Convergence of calls as animals form social bonds, active compensation for noisy communication channels, and the evolution of vocal learning in mammals

The classic evidence for vocal production learning involves imitation of novel, often anthropogenic sounds. Among mammals, this has been reported for dolphins, elephants, harbor seals, and humans. A broader taxonomic distribution has been reported for vocal convergence, where the acoustic properties of calls from different individuals converge when they are housed together in captivity or form social bonds in the wild. Vocal convergence has been demonstrated for animals as diverse as songbirds, parakeets, hummingbirds, bats, elephants, cetaceans, and primates. For most species, call convergence is thought to reflect a group-distinctive identifier, with shared calls reflecting and strengthening social bonds. A ubiquitous function for vocal production learning that is starting to receive attention involves modifying signals to improve communication in a noisy channel. Pooling data on vocal imitation, vocal convergence, and compensation for noise suggests a wider taxonomic distribution of vocal production learning among mammals than has been generally appreciated. The wide taxonomic distribution of this evidence for vocal production learning suggests that perhaps more of the neural underpinnings for vocal production learning are in place in mammals than is usually recognized.     

Vocal group signatures in the goitred gazelle Gazella subgutturosa

The potential for vocal modification in mammals has recently been of great interest. This study focuses on the potential for vocal matching in juvenile and adolescent goitred gazelles Gazella subgutturosa that were group housed as part of an animal management programme. Two groups of animals (16 and 19 unrelated individuals, respectively) were recorded at two different ages, juvenile and adolescent, regarding 20–25 calls per individual per age; each group was evaluated in a separate year. Vocal similarity of group members compared to non-members was prominent in both ages, but higher in juveniles. Individual identity was prominent in both ages and higher in adolescents. The more prominent vocal indicators of group membership in juveniles could be related to their higher social dependence compared to adolescents. The more individualized calls of adolescents could be a mechanistic consequence of more stable growth at older age. Our results suggest vocal plasticity of goitred gazelles under social influences. These data add to recent evidence about domestic goat kids Capra hircus, suggesting that vocalizations of species that are not capable of imitation are more flexible than previously thought.     

Switching strategies: a dolphin’s use of passive and active acoustics to imitate motor actions

Scientists have long debated the extent to which animals can imitate. Observations of bottlenose dolphins suggest a sophisticated capacity for social imitation, but little is known about the nature of these abilities. Here, we explore the behavioral mechanisms underlying a dolphin’s ability to copy motor actions while blindfolded (i.e., wearing eyecups). When a dolphin was asked to imitate a dolphin, a human, and then another dolphin blindfolded, his accuracy remained relatively consistent across models. However, his blindfolded echolocation dramatically increased when copying a human as compared to other dolphins, suggesting he actively switched between strategies: recognizing behaviors via characteristic sounds when possible, but via echolocation for the more novel sounding behaviors of the human. Such flexibility in changing perceptual routes demonstrates that the dolphin’s imitation was not automatically elicited, but rather results from an intentional, problem-solving approach to imitation.     

Evidence suggests vocal production learning in a cross-fostered Risso’s dolphin (<Emphasis Type="Italic">Grampus</Emphasis><Emphasis Type="Italic">griseus</Emphasis>)

Vocal learning is a rare skill in mammals, and we have limited information about the contexts in which they use it. Previous studies suggested that cetaceans in general are skilled at imitating sounds, but only few species have been studied to date. To expand this investigation to another species and to investigate the possible influence of the social environment on vocal learning, we studied the whistle repertoire of a female Risso’s dolphin (Grampus griseus) that was stranded at an early age and was subsequently raised in a group of bottlenose dolphins (Tursiops truncatus). We show that this cross-fostered animal produced vocal signals more akin to those of its Tursiops poolmates than those of Risso’s dolphins in the wild. This is one of very few systematic cross-fostering studies in cetaceans and the first to suggest vocal production learning in the Risso’s dolphin. Our findings also suggest that social experience is a major factor in the development of the vocal repertoire in this species.     

