Constrained performance in a communication network: implications for the function of song-type matching and for the evolution of multiple ornaments

Many species of territorial songbirds exhibit a behavior known as song-type matching, in which a male sings the same song type that his neighbor is singing. Song-type matching is associated with increased aggression, but researchers have not come to a consensus on its adaptive function. Building on studies that identify singing performance as a variable relevant to sexual selection, we hypothesize that higher-performance singers benefit from matching their opponent's song type because matching improves eavesdroppers' ability to compare the two males' performances. We present a model of song-type choice that predicts that males that can outperform their rivals benefit by matching. In contrast, lower-performance males should avoid both matching and being matched. Our hypothesis is compatible with some existing hypotheses of song-matching function, but it is not compatible with the hypothesis that song matching is a conventional signal of aggression. We offer unique predictions that could be used to test our idea. We speculate that lower-performance individuals might have driven the evolution of repertoire complexity because they stand to benefit from novel, unmatchable songs. The phenomenon that dissimilar signals are less accurately compared than similar signals may favor the evolution of multiple ornaments and of plastic signal development (e.g., song learning) in general.     

Effects of Rapid Broadband Trills on Responses to Song Overlapping in Nightingales

In communication, animals often use complex signals with different traits carrying different information. In the song of some songbirds, both trills and song overlapping signal arousal or the readiness to escalate a contest in male‐male interactions, yet they also differ inherently from each other. Song overlapping is restricted to interactions and has a clear directive function as the songs are timed specifically to the songs of a counterpart. Trills, however, can be used without opponents actively singing and do not have such a directional character unless when combined with directed traits. This difference raises the question whether trills can enhance the agonistic function of song overlapping when being used simultaneously. Here, we exposed male nightingales (Luscinia megarhynchos) prior to pairing to overlapping playback treatments differing in the presence or absence of rapid broadband trills. Males responded differently to the two playback treatments suggesting that song overlapping and rapid broadband trills have some synergistic effects. Consequently, the separate or simultaneous use of trills and of song overlapping may allow males to adjust information encoded in their singing on a fine scale. Furthermore, males that remained unpaired throughout the breeding season responded differently to the playbacks than did subsequently paired males, emphasizing the implications of differences in territory defence behaviour on males subsequent pairing success.     

Eavesdropping on Male Singing Interactions Leads to Differential Allocation in Eggs

Females invest differently in their eggs depending on the quality of their mates. In oscines, female investment is influenced by the quality of male song. In domestic canaries Serinus canaria, as well as in black‐capped chickadees Poecile atricapillus, females pay attention not only to the intrinsic quality of male song but can also gather information, by eavesdropping on male–male singing interactions, on the relative quality of males. During these interactions, overlapping the song of the rival is more threatening than alternating. Moreover eavesdropping female canaries have been shown to prefer the overlapping song rather than the overlapped song. The present study was designed to assess the effect of the information gathered by eavesdropping on female investment in eggs. First, we broadcasted overlapping interactions to female canaries. Then, we broadcasted to each female one of the two songs previously heard and collected eggs. Females exposed to overlapping songs laid eggs with greater yolk ratio than females exposed to overlapped songs. In contrast, yolk testosterone quantity and concentration were not affected by the treatment. Moreover, we found a variation between eggs with regard to the testosterone deposited in yolk: both quantity and concentration increased with laying order. Our results suggest that female canaries use information gathered by eavesdropping to differentially allocate resources into the eggs. They suggest that singing interactions could influence chick quality via female investment.     

The Song Overlap Null model Generator (SONG): a new tool for distinguishing between random and non-random song overlap

Song overlapping, a behaviour in which an individual begins singing before its counterpart has completed its song, has been the subject of recent debate. Although many studies have suggested that song overlapping functions as a signal, the majority of these studies fail to address the possibility that overlapping is a chance occurrence. Part of the difficulty in determining whether overlap is intentional or accidental lies in the lack of compelling null models for estimating chance levels of song overlap. We have developed the Song Overlap Null model Generator (SONG), a software package for R. SONG uses resampling randomization to predict the expected amount of overlap due to chance, and is applicable to any system in which individuals engage in signalling interactions. To evaluate the effectiveness of SONG, we examined the overlapping behaviour of three avian species: black-capped chickadees (Poecile atricapillus), rufous-and-white wrens (Thryophilus rufalbus) and long-tailed manakins (Chiroxiphia linearis). Our analyses revealed that black-capped chickadees avoided overlapping the songs of playback-simulated intruders, duetting wrens overlapped the songs of their mates and manakins avoided overlapping the duets of their neighbours. We believe that SONG will prove to be a valuable tool for understanding signal timing in songbirds as well as other taxa.     

