Acoustic pattern variations in the female-directed birdsongs of a colony of laboratory-bred zebra finches

The acoustic profile of the zebra finch song is characterized by a series of identical repeating units, each comprising a distinctive sequence of acoustic elements, called syllables. Here, we perform an analysis of song pattern deviations caused by variabilities in the production of song syllables. Zebra finches produce four different kinds of syllable variabilities-syllable deletions, single or double syllable insertions, syllable alterations, and syllable repetitions. All these variabilities, with the exception of repetitions, are present in songs of more than two-thirds of the normal adult birds; repetitions are present in less than one-fifth of birds. The frequency of occurrence of these variabilities is independent of the amount of singing, suggesting that they are unlikely to result simply from singing-induced physiological changes such as fatigue. Their frequencies in tutor-deprived birds are not significantly different from those in normal birds, indicating that they are unlikely to be acquired due to deficiencies in tutor-dependent learning. The types, patterns of occurrence and relative frequencies of these song syllable variabilities might reveal insights into the functioning of the song motor control pathway.     

Respiratory units of motor production and song imitation in the zebra finch

Juvenile male zebra finches (Taeniopygia guttata) learn a stereotyped song by imitating sounds from adult male tutors. Their song is composed of a series of syllables, which are separated by silent periods. How acoustic units of song are translated into respiratory and syringeal motor gestures during the song learning process is not well understood. To learn about the respiratory contribution to the imitation process, we recorded air sac pressure in 38 male zebra finches and compared the acoustic structures and air sac pressure patterns of similar syllables qualitatively and quantitatively. Acoustic syllables correspond to expiratory pressure pulses and most often (74%) entire syllables are copied using similar air sac pressure patterns. Even notes placed within different syllables are generated with similar air sac pressure patterns when only segments of syllables are copied (9%). A few of the similar syllables (17%) are generated with a modified pressure pattern, typically involving addition or deletion of an inspiration. The high similarity of pressure patterns for like syllables indicates that generation of particular sounds is constrained to a narrow range of air sac pressure conditions. Following presentation of stroboscope flashes, song was typically interrupted at the end of an expiratory pressure pulse, confirming that expirations and, therefore, syllables are the smallest unit of motor production of song. Silent periods, which separate syllables acoustically, are generated by switching from expiration to inspiration. Switching between respiratory phases, therefore, appears to play a dominant role in organizing the stereotyped motor program for song production.     

Individual Signature in Canary Songs: Contribution of Multiple Levels of Song Structure

Through variations in features, both within and between individuals, songs of male passerines provide information on the identity of the singer. In domesticated canaries (Serinus canaria), these variations remain, for a large part, to be investigated. This led us to question whether individual identity might be coded at one or more hierarchical levels of song organization, i.e. in acoustic parameters, in the syllable repertoire and in the delivery order of syllables. A song as a whole had numerous individual distinctive acoustic features. However, the structure of its individual signature appeared to be complex. A repertoire combined syllables never sung by other individuals with those shared by other birds. But, most of the individual‐specific syllables that accounted for 16% of a repertoire did not recur frequently. Variation in sequences of multiple syllable types appeared to reflect the individual identity of a male canary. Nearly all sequences larger than three syllable types were specific to the individual that produced them. Some of these occurred recurrently in songs and differed in their acoustic structure between individuals. Focusing upon recurrent sequences might allow vocal recognition of an individual without requiring the knowledge of its full repertoire. However, acoustic parameters and repertoire composition might also serve as additional cues to limit confusion between individuals.     

