Avian vocal mimicry: a unified conceptual framework

Mimicry is a classical example of adaptive signal design. Here, we review the current state of research into vocal mimicry in birds. Avian vocal mimicry is a conspicuous and often spectacular form of animal communication, occurring in many distantly related species. However, the proximate and ultimate causes of vocal mimicry are poorly understood. In the first part of this review, we argue that progress has been impeded by conceptual confusion over what constitutes vocal mimicry. We propose a modified version of Vane‐Wright's (1980) widely used definition of mimicry. According to our definition, a vocalisation is mimetic if the behaviour of the receiver changes after perceiving the acoustic resemblance between the mimic and the model, and the behavioural change confers a selective advantage on the mimic. Mimicry is therefore specifically a functional concept where the resemblance between heterospecific sounds is a target of selection. It is distinct from other forms of vocal resemblance including those that are the result of chance or common ancestry, and those that have emerged as a by‐product of other processes such as ecological convergence and selection for large song‐type repertoires. Thus, our definition provides a general and functionally coherent framework for determining what constitutes vocal mimicry, and takes account of the diversity of vocalisations that incorporate heterospecific sounds. In the second part we assess and revise hypotheses for the evolution of avian vocal mimicry in the light of our new definition. Most of the current evidence is anecdotal, but the diverse contexts and acoustic structures of putative vocal mimicry suggest that mimicry has multiple functions across and within species. There is strong experimental evidence that vocal mimicry can be deceptive, and can facilitate parasitic interactions. There is also increasing support for the use of vocal mimicry in predator defence, although the mechanisms are unclear. Less progress has been made in explaining why many birds incorporate heterospecific sounds into their sexual displays, and in determining whether these vocalisations are functionally mimetic or by‐products of sexual selection for other traits such as repertoire size. Overall, this discussion reveals a more central role for vocal mimicry in the behavioural ecology of birds than has previously been appreciated. The final part of this review identifies important areas for future research. Detailed empirical data are needed on individual species, including on the structure of mimetic signals, the contexts in which mimicry is produced, how mimicry is acquired, and the ecological relationships between mimic, model and receiver. At present, there is little information and no consensus about the various costs of vocal mimicry for the protagonists in the mimicry complex. The diversity and complexity of vocal mimicry in birds raises important questions for the study of animal communication and challenges our view of the nature of mimicry itself. Therefore, a better understanding of avian vocal mimicry is essential if we are to account fully for the diversity of animal signals.     

Clicks and Communication: The Behavioural and Social Contexts of Hector's Dolphin Vocalizations

Hector's dolphins (Cephalorhynchus hectori) have a simple vocal repertoire, consisting almost entirely of ultrasonic clicks. They produce no whistles, and very few audible sounds. To examine acoustic communication in this species I analysed the relationship between click types and behaviour. The proportion of complex click types was greater in large groups, suggesting that these sounds have social significance. Clicks having 2 peaks in their time envelope and two frequency peaks were strongly associated with behaviours indicative of feeding. High pulse rate sounds, in which the repetition rate of ultrasonic clicks was audible as a “cry”, were most strongly associated with aerial behaviours. These data suggest that echo-location is not the sole function of Hector's dolphin clicks, and that echo-location and communication are likely to be closely linked. I hypothesize that dolphins may have the ability to gather information from the echoes of each other's sonar pulses. This may reduce the need for a large number of vocal signals, and may explain the apparent simplicity of the acoustic repertoires of some odontocetes.     

