Song Ontogeny Research Articles

Seasonal song ontogeny in western North Atlantic humpback whales: drawing parallels with songbirds

ABSTRACT The use of song as a reproductive display is common in the animal kingdom; however, for many taxa, little is known of song ontogeny. Male humpback whales produce elaborate songs on low latitude breeding grounds in winter and begin to sing on high latitude feeding grounds in late summer, yet songs from the two locations are rarely compared. Seasonal song ontogeny in western North Atlantic humpback whales was explored by comparing songs recorded in high latitude feeding grounds (Canada in spring 2016 and fall 2016 to winter 2017) with songs recorded in a low latitude breeding ground (Dominican Republic in winter and spring 2017). High-quality song samples were selected, and every phrase annotated. Song theme order, song duration, and number of phrase repetitions were compared across samples. The most variability in theme order was found between November and December in the Canadian recordings, a phase in song ontogeny that may be important for learning. Song duration gradually increased, via an increase in phrase repetitions, through the breeding season, before peaking in the Dominican Republic between January and March. A comparison to oscine bird seasonal song ontogeny revealed many similarities, highlighting potentially similar physiological processes between humpback whales and songbirds.

Ontogeny of vocal learning in a hummingbird

Hummingbirds have evolved to learn song from conspecifics independently of other bird clades that show this behaviour, such as parrots and oscine passerines. Little is known about how vocal learning occurs in hummingbirds. To determine the conditions necessary and sufficient for learning, we raised young Costa's hummingbirds, Calypte costae, in isolation in two experiments. The first experiment tested whether three pairs of males, raised either in silence or with only acoustic exposure to song, would produce wild-type song. They did not: each pair instead produced ‘isolate’ songs dissimilar to wild-type song. Each pair produced a unique isolate song with subtle differences from other pairs. Thus, exposure to song alone is insufficient to trigger learning. The second experiment tested whether individually housed males would learn songs when exposed to a live male model plus playback of song (1 h/day, 3 days/week, for 3 months). Seven of eight birds that heard Costa's-like songs learned to sing their tutor song. Each individual produced song that matched idiosyncratic features of the individual songs played to them, demonstrating attention to, and learning of the exact acoustic stimuli received. Two control birds exposed to acoustically dissimilar Anna's hummingbird, Calypte anna, song developed isolate song. Thus, exposure to species-specific song with a conspecific male is sufficient to trigger learning. The sensory phase began after fledging, around 23 days posthatch, and the sensorimotor phase began around 50 days posthatch, when singing also began. Song crystallization occurred approximately 125 days posthatch. Costa's also appear to be statistical learners; they learn to sing the songs they hear most often. Hummingbird song ontogeny appears to be similar to song ontogeny in passerines, despite its convergent origin.

Song ontogeny in Nuttall’s white-crowned sparrows tutored with individual phrases

Behavioral ontogeny involves the interaction of innate predispositions and experience. In bird song learning, one approach to exploring this interaction is to examine the songs rehearsed by young birds whose exposure to tutor models has been carefully controlled. Here, I analyzed the rehearsed repertoire in Nuttall’s white-crowned sparrows (Zonotrichia leucophrys nuttalli) tutored with individual phrases of conspecific and heterospecific songs. The proportions of phrase types rehearsed indicate that the learning biases evident in crystallized song are manifest early on, suggesting preferential memorization rather than preferential retention during attrition. The proportion of songs beginning with whistles increased during song rehearsal and phrase sequence variability decreased, consistent with the idea that innate syntax specifications guide song rehearsal. Single-phrase tutored birds overproduced phrases to the same extent previously observed in birds tutored with full, normal song but retained fewer phrase types in their crystallized repertoires. This suggests that in this subspecies, acquired syntax information does not affect the number of phrase types memorized and rehearsed but does affect repertoire attrition at the end of the sensorimotor phase. I discuss these results with a focus on the action of innate templates in song development and subspecies differences in this process.

