The most language-like aspect of the song of songbirds is its development: as with human speech, birdsong develops through vocal production learning, in which individuals modify the structure of ...their vocalizations in response to experience with the vocalizations of others. As is true of speech development, birdsong learning qualifies as a cognitive ability, as it involves the acquisition, storage and processing of information obtained from the environment. Accordingly, if cognitive abilities are in general positively associated in songbirds, as has been argued for humans and other mammals, then song learning ability should be positively associated with other cognitive abilities, and learned attributes of song should serve as an indicator of domain-general cognition. A review of studies in which songbirds have been subjected to batteries of cognitive tasks finds, however, that different cognitive measures are not consistently positively associated. Moreover, learned attributes of birdsong do not show consistent positive associations with other cognitive measures. These results argue that, rather than being a component of domain-general cognition, song learning is an autonomous cognitive module. Birdsong learning shows other characteristics of modularization in that it is domain specific, is based on a localized and highly structured neural system and exhibits a level of innate specification. Whether language learning in humans is similarly modularized has been much debated. Despite a possible difference in modularization, much can be learned about the evolution of human language learning from studying birdsong learning. Aspects of birdsong learning that are especially relevant include vocal interaction learning, pragmatics and the initial selective benefits and neural underpinnings of vocal production learning.
•Song learning in songbirds satisfies the criteria for a cognitive task.•Different cognitive abilities do not tend to be positively associated in songbirds.•Measures of song quality are not correlated with cognitive performance measures.•Song learning is likely an autonomous cognitive module in songbirds.•Birdsong learning can teach us much about the evolution of language learning.
Many birds emit tonal song syllables even though the sound sources generate sound with rich upper harmonic energy content. This tonality is thought to arise in part from dynamically adjusted ...filtering of harmonic content. Here, we compare tonality of song syllables between vocal learners and non-learners to assess whether this characteristic is linked to the increased neural substrate that evolved with vocal learning. We hypothesize that vocal learning ability is correlated with enhanced ability for generating tonal sounds, because vocal production learners might also have an enhanced ability to articulate their vocal tracts and sound source for producing tonality. To test this hypothesis, we compared vocal learners and non-learners from two groups (186 passerines and 42 hummingbirds) by assessing tonality of song syllables. The data suggest that vocal learners in both clades have evolved to sing songs with higher tonality than the related, non-vocal learning clades, which is consistent with stronger roles for broadband dynamic filtering and adjustments to the sound source. In addition, oscine songs display higher tonality than those of hummingbirds. A complex interplay of vocal tract biomechanics, anatomical differences of the sound source as well as increased motor control through vocal learning facilitates generation of broad tonality.
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.
The northern mockingbird (Mimus polyglottos) is considered a classic example of a species in which individuals learn songs throughout adulthood, but this assumption has not been tested rigorously. Longitudinal song data from 15 free‐living, banded, adult males in an earlier year and a later year showed limited evidence for song‐learning (paired t test, t14 = 2.09, p = .055). Furthermore, a field song‐tutoring experiment produced no evidence adults learned from tutors.
Although the effects of learning on song structure have been extensively studied in songbirds, little attention has been given to the learning of syntax at the level of song sequences. Here we ...investigate song syntax learning in two cohorts of hand-reared song sparrows, Melospiza melodia: an isolate group, consisting of four males raised with no exposure to external song models, and a trained group, consisting of 17 males exposed to recorded song sequences during the sensitive period for song learning. The isolate males followed three syntactical rules previously described for field-recorded song sparrows: (1) they produced their song type repertoires with eventual variety, repeating a song type multiple times before switching to another; (2) they cycled through their repertoires using close to the minimum number of bouts; and (3) they showed consistent preferences for singing certain of their song types more than others. The trained males were tutored with sequences with exaggerated eventual variety and cycling patterns and no usage preferences, but their syntax was little affected by any of these training features. One syntactical pattern that was affected by external experience was the rule that long bouts of a song type are followed by long recurrence intervals before that type is produced again. Isolate males showed no bout length/recurrence interval correlations while trained males showed reduced correlations relative to field-recorded males, implicating learning in the development of the normal pattern. Other songbird species have been found to preferentially use song type transitions as adults that they were tutored with as juveniles, but the trained song sparrows in this study showed no evidence of such effects.
•We examined the development of between-song syntax in song sparrows.•Singing with eventual variety is one syntactical pattern little affected by learning.•A second is the tendency to cycle efficiently through the song type repertoire.•Song sparrows do not learn first-order transition preferences from tutor sequences.•Usage learning is thus less prevalent than vocal production learning in this species.