Cross-Taxa Similarities in Affect-Induced Changes of Vocal Behavior and Voice in Arboreal Monkeys

Measuring the affective state of an individual across species with comparable non-invasive methods is a current challenge in animal communication research. This study aims to explore to which extent affect intensity is conveyed in the vocal behaviours of three nonhuman primate species (Campbell''s monkeys, De Brazza''s monkeys, red-capped mangabeys), which vary in body size, ecological niche and social system. Similarly in the three species, we experimentally induced a change in captive social groups'' affect by locking all group members together in their outside enclosure. The two experimental conditions which varied in affect intensity consisted in imposing a pre-reunion 90 mn-separation by splitting up the respective group into two subgroups (High affect condition) or not (Low affect condition). We measured call rates as well as voice features at the time of reunion in both conditions. The three studied species reacted in a very similar way. Across species, call rates changed significantly between the behaviourally defined states. Furthermore, contact call duration and, to some extent, voice pitch increased. Our results suggest, for the first time in arboreal Old World monkeys, that affect intensity is conveyed reliably in vocal behaviour and specific acoustic characteristics of voice, irrespective of body size and ecological niche differences between species. Cross-taxa similarities in acoustic cues of affect intensity point to phylogenetic constraints and inheritance from a common ancestor, whereas variations in vocal behaviour and affect intensity-related acoustic cues between species may be an adaptation to specific social requirements and depend on social systems. Our findings as well as a comparison with published works on acoustic communication in other vertebrate groups support the hypothesis that affect intensity in human voice originates from precursors already found deep inside the vertebrate phylogeny.     

Structural Classification of Wild Boar (Sus scrofa) Vocalizations

Determining whether a species' vocal communication system is graded or discrete requires definition of its vocal repertoire. In this context, research on domestic pig (Sus scrofa domesticus) vocalizations, for example, has led to significant advances in our understanding of communicative functions. Despite their close relation to domestic pigs, little is known about wild boar (Sus scrofa) vocalizations. The few existing studies, conducted in the 1970s, relied on visual inspections of spectrograms to quantify acoustic parameters and lacked statistical analysis. Here, we use objective signal processing techniques and advanced statistical approaches to classify 616 calls recorded from semi‐free ranging animals. Based on four spectral and temporal acoustic parameters—quartile Q25, duration, spectral flux, and spectral flatness—extracted from a multivariate analysis, we refine and extend the conclusions drawn from previous work and present a statistically validated classification of the wild boar vocal repertoire into four call types: grunts, grunt‐squeals, squeals, and trumpets. While the majority of calls could be sorted into these categories using objective criteria, we also found evidence supporting a graded interpretation of some wild boar vocalizations as acoustically continuous, with the extremes representing discrete call types. The use of objective criteria based on modern techniques and statistics in respect to acoustic continuity advances our understanding of vocal variation. Integrating our findings with recent studies on domestic pig vocal behavior and emotions, we emphasize the importance of grunt‐squeals for acoustic approaches to animal welfare and underline the need of further research investigating the role of domestication on animal vocal communication.     

Restricted responsiveness to noise interference in two anurans from the southern temperate forest

Animals adopt different strategies to communicate by means of sound in noisy environments such that some species increase, while others decrease their vocal activity in the presence of interference. Anuran amphibians from diverse latitudes exhibit both kinds of responses. Recent studies have shown that males of Batrachyla taeniata and Batrachyla antartandica from the temperate austral forest do not call in response to the presentation of advertisement calls of sympatric congeneric species. In contrast, Batrachyla leptopus responds to these signals in a similar way as to conspecific calls. The responsiveness of B. taeniata to natural abiotic interference has also been tested and found that noises of such sources produce strong increases in vocal activity. To assess the diversity in responsiveness to acoustic intrusion in this group, we exposed males of B. leptopus and B. antartandica to prolonged pre‐recorded natural abiotic noises of wind, creek, rain, and to a band‐pass noise centered at 2,000 Hz, at 67 dB Sound Pressure Level (SPL). The subjects did not increase their vocal activity significantly when exposed to these sounds and to band‐pass noise at increasing intensities (55–79 dB SPL). These results contrast with the increase in vocal activity observed previously in B. taeniata to continuous abiotic noise and point to the existence of diverse strategies to confront acoustic intrusion among related species. The lack of vocal activation observed also contrasts with the responsiveness of B. leptopus to heterospecific signals, but parallels the lack of response to such sounds in B. antartandica. Furthermore, the results obtained contrast with the responsiveness of these species to synthetic prolonged sounds observed in previous studies, suggesting that the modes of responses to acoustic intrusion may depend on previous experience, rather than having a species‐specific nature.     