Testosterone regulates birdsong in an anatomically specific manner

The functions of birdsong include attracting a mate and repelling competitors. It is therefore not surprising that, in males in the temperate zone especially, birdsong is often produced in the context of reproduction. Testosterone of gonadal origin increases during the reproductive phase of the annual cycle and can significantly influence song production as well as song development via effects on song crystallization (testosterone secretion at the time of sexual maturity is essential for full crystallization to occur). In males, testosterone of gonadal origin can exert its effects in the brain on song and other reproductive behaviour via its oestrogenic and androgenic metabolites. The widespread distribution of nuclear androgen receptors in the song system and the occurrence of oestrogen receptors in one key forebrain nucleus in certain species as well as the presence of both receptor types in the diencephalon and the midbrain raises questions as to where and how testosterone is exerting its myriad effects on song. By selectively implanting testosterone into specific brain regions of castrated male canaries, Serinus canaria, we have identified the medial preoptic area as a critical site for the induction of a generalized increase in motivation that includes the motivation to sing. Testosterone action in the forebrain song nucleus HVC in contrast increases song stereotypy. Canaries receiving testosterone in the preoptic area and HVC sing stereotypic songs but at a much lower amplitude, indicating that testosterone's effects on amplitude are regulated elsewhere in the brain or the periphery. The lateral part of the magnocellular nucleus anterior nidopallium (LMAN) is a song nucleus that expresses a high density of androgen receptors and plays a role as a song variability generator during song learning. When adult female canaries are treated with testosterone, their song becomes more complex. Lesions to LMAN attenuate these effects on adult behavioural change, suggesting that testosterone may act in LMAN during song ontogeny to modulate changes associated with song crystallization. These anatomically specific effects illustrate how a single hormone can coordinate changes in many aspects of a complex behaviour to facilitate successful reproduction.

The interplay of within-species perceptual predispositions and experience during song ontogeny in zebra finches (Taeniopygia guttata).

Vocal acquisition in songbirds and humans shows many similarities, one of which is that both involve a combination of experience and perceptual predispositions. Among languages some speech sounds are shared, while others are not. This could reflect a predisposition in young infants for learning some speech sounds over others, which combines with exposure-based learning. Similarly, in songbirds, some sounds are common across populations, while others are more specific to populations or individuals. We examine whether this is also due to perceptual preferences for certain within-species element types in naive juvenile male birds, and how such preferences interact with exposure to guide subsequent song learning. We show that young zebra finches lacking previous song exposure perceptually prefer songs with more common zebra finch song element types over songs with less common elements. Next, we demonstrate that after subsequent tutoring, birds prefer tutor songs regardless of whether these contain more common or less common elements. In adulthood, birds tutored with more common elements showed a higher song similarity to their tutor song, indicating that the early bias influenced song learning. Our findings help to understand the maintenance of similarities and the presence of differences among birds' songs, their dialects and human languages.

Song organization and variability in Northern House Wrens (Troglodytes aedon parkmanii) in western Canada

ABSTRACT. Detailed descriptions of song structure are critical to understanding the ontogeny, evolution, and function of bird song, particularly for species with large song repertoires. We provide a first detailed characterization of song organization and variability in a migratory population of House Wrens (Troglodytes aedon) breeding in western Canada, using a sample of 15,608 songs from 15 males. Males sang with high intensity in protracted bouts prior to pairing and often resumed high-intensity singing later in the breeding cycle to attract a second mate. The high-amplitude terminal portion of songs comprised rapid trills of frequency-modulated notes organized into discrete syllable types with a mean of 10 syllables and 4 syllable types per song. The population syllable repertoire was large (n = 27) and mostly shared but was used to produce much larger repertoires of song types, most of which were unique. Individual males sang up to 194 different song types, with no evidence of a ceiling. However, mal...

Quantitative tools for examining the vocalizations of juvenile songbirds.

The singing of juvenile songbirds is highly variable and not well stereotyped, a feature that makes it difficult to analyze with existing computational techniques. We present here a method suitable for analyzing such vocalizations, windowed spectral pattern recognition (WSPR). Rather than performing pairwise sample comparisons, WSPR measures the typicality of a sample against a large sample set. We also illustrate how WSPR can be used to perform a variety of tasks, such as sample classification, song ontogeny measurement, and song variability measurement. Finally, we present a novel measure, based on WSPR, for quantifying the apparent complexity of a bird's singing.

