Northern Mockingbirds produce syntactical patterns of vocal mimicry that reflect taxonomy of imitated species

ABSTRACT Detailed studies of the patterns and processes associated with avian vocal mimicry are rare. Some vocal mimics, such as Northern Mockingbirds (Mimus polyglottos), often produce song types in rapid succession, but no published data exist concerning the syntactical organization of this behavior. We follow up on an undocumented assertion from the literature that mockingbirds cluster temporally their imitations of the same species. We examined long bouts of singing by 18 male mockingbirds and classified all songs as either mockingbird‐specific song or one of 55 mimetic types defined by the species mimicked and the song or call type of that species. Temporal pairs consisting of two exemplars of a single mimetic type were found at 2.6 times the level predicted by ordering songs by chance. Temporal pairs consisting of two mimetic types from the same species were found at 4.2 times chance levels. Temporal pairs consisting of mimetic types from two different species in the same family were found at 1.7 times chance levels, though this pattern was just above the significance threshold. We examined two functional hypotheses to explain these patterns, one involving female preferences and one involving interspecies communication, but found no support for either hypothesis. Detailed field observations of the social contexts in which temporal pairs are used by mockingbirds will be needed to better understand their function.     

Flight Phases in the Song of Skylarks: Impact on Acoustic Parameters and Coding Strategy

Skylarks inhabit open fields and perform an aerial song display which serves as a territorial signal. The particularly long and elaborate structure of this song flight raises questions about the impact of physical and energetic constraints acting on a communication signal. Song produced during the three distinct phases of the flight - ascending, level and descending phase could be subject to different constraints, serve different functions and encode different types of information. We compared song parameters during the ascending and the level phases. We found that the structure of the song varied with the phase of the flight. In particular, song had a higher tempo when skylarks were ascending which might be related to higher oxygen and energetic demands. We also explored which phase of the song flight might encode individuality. Earlier studies reported that skylarks reduced their territorial response to established neighbours if the neighbour song was broadcasted from the correct adjacent boundary, but reacted aggressively if the neighbour songs were broadcasted from an incorrect boundary (mimicking a displaced neighbour). Such differential response provides some evidence for individual recognition. Here, we exposed subjects to playback stimuli of neighbour song in which we had replaced either the song produced during the level or the ascending phase by the relevant song of the neighbour from the incorrect border. Singing response was higher towards stimuli in which the ‘level phase song’ was replaced, indicating that skylarks could be able to recognise their neighbours based on song of this phase. Thus, individuality seems to be primarily coded in the level phase of the flight song.     

Responses of a sub-oscine bird during playback: effects of different song variants and breeding period

Vermilion flycatchers (Pyrocephalus rubinus) vary their song rate and song length across the breeding season. Males sing more and longer songs after nest construction than before. Here we explored the possibility that this variation is meaningful to territorial males. Using a playback approach, we tested several males with different variations in song output (i.e. variations in song length and song rate) in different periods of the breeding season (i.e. before and after the onset of nest construction). We found that males call more in response to playbacks of long and short songs before the onset of nest construction. However, after nest construction began they responded flying more when exposed to long songs than to short songs. These results show that vermilion flycatcher discriminates between different variants of song length, and suggest that males react to long songs as if they were more threatening signals than short songs, especially after the onset of nest construction. We did not find evidence of males discriminating between a high and a low song rate. We discuss some possible implications for song function in this sub-oscine species, and compare these findings with other results in oscine species.     

Comparative study of long-term reduction of high-frequency song syllables in deafened zebra and Bengalese finches: implications for the role of auditory feedback in song maintenance

Auditory feedback is necessary for adult song maintenance in both oscines and psittacines. Although belonging to phylogenically separated orders, deafened adult oscine Bengalese finches and psittacine budgerigars exhibit similarities in certain aspects of song changes. An interesting question is whether these birds share common mechanisms for song maintenance. Therefore, it is important to compare the effects of deafening on adult song patterns among and within orders. Although zebra and Bengalese finches are closely related oscine species, few studies have performed direct, long-term, quantitative comparisons of their songs after deafening because suitable song characteristics have not been identified. Based on our previous findings for Bengalese finch songs, we analyzed zebra finch songs over 9 months after deafening, focusing on changes in the number of syllables categorized according to fundamental frequencies. Deafened zebra finches demonstrated a gradual but significant decrease in high-frequency syllables and a tendency to increase low-frequency syllables, similar to deafened Bengalese finches. Although this change took longer in zebra finches, the altered proportion of syllables eventually stabilized. Results indicated that adult songs show similar aspects after auditory deprivation, and that neural mechanisms involved in the maintenance of high-frequency song syllables, using auditory feedback, may be present in both finches despite species differences.     

