Singing Behavior Research Articles

Female and male Blue Tits (Cyanistes caeruleus) sing in response to experimental predator exposition

Female song is recognized to serve a similar function as male song and underlies sexual selection processes; yet certain patterns of the expression of female singing behaviour are not in line with traditional explanations known from male songbirds. In particular, in northern hemisphere songbirds, female singing behaviour is regarded to occur only rarely, and; therefore, studies investigating it are sparse. Within the framework of an experimental study on nest defence behaviour, we observed female singing in a common European passerine, namely, the Blue Tit (Cyanistes caeruleus). Females expressed singing behaviour when a dummy of a Sparrow Hawk was exposed to the nest, raising the idea that song might be multifunctional in this species.

Song structure and cadence of the Veery (Catharus fuscescens) in the Appalachian Mountains

ABSTRACT We recorded the natural song of male Veeries (Catharus fuscescens) on breeding territories to examine variation in song structure, repertoire size, and patterns of song delivery. Despite wide distribution of Veeries, many aspects of their biology are largely unknown, including a clear characterization of song and singing behavior. Recordings were made in four regions through the Appalachian Mountains in the USA. Visual analysis of song spectrogram images revealed that Veeries present their song repertoires in an oscillating frequency pattern, a previously undocumented feature of their singing behavior. Analysis showed Veeries’ repertoire ranges from 1–6 different song types, which is larger than what was previously described in the literature. Spectrogram analysis suggested that Veeries present song repertoires in predictable patterns, and patterns of song presentation can change depending on repertoire size. Songs and singing behavior did not differ between dawn and dusk singing bouts.

Dopaminergic Contributions to Vocal Learning.

During skill learning, the brain relies on sensory feedback to improve motor performance. However, the neural basis of sensorimotor learning is poorly understood. Here, we investigate the role of the neurotransmitter dopamine in regulating vocal learning in the Bengalese finch, a songbird with an extremely precise singing behavior that can nevertheless be reshaped dramatically by auditory feedback. Our findings show that reduction of dopamine inputs to a region of the songbird basal ganglia greatly impairs vocal learning but has no detectable effect on vocal performance. These results suggest a specific role for dopamine in regulating vocal plasticity.

Watch Your Tone: Social Conditions Modulate Singing Strategies

AbstractBird 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.

GSK-3β Inhibition Affects Singing Behavior and Neurogenesis in Adult Songbirds

GSK-3 (glycogen synthase kinase-3) is a serine/threonine kinase which is a critical regulator in neuronal signaling, cognition, and behavior. We have previously shown that unlike other vertebrates that harbor both α and β GSK-3 genes, the α gene is missing in birds. Therefore, birds can be used as a new animal model to study the roles of GSK-3β in behavior and in regulating adult neurogenesis. In the present study, we inhibited GSK-3β in brains of adult male zebra finches (Taeniopygia guttata) and accordingly investigated how this inhibition affects behavior and cell proliferation. Our results show that GSK-3 inhibition: (1) affects specific aspects of singing behavior, which might be related to social interactions in birds, and (2) differentially affects cell proliferation in various parts of the ventricular zone. Taken together, our study demonstrates a role of GSK-3β in regulating singing behavior and neuronal proliferation in birds and highlights the importance of GSK-3β in modulating cognitive abilities as well as social behavior.

Reproductive state modulates testosterone-induced singing in adult female European starlings (Sturnus vulgaris)

