Social metrics of song learning

Five metrics of song learning are described for brown-headed cowbirds (Molothrus ater). The intent of these metrics is to capture not only the behavior of the song learner but the social context in which song learning occurs. Playback procedures, observations of mating, and acoustic and functional assessment of song content are combined to yield measures of song potency, functional validity, social dynamics, vocal flexibility, and social reactivity. Taken as a whole, the results revealed by these metrics indicate that males learn to be effective singers by attending to the social consequences of their behavior.     

Cultural transmission of vocal traditions in cowbirds (Molothrus ater) influences courtship patterns and mate preferences.

In this study, the authors tested the cultural transmission of vocal traditions in cowbirds (Molothrus ater). Young cowbirds from a South Dakota (SD) population were housed over winter with adults of the SD population or with adults from an Indiana (IN) population. Song differences between the original SD and IN adult models were acquired by South Dakota culture (SDC) and Indiana culture (INC) males, respectively, and were transmitted to a 2nd cultural generation of birds. During playback tests of SDC and INC songs, SD females gave more copulatory responses to SDC songs. Finally, males with SD-like songs courted SDC females preferentially in breeding season tests, whereas males with IN-like songs courted INC females preferentially. These results indicate that the transmission of vocal traditions plays a fundamental role in the courtship patterns and mating decisions of cowbirds.     

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.     

Developmental origins of sociality in brown-headed cowbirds (Molothrus ater)

Five variables were studied relating to the emergence of sociality in hand-reared cowbirds (Molothrus ater): proximity, sex assortment, reactions to adults, head-down displays, and vocalizations. The authors were especially interested in female sociality because adult female birds influence male courtship, song content, and use through proximity, attention, and displays. The authors found that young female birds failed to show same-sex affiliation typical of the species at any point in the study. Brief introduction of adults did not affect social patterns. Adults used more head-down displays than juveniles, who used more displays with familiar peers. Directed and undirected singing emerged concurrently; directed singing was positively correlated with earlier hatching. This is the first demonstration of the need for early learning in the development of female sociality.     

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.     

Perceptions of adults with childlike voices in two cultures

Two studies tested the hypothesis that adults with childlike voices would be perceived as having childlike psychological attributes. In Study 1, United States undergraduates listened to either 16 male or 16 female speakers reciting the English alphabet, and they rated psychological traits and vocal qualities of each speaker. The results revealed that speakers with vocal qualities perceived as childlike were also perceived as weaker, less competent, and warmer than their mature sounding counterparts, and these effects were independent of speakers' feminine vocal qualities, sex, and perceived age. Study 2 replicated Study 1, employing Korean undergraduates as subjects. The results revealed significant agreement between United States and Korean subjects' ratings of the United States speakers' traits. Moreover, the impact on trait ratings of a childlike voice was very similar for Korean and United States subjects. The results are discussed within a theoretical framework which argues that perceptions of adults with childlike voices may derive from the species-wide adaptive value of analogous reactions to the young.     

Slow development of vocal sequences through ontogeny in wild chimpanzees (Pan troglodytes verus)

The development of the unique, hierarchical, and endless combinatorial capacity in a human language requires neural maturation and learning through childhood. Compared with most non-human primates, where combinatorial capacity seems limited, chimpanzees present a complex vocal system comprising hundreds of vocal sequences. We investigated how such a complex vocal system develops and the processes involved. We recorded 10,929 vocal utterances of 98 wild chimpanzees aged 0–55 years, from Taï National Park, Ivory Coast. We developed customized Generalized non-Linear Models to estimate the ontogenetic trajectory of four structural components of vocal complexity: utterance length, diversity, probability of panting (requiring phonation across inhalation and exhalation), and probability of producing two adjacent panted units. We found chimpanzees need 10 years to reach adult levels of vocal complexity. In three variables, the steepest increase coincided with the age of first non-kin social interactions (2–5 years), and plateaued in sub-adults (8–10 years), as individuals integrate into adult social life. Producing two adjacent panted units may require more neuromuscular coordination of the articulators, as its emergence and steepest increase appear later in development. These results suggest prolonged maturational processes beyond those hitherto thought likely in species that do not learn their vocal repertoire. Our results suggest that multifaceted ontogenetic processes drive increases in vocal structural complexity in chimpanzees, particularly increases in social complexity and neuro-muscular maturation. As humans live in a complex social world, empirical support for the “social complexity hypothesis” may have relevance for theories of language evolution.