The song of Skylarks Alauda arvensis indicates the deterioration of an acoustic environment resulting from wind farm start‐up

The rapid development of wind energy may have negative effects on bird populations, including collisions with turbines, displacement due to disturbance or habitat loss, indirect effects of reduced breeding success and barrier effects. This challenging conservation issue has attracted a great deal of interest, but the noise generated by turbines has been largely overlooked. Here, we studied acoustic behaviour of Skylarks Alauda arvensis in relation to wind farm start‐up to assess whether a change in song parameters can indicate a deterioration in the acoustic environment. We recorded territorial males displaying close to operating and non‐operating turbines and at a control site without turbines. In the following breeding season, we undertook replications at the same sites, except that the non‐operating turbines were now in operation. We found that Skylarks displaying at the wind farm were affected by wind turbine noise. Males singing close to operating wind turbines sang higher‐frequency songs than males from a control site and those that displayed near non‐operating turbines. In addition, an upward frequency shift in songs was observed when non‐operating turbines started to operate in the consecutive season. We therefore conclude that the frequency shift observed did not result from turbine presence, but from the noise they started to generate. This shows that a change in song parameters may reliably and within a relatively short time indicate a significant deterioration of the acoustic environment as a consequence of wind farm start‐up. This may help conservation biologists to identify species and populations that are particularly susceptible to wind farm noise.     

Rock wrens preferentially use song types that improve long distance signal transmission during natural singing bouts

When animals are capable of producing variable signals they may preferentially use some signal types over others. Among songbirds, individuals are known to alter song type form and usage patterns in contest and mating situations, but studies have not examined how song choice improves signal efficacy during broadcast song. For this study we investigated rock wren Salpinctes obsoletus song type use rates during natural singing bouts. We tested three hypotheses for adaptive song use during broadcast song: 1) birds improve signal content by increasing the use of high quality songs, 2) birds optimize for signal propagation by preferentially using songs that transmit well, and 3) birds maintain energy by reducing the use of costly songs. The study included 19 058 songs sung by 12 individuals, each of which had a measured song repertoire of between 52 and 117 song types which were produced at highly variable rates. Results indicated that rock wrens did not preferentially sing song types with shorter durations or fewer frequency switches, as would be expected if they selected song types to minimize delivery costs. They also did not favor songs with more rapid trills or more frequency switches, as would be expected if they adjusted song use primarily to indicate quality. Focal birds did preferentially sing significantly longer songs with lower bandwidths, lower frequencies, and slower trill rates. Results suggest that natural broadcast singing patterns are shaped more by the benefits of long distance transmission than by the benefits of advertising performance ability or the costs of song production.     

Complementary neural systems for the experience‐dependent integration of mate‐choice cues in European starlings

Choice of a particular mate phenotype may arise out of experience with the very phenotypes under consideration. Female European starlings (Sturnus vulgaris) prefer males that sing predominantly long‐bout songs over males that sing predominantly short‐bout songs, and thus, song‐bout length is a phenotypic parameter instrumental in releasing the female's mate choice. The preferred long‐bout songs induce higher expression of the immediate early gene (IEG) ZENK in the female auditory telencephalon than short‐bout songs do, but this sensitivity to song length depends on the female's recent song experience. Here, we compared the experience‐dependent modulation of ZENK with that of another IEG, FOS, and report that ZENK and FOS expression in the caudomedial mesopallium and caudomedial nidopallium show different modulation properties that complement natural variation in song‐bout length. As reported previously, ZENK expression was greater in response to novel long‐bout than to novel short‐bout songs following a 1‐week experience with long‐bout but not short‐bout songs. In contrast, FOS expression was greater in response to novel long‐bout than to novel short‐bout songs following a 1‐week experience with short‐bout but not long‐bout songs. Thus, the ZENK and FOS signaling pathways are made sensitive to variation in song length by experiences with songs at opposite ends of the starling song‐variation continuum, suggesting the presence of complementary neural systems made sensitive in register with the natural axis of phenotypic variation fundamental to the female's mate choice. © 2004 Wiley Periodicals, Inc. J Neurobiol, 2005     

Age‐dependent song changes in a closed‐ended vocal learner: elevation of song performance after song crystallization