European starlings (Sturnus vulgaris) exhibit seasonal changes in singing and in the volumes of the neural substrate. Increases in song nuclei volume are mediated at least in part by increases in day length, which is also associated with increases in plasma testosterone (T), reproductive activity, and singing behavior in males. The correlations between photoperiod (i.e. daylength), T, reproductive state and singing hamper our ability to disentangle causal relationships. We investigated how photoperiodic-induced variation in reproductive state modulates the effects of T on singing behavior and song nuclei volumes in adult female starlings. Female starlings do not naturally produce measureable levels of circulating T but nevertheless respond to exogenous T, which induces male-like singing. We manipulated photoperiod by placing birds in a photosensitive or photorefractory state and then treated them with T-filled or empty silastic implants. We recorded morning singing behavior for 3weeks, after which we assessed reproductive condition and measured song nuclei volumes. We found that T-treated photosensitive birds sang significantly more than all other groups including T-treated photorefractory birds. All T-treated birds had larger song nuclei volumes than with blank-treated birds (despite photorefractory T-treated birds not increasing song-rate). There was no effect of photoperiod on the song nuclei volumes of T-treated birds. These data show that the behavioral effects of exogenous T can be modulated by reproductive state in adult female songbirds. Furthermore, these data are consistent with other observations that increases in singing rate in response to T are not necessarily due to the direct effects of T on song nuclei volume.

Two novel vocalizations are used by veeries (Catharus fuscescens) during agonistic interactions.

Avian vocalizations are common examples of the complex signals used by animals to negotiate during agonistic interactions. In this study, we used two playback experiments to identify agonistic signals in a songbird species with several acoustically complex songs and calls, the veery. In the first experiment, we compared veery singing behavior in response to simulated territorial intrusions including playback of three variations of veery song: 1) song alone as a control, 2) songs with added whisper calls, and 3) songs with introductory notes removed. In the second experiment, we used multimodal stimuli including songs, whisper calls and songs with introductory notes removed, along with a robotic veery mount. Focal males readily responded to all of the playback stimuli, approached the speaker and/or robotic mount, and vocalized. Male veeries gave more whisper calls, and sang more songs without the introductory note in response to all types of playback. However, veeries responded similarly to all types of stimuli presented, and they failed to physically attack the robotic mount. These results indicate that rival veeries use two different types of novel vocalizations: whisper calls and songs lacking the introductory note as agonistic signals, but do not allow us to discern the specific functions of these two vocalizations.

Using the canary genome to decipher the evolution of hormone-sensitive gene regulation in seasonal singing birds.

BackgroundWhile the song of all songbirds is controlled by the same neural circuit, the hormone dependence of singing behavior varies greatly between species. For this reason, songbirds are ideal organisms to study ultimate and proximate mechanisms of hormone-dependent behavior and neuronal plasticity.ResultsWe present the high quality assembly and annotation of a female 1.2-Gbp canary genome. Whole genome alignments between the canary and 13 genomes throughout the bird taxa show a much-conserved synteny, whereas at the single-base resolution there are considerable species differences. These differences impact small sequence motifs like transcription factor binding sites such as estrogen response elements and androgen response elements. To relate these species-specific response elements to the hormone-sensitivity of the canary singing behavior, we identify seasonal testosterone-sensitive transcriptomes of major song-related brain regions, HVC and RA, and find the seasonal gene networks related to neuronal differentiation only in the HVC. Testosterone-sensitive up-regulated gene networks of HVC of singing males concerned neuronal differentiation. Among the testosterone-regulated genes of canary HVC, 20% lack estrogen response elements and 4 to 8% lack androgen response elements in orthologous promoters in the zebra finch.ConclusionsThe canary genome sequence and complementary expression analysis reveal intra-regional evolutionary changes in a multi-regional neural circuit controlling seasonal singing behavior and identify gene evolution related to the hormone-sensitivity of this seasonal singing behavior. Such genes that are testosterone- and estrogen-sensitive specifically in the canary and that are involved in rewiring of neurons might be crucial for seasonal re-differentiation of HVC underlying seasonal song patterning.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-014-0578-9) contains supplementary material, which is available to authorized users.

Reward associated with singing behavior correlates with opioid-related gene expression in the medial preoptic nucleus in male European starlings.

