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Using the responses of territory owners to playback to infer the territorial function of acoustic signals is common practice. However, difficulties with interpreting the results of such experiments have obscured our understanding of territorial signaling. For instance, a stronger response to playback is often interpreted as more aggressive, but there is no consensus as to whether this should be in response to the least or most threatening simulated intruder. Rather than following a gradual increase or decrease, the relationship between signal intensity and response strength may instead describe a peaked curve. We manipulated banded wren (Thryophilus pleurostictus) songs to simulate low, median and high performance singers and used these songs as stimuli in playback experiments. Banded wrens were less likely to approach the high performance stimulus compared to the low and median performance stimuli. However, the birds that did approach the high performance stimulus sang more than those that approached the low performance stimulus. In addition, birds were more likely to match the songs when exposed to the median and high performance stimuli compared to the low performance stimuli and song matching predicted approach behavior. These results are in accordance with theoretical models of aggressive encounters in which low performance opponents are challenged without further assessment. Median and high performance opponents however, may require further assessment and the latter may be perceived as too intimidating for approach.

Interpreting receiver responses to on-territory playback of aggressive signals is problematic. One solution is to combine such receiver-perspective experiments with a sender-perspective experiment that allows subjects to demonstrate how their choice of singing strategies is associated with their approach behavior. Here we report the results of a sender-perspective study on the banded wren (Thryothorus pleurostictus), and combine information on context and results of previous receiver-perspective experiments to clarify function. Territorial males were presented with a 5-min playback consisting of song types present in their repertoire. We assessed the degree to which the subjects’ song matching rate, overlapping rate, and song-type versatility were correlated with their approach latency, closeness of approach, latency to first retreat, and time spent close to the speaker. Male age, breeding stage, and features of the playback stimuli were also considered. Song matching was associated with rapid and close approach, consistent with the receiver-perspective interpretation of type matching as a conventional signal of aggressive motivation. Overlapping was associated with earlier retreat, and together with the aversive receiver response to our previous overlapping playback experiment suggests that overlapping is a defensive withdrawal signal. High versatility was associated with slower first retreat from the speaker and high levels of reciprocal matching between subject and playback. Males with fledglings sang with particularly low versatility and approached the speaker aggressively, whereas males with nestlings overlapped more and retreated quickly. Finally, older males matched more but overlapped less.

Conventional signals impose costs on senders through receiver retaliation rather than through investment in signal production. While several visual conventional signals have been described (mainly 'badges of status'), acoustic examples are rare; however, several aspects of repertoire use in songbirds are potential candidates. We performed interactive playback experiments to determine whether song-type matches (responding to a song with the same song type), repertoire matches (responding to a song with a different song type, but one in the repertoires of both singers) and unshared song types serve as conventional signals during male-male territorial interactions in banded wrens, Thryothorus pleurostictus. Our results demonstrate that these three signals incite varying levels of receiver aggression: song-type matches induce faster approach than do repertoire matches, and repertoire matches induce faster approach than do unshared song types. Production costs do not differ, while the receiver response does. Because territorial banded wrens approach opponents who signal aggressively, such opponents risk attack. This system will punish and prevent cheaters, as weak males signalling aggression will be subject to escalation by stronger or more-motivated opponents.

We tested the signal value of song overlapping in banded wrens (Thryothorus pleurostictus), using interactive playback to either overlap or alternate with their songs. Males shortened song duration and decreased variability in song length when their songs were overlapped by playback, suggesting that they were attempting to avoid being overlapped and perhaps being less aggressive. A novel finding was an effect of long-term prior experience: song lengths remained relatively short in alternating trials 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 tended to stay further from the speaker during alternating treatments if they had previously been overlapped by playback. Some females paired to the male subjects sang in response to playback and were also influenced by prior experience, singing more during alternating trials that had not been preceded by an overlapping trial. Male overlappers may signal dominance over a rival to other male or female receivers in a communication network, but it is currently unclear whether overlapping indicates motivation to escalate an aggressive interaction, or whether this singing strategy is related to male quality. Banded wrens are long-lived and maintain year-round territories, so modifying responses to rivals based on prior experience is likely to be important for success.