Frequency shift in homologue syllables of the Ortolan Bunting Emberiza hortulana

Results of this study indicate that in the Ortolan Bunting Emberiza hortulana, syllables of the same shape on sonograms (i.e. homologue syllables) often significantly differ between males in frequency parameters. Typically, homologue syllables of different males in the studied population had a similar bandwidth but shifted minimal and maximal frequencies. We found no strong evidence supporting that the frequency of homologue syllables is affected by the body size variation of males. Besides, frequency parameters of different song types within a male's repertoire did not correlate with each other. Moreover, we found that some males within the population sing two versions of apparently 'the same' song type, which differ in frequency parameters of syllables. Such different frequency versions were sung with eventual variety, which suggests that they are treated as different song types by birds. All these results support the idea that the fine acoustic structure of syllables (and song) is under a strong influence of the acoustic template (i.e. depend mainly on from whom the song was copied). We also found that the frequency of initial syllables within the song strophe is much more variable between males than in case of final syllables. Regardless of the great between-individual variation in initial syllable frequency, the syllables forming the final part of the song are kept within a very restricted bandwidth. These results support our earlier finding that strict syntactic rules of song formation exist in this species. These rules condition the acoustic variation of the initial and final part of the song. At least potentially, such a system enables species recognition and individual variation irrespective of repertoire level. Results of this study indicate that more attention should be paid to the problem of minimal units of song repertoire and to identity of such units within the bird population.     

Manipulations of sensory experiences during development reveal mechanisms underlying vocal learning biases in zebra finches

Biological predispositions in learning can bias and constrain the cultural evolution of social and communicative behaviors (e.g., speech and birdsong), and lead to the emergence of behavioral and cultural “universals.” For example, surveys of laboratory and wild populations of zebra finches (Taeniopygia guttata) document consistent patterning of vocal elements (“syllables”) with respect to their acoustic properties (e.g., duration, mean frequency). Furthermore, such universal patterns are also produced by birds that are experimentally tutored with songs containing randomly sequenced syllables (“tutored birds”). Despite extensive demonstrations of learning biases, much remains to be uncovered about the nature of biological predispositions that bias song learning and production in songbirds. Here, we examined the degree to which “innate” auditory templates and/or biases in vocal motor production contribute to vocal learning biases and production in zebra finches. Such contributions can be revealed by examining acoustic patterns in the songs of birds raised without sensory exposure to song (“untutored birds”) or of birds that are unable to hear from early in development (“early‐deafened birds”). We observed that untutored zebra finches and early‐deafened zebra finches produce songs with positional variation in some acoustic features (e.g., mean frequency) that resemble universal patterns observed in tutored birds. Similar to tutored birds, early‐deafened birds also produced song motifs with alternation in acoustic features across adjacent syllables. That universal acoustic patterns are observed in the songs of both untutored and early‐deafened birds highlights the contribution motor production biases to the emergence of universals in culturally transmitted behaviors.     

Seasonal activation and inactivation of song motor memories in wild canaries is not reflected in neuroanatomical changes of forebrain song areas

Seasonal, testosterone-dependent changes in sexual behaviors are common in male vertebrates. In songbirds such seasonal changes occur in a learned behavior--singing. Domesticated male canaries (Serinus canaria) appear to lose song units (syllables) after the breeding season and learn new ones until the next breeding season. Here we demonstrate in a longitudinal field study of individual, free-living nondomesticated (wild) canaries (S. canaria) a different mode of seasonal behavioral plasticity, seasonal activation, and inactivation of auditory-motor memories. The song repertoire composition of wild canaries changes seasonally: about 25% of the syllables are sung seasonally; the remainder occur year-round, despite seasonal changes in the temporal patterns of song. In the breeding season, males sing an increased number of fast frequency-modulated syllables, which are sexually attractive for females, in correlation with seasonally increased testosterone levels. About 50% of the syllables that were lost after one breeding season reappear in the following breeding season. Furthermore, some identical syllable sequences are reactivated on an annual basis. The seasonal plasticity in vocal behavior occurred despite the gross anatomical and ultrastructural stability of the forebrain song control areas HVc and RA that are involved in syllable motor control.     

