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.     

Temporal precision and temporal drift in brain and behavior of zebra finch song.

In the zebra finch forebrain nucleus robustus archistriatalis (RA), neurons burst during singing. We showed that the internal structure of spike bursts was regulated with a precision of circa 0.2 ms, and yielded alignment of acoustic features of song with a precision of circa 1 ms. In addition, interburst intervals and corresponding syllable durations displayed systematic variation within song (average elongation 0.3 ms/s song), and slower "drift" across songs. Systematic variation on even a coarser time scale might be difficult to detect in other systems, but could affect the analysis of temporal patterning. The close relationship between precise timing of individual spikes and stereotypic behavior suggests that song is represented in RA by a temporal code.     

Rufous‐capped Warblers Basileuterus rufifrons show seasonal,temporal and annual variation in song use

In the majority of songbird species, males have repertoires of multiple song types used for mate attraction and territory defence. The wood‐warblers (family Parulidae) are a diverse family of songbirds in which males of many migratory species use different song types or patterns of song delivery (known as ‘singing modes’) depending on context. The vocal behaviour of most tropical resident warblers remains undescribed, although these species differ ecologically and behaviourally from migratory species, and may therefore differ in their vocal behaviour. We test whether male Rufous‐capped Warblers Basileuterus rufifrons use distinct singing modes by examining song structure and context‐dependent variation in their songs. We recorded multiple song bouts from 50 male Warblers in a Costa Rican population over 3 years to describe seasonal, diel and annual variation in song structure and vocal behaviour. We found that Rufous‐capped Warbler songs are complex, with many syllable types shared both within and between males’ repertoires. Males varied their song output depending on context: they sang long songs at a high rate at dawn and during the breeding season, and shortened songs in the presence of a vocalizing female mate. Unlike many migratory species, Rufous‐capped Warblers do not appear to have different singing modes; they did not change the song variants used or the pattern of song delivery according to time of day, season or female vocal activity. Our research provides the first detailed vocal analysis of any Basileuterus warbler species, and enhances our understanding of the evolution of repertoire specialization in tropical resident songbirds.     

Song environment affects singing effort and vasotocin immunoreactivity in the forebrain of male Lincoln's sparrows

Male songbirds often establish territories and attract mates by singing, and some song features can reflect the singer's condition or quality. The quality of the song environment can change, so male songbirds should benefit from assessing the competitiveness of the song environment and appropriately adjusting their own singing behavior and the neural substrates by which song is controlled. In a wide range of taxa, social modulation of behavior is partly mediated by the arginine vasopressin or vasotocin (AVP/AVT) systems. To examine the modulation of singing behavior in response to the quality of the song environment, we compared the song output of laboratory-housed male Lincoln's sparrows (Melospiza lincolnii) exposed to 1 week of chronic playback of songs categorized as either high or low quality, based on song length, complexity, and trill performance. To explore the neural basis of any facultative shifts in behavior, we also quantified the subjects' AVT immunoreactivity (AVT-IR) in three forebrain regions that regulate sociosexual behavior: the medial bed nucleus of the stria terminalis (BSTm), the lateral septum (LS), and the preoptic area. We found that high-quality songs increased singing effort and reduced AVT-IR in the BSTm and LS, relative to low-quality songs. The effect of the quality of the song environment on both singing effort and forebrain AVT-IR raises the hypothesis that AVT within these brain regions plays a role in the modulation of behavior in response to competition that individual males may assess from the prevailing song environment.     

Male response to historical and geographical variation in bird song

In many species, individuals discriminate among sexual signals of conspecific populations in the contexts of mate choice and male–male competition. Differences in signals among populations (geographical variation) are in part the result of signal evolution within populations (temporal variation). Understanding the relative effect of temporal and geographical signal variation on signal salience may therefore provide insight into the evolution of behavioural discrimination. However, no study, to my knowledge, has compared behavioural response to historical signals with response to current signal variation among populations. Here, I measured the response of male white-crowned sparrows (Zonotrichia leucophrys) to historical songs compared with current songs from their local population, a nearby non-local population and a distant population. Males responded most strongly to current local songs, less, but equally, to historical local and current non-local songs, and least to songs of the distant population. Moreover, response to both temporal and geographical variation in song was proportional to how much songs differed acoustically from current local songs. Signal evolution on an ecological time scale appears to have an effect on signal salience comparable to differences found between current neighbouring populations, supporting the idea that behavioural discrimination among learned signals of conspecific populations can evolve relatively rapidly.     