In a variety of songbirds the production of trilled song elements is constrained by a performance tradeoff between how fast a bird can repeat trill units (trill rate) and the range of frequencies each unit can span (frequency bandwidth). High-performance trills serve as an assessment signal for females, but little is known about the signal value of vocal performance for male receivers. We investigated the relationship between trill rate and frequency bandwidth in banded wren (Thryothorus pleurostictus) songs. Trilled song elements showed the same performance tradeoff found in other passerines and individuals differed in performance of some trill types. We tested the hypothesis that males of this species assess each other based on trill performance with a two-speaker experiment, in which territory owners were presented with alternating renditions of the same song type manipulated to differ in trill rate. Subjects were significantly more likely to approach the faster trill stimulus first. However, subjects that received trill types closer to the performance limit spent less time close to the fast speaker. Our results show that male banded wrens discriminate and respond differently to songs based on their vocal performance. Thus, performance of physically challenging songs may be important in intra- as well as inter-sexual assessment.

In a variety of songbirds the production of trilled song elements is constrained by a performance tradeoff between how fast a bird can repeat trill units (trill rate) and the range of frequencies each unit can span (frequency bandwidth). High-performance trills serve as an assessment signal for females, but little is known about the signal value of vocal performance for male receivers. We investigated the relationship between trill rate and frequency bandwidth in banded wren (Thryothorus pleurostictus) songs. Trilled song elements showed the same performance tradeoff found in other passerines and individuals differed in performance of some trill types. We tested the hypothesis that males of this species assess each other based on trill performance with a two-speaker experiment, in which territory owners were presented with alternating renditions of the same song type manipulated to differ in trill rate. Subjects were significantly more likely to approach the faster trill stimulus first. However, subjects that received trill types closer to the performance limit spent less time close to the fast speaker. Our results show that male banded wrens discriminate and respond differently to songs based on their vocal performance. Thus, performance of physically challenging songs may thus be important in intra- as well as intersexual assessment.

Older males tend to have a competitive advantage over younger males in sexual selection. Therefore, it is expected that signals used in sexual selection change with age. Although song repertoire size in songbirds is often mentioned as an age-related trait, many species, including the banded wren (Thryothorus pleurostictus), do not increase their repertoires after the first year. Here, we show that banded wrens reproduce the trill notes in their songs with less variability between them (i.e. more consistently) when they grow older. In a playback experiment, we also show that banded wrens discriminate between younger and older birds based on structural aspects of their song. In a second experiment, banded wrens also respond differentially to natural songs versus songs with artificially enhanced consistency. We argue that consistency in trill note reproduction may be achieved through practice. Sexual selection in the form of male–male competition may therefore operate on a phenotypic trait, the expression of which is enhanced by practice.

Song-type matching is a singing strategy found in some oscine songbirds with repertoires of song types and at least partial sharing of song types between males. Males reply to the song of a rival male by subsequently singing the same song type. For type matching to serve as an effective long-distance threat signal, it must be backed up by some probability of aggressive approach and impose some type of cost on senders that minimizes the temptation to bluff. Western subspecies of the song sparrow exhibit moderate levels of song-type sharing between adjacent males and sometimes type match in response to playback of song types they possess in their repertoires. Interactive playback experiments were used in order to examine the subsequent behaviour of type-matching birds and to quantify the responses of focal birds to type-matching versus non-matching stimuli. Birds that chose to type match the playback of a shared song type subsequently approached the speaker much more aggressively than birds that did not type match. Moreover, birds approached a type-matching stimulus much more aggressively than a non-matching stimulus. These results and consideration of alternatives suggest that type matching in song sparrows is a conventional signal in which honesty is maintained by a receiver retaliation cost against bluffers.

