Latent song type memories are accessible through auditory stimulation in a hand-reared songbird

The production of learned vocalizations such as in birdsong is often used to judge whether stimuli had been memorized upon their presentation. However, failures in the imitation of certain song patterns may also reflect impaired development of motor programmes or impaired memory retrieval rather than failures in stimulus memorization during auditory acquisition. To study this issue, we confronted adult hand-reared nightingales, Luscinia megarhynchos, with interactive playback experiments and used vocal matching as a behavioural tool to investigate their song type memories. Vocal matching is a common pattern-specific response that songbirds use in territorial countersinging. We distinguished two forms of pattern-specific matching: (1) song type matching (i.e. a bird replied with the same song type as the stimulus song), and (2) song group matching (i.e. the bird replied with a different song type which was, however, sequentially associated with the playback song presented earlier, i.e. during the tutoring). Some subjects used both song type and song group matching in response to song types they had not imitated from the tutor programme prior to the playback experiments. Our results indicate that nightingales store more song types in their sensory phase than they spontaneously recall from memory as adults. That is, memories of song types that were not performed in overt behaviour could be activated by vocal interactions, here induced by the interactive playback. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Age-dependent effects of song exposure: song crystallization sets a boundary between fast and delayed vocal imitation

Song crystallization is a prominent developmental phase of oscine birds in which there is a transition from a production of plastic vocal material to a performance of elaborated song patterns that are typical for adult birds. Here we show that crystallization can be related to a marked change in memory properties involved in supplementary learning of song occurring during this phase. We studied nightingales, Luscinia megarhynchos, a species renowned for its large repertoire of song types. After a period of early tutoring as fledglings, hand-reared subjects (N=8) were exposed to a set of temporally distributed training experiences as juveniles and young adults. Analyses of the birds' singing yielded clear evidence for late song learning and also a striking phase-related shift in their memory properties. New songs heard shortly before crystallization (at an age of 40-42 weeks) were imitated within a few days and their structural and syntactical ‘quality’ seemed not to be inferior to imitations developed from songs heard earlier. In contrast, none of the songs experienced soon after song crystallization (at 45-47 weeks) appeared as imitations in the repertoires of the young adults (at 48-55 weeks). However, birds had clearly memorized these songs, as they produced imitations of them in their second spring. Our findings show that auditory song acquisition in nightingales extends well into the phase of vocal production. At the same time, however, the boundary between an immediate and a delayed form of vocal imitation suggests that song crystallization reflects a marked change in memory properties. That is, song crystallization seems to constrain the ability to develop motor programs for song patterns that are heard even though these are committed to memory. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Memory-dependent adjustment of vocal response latencies in a territorial songbird

Vocal interactions in songbirds can be used as a model system to investigate the interplay of intrinsic singing programmes (e.g. influences from vocal memories) and external variables (e.g. social factors). When characterizing vocal interactions between territorial rivals two aspects are important: (1) the timing of songs in relation to the conspecific’s singing and (2) the use of a song pattern that matches the rival’s song. Responses in both domains can be used to address a territorial rival. This study is the first to investigate the relation of the timing of vocal responses to (1) the vocal memory of a responding subject and (2) the selection of the song pattern that the subject uses as a response. To this end, we conducted interactive playback experiments with adult nightingales (Luscinia megarhynchos) that had been hand-reared and tutored in the laboratory. We analysed the subjects’ vocal response latencies towards broadcast playback stimuli that they either had in their own vocal repertoire (songs shared with playback) or that they had not heard before (unknown songs). Likewise, we compared vocal response latencies between responses that matched the stimulus song and those that did not. Our findings showed that the latency of singing in response to the playback was shorter for shared versus unknown song stimuli when subjects overlapped the playback stimuli with their own song. Moreover birds tended to overlap faster when vocally matching the stimulus song rather than when replying with a non-matching song type. We conclude that memory of song patterns influenced response latencies and discuss possible mechanisms.     

