Altered auditory BOLD response to conspecific birdsong in zebra finches with stuttered syllables

How well a songbird learns a song appears to depend on the formation of a robust auditory template of its tutor's song. Using functional magnetic resonance neuroimaging we examine auditory responses in two groups of zebra finches that differ in the type of song they sing after being tutored by birds producing stuttering-like syllable repetitions in their songs. We find that birds that learn to produce the stuttered syntax show attenuated blood oxygenation level-dependent (BOLD) responses to tutor's song, and more pronounced responses to conspecific song primarily in the auditory area field L of the avian forebrain, when compared to birds that produce normal song. These findings are consistent with the presence of a sensory song template critical for song learning in auditory areas of the zebra finch forebrain. In addition, they suggest a relationship between an altered response related to familiarity and/or saliency of song stimuli and the production of variant songs with stuttered syllables.     

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.     

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.     

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.     

Contributions of syringeal muscles to respiration and vocalization in the zebra finch

Acute and chronic electromyographic (EMG) recordings from individual syringeal muscles were used to study syringeal participation in respiration and vocalization. In anesthetized birds, all syringeal muscles recorded were active to some degree during the expiratory phase of respiration, following activity in the abdominal musculature and preceding the emergence of breath from the nostril. In awake birds, the ventralis (V) muscle fired a strong, consistent burst, but the dorsalis (D) was variable both in strength and timing. Denervation of V is sufficient to produce the wheezing respiration originally seen in birds with complete bilateral section of the tracheosyringeal nerve. Complete syringeal denervation also removed almost all the acoustic features that distinguish individual song syllables, but had a minor effect on the temporal structure of song. When activity in V and D was recorded in awake, vocalizing birds, D was active before and during sound production, and V showed a small burst before sound onset and a vigorous burst timed to the termination of sound. During song, V was consistently active at sound offset, but also participated during sound for narrow bandwidth syllables. For some syllables (simple harmonic stacks), neither muscle was active. These data suggest that V contributes to syllable termination during vocalization and may silence the syrinx during normal respiration. D contributes to the acoustic structure of most syllables, and V may contribute to a special subset of syllables. In summary, the syringeal muscles show different activity patterns during respiration and vocalization and can be independently activated during vocalization, depending on the syllable produced.     

Motor stereotypy and diversity in songs of mimic thrushes

The relationship between the motor and acoustic similarity of song was examined in brown thrashers (Toxostoma rufum) and grey catbirds (Dumetella carolinensis) (family Mimidae), which have very large song repertoires and sometimes mimic other species. Motor similarity was assessed by cross correlation of syringeal airflows and air sac pressures that accompany sound production. Although most syllables were sung only once in the song analyzed, some were repeated, either immediately forming a couplet, or after a period of intervening song, as a distant repetition. Both couplets and distant repetitions are produced by distinctive, stereotyped motor patterns. Their motor similarity does not decrease as the time interval between repetitions increases, suggesting that repeated syllables are stored in memory as fixed motor programs. The acoustic similarity between nonrepeated syllables, as indicated by correlation of their spectrograms, has a significant positive correlation with their motor similarity. This correlation is weak, however, suggesting that there is no simple linear relationship between motor action and acoustic output and that similar sounds may sometimes be produced by different motor mechanisms. When compared without regard to the sequence in which they are sung, syllables paired for maximum spectral similarity form a continuum with repeated syllables in terms of their acoustic and motor similarity. The prominence of couplets in the “syntax” of normal song is enhanced by the dissimilarity of successive nonrepeated syllables that make up the remainder of the song. © 1996 John Wiley & Sons, Inc.     

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.     