Birdsong consists of species-specific learned vocal sequences that are used primarily to attract mates and to repel competitors during the breeding season. However, many birds continue to sing at times when vocal production has no immediate or obvious impact on conspecific behavior. The mechanisms that ensure that animals produce important behaviors in contexts in which the function of these behaviors is not immediate or obvious are not known. One possibility is that animals engage in such behaviors because they are associated with pleasure. Here we examined the hypothesis that male European starlings sing outside of the breeding season in part because the act of singing in this context is facilitated and/or maintained by opioid-mediated reward. We measured song-associated reward using a conditioned place preference (CPP) test in male starlings producing fall, non-breeding season-typical song. We used quantitative real time PCR to measure expression of the enkephalin opioid precursor preproenkephalin (PENK) and mu opioid receptors (MOR) in the medial preoptic nucleus (POM; a region in which opioids are implicated in both reward and starling fall song) and additionally the song control region HVC as a control. Starlings developed a strong preference for a place that had been paired previously with the act of producing fall-typical song, indicating that fall song production was associated with a positive affective state. Both PENK and MOR mRNA expression in the POM, but not HVC, correlated positively with both individual reward state (as reflected in CPP) and undirected singing behavior. These results suggest that singing induces opioid receptor and enkephalin expression in the POM and consequent reward, and/or that opioid release in the POM induced by individual or environmental factors (e.g., the presence of food, safety of a flock or the absence of predators) induces a positive affective state which then facilitates singing behavior.

Kloss gibbon (Hylobates klossii) behavior facilitates the avoidance of human predation in the Peleonan forest, Siberut Island, Indonesia.

Kloss gibbons (Hylobates klossii) are endemic to the Mentawai Islands in Indonesia and have been subject to human predation for more than 2000 years in the absence of any other significant predators. We investigate the behavior of Kloss gibbons that may be attributed to avoiding human predation. We observed Kloss gibbons in the Peleonan forest in the north of Siberut Island, the northernmost of the Mentawai island chain, over 18 months in 2007 and 2008, and collected data on their singing behavior, the number of individuals present during different conditions and their responses to humans. We examine behaviors that may reduce the risk of predation by humans during singing (the most conspicuous gibbon behavior), daily non-singing activities and encounters with humans. The individual risk of being stalked by hunters is reduced by singing in same-sex choruses and the risk of successful capture by hunters during singing is reduced by singing less often during daylight hours and by leaving the location of male pre-dawn singing before full light (reducing the visual signal to hunters). Groups in the Peleonan also fission during non-singing daily activity and rarely engage in play or grooming, enhancing the crypticity of their monochromatic black pelage in the canopy. We also observed a coordinated response to the presence of humans, wherein one adult individual acted as a "decoy" by approaching and distracting human observers, while other group members fled silently in multiple directions. "Decoy" behavior occurred on 31% of 96 encounters with unhabituated Kloss gibbons that detected our presence. "Decoy" individuals may put themselves at risk to increase the survival of related immatures (and adult females with infants) who have a greater risk of predation. We argue that, in combination, these behaviors are an evolved response to a long history of predation by humans.

Singing and social inclusion.

There is a growing body of neurological, cognitive, and social psychological research to suggest the possibility of positive transfer effects from structured musical engagement. In particular, there is evidence to suggest that engagement in musical activities may impact on social inclusion (sense of self and of being socially integrated). Tackling social exclusion and promoting social inclusion are common concerns internationally, such as in the UK and the EC, and there are many diverse Government ministries and agencies globally that see the arts in general and music in particular as a key means by which social needs can be addressed. As part of a wider evaluation of a national, Government-sponsored music education initiative for Primary-aged children in England (“Sing Up”), opportunity was taken by the authors, at the request of the funders, to assess any possible relationship between (a) children's developing singing behavior and development and (b) their social inclusion (sense of self and of being socially integrated). Subsequently, it was possible to match data from n = 6087 participants, drawn from the final 3 years of data collection (2008–2011), in terms of each child's individually assessed singing ability (based on their singing behavior of two well-known songs to create a “normalized singing score”) and their written responses to a specially-designed questionnaire that included a set of statements related to children's sense of being socially included to which the children indicated their level of agreement on a seven-point Likert scale. Data analyses suggested that the higher the normalized singing development rating, the more positive the child's self-concept and sense of being socially included, irrespective of singer age, sex and ethnicity.