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

Song-type switching rate and song matching have been shown to function as territorial signals in male solo song but, to our knowledge, seem not to have been previously studied in a duetting species. We studied the plain wren (Thryothorus modestus zeledoni), to test whether duets signalled threat through song-switching rates, or through phrase type or duet type matching. Increases in the rate of song switching appear to function as an anti-habituation device rather than as a specific signal of threat. Fitting with previous results that same-sex individuals share phrase types, but pairs do not share duet types, both males and females used duets to phrase type match to playback. Pairs, however, did not duet type match in response to playback, and this suggests that within the cooperative territory defence of the duet, each sex is targeting its aggression at same-sex competitors.

In many birds, individuals ‘answer’ the songs of their pair-mates to produce vocal ‘duets’. One hypothesized function of song answering is that it prevents extra-pair birds from intruding into the duetting pair's territory to obtain copulations or usurp one of the pair-mates. In this capacity, answering may signal that the pair-mates are close together, and so are prepared to defend against such an intrusion. Another functional hypothesis states that answering helps pair-mates maintain contact, and so predicts that a bird is more likely to approach its mate after a duet than after a solo song. I used radio-telemetry to monitor the distance between mated black-bellied wrens (Pheugopedius fasciatoventris). I found that birds of both sexes were more likely to answer their mate's song when the mate was close, and that maximum duet length was negatively related to the distance between pair-mates. Furthermore, song answering positively affected the likelihood of one pair-mate approaching the other after a song. In a significant majority of the approaches after duet songs, the answering bird approached the initiator. I conclude that in the black-bellied wren, (i) the occurrence and duration of vocal duets covary with physical closeness and (ii) contact maintenance is a secondary function of duet participation.

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.

We studied the use of song types and their acoustic features in different social contexts in the banded wren (Thryothorus pleurostictus), a resident tropical songbird in which males possess about 20 distinctive song types varying in duration, bandwidth, note composition, and trill structure. We recorded six focal males intensively for four days each while we observed context information such as during versus after dawn chorus, presence of the female, counter-versus solo-singing, location at the edge versus centre of the territory, and proximity to the nest. All males used at least some song types differentially during each of these pairs of alternative contexts. Males also preferentially used the song types they shared with a given neighbour when interacting with that bird. Songs delivered during dawn chorus were significantly longer, wider in bandwidth, often compound (double songs), and more likely to contain a rattle or buzz and an up-sweeping trill, compared to songs delivered after dawn chorus. Similar features were also more commonly observed when birds were engaged in intense male-male interactions and boundary disputes after dawn chorus, especially when countersinging at the edge of the territory. The presence of the female caused the male to deliver song types with narrower whole-song and trill bandwidth and fewer rattles and buzzes, and song-type diversity and fraction of compound songs were higher when the female was present. Thus, in addition to using type matching and variations in song-type switching and diversity to signal different levels of aggressive intention, male banded wrens also select song types based on their acoustic structure in different social contexts.

Birdsong serves to attract mates and to deter territorial rivals. Even though song is not restricted to males, this dual function has almost exclusively been demonstrated for male song. To test the generality of hypotheses on birdsong, we investigated female song in the sex-role reversed, classically polyandrous African black coucal (Centropus grillii) in the context of female–female competition. We compared spontaneously vocalizing females with females vocally responding to a playback simulating a conspecific intruder. Females changed vocal parameters in response to playbacks: They lowered the pitch of their vocalizations and enhanced the duration of song elements when being challenged. Also, the composition of the vocalizations was altered. There was no significant correlation between pitch and body size parameters in spontaneous song, but there was for response songs, with larger females having a lower pitch. These changes in vocal properties suggest that the vocalizations are important for mutual assessment of competitive abilities in females. Our findings confirm the general role of intrasexual competition in vocal communication of birds.