Research Highlights

• Chimpanzees need around 10 years to develop the vocal structural complexity present in the adult repertoire, way beyond the age of emergence of every single vocal unit.
• Multifaceted ontogenetic processes may drive increases in vocal structural complexity in chimpanzees, particularly increases in social complexity and neuro-muscular maturation.
• Non-linear increases in vocal complexity coincide with social developmental milestones.
• Vocal sequences requiring rapid articulatory change emerge later than other vocal sequences, suggesting neuro-muscular maturational processes continue through the juvenile years.

     

Directedness and engagement in chimpanzee vocal ontogeny

Directedness and engagement during pre-verbal vocal communication play a major role in language development. What was their role in the evolution of language? This question invites us to examine these behaviours in chimpanzee vocal ontogeny. We collected observational data on infant (N = 15) and juvenile (N = 13) chimpanzees at Chimfunshi Wildlife Orphanage, Zambia. We examined the impact of age and vocalization type (grunts, whimpers, laughs and screams) on directed cues (gaze directedness and face directedness) and engagement (mutual face directedness) during vocal communication. We also assessed the impact of directed cues and engagement on social interactions by coding the behaviour of social partners before, during and after a vocalisation, and examining whether they contingently changed their behaviour in response to the vocalisation if it was directed or if engagement occurred. We found that face directed vocalisations showed a general increase during ontogeny and we observed call-type dependent effects of age for mutual face directedness. Only face directed vocalisations were significantly predictive of behavioural responses in social partners. We conclude that like young humans, young chimpanzees routinely exhibit directed behaviours and engagement during vocal communication. This social competency improves during ontogeny and benefits individuals by increasing the chances of eliciting behavioural responses from social partners. Directedness and engagement likely provide a foundation for language phylogenetically, as well as ontogenetically.

Research Highlights

• We show that directedness and engagement routinely occur during early chimpanzee vocalisations.
• Directedness increases throughout chimpanzee vocal ontogeny, similar to human infants.
• Directedness enhances social partner responsiveness, demonstrating a direct benefit to this style of communication.
• Directedness and engagement could provide a route towards language phylogenetically as well as ontogenetically.

     

Sexual differences in memory in shiny cowbirds

Avian brood parasites depend on other species, the hosts, to raise their offspring. During the breeding season, parasitic cowbirds (Molothrus sp.) search for potential host nests to which they return for laying a few days after first locating them. Parasitic cowbirds have a larger hippocampus/telencephalon volume than non-parasitic species; this volume is larger in the sex involved in nest searching (females) and it is also larger in the breeding than in the non-breeding season. In nature, female shiny cowbirds Molothrus bonariensis search for nests without the male’s assistance. Here we test whether, in association with these neuroanatomical and behavioural differences, shiny cowbirds display sexual differences in a memory task in the laboratory. We used a task consisting of finding food whose location was indicated either by the appearance or the location of a covering disk. Females learnt to retrieve food faster than males when food was associated with appearance cues, but we found no sexual differences when food was associated with a specific location. Our results are consistent with the view that parasitism and its neuroanatomical correlates affect performance in memory tasks, but the effects we found were not in the expected direction, emphasising that the nature of avian hippocampal function and its sexual differences are not yet understood. Received: 30 April 1998 / Accepted after revision: 5 September 1998     

Sex differences in face cognition

Although there is abundant evidence for female superiority in Face Cognition (FC), a number of questions regarding sex differences remain to be addressed. Here we report a reanalysis of data on the level of latent factors, modeled on the basis of an extensive test battery applied to three samples of over 800 adults in all. In independent samples the measurement structure of FC was invariant for both sexes, indicating that the measurement of the construct does not depend on the context variable sex, and investigating mean performance differences will not be biased by measurement issues — a neglected aspect in previous studies. We confirmed female superiority for face perception (FP) and face memory (FM). For the first time we could show that these sex differences prevailed after accounting for sex differences in broadly measured general cognitive functioning and in object perception. Across adult age, sex differences in FM increased due to the rapid decline of this ability in men, whereas performance in women remained stable across adult age. Self-reported social involvement and things-oriented activities moderated sex-differences in FM. Results show that sex differences are salient at the level of specific FC constructs and that they can be partially explained by social involvement.     

