Soft song is a reliable signal of aggressive intent in song sparrows

Animals frequently use signals to modulate aggressive interactions. Establishing that a signal is aggressive or threatening requires demonstrating that it is more commonly used in agonistic contexts, that it predicts subsequent aggressive behaviors by the sender, and that receivers respond differently to this signal. Like many birds, song sparrows (Melospiza melodia) produce a low-amplitude “soft song” vocalization that has been hypothesized to be an aggressive signal. Soft song meets the first two criteria, but previous research has failed to demonstrate that soft song provokes aggression or that receivers even perceive soft song differently from normal loud song. We used a playback experiment with taxidermic mount presentation to test whether territorial male song sparrows respond differently to loud and soft song playbacks. Subjects reacted more strongly to the soft song playback by approaching the mount more closely, increasing wing wave displays, and increasing the proportion of their own songs that were soft songs, with further trends toward increasing the number of flights and attacks. These results confirm that soft song is a conventional signal of aggression in song sparrows and that increased receiver retaliation maintains its reliability.     

Soft song in song sparrows: response of males and females to an enigmatic signal

Low-amplitude “soft song” is used by a variety of songbirds; in some species during aggressive encounters, in others during courtship, and yet others in both these contexts. In song sparrows (Melospiza melodia), soft song has thus far been observed only in aggressive encounters, where its production is a more reliable predictor of attack than any other signaling behavior. We used song playback to test the response of both male and female song sparrows to soft song. The design of the playback experiments took into account the existence of two classes of soft song: crystallized soft song, which consists of song types also found in the broadcast repertoire, and warbled soft song, which consists of less-structured song types not found in the broadcast repertoire. Female song sparrows responded with significantly less courtship display to the playback of crystallized soft song than to that of normal broadcast song, and response to warbled soft song was if anything lower than to that of crystallized soft song. Male song sparrows responded equally aggressively to normal broadcast song as to crystallized soft song, and equally aggressively to warbled soft song as to crystallized soft song. The female results support the conclusion that neither form of soft song functions in courtship. The male results suggest that the reliability of soft song as a signal of aggressive intent is not maintained by a receiver retaliation rule.     

Vocal interactions in common nightingales (<Emphasis Type="Italic">Luscinia megarhynchos</Emphasis>): males take it easy after pairing

Seasonal patterns of bird song have been studied intensively with a focus on individual males. However, little is known about seasonal patterns of singing during vocal interactions between males. Vocal interactions have been shown to be important in sexual selection as males may signal aspects of motivation or quality. Here, we investigated in nightingales (Luscinia megarhynchos) whether a male’s behaviour in vocal interactions at different stages of the breeding season is influenced by its mating status. We examined how males that differ in their subsequent mating success respond to a non-interactive, nocturnal playback presented during the period of mate attraction and subsequently during the egg-laying period. We found that mated males overlapped fewer songs and had a lower song rate during the egg-laying period compared to their responses during the mate-attraction period, whereas unpaired males did not vary in their responses between the two periods. Our results suggest that mating status is a key factor affecting singing behaviour in vocal interactions and that a time-specific singing pattern like song overlapping is used flexibly during vocal interactions. Because song overlapping is thought to be a signal of aggression in male–male vocal interactions, it seems that males vary the level of aggression in vocal interactions according to their mating status and to the stage in the breeding season.     

Response of American redstarts (suborder Passeri) and least flycatchers (suborder Tyranni) to heterospecific playback: the role of song in aggressive interactions and interference competition

Least flycatchers (Empidonax minimus) and American redstarts (Setophaga ruticilla) overlap in the use of food resources on their breeding grounds, promoting high levels of interspecific aggression by the socially dominant flycatcher. We examined the role of song in this interspecific aggression by using repeated-measures-designed playback experiments and observational data on induced aggressive interactions. Flycatchers were more likely to approach the speaker during presentation of redstart song than during intervals of no song or presentation of control song. Approach was close enough to enable visual contact with a singing redstart. In contrast, redstarts made significantly fewer flights following presentation of flycatcher song, when risk of flycatcher attack may be greatest. Reducing the number of flights likely reduces the risk of flycatcher attack on the redstart, as flycatchers do not attack stationary redstart models and are apparently dependent on cues from redstart flight for visual heterospecific recognition. Flycatcher-specific responses of redstarts and marked differences in song morphology rule out misdirected intraspecific aggression as a proximate or ultimate cause of interspecific response to song. Results indicate that song is an important component in aggressive interactions between these two species, and reflect the dominant role of the flycatcher in such interactions. Our results also illustrate the capacity for interspecific interference competition to influence behavior and heterospecific song recognition in two distant avian taxa. Received: 10 January 1995/Accepted after revision: 8 June 1996     

Temporal performance roles during vocal interactions in nightingales (Luscinia megarhynchos B.)