Electronic supplementary material

The online version of this article (doi:10.1007/s00265-009-0836-0) contains supplementary material, which is available to authorized users.

Individuals often differ consistently in behaviour across time and contexts, and such consistent behavioural differences are commonly described as personality. Personality can play a central role in social behaviour both in dyadic interactions and in social networks. We investigated whether explorative behaviour, as proxy of personality of territorial male great tits (Parus major), predicts their own and their neighbours' territorial responses towards simulated intruders. Several weeks prior to playback, subjects were taken from the wild to test their exploratory behaviour in a standard context in the laboratory. Exploratory behaviour provides a proxy of personality along a slow–fast explorer continuum. Upon release, males were radio-tracked and subsequently exposed to interactive playback simulating a more or a less aggressive territorial intruder (by either overlapping or alternating broadcast songs with the subjects' songs). At the same time, we radio-tracked a neighbour of the playback subject. Male vocal responses during playback and spatial movements after playback varied according to male explorative behaviour and playback treatment. Males with lower exploration scores approached the loudspeaker less, and sang more songs, shorter songs and songs with slower element rates than did males with higher exploration scores. Moreover, neighbour responses were related to the explorative behaviour of the subject receiving the playback but not to their own explorative behaviour. Our overall findings reveal for the first time how personality traits affect resource defence within a communication network providing new insights on the cause of variation in resource defence behaviour.

Although vocal interactions in songbirds have been well studied, little is known about the extent to which birds attend to their conspecifics' interactions. Attending to others' interactions can provide valuable information since vocal interactions are often asymmetrical and can reflect differences in the state or quality of the signallers. Playback experiments with simulated dyadic interactions showed that male territorial nightingales (Luscinia megarhynchos) attend to asymmetries in interactions and respond more strongly to rivals that overlap the songs of their counterpart. In order to test if nightingales respond differently to two interacting rivals that are alternating songs asymmetrically (with leader–follower roles), we simulated an interaction using a dual-speaker design. Subjects discriminated between the simulated singing strategies and responded more intensely at the loudspeaker playing the preceding songs. This suggests that individuals whose songs precede in an interaction when there is no acoustic overlap are perceived as more serious rivals. Intense responses to the preceding songs compared with intense responses to the overlapping (non-preceding) songs in a previous study also indicate that discrimination is not the result of one specific proximate cue such as greater attention to the first- or last-heard stimulus. Thus, these results provide further evidence that by listening to asymmetries in conspecifics vocal interactions, receivers can obtain valuable information on their relative differences.

Songbirds respond to initial playback of a recorded conspecific song in numerous ways, from changes in gene expression in the brain to changes in overt physical activity. When the same song is presented repeatedly, responses have been observed to habituate at multiple levels: molecular, cellular and organismal. Core criteria of habituation have been established at each level, although in no case have all the formal parameters been rigorously measured. At the level of overt behavior, classical field studies showed that territorial birds respond to the song of a potential challenger with a variety of behaviors, and many (but not all) of these behaviors decline with repeated stimulus presentation. More recent laboratory studies have defined analogous responses to song presentation in the zebra finch (Taeniopygia guttata), the dominant species in current molecular and neurobiological research and one that does not use song for territorial defense. Studies in the zebra finch have also demonstrated activation followed by habituation of responses measured at both electrophysiological and molecular (gene expression and signal transduction) levels. In all cases, habituation is specific for a very particular stimulus - an individual song presented in a particular context. There are strong correlations between habituation measurements made at these different levels, but some dissociations have also been observed, implying that molecular, electrophysiological and behavioral habituations are not equivalent manifestations of a single core process.

