Complexity,Predictability and Time Homogeneity of Syntax in the Songs of Cassin’s Vireo (Vireo cassinii)

Many species of animals deliver vocalizations in sequences presumed to be governed by internal rules, though the nature and complexity of these syntactical rules have been investigated in relatively few species. Here I present an investigation into the song syntax of fourteen male Cassin’s Vireos (Vireo cassinii), a species whose song sequences are highly temporally structured. I compare their song sequences to three candidate models of varying levels of complexity–zero-order, first-order and second-order Markov models–and employ novel methods to interpolate between these three models. A variety of analyses, including sequence simulations, Fisher’s exact tests, and model likelihood analyses, showed that the songs of this species are too complex to be described by a zero-order or first-order Markov model. The model that best fit the data was intermediate in complexity between a first- and second-order model, though I also present evidence that some transition probabilities are conditioned on up to three preceding phrases. In addition, sequences were shown to be predictable with more than 54% accuracy overall, and predictability was positively correlated with the rate of song delivery. An assessment of the time homogeneity of syntax showed that transition probabilities between phrase types are largely stable over time, but that there was some evidence for modest changes in syntax within and between breeding seasons, a finding that I interpret to represent changes in breeding stage and social context rather than irreversible, secular shifts in syntax over time. These findings constitute a valuable addition to our understanding of bird song syntax in free-living birds, and will contribute to future attempts to understand the evolutionary importance of bird song syntax in avian communication.     

Serial order in wood thrush song

In a study of two captive male wood thrushes (Hylocichla mustelina), I found that each bird had a preferred serial order of songs when it sang in isolation. This order could be disrupted by playback. When the stimulus was one of the subject's own songs, the bird often answered with the song that followed the stimulus song in the preferred order. This result supports the following hypothesis: the preferred serial order of songs delivered by a wood thrush is based, in part, on a mechanism by which one song facilitates, via a loop involving audition, the production of the next song in the sequence. I gained further insight into this mechanism by analysing the response of the birds to each other's songs and to experimentally altered songs.     

Juvenile sparrows preferentially eavesdrop on adult song interactions

Recent research has demonstrated that bird song learning is influenced by social factors, but so far has been unable to isolate the particular social variables central to the learning process. Here we test the hypothesis that eavesdropping on singing interactions of adults is a key social event in song learning by birds. In a field experiment, we compared the response of juvenile male song sparrows (Melospiza melodia) to simulated adult counter-singing versus simulated solo singing. We used radio telemetry to follow the movements of each focal bird and assess his response to each playback trial. Juveniles approached the playback speakers when exposed to simulated interactive singing of two song sparrows, but not when exposed to simulated solo singing of a single song sparrow, which in fact they treated similar to heterospecific singing. Although the young birds approached simulated counter-singing, neither did they approach closely, nor did they vocalize themselves, suggesting that the primary function of approach was to permit eavesdropping on these singing interactions. These results indicate that during the prime song-learning phase, juvenile song sparrows are attracted to singing interactions between adults but not to singing by a single bird and suggest that singing interactions may be particularly powerful song-tutoring events.     

Interspecific Response to Playback of Bird Song

Responses to bird song have usually only been studied at the intraspecific level. I experimentally tested whether playback of the song of the black wheatear Oenanthe leucura in an area in S Spain resulted in responses from conspecifics as well as heterospecific birds by comparing the numbers of individuals singing before and after playback. The number of singing male black wheatears increased considerably, but also the number of singing males of five other passerine species increased significantly. The heterospecific response to playback may be due (1) to interspecific territoriality, (2) to black wheatear song signalling the absence of predators, or (3) to heterospecifics confusing the species-identity of the singer. The second alternative is considered more likely, since an ecologically wide array of species increased their song rate following playback. The conspicuous dawn (and dusk) chorus of bird song may be augmented by social facilitation due to the singing of conspecifics as well as heterospecifics.     