Incomplete and Inaccurate Vocal Imitation after Knockdown of FoxP2 in Songbird Basal Ganglia Nucleus Area X

The gene encoding the forkhead box transcription factor, FOXP2, is essential for developing the full articulatory power of human language. Mutations of FOXP2 cause developmental verbal dyspraxia (DVD), a speech and language disorder that compromises the fluent production of words and the correct use and comprehension of grammar. FOXP2 patients have structural and functional abnormalities in the striatum of the basal ganglia, which also express high levels of FOXP2. Since human speech and learned vocalizations in songbirds bear behavioral and neural parallels, songbirds provide a genuine model for investigating the basic principles of speech and its pathologies. In zebra finch Area X, a basal ganglia structure necessary for song learning, FoxP2 expression increases during the time when song learning occurs. Here, we used lentivirus-mediated RNA interference (RNAi) to reduce FoxP2 levels in Area X during song development. Knockdown of FoxP2 resulted in an incomplete and inaccurate imitation of tutor song. Inaccurate vocal imitation was already evident early during song ontogeny and persisted into adulthood. The acoustic structure and the duration of adult song syllables were abnormally variable, similar to word production in children with DVD. Our findings provide the first example of a functional gene analysis in songbirds and suggest that normal auditory-guided vocal motor learning requires FoxP2.

An Assessment of Song Admixture as an Indicator of Hybridization in Black-Capped Chickadees (Poecile Atricapillus) and Carolina Chickadees (P. Carolinensis)

AbstractVocal admixture often occurs where differentiated populations or species of birds meet. This may entail song sympatry, bilingually singing birds, and songs with intermediate or atypical characteristics. Different levels of vocal admixture at the range interface between Black-capped Chickadees (Poecile atricapillus) and Carolina Chickadees (P. carolinensis) have been interpreted as indicating that hybridization is frequent at some locations but not others. However, song ontogeny in these birds has a strong nongenetic component, so that inferences regarding hybridization based on vocal admixture require confirmation. We used diagnostic genetic markers and quantitative analyses of song to characterize population samples along two transects of the chickadee contact zone in the Appalachian Mountains. More than 50% of individuals at the range interface were of hybrid ancestry, yet only 20% were observed to be bilingual or to sing atypical songs. Principal component analysis revealed minimal song intermediacy. This result contrasts with an earlier analysis of the hybrid zone in Missouri that found considerable song intermediacy. Re-analysis of the Missouri data confirmed this difference. Correlation between an individual’s genetic composition and its song type was weak in Appalachian hybrid populations, and genetic introgression in both forms extended far beyond the limits of vocal admixture. Therefore, song is not a reliable indicator of levels of hybridization or genetic introgression at this contact zone. Varying ecological factors may play a role in producing variable levels of song admixture in different regions of the range interface.Una Evaluación de la Mixtura de Cantos como Indicador de Hibridación en Poecile atricapillus y P. carolinensis

AN ASSESSMENT OF SONG ADMIXTURE AS AN INDICATOR OF HYBRIDIZATION IN BLACK-CAPPED CHICKADEES (POECILE ATRICAPILLUS) AND CAROLINA CHICKADEES (P. CAROLINENSIS)

Vocal admixture often occurs where differentiated populations or species of birds meet. This may entail song sympatry, bilingually singing birds, and songs with intermediate or atypical characteristics. Different levels of vocal admixture at the range interface between Black-capped Chickadees (Poecile atricapillus) and Carolina Chickadees (P. carolinensis) have been interpreted as indicating that hybridization is frequent at some locations but not others. However, song ontogeny in these birds has a strong nongenetic component, so that inferences regarding hybridization based on vocal admixture require confirmation. We used diagnostic genetic markers and quantitative analyses of song to characterize population samples along two transects of the chickadee contact zone in the Appalachian Mountains. More than 50% of individuals at the range interface were of hybrid ancestry, yet only 20% were observed to be bilingual or to sing atypical songs. Principal component analysis revealed minimal song intermediacy. This result contrasts with an earlier analysis of the hybrid zone in Missouri that found considerable song intermediacy. Re-analysis of the Missouri data confirmed this difference. Correlation between an individual’s genetic composition and its song type was weak in Appalachian hybrid populations, and genetic introgression in both forms extended far beyond the limits of vocal admixture. Therefore, song is not a reliable indicator of levels of hybridization or genetic introgression at this contact zone. Varying ecological factors may play a role in producing variable levels of song admixture in different regions of the range interface. Una Evaluación de la Mixtura de Cantos como Indicador de Hibridación en Poecile atricapillus y P. carolinensis