To investigate the ecological relevance of brain gene regulation associated with singing behavior in songbirds, we challenged freely ranging song sparrows with conspecific song playbacks within their breeding territories. Males responded by approaching the speaker, searching for an intruder and actively singing. In situ hybridization of brain sections revealed significantly higher expression of the transcriptional regulator ZENK in challenged birds than in unstimulated controls in several auditory structures and song control nuclei. We conclude that singing behavior in the context of territorial defense is associated with gene regulation in brain centers that control song perception and production, and that behaviorally regulated gene expression can be used to investigate brain areas involved in the natural behaviors of freely ranging animals.

In studies of birdsong learning, imitation-based assays of stimulus memorization do not take into account that tutored song types may have been stored, but were not retrieved from memory. Such a 'silent' reservoir of song material could be used later in the bird's life, e.g. during vocal interactions. We examined this possibility in hand-reared nightingales during their second year. The males had been exposed to songs, both as fledglings and later, during their first full song period in an interactive playback design. Our design allowed us to compare the performance of imitations from the following categories: (i) songs only experienced during the early tutoring; (ii) songs experienced both during early tutoring and interactive playbacks; and (iii) novel songs experienced only during the simulated interactions. In their second year, birds imitated song types from each category, including those from categories (i) and (ii) which they had failed to imitate before. In addition, the performance of these song types was different (category (ii) > category (i)) and more pronounced than for category (iii) songs. Our results demonstrate 'silent' song storage in nightingales and point to a graded influence of the time and the social context of experience on subsequent vocal imitation.

While birdsong is a model system for animal communication studies, our knowledge is derived primarily from the study of only one sex and is therefore incomplete. The study of song in a role-reversed species would provide a unique opportunity to study selective pressures and mechanisms specific to females, and to test the robustness of current theories in an empirically novel manner. We investigated function of female song in stripe-headed sparrows (Aimophila r. ruficauda), a Neotropical, duetting passerine, and found that during simulated territorial intrusions by a female, male or duetting pair, females: (i) sang more than males to same-sex and duet playback, (ii) played a leading singing role in all contexts, and (iii) showed a longer term song response than males. These results suggest that females sing competitively against other females, and that intrasexual selection may be greater among females than among males. This is the first songbird study to show a stronger vocal role in territory defence for females than males. Stripe-headed sparrows are group-living cooperative breeders, and preliminary data suggest that polyandry and/or resource defence may explain strong female singing behaviour. Stripe-headed sparrows may be a useful study species for expanding our knowledge of vocal communication in female animals.

Although elaborate bird song provides one of the prime examples of a trait that evolved under sexual selection, it is still unclear whether females judge the quality of males by attributes of their song and whether these song features honestly signal a male's genetic quality. We measured the ability of male dusky warblers Phylloscopus fuscatus to maintain a high sound amplitude during singing, which probably reflects an individual's physiological limitations. This new measure of singing performance was correlated with male longevity and with extra-pair paternity, indicating that females who copulated with better singers obtained 'good genes' for their offspring. Our findings are consistent with the idea that females assess male quality by subtle differences in their performance during the production of notes, rather than by the quantity or versatility of song. In addition, observations on territorial conflicts indicate that attractive males invest less in competition over territories because they can reproduce via extra-pair paternity.

Background

Discriminating threatening individuals from non-threatening ones allow territory owners to modulate their territorial responses according to the threat posed by each intruder. This ability reduces costs associated with territorial defence. Reduced aggression towards familiar adjacent neighbours, termed the dear-enemy effect, has been shown in numerous species. An important question that has never been investigated is whether territory owners perceive distant neighbours established in the same group as strangers because of their unfamiliarity, or as dear-enemies because of their group membership.

Methodology/Principal Findings

To investigate this question, we played back to male skylarks (Alauda arvensis) songs of adjacent neighbours, distant neighbours established a few territories away in the same microdialect area and strangers. Additionally, we carried out a propagation experiment to investigate how far skylark songs are propagated in their natural habitat and we estimated repertoire similarity between adjacent neighbours, distant neighbours and strangers. We show that skylarks, in the field, respond less aggressively to songs of their distant and likely unfamiliar neighbours, as shown by the propagation experiment, compared to stranger songs. The song analysis revealed that individuals share a high amount of syllables and sequences with both their adjacent and distant neighbours, but only few syllables and no sequences with strangers.

