Of Mice,Birds, and Men: The Mouse Ultrasonic Song System Has Some Features Similar to Humans and Song-Learning Birds

Humans and song-learning birds communicate acoustically using learned vocalizations. The characteristic features of this social communication behavior include vocal control by forebrain motor areas, a direct cortical projection to brainstem vocal motor neurons, and dependence on auditory feedback to develop and maintain learned vocalizations. These features have so far not been found in closely related primate and avian species that do not learn vocalizations. Male mice produce courtship ultrasonic vocalizations with acoustic features similar to songs of song-learning birds. However, it is assumed that mice lack a forebrain system for vocal modification and that their ultrasonic vocalizations are innate. Here we investigated the mouse song system and discovered that it includes a motor cortex region active during singing, that projects directly to brainstem vocal motor neurons and is necessary for keeping song more stereotyped and on pitch. We also discovered that male mice depend on auditory feedback to maintain some ultrasonic song features, and that sub-strains with differences in their songs can match each other''s pitch when cross-housed under competitive social conditions. We conclude that male mice have some limited vocal modification abilities with at least some neuroanatomical features thought to be unique to humans and song-learning birds. To explain our findings, we propose a continuum hypothesis of vocal learning.     

Effects of reproductive and social context on vocal communication in captive female African elephants (Loxodonta africana)

Female African elephants advertise changes in reproductive condition to males through a variety of modalities, including an increase in low‐frequency vocalizations, presumed to travel long distances. Although males respond to these vocalizations, it has been suggested that their proximate function may be to signal to nearby females rather than to distant males. Because elephants live in a female‐bonded society, it is likely that changes in female reproductive condition also affect close‐range interactions between high‐ and low‐ranking females and that vocalizations may mediate these interactions. To examine female–female interactions related to vocal production and the ovulatory cycle, this year‐long study monitored behavior, vocalizations and hormonal cycles for a group of six female captive African elephants at Disney's Animal Kingdom. Rates of several types of close‐range interactions were observed to change over the phases of the estrous cycle, and rank seemed to affect whether or not low‐frequency vocalizations were given in association with these interactions. Results of this study suggest that a female African elephant's immediate social context and rank in the social hierarchy interact with the hormonal cycle in the production of low‐frequency vocalizations, thus many of these vocalizations may not function proximately as signals to distant males, but may be a result of the changing dynamics among females. Zoo Biol 0:1–17, 2005. © 2005 Wiley‐Liss, Inc.     

Oxytocin and social affiliation in humans

A conceptual model detailing the process of bio-behavioral synchrony between the online physiological and behavioral responses of attachment partners during social contact is presented as a theoretical and empirical framework for the study of affiliative bonds. Guided by an ethological behavior-based approach, we suggest that micro-level social behaviors in the gaze, vocal, affective, and touch modalities are dynamically integrated with online physiological processes and hormonal response to create dyad-specific affiliations. Studies across multiple attachments throughout life are presented and demonstrate that the extended oxytocin (OT) system provides the neurohormonal substrate for parental, romantic, and filial attachment in humans; that the three prototypes of affiliation are expressed in similar constellations of social behavior; and that OT is stable over time within individuals, is mutually-influencing among partners, and that mechanisms of cross-generation and inter-couple transmission relate to coordinated social behavior. Research showing links between peripheral and genetic markers of OT with concurrent parenting and memories of parental care; between administration of OT to parent and infant's physiological readiness for social engagement; and between neuropeptides and the online synchrony of maternal and paternal brain response in social-cognitive and empathy networks support the hypothesis that human attachment develops within the matrix of biological attunement and close behavioral synchrony. The findings have conceptual implications for the study of inter-subjectivity as well as translational implications for the treatment of social disorders originating in early childhood, such as autism spectrum disorders, or those associated with disruptions to early bonding, such as postpartum depression or child abuse and neglect. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.     