Antiphonal Vocalization of a Subterranean Rodent, the Naked Mole-Rat (Heterocephalus glaber)

Acoustic signalling is one of the most common communication mediums in a broad range of social animals, and it often encodes attributes of the signaller such as sex, kin relatedness and dominance rank. Particularly, antiphonal vocalization has been regarded to have an important function in animals living in an environment where visual cues are unreliable. Antiphony enables to acknowledge that one's signal was received with certainty. We show the first evidence of such acoustic signals among rodents: the naked mole‐rat. The society of this eusocial subterranean species is organized hierarchically according to body size. Naked mole‐rats are functionally blind, and rely highly on acoustic communication. We focused on one of their vocalizations: the soft chirp (SC). SCs are the most frequent sounds, and are often emitted upon physical contact. We expected the SC to be antiphonal, and if so, SC may function to distinguish colony members from intruders, and/or identify social rank and individuality. To examine our predictions, we placed pairs of individuals of different size together, and recorded their vocal behaviour. The intervals between the SCs of two individuals were shorter than expected intervals which were based on the assumption that animals vocalized without reference of the preceding SC. The acoustic properties of SCs varied among individuals according to body weight and colony of origin. The emission rate was positively related to the relative difference in body weight. Therefore, SCs have an antiphonal nature and may function as expected. These characteristics of SC were highly similar to those of antiphonal sounds in other social species.     

Social and vocal behavior in adult greater tube-nosed bats (Murina leucogaster)

Many studies have revealed the significant influence of the social nature and ecological niche of a species on the design and complexity of their communication sounds. The knowledge of communication sounds and particularly of the flexibility in their use among mammals, however, remains patchy. Being highly vocal and social, bats are well suited for investigating vocal plasticity as well as vocal diversity. Thus, the overall aim of this study was to test the presence of structural overlap between calls used in social communication and echolocation pulses emitted during foraging in greater tube-nosed bats (Murina leucogaster). Acoustic analysis and spectrotemporal decomposition of calls revealed a rich communication repertoire comprising 12 simple syllables and 5 composites with harmonics in the ultrasonic range. Simultaneous recording of vocal and social behavior in the same species yielded a strong correspondence between distinct behaviors and specific call types in support of Morton's motivation-structure hypothesis. Spectrographic analysis of call types also revealed the presence of modified components of echolocation pulses embedded within social calls. Altogether, the data suggest that bats can parse complex sounds into structurally simpler components that are recombined within behaviorally meaningful and multifunctional contexts.     

Music in Our Ears: The Biological Bases of Musical Timbre Perception

Timbre is the attribute of sound that allows humans and other animals to distinguish among different sound sources. Studies based on psychophysical judgments of musical timbre, ecological analyses of sound''s physical characteristics as well as machine learning approaches have all suggested that timbre is a multifaceted attribute that invokes both spectral and temporal sound features. Here, we explored the neural underpinnings of musical timbre. We used a neuro-computational framework based on spectro-temporal receptive fields, recorded from over a thousand neurons in the mammalian primary auditory cortex as well as from simulated cortical neurons, augmented with a nonlinear classifier. The model was able to perform robust instrument classification irrespective of pitch and playing style, with an accuracy of 98.7%. Using the same front end, the model was also able to reproduce perceptual distance judgments between timbres as perceived by human listeners. The study demonstrates that joint spectro-temporal features, such as those observed in the mammalian primary auditory cortex, are critical to provide the rich-enough representation necessary to account for perceptual judgments of timbre by human listeners, as well as recognition of musical instruments.     