The day after: effects of vocal interactions on territory defence in nightingales

1. Models on territory acquisition and tenure predict that territorial animals benefit by adjusting territorial defence behaviour to previous challenges they had experienced within the socially complex environment of communication networks. 2. Here, we addressed such issues of social cognition by investigating persisting effects of vocal contests on territory defence behaviour in nightingales Luscinia megarhynchos (Brehm). 3. Using interactive playback during nocturnal song of subjects, a rival was simulated to countersing either aggressively (by song overlapping) or moderately (by song alternating) from outside the subjects' territory. Thereby, the time-specific singing strategy provided an experimentally controlled source of information on the motivation of an unfamiliar rival. 4. Expecting that nightingales integrate information with time, the same rival was simulated to return as a moderately singing intruder on the following morning. 5. The results show that the vigour with which male nightingales responded to the simulated intrusion of an opponent during the day depended on the nature of the nocturnal vocal interaction experienced several hours before. 6. Males that had received the song overlapping playback the preceding night approached the simulated intruder more quickly and closer and sang more songs near the loudspeaker than did males that had received a song alternating playback. 7. This adjustment of territory defence strategies depending on information from prior signalling experience suggests that integrating information with time plays an important part in territory defence by affecting a male's decision making in a communication network.     

Male-male vocal interactions and the adjustment of song amplitude in a territorial bird

Recent studies have shown that territorial songbirds do not maximize vocal amplitude. Instead, song intensity appears to be a flexible trait that is individually regulated. Given the benefits of singing loudly with regard to signal transmission in the context of territory defence and mate attraction, we investigated whether songbirds adjust the sound level of their territorial songs depending on social influences. While interacting with the playback of a simulated conspecific rival, seven male nightingales, Luscinia megarhynchos, increased the sound level of their songs, on average, by more than 5 dB. The nightingales increased their song level to significantly lower values (about 1 dB) in response to control songs of other species, so the revealed increase in vocal intensity during interactions cannot be fully explained by the acoustical masking of the interfering conspecific songs. Thus, the birds improved signal transmission to a higher degree during conspecific male-male interactions.     

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.     

Former Experience Can Modify Social Selectivity during Song Learning in the Nightingale (Luscinia megarhynchos)

Changes in preference for a specific song-learning context, characterized by close proximity of a tutor, were investigated in the nightingale, Luscinia megarhynchos. Two groups of males were tutored with conspecific song for two periods, days 42 to 56, and days 57 to 71. Song types were either presented from tape alone (group A) or were played in the presence of a familiar tutor, i.e. the person who hand-raised the birds (group B). Acquisition success did not differ between the groups for period 2. However, while males of group B acquired songs during both tutoring periods, males of group A learned only during period 2. This indicates that in nightingales the preference for a specific song-learning context decreases during development. A comparison with an earlier study suggests that this shift is not age dependent but primarily due to auditory experience with the song patterns to be learned. Such a mechanism has also been described for the termination of sensitive phases for song learning. Because song acquisition in adult nightingales does not depend any more on close spatial proximity of a familiar tutor, a male in his first spring and later on can learn from a number of singing territorial neighbours, and by this means acquire the large song-type repertoire typical for the species.     

How songbirds deal with large amounts of serial information: retrieval rules suggest a hierarchical song memory

Many songbirds develop remarkably large vocal repertoires, and this has prompted questions about how birds are able to successfully learn and use the often enormous amounts of information encoded in their various signal patterns. We have studied these questions in nightingales (Luscinia megarhynchos), a species that performs more than 200 different types of songs (strophen), or more than 1000 phonetically different elements composing the songs. In particular, we investigated whether and how both song repertoires and song performance rules of nightingales were coded by auditory stimuli presented in serial learning experiments. Evaluation of singing episodes produced by our trained birds revealed that nightingales cope well with an exposure to even long strings of master song-types. They can readily acquire information encoded within and between the different master songs, and they memorize, for example, which master song-types they have experienced in the same learning context. Imitations of such song-types form distinct sequential associations that are termed “context groups”. Additionally, nightingales develop other song-type associations that are smaller in size and termed “package groups”. Package formation results from constraints of the acquisition mechanisms which obviously lead to a segmentation of auditorily perceived master song sequences. Further experimentation validated that the song memory of nightingales is organized in a hierarchical manner and holding information about “context groups” composed of packages, “package groups” composed of songs, and songs composed of song elements. The evidence suggests that implementation of such a hierarchical organization facilitates a quick retrieval of particular songs, and thereby provides an essential prerequisite for a functionally appropriate use of large vocal repertoire is in songbirds. Received: 4 October 1997 / Accepted in revised form: 26 August 1998     

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.     