Vocal Repertoire of Cebus capucinus: Acoustic Structure, Context, and Usage

Researchers studying nonhuman primate vocal repertoires suggest that convergent environmental, social, and motivational factors account for intra- and interspecific vocal variation. We provide a detailed overview of the vocal repertoire of white-faced capuchins, including acoustic analyses and contextual information of vocal production and vocal usage by different age-sex classes in social interactions. The repertoire is a mixture of graded and discrete vocalizations. In addition, there is general support for structural variation in vocalizations with changes in arousal level. We also identified several combined vocalizations, which might represent variable underlying motivations. Lastly, by including data on the social contexts and production of vocalizations by different age-sex classes, we provide preliminary information about the function of vocalizations in social interactions for individuals of different rank, age, and sex. Future studies are necessary to explore the function of combined vocalizations and how the social function of vocalizations relate to their acoustic structure, because social use of vocalizations may play an important role in shaping vocal evolution.     

Visualizing Sound Emission of Elephant Vocalizations: Evidence for Two Rumble Production Types

Recent comparative data reveal that formant frequencies are cues to body size in animals, due to a close relationship between formant frequency spacing, vocal tract length and overall body size. Accordingly, intriguing morphological adaptations to elongate the vocal tract in order to lower formants occur in several species, with the size exaggeration hypothesis being proposed to justify most of these observations. While the elephant trunk is strongly implicated to account for the low formants of elephant rumbles, it is unknown whether elephants emit these vocalizations exclusively through the trunk, or whether the mouth is also involved in rumble production. In this study we used a sound visualization method (an acoustic camera) to record rumbles of five captive African elephants during spatial separation and subsequent bonding situations. Our results showed that the female elephants in our analysis produced two distinct types of rumble vocalizations based on vocal path differences: a nasally- and an orally-emitted rumble. Interestingly, nasal rumbles predominated during contact calling, whereas oral rumbles were mainly produced in bonding situations. In addition, nasal and oral rumbles varied considerably in their acoustic structure. In particular, the values of the first two formants reflected the estimated lengths of the vocal paths, corresponding to a vocal tract length of around 2 meters for nasal, and around 0.7 meters for oral rumbles. These results suggest that African elephants may be switching vocal paths to actively vary vocal tract length (with considerable variation in formants) according to context, and call for further research investigating the function of formant modulation in elephant vocalizations. Furthermore, by confirming the use of the elephant trunk in long distance rumble production, our findings provide an explanation for the extremely low formants in these calls, and may also indicate that formant lowering functions to increase call propagation distances in this species''.     

Importance of sleep for avian vocal communication

Sleep is one of the few truly ubiquitous animal behaviours, and though many animals spend enormous periods of time asleep, we have only begun to understand the consequences of sleep disturbances. In humans, sleep is crucial for effective communication. Birds are classic models for understanding the evolution and mechanisms of human language and speech. Bird vocalizations are remarkably diverse, critical, fitness-related behaviours, and the way sleep affects vocalizations is likely similarly varied. However, research on the effects of sleep disturbances on avian vocalizations is shockingly scarce. Consequently, there is a critical gap in our understanding of the extent to which sleep disturbances disrupt communication. Here, we argue that sleep disturbances are likely to affect all birds'' vocal performance by interfering with motivation, memory consolidation and vocal maintenance. Further, we suggest that quality sleep is likely essential when learning new vocalizations and that sleep disturbances will have especially strong effects on learned vocalizations. Finally, we advocate for future research to address gaps in our understanding of how sleep influences vocal learning and performance in birds.     

Observational Evidences of Vocal Learning in Southern Elephant Seals: a Longitudinal Study

Vocal learning in mammals is sparsely documented, and there are few reports of vocal learning by wild mammals. In particular, no information based on longitudinal data for identified individuals exists, even for well‐studied highly social species in which vocal communication is an important aspect of social life. We present such information for the southern elephant seal (Mirounga leonina). We studied a small breeding population in the Falkland Islands over 8 yr (1995–2002). We recorded approx. 2400 agonistic vocalizations from approx. 285 different males, including many recorded over more than one breeding season (55 males were recorded for >2 yr and 29 were recorded throughout vocal development). Vocalizations are a key element of male agonistic behaviour in this species, the world's most polygynous vertebrate. For male agonistic vocalizations, we show that: (1) a limited number of discrete vocal types exists; (2) proportions of vocal types change over time; (3) observed trends of increase or decrease of vocal types are well explained by a process of vocal learning, in which younger peripheral males imitate vocal types of older more successful breeders.     