Variation in Vocal Performance in the Songs of a Wood-Warbler: Evidence for the Function of Distinct Singing Modes

Male North American wood‐warblers (family Parulidae) subdivide their song repertoires into two different categories, or modes, of singing (first and second category songs). These two modes are thought to be specialized for interacting with females and males, although the data are inconclusive. I conducted an acoustic analysis of the song types used by yellow warblers (Dendroica petechia) for type I (first category) and type II (second category) singing to ask whether there are consistent structural differences between them which could provide insight into how they might function as separate signals. I found that type I songs are performed closer to the upper boundary of a song performance limit, measured in terms of the difficulty of production, compared with type II songs. By contrast, the performance of specific song types did not depend on whether they were used for type I singing vs. type II singing by different males. In addition, type I songs had a greater amplitude increase across the first two syllables compared with type II songs. There was no relationship between the performance of type I or type II songs and male condition. These results suggest that wood‐warblers might subdivide their song repertoire into distinct categories to highlight the relative vocal performance of their songs.     

Intraspecific Social Stimulation and Temporal Displacement of Songs of the Lesser Skylark,Alauda gulgula

Temporal patterning of flight song activity was examined in a population of Lesser Skylarks in Viet Nam. Onset and termination of songs were timed. Temporal dispersion of songs was analyzed from the distribution of intersong intervals, and the tendency of songs to be started prior to, shortly after, or long after cessation of a neighbor's song was examined. Skylarks tended to sing sequentially, clustering their songs in time after long periods of silence. However, they showed a strong tendency to avoid overlapping songs, perhaps because of the possibility of jamming by songs of neighbors. These two factors, intraspecific social stimulation and temporal avoidance, appear to be important determinants of singing behavior in this species.     

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.     

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.     

Persistence of song types in Darwin's finches,Geospiza fortis,over four decades

Learned bird songs evolve via cultural evolution, with song patterns transmitted across generations by imitative learning. In Darwin''s finches of the Galápagos Islands, males learn songs from their fathers, and song types can be maintained across multiple generations. However, little is known about the time frame over which specific song types are preserved, in the face of copy errors and corresponding modifications to song structure. Here we investigate cultural evolution in songs of male Geospiza fortis, at Academy Bay, Santa Cruz Island, comparing songs recorded in 1961 by R. Bowman (20 individuals) to those recorded in 1999 by J. Podos (16 individuals). For each individual, we characterized four timing and six frequency parameters, and assessed inter-individual variation in song structure using multivariate analysis. Several 1961 song types persisted into 1999, some with remarkable fidelity. Variation among song types was extensive during both years, and we detected no changes in 10 vocal parameters across the sampling period. These results illustrate temporal continuity in a culturally acquired trait, and raise questions about mechanisms that promote stability in song structure.     

Individual Distinctiveness in the Fine Structural Features and Repertoire Characteristics of the Songs of White‐eared Ground‐sparrows

Communication between social animals is often more effective when signals facilitate individual recognition. Two critical requirements for individual recognition are the occurrence of characteristics that are unique to each individual, and the consistency of these characteristics through time. In some animals, characteristics of acoustic signals are known to vary over time due to changes in a variety of factors, including physiological and environmental features. Such temporal variation requires careful evaluation when exploring the individual distinctiveness of animal signals. In this study, we evaluate individual distinctiveness in the songs of male white‐eared ground‐sparrows Melozone leucotis and the persistence of distinctive characteristics over time. We collected focal recordings from populations of banded ground‐sparrows during two consecutive breeding seasons, including multiple recording sessions within each breeding season. We evaluated individual distinctiveness in fine structural acoustic features of songs. We also extended our analysis to repertoire characteristics, focusing on whether the relative frequency of song type use may provide cues to individual identity. We found that each male white‐eared ground‐sparrow sang individually distinctive songs, although their fine structural features varied between recording sessions. We found the frequency with which males sang different song types was also individually distinctive, and this feature varied little between recording sessions. Receivers may be able to use these distinctive characteristics to differentiate individuals over extended time periods; this may be especially important for species that engage in long‐term social interactions, such as tropical birds that defend territories against rival conspecific animals throughout the year.     

No Correlation Between Three Selected Trade‐Offs in Birdsong Performance and Male Quality for a Species With Song Repertoires

Demanding performance of vocal signals, such as birdsong, may be evaluated by trade‐offs among acoustic traits. If individuals differ in their ability to sustain physiologically demanding singing, then aspects of song performance resulting from such trade‐offs could signal individual quality. Song performance can also differ among song types, and it is not known whether this influences the assessment of individual quality. We asked whether three trade‐off‐based measures of song performance indicate male age or aspects of condition (body condition, hematocrit and ectoparasite load) in the dark‐eyed junco (Junco hyemalis), a species with small repertoires. Across a sample of over 100 males, no measure of song performance was related to male age or condition, nor did song performance improve with age for those males recorded in consecutive years. In all cases, the variation in song performance explained by these predictors was small (<4%). Instead, the more song types we recorded from a male, the more likely we were to record high‐performance songs, and this sampling effect was stronger than putative correlations with male quality. These results complement a previous study on this population showing that most variation in performance is found among song types rather than among males. Collectively, the lack of association between trade‐off‐based aspects of song performance and male age or condition, plus variation among song types that interferes with rapid assessment of a male's best performance, indicate that these aspects of song performance do not allow a good assessment of male quality in juncos, and perhaps more generally in species with song repertoires.     

