Song correlates with social context,testosterone and body condition in male barn swallows

Bird song, like many other male secondary sexual characters, may have evolved as intra- or inter-sexual signals of male phenotypic quality. The hypotheses that song rate and song features reflect androgen levels and body condition, qualities useful in male–male competition, and that they are also influenced by social context, was tested for the first time in the present correlational study. The relationships between song rate and 14 variables describing song structure, respectively, and absolute plasma testosterone levels, body mass, body condition, number of neighbouring males and distances between nest sites in male barn swallows,Hirundo rustica, were analysed. Song rate was not correlated with any of the song features nor with male or social context characteristics. By contrast, a harsh song syllable, the ‘rattle’, was positively related to plasma testosterone levels, and its peak amplitude frequency varied inversely with male body mass and condition. In addition, eight features of song varied according to the social environment of each male. In particular, males sang longer and more varied songs when they had few or no neighbours, whereas males in highly competitive contexts uttered short songs, interrupted them more frequently, and emphasized the rattle. Neighbouring males also sang more similar songs than distant males, and this resulted in matched countersinging. The quality of song output therefore reflects aspects of male competitive potential, and relationships between song structure and social context suggest that some features, such as the rattle, might have originally evolved to serve in male–male interactions; a female preference may have further promoted song evolution leading to complex syllable repertoires.     

Immune challenge mediates vocal communication in a passerine bird: an experiment

Secondary sexual characters may have evolved in part to signalresistance to parasites. Avian song has been hypothesized tobe involved in this process, but the role of parasites in modulatingacoustic communication systems in birds remains largely unknown,owing to lack of experiments. We studied the relationship betweenparasitism, testosterone, song performance, and mating successin male collared flycatchers (Ficedula albicollis) by experimentallychallenging their immune system with a novel antigen. We predictedthat a challenge of the immune system would reduce song performance,and that this reduction would be conditional on the size ofa visual sexual signal, the forehead patch that was previouslyfound to reflect resistance. An antagonistic linkage betweentestosterone and immune function would predict that a challengeof the immune system should suppress testosterone level. Animmunological treatment by sheep red blood cells (SRBCs) triggereda decrease in body mass, testosterone level, and song rate,but other song traits were not significantly affected by theantigen challenge. Initial testosterone level was associatedwith forehead patch size and all song traits except song rate.SRBC injection caused stronger reduction in song rate amongmales with smaller forehead patches, and the change in songrate was also predictable by song features such as strophe complexityand length. We show that song rate and other song characteristicsmay be important cues in male-male competition and female choice.These results suggest that parasite-mediated sexual selectionhas contributed in shaping a complex acoustic communicationsystem in the collared flycatcher, and that testosterone mayplay an important role in this process. Parasitism may drivea multiple signaling mechanism involving acoustic and visualtraits with different signal function.     

Sons learn songs from their social fathers in a cooperatively breeding bird

Song learning is hypothesized to allow social adaptation to a local song neighbourhood. Maintaining social associations is particularly important in cooperative breeders, yet vocal learning in such species has only been assessed in systems where social association was correlated with relatedness. Thus, benefits of vocal learning as a means of maintaining social associations could not be disentangled from benefits of kin recognition. We assessed genetic and cultural contributions to song in a species where social association was not strongly correlated with kinship: the cooperatively breeding, reproductively promiscuous splendid fairy-wren (Malurus splendens). We found that song characters of socially associated father-son pairs were more strongly correlated (and thus songs were more similar) than songs of father-son pairs with a genetic, but no social, association (i.e. cuckolding fathers). Song transmission was, therefore, vertical and cultural, with minimal signatures of kinship. Additionally, song characters were not correlated with several phenotypic indicators of male quality, supporting the idea that there may be a tradeoff between accurate copying of tutors and quality signalling via maximizing song performance, particularly when social and genetic relationships are decoupled. Our results lend support to the hypothesis that song learning facilitates the maintenance of social associations by permitting unrelated individuals to acquire similar signal phenotypes.     

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.     