Sound Spectrum Characteristics of Songs of Hainan Gibbon (Nomascus hainanus)

Gibbons are characterized by their species-specific calls, or songs. There are few studies of songs of Hainan gibbon (Nomascus hainanus). To study the sound spectrum characteristics and test for intergroup differences in Hainan gibbon song, we studied the singing behavior of Hainan gibbons in Bawangling National Nature Reserve, Hainan Province, China, intermittently from August 2002 to February 2013, collecting 184 recordings. Our results show that: 1) Hainan gibbon song bouts occur mainly 0–4 h after dawn. 2) The songs of adult males living in groups are composed mainly of one to three short notes and one to five long notes, while solitary adult male songs consist only of long frequency modulated notes and no short or single notes. 3) The song chorus is dominated by adult males, while females add a great call. Males do not have a great call, unlike those in other gibbon species. There are no female solos. 4) The sound spectrum frequency is similar in adult males living in two different groups, but the duration of the first long note differed significantly between the groups. The sonic frequencies of male and female songs are lower than those of other gibbons: no more than 2 kHz. Hainan gibbon sound structure is simple, although females participate in the chorus, reflecting their primitive status among gibbon species.

White-throated sparrows alter songs differentially in response to chorusing anurans and other background noise

Animals can use acoustic signals to attract mates and defend territories. As a consequence, background noise that interferes with signal transmission has the potential to reduce fitness, especially in birds that rely on song. While much research on bird song has investigated vocal flexibility in response to urban noise, weather and other birds, the possibility of inter-class acoustic competition from anurans has not been previously studied. Using sound recordings from central Ontario wetlands, we tested if white-throated sparrows (Zonotrichia albicolis) make short-term changes to their singing behaviour in response to chorusing spring peepers (Pseudacris crucifer), as well as to car noise, wind and other bird vocalizations. White-throated sparrow songs that were sung during the spring peeper chorus were shorter with higher minimum frequencies and narrower bandwidths resulting in reduced frequency overlap. Additionally, sparrows were less likely to sing when car noise and the vocalizations of other birds were present. These patterns suggest that birds use multiple adjustment strategies. This is the first report to demonstrate that birds may alter their songs differentially in response to different sources of noise.This article is part of a Special Issue entitled: insert SI title.

Hormonal regulation of vasotocin receptor mRNA in a seasonally breeding songbird

Behaviors associated with breeding are seasonally modulated in a variety of species. These changes in behavior are mediated by sex steroids, levels of which likewise vary with season. The effects of androgens on behaviors associated with breeding may in turn be partly mediated by the nonapeptides vasopressin (VP) and oxytocin (OT) in mammals, and vasotocin (VT) in birds. The effects of testosterone (T) on production of these neuropeptides have been well-studied; however, the regulation of VT receptors by T is not well understood. In this study, we investigated steroid-dependent regulation of VT receptor (VTR) mRNA in a seasonally breeding songbird, the white-throated sparrow (Zonotrichia albicollis). We focused on VTR subtypes that have been most strongly implicated in social behavior: V1a and oxytocin-like receptor (OTR). Using in situ hybridization, we show that T-treatment of non-breeding males altered V1a and OTR mRNA expression in several regions associated with seasonal reproductive behaviors. For example, T-treatment increased V1a mRNA expression in the medial preoptic area, bed nucleus of the stria terminalis, and ventromedial hypothalamus. T-treatment also affected both V1a and OTR mRNA expression in nuclei of the song system; some of these effects depended on the presence or absence of a chromosomal rearrangement that affects singing behavior, plasma T, and VT immunolabeling in this species. Overall, our results strengthen evidence that VT helps mediate the behavioral effects of T in songbirds, and suggest that the chromosomal rearrangement in this species may affect the sensitivity of the VT system to seasonal changes in T.