Recent research has established the importance of animal personality traits in behavioural ecology, encompassing domains such as mate choice, cognition and social interactions. However, less is known ...about how personality traits predict parental behaviour. In the current study, we investigate these relationships in the zebra finch, Taeniopygia gutatta, a species that provides biparental care and in which social feedback from parents shapes juvenile song learning. Adults were first assessed on exploratory tendency in a novel environment, then allowed to pair and rear cross-fostered young. Birds were housed in single-family cages within the colony, allowing for visual and auditory interaction between families. We examined foster parent–juvenile interactions over the course of song learning (35–65 days posthatch), recording parental responsiveness (responses contingent on juvenile songs) as these responses are known to influence song learning outcomes. Exploration scores predicted parental responsiveness in contrasting ways: low-exploring males provided more contingent responses to the immature song of juveniles, while high-exploring females increased their responsiveness to a greater degree over the course of juvenile song development. Over the period of offspring song development, females were more responsive to changes in juvenile vocal production, increasing the number of responses provided as juveniles increased their rate of singing. In contrast, males were less variable in their response rate across development; their contingent singing was not sensitive to changes in the rate of juvenile singing. The importance of exploration as a predictor of parental responsiveness to offspring behaviour demonstrates the possible significance of previous findings that adults pair based on the trait of exploration.
•Previous studies have shown that adults pair on the basis of exploration.•We examine whether exploration predicts parental responsiveness to juveniles' song.•Low-exploring males provided more contingent responses to offspring song.•High-exploring females increased their responsiveness to offspring song over time.•Sex differences in responsiveness may stem from differences in reproductive strategy.
Active guidance of vocal learning by conspecifics has recently been found in several species, including some cetaceans and primates. However, in the zebra finch, Taeniopygia guttata, a commonly ...studied songbird, vocal learning was traditionally considered the product of memorization and imitation of a song model. Only recently have specific social feedback cues been shown to enhance song learning. What mechanisms drive the superior learning associated with social interactions? We recently found that ‘fluff-ups’, a nonvocal female arousal cue, facilitated song learning when played over video contingently on juvenile song production throughout development. However, it is unknown whether adults naturally respond in a contingent fashion to immature song, and whether young finches incorporate naturally occurring feedback into song learning. To investigate whether social influences affect song learning, the present study addressed the nature and significance of maternal and paternal cues associated with song development. We recorded unmanipulated zebra finch families throughout juvenile development and analysed their social interactions. We found that behaviours of both parents were associated with offspring song outcomes. Juvenile song learning could be predicted by the amount of contingent ‘fluff-up’ behaviours they received from their mothers throughout development. Fathers often sang immediately after a juvenile had sung, and paternal singing after juvenile singing was positively correlated with more accurate song learning in their sons. Conversely, when fathers sang before the juvenile sang, juveniles learned song less accurately. Our data suggest that parental vocal and gestural feedback plays a reinforcing role for song learning in zebra finches. There are many nonavian species, including chiropterans, pachyderms and pinnipeds, that modify their vocalizations in different developmental or social contexts but whose mechanisms of vocal learning are not known. Our findings suggest that these species should be closely examined for adult sensitivity to immature vocalizations and developmental capacity to learn from social feedback.
•Social interaction enhances song learning in some birds, but mechanisms are unknown.•Zebra finch parents naturally display contingent responses to juvenile plastic song.•Song learning significantly correlated with contingent maternal ‘fluff-ups’.•Juvenile song accuracy positively correlated with contingent paternal song.•Parental gestural and vocal feedback may reinforce song learning.
Environmental changes caused by urbanization and noise pollution can have profound effects on acoustic communication. Many organisms use higher sound frequencies in urban environments with ...low-frequency noise, but the developmental and evolutionary mechanisms underlying these shifts are generally unknown. We used a common garden experiment to ask whether changes in minimum song frequency observed 30 years after a songbird colonized an urban environment are a consequence of behavioural flexibility. We captured male juvenile dark-eyed juncos, Junco hyemalis thurberi, from two populations (urban and mountain) soon after they reached independence (aged 25–40 days), raised them in identical indoor aviaries and studied their songs at an age of 3 years. We found that the large population difference in minimum frequency observed in the field persisted undiminished in the common garden despite the absence of noise. We also found some song sharing between the common garden and natal field populations, indicating that early song memorization before capture could contribute to the persistent song differences in adulthood. These results are the first to show that frequency shifts in urban birdsong are maintained in the absence of noise by genetic evolution and/or early life experiences.
•Animals in urban environments often produce higher-frequency sounds.•Frequency differences of urban and rural birds persisted in a quiet, common garden.•Higher minimum frequencies of urban birds are not a plastic response to noise.•Genetic evolution and/or early life experiences appear to cause this difference.•Urban environments may rapidly generate permanent shifts in song frequencies.