Conveying information with one song type: changes in dawn song performance correspond to different female breeding stages

Many bird species participate in dawn singing, a behaviour categorized by intensive singing at dawn; however, many of these species deliver only one song type at dawn. While there are many proximate and ultimate hypotheses for why birds sing at dawn, little is known about whether males are able to vary one simple song to convey different information. We used autonomous acoustic recorders to record dawn songs of field sparrows and quantified three parameters of singing performance: 1) bout length, 2) song rate, and 3) song complexity. We found that males sang the longest dawn bouts during their mate's fertile period, the highest song rates during the post-fertile period, and the most complex songs during the pre-fertile period. The change in dawn singing behaviour with their mate's breeding stage suggest the purpose of dawn song may be context dependent. Our results demonstrate that male field sparrows, while only having a single song type sung at dawn, may convey information for both intra- and intersexual purposes. While it is generally assumed that dawn song has a specific function, the variability in the duration, rate, and complexity of dawn song in field sparrows suggests that they are conveying different information and that dawn song likely has multiple functions.     

Condition-dependent traits and the capture of genetic variance in male advertisement song

The occurrence of additive genetic variance (VA) for male sexual traits remains a major problem in evolutionary biology. Directional selection normally imposed by female choice is expected to reduce VA greatly, yet recent surveys indicate that a substantial amount remains in many species. We addressed this problem, also known as the 'lek paradox', in Achroia grisella (Lepidoptera: Pyralidae), an acoustic moth in which males advertise to females with a pulsed ultrasonic song. Using a standard half-sib/full-sib breeding design, we generated F1 progeny from whom we determined VA and genetic covariance (COVA) among seven traits: three song characters, an overall index of song attractiveness, nightly singing period, adult lifespan, and body mass at adult eclosion. Because A. grisella neither feed nor drink as adults, the last trait, eclosion body mass, is considered a measure of 'condition'. We found significant levels of VA and narrow-sense heritabilities (h2) for all seven traits and significant genetic correlations (= COVAi,j / radical (VA i x VA j)) between most pairs of traits (i, j). Male attractiveness was positively correlated with body mass (condition), adult lifespan, and nightly singing period, which we interpret as an energy constraint preventing males in poor condition from singing attractively, from singing many hours per night, and from surviving an extended lifespan. The positive genetic correlation (r = 0.79) between condition and attractiveness, combined with significant levels of VA for both traits, indicates that much of the variation in male song can be explained by VA for condition. Finally, we discuss the morphological and physiological links between condition and song attractiveness, and the ultimate factors that may maintain VA for condition.     

Honest advertisement and song output during the dawn chorus of black-capped chickadees

Costly signals can evolve under sexual selection, as only thosesignals that are difficult to produce and reflect the relativequality of individuals should be important in mate choice. Onesuch signal may be dawn singing behavior in birds. We assessedwhether the song output at dawn of breeding male black-cappedchickadees Parus atricapilhis honestly reflects quality, whererelative quality is assessed by relative dominance rank in winterflocks. Dawn choruses were recorded from 20 male chickadeesfrom 10 flocks during the fertile period of their mates in 1992,1994, and 1995. Dominance ranks of males were assessed by tabulatinginteractions at winter feeders from 1993 to 1995. A comparisonof the dawn singing behavior of the high-ranking and the low-rankingmales from each of the 10 flocks showed that high-ranking malesbegan singing earlier, sang longer, and sang at higher averageand maximum rates than low-ranking flockmates. Age of the maleshad less effect on song output at dawn than rank; older malestended to sing longer dawn choruses, but there was no differencein onset of singing, average song rate, or maximum song rateat dawn between hatch year and after-hatch year males. Our findingssuggest the dawn chorus can provide an accurate signal to femalesof the relative quality of their mate compared to neighboringmales     

Song repertoire size varies with HVC volume and is indicative of male quality in song sparrows (Melospiza melodia)

Complex birdsong is a classic example of a sexually selected ornamental trait. In many species, females prefer males with large song repertoires, possibly because repertoire size is limited by the size of song control nuclei which reflect developmental success. We investigated whether song repertoire size was indicative of brain area and male quality in song sparrows (Melospiza melodia) by determining if repertoire size was related to the volume of song control nucleus HVC, as well as several morphological, immunological and genetic indices of quality. We found that males with large repertoires had larger HVCs and were in better body condition. They also had lower heterophil to lymphocyte ratios, indicating less physiological stress and a robust immune system as measured by the number of lymphocytes per red blood cell. Song repertoire size also tended to increase with neutral-locus genetic diversity, as assessed by mean d2, but was not related to internal relatedness. Our results suggest several mechanisms that might explain the finding of a recent study that song sparrows with large song repertoires have higher lifetime fitness.     