Latent song type memories are accessible through auditory stimulation in a hand-reared songbird

The production of learned vocalizations such as in birdsong is often used to judge whether stimuli had been memorized upon their presentation. However, failures in the imitation of certain song patterns may also reflect impaired development of motor programmes or impaired memory retrieval rather than failures in stimulus memorization during auditory acquisition. To study this issue, we confronted adult hand-reared nightingales, Luscinia megarhynchos, with interactive playback experiments and used vocal matching as a behavioural tool to investigate their song type memories. Vocal matching is a common pattern-specific response that songbirds use in territorial countersinging. We distinguished two forms of pattern-specific matching: (1) song type matching (i.e. a bird replied with the same song type as the stimulus song), and (2) song group matching (i.e. the bird replied with a different song type which was, however, sequentially associated with the playback song presented earlier, i.e. during the tutoring). Some subjects used both song type and song group matching in response to song types they had not imitated from the tutor programme prior to the playback experiments. Our results indicate that nightingales store more song types in their sensory phase than they spontaneously recall from memory as adults. That is, memories of song types that were not performed in overt behaviour could be activated by vocal interactions, here induced by the interactive playback. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Comparative approaches to avian song system function: insights into auditory and motor processing

Many fundamental advances in our understanding of basic neural function have been made using bird song learning and performance as a model system. These advances have included a greater understanding of higher-order neural processing, developmental and hormonal influences on behavior, and the realization that neurogenesis plays an important role in normal adult brain function. The great diversity of passerine birds and song-related behaviors they exhibit suggest that oscine songbirds are ideally suited for comparative studies. While the comparative approach has been used successfully in the past to study song-related phenomena at anatomical and behavioral levels, it has been underutilized in addressing questions at the neurophysiological level. Most neurophysiological studies of songbird auditory and motor processing have been performed in one species, the zebra finch (Taeniopygia guttata). We present and compare neurophysiological studies we have performed in zebra finches and song sparrows (Melospiza melodia), species that differ markedly in their singing behavior and song repertoire characteristics. Interspecific similarities, and striking differences, in song neural processing are apparent. While preliminary, these data suggest that comparative neurophysiological studies of species carefully chosen for their vocal repertoire and singing behavior will contribute significantly to our understanding of vertebrate sensory and motor neural processing.     

Comparative approaches to the avian song system

There is extensive diversity among the 4000 species of songbirds in different aspects of song behavior, including the timing of vocal learning, sex patterns of song production, number of songs that are learned (i.e., repertoire size), and seasonality of song behavior. This diversity provides unparalleled opportunities for comparative studies of the relationship between the structure and function of brain regions and song behavior. The comparative approach has been used in two contexts: (a) to test hypotheses about mechanisms of song control, and (b) to study the evolution of the control system in different groups of birds. In the first context, I review studies in which a comparative approach has been used to investigate sex differences in the song system, the relationship between the number of song types a bird sings and the size of the song nuclei, and seasonal plasticity of the song control circuits. In the second context, I discuss whether the vocal control systems of parrots and songbirds were inherited from a common ancestor or independently evolved. I also consider at what stage in the phylogeny of songbirds the hormone-sensitive forebrain circuit found in modern birds first evolved. I conclude by identifying directions for future research in which a comparative approach would be productive. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 517–531, 1997     

Classification of group-specific variations in songs within House Wren species using machine learning models

Songbirds have shown variation in vocalizations across different populations and different geographical ranges. Such variations can over time lead to divergence in song characteristics, sometimes referred to as dialects. House Wren (Troglodytes aedon) is one such widely distributed bird species that has shown variation in its song characteristics within different populations. Traditionally, such studies have been conducted using manual approaches for classification. In this work we explore the use of machine learning models that can assist in performing classification of bird songs at a conspecific level. Two machine learning techniques, the random forest and a shallow feed forward neural network, are fed with pre-computed sound features to classify vocal variation in House Wren species across different reported population groups and latitudinal areas. A randomized approach is employed to create balanced subsets of sounds from different locations for repeated classification runs in order to provide a reliable estimate of performance. It is observed that such an automated approach is able to classify variations in songs within House Wren with high accuracy. We were also able to confirm the latitudinal variation of House Wren songs reported in previous studies. Given these results, we believe, such a purely data-driven way of analyzing bird songs in general can provide useful hints to biologists on where to look for interesting patterns in order to understand the evolutionary divergence in song characteristics.     