Developmental Changes in the Effects of the Physical and Vocal Attractiveness Stereotypes

Age changes in the effects of the physical and vocal attractiveness stereotypes on perceivers′ interpersonal impressions were examined. Perceivers were students attending elementary school (grade 2 and up), high school, and college. The effect of physical attractiveness declined with age, particularly for female targets. The effect of vocal attractiveness increased with age, particularly for male targets. A physical attractiveness by vocal attractiveness interaction was also obtained, indicating that the effect of one stereotype was more pronounced for higher levels of the other stereotype. The interaction was more pronounced for higher ages, particularly for female targets. Implications of the age changes in attractiveness effects and the moderator effects of target sex were discussed.     

Discrimination between host songs by brood parasitic brown-headed cowbirds ( Molothrus ater)

Songbirds can learn both to produce and to discriminate between different classes of acoustic stimuli. Varying levels of auditory discrimination may improve the fitness of individuals in certain ecological and social contexts and, thus, selection is expected to mold the cognitive abilities of different species according to the potential benefits of acoustic processing. Although fine-scale auditory discrimination of conspecific songs and calls has been frequently reported for brood parasitic brown-headed cowbirds (Molothrus ater), it remains unclear why and how they perceive differently the songs of their many host species. Using habituation-dishabituation paradigms and measuring behavioral and physiological (heart-rate) responses, we found that captive female cowbirds consistently discriminated between songs of two host species, the song sparrow (Melospiza melodia) and the red-winged blackbird (Agelaius phoeniceus). Playback experiments with stimuli composed of con-specific followed by heterospecific vocalizations in the field also demonstrated discrimination between these heterospecific songs even though cowbirds were not attracted to playbacks of either host species' songs alone. Our results do not directly support a nest-searching function of heterospecific song discrimination by cowbirds and are most consistent with a function of the parasites' avoidance of attacks by their agressive hosts. These data demonstrate discrimination between heterospecific vocalizations by brown-headed cowbirds and add a novel dimension to the already expansive auditory perceptual abilities of brood parasitic species and other songbirds. Electronic Publication     

In the beginning was the familiar voice: personally familiar voices in the evolutionary and contemporary biology of communication

The human voice is described in dialogic linguistics as an embodiment of self in a social context, contributing to expression, perception and mutual exchange of self, consciousness, inner life, and personhood. While these approaches are subjective and arise from phenomenological perspectives, scientific facts about personal vocal identity, and its role in biological development, support these views. It is our purpose to review studies of the biology of personal vocal identity—the familiar voice pattern—as providing an empirical foundation for the view that the human voice is an embodiment of self in the social context. Recent developments in the biology and evolution of communication are concordant with these notions, revealing that familiar voice recognition (also known as vocal identity recognition or individual vocal recognition) has contributed to survival in the earliest vocalizing species. Contemporary ethology documents the crucial role of familiar voices across animal species in signaling and perceiving internal states and personal identities. Neuropsychological studies of voice reveal multimodal cerebral associations arising across brain structures involved in memory, emotion, attention, and arousal in vocal perception and production, such that the voice represents the whole person. Although its roots are in evolutionary biology, human competence for processing layered social and personal meanings in the voice, as well as personal identity in a large repertory of familiar voice patterns, has achieved an immense sophistication.     

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.     

Learning how to learn from social feedback: The origins of early vocal development

Infants’ prelinguistic vocalizations reliably organize vocal turn-taking with social partners, creating opportunities for learning to produce the sound patterns of the ambient language. This social feedback loop supporting early vocal learning is well-documented, but its developmental origins have yet to be addressed. When do infants learn that their non-cry vocalizations influence others? To test developmental changes in infant vocal learning, we assessed the vocalizations of 2- and 5-month-old infants in a still-face interaction with an unfamiliar adult. During the still-face, infants who have learned the social efficacy of vocalizing increase their babbling rate. In addition, to assess the expectations for social responsiveness that infants build from their everyday experience, we recorded caregiver responsiveness to their infants’ vocalizations during unstructured play. During the still-face, only 5-month-old infants showed an increase in vocalizing (a vocal extinction burst) indicating that they had learned to expect adult responses to their vocalizations. Caregiver responsiveness predicted the magnitude of the vocal extinction burst for 5-month-olds. Because 5-month-olds show a vocal extinction burst with unfamiliar adults, they must have generalized the social efficacy of their vocalizations beyond their familiar caregiver. Caregiver responsiveness to infant vocalizations during unstructured play was similar for 2- and 5-month-olds. Infants thus learn the social efficacy of their vocalizations between 2 and 5 months of age. During this time, infants build associations between their own non-cry sounds and the reactions of adults, which allows learning of the instrumental value of vocalizing.     