The song structure and seasonal patterns of vocal behavior of male and female bellbirds (Anthornis melanura)

The bellbird (Anthornis melanura) is a honeyeater endemic to New Zealand, which uses song to defend breeding territories and/or food resources year round. Both sexes sing and the song structure and singing behavior have not yet been quantified. The number of song types, spectral structure, repertoire size, and singing behavior of male and female bellbirds was investigated for a large island population. Song types differed between the sexes with males singing a number of structurally distinct song types and females producing song types that overlapped in structure. Singing behavior also differed between the sexes; males often sung long series of songs while females sung each song at relatively long and variable intervals. Singing by both sexes occurred year round but the frequency of male and female singing bouts showed contrasting seasonal patterns. The frequency of female singing bouts increased as the breeding season progressed, whereas male singing bouts decreased. In contrast to almost all studied passerines, female bellbirds exhibited significant singing behavior and sung songs of complex structure and variety that parallel male song. These results provide a quantitative foundation for further research of song in bellbirds and in particular the function of female vocal behavior.     

Duetting behavior in a Neotropical ovenbird: sexual and seasonal variation and adaptive signaling functions

Duetting is a collective behavior and might have multiple functions, including joint territory defense and mate guarding. An important step toward understanding the adaptive function of bird song is to determine if and how singing behavior varies seasonally. However, seasonal patterns for duetting species are different from the pattern described for species in which only the male sings, because song function may vary according to sex, singing role (initiator vs responder) and level of duet organization (individual vs pair). We investigated whether patterns of seasonal variation in duetting depends on these factors, which would suggest different interpretations of song function. We studied social pairs of a Neotropical bird species (rufous hornero Furnarius rufus) for seven consecutive months, recording vocal and territorial behaviors. Overall, partners coordinated 61% of their songs into duets and many song traits (song initiation rate, song output and duet rate) peaked in territorial contexts. Males engaged in territorial interactions with strangers more often, initiated more songs, and answered proportionately more of their partners’ songs than females. Male song initiation rate peaked during the pre‐ and post‐breeding stages, whereas females initiated more songs during the non‐breeding season. Both sexes answered partner songs faster and at higher rates during the pre‐breeding and female fertile stages. Partners duetted at a higher rate during the pre‐ and post‐breeding stages. Finally, song initiation rates and duet rate, but not song answering rates, correlated with frequency of territorial interactions with strangers. Although our findings indicate that song function may vary with sex, singing role and level of duet organization, our results suggest that in general duet functions to defend common territories and as a mutual mate guarding strategy in the rufous hornero.     

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

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

The blue tit's song is an inconsistent signal of male condition

Sexually selected traits are often hypothesized to signal malecondition or quality, though empirical evidence is mixed, anda number of alternative models of sexual selection do not requirecondition dependence. We examined the relationship between variousmeasures of condition and dawn songs in male blue tits (Cyanistescaeruleus). We detected 6 largely independent measures of variation(i.e., variables) in these songs. None of these variables wererelated to blue tits' ultraviolet–blue plumage, a demonstratedsexual signal, thus failing to support the redundant signalhypothesis. We found some evidence that the song variables wemeasured signaled male quality. There were correlations betweenbody size and certain song traits, though neither male age normale recapture in the subsequent breeding season (apparent localsurvival) predicted any song variation. We combined our resultswith published effect sizes comparing blue tit song with malequality variables using meta-analysis and found that a few songmeasures are correlates of male quality, though as in our fielddata, neither male age nor survival appeared related to song.Our relatively large sample sizes (>60), combined with ourmeta-analytical integration of 89 effect sizes, make the resultsregarding the signaling value of our measured components ofblue tit song robust. These results demonstrate that 1) onlycertain aspects of signal variation may be condition dependentand 2) even when components of a sexual signal appear correlatedwith condition in some studies, these signal components maybe unrelated or inconsistently related to a variety of conditionindices.     