Conclusions

The observed reduction of aggression between distant neighbours thus probably results from their familiarity with the vocal group signature shared by all members of the neighbourhood. Therefore, in skylarks, dear-enemy-like relationships can be established between unfamiliar individuals who share a common acoustic code.

The question of why animals participate in duets is an intriguing one, as many such displays appear to be more costly to produce than individual signals. Mated pairs of yellow-naped amazons, Amazona auropalliata, give duets on their nesting territories. We investigated the function of those duets with a playback experiment. We tested two hypotheses for the function of those duets: the joint territory defense hypothesis and the mate-guarding hypothesis, by presenting territorial pairs with three types of playback treatments: duets, male solos, and female solos. The joint territory defense hypothesis suggests that individuals engage in duets because they appear more threatening than solos and are thus more effective for the establishment, maintenance and/or defense of territories. It predicts that pairs will be coordinated in their response (pair members approach speakers and vocalize together) and will either respond more strongly (more calls and/or more movement) to duet treatments than to solo treatments, or respond equally to all treatments. Alternatively, the mate-guarding hypothesis suggests that individuals participate in duets because they allow them to acoustically guard their mate, and predicts uncoordinated responses by pairs, with weak responses to duet treatments and stronger responses by individuals to solos produced by the same sex. Yellow-naped amazon pairs responded to all treatments in an equivalently aggressive and coordinated manner by rapidly approaching speakers and vocalizing more. These responses generally support the joint territory defense hypothesis and further suggest that all intruders are viewed as a threat by resident pairs.

The ultrasonic vocalizations of mice are attracting increasing attention, because they have been recognized as an informative readout in genetically modified strains. In addition, the observation that male mice produce elaborate sequences of ultrasonic vocalizations (‘song’) when exposed to female mice or their scents has sparked a debate as to whether these sounds are—in terms of their structure and function—analogous to bird song. We conducted playback experiments with cycling female mice to explore the function of male mouse songs. Using a place preference design, we show that these vocalizations elicited approach behaviour in females. In contrast, the playback of pup isolation calls or whistle-like artificial control sounds did not evoke approach responses. Surprisingly, the females also did not respond to pup isolation calls. In addition, female responses did not vary in relation to reproductive cycle, i.e. whether they were in oestrus or not. Furthermore, our data revealed a rapid habituation of subjects to the experimental situation, which stands in stark contrast to other species' responses to courtship vocalizations. Nevertheless, our results clearly demonstrate that male mouse songs elicit females' interest.

Despite their large vocal repertoires and otherwise highly versatile singing style, male mockingbirds sometimes sing in a highly repetitive fashion. We conducted a playback experiment to determine the possible signal value of different syllable presentation patterns during simulated male intrusions in the Tropical Mockingbird (Mimus gilvus) testing the hypothesis that more repetitive singing represents a stronger threat and generates a stronger aggressive response. Responses were measured in terms of approach and singing behavior and were analyzed using McGregor’s (1992) multivariate method. We also introduce the use of survival analysis for analyzing response variables for which subjects do not perform the behavior in question in at least one of the replicates (known as ‘right-censored variables’ in the statistical literature). As predicted by theory, experimental subjects responded more aggressively to songs composed of a single note than to variable ones. However, versatility at the between-song level had an opposite effect as high song switching rates generated stronger responses than low ones. Given the lack of a statistical interaction between within-song versatility and switching rate, we conclude that these two parameters may serve independent purposes and possibly transmit different information. We discuss the possibility that the signal value of variation in vocal versatility lies in the mediation of territorial conflicts, the attraction of female partners and/or the mediation of conflicts over access to reproductive females.