Advertising vocalization of the clamorous reed warbler (<Emphasis Type="Italic">Acrocephalus stentoreus</Emphasis>, Sylviidae)

The advertising vocalization of the clamorous reed warbler, one of the least studied representatives of the genus in the Palearctic, has been analyzed. In this species, advertising vocalization consists of compact acoustic constructs (songs) separated by pauses. The duration of songs (median 3.6 s) and pauses (median 2.9 s) varies only slightly. Each song consists of three to four different or identical syllables. Syllables (stereotyped acoustic constructs) consist of two to four notes. Each male has from 5 to 25 syllables in his repertoire. A sharp contrast between low-frequency and high-frequency notes and strict sequence of these notes in syllables (low-frequency notes come first, then follow high-frequency notes) are characteristic of this song. All types of syllables in the song of a given male can be divided into two groups: initiator syllables and other syllables. Initiator syllables most often occur at the beginning, while others occur in the middle or at the end of the song. Stable links between syllables have been revealed: the majority of them occur in the song together with certain syllables (one or two) of other types. The whole range of songs of each individual can be divided into several classes. A certain type of initiator syllable and a certain set of subsequent syllables are characteristic of each class. However, the variability of songs within each class is quite high. Modes of immediate and eventual variety alternate in the sequence of songs from different classes. Thus, 47.4% of songs are followed by a song from the same class (eventual variety), while 52.6% of songs are followed by a song from a different class (immediate variety). The advertising vocalization of the clamorous reed warbler is compared with that of other representatives of the genus Acrocephalus.     

Are Unfamiliar Neighbours Considered to Be Dear-Enemies?

Background

Discriminating threatening individuals from non-threatening ones allow territory owners to modulate their territorial responses according to the threat posed by each intruder. This ability reduces costs associated with territorial defence. Reduced aggression towards familiar adjacent neighbours, termed the dear-enemy effect, has been shown in numerous species. An important question that has never been investigated is whether territory owners perceive distant neighbours established in the same group as strangers because of their unfamiliarity, or as dear-enemies because of their group membership.

Methodology/Principal Findings

To investigate this question, we played back to male skylarks (Alauda arvensis) songs of adjacent neighbours, distant neighbours established a few territories away in the same microdialect area and strangers. Additionally, we carried out a propagation experiment to investigate how far skylark songs are propagated in their natural habitat and we estimated repertoire similarity between adjacent neighbours, distant neighbours and strangers. We show that skylarks, in the field, respond less aggressively to songs of their distant and likely unfamiliar neighbours, as shown by the propagation experiment, compared to stranger songs. The song analysis revealed that individuals share a high amount of syllables and sequences with both their adjacent and distant neighbours, but only few syllables and no sequences with strangers.

Conclusions

The observed reduction of aggression between distant neighbours thus probably results from their familiarity with the vocal group signature shared by all members of the neighbourhood. Therefore, in skylarks, dear-enemy-like relationships can be established between unfamiliar individuals who share a common acoustic code.     

Disconnection of a basal ganglia circuit in juvenile songbirds attenuates the spectral differentiation of song syllables

Similar to language acquisition by human infants, juvenile male zebra finches (Taeniopygia guttata) imitate an adult (tutor) song by transitioning from repetitive production of one or two undifferentiated protosyllables to the sequential production of a larger and spectrally heterogeneous set of syllables. The primary motor region that controls learned song is driven by a confluence of input from two premotor pathways: a posterior pathway that encodes the adult song syllables and an anterior pathway that includes a basal ganglia (BG)‐thalamo‐cortical circuit. Similar to mammalian motor‐learning systems, the songbird BG circuit is thought to be necessary for shaping juvenile vocal behaviour (undifferentiated protosyllables) toward specific targets (the tutor's song syllables). Here, we tested the hypothesis that anterior pathway activity contributes to the process of protosyllable differentiation. Bilateral ablation of lateral magnocellular nucleus of the anterior nidopallium (LMAN) was used to disconnect BG circuitry at ages before protosyllable production and differentiation. Comparison to surgical controls revealed that protosyllables fail to differentiate in birds that received juvenile LMAN ablation—the adult songs of birds with >80% bilateral LMAN ablation consisted of only one or two syllables produced with the repetitive form and spectral structure that characterizes undifferentiated protosyllables in normal juveniles. Our findings support a role for BG circuitry in shaping juvenile vocal behaviour toward the acoustic structure of the tutor song and suggest that posterior pathway function remains in an immature “default” state when developmental interaction with the anterior pathway is reduced or eliminated. © 2013 Wiley Periodicals, Inc. Develop Neurobiol 74: 574–590, 2014     