Why birds sing at dawn: the role of consistent song transmission

The dawn chorus is a widely observed phenomenon. One of the common, but inadequately studied, explanations for the occurrence of the dawn chorus is based on the rationale that atmospheric turbulence, which impairs acoustic communication, is least at dawn, and thus singing at dawn in some way maximizes signal performance. To investigate what possible acoustic benefit is gained through singing at dawn, we transmitted Swamp Sparrow Melospiza georgiana and White-throated Sparrow Zonotrichia albicollis song through open grassland and closed forest both at dawn and at midday. The transmitted songs were re-recorded at four distances from 25 to 100 m. Our results show that the mean overall absolute transmission quality of the signals was not significantly better at dawn than at midday. However, the signal transmission quality was significantly more consistent at dawn than at midday. Also, in general, signal transmission quality decreased with increasing distance. Variability in the transmission quality increased with distance for the White-throated Sparrow song, but not for the Swamp Sparrow song. Consistency in signal transmission quality is a factor that, arguably, is crucial for the identity function of song. This study strongly supports the acoustic transmission hypothesis as an explanation for the existence of the dawn chorus while the demonstration of variability as a key factor in singing at dawn is novel.     

Disentangling Relations among Repertoire Size,Song Rate,Signal Redundancy and Ambient Noise Level in European Songbird

The majority of male songbirds have small repertoires and sing with eventual variety; that is, they present one song type several times before switching to the next one. Several hypotheses have been proposed to explain this phenomenon. The antiexhaustion hypothesis argues that song‐type switching prevents muscle fatigue in the syrinx. The signal redundancy hypothesis suggests that repeating the same signal increases transmission success. Here, we have studied the song behaviour of the chaffinch, Fringilla coelebs, a common Eurasian species in which the males sing a few different song types and provide eventual variety. We tested different hypotheses to explain the temporal organisation of song output (repertoire size, song rate, bout duration, etc.) as a function of ambient noise by comparing birds from the same macrogeographic region in which the birds live either in a noisy town (n = 71) or in a quieter forest habitat (n = 68). Contrary to the prediction of the signal redundancy hypothesis and the results of earlier work on chaffinches living close to noisy streams, we found no significant differences in song characteristics between the town and forest populations. Our results support the antiexhaustion hypothesis because males with larger repertoires were able to sing with a significantly higher rate due to faster switching between different song types and producing shorter bouts. Sample size or population differences between our study and earlier investigations of the same species may explain the inconsistency with previous findings. Future studies should focus on determining the relations between song organisation and the directly measured quality of males and females' choice using, preferably, a longitudinal approach.     

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.     

Effects of song overlapping and alternating on nocturnally singing nightingales

The timing of songs during vocal interactions in male passerines is an important component in territorial signalling as it can reflect information on the singer's state or possibly its quality. Using interactive playback, I investigated effects of song alternation and song overlapping on the nocturnal singing behaviour of nightingales, Luscinia megarhynchos. Subjects timed their songs differently depending on whether the playback songs overlapped their songs or alternated with them. During overlapping treatments, subjects sang at higher rates and interrupted more songs than during alternating treatments. In addition, during alternating treatments subjects sang at higher rates when they had been exposed to the overlapping treatment than when the alternating treatment was the first treatment they had received. These latter responses indicate that timing of songs is not just an immediate effect such as to avoid signal masking but that prior experience with a rival influences the way an individual uses its song. The results thus suggest that not only song overlapping but also the timing of songs during alternating singing carries important information. Individual differences in response suggest further that state (e.g. arousal or motivation) or possibly quality of a territorial male is important for decisions on how it responds vocally. Copyright 1999 The Association for the Study of Animal Behaviour.     

