A beluga whale socialized with bottlenose dolphins imitates their whistles

The research on imitation in the animal kingdom has more than a century-long history. A specific kind of imitation, auditory–vocal imitation, is well known in birds, especially among songbirds and parrots, but data for mammals are limited to elephants, marine mammals, and humans. Cetaceans are reported to imitate various signals, including species–specific calls, artificial sounds, and even vocalizations from other species if they share the same habitat. Here we describe the changes in the vocal repertoire of a beluga whale that was housed with a group of bottlenose dolphins. Two months after the beluga’s introduction into a new facility, we found that it began to imitate whistles of the dolphins, whereas one type of its own calls seemed to disappear. The case reported here may be considered as an interesting phenomenon of vocal accommodation to new social companions and cross-species socialization in cetaceans.     

Social processes in communication and cognition in callitrichid monkeys: a review

Studies of vocal development in nonhuman primates have found little evidence for plasticity in vocal production, somewhat more for usage of calls, with the greatest plasticity arising in response to calls of others. Generally, similar results were obtained with callitrichid monkeys, the marmosets and tamarins, but with several interesting exceptions. Infant pygmy marmosets show babbling behavior with improvement in adult call structure related to the amount and diversity of babbling. Adult marmosets alter call structure in response to changes in social partners, and wild marmosets have vocal dialects and modify call structure according to how far they are from other group members, suggesting the potential to modify call structure in different social and environmental contexts, though direct learning of novel vocalizations has not been observed. Infant cotton-top tamarins do not produce adult-like calls in appropriate contexts, at least in the first few months of life, but through food sharing from adults infants learn about appropriate foods and the appropriate contexts for food vocalizations. Tamarins modify call structure and usage with changes in social status. Tamarins, unlike other monkeys tested, can learn to avoid noxious foods through observation of other group members, and can learn about novel food locations. Recent studies provide evidence of contextual imitation in marmosets. The plasticity in vocal communication and evidence of social learning in marmosets and tamarins relative to other monkeys may be related to the cooperative breeding system of marmosets and tamarins. With a high degree of behavioral coordination among group members, there is a priority on monitoring signals and behavior of others and adjusting one's own signals and behavior. This creates the context for vocal plasticity and social learning. Accepted after revision: 23 May 2001 Electronic Publication     

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.     

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.     

Vocal imitation between mothers and infants

The aim of the present mixed cross-sectional and longitudinal study was to observe and describe some aspects of vocal imitation in natural mother-infant interaction. Specifically, maternal imitation of infant utterances was observed in relation to the imitative modeling, mirrored equivalence, and social guided learning models of infant speech development. Nine mother-infant dyads were audio-video recorded. Infants were recruited at different ages between 6 and 11 months and followed for 3 months, providing a quasi-longitudinal series of data from 6 through 14 months of age. It was observed that maternal imitation was more frequent than infant imitation even though vocal imitation was a rare maternal response. Importantly, mothers used a range of contingent and noncontingent vocal responses in interaction with their infants. Mothers responded to three-quarters of their infant's vocalizations, including speech-like and less mature vocalization types. The infants’ phonetic repertoire expanded with age. Overall, the findings are most consistent with the social guided learning approach. Infants rarely imitated their mothers, suggests a creative self-motivated learning mechanism that requires further investigation.     

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.     

Reinforcement of vocalizations through contingent vocal imitation

Maternal vocal imitation of infant vocalizations is highly prevalent during face-to-face interactions of infants and their caregivers. Although maternal vocal imitation has been associated with later verbal development, its potentially reinforcing effect on infant vocalizations has not been explored experimentally. This study examined the reinforcing effect of maternal vocal imitation of infant vocalizations using a reversal probe BAB design. Eleven 3- to 8-month-old infants at high risk for developmental delays experienced contingent maternal vocal imitation during reinforcement conditions. Differential reinforcement of other behavior served as the control condition. The behavior of 10 infants showed evidence of a reinforcement effect. Results indicated that vocal imitations can serve to reinforce early infant vocalizations.     

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.     