Song and brain development in canaries raised under different conditions of acoustic and social isolation over two years

Early isolation experiments indicate that male songbirds learn their songs during an early sensitive period, although later work has shown that some open-ended learners modify songs in later years. Recent isolation experiments suggest that in some species song has a stronger genetic basis than previously thought. This study raised domestic canaries under different combinations of acoustic and social isolation and followed song development into the second year. Males raised alone in acoustic isolation developed songs with normal syllables, but larger repertoires and also produced syllables with lower repetition rates when compared to controls. The smallest repertoire occurred in males raised in a peer group. Isolate males had a smaller song control nucleus HVC than controls, but there was no effect on nucleus RA or on brain weight in general. In the second year, after introduction into a large normal colony, isolate and peer group males adjusted their syllable repertoire to normal size. In particular, the isolates reduced their repertoire even though the size of HVC showed a significant increase in volume. However, songs of isolate and peer group males still differ in repetition rate and number of single syllables in the common aviary. In contrast, control males showed low syllable turnover and no significant change in repertoire size. Nor did they show any significant change in the volumes of song control nuclei. It seems that complete isolation affects only some aspects of song and brain development, and later socialization corrects some but not all of these in the second year.     

Song retuning with tutor model by adult zebra finches

Songbirds first memorize a tutor song in youth and develop their own song after the remembered model. As birds sexually mature, their song becomes crystallized and refractory to further tutoring. Here, we show that the song syllables of adult zebra finches gradually drift from their once crystallized forms, when individual birds are kept in auditory isolation or in company of cage mates singing different song syllables. Furthermore, when birds with drifted syllables are tutored with the same model again, they amend the fine structure of their syllables towards the model. In contrast, retutoring does not affect syllable sequences that differ from those of the original tutor.     

Song characterization in the spectacled warbler (Sylvia conspicillata): a circum-Mediterranean species with a complex song structure

The spectacled warbler (Sylvia conspicillata) is a small passerine with a patchy distribution throughout the circum-Mediterranean region, including the North Atlantic archipelagos of Madeira, Canary Islands and Cape Verde. Here we characterize the species song structure on the island of Fuerteventura, quantifying repertoire size, inter- and intra-individual spectrographic variation, to determine whether acoustic variation occurred within an island population. Male song display was organized in song bouts of a variable number of song phrases, which in turn were made up of 4–69 syllables. We classified syllable types to derive a measure of repertoire size (number of different syllables) per song bout, and then used rarefaction methods to calculate the estimated repertoire size for our population of males. Three categories of song bout length were considered in analyses: short song bouts of 10 phrases, average bouts of 19 phrases and long bouts of ≥ 29 phrases. The observed and estimated repertoire size per male (between 43 and 126 syllables per male) increased with song bout duration, although the relationship was not significant for the estimated values. To test whether songs could be individually specific, we measured 11 spectrotemporal parameters of the song. A discriminant analysis using these variables performed poorly in classifying songs to the individuals that uttered them, but we found less variation in the individual than in the population for three out of the 11 variables. These individually specific variables, involving the first or the most common syllable of the song, the trill, were the duration of the first syllable of the phrase, the duration and the dominant frequency of the trill syllable. Our study emphasizes the complexity of spectacled warbler songs, in which males continuously add novel syllables over the entire song bout. This complexity appears to be determined by individual innovation capabilities rather than by the behaviour of copying neighbour repertoires, since songs of close birds were not more similar than songs from far-away territories.     

The relative roles of cultural drift and acoustic adaptation in shaping syllable repertoires of island bird populations change with time since colonization

In birds, song divergence often precedes and facilitates divergence of other traits. We assessed the relative roles of cultural drift, innovation, and acoustic adaptation in divergence of island bird dialects, using silvereyes (Zosterops lateralis). In recently colonized populations, syllable diversity was not significantly lower than source populations, shared syllables between populations decreased with increasing number of founder events, and dialect variation displayed contributions from both habitat features and drift. The breadth of multivariate space occupied by recently colonized Z. l. lateralis populations was comparable to evolutionarily old forms that have diverged over thousands to hundreds of thousands of years. In evolutionarily old subspecies, syllable diversity was comparable to the mainland and the amount of variation in syllable composition explained by habitat features increased by two‐ to threefold compared to recently colonized populations. Together these results suggest that cultural drift influences syllable repertoires in recently colonized populations, but innovation likely counters syllable loss from colonization. In evolutionarily older populations, the influence of acoustic adaptation increases, possibly favoring a high diversity of syllables. These results suggest that the relative importance of cultural drift and acoustic adaptation changes with time since colonization in island bird populations, highlighting the value of considering multiple mechanisms and timescale of divergence when investigating island song divergence.     

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.     