Age‐dependent song changes in a closed‐ended vocal learner: elevation of song performance after song crystallization

Birdsong is a sexual signal that serves as an indicator of male quality. There is already abundant evidence that song elaboration reflects early life‐history because early developmental stress affects neural development of song control systems, and leaves irreversible adverse effects on song phenotypes. Especially in closed‐ended vocal learners, song features crystallized early in life are less subject to changes in adulthood. This is why less attention has been paid to lifelong song changes in closed‐ended learners. However, in the eyes of female birds that gain benefits from choosing mates based on male songs, not only past but also current conditions encoded in songs would be meaningful, given that even crystallized songs in closed‐ended learners would not be identical in the long term. In this study, we examine within‐individual song changes in the Java sparrow Lonchura oryzivora, with the aim of shedding light on the relationship between song and long‐term life history. Specifically, we compared song length, tempo, and song complexity measures between the point just after song crystallization and around 1 yr later, and also compared those traits between fathers and sons to clarify the effect of vocal learning. While it is not surprising that song complexity did not differ depending on age or between fathers and sons, we found that song length and tempo increased with age. Follow‐up analyses have revealed that frequency bandwidth and peak frequency of song notes also elevated with age. Our results show that song performance related to motor skills can be improved even after song crystallization. We also suggest that song performance in closed‐ended vocal learners gives a reliable clue for mate choice by reflecting male quality with aging.     

First-Year Common Nightingales (Luscinia megarhynchos) Have Smaller Song-Type Repertoire Sizes Than Older Males

Based on the assumptions that birdsong indicates male quality and that quality is related to age, one might expect older birds to signal their age. That is, in addition to actual body condition, at least some song features should vary with age, presumably towards more complexity. We investigated this issue by comparing repertoire sizes of free‐ranging common nightingale males in their first breeding season with those of older males. Nightingales are a good model species as they are open‐ended learners, where song acquisition is not confined to an early sensitive period of learning. Moreover, nightingales develop an extraordinarily large song‐type repertoire (approx. 180 different song types per male), and differences in repertoire size among males are pronounced. We analysed repertoire characteristics of the nocturnal song of nine nightingales in their first breeding season and compared them with the songs of nine older males. The repertoire size of older males was on average 53% larger than that of yearlings. When analysing two song categories of nightingales, whistle and non‐whistle songs separately, we found similar results. Our findings show marked differences in repertoire size between age categories, suggesting that this song feature may reflect a male's age. We discuss those mechanisms that may constrain the development of larger repertoires in first‐year males. Whether repertoire sizes are crucial for female mate choice or in vocal interactions among conspecific males remains open to further investigations.     

Negative impact of urban noise on sexual receptivity and clutch size in female domestic canaries

In oscines, male song stimulates female reproduction and females are known to adjust both their sexual preferences and their maternal investment according to song quality. Female domestic canaries are especially responsive to wide frequency bandwidth (4 kHz) male songs emitted with a high‐repetition syllable rate and low minimal frequencies (1 kHz). We previously showed that low‐frequency urban noise decreases female sexual responsiveness for these low‐frequency songs (1–5 kHz) through auditory masking. Based on the differential allocation hypothesis, we predicted that urban noise exposure will equally affect female maternal investment. Using a crossover design, we broadcast low‐frequency songs to females either in an overlapping noise condition or in an alternating noise condition. Females decreased both their sexual responsiveness and their clutch size in the overlapping noise treatment relative to the alternative noise treatment. No differences were found concerning egg size or egg composition (yolk and albumen mass, testosterone concentration). Due to our experimental design, we can exclude a general impact of noisy conditions and thereby provide evidence for a detrimental effect through masking on avian courtship and reproductive output. These results suggest that noisy conditions may also affect avian communication in outdoor conditions, which may partly explain field reports on noise‐dependent breeding success and reduced breeding densities at noisy sites.     

Non-breeding song rate reflects nutritional condition rather than body condition

Numerous studies have focused on song in songbirds as a signal involved in mate choice and intrasexual competition. It is expected that song traits such as song rate reflect individual quality by being dependent on energetic state or condition. While seasonal variation in bird song (i.e., breeding versus non-breeding song) and its neural substrate have received a fair amount of attention, the function and information content of song outside the breeding season is generally much less understood. Furthermore, typically only measures of condition involving body mass are examined with respect to song rate. Studies investigating a potential relationship between song rate and other indicators of condition, such as physiological measures of nutritional condition, are scant. In this study, we examined whether non-breeding song rate in male European starlings (Sturnus vulgaris) reflects plasma metabolite levels (high-density lipoproteins (HDL), albumin, triglycerides and cholesterol) and/or body mass. Song rate was significantly positively related to a principal component representing primarily HDL, albumin and cholesterol (and to a lesser degree plasma triglyceride levels). There was only a trend toward a significant positive correlation between song rate and body mass, and no significant correlation between body mass and the abovementioned principal component. Therefore, our results indicate that nutritional condition and body mass represent different aspects of condition, and that song rate reflects nutritional rather than body condition. Additionally, we also found that intra-individual song rate consistency (though not song rate itself) was significantly positively related to lutein levels, but not to body mass or nutritional condition. Together our results suggest that the relation between physiological measures of nutritional condition and song rate, as well as other signals, may present an interesting line of future research, both inside and outside the breeding season.     