Imitation and repetition of prosodic contour in vocal interaction at 3 months

This study investigates vocal imitation of prosodic contour in ongoing spontaneous interaction with 10- to 13-week-old infants. Audio recordings from naturalistic interactions between 20 mothers and infants were analyzed using a vocalization coding system that extracted the pitch and duration of individual vocalizations. Using these data, the authors categorized a sample of 1,359 vocalizations on the basis of 7 predetermined contours. Pairs of identical successive vocalizations were considered to be imitations if they involved both partners or repetitions if they were produced by the same partner. Results show that not only do mothers and infants imitate and repeat prosodic contour types in the course of vocal interaction but they do so selectively. Indeed, different contours are imitated and repeated by each partner. These findings suggest that imitation and repetition of prosodic contours have specific functions for communication and vocal development in the 3rd month of life.     

Mouse vocal communication system: Are ultrasounds learned or innate?

Mouse ultrasonic vocalizations (USVs) are often used as behavioral readouts of internal states, to measure effects of social and pharmacological manipulations, and for behavioral phenotyping of mouse models for neuropsychiatric and neurodegenerative disorders. However, little is known about the neurobiological mechanisms of rodent USV production. Here we discuss the available data to assess whether male mouse song behavior and the supporting brain circuits resemble those of known vocal non-learning or vocal learning species. Recent neurobiology studies have demonstrated that the mouse USV brain system includes motor cortex and striatal regions, and that the vocal motor cortex sends a direct sparse projection to the brainstem vocal motor nucleus ambiguous, a projection previously thought be unique to humans among mammals. Recent behavioral studies have reported opposing conclusions on mouse vocal plasticity, including vocal ontogeny changes in USVs over early development that might not be explained by innate maturation processes, evidence for and against a role for auditory feedback in developing and maintaining normal mouse USVs, and evidence for and against limited vocal imitation of song pitch. To reconcile these findings, we suggest that the trait of vocal learning may not be dichotomous but encompass a broad spectrum of behavioral and neural traits we call the continuum hypothesis, and that mice possess some of the traits associated with a capacity for limited vocal learning.     

Communicative and other cognitive characteristics of bottlenose dolphins

Scientists have tried to capture the rich cognitive life of dolphins through field and laboratory studies of their brain anatomy, social lives, communication and perceptual abilities. Encopheliration quotient data sugest a level of intelligence or cognitive processing in the large-brained dolphin that is closer to the human range than are our nearest primate relatives. Field studies indicate a fission-fusion type of social structure, showing social complexity rivaling that found in chimpanzee societies. Notably, cetaceans are the only mammals other than humans that clearly demonstrate vocal learning and parallels in stages of vocal learning have been reported for humans, birds and dolphins. The dolphin's vocal plasticity from infancy through adulthood, in what is probably an 'open' communication system, is likely to be related to their fission-fusion social structure and, specifically, to the fluidity of their short-term associations. However, conflicting evidence exists on the composition and organization of the dolphins whistle repertoire. In general, the level of dolphin performance on complex auditory learning and memory tasks has been compared with that of primates on similar visual tasks; however, dolphins have also demonstrated sophistrcated visual processing abilities. Laboratory studies have also provided suggestive, evidence of minor self-recognition in the dolphin, an ability previously thought to be exclusive to humans humans and apes.     

What’s in a voice? Dolphins do not use voice cues for individual recognition

Most mammals can accomplish acoustic recognition of other individuals by means of “voice cues,” whereby characteristics of the vocal tract render vocalizations of an individual uniquely identifiable. However, sound production in dolphins takes place in gas-filled nasal sacs that are affected by pressure changes, potentially resulting in a lack of reliable voice cues. It is well known that bottlenose dolphins learn to produce individually distinctive signature whistles for individual recognition, but it is not known whether they may also use voice cues. To investigate this question, we played back non-signature whistles to wild dolphins during brief capture-release events in Sarasota Bay, Florida. We hypothesized that non-signature whistles, which have varied contours that can be shared among individuals, would be recognizable to dolphins only if they contained voice cues. Following established methodology used in two previous sets of playback experiments, we found that dolphins did not respond differentially to non-signature whistles of close relatives versus known unrelated individuals. In contrast, our previous studies showed that in an identical context, dolphins reacted strongly to hearing the signature whistle or even a synthetic version of the signature whistle of a close relative. Thus, we conclude that dolphins likely do not use voice cues to identify individuals. The low reliability of voice cues and the need for individual recognition were likely strong selective forces in the evolution of vocal learning in dolphins.     