Vocal production in nonhuman primates: Acoustics,physiology, and functional constraints on “honest” advertisement

The physiological mechanisms and acoustic principles underlying sound production in primates are important for analyzing and synthesizing primate vocalizations, for determining the range of calls that are physically producible, and for understanding primate communication in the broader comparative context of what is known about communication in other vertebrates. In this paper we discuss what is known about vocal production in nonhuman primates, relying heavily on models from speech and musical acoustics. We first describe the role of the lungs and larynx in generating the sound source, and then discuss the effects of the supralaryngeal vocal tract in modifying this source. We conclude that more research is needed to resolve several important questions about the acoustics of primate calls, including the nature of the vocal tract's contribution to call production. Nonetheless, enough is known to explore the implications of call acoustics for the evolution of primate communication. In particular, we discuss how anatomy and physiology may provide constraints resulting in “honest” acoustic indicators of body size. © 1995 Wiley-Liss, Inc.     

Investigating the potential for call combinations in a lifelong vocal learner

The ability for humans to create seemingly infinite meaning from a finite set of sounds has likely been a critical component in our success as a species, allowing the unbounded communication of information. Syntax, the combining of meaningful sounds into phrases, is one of the primary features of language that enables this extensive expressivity. The evolutionary history of syntax, however, remains largely debated, and it is only very recently that comparative data for syntax in animals have been revealed. Here, we provide further evidence for a structural basis of potential syntactic‐like call combinations in the vocal communication system of a group‐living songbird. Acoustic analyses indicate that Western Australian magpies (Gymnorhina tibicen dorsalis) structurally combine generic alarm calls with acoustically distinct alert calls to produce an alarm alert sequence. These results are distinct from previous examples of call combinations as, to our knowledge, evidence for this capacity is yet to be demonstrated in the natural communication of a non‐human species that is capable of vocal learning throughout life. These findings offer prospects for experimental investigation into the presence and function of magpie call combinations, extending our understanding of animal vocal complexity.     

Acoustic communication and the evolution of hearing in fishes

Fishes have evolved a diversity of sound-generating organs and acoustic signals of various temporal and spectral content. Additionally, representatives of many teleost families such as otophysines, anabantoids, mormyrids and holocentrids possess accessory structures that enhance hearing abilities by acoustically coupling air-filled cavities to the inner ear. Contrary to the accessory hearing structures such as Weberian ossicles in otophysines and suprabranchial chambers in anabantoids, sonic organs do not occur in all members of these taxa. Comparison of audiograms among nine representatives of seven otophysan families from four orders revealed major differences in auditory sensitivity, especially at higher frequencies (> 1 kHz) where thresholds differed by up to 50 dB. These differences showed no apparent correspondence to the ability to produce sounds (vocal versus non-vocal species) or to the spectral content of species-specific sounds. In anabantoids, the lowest auditory thresholds were found in the blue gourami Trichogaster trichopterus, a species not thought to be vocal. Dominant frequencies of sounds corresponded with optimal hearing bandwidth in two out of three vocalizing species. Based on these results, it is concluded that the selective pressures involved in the evolution of accessory hearing structures and in the design of vocal signals were other than those serving to optimize acoustic communication.     

Vocal Learning in Songbirds and Humans: A Retrospective in Honor of Peter Marler

Peter Marler made a number of significant contributions to the field of ethology, particularly in the area of animal communication. His research on birdsong learning gave rise to a thriving subfield. An important tenet of this growing subfield is that parallels between birdsong and human speech make songbirds valuable as models in comparative and translational research, particularly in the case of vocal learning and development. Decades ago, Marler pointed out several phenomena common to the processes of vocal development in songbirds and humans—including a dependence on early acoustic experience, sensitive periods, predispositions, auditory feedback, intrinsic reinforcement, and a progression through distinct developmental stages—and he advocated for the value of comparative study in this domain. We review Marler's original comparisons between birdsong and speech ontogeny and summarize subsequent progress in research into these and other parallels. We also revisit Marler's arguments in support of the comparative study of vocal development in the context of its widely recognized value today.     