Mechanisms of song differentiation in introduced populations of Chaffinches Fringilla coelebs in New Zealand

Chaffinches Fringilla coelebs were introduced to New Zealand from Great Britain over 100 years ago, and since then their songs have diverged from British ones in both syllable structure and basic organization of syllable sequences. The New Zealand populations seem to be unique in that their songs have undergone differentiation of trill segments by progressive elaboration of syllable morphology and hp ascending and descending changes of pitch. Published sonagrams of British song types have significantly more trill phrases and significantly fewer syllables in the end phrase than do Yew Zealand ones. Many New Zealand song types have much elaborated end phrases and concomitantly simpler trill segments, with songs quite commonly having only one trill phrase. This reversal of complexity between the trill and end phrase in New Zealand seems to have been derived by progressive reduction of the ultimate trill phrase to one syllable, and by recombination of end phrase syllables from different song types into one compound end phrase. The significance of the increased complexity in the end phrases of many song types may relate to the sound transmission properties of dense pine forests in New Zealand, in which Chaffinches are ubiquitous. Elaborate end phrases degrade much less from reverberation in pine forests because individual syllables have more dispersed temporal patterning.
Recombination of syllables to form new song types is a major mechanism of song differentiation in New Zealand. Although whole song copying is the predominant mode of replication, very few song types in a locality sample are composed of a unique set of syllables. Rather, song types in an area are interconnected by different combinations of shared syllables, suggesting that the incorporation of some local syllables in a bird's repertoire is sufficient to signal its status as a member of a neighbourhood and also allows the evolution of broadcast complexity.     

10种鸣禽鸣唱复杂性与发声核团体积的聚类分析

选用捕自野外和人工繁殖的10种雄性成鸟(一年龄以上)作为实验材料。当鸟适应环境后录音,用VS-99语音工作站软件进行声谱分析。鸣唱的复杂性采用语句短语总数、短语的音节数之和、短语的音节种类数之和、每个短语中所含的平均音节数、每个短语中所含的平均音节种类数、每种鸣禽最长短语的音节数和最长短语的音节种类数7项指标表示。然后测定前脑的上纹状体腹侧尾端(HVC)、古纹状体粗核(RA)以及嗅叶的X核(Areax)3个主要鸣唱控制核团的体积。最后分别对10种鸣禽3个发声控制核团体积和鸣唱复杂性的7项指标进行聚类分析。10种鸣禽的7项指标值相差较大,即使同一科也如此。蒙古百灵的3种核团体积比值均最大,其次是金丝雀和黄喉鹉。10种鸣禽鸣唱语句复杂性的7个指标和3种核团体积聚类分析树形图显示的结果各不相同;仅RA和Areax核团体积的树形图显示蒙古百灵远离其他9种鸣禽,与现代分类学和DNA分析得到的进化树一致。     

The Role of Song Phonology and Syntax in Vocal Learning Preferences in the Song Sparrow,Melospiza melodia

Are young songbirds ready to learn virtually any song, or are they predisposed to learn songs of their own species? To explore this question tests were conducted on the equipotentiality of auditory song learning stimuli in the song sparrow. 23 males reared as nestlings were exposed to tape recordings of their own and other species songs in early life and subsequent song production was analyzed for imitations. Birds exposed to natural song sparrow songs, including their fathers', and equal numbers of swamp sparrow songs, strongly preferred conspecific songs. They neither favored nor eschewed paternal songs despite having had access to them for 6–10 days as nestlings. In three other experiments synthetic songs were used in which some properties were held constant and others were systematically varied. Birds were exposed to 1–4 segmented songs varying in phrase order, tempo and syllable number, each synthesized in two versions, one from conspecific and the other from heterospecific (swamp sparrow) song syllables. With one-segmented songs (alien syntax) subjects favored conspecific over heterospecific syllable songs. Heterospecific syllables were rendered more acceptable by incorporation into two-segmented trilled songs (more song sparrow-like syntax). Heterogeneous summation of phonological and syntactical cues appeared to occur. There was also evidence of interaction between phonology and syntax. When another phrase type, the note complex, was added, in three- and four-segmented songs, a preference for conspecific syllables reappeared. Heterospecific syllables may be more readily accepted as a trilled sequence than without repetition, as in a note-complex. When phrase structure within four-segmented songs was varied, birds favored patterns most like normal conspecific song. We conclude that there are innate learning preferences in the song sparrow, based on note and syllabic structure (phonology and syllabic syntax), and temporal organization of phrases (segmental syntax), differing from those of the closely related swamp sparrow, Melospiza georgiana, in which song syntax plays no role in learning preferences.     