Attention to elders' voice in non-human primates

The observed respect and attention to elders'' speech in traditional cultures appears to have a ‘universal’ component which questions its possible biological bases. Animals present differential attention to the vocalizations of other individuals according to their characteristics but little is known about the potential propensity to pay more attention to vocalizations of elders. On the basis of several hundreds of vocal exchanges recorded, here we show that aged female Campbell''s monkeys (Cercopithecus campbelli), despite being significantly less ‘loquacious’ than their younger adult counterparts, elicit many more responses when calling. These findings show that attention to elders'' vocal production appears in non-human primates, leading to new lines of questioning on human culture and language evolution.     

Vocal Repertoire of Captive Capybara (Hydrochoerus hydrochaeris): Structure,Context and Function

In this work we describe the structure, behavioral context and functionality of the vocal repertoire of capybaras, a social Caviomorph rodent. Additionally, since territoriality is present in this species, we hypothesize the occurrence of vocal differences among social groups. We analyzed a total of 2069 calls emitted by 28 animals from three different social groups. The capybara’s repertoire is comprised by seven call types (whistle, cry, whine, squeal, bark, click and tooth‐chattering). The vocalizations were functionally categorized as contact, alarm, distress and agonistic calls considering their behavioral contexts. The click calls emitted by the adults of the three captive capybara groups were significantly different, confirming our hypothesis of social groups’ vocal differences. The richness of interactions mediated by vocalization in capybaras suggests that the species’ communication is an important mechanism to regulate social encounters and to alert members of the group about environmental cues.     

VOCAL REPERTOIRE OF WILD BREEDING ORANGE-WINGED PARROTS AMAZONA AMAZONICA IN AMAZONIA

ABSTRACT

The vocal repertoire of Amazona amazonica during its breeding season has been recorded from wild individuals in Santa Bárbara do Pará, Pará State, Brazil. At individual nests, we continuously recorded vocalizations and behaviour for four hours in the early morning and three hours in the late afternoon, three times a week throughout the breeding season. We identified nine vocalizations that we classified in three behavioural categories: (1) Flight call—emitted when parrots arrive in the nest area; (2) Perched contact calls—two different vocalizations, one of them related to feeding, were emitted when the pair was perched in the nest area and interacted socially between themselves or with other individuals; (3) Aggressive calls—emitted when birds were in a dangerous situation, i.e. alarm (three types of calls), agonistic contact and distress calls (two types of call). The Orange-winged Parrot is a highly social species and the complexity of its social interactions is reflected in the diversity of its vocal repertoire.     

Cultures, genes, and neurons in the development of song and singing in brown-headed cowbirds (Molothrus ater)

In brown-headed cowbirds, Molothrus ater, as in many songbird species, vocalizations are fundamental to reproduction. In our studies, experiments utilizing different social housing regimes and geographic comparisons have indicated the social learning of males' vocalizations and associated abilities to use vocalizations effectively during the breeding season. Here, we describe studies indicating roles of cultural and genetic background, and of social influences from females, on male vocal development. These influences can interact with neural regions, including song learning and song control nuclei, but also visual-processing nuclei, in the development of signaling. We argue that a developmental systems approach to the study of vocal behavior provides a structure to organize these different influences and how they may interact with one another over development. A systems approach requires that researchers study the social context in which signals and signalers develop - both the ontogenetic arena in which young animals learn their signals from older animals, and the functional arena in which young and older animals socially interact with one another.     

