that different components either serve as back-up messages or provide multiple meanings. Here we discuss how this conceptual dichotomy might have hampered a more integrative, perception encompassing understanding of multimodal communication: neither the multiple message nor the back-up signal hypotheses address the possibility that multimodal signals are integrated neurally into one percept. Therefore, when studying multimodal mating signals, we should be aware that they can give rise to multimodal percepts. This means that receivers can gain access to additional information inherent in combined signal components only (“the whole is something different than the sum of its parts”). We review the evidence for the importance of multimodal percepts and outline potential avenues for discovery of multimodal percepts in animal communication

RoboFinch: A versatile audio-visual synchronised robotic bird model for laboratory and field research on songbirds

1. Singing in birds is accompanied by beak, head and throat movements. The role of these visual cues has long been hypothesised to be an important facilitator in vocal communication, including social interactions and song acquisition, but has seen little experimental study. 2. To address whether audio-visual cues are relevant for birdsong we used high-speed video recording, 3D scanning, 3D printing technology and colour-realistic painting to create RoboFinch, an open source adult-mimicking robot which matches temporal and chromatic properties of songbird vision. We exposed several groups of juvenile zebra finches during their song developmental phase to one of six singing robots that moved their beaks synchronised to their song and compared them with birds in a non-synchronised and two control treatments. 3. Juveniles in the synchronised treatment approached the robot setup from the start of the experiment and progressively increased the time they spent singing, contra to the other treatment groups. Interestingly, birds in the synchronised group seemed to actively listen during tutor song playback, as they sung less during the actual song playback compared to the birds in the asynchronous and audio-only control treatments. 4. Our open source RoboFinch setup thus provides an unprecedented tool for systematic study of the functionality and integration of audio-visual cues associated with song behaviour. Realistic head and beak movements aligned to specific song elements may allow future studies to assess the importance of multisensory cues during song development, sexual signalling and social behaviour. All software and assembly instructions are open source, and the robot can be easily adapted to other species. Experimental manipulations of stimulus combinations and synchronisation can further elucidate how audio-visual cues are integrated by receivers and how they may enhance signal detection, recognition, learning and memory

Adding colour-realistic video images to audio playbacks increases stimulus engagement but does not enhance vocal learning in zebra finches

Bird song and human speech are learned early in life and for both cases engagement with live social tutors generally leads to better learning outcomes than passive audio-only exposure. Real-world tutor–tutee relations are normally not uni- but multimodal and observations suggest that visual cues related to sound production might enhance vocal learning. We tested this hypothesis by pairing appropriate, colour-realistic, high frame-rate videos of a singing adult male zebra finch tutor with song playbacks and presenting these stimuli to juvenile zebra finches (Taeniopygia guttata). Juveniles exposed to song playbacks combined with video presentation of a singing bird approached the stimulus more often and spent more time close to it than juveniles exposed to audio playback only or audio playback combined with pixelated and time-reversed videos. However, higher engagement with the realistic audio–visual stimuli was not predictive of better song learning. Thus, although multimodality increased stimulus engagement and biologically relevant video content was more salient than colour and movement equivalent videos, the higher engagement with the realistic audio–visual stimuli did not lead to enhanced vocal learning. Whether the lack of three-dimensionality of a video tutor and/or the lack of meaningful social interaction make them less suitable for facilitating song learning than audio–visual exposure to a live tutor remains to be tested

Understanding Sex Differences in Form and Function of Bird Song: The Importance of Studying Song Learning Processes

Birdsong is a culturally transmitted mating signal. Due to historical and geographical biases, song (learning) has been predominantly studied in the temperate zones, where female song is rare. Consequently, mechanisms and function of song learning have been almost exclusively studied in male birds and under the premise that inter- and intrasexual selection favoured larger repertoires and complex songs in males. However, female song is not rare outside the temperate zones and song in both sexes probably is the ancestral state in songbirds. Some song dimorphisms seen today might therefore be manifestations of secondary losses of female song. What selection pressures have favoured such losses and other sexual dimorphisms in song? Combined mapping of phylogenetic and ecological correlates of sex differences in song structure and function might provide important clues to the evolution of male and female song. This requires parameterization of the degree of sexual dimorphism. Simple comparison of male-female song might not provide enough resolution, because the same magnitude of difference (e.g. repertoire overlap) could result from different processes: the sexes could differ in how well they learn (‘copying fidelity’) or from whom they learn (‘model selection’). Different learning mechanisms might provide important pointers towards different selection pressures. Investigating sex-specific learning could therefore help to identify the social and ecological selection pressures contributing to sex differences in adult song. The study of female song learning in particular could be crucial to our understanding of i) song function in males and females and ii) the evolution of sex-specific song

Social facilitation of male song by male and female conspecifics in the zebra finch, Taeniopygia guttata

Zebra finches are an ubiquitous model system for the study of vocal learning in animal communication. Their song has been well described, but its possible function(s) in social communication are only partly understood. The so-called ‘directed song’ is a high-intensity, high-performance song given during courtship in close proximity to the female, which is known to mediate mate choice and mating. However, this singing mode constitutes only a fraction of zebra finch males’ prolific song output. Potential communicative functions of their second, ‘undirected’ singing mode remain unresolved in the face of contradicting reports of both facilitating and inhibiting effects of social company on singing. We addressed this issue by experimentally manipulating social contexts in a within-subject design, comparing a solo versus male or female only company condition, each lasting for 24 hours. Males’ total song output was significantly higher when a conspecific was in audible and visible distance than when they were alone. Male and female company had an equally facilitating effect on song output. Our findings thus indicate that singing motivation is facilitated rather than inhibited by social company, suggesting that singing in zebra finches might function both in inter- and intrasexual communication