SIGNAL DESIGN AND PERCEPTION IN HYPOCNEMIS ANTBIRDS: EVIDENCE FOR CONVERGENT EVOLUTION VIA SOCIAL SELECTION

Natural selection is known to produce convergent phenotypes through mimicry or ecological adaptation. It has also been proposed that social selection—i.e., selection exerted by social competition—may drive convergent evolution in signals mediating interspecific communication, yet this idea remains controversial. Here, we use color spectrophotometry, acoustic analyses, and playback experiments to assess the hypothesis of adaptive signal convergence in two competing nonsister taxa, Hypocnemis peruviana and H. subflava (Aves: Thamnophilidae). We show that the structure of territorial songs in males overlaps in sympatry, with some evidence of convergent character displacement. Conversely, nonterritorial vocal and visual signals in males are strikingly diagnostic, in line with 6.8% divergence in mtDNA sequences. The same pattern of variation applies to females. Finally, we show that songs in both sexes elicit strong territorial responses within and between species, whereas songs of a third, allopatric and more closely related species (H. striata) are structurally divergent and elicit weaker responses. Taken together, our results provide compelling evidence that social selection can act across species boundaries to drive convergent or parallel evolution in taxa competing for space and resources.     

Perception of timbral analogies.

Recent studies have investigated the structure of perceptual relations among musical instrument timbres by multidimensional scaling (MDS) techniques. These studies have employed both acoustically produced tones and digitally synthesized imitations and hybrids of acoustic instrument tones. The analyses of dissimilarity ratings for all pairs of a set of tones are usually represented as geometrical structures in a two- or three-dimensional Euclidean space in which the shared 'perceptual' axes are shown to have a qualitative correspondence to acoustic properties such as spectral energy distribution, onset characteristics and degree of change in spectral distribution over the duration of the tone. The present study took as a point of departure a MDS analysis for complex, synthetic tones with the aim of testing whether musician and non-musician listeners used the relations defined by the perceptual space to perform an analogies task of the sort: timbre A is to timbre B as timbre C is to which of two possible timbres, D or D'? A parallelogram model was used to select the D timbres: if the relation between A and B is represented as a vector with both magnitude and direction components, then the appropriate D should form a vector with C having similar magnitude and direction in the timbre space. Aside from conceptual difficulties with the task for both non-musicians and composers, choices for both groups provide support for the parallelogram model indicating a capacity in listeners to perceive abstract relations among the timbres of complex sounds without specific training in such a task.     

Vocal mimicry by the Black-browed Reed Warbler Acrocephalus bistrigiceps: objective identification of mimetic sounds

Vocal mimicry by the Black-browed Reed Warbler Acrocephalus bistrigiceps was investigated. To identify mimicry objectively, we measured similarities between the sounds of models and those of Warblers by means of Principal Component Analysis (PCA) using a set of acoustic parameters. Of the sounds suspected of being mimicry according to visual inspection of sonagrams, only 57% were identifiable as mimicry according to PCA. Previous studies have not included quantitative criteria for assessing vocal mimicry, and our results suggest that judgements might not be reliable in the absence of objective criteria. Male Warblers incorporated the mimetic sounds into their songs, and each male mimicked 2–5 species. We found no evidence that females preferred males with large mimetic repertoires. This suggests that vocal mimicry has not evolved in response to selection by females in this species, although our analysis did not reveal entire mimetic repertoires in the Warbler songs.     