Context-related vocalizations in African grey parrots (Psittacus erithacus)

A few animal species are capable of vocal learning. Parrots are well known for their vocal imitation abilities. In this study, we investigated whether African grey parrots (Psittacus erithacus) emit specific vocalizations in specific contexts. We first described the vocal repertoire and its ontogenesis of four captive grey parrots. After a comparison with vocalizations emitted by wild and other captive African grey parrots, we observed that only three call categories were shared by all grey parrots populations, suggesting that isolated populations of parrots develop population-specific calls. Then, we artificially provoked ten different contexts and recorded vocalizations of four captive grey parrots in these situations. Parrots predominantly emitted call categories in some contexts: distress, protestation, alarm, asking (i.e. emitted when a bird wanted something from an experimenter) and contact calls. These results suggest that some calls are learned and can be used in specific contexts.     

Vocal Quality is Correlated with Levels of Stress Hormones in Domestic Pigs

Our study examined whether vocalizations of domestic pigs Sus scrofa domestica provide reliable cues for particular endocrine stress responses. To induce stress responses, we separated subjects individually from groupmates (SEP) and controlled potential effects of motor activity by a second treatment in which subjects were also immobilized (SEP + 1M). We analysed blood samples taken at short intervals via an indwelling catheter for titres of stress hormones to estimate endocrine stress responses. To identify behavioural responses we analysed recordings of vocalizations and non-vocal activities. Data evaluation yielded the following results. Multi-parametric sound analysis enabled us to distinguish four categories of vocalizations within treatments. Increasing rates of ‘squeal-grunts’ indicated increasing plasma levels of adrenaline, whereas the rates of ‘grunts’ decreased when the levels of cortisol increased. Acoustic parameters within the vocal categories distinguished did not correlate consistently with levels of any of the measured stress hormones; thus, our results show that peripheral endocrine stress responses are accompanied by changing rates of specific types of vocalizations. These relationships remained consistent, even when subjects' motor activity was restricted. Our results suggest possible effects of central stress reactions on both the control of vocalization and the activation of endocrine stress responses.     

Vocal repertoire of the social Mashona mole-rat (Fukomys darlingi) and how it compares with other mole-rats

Vocalizations play a major role in communication of mammals with subterranean lifestyles since other senses are dramatically restricted in the environment of below ground burrows. In our study, we recorded vocalizations of 10 adult males and 10 adult females of a social bathyergid, the Mashona mole-rat (Fukomys darlingi) in different behavioural contexts. Vocalizations were divided into four categories according to behavioural contexts. Similar to other subterranean mammals, the range of Mashona mole-rat calls is shifted towards lower frequencies. We described 10 types of true vocal signals and 2 mechanical sounds. The vocal repertoire of the Mashona mole-rat is less rich compared to other social mole-rats, corresponding with its low mean family size. Interestingly, this species has a higher diversity in contact and distress calls, while using a relatively low number of aggressive signals.     

Vocal signature in capybara,Hydrochoerus hydrochaeris

Social groups of capybaras are stable and cohesive. The species’ vocal communication is complex and mediates social interaction. The click call is emitted in a variety of contexts by animals from all age groups, but differs among groups; its attributed function is to keep contact among animals. To evaluate the presence of individual characteristics in the click call of capybaras, we recorded the vocalizations emitted spontaneously by six adults kept either solitary or in groups. We selected and measured the acoustic parameters of 300 click call phrases, 50 per individual. The parameters were submitted to a discriminant function analysis that revealed a classification accuracy of 76.8 %. A General Linear Model analysis revealed significant differences among the six individuals, and post hoc results showed that differences between a given pair were different from those of any other pair. The acoustic parameters that most contributed to discriminate the individual calls were click interval duration and click duration, suggesting that temporal parameters are more important than frequency parameters for individuals’ discrimination. The findings of individual characteristics in the click calls indicate that these vocalizations can be used as vocal signatures during social interactions.     