Imitation: definitions, evidence, and mechanisms

Imitation can be defined as the copying of behavior. To a biologist, interest in imitation is focused on its adaptive value for the survival of the organism, but to a psychologist, the mechanisms responsible for imitation are the most interesting. For psychologists, the most important cases of imitation are those that involve demonstrated behavior that the imitator cannot see when it performs the behavior (e.g., scratching one's head). Such examples of imitation are sometimes referred to as opaque imitation because they are difficult to account for without positing cognitive mechanisms, such as perspective taking, that most animals have not been acknowledged to have. The present review first identifies various forms of social influence and social learning that do not qualify as opaque imitation, including species-typical mechanisms (e.g., mimicry and contagion), motivational mechanisms (e.g., social facilitation, incentive motivation, transfer of fear), attentional mechanisms (e.g., local enhancement, stimulus enhancement), imprinting, following, observational conditioning, and learning how the environment works (affordance learning). It then presents evidence for different forms of opaque imitation in animals, and identifies characteristics of human imitation that have been proposed to distinguish it from animal imitation. Finally, it examines the role played in opaque imitation by demonstrator reinforcement and observer motivation. Although accounts of imitation have been proposed that vary in their level of analysis from neural to cognitive, at present no theory of imitation appears to be adequate to account for the varied results that have been found.     

Primate vocal production and the riddle of language evolution

Trying to uncover the roots of human speech and language has been the premier motivation to study the signalling behaviour of nonhuman primates for several decades. Focussing on the question of whether we find evidence for linguistic reference in the production of nonhuman primate vocalizations, I will first discuss how the criteria used to diagnose referential signalling have changed over time, and will then turn to the paradigmatic case of semantic communication in animals, the alarm calls of vervet monkeys, Chlorocebus pygerythrus. A recent in-depth analysis of the original material revealed that, while the alarm calls could be well distinguished, calls of similar structure were also used in within- and between-group aggression. This finding is difficult to reconcile with the idea that calls denote objects in the environment. Furthermore, nonhuman primates show only minimal signs of vocal production learning, one key prerequisite for conventionalized and symbolic communication. In addition, the structure of calls in different populations or closely related species is highly conserved. In conclusion, any continuity between nonhuman primate and human communication appears to be found at the level of the processing of signals. Why and how the ancestors of our own species one day began to talk to each other continues to be an enigma. Future research should focus on changes in the neural structure supporting volitional control over vocalizations, the gene networks associated with vocal production, and the developmental processes involved in the integration of production and perception of vocalizations.     

Evolution of the brain and intelligence

Intelligence has evolved many times independently among vertebrates. Primates, elephants and cetaceans are assumed to be more intelligent than 'lower' mammals, the great apes and humans more than monkeys, and humans more than the great apes. Brain properties assumed to be relevant for intelligence are the (absolute or relative) size of the brain, cortex, prefrontal cortex and degree of encephalization. However, factors that correlate better with intelligence are the number of cortical neurons and conduction velocity, as the basis for information-processing capacity. Humans have more cortical neurons than other mammals, although only marginally more than whales and elephants. The outstanding intelligence of humans appears to result from a combination and enhancement of properties found in non-human primates, such as theory of mind, imitation and language, rather than from 'unique' properties.     

Is language acquired through imitation?

The role of imitation in language acquisition is examined, including data from the psycholinguistic, operant, and social learning areas. From the psycholinguistic data, four empirical statements have been extracted: (1) there is no evidence that spontaneous imitations of adult speech influence grammatical development, (2) imitation of speech does not appear to occur with frequency beyond age 3 years, (3) speech and hence imitation are not necessary for the comprehension of linguistic structures, and (4) most utterances of a child are novel and therefore could not have been exactly modeled. The first and second propositions are seen to be based on a too restrictive definition of imitation-immediate and exact copying. Selective imitation-a functional relationship involving similarity of a particular form or function of the model's responses-is proposed as an alternative, thus leaving the validity of statements (1) and (2) in question. Concerning assertion (4), certain data from the operant literature are presented as evidence of the compatibility of novel responding and modeling, imitation, and reinforcement. Finally, it is proposed that statement (3) suggests a mechanism by which selective imitation can be understood. A three-stage process is proposed in which comprehension of a grammatical form sets the stage for selective imitation of that structure, which leads in turn to spontaneous production. Thus imitation is a process by which new syntactic structures can be first introduced into the productive mode.     

Vocal learning in birds and humans

Vocal learning is the modification of vocal output by reference to auditory information. It allows for the imitation and improvisation of sounds that otherwise would not occur. The emergence of this skill may have been a primary step in the evolution of human language, but vocal learning is not unique to humans. It also occurs in songbirds, where its biology can be studied with greater ease. What follows is a review of some of the salient anatomical, developmental, and behavioral features of vocal learning, alongside parallels and differences between vocal learning in songbirds and humans.     