Does age matter in song bird vocal interactions? Results from interactive playback experiments

The song of oscines provides an extensively studied model of age-dependent behaviour changes. Male and female receivers might use song characteristics to obtain information about the age of a signaller, which is often related to its quality. Whereas most of the age-dependent song changes have been studied in solo singing, the role of age in vocal interactions is less well understood. We addressed this issue in a playback study with common nightingales (Luscinia megarhynchos). Previous studies showed that male nightingales had smaller repertoires in their first year than older males and males adjusted their repertoire towards the most common songs in the breeding population. We now compared vocal interaction patterns in a playback study in 12 one year old and 12 older nightingales (cross-sectional approach). Five of these males were tested both in their first and second breeding season (longitudinal approach). Song duration and latency to respond did not differ between males of different ages in either approach. In the cross-sectional approach, one year old nightingales matched song types twice as often as did older birds. Similarly, in the longitudinal approach all except one bird reduced the number of song type matches in their second season. Individuals tended to overlap songs at higher rates in their second breeding season than in their first. The higher levels of song type matches in the first year and song overlapping by birds in their second year suggest that these are communicative strategies to establish relationships with competing males and/or choosy females.     

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

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

The Return of the Intruder: Immediate and Later Effects of Different Approach Distances in a Territorial Songbird

Male songbirds often maintain territories throughout the breeding season, and one of the main functions of song is to deter invaders. Therefore, the distance of an unknown singing rival should play a crucial role within territorial singing interactions of males. This distance is expected to be assessed as more threatening the closer the rival approaches. Here, we tested this assumption by conducting nocturnal playbacks from two different distances in territorial Common nightingales (Luscinia megarhynchos). Immediate vocal responses of birds were examined by analysing changes in song structure as well as temporal response features. The next morning, follow‐up playbacks from an intermediate distance allowed us to investigate longer‐lasting effects of nocturnal playbacks. We found that the distance of a simulated rival had an effect on both immediate and later vocal responses of territorial male nightingales with different song parameters being affected during nocturnal and diurnal singing. This indicates that birds perceive intruder distances and adjust their response behaviour both immediately and in later interactions.     

Song Sharing in Neighboring and Non-Neighboring Thrush Nightingales (Luscinia luscinia) and its Implications for Communication

In many passerines, males have repertoires of different songs of which some songs are often shared with other males. Sharing of song repertoires among males can provide insights into the context in which songs were acquired and on the role of song repertoires in inter- and intrasexual communication. Here we studied repertoire sharing in male territorial thrush nightingales ( Luscinia luscinia ). We compared male vocal repertoires of the basic song components, full songs, and the sequencing of songs in a bout. The results show that males differed significantly in the size of their song repertoires but not in the size of the repertoire of basic song components. Moreover, they shared almost all (80%) the repertoire of song components but only 30% of their song types. Neighboring males shared significantly more song types than did non-neighboring males but interestingly they did not share more basic song components than non-neighboring males. These results show that the repertoire of basic song components is under much less sexual selection than the size of song repertoires. Sharing of song repertoires among neighbors presumably results from repertoire conversion over time and from males returning to their territories in the following season. Repertoire sharing then can be an indicator of territory tenure and thus it can be important in repelling rivals and in female choice.     

Noise-dependent song amplitude regulation in a territorial songbird

Some animals that use sound to communicate compensate for interference from background noise by adjusting the amplitude of their vocalizations as environmental noise levels vary. Territorial songbirds may have evolved a different strategy, since they can be expected to benefit from maximizing the amplitude of their songs to defend territories and attract females. We tested this hypothesis with calibrated measurements of the song level of male nightingales, Luscinia megarhynchos. All birds increased the sound level of their songs in response to an increase in white noise broadcast to them. A second experiment revealed that noise in the spectral region of their own songs was most effective in inducing the birds to increase vocal intensity. These findings show that nightingales do not maximize song amplitude but regulate vocal intensity dependent on the level of masking noise. The adjustment of vocal amplitude may serve to maintain a specific signal-to-noise ratio that is favourable for signal production. Concurrently, increasing the intensity of songs can maintain a given active space for communication. Thus, vocal amplitude in a territorial songbird can be interpreted as a flexible trait, which is individually regulated according to ecological demands from signal transmission. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Overlapping and matching in the song contests of black-capped chickadees

During vocal contests, animals alter both the timing and the patterning of responses to their opponents. Time-specific responses (such as overlapping an opponent's song) and pattern-specific responses (such as matching the type of an opponent's song) may reveal information about interacting animals. Here we explore the consequences of overlapping and frequency matching during song contests of male black-capped chickadees, Poecile atricapillus. Using interactive playback, we engaged birds of high and low dominance status in vocal interactions with a simulated territorial intruder. The playback intruder either overlapped or avoided overlapping the subjects' songs and either matched or avoided matching the frequency of the subjects' songs. Individuals who were overlapped by the playback intruder showed higher variability in their song length and song timing than individuals who were not overlapped. Individuals who were frequency-matched by the playback intruder responded with more agitated responses (more flights and passes over the speaker and closer distances of closest approach) and spent more time farther away from the loudspeaker. We argue that the timing of song delivery and the choice of song type are distinct functional components of vocal interactions, where overlapping and matching songs are threatening signals that have separate consequences for opponent behaviour and song performance. High-ranking males responded at greater distances from the loudspeaker in all treatments and responded with lower agitation levels than low-ranking males. We demonstrate that males of different quality show different behavioural responses to territorial intruders, where males of high status appear reluctant to engage an intruder as intensely as males of low status.     