Summary The temporal patterning of vocal interactions between territorial nightingales (Luscinia megarhynchos B). was investigated during nocturnal dyadic singing. We distinguished three forms of temporal performance roles (Table 1; Fig. 3): inserter (preferred song start 0.5–1.0 s after offset of a neighbour's song), overlapper (preferred song start 0.5–1.0 s after onset of a neighbour's song), and Autonomous bird (no evidence for temporal responses adjusted to the timing of a neighbour's singing; Fig. 4). With the beginning of the daily dawn chorus, mutual temporal adjustment of song performances could no longer be ascertained (Fig. 2). To test the flexibility of song onset timing, we presented subjects with three playback programs (I, II, III) simulating a non-flexible conspecific bird. Sequences of songs recorded from a stranger that shared no song types with the subjects were used; intersong pauses were unaltered in I, lengtened in II, and shortened in III. Results confirmed that the timing of song onset can be influenced by the temporal patterning of auditory stimuli (Table 1; Fig. 5): Inserters and overlappers sang at a slower rate during program II than during program I. During program III, which by accelerated stimulus succession caused frequent overlap of songs, inserters and overlappers interrupted their singing behaviour (Fig. 6). This suggests that overlapping, which results in signal interference, is of some functional significance in vocal interactions.     

Responses to playback of whistle songs and normal songs in male nightingales: effects of song category, whistle pitch, and distance

In most species of song birds, males develop song repertoires of several different songs. Among this variety, different songs may be used differently in communication and, thus, may have different functions. Here we studied vocal responses to playback of structurally different songs in male territorial nightingales (Luscinia megarhynchos). Nightingales have enormous vocal repertoires of about 200 song types. Among these songs, one category, whistle songs, sticks out syntactically and acoustically. Here we tested whether or not male nightingales match whistle songs with whistle songs and, if so, whether they also match the pitch of the broadcast whistles. Furthermore, we also tested if nightingales treat whistle songs as a separate category of songs. We conducted interactive playback experiments on nocturnal song in which each male received three playback treatments that differed in the number of whistle songs broadcast. Males responded differently during playbacks by singing significantly more whistle songs when the playback tapes contained many whistle songs than when they contained no whistle songs. Males also frequently matched the pitch of the broadcast whistle songs. In contrast to responses during playback, after the playback terminated males sang more whistle songs when no whistle songs were broadcast than when many whistle songs were broadcast. These findings suggest that whistle songs have a specific signal value and that nightingales treat them as a special song category. Electronic supplementary material to this paper can be obtained by using the Springer Link server located at http://dx.doi.org/10.1007/s00265-002-0511-1.     

Song type variants and aggressive context

We asked whether switching among song type variants functions as a graded signal of aggression in song sparrows (Melospiza melodia). Song type variants are different versions of a given song type and are defined by much smaller acoustic differences than those defining separate song types. The principal evidence that switching between song types functions as an aggressive signal, in song sparrows and other species, is that song type switching frequencies increase during aggressive contexts, for example during simulated territorial intrusions. We tested whether variant switching frequencies change in the same way, using playback of conspecific song to simulate intrusions. Male song sparrows showed a significant increase in variant switching frequencies during intrusion relative to before intrusion. After intrusions, variant switching frequencies returned to pre-intrusion levels. These results are consistent with the hypothesis that variant switching is a graded aggressive signal, but other interpretations are possible, for example, that variant switching is a signal of submission or represents simple production error. Received: 20 January 2000 / Revised: 15 July 2000 / Accepted: 30 July 2000     

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.     