Culture in whales and dolphins

Studies of animal culture have not normally included a consideration of cetaceans. However, with several long-term field studies now maturing, this situation should change. Animal culture is generally studied by either investigating transmission mechanisms experimentally, or observing patterns of behavioural variation in wild populations that cannot be explained by either genetic or environmental factors. Taking this second, ethnographic, approach, there is good evidence for cultural transmission in several cetacean species. However, only the bottlenose dolphin (Tursiops) has been shown experimentally to possess sophisticated social learning abilities, including vocal and motor imitation; other species have not been studied. There is observational evidence for imitation and teaching in killer whales. For cetaceans and other large, wide-ranging animals, excessive reliance on experimental data for evidence of culture is not productive; we favour the ethnographic approach. The complex and stable vocal and behavioural cultures of sympatric groups of killer whales (Orcinus orca) appear to have no parallel outside humans, and represent an independent evolution of cultural faculties. The wide movements of cetaceans, the greater variability of the marine environment over large temporal scales relative to that on land, and the stable matrilineal social groups of some species are potentially important factors in the evolution of cetacean culture. There have been suggestions of gene-culture coevolution in cetaceans, and culture may be implicated in some unusual behavioural and life-history traits of whales and dolphins. We hope to stimulate discussion and research on culture in these animals.     

Keeping an “I” on PRIDE: Measuring Imitation in Parent-Child Interaction Therapy

In parent–child interaction therapy (PCIT), therapists encourage parents to imitate child behaviors in order to convey approval of the child’s actions and promote the development of linguistic and social–cognitive skills. However, the Dyadic Parent-Child Interaction Coding System (DPICS-IV), used to measure skills taught during PCIT, does not include guidelines for coding parent–child imitation, making it difficult to determine how PCIT affects it. The current study addresses this problem by developing guidelines for coding imitation, which were then used to code DPICS-IV segments from 58 Mexican American families that participated in a past clinical trial. Results suggest that these coding guidelines can be used to reliably measure parent and child imitation. A series of additional analyses supported the construct validity of the codes. Specifically, there was a trend for parent imitation, but not child imitation, to increase more from pre–post treatment in PCIT relative to treatment as usual. In addition, parents who imitate their children were found to have children who imitate them more in return. Finally, improvement in parent imitation, but not child imitation, was significantly related to a decrease in child behavior problems. Further study is needed to determine the optimal frequency of imitation, and findings suggest that additional attention to coaching imitation may be warranted.     

On the function of redfronted lemur’s close calls

In order to maintain group cohesion, many social mammals and birds regularly produce close calls. In some primate species, close calls appear to have a dual function: calls addressed at a broad class of targets serve to maintain group cohesion, whereas the same calls directed at a specific target serve to regulate subsequent social interactions. Redfronted lemurs (Eulemur rufifrons) produce different types of close calls: grunts, long grunts, hoos and meows. In order to study the function of these calls, we conducted focal observations and vocal recordings from eight adult males and females out of four social groups in Kirindy Forest, Western Madagascar. Redfronted lemurs produce long grunts, hoos and meows at relatively low rates during foraging, resting or group movements, respectively. Grunts were given most often and more or less constantly during foraging and traveling. Calling rate increased when the risk of separation increased and may thus promote group cohesion. Grunts given during approaches of other group members resulted more often in friendly interactions than approaches that were not accompanied by a grunt. Thus, redfronted lemurs produce specific but also generic contact calls, whereas the latter calls have a dual function that varies depending on the addressed audience: they act as an auditory beacon to maintain group cohesion and serve as signals of benign intent to avoid costly conflicts and facilitating social interactions.     

Horse (Equus caballus) whinnies: a source of social information

Many animal species that rely mainly on calls to communicate produce individual acoustic structures, but we wondered whether individuals of species better known as visual communicants, with small vocal repertoires, would also exhibit individual distinctiveness in calls. Moreover, theoretical advances concerning the evolution of social intelligence are usually based on primate species data, but relatively little is known about the social cognitive capacities of non-primate mammals. However, some non-primate species demonstrate auditory recognition of social categories and possess mental representation of their social network. Horses (Equus caballus) form stable social networks and although they display a large range of visual signals, they also use long-distance whinny calls to maintain contact. Here, we investigated the potential existence of individual acoustic signatures in whinny calls and the ability of horses to discriminate by ear individuals varying in their degree of familiarity. Our analysis of the acoustic structure of whinnies of 30 adult domestic horses (ten stallions, ten geldings, ten mares) revealed that some of the frequency and temporal parameters carried reliable information about the caller’s sex, body size and identity. However, no correlations with age were found. Playback experiments evaluated the behavioural significance of this variability. Twelve horses heard either control white noise or whinnies emitted by group members, familiar neighbours or unfamiliar horses. While control sounds did not induce any particular response, horses discriminated the social category of the callers and reacted with a sound-specific behaviour (vigilance and attraction varied with familiarity). Our results support the existence of social knowledge in horses and suggest a process of vocal coding/decoding of information.     