Rock sparrow song reflects male age and reproductive success

The evolution of mating signals is closely linked to sexual selection. Acoustic ornaments are often used as secondary sexual traits that signal the quality of the signaller. Here we show that song performance reflects age and reproductive success in the rock sparrow (Petronia petronia). In an Alpine population in south-east France, we recorded the songs of males and assessed their genetic breeding success by microsatellite analysis. In addition to temporal and spectral song features, we also analysed for the first time whether the sound pressure level of bird song reflects reproductive success. Males with higher breeding success sang at a lower rate and with a higher maximum frequency. We found also that older males gained more extra-pair young and had a higher overall breeding success, although they also differed almost significantly by having a higher loss of paternity in their own nests. Older males could be distinguished from yearlings by singing at lower rate and higher amplitudes. Our findings suggest that song rate may be used as a signal of age and together with song pitch as a signal of reproductive success in this species. Alternatively, younger and less successful males might try to compensate their inferior status by increased song rates and lower pitch. Independent of age and quality, high-amplitude songs correlated with paternity loss in the own nest, suggesting that in this species song amplitude is not an indicator of male quality but high-intensity songs may be rather a response to unfaithful social mates.     

A Novel Context for Bird Song: Predator Calls Prompt Male Singing in the Kleptogamous Superb Fairy-wren,Malurus cyaneus

The cooperatively breeding superb fairy-wren, Malurus cyaneus, sings two types of song; a variable, complex song sung by both sexes, and a relatively invariant, stereotyped song sung only by males. Field observations and playback experiments revealed that the male song could be triggered by a variety of loud avian and non-avian vocalizations, but was triggered most frequently by the calls of predators or potential predators. The male song is sung both within the territory and in winter feeding flocks outside the territory. Acoustic properties of the song suggest that it is a long-range signal. A possible explanation for this unusual phenomenon is that the male song has evolved through sexual selection as an honest signal to females of male quality, for the purpose of obtaining extra-pair copulations.     

Song rate as a signal of male aggressiveness during territorial contests in the wood warbler

Aggressive signaling is an important component in animal communication, as it provides an efficient mechanism for settling conflicts over resources between competitors. In songbirds, a number of singing behaviors have been proposed to be aggressive signals used in territory defense, including song rate. Although aggressive signaling in songbirds has received considerable research attention, adequate evidence for most putative aggressive signals is not available. In this study, we experimentally investigated whether the song rate of male wood warblers Phylloscopus sibilatrix is a signal of their aggressive intent in male–male interactions. We found that males responded differentially to simulated territorial intrusions depending on the song rate of an intruder. Moreover, males that continued to sing during territorial contests increased their song rates, and this behavior predicted the strength of aggressive escalation by the signaler. These results suggest that song rate is an aggressive signal during male–male interactions in the wood warbler. We also found high intra‐individual repeatability in the strength of aggressive response to simulated intrusions, likely reflecting differences in personality (aggressiveness) or quality of male wood warblers. We conclude that changes in singing rate may be an efficient mechanism of signaling immediate shifts in motivation of signalers during territorial contests, especially in species that lack large repertoires or have simple songs.     

The fitness consequences of honesty: Under‐signalers have a survival advantage in song sparrows

How honest or reliable signaling can evolve and be maintained has been a major question in evolutionary biology. The question is especially puzzling for a particular class of signals used in aggressive interactions: threat signals. Here, we report a study on song sparrows (Melospiza melodia) in which we assayed males with playbacks on their territories to quantify their aggressiveness (flights and close proximity) and aggressive signaling levels (rates of soft song, a close‐range signal reliably predicting attack) and asked whether these traits affect individuals’ survival on territory. We found that the effect of aggressive signaling via soft song interacted with aggressive behaviors such that there was a negative correlational selection: among males with low aggression, those males that signaled at higher levels (over‐signalers) had higher survival whereas among males with high aggression those that signaled at low levels (under‐signalers) survived longer. In other words, males that deviate from reliable signaling have a survival advantage. These results, along with previous research that suggested most of the deviation from reliable signaling in this system is in the form of under‐signaling (high‐aggression males signaling at low levels) pose a puzzle for future research on how this reliable signaling system is maintained.     