Nonlocal male mountain white-crowned sparrows have lower paternity and higher parasite loads than males singing local dialect

Bird song often varies geographically, and when this geographicvariation has distinct boundaries, the shared song types arereferred to as song dialects. We investigated the role of songdialect in male mating success in a wild breeding populationof mountain white-crowned sparrows (Zonotrichia leucophrysoriantha). In 2 of 3 years, males singing unusual songs ("nonlocal"males) had lower total fertilization success (measured by microsatellitepaternity analysis) than did males singing the local dialect ("local" males). Similarly, females produced disproportionately more young with local than with nonlocal males. However, dialectwas not a significant predictor of male mating success whencontrolling for other factors that might affect paternity.Instead, the low mating success of nonlocal males was apparentlydue to an interaction between song dialect and parasite load.Nonlocal males were more severely infected by bloodborne Haemoproteusthan were local males, although they did not differ in anyother measured aspect of quality. Immigrant birds may be immunologically disadvantaged, possibly due to a lack of previous experiencewith the local parasite fauna, resulting in low mating success.     

The learning advantage: bird species that learn their song show a tighter adjustment of song to noisy environments than those that do not learn

Song learning has evolved within several avian groups. Although its evolutionary advantage is not clear, it has been proposed that song learning may be advantageous in allowing birds to adapt their songs to the local acoustic environment. To test this hypothesis, we analysed patterns of song adjustment to noisy environments and explored their possible link to song learning. Bird vocalizations can be masked by low‐frequency noise, and birds respond to this by singing higher‐pitched songs. Most reports of this strategy involve oscines, a group of birds with learning‐based song variability, and it is doubtful whether species that lack song learning (e.g. suboscines) can adjust their songs to noisy environments. We address this question by comparing the degree of song adjustment to noise in a large sample of oscines (17 populations, 14 species) and suboscines (11 populations, 7 species), recorded in Brazil (Manaus, Brasilia and Curitiba) and Mexico City. We found a significantly stronger association between minimum song frequency and noise levels (effect size) in oscines than in suboscines, suggesting a tighter match in oscines between song transmission capacity and ambient acoustics. Suboscines may be more vulnerable to acoustic pollution than oscines and thus less capable of colonizing cities or acoustically novel habitats. Additionally, we found that species whose song frequency was more divergent between populations showed tighter noise–song frequency associations. Our results suggest that song learning and/or song plasticity allows adaptation to new habitats and that this selective advantage may be linked to the evolution of song learning and plasticity.     

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.     

Social context affects testosterone‐induced singing and the volume of song control nuclei in male canaries (Serinus canaria)

The contribution of social factors to seasonal plasticity in singing behavior and forebrain nuclei controlling song, and their interplay with gonadal steroid hormones are still poorly understood. In many songbird species, testosterone (T) enhances singing behavior but elevated plasma T concentrations are not absolutely required for singing to occur. Singing is generally produced either to defend a territory or to attract a mate and it is therefore not surprising that singing rate can be influenced by the sex and behavior of the social partner. We investigated, based on two independent experiments, the effect of the presence of a male or female partner on the rate of song produced by male canaries. In the first experiment, song rate was measured in dyads composed of one male and one female (M‐F) or two males (M‐M). Birds were implanted with T‐filled Silastic capsules or with empty capsules as control. The number of complete song bouts produced by all males was recorded during 240 min on week 1, 2, 4, and 8 after implantation. On the day following each recording session, brains from approximately one‐fourth of the birds were collected and the volumes of the song control nuclei HVC and RA were measured. T increased the singing rate and volume of HVC and RA but these effects were affected by the social context. Singing rates were higher in the M‐M than in the M‐F dyads. Also, in the M‐M dyads a dominance‐subordination relationship soon became established and dominant males sang at higher rates than subordinates in T‐treated but not in control pairs. The differences in song production were not reflected in the size of the song control nuclei: HVC was larger in M‐F than in M‐M males and within the M‐M dyads, no difference in HVC or RA size could be detected between dominant and subordinate males. At the individual level, the song rate with was positively correlated with RA and to a lower degree HVC volume, but this relationship was observed only in M‐M dyads, specifically in dominant males. A second experiment, carried out with castrated males that were all treated with T and exposed either to another T‐treated castrate or to an estradiol‐implanted female, confirmed that song rate was higher in the M‐M than in the M‐F condition and that HVC volume was larger in heterosexual than in same‐sex dyads. The effects of T on singing rate and on the volume of the song control nuclei are thus modulated by the social environment, including the presence/absence of a potential mate and dominance status among males. 2006 Wiley Periodicals, Inc. J Neurobiol, 2006     

Vocal performance influences female response to male bird song: an experimental test