The development of generalized imitation within topographically determined boundaries

A multiple baseline technique was employed to examine the experimental development of an imitative repertoire within preselected topographical boundaries. Four severely retarded children, initially nonimitative, were individually trained to imitate a number of motor and vocal responses by shaping and fading procedures. Other untrained responses (probes) were demonstrated to the subjects systematically throughout the ongoing training. Training responses were divided into three topographical types: small motor, large motor, and short vocal responses. Probe responses were divided into four topographical types: small motor, large motor, short vocal, and long vocal responses. Following a multiple baseline format, sequential training of the first three types was begun at different temporal periods of the study; unreinforced imitative generalization was continually measured by the probes. Generalized imitation was observed in each subject (untrained responses were imitated even though unreinforced); but this generalization was restricted to the topographical type of imitation currently receiving training or having previously received training.     

Selective and faithful imitation at 12 and 15 months

Research on imitation in infancy has primarily focused on what and when infants imitate. More recently, however, the question why infants imitate has received renewed attention, partly motivated by the finding that infants sometimes selectively imitate the actions of others and sometimes faithfully imitate, or overimitate, the actions of others. The present study evaluates the hypothesis that this varying imitative behavior is related to infants' social traits. To do so, we assessed faithful and selective imitation longitudinally at 12 and 15 months, and extraversion at 15 months. At both ages, selective imitation was dependent on the causal structure of the act. From 12 to 15 months, selective imitation decreased while faithful imitation increased. Furthermore, infants high in extraversion were more faithful imitators than infants low in extraversion. These results demonstrate that the onset of faithful imitation is earlier than previously thought, but later than the onset of selective imitation. The observed relation between extraversion and faithful imitation supports the hypothesis that faithful imitation is driven by the social motivations of the infant. We call this relation the King Louie Effect: like the orangutan King Louie in The Jungle Book, infants imitate faithfully due to a growing interest in the interpersonal nature of interactions. A video abstract of this article can be viewed at http://youtu.be/qlnIof1k-u8 .     

Effects of stimulus response compatibility on covert imitation of vowels

When we observe someone else speaking, we tend to automatically activate the corresponding speech motor patterns. When listening, we therefore covertly imitate the observed speech. Simulation theories of speech perception propose that covert imitation of speech motor patterns supports speech perception. Covert imitation of speech has been studied with interference paradigms, including the stimulus–response compatibility paradigm (SRC). The SRC paradigm measures covert imitation by comparing articulation of a prompt following exposure to a distracter. Responses tend to be faster for congruent than for incongruent distracters; thus, showing evidence of covert imitation. Simulation accounts propose a key role for covert imitation in speech perception. However, covert imitation has thus far only been demonstrated for a select class of speech sounds, namely consonants, and it is unclear whether covert imitation extends to vowels. We aimed to demonstrate that covert imitation effects as measured with the SRC paradigm extend to vowels, in two experiments. We examined whether covert imitation occurs for vowels in a consonant–vowel–consonant context in visual, audio, and audiovisual modalities. We presented the prompt at four time points to examine how covert imitation varied over the distracter’s duration. The results of both experiments clearly demonstrated covert imitation effects for vowels, thus supporting simulation theories of speech perception. Covert imitation was not affected by stimulus modality and was maximal for later time points.

     

Imitation improves language comprehension

Humans imitate each other during social interaction. This imitative behavior streamlines social interaction and aids in learning to replicate actions. However, the effect of imitation on action comprehension is unclear. This study investigated whether vocal imitation of an unfamiliar accent improved spoken-language comprehension. Following a pretraining accent comprehension test, participants were assigned to one of six groups. The baseline group received no training, but participants in the other five groups listened to accented sentences, listened to and repeated accented sentences in their own accent, listened to and transcribed accented sentences, listened to and imitated accented sentences, or listened to and imitated accented sentences without being able to hear their own vocalizations. Posttraining measures showed that accent comprehension was most improved for participants who imitated the speaker's accent. These results show that imitation may aid in streamlining interaction by improving spoken-language comprehension under adverse listening conditions.     