Birdsong is a sexual signal that serves as an indicator of male quality. There is already abundant evidence that song elaboration reflects early life‐history because early developmental stress affects neural development of song control systems, and leaves irreversible adverse effects on song phenotypes. Especially in closed‐ended vocal learners, song features crystallized early in life are less subject to changes in adulthood. This is why less attention has been paid to lifelong song changes in closed‐ended learners. However, in the eyes of female birds that gain benefits from choosing mates based on male songs, not only past but also current conditions encoded in songs would be meaningful, given that even crystallized songs in closed‐ended learners would not be identical in the long term. In this study, we examine within‐individual song changes in the Java sparrow Lonchura oryzivora, with the aim of shedding light on the relationship between song and long‐term life history. Specifically, we compared song length, tempo, and song complexity measures between the point just after song crystallization and around 1 yr later, and also compared those traits between fathers and sons to clarify the effect of vocal learning. While it is not surprising that song complexity did not differ depending on age or between fathers and sons, we found that song length and tempo increased with age. Follow‐up analyses have revealed that frequency bandwidth and peak frequency of song notes also elevated with age. Our results show that song performance related to motor skills can be improved even after song crystallization. We also suggest that song performance in closed‐ended vocal learners gives a reliable clue for mate choice by reflecting male quality with aging.     

Organization of song of rose-breasted grosbeaks

Rose-breasted grosbeaks (Pheucticus ludovicianus) in Quebec had repertoires of fifteen to twenty-three syllables per bird, some of which were similar among neighbours. These were presented in songs with modes of nine to eleven syllables per song. Consecutive songs often began with the same syllables, even as many as three or four in succession, but overall sequences were usually different. The sequences were found to fit first and second order Markov models. Immediate repetitions of syllables within songs occurred uncommonly and were peculiar to particular syllables. The duration of intervals usually related directly to the immediately preceding syllables and song types. Where two syllables frequently followed another, the time intervals at the switches were usually significantly different between the two although the differences did not relate to the probabilities of the switches. There was a tendency to alternate long and short syllables. The applications of these findings to models of neural control are discussed.     

Stereotyped and non-stereotyped features of the temporal patterning of singing sessions in the ovenbird Seiurus auricapillus

Temporal patterning of recorded singing sessions of 26 different male ovenbirds Seiurus auricapillus (Fringillidae: Parulini) was analyzed computationally, in order to test whether differences among songs are potentially informative or merely reflect performance errors. Repeated songs within a singing session by a given male showed relatively little inter-individual variation in the duration of the song or in the number of units composing it, although these features varied substantially among individuals. On the other hand, within a session of singing by an individual male, the most variable and potentially informative aspect of temporal patterning was the relative placement of the peak amplitude within the song. These results support the hypothesis that diversity in the vocalization sessions of oscine passerines can be produced by other means than the use of a varied song repertoire, even in a species like the ovenbird that uses just one song type. Because variation among song was focused on a single feature, performance errors are an unlikely explanation, suggesting that the temporal patterning of singing sessions may play an informative role, such as the minimization of habituation on the part of receivers.     

Song learning by prairie warblers: When,where, and from whom

Songbirds of many species acquire their songs by imitating the songs of conspecific singers. Conclusive evidence of such imitation comes from controlled laboratory studies, but such studies do not reveal when and where songbirds learn their songs under natural conditions. To determine the timing and location of song learning in a population of prairie warblers, we compared the songs of yearling prairie warblers of known hatching location to the songs of other birds in the yearlings' natal and first breeding areas. The comparisons yielded a likely model song (and model singer) for each of the song types used by the focal yearlings. We supplemented our findings from the song comparisons with inferences drawn from an analysis of local geographic variation in songs. This analysis revealed that shared song types showed no tendency to be geographically clustered within the study area. Taken together, our data suggest that prairie warblers learn their songs during the hatch year, at locations somewhat distant (mean distance 1,437 m) from their natal site, most likely as birds wander about during the post-fledging period.     

Song Learning in Song Sparrows: Relative Importance of Autumn vs. Spring Tutoring

We examined ‘late’ song learning in song sparrows (Melospiza melodia), i.e., song learning that occurs after the first few months, or classical sensitive period, of the natal summer. Fledgling juveniles were brought into the laboratory at 2–3 mo of age and exposed to computer‐simulated song tutors in three different time periods: late in the natal summer, the autumn, and the next spring. As expected, the birds’ final repertoires consisted mostly of songs heard in the field, but 30% of the birds’ songs were influenced by songs heard in the laboratory (selective retention) and another 8% were learned de novo in the laboratory. Parallel results were obtained for a second group of birds who received laboratory tutoring only in the spring. In fact, the results suggested that autumn tutoring may even be inhibitory. We conclude that the songs a young song sparrow hears in his first spring may be critical to his final repertoire development, indicating that the song learning process in song sparrows is longer and more flexible than previously supposed.     