Vocal Signature in Wild Infant Chimpanzees

A large array of communication signals supports the fission/fusion social organization in chimpanzees, and among them the acoustic channel plays a large part because of their forest habitat. Adult vocalizations convey social and ecological information to their recipients allowing them to obtain cues about an ongoing event from calls only. In contrast to adult vocalizations, information encoded in infant calls had been hardly investigated. Studies mainly focused on vocal development. The present article aims at assessing the acoustic cues that support individual identity coding in infant chimpanzees. By analyzing recordings performed in the wild from seven 3‐year‐old infant chimpanzees, we showed that their calls support a well‐defined individual vocal signature relying on spectral cues. To assess the reliability of the signature across the calls of an individual, we defined two subsets of recordings on the basis of the characteristics of the frequency modulation (whimpers and screams) and showed that both call types present a reliable vocal signature. Early vocal signature may allow the mother and other individuals in the group to identify the infant caller when visual contact is broken. Chimpanzee mothers may have developed abilities to cope with changing vocal signatures while their infant, still vulnerable, gains in independence in close habitat. Am. J. Primatol. 75:324‐332, 2013. © 2012 Wiley Periodicals, Inc.     

Auditory–vocal mirroring in songbirds

Mirror neurons are theorized to serve as a neural substrate for spoken language in humans, but the existence and functions of auditory–vocal mirror neurons in the human brain remain largely matters of speculation. Songbirds resemble humans in their capacity for vocal learning and depend on their learned songs to facilitate courtship and individual recognition. Recent neurophysiological studies have detected putative auditory–vocal mirror neurons in a sensorimotor region of the songbird''s brain that plays an important role in expressive and receptive aspects of vocal communication. This review discusses the auditory and motor-related properties of these cells, considers their potential role on song learning and communication in relation to classical studies of birdsong, and points to the circuit and developmental mechanisms that may give rise to auditory–vocal mirroring in the songbird''s brain.     

GEOGRAPHIC VARIATION IN THE SONGS OF NEOTROPICAL SINGING MICE: TESTING THE RELATIVE IMPORTANCE OF DRIFT AND LOCAL ADAPTATION

Patterns of geographic variation in communication systems can provide insight into the processes that drive phenotypic evolution. Although work in birds, anurans, and insects demonstrates that acoustic signals are sensitive to diverse selective and stochastic forces, processes that shape variation in mammalian vocalizations are poorly understood. We quantified geographic variation in the advertisement songs of sister species of singing mice, montane rodents with a unique mode of vocal communication. We tested three hypotheses to explain spatial variation in the song of the lower altitude species, Scotinomys teguina: selection for species recognition in sympatry with congener, S. xerampelinus, acoustic adaptation to different environments, and stochastic divergence. Mice were sampled at seven sites in Costa Rica and Panamá; genetic distances were estimated from mitochondrial control region sequences, between‐site differences in acoustic environment were estimated from climatic data. Acoustic, genetic and geographic distances were all highly correlated in S. teguina, suggesting that population differentiation in song is largely shaped by genetic drift. Contrasts between interspecific genetic‐acoustic distances were significantly greater than expectations derived from intraspecific contrasts, indicating accelerated evolution of species‐specific song. We propose that, although much intraspecific acoustic variation is effectively neutral, selection has been important in shaping species differences in song.     

Suffixation influences receivers' behaviour in non-human primates

Compared to humans, non-human primates have very little control over their vocal production. Nonetheless, some primates produce various call combinations, which may partially offset their lack of acoustic flexibility. A relevant example is male Campbell''s monkeys (Cercopithecus campbelli), which give one call type (‘Krak’) to leopards, while the suffixed version of the same call stem (‘Krak-oo’) is given to unspecific danger. To test whether recipients attend to this suffixation pattern, we carried out a playback experiment in which we broadcast naturally and artificially modified suffixed and unsuffixed ‘Krak’ calls of male Campbell''s monkeys to 42 wild groups of Diana monkeys (Cercopithecus diana diana). The two species form mixed-species groups and respond to each other''s vocalizations. We analysed the vocal response of male and female Diana monkeys and overall found significantly stronger vocal responses to unsuffixed (leopard) than suffixed (unspecific danger) calls. Although the acoustic structure of the ‘Krak’ stem of the calls has some additional effects, subject responses were mainly determined by the presence or the absence of the suffix. This study indicates that suffixation is an evolved function in primate communication in contexts where adaptive responses are particularly important.