Temporal Aspects of Singing Interactions among Territorial Ovenbirds (Seiurus aurocapillus)

The temporal aspects of singing interactions among birds have received relatively little attention. To determine if the song delivery of one individual is affected by that of its territorial neighbor, I recorded singing interactions between territorial ovenbirds (Seiurus aurocapillus). Ovenbirds appeared to adopt one of two roles during singing interactions, Type I or Type II singers. Type II singers placed more of their songs immediately after the song of their neighbor than expected. The singing pattern of Type I singers could not be distinguished from a random pattern with respect to their neighbor's songs. In each observed pair of interacting birds, one individual was a Type I singer and one was a Type II singer. Although there was some intra-individual variation, most birds maintained the same role with each of their recorded territorial neighbors. Variation occurred between the two study sites in the extent that individuals overlapped the songs of their neighbors. Song overlap was common at one site, but occurred as, or less, often than expected at the other site.     

Sexually dimorphic phrase organization in the song of the indris (Indri indri)

Animal acoustic communication often takes the form of complex sequences, composed of multiple distinct acoustic units, which can vary in their degree of stereotypy. Studies of sequence variation may contribute to our understanding of the structural flexibility of primates' songs, which can provide essential ecological and behavioral information about variability at the individual, population, and specific level and provide insights into the mechanisms and drivers responsible for the evolutionary change of communicative traits. Several methods have been used for investigating different levels of structural information and sequence similarity in acoustic displays. We studied intra and interindividual variation in the song structuring of a singing primate, the indri (Indri indri), which inhabits the montane rain forests of Madagascar. Indri groups emit duets and choruses in which they combine long notes, short single units, and phrases consisting of a variable number of units (from two to six) with slightly descending frequency. Males' and females' contributions to the song differ in the temporal and frequency structure of song units and repertoire size. We calculated the similarity of phrase organization across different individual contributions using the Levenshtein distance, a logic distance that expressed the minimum cost to convert a sequence into another and can measure differences between two sequences of data. We then analyzed the degree of similarity within and between individuals and found that: (a) the phrase structure of songs varied between reproductive males and females: female structuring of the song showed a higher number of phrases if compared to males; (b) male contributions to the song were overall more similar to those of other males than were female contributions to the song of other females; (c) male contributions were more stereotyped than female contributions, which showed greater individual flexibility. The picture emerging from phrase combinatorics in the indris is in agreement with previous findings of rhythmic features and song repertoire size of the indris, which also suggested that female songs are potentially less stereotyped than those of males.     

Versatility and Stereotypy of Free-Tailed Bat Songs

In mammals, complex songs are uncommon and few studies have examined song composition or the order of elements in songs, particularly with respect to regional and individual variation. In this study we examine how syllables and phrases are ordered and combined, ie “syntax”, of the song of Tadarida brasiliensis, the Brazilian free-tailed bat. Specifically, we test whether phrase and song composition differ among individuals and between two regions, we determine variability across renditions within individuals, and test whether phrases are randomly ordered and combined. We report three major findings. First, song phrases were highly stereotyped across two regions, so much so that some songs from the two colonies were almost indistinguishable. All males produced songs with the same four types of syllables and the same three types of phrases. Second, we found that although song construction was similar across regions, the number of syllables within phrases, and the number and order of phrases in songs varied greatly within and among individuals. Last, we determined that phrase order, although diverse, deviated from random models. We found broad scale phrase-order rules and certain higher order combinations that were highly preferred. We conclude that free-tailed bat songs are composed of highly stereotyped phrases hierarchically organized by a common set of syntactical rules. However, within global species-specific patterns, songs male free-tailed bats dynamically vary syllable number, phrase order, and phrase repetitions across song renditions.     

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.     

Singing Activity Reveals Personality Traits in Great Tits

In animal communication, sexually selected signals have been shown to often signal individual attributes such as motivation or quality. Birdsong is among the best studied signalling systems, and song traits vary substantially among individuals. The question remains if variation in signalling also reflects more general and consistent individual characteristics. Such consistent individual differences in behaviour that are relatively stable over time and contexts are referred to as personality or behavioural syndromes. Here, we studied the relation between singing and explorative behaviour, a well‐studied personality trait, using great tits (Parus major) under standardized aviary conditions. The results show that singing activity measured as the number of songs sung in spring prior to breeding correlated with male but not with female explorative behaviour. In contrast, song repertoire was not related to explorative behaviour but varied over the day. The link between explorative and singing behaviour suggests that sexually selected signals are more than signals of quality but can also reflect other intrinsic behavioural characteristics such as personality traits.