Vocal production learning in mammals revisited

Vocal production learning, the ability to modify the structure of vocalizations as a result of hearing those of others, has been studied extensively in birds but less attention has been given to its occurrence in mammals. We summarize the available evidence for vocal learning in mammals from the last 25 years, updating earlier reviews on the subject. The clearest evidence comes from cetaceans, pinnipeds, elephants and bats where species have been found to copy artificial or human language sounds, or match acoustic models of different sound types. Vocal convergence, in which parameter adjustments within one sound type result in similarities between individuals, occurs in a wider range of mammalian orders with additional evidence from primates, mole-rats, goats and mice. Currently, the underlying mechanisms for convergence are unclear with vocal production learning but also usage learning or matching physiological states being possible explanations. For experimental studies, we highlight the importance of quantitative comparisons of seemingly learned sounds with vocal repertoires before learning started or with species repertoires to confirm novelty. Further studies on the mammalian orders presented here as well as others are needed to explore learning skills and limitations in greater detail. This article is part of the theme issue ‘Vocal learning in animals and humans’.

Vocal repertoire and group-specific signature in the Smooth-billed Ani, Crotophaga ani Linnaeus, 1758 (Cuculiformes, Aves)

Vocal plasticity reflects the ability of animals to vary vocalizations according to context (vocal repertoire) as well as to develop vocal convergence (vocal group signature) in the interaction of members in social groups. This feature has been largely reported for oscine, psittacine and trochilid birds, but little has been investigated in birds that present innate vocalization. The smooth-billed ani (Crotophaga ani) is a social bird that lives in groups between two and twenty individuals, and which presents innate vocalization. Here we analyzed the vocal repertoire of this species during group activities, and further investigated the existence of a vocal group signature. The study was conducted in the Southeast of Brazil between May 2017 and April 2018. Two groups of smooth-billed anis were followed, Guararema and Charqueada groups, and their vocalizations were recorded and contextualized as to the performed behavior. The vocal repertoire was analyzed for its composition, context and acoustic variables. The acoustic parameters maximum peak frequency, maximum fundamental frequency, minimum frequency, maximum frequency and duration were analyzed. To verify the vocal signature of the group, we tested whether there was variation in the acoustic parameters between the monitored groups. We recorded ten vocalizations that constituted the vocal repertoire of the Smooth-billed Ani, five of which (“Ahnee”, “Whine”, “Pre-flight”, “Flight” and “Vigil”) were issued by the two groups and five exclusive to the Charqueada group. There were significant differences in the acoustic parameters for “Flight” and “Vigil” vocalizations between the groups, suggesting vocal group signature for these sounds. We established that the Smooth-billed Ani has a diverse vocal repertoire, with variations also occurring between groups of the same population. Moreover, we found evidence of vocal group signature in vocalizations used in the context of cohesion, defense and territory maintenance.

Vocal convergence in a multi-level primate society: insights into the evolution of vocal learning

The extent to which nonhuman primate vocalizations are amenable to modification through experience is relevant for understanding the substrate from which human speech evolved. We examined the vocal behaviour of Guinea baboons, Papio papio , ranging in the Niokolo Koba National Park in Senegal. Guinea baboons live in a multi-level society, with units nested within parties nested within gangs. We investigated whether the acoustic structure of grunts of 27 male baboons of two gangs varied with party/gang membership and genetic relatedness. Males in this species are philopatric, resulting in increased male relatedness within gangs and parties. Grunts of males that were members of the same social levels were more similar than those of males in different social levels ( N = 351 dyads for comparison within and between gangs, and N = 169 dyads within and between parties), but the effect sizes were small. Yet, acoustic similarity did not correlate with genetic relatedness, suggesting that higher amounts of social interactions rather than genetic relatedness promote the observed vocal convergence. We consider this convergence a result of sensory–motor integration and suggest this to be an implicit form of vocal learning shared with humans, in contrast to the goal-directed and intentional explicit form of vocal learning unique to human speech acquisition.