Responses of song sparrows to song-type matching via interactive playback

The aggressive and singing responses of ten territorial male song sparrows, Melospiza melodia, to sustained song-type matching via interactive playback were examined. This auditory stimulus, which involves both synchronous switching and song-type matching, was hypothesized to be a strong aggressive threat. Responses were compared to five other trial types in which the switching pattern and song-type similarity were independently varied. The six trial types were organized into a factorial design with three switching levels (no switching, synchronized switching, and rapid unsynchronized switching) and two matching levels (shared song-types and unshared song-types). The aggressive response of the birds, a composite index of the correlated behaviors of singing rate, perch change rate, and time spent close to the speaker, showed significant main effects of both the switching and the matching factors, with no interaction effect. The response was highest for the shared/unsynchronized switching trial and lowest for the unshared/no switching trial. Since the synchronous switching trials produced aggressive responses intermediate between the no switching and rapid unsynchronized switching trials, our results corroborate earlier studies showing that switching rate, song-type diversity and song similarity are the key determinants of aggressive approach. However, the switching rate of the focal birds during playback was not correlated with the other response variables and showed a very different pattern from the aggressive response. Switching rate increased during unshared/synchronized trials and decreased during shared/synchronized (i.e., song-type matching) trials. The tendency of the birds to refrain from switching when they were song-type matched by playback led to long bouts of matched-type countersinging. These results suggest that song-type matching locks two countersinging birds into a new level of interaction in which information other than aggressive motivation exchanged.     

Bird song as a signal of aggressive intent

A central question in animal communication research concerns the reliability of animal signals. The question is particularly relevant to aggressive communication, where there often may be advantages to signaling an exaggerated likelihood of attack. We tested whether aggressive signals are indeed reliable signals of attack in song sparrows (Melospiza melodia). We elicited aggressive signaling using a 1-min playback on a male’s territory, recorded the behavior of the male for 5 min, and then gave him the opportunity to attack a taxidermic mount of a song sparrow associated with further playback. Twenty subjects attacked the mount and 75 did not. Distance to the speaker was a significant predictor of attack for both the initial recording period and the 1 min before attack. For the initial recording period, none of the measures of singing behavior that we made was a significant predictor of attack, including song-type matching, type-switching frequency, and song rate. For the 1-min period immediately before attack, only the number of low amplitude “soft songs” was a significant predictor of attack. Although most aggressive signals contained little information on attack likelihood, as some models suggest should be the case, the unreliability of these signals was not caused by convergence of individuals on a single signaling strategy, as those models argue should occur.     

Singing onstage: female and male common nightingales eavesdrop on song type matching

In bird communication, listening individuals may obtain information on the quality and motivation of a male not only from solo-singing, but also from song interactions and listeners base their future decisions in territorial and mating contexts on such public information. Eavesdropping on male interactions may thus have a strong influence on sexual selection. In singing interactions, temporal coordination (e.g. overlapping vs. alternating) of two singers as well as structural interaction patterns (e.g. song type matching or repertoire matching) have been described, but the latter is far less studied. By conducting dual-speaker playback experiments with common nightingales Luscinia megarhynchos, we simulated an interaction where one singer was repeatedly song–type matching his counterpart. Playbacks were broadcast to male and female nightingales, and their approach behaviour and singing responses (in the case of male focals) were analysed. We found that both, males and females, spent more time with the matched bird, whereas males additionally sang more songs towards the matching bird. This can be taken as strong hint that eavesdropping occurs in nightingale communication and that listening to male vocal contests might be an important strategy for both sexes to adjust their behavioural output. With regard to the function of song matching, we assume that song-matching is not an aggressive signal per se in nightingales. We rather conclude that vocal leaders within an interaction, here the matched bird, may elicit stronger responses in conspecifics than vocal followers, here the matching bird.     

Heterospecific song matching in two closely related songbirds (Parus major and P. caeruleus): great tits match blue tits but not vice versa

To date, song research has focused primarily on the interactions of conspecifics. However, frequent interactions of songbirds with heterospecifics may necessitate adequate communication outside the species boundary. In this study, we focus on heterospecific communication behaviour of two small sympatric congeneric passerines, great and blue tits (Parus major and Parus caeruleus), which breed in overlapping territories and compete for food and nesting cavities. By means of a first playback experiment, we show that (1) heterospecific matching (imitating songs of the other species) is a strategy frequently used by great tits but not by blue tits, (2) both blue tit trilled and untrilled song can be accurately matched by great tits and that (3) almost half of the great tits in our study population match at least one blue tit song across all studied breeding stages, indicating that this heterospecific matching behaviour is a common feature in this population. A second playback experiment showed that these great tit imitations of blue tit songs do not function in intraspecific communication between male great tits. Hence, these heterospecific imitations appear to be designed for interspecific communication with blue tits. These findings suggest a strong heterospecific influence on the vocal learning process, repertoire composition and repertoire use in great tits and provide a possible mechanism that can drive song convergence in songbirds.     