Adult bengalese finches (Lonchura striata var. domestica) require real-time auditory feedback to produce normal song syntax

Songbirds develop their songs by imitating songs of adults. For song learning to proceed normally, the bird's hearing must remain intact throughout the song development process. In many species, song learning takes place during one period early in life, and no more new song elements are learned thereafter. In these so-called close-ended learners, it has long been assumed that once song development is complete, audition is no longer necessary to maintain the motor patterns of full song. However, many of these close-ended learners maintain plasticity in overall song organization; the number and the sequence of song elements included in a song of an individual vary from one utterance to another, although no new song elements are added or lost in adulthood. It is conceivable that these species rely on continued auditory feedback to produce normal song syntax. The Bengalese finch is a close-ended learner that produces considerably variable songs as an adult. In the present study, we found that Bengalese finches require real-time auditory feedback for motor control even after song learning is complete; deafening adult finches resulted in development of abnormal song syntax in as little as 5 days. We also found that there was considerable individual variation in the degree of song deterioration after deafening. The neural mechanisms underlying adult song production in different species of songbirds may be more diverse than has been traditionally considered. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 343–356, 1997     

Song matching in the great tit (Parus major): The effect of similarity and familiarity

Great tits were played recordings of one of their own songs, and a song of the same type from a neighbour and one from a stranger (from more than 500 m away). The birds matched their own songs most often and those of strangers least. We had predicted that strangers would be matched most, because previous work had shown an association between matching and a strong response. An analysis using a difference index showed that the birds matched most often when the stimulus song was very similar in detailed structure to their own rendition of the song. This was confirmed in a second experiment in which we played ‘similar’ and ‘different’ renditions recorded from strangers. However, once the effect of similarity was partialled out there was a residual tendency to match strangers more than neighbours, as we had first predicted. We discuss the implications of these results for perception of song categories by the birds, possible use by the birds of their own songs as ‘standards’ and the functional significance of matching.     

Watch Your Tone: Social Conditions Modulate Singing Strategies

Bird song is typically depicted as a male singing a long‐distance signal to potentially unknown receivers to (1) deter males and (2) attract females. Nevertheless, many songbirds sing from close distances to a known receiver; males of these species may be under more intense selective pressure to modify their songs depending on the sex of the receiver in order to convey different motivational states (aggression versus courtship) to the different sexes. In a laboratory setting, we examined how receiver sex affected within‐song variation of the close‐range singing behavior in the brown‐headed cowbird (Molothrus ater). Although we know that cowbird song is influenced by flock composition, it is still unclear as to how the cowbird modifies his song based on social context. Using a cross‐correlation analysis of each male's different song types, we found that pairs of songs were significantly more dissimilar if they were directed to females compared with songs directed to males. We subsequently tested whether there were any consistent spectral or temporal patterns in the songs males gave to females versus to males. Our results lend support for the Motivational Structural Rules Hypothesis as songs directed toward males had higher entropy (i.e., harshness) than the same song type directed toward females. Our results suggest that cowbirds may have evolved the ability to alter multiple dimensions of their singing behavior based on receiver sex.     

Sex role similarity and sexual selection predict male and female song elaboration and dimorphism in fairy‐wrens

Historically, bird song complexity was thought to evolve primarily through sexual selection on males; yet, in many species, both sexes sing and selection pressure on both sexes may be broader. Previous research suggests competition for mates and resources during short, synchronous breeding seasons leads to more elaborate male songs at high, temperate latitudes. Furthermore, we expect male–female song structure and elaboration to be more similar at lower, tropical latitudes, where longer breeding seasons and year‐round territoriality yield similar social selection pressures in both sexes. However, studies seldom take both types of selective pressures and sexes into account. We examined song in both sexes in 15 populations of nine‐fairy‐wren species (Maluridae), a Southern Hemisphere clade with female song. We compared song elaboration (in both sexes) and sexual song dimorphism to latitude and life‐history variables tied to sexual and social selection pressures and sex roles. Our results suggest that song elaboration evolved in part due to sexual competition in males: male songs were longer than female songs in populations with low male survival and less male provisioning. Also, female songs evolved independently of male songs: female songs were slower paced than male songs, although only in less synchronously breeding populations. We also found male and female songs were more similar when parental care was more equal and when male survival was high, which provides strong evidence that sex role similarity correlates with male–female song similarity. Contrary to Northern Hemisphere latitudinal patterns, male and female songs were more similar at higher, temperate latitudes. These results suggest that selection on song can be sex specific, with male song elaboration favored in contexts with stronger sexual selection. At the same time, selection pressures associated with sex role similarity appear to favor sex role similarity in song structure.     