The Influence of Song Mode on Responses of Male American Redstarts

Male American redstarts (Setophaga ruticilla) exhibit two modes of singing: repeat and serial mode. Repeat mode consists of repetitions of a single song type, usually one possessing an accented terminal note. Serial mode is constituted by a series of different songs with unaccented terminal notes, sung in a versatile sequence. Different authors have observed that males discriminate between these two modes. In the experiments reported in this paper, we tested whether males use accented terminal notes, song versatility or both to discriminate between the two song modes. We observed that males responded more intensively to the accented song. The accented note seems a very important song characteristic for evoking male American redstart responses. In contrast, males did not show any difference in their response to single and varied serial songs.     

Temporal pattern changes in the calling song of the katydidMygalopsis marki Bailey in response to conspecific song (Orthoptera: Tettigoniidae)

Males of Mygalopsis markiBailey (Tettigoniidae: Orthoptera) alter the temporal structure of their song in response to other competing males. The song of males calling in aggregations has a high variance in the number of syllables per chirp, with short intervals between each chirp. In contrast, the temporal pattern of the song of isolated males is more evenly spaced, with an increase in length of the interchirp intervals and low variance in the number of syllables per chirp. In order to simulate a calling male moving closer to a male in an aggregation, a playback technique was adopted whereby the recorded calling song of a male was presented to itself via a loudspeaker in increments of 2dB. The change in song pattern of the resident male involved a reduction in the number of syllables per chirp and an increase in the interchirp interval, with the number of chirps per second remaining constant. This reduction in the output of the song, instead of not calling as a result of an acoustic contest, may still allow males to continue calling for females.     

Functional organization of forebrain pathways for song production and perception

This article reviews the organization of the forebrain nuclei of the avian song system. Particular emphasis is placed on recent physiologic recordings from awake behaving adult birds while they sing, call, and listen to broadcasts of acoustic stimuli. The neurons in the descending motor pathway (HVc and RA) are organized in a hierarchical arrangement of temporal units of song production, with HVc neurons representing syllables and RA neurons representing notes. The nuclei Uva and NIf, which are afferent to HVc, may help organize syllables into larger units of vocalization. HVc and RA are also active during production of all calls. The patterns of activity associated with calls differ between learned calls and those that are innately specified, and give insight into the interactions between the forebrain and midbrain during calling, as well as into the evolutionary origins of the song system. Neurons in Area X, the first part of the anterior forebrain pathway leading from HVc to RA, are also active during singing. Many HVc neurons are also auditory, exhibiting selectivity for learned acoustic parameters of the individual bird's own song (BOS). Similar auditory responses are also observed in RA and Area X in anesthetized birds. In contrast to HVc, however, auditory responses in RA are very weak or absent in awake birds under our experimental paradigm, but are uncovered when birds are anesthetized. Thus, the roles of both pathways beyond HVc in adult birds is under review. In particular, theories hypothesizing a role for the descending motor pathway (RA and below) in adult song perception do not appear to obtain. The data also suggest that the anterior forebrain pathway has a greater motor role than previously considered. We suggest that a major role of the anterior forebrain pathway is to resolve the timing mismatch between motor program readout and sensory feedback, thereby facilitating motor programming during birdsong learning. Pathways afferent to HVc may participate more in sensory acquisition and sensorimotor learning during song development than is commonly assumed. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 671–693, 1997     