How sleep affects the developmental learning of bird song

Sleep affects learning and development in humans and other animals, but the role of sleep in developmental learning has never been examined. Here we show the effects of night-sleep on song development in the zebra finch by recording and analysing the entire song ontogeny. During periods of rapid learning we observed a pronounced deterioration in song structure after night-sleep. The song regained structure after intense morning singing. Daily improvement in similarity to the tutored song occurred during the late phase of this morning recovery; little further improvement occurred thereafter. Furthermore, birds that showed stronger post-sleep deterioration during development achieved a better final imitation. The effect diminished with age. Our experiments showed that these oscillations were not a result of sleep inertia or lack of practice, indicating the possible involvement of an active process, perhaps neural song-replay during sleep. We suggest that these oscillations correspond to competing demands of plasticity and consolidation during learning, creating repeated opportunities to reshape previously learned motor skills.

Neighbor-stranger discrimination by song in a suboscine bird, the alder flycatcher, Empidonax alnorum

Bird song and its functions have been studied extensively for more than 50 years, but almost entirely in oscine passerines. Few studies have investigated any aspect of song in suboscine passerines. This is significant because song development and the extent of individual variation in song differs greatly between these groups. Learning and auditory feedback play major roles in song development in all oscines studied, but apparently no part in song ontogeny in suboscines. The ability of territorial oscine males to discriminate between songs of neighbors and strangers has received considerable attention, but this phenomenon is virtually unstudied in suboscines. We tested whether a suboscine bird, the alder flycatcher (Empidonax alnorum), was able to discriminate between songs of neighbors and strangers despite limited individual variation in song. We performed playback experiments to measure responses of males to songs of neighbors and strangers broadcast from the territory boundary shared by the subject and the neighbor. Subjects responded more aggressively to songs of strangers than to songs of neighbors. These results further our understanding of the evolution of song and its functions in suboscines by demonstrating that, similar to their oscine relatives, they can discriminate between the songs of neighbors and strangers.

Causes and consequences of song amplitude adjustment in a territorial bird: a case study in nightingales.

Vocal amplitude, one of the crucial factors for the exchange of acoustic signals, has been neglected in studies of animal communication, but recent studies on song variation in Common Nightingales Luscinia megarhynchos have revealed new insights into its importance in the singing behavior of territorial birds. In nightingales song amplitude is not maximized per se, but is individually regulated according to the level of masking background noise. Also, birds adjust their vocal intensity according to social variables, as in male-male interactions. Moreover, during such interactions, males exploited the directionality of their songs to broadcast them in the direction of the intended receivers ensuring the most effective signal transmission. Studies of the development of this typical long-range signaling suggest that sound level is highly interrelated with overall developmental progression and learning, and thus should be viewed as an integral part of song ontogeny. I conclude that song amplitude is a dynamic feature of the avian signal system, which is individually regulated according to the ecological demands of signal transmission and the social context of communication.

Song learning and vocal tradition in Nuttall's white-crowned sparrows

We investigated song sharing and dispersion of song types in the wild in a colour-marked population of the non-migratory Nuttall's white-crowned sparrow,Zonotrichia leucophrys nuttalli. The songs of fathers, their male progeny (sons), and the neighbours of the sons at recruitment sites were analysed spectrographically and compared qualitatively and quantitatively. To determine whether a son's song more closely matched that of his father or a neighbour at the site settled, we subjected frequency and temporal characteristics of songs within each father–son–neighbour triad to multivariate cluster analysis. The songs of 14 of 16 sons clustered with their neighbours’ rather than their fathers’ songs, confirming that song matching of neighbours is an integral component of territory settlement by juveniles. Principal components analysis of frequency and temporal measurements of song within a dialectal area show that songs group into neighbourhoods and are non-randomly distributed. Multivariate analysis suggests that sons may entrain on frequency and temporal characteristics of a neighbour's song without matching phrases or complex syllables. Implications for models of instructive versus selective learning are discussed. The timing of closure of the sensitive phase, the length of the silent interval between the sensory phase and plastic song stage, and the time to song crystallization remain open questions in song ontogeny.