Female songbirds are thought to assess males based on aspectsof song, such as repertoire size or amount of singing, thatcould potentially provide information about male quality. Arelatively unexplored aspect of song that also might serve asan assessment signal is a male's ability to perform physicallychallenging songs. Trilled songs, such as those produced byswamp sparrows (Melospiza georgiana), present males with a performancechallenge because trills require rapid and precise coordinationof vocal tract movements, resulting in a trade-off between trillrate and frequency bandwidth. This trade-off defines a constrainton song production observed as a triangular distribution inacoustic space of trill rate by frequency bandwidth, with anupper boundary that represents a performance limit. Given thisbackground on song production constraints, we are able to identifya priori which songs are performed with a higher degree of proficiencyand, thus, which songs should be more attractive to females.We determined the performance limit for a population of swampsparrows and measured how well individual males performed songsrelative to this limit ("vocal performance"). We then comparedfemale solicitation responses to high-performance versus low-performanceversions of the same song type produced by different males.Females displayed significantly more to high-performance songsthan to low-performance songs, supporting the hypothesis thatfemales use vocal performance to assess males.     

Inferring performance in the songs of dark-eyed juncos (Junco hyemalis)

Within bird species, songs differ in their attractiveness tofemales or effectiveness in male–male interactions. Somesongs are more difficult to sing than others, and receiversmay use a singer's performance of difficult songs as a meansfor evaluating the quality of the singer. The concept of songperformance aims at quantifying how physiologically demandingare different songs. Using variation between song types of dark-eyedjuncos, Junco hyemalis, we show that some song traits tradeoff with costly aspects of song output—short intervalsbetween syllables or loud sound amplitude—suggesting thatthose traits are difficult to sing. First, after controllingfor other traits, long syllables require longer intervals forrecovery. This supports the idea that a measure of "respiratoryperformance" could be based on the relative lengths of syllablesand intervals. Second, some syllable traits trade off stronglywith sound amplitude, suggesting that these traits may be difficultto sing at high amplitudes. The ratio of frequency bandwidthand trill rate has been used to infer performance in other birdspecies, but we found no evidence that frequency bandwidth tradesoff with any aspect of song output in the junco. The negativeassociation of bandwidth with trill rate may instead be a passiveconsequence of syllable length, with longer syllables randomlyaccumulating frequency modulation. We conclude that bird receiversmay best evaluate how well a song is performed if they integratemultiple cues and discuss how researchers may similarly devisemeasures of song performance.     

Song and Male Quality in Prairie Warblers

To determine if the songs of male prairie warblers could potentially reveal to female listeners information about the quality of singers, we compared various aspects of prairie warbler song structure and performance to attributes that might reflect a male singer's potential to enhance the fitness of his mate. We found that all the tested male attributes—arrival date, age, body size, annual survival, and fledging success—were associated with singing, most with multiple aspects of singing. Several of the song traits that were associated with potential indicators of male quality had also been found previously to be good predictors of female social mate choice. In particular, longer songs with longer elements, performed at lower frequency and with greater consistency, were associated with both female mate choice and potential indicators of quality. Thus, female prairie warblers may assess potential mates with the help of a set of song characteristics that collectively reveal an array of attributes that together indicate overall male quality.     

Overlapping signals in banded wrens: long-term effects of prior experience on males and females

We tested the signal value of song overlapping in banded wrens(Thryothorus pleurostictus), using interactive playback to eitheroverlap or alternate with their songs. Males shortened songduration and decreased variability in song length when theirsongs were overlapped by playback, suggesting that they wereattempting to avoid being overlapped and perhaps being lessaggressive. A novel finding was an effect of long-term priorexperience: song lengths remained relatively short in alternatingtrials that followed two or more days after overlapping trials.Approach responses to the two treatments did not differ overall,but there was a parallel effect of prior experience: males tendedto stay further from the speaker during alternating treatmentsif they had previously been overlapped by playback. Some femalespaired to the male subjects sang in response to playback andwere also influenced by prior experience, singing more duringalternating trials that had not been preceded by an overlappingtrial. Male overlappers may signal dominance over a rival toother male or female receivers in a communication network, butit is currently unclear whether overlapping indicates motivationto escalate an aggressive interaction or whether this singingstrategy is related to male quality. Banded wrens are long livedand maintain year-round territories, so modifying responsesto rivals based on prior experience is likely to be importantfor success.