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     

Sex and species recognition by wild male southern white rhinoceros using contact pant calls

Recognition of information from acoustic signals is crucial in many animals, and individuals are under selection pressure to discriminate between the signals of conspecifics and heterospecifics or males and females. Here, we first report that rhinos use information encoded in their calls to assess conspecifics and individuals of closely related species. The southern (Ceratotherium simum) and critically endangered northern (C. cottoni) white rhinos are the most social out of all the rhinoceros species and use a contact call pant. We found that southern white rhino pant calls provide reliable information about the caller’s sex, age class and social situation. Playback experiments on wild territorial southern white rhinoceros males revealed that they responded more strongly to the pant calls of conspecific females compared to the calls of other territorial males. This suggests that pant calls are more important form of communication between males and females than between territorial males. Territorial southern males also discriminated between female and territorial male calls of northern species and reacted more intensively to the calls of northern than southern males. This might be caused by a novelty effect since both species naturally live in allopatry. We conclude that white rhinos can directly benefit from assessing individuals at long distances using vocal cues especially because their eyesight is poor. Pant calls thus likely play a significant role in their social relationships and spatial organization. In addition, better understanding of vocal communication in white rhinos might be helpful in conservation management particularly because of their low reproduction in captivity.     

Counting Chicks Before They Hatch: Female Cowbirds Can Time Readiness of a Host Nest for Parasitism

ABSTRACT— Here we show that demands associated with brood parasitism have favored sophisticated cognitive abilities in female brown-headed cowbirds. We discovered that cowbirds can use the rate at which eggs are added to a nest across days to assess the readiness of the nest for incubation, which would allow them to synchronize laying with the host and avoid nests where incubation has most likely commenced. In three experiments, cowbirds investigated and laid eggs in artificial nests that differed in the number of eggs they contained. Across days, we added eggs to nests at different rates to simulate differences in the timing of reproduction of the hosts. Cowbirds avoided a nest if the number of eggs that had been added was less than the number of days that had elapsed. The ability of females to remember egg number and compare changes in egg number across days allows them to select nests most suitable for parasitism.     

Mathematical models for coordinated interpersonal timing in mother-infant interactions in the first year of life

Two mathematical models of social contingency are examined in terms of their development over the first year of life. The interactions of 53 mothers and their infants were recorded at 6 weeks, 4 months, and 12 months. The infants' gazes at 6 weeks, the mothers' vocal behavior at 6 weeks, and the vocal behavior of the mother and infant at 4 and 12 months were automatically coded in terms of four states. The conditional dependence model and the response effects model were computed for each interaction at each age, and the coefficients of the models were examined as a function of age. The relative success of the models as estimates of moment-to-moment contingency as well as their variations with age are discussed.     

The contribution of social rank and attachment theory to depression in a non clinical sample of adolescents

This study explores the relative contribution of the overall quality of attachment to the mother, to the father and to peers (Inventory of Parent and Peer Attachment scales), the style of attachment towards peers (Attachment Questionnaire for Children scale), the social rank variables (submissive behavior and social comparison), and sex and age variables in predicting the depression score (Center of Epidemiological Studies Depression Scale) on a non-psychiatric sample of 13-18 year old adolescents (n = 225). Results of our integrated model (adjusted R-Square of .50) show that attachment variables (overall quality of attachment to the father and to the mother), social rank variables (social comparison and submissive behavior), age and sex are important in predicting depressive symptoms during adolescence. Moreover, the attachment to peers variables (quality of attachment to peers, secure and ambivalent style of attachment) and sex are mediated by the social rank variables (social comparison and submissive behavior).