Signalling through acoustic windows: nightingales avoid interspecific competition by short-term adjustment of song timing

The function of bird song is closely linked to sexual selection through female choice and male–male competition, and thus variation in communication success is likely to have major fitness consequences for a singing male. A crucial constraint on signal transmission is imposed by background noise, which may include songs from other species. I investigated whether singing nightingales (Luscinia megarhynchos) avoid temporal overlap with the songs of other bird species in a playback experiment. I analysed the temporal song patterns of six males, each of which were exposed to songs of other species. The nightingales significantly avoided overlapping their songs with the playback songs, and started singing preferentially during the silent intervals between the heterospecific songs. This timing of song onset produced a greater variability in pause duration compared to the nightingales’ undisturbed solo singing. These findings suggest that birds adjust their song timing to avoid acoustic interference on short temporal scales, and thus are able to improve the efficiency of acoustic communication in complex sonic environments. Moreover, the results indicate that temporal song patterns can be affected by the songs of other species, and thus such influences should be taken into account when studying bird song in the field.     

Song type switching in the chaffinch, Fringilla coelebs : timing or counting?

The song of many bird species is relatively constant in form, yet each bird has more than one song type, making it an excellent model for studies of the mechanisms underlying switching between behaviour patterns. The chaffinch is a good example. Males sing with eventual variety, repeating each song type in the repertoire a few times before switching to another type. The mechanism triggering these switches is not known. We investigated long continuous recordings of spontaneous singing by six wild males to test two hypotheses: (1) that a maximum number of repetitions limits bout length; or (2) that a switch occurs after a song type bout reaches a maximum duration ('time window'). Strong evidence was found for a temporal limitation: song type bouts with many repetitions were delivered only at a fast rate, whereas bouts consisting of few songs were delivered either fast or slow. Copyright 1999 The Association for the Study of Animal Behaviour.     

A species-specific view of song representation in a sensorimotor nucleus

Songbirds constitute a powerful model system for the investigation of how complex vocal communication sounds are represented and generated, offering a neural system in which the brain areas involved in auditory, motor and auditory–motor integration are well known. One brain area of considerable interest is the nucleus HVC. Neurons in the HVC respond vigorously to the presentation of the bird’s own song and display song-related motor activity. In the present paper, we present a synthesis of neurophysiological studies performed in the HVC of one songbird species, the canary (Serinus canaria). These studies, by taking advantage of the singing behavior and song characteristics of the canary, have examined the neuronal representation of the bird’s own song in the HVC. They suggest that breeding cues influence the degree of auditory selectivity of HVC neurons for the bird’s own song over its time-reversed version, without affecting the contribution of spike timing to the information carried by these two song stimuli. Also, while HVC neurons are collectively more responsive to forward playback of the bird’s own song than to its temporally or spectrally modified versions, some are more broadly tuned, with an auditory responsiveness that extends beyond the bird’s own song. Lastly, because the HVC is also involved in song production, we discuss the peripheral control of song production, and suggest that interspecific variations in song production mechanisms could be exploited to improve our understanding of the functional role of the HVC in respiratory–vocal coordination.     