VOCAL ONTOGENY OF NESTLING AND FLEDGLING BLACK-CAPPED CHICKADEES POECILE ATRICAPILLA IN NATURAL POPULATIONS

ABSTRACT

We studied the vocal ontogeny of black-capped chickadees Poecile atricapilla from hatching through approximately age 40 days, at which time the juveniles dispersed from their hatching area. Development of three vocalisations (chick-a-dee call, fee-bee song, gargle call) was monitored by tape recording daily. Spectrographs quantification and comparison were carried out with Sound Analysis software. Developmental changes in offspring vocalisations were compared to the parent birds, allowing a measure of acoustic similarity between adults and young throughout early life. The chick-a-dee call developed all four of its component syllables (ABCD) from a single sound of day-old nestlings, but the four syllables emerged in adult form at different times in ontogeny. The fee-bee song was produced in impressively adult form starting at about age 20 days, with no precursor sounds to indicate gradual emergence. The principal difference between adult and juvenile fee-bee songs was the persistent production of three or four notes by juveniles rather than the adults' species-typical two notes. Gargle calls appear to develop from “subsong” strings of precursor gargle syllables. Juvenile gargles began to be identifiable at about age 33–35 days but did not match any of the gargle calls of the local adult population. Post-dispersal juveniles may develop gargles that match the gargle types of local birds where they settle.     

Species Recognition by Song in the Veery (Catharus fuscescens: Aves)

Territorial male veeries (Catharus fuscescens) were presented with three series of reorganised songs to determine the functional properties of song structure. Songs consist of three parts: a low frequency initial phrase, a higher frequency middle phrase, and again a lower frequency end phrase. The latter two consist of vibrato syllables. Three series of experiments were performed, using various combinations of song syllables. In Series I, songs consisted of repetitions of a single syllable, one from each part of the song. Veeries responded to syllables from the middle and end phrases as to normal songs, both in localisation and in vocal responses. However, they showed little localisation and vocalisation responses to the introductory syllables. In Series II and III, veeries responded significantly more to songs in which syllables from the middle and end phrases were presented in proper sequence, rather than not. The minimum requirements for intraspecific recognition were determined in relation to the number and order of syllables in the song.     

Soft Song in Song Sparrows: Acoustic Structure and Implications for Signal Function

In many species of songbirds, males sometimes produce songs at distinctly lower amplitude than in normal singing. Depending on the species, these 'soft songs' may be sung in the context of female courtship, male–male aggression, or both. In song sparrows, males produce soft songs during aggressive interactions with other males, and the amount of soft song produced is the only singing behavior that can be used to reliably predict a subsequent attack by the singer. Although soft song is clearly an important signal in this species, little is known about the acoustic structure of soft song or about how that structure compares to the structure of normal 'broadcast song'. We recorded a large sample of soft songs and broadcast songs from 10 male song sparrows, and measured song amplitudes in the field while controlling the subject's distance to a calibrated microphone. We show that song sparrow males produce songs over a wide range of amplitudes, with soft songs in the range of 55–77 dB sound pressure level and broadcast songs in the range of 78–85 dB. We present evidence for two types of soft song: 'crystallized' soft songs that are broadcast repertoire song types sung at low amplitude, and 'warbled' soft songs that are not found in the broadcast repertoire. Although highly variable, warbled soft songs produced by individual birds could be grouped into song types based on spectrographic similarity. To our knowledge, a distinct repertoire of soft song types has not been previously reported for any songbird.     