Training social cognition: from imitation to Theory of Mind

Evidence for successful socio-cognitive training in typical adults is rare. This study attempted to improve Theory of Mind (ToM) and visual perspective taking in healthy adults by training participants to either imitate or to inhibit imitation. Twenty-four hours after training, all participants completed tests of ToM and visual perspective taking. The group trained to inhibit their tendency to imitate showed improved performance on the visual perspective-taking test, but not the ToM test. Neither imitation training, nor general inhibition training, had this effect. These results support a novel theory of social cognition suggesting that the same self-other discrimination process underlies imitation inhibition and perspective taking. Imitation, perspective taking and ToM are all pro-social processes--ways in which we reach out to others. Therefore, it is striking that perspective taking can be enhanced by suppressing imitation; to understand another, sometimes we need, not to get closer, but to pull away.     

Cooperation or dolphin ‘tug-of-war’? Comment on Kuczaj et al. and Eskelinen et al.

Two recent papers by Kuczaj et al. (Anim Cognit 18:543–550, 2015) and Eskelinen et al. (Anim Cognit 19:789–797, 2016) claim to have demonstrated that (i) bottlenose dolphins (Tursiops truncatus) cooperated to solve a novel task and (ii) vocal signals were important for coordinating these cooperative efforts. Although it is likely that bottlenose dolphins may share communicative signals in order to achieve a common goal, we suggest that this has not been demonstrated in the aforementioned studies. Here, we discuss the two main problems that preclude any definitive conclusions being drawn on cooperative task success and vocal communication from these studies. The first lies in the experimental design. The ‘cooperative task’, involving an apparatus that requires two dolphins to pull in opposite directions in order to achieve a food reward, is not conducive to cooperation, but could instead reflect a competitive ‘tug-of-war’. It is therefore of questionable use in distinguishing competitive from cooperative interactions. Second, the suggestion that the occurrence of burst-pulsed signals in this task was indicative of cooperation is disputable, as (i) this study could not determine which dolphins were actually producing the signals and (ii) this sound type is more commonly associated with aggressive signalling in dolphins. We commend the authors for investigating this exciting and topical area in animal communication and cognition, but the question of whether dolphins cooperate and communicate to solve a cooperative task remains as yet unanswered.     

From imitation to conversation: the first dialogues with human neonates

The functional maturity of the newborn infant's brain, the resemblances between neonatal imitation and imitation in adults and the possibly lateralized neonatal imitation suggest that the mirror neuron system may contribute to neonatal imitation. Newborn infants not only imitate but also initiate previously imitated gestures, and are able to participate in overlapping imitation–initiation communicative cycles. Additionally, these social responses in neonates are faster than previously thought, and may enable them to have long‐lasting intimate interactions much before language develops. Infants are equipped with a powerful, innate, reciprocal communicative ability already at birth. The earliest communication originates from imitation and this communicative ability presumably later evolves to language. Copyright © 2006 John Wiley & Sons, Ltd.     

Toward a reconceptualization of the reciprocal imitation phenomenon: Two experiments

This paper reports two experiments which consider the increased imitation exhibited by models who have been imitated. Experiment 1 was concerned with whether the reciprocal imitation effect is really reciprocal or if the subsequent imitation will generalize to someone else. It was found that adult subjects who were previously imitated at the 75% rate on a perceptual judgments task subsequently imitated their partner more, rated their partner more attractive, and felt more confidence when imitated than did subjects imitated at the 25% rate. These results were obtained regardless of which confederate the subjects imitated, thus indicating that reciprocal imitation is not necessarily reciprocal, but is generalizable. Experiment 2 assessed whether the subsequent imitation is the product of the effects of being imitated or is the result of the subject observing the imitator's imitation. The results indicated that after having observed imitation at a 75% rate, adult onlookers are more likely to subsequently imitate and be attracted to the imitator, the imitated person, and a person new to the situation than are onlookers who observed a 25% imitation rate. A theoretical modification is advanced which holds that subsequent imitation effects, whether from observing others imitate or from being the target of the imitation, result from a process of imitation of imitativeness. The results of these two experiments have implications for theory in imitation and social learning.