An arousing, musically enhanced bird song stimulus mediates circadian rhythm phase advances in dim light

A musically enhanced bird song stimulus presented in the early subjective night phase delays human circadian rhythms. This study determined the phase-shifting effects of the same stimulus in the early subjective day. Eleven subjects (ages 18-63 yr; mean +/- SD: 28.0 +/- 16.6 yr) completed two 4-day laboratory sessions in constant dim light (<20 lux). They received two consecutive presentations of either a 2-h musically enhanced bird song or control stimulus from 0600 to 0800 on the second and third mornings while awake. The 4-day sessions employing either the stimulus or control were counterbalanced. Core body temperature (CBT) was collected throughout the study, and salivary melatonin was obtained every 30 min from 1900 to 2330 on the baseline and poststimulus/postcontrol nights. Dim light melatonin onset and CBT minimum circadian phase before and after stimulus or control presentation was assessed. The musically enhanced bird song stimulus produced significantly larger phase advances of the circadian melatonin (mean +/- SD: 0.87 +/- 0.36 vs. 0.24 +/- 0.22 h) and CBT (1.08 +/- 0.50 vs. 0.43 +/- 0.37 h) rhythms than the control. The stimulus also decreased fatigue and total mood disturbance, suggesting arousing effects. This study shows that a musically enhanced bird song stimulus presented during the early subjective day phase advances circadian rhythms. However, it remains unclear whether the phase shifts are due directly to effects of the stimulus on the clock or are arousal- or dim light-mediated effects. This nonphotic stimulus mediates circadian resynchronization in either the phase advance or delay direction.     

Female response song in the ephippigerines Steropleurus stali and Platystolus obvius (Orthoptera,Tettigoniidae)

Stridulation by females of Steropleurus stali and Platystolus obvius in response to the calling song of the males was observed and recorded. The response has only been stimulated by the appropriate male song, either directly or from a recording. The structure of the files and the form of stridulation in both sexes is described. The male song of S. stali is remarkable in that only a few teeth on the file are struck in each wing movement. It is also notable that both opening and closing wing strokes contribute more or less equally to the syllable. The female song is similar but distinct. The song of P. obvius male is a single chirp involving nearly all the teeth on the file and with the main emphasis on the closing syllable. The response song of the female is a very brief chirp. These species are only sporadic singers, but when the female responds they are stimulated into greater activity. They thus contrast with reiterative singers like Ephippiger in which there is no female response. The implications of these contrasting behavioural patterns is discussed.     

Physically Challenging Song Traits,Male Quality,and Reproductive Success in House Wrens

Physically challenging signals are likely to honestly indicate signaler quality. In trilled bird song two physically challenging parameters are vocal deviation (the speed of sound frequency modulation) and trill consistency (how precisely syllables are repeated). As predicted, in several species, they correlate with male quality, are preferred by females, and/or function in male-male signaling. Species may experience different selective pressures on their songs, however; for instance, there may be opposing selection between song complexity and song performance difficulty, such that in species where song complexity is strongly selected, there may not be strong selection on performance-based traits. I tested whether vocal deviation and trill consistency are signals of male quality in house wrens (Troglodytes aedon), a species with complex song structure. Males’ singing ability did not correlate with male quality, except that older males sang with higher trill consistency, and males with more consistent trills responded more aggressively to playback (although a previous study found no effect of stimulus trill consistency on males’ responses to playback). Males singing more challenging songs did not gain in polygyny, extra-pair paternity, or annual reproductive success. Moreover, none of the standard male quality measures I investigated correlated with mating or reproductive success. I conclude that vocal deviation and trill consistency do not signal male quality in this species.     

The evolutionary importance of behavioural development: the ontogeny and phylogeny of bird song

It has been proposed that ontogeny may be an important constraint on the evolution of morphological traits. In this paper, ontogeny is discussed as a possible constraint on behavioural evolution. A literature review of the development of song in oscine birds (Passeriformes; Passeres) shows that song development follows von Baer's law; that is, that development proceeds from early, generally distributed stages to later, specialized stages. Song ontogeny is found to parallel phylogeny in a lineage of sparrows (Emberizidae; Emberizinae). Possible cases of paedomorphosis (slowing down or truncation of development) in bird song are discussed, specifically in the family Mimidae and in the reed warbler, Acrocephalus palustris (Muscicapidae; Sylviinae). Finally, the implications of developmental constraints for the study of the adaptive significance of behaviour are discussed.     