The social functions of babbling: acoustic and contextual characteristics that facilitate maternal responsiveness

What is the social function of babbling? An important function of prelinguistic vocalizing may be to elicit parental behavior in ways that facilitate the infant's own learning about speech and language. Infants use parental feedback to their babbling to learn new vocal forms, but the microstructure of parental responses to babbling has not been studied. To enable precise manipulation of the proximal infant cues that may influence maternal behavior, we used a playback paradigm to assess mothers’ responsiveness to prerecorded audiovisual clips of unfamiliar infants’ noncry prelinguistic vocalizations and actions. Acoustic characteristics and directedness of vocalizations were manipulated to test their efficacy in structuring social interactions. We also compared maternal responsiveness in the playback paradigm and in free play with their own infants. Maternal patterns of reactions to babbling were stable across both tasks. In the playback task, we found specific vocal cues, such as the degree of resonance and the transition timing of consonant‐vowel syllables, predicted contingent maternal responding. Vocalizations directed at objects also facilitated increased responsiveness. The responses mothers exhibited, such as sensitive speech and vocal imitation, are known to facilitate vocal learning and development. Infants, by influencing the behavior of their caregivers with their babbling, create social interactions that facilitate their own communicative development.     

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.     

Perceiving imitatible stimuli: consequences of isomorphism between input and output.

For more than a century, psychologists have been intrigued by the idea that mental representations of perceived human actions are closely connected with mental representations of performing those same actions. In this article, connections between input and output representations are considered in terms of the potential for imitation. A broad range of evidence suggests that, for imitatible stimuli, input and output representations are isomorphic to one another, allowing mutual influence between perception and motoric planning that is rapid, effortless, and possibly obligatory. Thus, the cognitive consequences of imitatibility may underlie such diverse phenomena as phoneme perception; imitation in neonates; echoic memory; stimulus-response compatibility; conduction aphasia; maintenance rehearsal; and a variety of developmental and social activities such as language acquisition, social learning, empathy, and monitoring one's own behavior.     

Social learning in captive African elephants (Loxodonta africana africana)

Social learning is a more efficient method of information acquisition and application than trial and error learning and is prevalent across a variety of animal taxa. Social learning is assumed to be important for elephants, but evidence in support of that claim is mostly anecdotal. Using a herd of six adult female African bush elephants (Loxodonta africana africana) at the San Diego Zoo’s Safari Park, we evaluated whether viewing a conspecific’s interactions facilitated learning of a novel task. The tasks used feeding apparatus that could be solved in one of two distinct ways. Contrary to our hypothesis, the method the demonstrating animal used did not predict the method used by the observer. However, we did find evidence of social learning: After watching the model, subjects spent a greater percentage of their time interacting with the apparatus than they did in unmodeled trials. These results suggest that the demonstrations of a model may increase the motivation of elephants to explore novel foraging tasks.     

Acoustic variability and individual distinctiveness in the vocal repertoire of red-capped mangabeys (Cercocebus torquatus)

Acoustic variability and individual distinctiveness of vocal signals are expected to vary with both their communicative function and the need for individual recognition during social interactions. So far, few attempts have been made to comparatively study these features across the different call types within a species' vocal repertoire. We collected recordings of the six most common call types from 14 red-capped mangabeys (Cercocebus torquatus) to assess intra- and interindividual acoustic variability, using a range of temporal and frequency parameters. Acoustic variability was highest in contact and threat calls, intermediate in food calls, and lowest in loud and alarm calls. Individual distinctiveness was high in contact, threat, loud and alarm calls, and low in food calls. In sum, calls mediating intragroup social interactions were structurally most variable and individually most distinctive, highlighting the key role that social factors must have played in the evolution of the vocal repertoire in this species. We discuss these findings in light of existing hypotheses of acoustic variability in primate vocal behavior.     

Context-related call combinations in female Diana monkeys

Non-human primates possess species-specific repertoires of acoustically distinct call types that can be found in adults in predictable ways. Evidence for vocal flexibility is generally rare and typically restricted to acoustic variants within the main call types or sequential production of multiple calls. So far, evidence for context-specific call sequences has been mainly in relation to external disturbances, particularly predation. In this study, we investigated extensively the vocal behaviour of free-ranging and individually identified Diana monkeys in non-predatory contexts. We found that adult females produced four vocal structures alone (‘H’, ‘L’, ‘R’ and ‘A’ calls, the latter consisting of two subtypes) or combined in non-random ways (‘HA’, ‘LA’ and ‘RA’ call combinations) in relation to ongoing behaviour or external events. Specifically, the concatenation of an introductory call with the most frequently emitted and contextually neutral ‘A’ call seems to function as a contextual refiner of this potential individual identifier. Our results demonstrate that some non-human primates are able to increase the effective size of their small vocal repertoire not only by varying the acoustic structure of basic call types but also by combining them into more complex structures. We have demonstrated this phenomenon for a category of vocalisations with a purely social function and discuss the implications of these findings for evolutionary theories of primate vocal communication.