Factors Associated With Singers' Perceptions of Choral Singing Well-Being

Choral singing is a popular vocational pastime across cultures. The potential health benefits associated with choral singing, including positive effect on well-being, are a topic of interest in health research. However, anecdotal reports from voice professionals suggest that the unique demands of choral singing may enforce unhealthy singing habits. This study explores suboptimal vocal behaviors that are sometimes associated with choral singing, which include singing outside comfortable pitch range, singing too loudly, and singing too softly for blend. The relationships between suboptimal choral singing habits, vocal warm-ups (WUs), vocal fatigue, and singing-related well-being were assessed via a 14-item Likert-based response format questionnaire. Participants consisted of 196 attendees of the international World Choir Games. The final study group consisted of 53 male and 143 female international amateur singers aged 10-70. Results indicated a positive correlation between vocal fatigue and suboptimal singing behaviors (r = 0.34, P < 0.0001). Participants who did not engage in suboptimal singing behavior experienced increased singing-related well-being (r = -0.32, P < 0.0001, N = 141). Vocal WUs were not related to vocal fatigue or singing well-being. Substantially, more participants from this demographic preferred choir over solo singing (X²[1, N = 196] = 22.93, P < 0.0001). Suboptimal choral singing behaviors may result in vocal fatigue and reduction of choral singing well-being and should therefore be considered when examining the effect of choral singing on singing-related well-being and health. Future research will compare the amateurs' perceptions of choral singing with perceptions from professional singers and will look at determinants of choral singing well-being.

How a songbird with a continuous singing style modulates its song when territorially challenged.

In songbirds of the temperate zone, often only males sing and their songs serve to attract females and to deter territorial rivals. In many species, males vary certain aspects of their singing behavior when engaged in territorial interactions. Such variation may be an honest signal of the traits of the signaler, such as fighting strength, condition, or aggressive motivation, and may be used by receivers in decisions on whether to retreat or to escalate a fight. This has been studied intensively in species that sing discontinuously, in which songs are alternating with silent pauses. We studied contextual variation in the song of skylarks (Alauda arvensis), a songbird with a large vocal repertoire and a continuous and versatile singing style. We exposed subjects to simulated territorial intrusions by broadcasting conspecific song and recorded their vocal responses. We found that males sing differently if they are singing spontaneously with no other conspecific around than if they are territorially challenged. In this last case, males produced lower-frequency syllables. Furthermore, they increased the sound density of their song: they increased the proportion of sound within song. They seem to do so by singing different elements of their repertoire when singing reactively. Furthermore, they increased the consistency of mean peak frequency: they repeated syllable types with less variability when singing reactively. Such contextual variation suggests that skylarks might use low frequencies, sound density, and song consistency to indicate their competitive potential, and thus, those song features might be important for mutual assessment of competitive abilities.

Interspecific song imitation by a Prairie Warbler

Song development in oscine songbirds relies on imitation of adult singers and thus leaves developing birds vulnerable to potentially costly errors caused by imitation of inappropriate models, such as the songs of other species. In May and June 2012, we recorded the songs of a bird that made such an error: a male Prairie Warbler (Setophaga discolor) in western Massachusetts that sang songs seemingly acquired by imitating the songs of a Field Sparrow (Spizella pusilla). Another song type in the bird's repertoire was a near-normal Group A Prairie Warbler song, but the bird used this song in contexts normally reserved for Group B songs. Despite its abnormal singing behavior, the aberrant bird successfully defended a territory and attracted a mate that laid two clutches of eggs. Results of playbacks of the focal bird's heterospecific song suggested that neighboring conspecific males learned to associate the Field Sparrow-like song with the focal male, and responded to the song as if it were a Prairie Warbler song. Our evidence suggests that the focal bird's aberrant singing evoked normal responses from potential mates and rivals. If such responses are widespread among songbirds, the general failure of heterospecific songs, once acquired, to spread through populations by cultural transmission is probably not attributable to a lack of recognition by conspecifics of the songs of heterospecific singers.