Female canaries display to songs of early isolated males

We tested the sexual responsiveness of female canaries,Serinus canaria, to two sets of different types of male conspecific songs. In each set, three of the male songs had been recorded in a young bird which was isolated at an early age from conspecifics. Each bird was recorded during three stages of the song ontogeny (early plastic songs, late plastic songs and crystallized songs). We used copulation solicitation displays (CSD) as an index of female sexual response. Playbacks were performed during a period of natural sexual responsiveness of the females to song. We demonstrated that, in both experiments, very weak sexual displays of female canaries were recorded to the two stages of ‘isolate’ plastic songs. Each of the two different types of ‘isolate’ crystallized songs elicited high levels of CSD. These levels are not significantly different from the adult domesticated control song. Taken together, these results suggest that even isolate songs may convey sexual information. We discuss prominent acoustic features that must be present to ensure female sexual responses.

Relations between song repertoire size and the volume of brain nuclei related to song: comparative evolutionary analyses amongst oscine birds

Song and brain structure are compared amongst 41 species of oscine birds by using the method of independent evolutionary contrasts. We find a significant correlation between the relative volume of the song control centre, the high vocal centre (HVC), and the number of song types typically found in the repertoire. Relative HVC volume is not correlated with the number of different syllable types per song bout. The relative volume of a second song nucleus, area X, is not significantly correlated with either measure. Relative HVC volume is uncorrelated with relative volume of the hippocampus, a brain area involved in other forms of memory. This is the first evidence for repeated independent evolution of an association between complexity of learned song and the relative volume of one of the song control nuclei though to be involved in song learning.

Development of two song categories by chestnut-sided warblers

Unlike most songbirds, individuals of several wood-warbler species have song repertoires that contain two song classes, each with distinct patterns of use and geographical variation. These patterns suggest that the modes of song development of the two categories could differ in important ways, such as in the nature of auditory and social experience required during song ontogeny. That possibility was tested in an experiment with a representative paruline species, the chestnut-sided warbler Dendroica pensylvanica. Of three experimental groups, one heard no tutor songs. A second group heard tutor tapes of both the unaccented-ending (UE) and accented-ending (AE) song categories, and a third group heard the tutor tapes but also saw and heard live adult males. The untutored birds developed no species-typical songs. Some of the tutored individuals learned songs from tapes alone, but learning and performance quality were greatly enhanced by the presence of a live tutor. Birds exposed only to tape tutoring imitated AE songs but failed to learn UE songs; live-tutored birds imitated songs from both categories. These results, interpreted in the context of field data, support the hypothesis that chestnut-sided warbler song development is somewhat compartmentalized, with AE song development more restricted by a neural ‘template’ and UE song more dependent on, and subject to influence by, social interaction.

A Comparison Between Development of Bird Song and Development of Other Displays

The ontogeny of bird song is compared with that of other vocal and postural displays. At the level of description both types of display show a gradual development towards a more conspicuous and stereotyped form. In addition, the developmental outcome shows in both cases plasticity under the influence of social experience. At the level of mechanisms similarities and differences are discussed. Although song development has been studied mainly from the perspective of learning, and development of other displays from the perspective of motivational changes, both these mechanisms play a role in the development of both types of display. The development of both types may be influenced by the reactions of conspecifics to the display performed and sex hormones. The latter may enhance the expression of species specific properties and influence crystallization or form fixation in both song and other displays. Imitation, so important for normal song development in many song bird species, does not seem to influence the development of postural displays, but there is some preliminary evidence that it may influence the development of vocal display other than song. The influence of sensory-motor learning (motor matching) is discussed.