Singing the Popular Songs? Nightingales Share More Song Types with Their Breeding Population in Their Second Season than in Their First

Signals used in communication often change throughout an individual’s life course. For example, in many song bird species, males modify their song especially between their first and second breeding season. To address one possible reason of such modification, we investigated whether common nightingales Luscinia megarhynchos adjust their song type repertoires to sing the song types commonly occurring in their breeding population. We analysed nocturnal singing of six nightingales in their first and second breeding season and compared their repertoire composition and usage to the ‘typical’ repertoire and usage on the breeding ground (represented by seven reference birds). Songs that were maintained between the first and second season by the six focal birds occurred in most of the repertoires of the seven reference birds and were sung often. In contrast, song types that were dropped from the repertoires occurred less often in the reference birds’ repertoires and were sung less often. Furthermore, in the first year, each focal nightingale’s repertoire was less similar to the reference birds’ repertoires than in the second year. Thus, nightingales adjusted their singing towards the songs popular in the breeding grounds by keeping song types that were common and frequently sung by other individuals in their breeding area and by disposing of infrequently performed ones. This resulted in increased similarity with the population’s repertoire from the first to the second year. We discuss possible ontogenetic processes that may lead to such an adjustment and suggest an improved ability to match song types as possible adaptive value.     

Effects of Song Experience and Song Quality on Immediate Early Gene Expression in Female Canaries (Serinus canaria)

Female songbirds are thought to make mate choices based on aspects of male song quality. Male canaries (Serinus canaria) produce songs with “special” syllables that have been shown to be highly salient to female listeners – eliciting high rates of sexual displays and enhanced immediate early gene (IEG) expression. Immunohistochemistry for the IEG ZENK was used to examine the effects of experience with these syllables on activity in the caudal mesopallium (CMM) and nidocaudal mesopallium (NCM), two auditory areas important in processing conspecific song. Photostimulated female canaries were housed in sound attenuated chambers and played pseudosongs containing either three special syllables or three non‐special syllables, an intro, and an outro sequence. Females that heard special syllable pseudosongs exhibited higher ZENK expression in CMM. To assess the effects of experience, photostimulated females were pair housed and exposed to playback of song with or without special syllables for 14 days. After transfer to individual housing, birds were played one of the aforementioned stimuli or silence. ZENK expression in CMM and NCM was equivalent for song with and without special syllables, but significantly lower for silence. Females who experienced song with special syllables had lower plasma estradiol concentrations after final song playback. This study indicates that CMM exhibits an IEG response bias to special syllables in limited acoustic contexts, but not in full song, which may contain additional biologically relevant information. Furthermore, estradiol concentrations may mediate changes in song responses, serving as a mechanism for modulating mate choice in differing song environments.     

Airflow and pressure during canary song: direct evidence for mini-breaths

Summary Male canaries (Serinus canaria) produce songs of long duration compared to the normal respiratory cycle. Each phrase in a song contains repetitions of a particular song syllable, with repetition rates for different syllables ranging from 3 to 35 notes/s. We measured tracheal airflow and air sac pressure in order to investigate respiratory dynamics during song.Song syllables (11–280 ms) are always accompanied by expiratory tracheal airflow. The silent intervals (15–90 ms) between successive syllables are accompanied by inspiration, except for a few phrases where airflow ceases instead of reversing. Thus, the mini-breath respiratory pattern is used most often by the five birds studied and pulsatile expiration is used only occasionally.Songs and phrases accompanied by minibreaths were of longer duration than those accompanied by pulsatile expiration, presumably because the animal's finite vital capacity is not a limiting factor when the volume of air expired for one note is replaced by inspiration prior to the next. Pulsatile expiration was used for only a few syllable types from one bird that were produced at higher repetition rates than syllables accompanied by mini-breaths. We suggest that male canaries switch to pulsatile expiration only when the syllable repetition rate is too high (greater than about 30 Hz) for them to achieve mini-breaths.Changes in syringeal configuration that may accompany song are discussed, based on the assumption that changes in the ratio of subsyringeal (air sac) pressure to tracheal flow rate reflect changes in syringeal resistance.