Vocal culture in New Caledonian crows Corvus moneduloides

While recent research suggests that some animal species may possess ‘cultural’ traditions, much of the current evidence for wild populations remains contentious. This is largely due to the difficulty of demonstrating a fundamental prerequisite for the existence of culture: social learning. As the only case where social learning has been demonstrated conclusively, and subsequently linked to spatial or temporal trait variation, avian vocal dialects are the best studied, and most widely accepted, form of animal culture. Here, we investigate the potential for vocal culture in one of the few animals for which material culture has been suggested: the New Caledonian crow Corvus moneduloides. We show that this species: (1) possesses the capacity for social learning of vocalizations (experimental evidence in the form of a captive subject that reproduces human speech and other anthropogenic noises); and (2) exhibits significant large‐scale, population‐level variation in its vocalizations (cross‐island playback experiments, with analyses controlling for a substantial set of potentially confounding variables). In combination, this provides strong evidence for the existence of ‘culture’ in these birds. More specifically, our findings reveal that the species exhibits sufficient social learning mechanisms, and within‐population structuring, to generate and perpetuate cultural variation in at least one behavioural domain. This is a critical first step towards demonstrating cultural transmission in other behaviours, including tool manufacture and tool use, opening the door for the simultaneous investigation of vocal and material culture in a nonhuman species. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 767–776.     

Social Environment Affects Peripheral Oxytocin and Cortisol during Stress Responses in Guinea-Pigs

Numerous studies have demonstrated interactions between oxytocin (OT) secretion, adrenal activity, an animal's social environment, and stress responses. In the present study, we hypothesized that partner preference and pair bonding cause increased peripheral OT, which down‐regulates the adrenal and behavioral response in stress. In addition, we tested whether these interactions depended on sex, the social environment of the individual, or the type of stressor. Experiments were carried out on guinea‐pigs held in sexual‐pairs or stressed by isolation. Among the paired individuals choice tests were carried out to document partner preference. Female preference for a male was expressed by spatial cohesion. Stress responses to abiotic stimuli were examined and compared between isolated and cohabited animals with or without preference. Results show that OT of cohabited animals was significantly higher than during isolation. OT levels were further increased in males preferred by females. Cortisol (CORT) levels were elevated in isolated animals. There were no significant differences between pairs with and without female preference. Behaviorally, partner preferences were expressed by high amounts of tactile contact. The stress‐induced behavioral immobility response after exposure to a noise stressor was significantly reduced in preferred males and to a lesser extent in their female partners. Only females with preferences showed an endocrine stress response. Their levels of OT increased. There was no consistent post‐stressor release of CORT. The data indicate that the social environment of an individual, here expressed as preference or isolation, influences peripheral OT secretion. Behavioral stress responses were similarly affected by social factors without a clear involvement of peripheral CORT or OT.     

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

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

Cues to Androgens and Quality in Male Gibbon Songs

Animal vocal signals may provide information about senders and mediate important social interactions like sexual competition, territory maintenance and mate selection. Hence, it is important to understand whether vocal signals provide accurate information about animal attributes or status. Gibbons are non-human primates that produce loud, distinctive and melodious vocalizations resembling more those of birds than of other non-human primates. Wild gibbons are characterized by flexibility in social organization (i.e., pairs and multimale units) as well as in mating system (i.e., monogamy and polyandry). Such features make them a suitable model to investigate whether the physiology (hormonal status) and socio-demographic features find their correspondence in the structure of their songs. By combining male solo song recordings, endocrine outputs using non-invasive fecal androgen measures and behavioral observations, we studied 14 groups (10 pair-living, 4 multimale) of wild white-handed gibbons (Hylobates lar) residing at Khao Yai National Park, Thailand. We collected a total of 322 fecal samples and recorded 48 songs from 18 adult animals. Our results confirmed inter-individuality in male gibbon songs, and showed a clear correlation between androgen levels and song structures. Gibbons with higher androgen levels produced calls having higher pitch, and similarly adult individuals produced longer calls than senior males. Thus, it is plausible that gibbon vocalizations provide receivers with information about singers'' attributes.