Steroidal Control of Behavioural, Neuroendocrine and Brain Sexual Differentiation: Studies in a Carnivore, the Ferret

More than 30 years have passed since the publication ( I ) showing that transplacental administration of testosterone to female guinea-pigs caused permanent changes in their ability to exhibit reproductive behaviours in response to ovarian steroids in adulthood. Over the intervening years articles have appeared which have extended this type of observation to numerous other mammalian species, including rat, hamster, gerbil, mouse, dog, ferret, pig, sheep, rhesus monkey, and marmoset (2, 3). In many instances inferences have been made about the probable existence of steroid-induced changes in the structure and function of the nervous system which underlie these changes in behaviour. These so-called ‘organizational’ effects of perinatal steroid exposure on the developing nervous system are often distinguished from the later ‘activational’ effects of these same steroids on the expression of sociosexual behaviours in adulthood. The number of different mammalian species used for mechanistic studies on the organizational effects of steroids, such as determining the precise perinatal timing of hormone action, the identity of the steroid(s) responsible for behavioural sexual differentiation, and the neural sites of steroid action, has been relatively small, and generally restricted to rodents. In the late 1970’s sex steroids acting during development were first implicated in the differentiation of sexually dimorphic telencephalic structures in passerine song birds which control singing associated with courtship (4, 5) . Since this early work, numerous studies have exploited the canary and zebra finch to explore mechanisms of steroid action in controlling the ontogeny of song in the male and the underlying changes in the nervous system. Other studies using the rat have explored in detail the role of androgen and oestrogen in controlling the differentiation in males of patterns of reproductive behaviour (2) as well as aspects of neural sex dimorphisms in the preoptic area/anterior hypothalamus (POA/AH) (6) and in the lumbar spinal cord (7). The concentration of mechanistic (behavioural, biochemical, neuroanatomical) studies of steroidal effects on sexually dimorphic behavioural potential in a few avian and rodent species is understandable, in light of their relative availability, low expense, and rapid time-course of neural development. Despite the substantial progress already made using these lower vertebrate models in promoting our understanding of how sex steroids influence neural and behavioural development, extrapolation of the results obtained in these studies to higher mammals including man cannot occur in the absence of some degree of empirical verification. Obviously, experimental manipulations of steroidal exposure during the development of human subjects would be unethical, thus we are left with experiments of nature (e.g. congenital adreno-genital syndrome,androgen insensitivity syndrome, and Sa-reductase deficient pseudohermaphroditism; details in later sections) with which to ask questions about the role of sex steroids in controlling psychosexual development in man. This work using clinical populations has been complemented by studies (8, 9) on two populations of rhesus female pseudohermaphrodites, created by transplacental administration of either testosterone or dihydrotestosterone (DHT) and by a study of female pseudohermaphroditic marmosets created by neonatal treatment with testosterone (10). While highly informative as far as they go, this research has not led to mechanistic studies using non-human primates to explore such questions as the critical perinatal periods of steroid action, the relative role of oestrogens versus androgens in controlling behavioural sexual differentiation in the male, or the relationship between steroidal control of sex dimorphisms in brain structure and behaviour. We have used the European ferret (Mustelufuro) in a n effort to develop a model system in which such questions can be addressed in a higher mammal. This carnivore is ideally suited for such experiments in that it is commercially available at a reasonable cost, is easily kept and handled in the laboratory, and produces relatively large litters (6 to 12 kits) which are born in an altricial state after a relatively short gestation (41 days) and which reach adulthood within 5 months. Normally, ferrets breed seasonally in response to lengthening photoperiod. A commercial breeder (Marshall Farms, North Rose, NY, USA) provides pregnant ferrets for our experiments throughout the year by the judicious use of artificial photoperiods in their breeding facility. Upon arrival in the laboratory, all ferrets used in our research are continuously

Vocal communication in New World monkeys

Many features of the vocal communication systems of New World primates are similar to the most complex vocal systems known: human speech and bird song. This paper reviews the parallels between vocal communication in New World monkeys and phenomena of bird song and human speech. The long or loud calls of New World monkeys are functionally similar to bird song, being used for maintaining territories, for intragroup cohesion and for mate attraction. These long calls have features that allow for species, subspecies and individual recognition. While the long and loud calls of some New World primates fit the design features that maximize long distance transmission in tropical habitats, the long calls of most callitrichids are pitched too high for maximal distance of transmission. There are parallels in the ontogeny of bird song and the ontogeny of long calls. A highly variable set of calls is used by immature animals crystallizing into a stereotyped form with reproductive maturation. There is evidence of phonetic variation with categorical perception of different calls in pygmy marmosets. A rudimentary syntax and orderly turn taking behavior have been found in many New World primates. In squirrel monkeys there is evidence of a metacommunicative function of calls. The vocal communication systems of New World monkeys represent some of the most sophisticated vocal systems found in nonhuman primates.