Corn bunting (<Emphasis Type="Italic">Miliaria calandra</Emphasis>) males respond differently to alternating and overlapping playback of song

Interactive playback experiments were used to study the signal value to the corn bunting, Miliaria calandra, of alternating and overlapping singing. We subjected 15 males to two stimuli that differed in the temporal pattern of song playback (alternating or overlapping). We measured eight characteristics of the males’ response in two categories—song output and movements. Overlapping and alternating playback elicited a similar song response, characteristic of highly aroused males. Song response correlated positively with males’ singing activity before playback, irrespective of stimulus. There were significant differences between latency of approach to the loudspeaker and number of flights. Birds approached the loudspeaker more quickly and spent more time close to it when playback alternated with their songs. The results suggest overlapping song could be interpreted as a stronger threat but elicits a more cautious, rather than stronger, response than the alternating pattern. Males were found to shorten songs during the playback compared with songs sung before and after stimulation. The only predictor of degree of song shortening was song activity before the playback began. It should, therefore, be regarded as a signal which is related to escalated, close-distance counter-singing.     

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.     

Diet and birdsong: short‐term nutritional enrichment improves songs of adult Bengalese finch males

Song is a notable sexual signal of birds, and serves as an honest indicator of male quality. Condition dependence of birdsong has been well examined from the viewpoint of the developmental stress hypothesis, which posits that complex songs assure fitness because learned acoustic features of songs are especially susceptible to early‐life stress that young birds experience in song learning periods. The effect of early stress on song phenotypes should be crucial, especially in age‐limited song learners which sing stereotyped songs throughout life. However, little attention has been paid to non‐learned song features that can change plastically even in adulthood of age‐limited song‐learners. Although it has been shown that food availability affects song rate in wild songbirds, there is limited evidence of the link between favorable nutritional conditions and song phenotypes other than song rate. Under the prediction that singing behavior reflects an individual's recent life history, we kept adult Bengalese finch males under high‐nutrition or normal diet for a short term, and examined changes in body mass and songs. We found that birds on a high‐nutrition diet showed higher song output (e.g. song rate and length) compared with those of the control group, while changes in body mass were moderate. In addition, note repertoire became more consistent and temporal structures got faster in both nutrition and control groups, which indicates that songs were subject to other factors than nutrition. Considering that female estrildid finches, including Bengalese and zebra finches, show a preference toward complex songs as well as longer songs and higher song rate, it is plausible that different aspects of singing behavior signal different male qualities, and provide multifaceted clues to females that choose mates.     

Broad Selectivity for Courtship Song in the Cricket Gryllus bimaculatus

Various characteristics of a long‐distance acoustic signal have been shown to vary to different degrees. It has been suggested that female preferences based on stable song parameters are stabilising or weakly directional, and preferences based on variable parameters are strongly directional. We tested this hypothesis based on a short‐distance signal (courtship song) produced by the field cricket, Gryllus bimaculatus. We studied the degree of variability of different courtship song parameters and the behavioural importance of several parameters using synthesised song models in playback experiments. We found that most of the courtship song elements of G. bimaculatus were quite variable (coefficient of variation, CV, in the range of 20–53%). The most variable parameter of the courtship song was the relative amplitude of two elements: high‐amplitude ticks and low‐amplitude pulses. Because songs containing only ticks (of rare occurrence) appeared to be more effective than songs with both ticks and pulses (of frequent occurrence), we consider female preferences to be directional. Alteration of less variable traits, such as the carrier frequency and duration of ticks (CV = 20–25%), had a different effect on female responsiveness. The synthesised songs with different carrier frequencies of ticks were as attractive to females as the positive control (courtship of muted males accompanied by playback of the recorded song). Altering the duration of ticks had a crucial effect on the female response rate, decreasing female responsiveness to the level observed in the negative control (courtship of muted males). Thus, we did not find a strong relationship between the variability of individual song parameters and their potential importance in song recognition and the evaluation of male quality. The partial inconsistency of our results with the data of other authors may be due to different patterns of past and current selection on long‐distance and short‐distance acoustic signals.