An experimental study on the causal relationships between (ecto-)parasites, testosterone and sexual signalling

Bird song is considered to have evolved via sexual selection and should as such honestly signal aspects of the quality of its bearer. To ensure honesty, the immunocompetence handicap hypothesis proposed a dual role of testosterone, having positive effects on sexual signalling but suppressive effects on immune function. However, recent studies showed that it is rather an immune activation that suppresses the androgen production. This reversed chain of causation may significantly alter the pathways, which translate the effects of parasites and pathogens into changes in the expression of male sexual traits. We infested male canaries with Ixodes ricinus tick nymphs to investigate the causal relationships between (ecto-)parasites, testosterone and sexual signalling, here singing behaviour. We focused on flexible song traits, which may quickly reflect changes in the infestation status, and tested whether these effects relate to changes in the plasma testosterone levels or health state. The experimental tick infestation altered the males’ song performance by reducing song consistency, a trait that had previously been identified to reflect male quality. The tick infestation lowered the plasma testosterone levels and had a negative effect on the health status in terms of a reduced hematocrit. Our pathway analysis then revealed that it is the parasite-induced reduction of the plasma testosterone levels but not of the health state that caused the changes in song consistency. Thus, our study supports the view that it is the effect of parasites and immune activation on plasma testosterone levels that generates the trade-off between immunocompetence and sexual signalling.     

Do male barn swallows (<Emphasis Type="Italic">Hirundo rustica</Emphasis>) experience a trade-off between the expression of multiple sexual signals?

Some sexual selection models envisage exaggerated male secondary sexual characters to be costly and therefore reliable indicators of the quality of potential mates to choosy females. If male secondary sexual characters have a natural selection cost, they may be linked to each other by reciprocally constraining relationships that would prevent individual males from increasing their level of multiple signaling. Barn swallow (Hirundo rustica) males have at least two costly signals relevant to socio-sexual interactions: tail length and song. Under the hypothesis that a trade-off exists between male signals, we manipulated the maintenance cost of tail ornaments to test whether this reduced the quantity and quality of song, a condition-dependent, phenotypically plastic signal. Contrary to our expectation, tail elongation had no effect on singing activity and song complexity. However, tail-elongated males produced songs with longer terminal parts ('rattles'). Long rattles are associated with highly competitive social contexts and high circulating levels of testosterone, suggesting that tail-elongated males were more frequently involved in either male-male aggressive or inter-sexual interactions. Therefore, this study shows that males are not displaying multiple signals at the maximum possible level, implying that this system is open to unreliable communication. However, long-term trade-offs between signal expression and viability may prevent males from displaying both signals at higher rates.Communicated by: M. Webster     

Sound degradation as a distance cue in great tit (Parus major) song

Summary We report an experiment designed to test the ideas that: 1. male songbirds can use cues from the distortion of song by environmental factors (degradation) to estimate the distance of another singing male; 2. song degradation is assessed by reference to an internal standard. Great tits respond more strongly to undegraded than to degraded songs when both are played at the same amplitude and from the same position in the territory. This difference in response is shown only if the playback song is familiar to the test bird; familiar songs being those sung either by the test bird or neighbours of the test bird. We interpret these results as evidence that cues from song degradation can be used to estimate the distance of a singing conspecific and that degradation assessment is only possible if the bird has an internal representation of the song (because either it and/or a neighbour sings the song). We discuss the implications of these results for Morton's (1982) ranging hypothesis, and for the distinction between learning and performance in bird song. Our results partially support the ranging hypothesis, but question the nature of unrangeable songs sensu Morton. The finding that birds can assess the degree of degradation of songs that they do not sing, supports the idea that birds learn more songs than they sing.     

Discrimination of vocal performance by male swamp sparrows

In aggressive communication, the interests of signalers and receivers are directly opposed, presenting a challenge to the maintenance of reliable signaling. Index signals, whose production is constrained by physical ability, offer one solution to the reliable signaling problem. Vocal performance, the ability to produce physically challenging songs, is likely such a signal in swamp sparrows. Maximum vocal performance varies between males and is correlated with aspects of quality. However, vocal performance can be modulated in aggressive contexts by increasing the frequency bandwidth and trill rate of songs. This study examines receiver response to (1) differences in performance of the same song types by different signalers and (2) individual modulation of performance between contexts. Results demonstrate that male receivers show differential response to between-male differences in song type performance, but do not show differential response to the smaller scale modulations of performance produced by individuals singing the same song type at different times. This pattern suggests that vocal performance cannot be effectively cheated and may therefore serve as a good example of an index signal.     