Social communication often involves vocal learning, whereby young animals learn their vocalizations early in life by imitating the sounds of adults. In animals that learn their vocalizations, it is ...common to find patterns of geographical variation known as ‘vocal dialects’, acoustic features shared within a cluster of animals that differ from the vocalizations of animals in nearby clusters. Dialects may form when animals learn their vocalizations early in life and then disperse short distances, or when they modify their vocalizations to match local vocal patterns after dispersal. Dialects are typically studied at a regional or continental scale, but they may also persist at smaller scales in so-called ‘microgeographical song dialects’ or ‘microdialects’. Microdialects have received little research attention. In this study, we investigate microdialects and dispersal distance in song-learning Savannah sparrows, Passerculus sandwichensis, through a 4-year study of birds living on three islands in the Bay of Fundy, Canada. Our analyses yield evidence of microgeographical variation: birds showed higher acoustic similarity to their neighbours than to faraway individuals in the same population. When we classified songs on the basis of their highly variable middle sections, we found that particular song types formed spatial clusters of similar-sounding individuals. Therefore, acoustic variation in Savannah sparrow song appears to show dialects across small geographical distances. In an analysis of dispersal from natal sites to breeding sites, we found a median distance of 189 m, consistent with previous findings. Our results suggest that limited dispersal distances, combined with the social processes of vocal learning (overproduction and selective attrition), likely contribute to the presence of microdialects.
•Vocal dialects are well known at broad scales, but rarely studied at small scales.•We studied microdialects in Savannah sparrows over 4 years on three islands.•The songs of males were more similar to those of neighbours than to distant birds.•Savannah sparrows dispersed short distances from their natal nest.•Thus, local song learning and limited dispersal likely give rise to microdialects.
Assortative mating depends on species distinctiveness in mating traits and preferences, which can be challenging to maintain when traits and/or preferences are learned. This is because learning may ...cause individuals to copy heterospecific signals. Juvenile songbirds possess innate sensory biases favouring them to learn and to prefer conspecific songs, but the effectiveness of these biases relies on consistent and sufficient differences between the songs produced by different species. However, mating signals, including learned songs, sometimes converge in sympatry, and the species-specific cues that individuals use to shape their preferences are often unknown. In Ficedula flycatchers, a stereotyped and highly species-specific alarm call is often incorporated as the first syllable of their songs. However, where the two species co-occur, pied flycatchers, Ficedula hypoleuca, learn to incorporate the introductory calls of the closely related collared flycatcher, Ficedula albicollis, into their songs. In this study, we investigated the role of introductory alarm calls for song discrimination in collared flycatchers, using playback experiments of both manipulated and unmanipulated songs on adults and nestlings within the hybrid zone of Öland, Sweden. We predicted that the introductory alarm call would be sufficient to trigger song responses, such that adults and nestlings would respond similarly to song phrases including the call, whether it is followed by conspecific or heterospecific notes. Our results provide evidence that the introductory alarm call is sufficient to trigger song discrimination in nestlings, but not in adult males, potentially due to their greater experience with songs and, therefore, subtler discrimination. Altogether, this study highlights the often-overlooked importance of calls within or associated with songs.
•Collared flycatchers often start their songs with an alarm call.•The alarm call seems sufficient to drive song responses in nestlings.•We argue that the call could guide learning onto appropriate songs.•However, the call alone is unlikely to be sufficient for discrimination in adults.•We discuss the broader implication of incorporation of calls into songs.
•Early exposure to salient cues can critically shape the development of social behaviors.•Different acoustic playbacks in ovo alter genome-wide methylation of the auditory forebrain in late-stage ...zebra finch embryos.•Immediate early gene activation is negatively correlated to relative global methylation in the same sample of individuals.•The data support a methylation-mediated embryonic acoustic programming hypothesis for songbird social and communicative behavioral development.
Early exposure to salient cues can critically shape the development of social behaviors. For example, both oscine birds and humans can hear and learn to recognize familiar sounds in ovo and in utero and recognize them following hatching and birth, respectively. Here we demonstrate that different chronic acoustic playbacks alter genome-wide methylation of the auditory forebrain in late-stage zebra finch (Taeniopygia guttata) embryos. Within the same subjects, immediate early gene activation in response to acute con- or heterospecific song exposure is negatively correlated with methylation extent in response to repeated daily prior exposure to the same type of stimuli. Specifically, we report less relative global methylation following playbacks of conspecific songs and more methylation following playbacks of distantly-related heterospecific songs. These findings offer a neuroepigenomic mechanism for the ontogenetic impacts of early acoustic experiences in songbirds.
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