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.     

Song Motor control organizes acoustic patterns on two levels in Bengalese finches (<Emphasis Type="Italic">Lonchura striata</Emphasis> var. <Emphasis Type="Italic">domestica</Emphasis>)

Based on statistical analyses of song sequences, Bengalese finch (Lonchura striata var. domestica) songs do not show unvarying motif repetition as has been found in zebra finches (Taeniopygia guttata). Instead, there are variations of partially stereotyped sequences of song syllables. Although these stereotyped sequences consist of multiple syllables, in most cases these syllables occur together. To examine whether such structures really exist as a vocal production unit, we subjected singing birds to a light flash and determined when the stimulus stopped the songs. When light interruptions were presented within the statistically stereotyped sequences, the subsequent syllables tended to be produced, whereas interruptions presented during the statistically variable sequences tended to cause instantaneous song termination. This suggests that the associations among the song syllables that compose the statistically stereotyped sequences are more order dependent than those for the statistically variable sequences, and the tolerances of syllable pairs to visual interruptions are consistent with the statistical song structures. Additionally, following interruptions, several types of song sequence variations were observed that had not been previously reported. These phenomena might be caused by various effects of the visual stimulus on the hierarchical motor control program.     

The complex stridulatory behavior of the cricket Eneoptera guyanensis Chopard (Orthoptera: Grylloidea: Eneopterinae)

Crickets produce stridulated sounds by rubbing their forewings together. The calling song of the cricket species Eneoptera guyanensis Chopard, 1931 alternates two song sections, at low and high dominant frequencies, corresponding to two distinct sections of the stridulatory file. In the present study we address the complex acoustic behavior of E. guyanensis by integrating information on the peculiar morphology of the stridulatory file, the acoustic analysis of its calling song and the forewing movements during sound production. The results show that even if E. guyanensis matches the normal cricket functioning for syllable production, the stridulation involves two different closing movements, corresponding to two types of syllables, allowing the plectrum to hit alternately each differentiated section of the file. Transition syllables combine high and low frequencies and are emitted by a complete forewing closure over the whole file. The double-teeth section of the stridulatory file may be used as a multiplier for the song frequency because of the morphological multiplication due to the double teeth, but also because of an increase of wing velocity when this file section is used. According to available phylogenetic and acoustic data, this complex stridulation may have evolved in a two-step process.     

山地隔离和空间距离对高黎贡山灰腹地莺(Tesia cyaniventer)鸣唱特征的影响

鸟类鸣唱存在广泛的地理变异，研究鸟类鸣唱变异的模式及其影响因素可帮助解释自然界中广泛而复杂的鸣声变异现象。灰腹地莺（Tesia cyaniventer）是在高黎贡山海拔2000-2800 m分布的小型地栖性森林鸟类。高黎贡山南北走向的山脊海拔通常在3000m以上，这导致灰腹地莺东、西坡种群被山脊所隔离。该种小鸟鸣声洪亮易于鉴别，其鸣声地理变异可揭示山地对鸟类种群产生的隔离效应。在高黎贡山片马垭口和独龙江垭口的东西坡4个地点录制了灰腹地莺的鸣声（n=58），基于声谱分析比较了种群间鸣唱的质量特征，发现种群间鸣唱型的共享程度极低，而音节型在4个种群间均有共享。进一步测量了11个鸣唱的数量特征参数，有6个参数在不同种群间有显著差异：最低频率、中心频率、频率宽度、起始音节频率、首二音节的时间间隔、句子平均音节数。种群间的两两比较表明，鸣声特征差异呈现"隔离-距离"共同作用的格局，但隔离的影响更大。研究表明山地系统中影响鸟类鸣声地理变异的因素较为复杂，山地隔离和空间距离均对灰腹地莺的鸣唱特征产生了影响。