Robust autumn social attributes predict spring courtship skills in juvenile female brown-headed cowbirds, Molothrus ater

Individuals often show predictable variation in social tendencies over time and across contexts. In species that rely on social interaction for the development of courtship behaviours, predictable variation in juvenile social behaviour may influence the ontogeny of courtship skills by exposing young individuals to different levels of contact with conspecifics. During the autumn and winter, brown-headed cowbirds utilize a social display known as the head-down to facilitate close social interaction with others. In this study we investigated whether head-downs rates are correlated across social contexts, and thus constitute a social temperament trait, and whether variation in head-down rates predicts subsequent courtship behaviour in juvenile cowbirds. During the autumn, we used a fission–fusion perturbation on a flock of juvenile females and males, and recorded the number of approaches and head-downs across social contexts. All individuals were then followed into the breeding season, where we recorded male singing behaviour, female chatter vocalization and consort status. We found that female head-down rates were correlated across contexts during the autumn, and that females that engaged in more head-down displays received more songs from males, responded to more songs with chatter vocalizations and were more likely to be in a consortship during the breeding season. As far as we know, this study presents the first demonstration that a social temperament trait can predict competent adult-like courtship behaviour in juvenile birds, and suggests that juvenile sociability may be an important developmental mechanism in the emergence of reproductive competence. ► We observed a flock of juvenile brown-headed cowbirds during autumn and spring of their first year. ► In autumn, we performed a fission–fusion flock perturbation to examine social behaviour across contexts. ► Females showed correlated rates of affiliative head-down displays across social contexts in autumn. ► Autumn head-down rates predicted spring courtship skills in females. ► Individual social attributes may shape the development of courtship skills in female birds.

Eavesdropping parasitoids do not cause the evolution of less conspicuous signalling behaviour in a field cricket

Males of many species produce conspicuous mating signals to attract females, but these signals can also attract eavesdropping predators and parasites. Males are thus expected to evolve signalling behaviours that balance the sexual selection benefits and the natural selection costs. In the variable field cricket, Gryllus lineaticeps, males sing to attract females, but these songs also attract the lethal parasitoid fly Ormia ochracea. The flies use male crickets as hosts for their larvae, primarily search for hosts during a 2 h period following sunset and prefer the same song types as female crickets. We tested whether males from high-risk populations reduce the risk of parasitism by singing less frequently or by shifting their singing activity to a time of the night when the risk of parasitism is low. We compared male singing activity and its temporal pattern between six high-risk and six low-risk populations that were reared in a common environment. There was no effect of parasitism risk on either total male singing activity or the temporal pattern of male singing activity. Males from high-risk populations thus sang as frequently as males from low-risk populations. These results suggest that sexual selection on male singing behaviour may be substantially stronger in high-risk populations than in low-risk populations. It is possible that other traits may have evolved to reduce parasitism risk without compromising mate attraction.

Effects of Population Size on Singing Behavior of a Rare Duetting Songbird

Although the genetic and ecological effects of population declines in endangered species have been well studied, little is known of the social consequences. Changes in signaling behavior may result in disrupted communication and affect both reproductive and conflict-resolution activities. The North Island Kōkako (Callaeas wilsoni) is an endangered, duetting (i.e., alternating, coordinated singing by mated pairs) songbird endemic to New Zealand temperate rain forests. Scattered populations (approximately 1500 individuals in 13 surviving and 11 translocated populations) in isolated conservation areas of different sizes have been rescued from extirpation and are currently recovering. We examined key song attributes of the Kōkako to assess whether population size or growth rate are related to song complexity, the reduction of which may compromise effective communication. We analyzed song repertoire size and phrase-type sharing (i.e., Jaccard index of similarity), vocal performance (singing rates, song switching rates, and diversity of phrase types), and song syntactical characteristics (i.e., unpredictability in sequences of phrase types) in surviving and translocated populations (populations of approximately 19-250 territorial individuals). Population size was positively correlated with a population's song repertoire, song diversity, and switching of song phrase types and negatively correlated with shared phrase types and variation in syntactical structure of songs. Population growth rate correlated positively with pair repertoire size, population repertoire size, and singing rates during song bouts. As for solo-singing species in fragmented landscapes, songs in the fragmented populations of Kōkako appear to be undergoing microevolution as occurs in island colonization events. Our results suggest that vocal changes in small populations could affect population establishment and growth, particularly in multiple-source translocations. We believe measurement of vocal behavior could be used as a supplement to periodic population censuses to allow more frequent monitoring of population size.