Vocal convergence in a multi-level primate society: insights into the evolution of vocal learning

ABSTRACTThe extent to which nonhuman primate vocalizations are amenable to modification through experience is relevant for understanding the substrate from which human speech evolved. We examined the vocal behaviour of Guinea baboons, Papio papio, ranging in the Niokolo Koba National Park in Senegal. Guinea baboons live in a multi-level society, with units nested within parties nested within gangs. We investigated whether the acoustic structure of grunts of 27 male baboons of two gangs varied with party/gang membership and genetic relatedness. Males in this species are philopatric, resulting in increased male relatedness within gangs and parties. Grunts from members were more similar within than across social levels (N = 351 dyads for comparison within and between gangs, and N = 169 dyads within and between parties), but the effect sizes were small. Yet, acoustic similarity did not correlate with genetic relatedness, suggesting that higher amounts of social interactions rather than genetic relatedness promote the observed vocal convergence. We consider this convergence a result of sensory-motor integration and suggest this to be an implicit form of vocal learning shared with humans, in contrast to the goal-directed and intentional explicit form of vocal learning unique to human speech acquisition.

Age-related changes and vocal convergence in titi monkey duet pulses

Duets in pair-bonding primates serve as a primary mode of communication between pairs, and duets may provide cues to conspecifics regarding the calling individual or pair. Here, we test the hypothesis that pulse elements in coppery titi monkey duets vary with condition and identity of the caller. We predicted that pulse elements would vary with age, sex, or pair-bond length. We estimated pulse rate and duration for 378 pulse elements from the duets of 74 captive titi monkeys (Plecturocebus cupreus). We found inter-individual variation in both features, and evidence for vocal convergence among pair mates in pulse rate. Age was the best predictor of pulse rate, and pulse rate decreased with age. Age and pair-bond length reliably predicted pulse duration. Our results suggest that variation in titi monkey duets reflects differences in caller condition and pair identity, and contribute to growing evidence for vocal plasticity in nonhuman primates.

Convergence and divergence in Diana monkey vocalizations

Individually distinct vocalizations are widespread among social animals, presumably caused by variation in vocal tract anatomy. A less-explored source of individual variation is due to learned movement patterns of the vocal tract, which can lead to vocal convergence or divergence in social groups. We studied patterns of acoustic similarity in a social call produced by 14 female Diana monkeys ( Cercopithecus diana ) in two free-ranging groups. Calls showed variability in fundamental frequency contours owing to individual identity and external context. Vocal divergence increased significantly between females during poor visibility and tended to increase in the presence of neighbours. In contrast, vocal convergence increased significantly between females during vocal interactions, because females matched the frequency contour of their own call with another female's preceding call. Our findings demonstrate that these primates have some control over the acoustic fine structure of their most important social vocalization. Vocal convergence and divergence are two opposing processes that enable callers to ensure spatial proximity and social cohesion with other group members.

Chorusing and Call Convergence in Chimpanzees: Tests of Three Hypotheses

Male chimpanzees produce a species-typical long distance call known as the pant hoot. Males give acoustically similar pant hoots when calling together during choruses, but the process by which this vocal convergence takes place is unclear. Three potential mechanisms might account for call matching. First, vocal convergence could represent the passive effect of male chimpanzees sharing a common affective state during choruses. Second, matching could result through the active modification of calls. Such modification might occur if males modeled their calls after those produced by their current chorusing partner. Alternatively, actively mediated convergence would result if males mimicked the calls given by high-ranking males. We examined acoustic variation in calls given during choruses and while alone to test these three hypotheses. Results showed that a similar call type is not given repeatedly during successive choruses. In addition, low-ranking individuals did not produce calls that matched those of the alpha male. Chorused calls produced by two dyadic pairs were more similar to each other than they were to calls delivered during other choruses. The higher ranking, yet dependent, member of one of these dyads appeared to give calls that converged on those produced by the other individual. These data are consistent with the hypothesis that male chimpanzees accomodate each other vocally through the active alteration of their calls during choruses. We suggest that a similar form of accomodation takes place in animals from a wide range of other taxa and that the process serves to maintain and strengthen social bonds between individuals.