Diet and birdsong: short‐term nutritional enrichment improves songs of adult Bengalese finch males

Song is a notable sexual signal of birds, and serves as an honest indicator of male quality. Condition dependence of birdsong has been well examined from the viewpoint of the developmental stress hypothesis, which posits that complex songs assure fitness because learned acoustic features of songs are especially susceptible to early‐life stress that young birds experience in song learning periods. The effect of early stress on song phenotypes should be crucial, especially in age‐limited song learners which sing stereotyped songs throughout life. However, little attention has been paid to non‐learned song features that can change plastically even in adulthood of age‐limited song‐learners. Although it has been shown that food availability affects song rate in wild songbirds, there is limited evidence of the link between favorable nutritional conditions and song phenotypes other than song rate. Under the prediction that singing behavior reflects an individual's recent life history, we kept adult Bengalese finch males under high‐nutrition or normal diet for a short term, and examined changes in body mass and songs. We found that birds on a high‐nutrition diet showed higher song output (e.g. song rate and length) compared with those of the control group, while changes in body mass were moderate. In addition, note repertoire became more consistent and temporal structures got faster in both nutrition and control groups, which indicates that songs were subject to other factors than nutrition. Considering that female estrildid finches, including Bengalese and zebra finches, show a preference toward complex songs as well as longer songs and higher song rate, it is plausible that different aspects of singing behavior signal different male qualities, and provide multifaceted clues to females that choose mates.     

Levels of Organization in the Song of the Bobolink (Icteridae: Dolichonyginae)

By comparison with other icterids, the bobolink (Dolichonyx oryzivorus) sings an unusually long and complex song. The songs of four male bobolinks were analysed in terms of units at four different levels of analysis: the figure, the figure-sequence, the song-pattern, and the song. The different levels of analysis show different degrees of stereotypy and variation. Individual males in the study area differed in the frequency of use of the different song-patterns and in the way they assembled them into songs. Immediate repetition of song patterns within a song was unusual. Songs sung from fixed perches were shorter than songs sung in flight. The results suggest that the length of bobolink song is in part a consequence of its use of the song as a part of an elaborate flight display, and that the unit we called the “song-pattern” was closest to the unit designated “song” in most other species.     

Is the Tonal Quality of Birdsong Learned? Evidence from Song Sparrows

Song sparrow (Melospiza melodia) songs are composed largely of pure-tonal sounds. This paper investigates the role that learning plays in the development of the tonal structure of song sparrow songs, as well as the role that tonal quality plays in determining the suitability of songs as models for learning. 20 birds were trained with both normal pure-tonal songs and modified songs that included harmonic overtones. The harmonic-modified songs were obtained from birds singing in a helium atmosphere, the result of which is to perturb vocal tract resonances and thus alter a song's tonal quality. Subjects learned equally well from normal and harmonic models. Birds that learned material from harmonic models reproduced some of this material with harmonic overtones, but the majority of notes learned from harmonic models were subsequently reproduced as pure-tonal copies. Thus, the tonal structure of songs does not influence young song sparrows in their selection of song models, but there is a strong tendency to reproduce songs in a pure-tonal fashion, even if learned from harmonic models.     

Female choice for song characteristics in the house finch

Song has been proposed to function in mate choice, and such a role has been demonstrated experimentally in a number of species. We presented captive female house finches, Carpodacus mexicanus, with a choice of two songs, each of which was identical except for a single parameter that had been either accentuated or minimized. To ensure that our playback tapes offered choices within the normal range of variation in house finch song, we recorded wild male finches, then created playback tapes using values for the song parameters under consideration that were above or below the mean for the local population, but within the natural range of variation. We presented females that had not previously mated with choices between songs that (1) were long or short, (2) were given at fast or slow rates, and (3) included a large or small repertoire of unique song elements. Females showed significant preferences for long songs and for songs presented at a faster rate, but there was no significant preference for large or small repertoires of unique song elements. Song length and rate each seem likely to indicate a male's energy reserves, and thus could be important sources of information for females choosing mates.