Imitation and Invention in Song Learning in Nightingales (Luscinia megarhynchos B., Turdidae)

Song learning in oscine birds is often defined solely as a process of song imitation; nonetheless, not all songs produced by laboratory‐tutored birds are imitations of the model songs. If song learning were strictly a process of imitation, these non‐imitated songs (inventions) would be expected to contain no learned attributes. To determine whether species‐typical song attributes can be learned in the absence of imitation, we compared the imitations and inventions of laboratory‐tutored nightingales (Luscinia megarhynchos B.) with the songs of wild nightingales and the songs of laboratory‐reared, untutored nightingales. The species‐typical song attribute measured was stereotypy. We quantified stereotypy by four variables: (1) percentage of notes shared between two renditions of the same song type (2) difference in repetition rates of the same trill in two renditions of the same song type (3) acoustic similarity of the same note in two renditions of the same song type, and (4) acoustic similarity of the same note repeated within a trill. Wild songs and imitated songs were significantly more stereotypical than the songs of untutored birds for all measures. For the percentage of notes shared (1), and the acoustic similarity of notes in two renditions of the same song type (3), invented songs did not differ from the songs of untutored birds, suggesting that imitation is necessary for the acquisition of these song characteristics. However, invented songs were significantly more stereotypical than the songs of untutored birds for measures of stereotypy related to trills (2 and 4), and neither imitated nor invented songs differed significantly from the songs of wild birds in terms of trill rate stereotypy (2). Thus, it appears that the process of learning to produce trills may differ from the process of learning non‐repetitive song components: increased stereotypy in trills occurs even when the trills themselves are not copied from song models. Strict imitation does not fully account for the acquisition of some learned song attributes.     

Nightingales respond more strongly to vocal leaders of simulated dyadic interactions

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.     

Signalling through acoustic windows: nightingales avoid interspecific competition by short-term adjustment of song timing

The function of bird song is closely linked to sexual selection through female choice and male–male competition, and thus variation in communication success is likely to have major fitness consequences for a singing male. A crucial constraint on signal transmission is imposed by background noise, which may include songs from other species. I investigated whether singing nightingales (Luscinia megarhynchos) avoid temporal overlap with the songs of other bird species in a playback experiment. I analysed the temporal song patterns of six males, each of which were exposed to songs of other species. The nightingales significantly avoided overlapping their songs with the playback songs, and started singing preferentially during the silent intervals between the heterospecific songs. This timing of song onset produced a greater variability in pause duration compared to the nightingales’ undisturbed solo singing. These findings suggest that birds adjust their song timing to avoid acoustic interference on short temporal scales, and thus are able to improve the efficiency of acoustic communication in complex sonic environments. Moreover, the results indicate that temporal song patterns can be affected by the songs of other species, and thus such influences should be taken into account when studying bird song in the field.     

Are northern mockingbirds classic open-ended song learners?

The northern mockingbird (Mimus polyglottos, Linnaeus) is considered a classic example of a species in which individuals learn songs throughout adulthood, but this assumption has not been tested rigorously. To assess whether mockingbirds should be categorized as open-ended learners, I conducted a longitudinal study and a field-based song-tutoring experiment. I recorded songs from 15 free-living, banded, adult males in an earlier year and a later year, and I classified 400 mimetic songs per year per individual, based on the species and vocalization type mimicked. For two of these “mimetic types,” I further classified all the song types of all individuals in their early and later samples. The number of song types increased significantly across years for both mimetic types, and the average number of observed mimetic types per individual was 46.4 and 47.7 in the early and late samples (p = .055). I found no evidence adults learned any tutor stimuli after six months of tutoring, but examples from the scientific literature suggest the tutoring regime might not have been adequate to pass the motivational threshold required for learning. I conclude that mockingbirds probably are open-ended learners, but that future research is needed to verify experimentally that adults can indeed imitate novel song types.     

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

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