Habituation and song repertoires in the great tit

Summary This paper is concerned with the idea that the song repertoires of passerine birds are an evolutionary adaptation to reduce habituation in listeners. In an experiment involving 16 territorial males I played either a single song or a repertoire of songs for 15 two-min trials through a single loudspeaker near the edge of the territory. In a second experiment with 10 birds I played the songs through one of two loudspeakers in different parts of the territory, alternating between loudspeakers on successive trials. The birds tended to habituate more rapidly to single song playback than to repertoires. In the second experiment the overall level of habituation was lower and the difference between the two treatments was less marked.Two features of song repertoire organisation are consistent with the habituation hypothesis (1) the avoidance of low recurrence intervals in switches between song types, and (2) the fact that within repertoire variability is as great or greater than between repertoire varability.The main problem with the habituation hypothesis is that habituation by listeners does not seem to be adaptive, so it is not clear why they should habituate. I suggest a hypothesis. Intruders may assess the density of birds in an area by listening to songs, so that habituation may be a mechanism by which this density assessment is achieved. Repertoires could be a mechanism by which resident birds cheat, through increasing the apparent density of singing birds.     

Response of territorial male song sparrows to song types and variations

Summary The song repertoires of male song sparrows (Melospiza melodia) are comprised of distinct song types and many overlapping variations within each type. This study examines the sensitivity of territorial male song sparrows to both multiple song types and variation within types. A playback experiment was conducted using stimulus tapes that had either single songs (but not variations), song variations (but not types) or a single song. Response during playback was similar for all three stimulus groups, but diminished sooner after playback for the single-song tape. Thus our results indicate that male song sparrows are sensitive to song variability both within and among song types.     

Trill performance components vary with age, season, and motivation in the banded wren

Acoustic displays with difficult-to-execute sounds are often subject to strong sexual selection because performance levels are related to the sender’s condition or genetic quality. Performance may also vary with age, breeding stage, and motivation related to social context. We focused on within-male variation in four components of trill performance in banded wren (Thryophilus pleurostictus) songs: note consistency, frequency bandwidth, note rate, and vocal deviation. The latter is a composite measure reflecting deviation from the performance limit on simultaneously maximizing both frequency bandwidth and note rate. We compared the changes in these song parameters at three time scales: over the course of years, across the breeding season, and at different times of the day with contrasting agonistic contexts. Vocal deviation decreased and note consistency increased between years, suggesting that experience may improve individual proficiency at singing trills. Consistency also increased across the season, confirming that practice is important for this parameter. Although there was no significant seasonal change in vocal deviation, one of its components, note rate, increased during the season. Neither vocal deviation nor consistency varied with agonistic context. However, note rate increased during playback experiments simulating territorial intrusions compared to dawn chorus singing. The magnitude of a male’s increase in note rate was positively correlated with his aggressive behavior during the playback experiment. Thus consistency, bandwidth, and vocal deviation indicate age, whereas trill rate flexibly indicates the singer’s aggressive motivation. We also found evidence of a within-male trade-off between vocal deviation and consistency.     

Seasonal variation in the duetting behaviour of rufous-and-white wrens (<Emphasis Type="Italic">Thryothorus rufalbus</Emphasis>)

Seasonal variation in animal signalling behaviour has been well documented and has contributed much to our understanding of male signals. In contrast, we know little about seasonal variation in female signals or signals produced jointly by males and females, such as the vocal duets of birds. Here, we examine how singing behaviour changes in relation to time of year and breeding stage in rufous-and-white wrens (Thryothorus rufalbus), neotropical songbirds where both males and females sing and where breeding partners coordinate songs to produce vocal duets. We recorded a colour-marked population of birds over an extended time period encompassing multiple breeding stages. Across all time frames and breeding stages, males sang at higher rates than females and male solos were more common than duets or female solos. Males and females showed divergent seasonal patterns of singing. Females sang more often early in the year, during the pre-breeding season, and female song tapered off as the breeding season progressed. Duetting followed a parallel pattern, which resulted from females showing less duet responsiveness to their partner’s songs later in the year. Male independent song rate peaked at the onset of the rainy season – a time when females become fertile – and males showed the highest level of duet responsiveness during this period. Our results suggest that early in the year, duets appear to be cooperative displays, functioning in joint territory defence and/or the coordination of breeding activities. When females are fertile, however, increased duet responsiveness by males is consistent with mate or paternity guarding.