A SYSTEM FOR DESCRIBING BIRD SONG UNITS

ABSTRACT

Bird song researchers have not agreed on a common set of units of analysis by which birds' songs of various different species might be described. Analysis of 50 papers reveals 28 unit designations and considerable variation in their application despite only three different methods for identifying units. The lack of consensus on units arises from the fact that units generated by the same methods at different levels of organization are given different names. A method for designating bird song units is offered for discussion which uses the concept of level of organization to stress the fundamental unanimity of method. It is hoped that consideration of this method will lead ultimately to greater standardization in the protocols by which researchers generate and name bird song units.     

Patterns of song evolution and sexual selection in the oropendolas and caciques

Although oscine bird song is widely thought to have evolvedunder the influence of sexual selection, few studies have usedphylogenetic comparative methods to investigate how these vocalizationshave changed historically. In the present study, we use a molecularphylogeny based on mitochondrial sequence data to reconstructvocal evolution in the oropendolas and caciques, an oscine groupwith diverse taxon-specific song patterns and a wide range inlevels of sexual size dimorphism. Our reconstructions show thatlarge changes in song organization and structure have occurredon branches of the phylogeny with relatively high levels ofsize dimorphism. The particular vocal components that changed,however, often differed in different phylogenetic lineages.These patterns indicate that sexual selection has had importantinfluences on song evolution in these birds, but has targeteddifferent components of song in different taxa. Our resultsprovide insight into how sexual selection influences bird songand suggest directions for future research to uncover the behavioralmechanisms driving vocal evolution.     

Differential geographic patterns in song components of male Albert’s lyrebirds

Geographic variation in bird song has received much attention in evolutionary studies, yet few consider components within songs that may be subject to different constraints and follow different evolutionary trajectories. Here, we quantify patterns of geographic variation in the socially transmitted “whistle” song of Albert''s lyrebirds (Menura alberti), an oscine passerine renowned for its remarkable vocal abilities. Albert''s lyrebirds are confined to narrow stretches of suitable habitat in Australia, allowing us to map likely paths of cultural transmission using a species distribution model and least cost paths. We use quantitative methods to divide the songs into three components present in all study populations: the introductory elements, the song body, and the final element. We compare geographic separation between populations with variation in these components as well as the full song. All populations were distinguishable by song, and songs varied according to the geographic distance between populations. However, within songs, only the introductory elements and song body could be used to distinguish among populations. The song body and final element changed with distance, but the introductory elements varied independently of geographic separation. These differing geographic patterns of within‐song variation are unexpected, given that the whistle song components are always produced in the same sequence and may be perceived as a temporally discrete unit. Knowledge of such spatial patterns of within‐song variation enables further work to determine possible selective pressures and constraints acting on each song component and provides spatially explicit targets for preserving cultural diversity. As such, our study highlights the importance for science and conservation of investigating spatial patterns within seemingly discrete behavioral traits at multiple levels of organization.     

Song learning and mate choice in estrildid finches raised by two species

Male zebra finches, Taeniopygia guttata, and Bengalese finches, Lonchura striata, were raised normally or cross-fostered to the other species until 35 days of age and then housed until 70 days old with two song tutors, one from each species. Males raised normally based their song on that of the conspecific tutor whereas cross-fostered males also learned from the other tutor, reflecting both own-species bias and a tendency to learn from the tutor whose song was similar to the father's. Males raised by one bird from each species learned from the father as well as the tutor(s) but were more likely to learn from the tutor whose song was similar to the father's if the father was a conspecific. Comparing these song learning results with those from male choice tests suggests there is no direct link between song learning and sexual imprinting.