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Vocal flexibility in nonhuman primates and the origins of human language

Flexibilité vocale chez les primates non-humains et origines du langage humain
Hélène Bouchet, Hiroki Koda, Nobuo Masataka et Alban Lemasson

Résumés

Nobuo Masataka (Université de Kyoto, Japon), Alban Lemasson (Université de Rennes 1, France) et leurs collègues collaborent depuis une décennie à des projets s'intéressant au comportement vocal des primates non-humains et contribuant à élucider la question des origines évolutives du langage. Ils ont travaillé ensemble sur des sujets variés incluant la flexibilité vocale sous influences sociales chez l'adulte, le développement des capacités communicatives au cours de l'ontogénie, et la perception auditive et visuelle de stimuli sociaux et non-sociaux. Dans cet article, nous passons en revue ce travail en l'inscrivant dans le cadre théorique de l'évolution du langage.

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Notes de la rédaction

Article reçu le 04/12/2015. Définitivement accepté le 27/01/2016.

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1 Collaboration history

1Nobuo Masataka is the head of the Cognition & Learning section of the Primate Research Institute (University of Kyoto, Japan). Alban Lemasson is the head of the Animal & Human Ethology lab (University of Rennes 1, France). Hiroki Koda and Hélène Bouchet are their former PhD students. Both our teams decided to engage in a long-term collaboration a decade ago, as we shared a common interest in nonhuman primates' vocal communication and in the evolutionary origins of human language.

2The collaboration started when Lemasson was hosted by Masataka as a post-doctoral fellow at the Primate Research Institute in Japan in 2004/2005. Upon Lemasson’s return to France, where he took a position as Lecturer at the University of Rennes 1, the two maintained strong bonds. Over the last decade, regular visits at each site have taken place, and several French and Japanese students and young researchers have taken part in the collaboration with co-supervised research programs (Assistant Professor: Hiroki Koda; Postdoctoral fellows: Hélène Bouchet, Malgorzata Arlet; PhD students: Chisako Oyakawa, Muriel Basile, Anna Sato; Bachelor and Master students: Manon Guilloux, Kévin Remeuf, Ludivine Glas). Research programs received financial support from the Japan Society for the Promotion of Science ("Postdoctoral Fellowship for Overseas Researchers" and "Young Researcher Overseas Visits" programs), the French Ministries of Foreign Affairs and of Higher Education and Research (Partenariat Hubert Curien "Sakura"), as well as the French National Centre for Scientific Research ("Projet International de Coopération Scientifique").

3Below, we first review the theoretical framework of research on vocal communication in nonhuman primates and its impact on the debate about the origins of human language, with illustrations from lab and field studies conducted independently by Masataka and Lemasson, and their colleagues. We then present our common research achievements along three axes: vocal flexibility under social influences in adults, vocal development in juveniles, and perceptual abilities.

2 Theoretical research framework: Separate contributions of the French and Japanese teams

4Language plays a pivotal role in human societies, and the question of its origins is a hotly debated topic. Like any complex biological trait, it is unlikely to have evolved de novo, and it probably has a long evolutionary history. However, it is nearly impossible to find direct fossil-based evidence of the evolutionary path of language properties because they are of a behavioural nature. One alternative way to address this question is to examine the anatomical features, communicative mechanisms and cognitive abilities of humans compared to those of more or less phylogenetically related animals. Nonhuman primates, our closest relatives, are prime candidates for such a comparative approach. To look for the roots of human language, which is primarily of an acoustic nature with a social function, it is valuable to investigate the characteristics of vocal communication in nonhuman primates and the underlying cognitive and social mechanisms; this is the approach taken by both Masataka's and Lemasson's teams.

5However, a few decades ago, the classic way to think of nonhuman primates' vocalizations was to consider them as reflex-driven expressions of the caller's internal state (Jürgens, 1995). Both our teams have conducted studies confirming the acoustic encoding of arousal, a phenomenon also described in humans (Breitenstein et al., 2010). For example, in squirrel monkeys, isolation calls given by all group members have a longer duration when infants are separated further away from their natal group (Masataka and Symmes, 1986). Similarly, in three species of Old World monkeys, a separation-reunion experimental paradigm provided evidence of affect-induced changes in the use of contact calls (higher call rates) and their structure (longer and higher-pitched calls) (Lemasson et al., 2012). But we now know that this is only part of the range of messages encoded acoustically, and that nonhuman primates have some degree of control over their vocal production. In line with this, studies using operant conditioning experiments and vocal adjustment during helium exposure have shown that white-handed gibbons can control their call emission and structure (Koda et al., 2007, 2012).

6Some nonhuman primates' calls also function as referential signals conveying information about external stimuli, a function analogous to semantics in human language. In Goeldi's marmosets, the acoustic structure of alarm calls provides reliable information about predator type (aerial versus terrestrial); this is used by listeners to decide whether to climb down and freeze (aerial danger) or to climb up and respond with warning calls (terrestrial danger) (Masataka, 1983). In Campbell's monkey males, alarm calls are produced in complex sequences whose composition (call types and order of call delivery) and rhythm of emission, as well as the acoustic structure of the calls itself (temporal and frequency parameters), encode information about the type of danger (e.g. tree fall, intergroup encounter, predator encounter and whether it is aerial or terrestrial) and the level of urgency (Ouattara et al., 2009a, 2009b; Lemasson et al., 2010c). By analysing the multi-level structure of monkeys' vocal emissions, these latter studies even revealed call combinations akin to affixation and syntax in human language (Zuberbühler and Lemasson, 2013; Coye et al., 2015). Also, by comparing populations living in habitats with different predator pressures, "lexical" dialects were found (Schlenker et al., 2014).

7The parallel with human language goes even further, with clear demonstrations of acoustic plasticity. In several primate species, contact calls have been found to function as "social badges". For example, acoustic analyses of contact coo calls in Japanese macaques revealed habitat-related population differences (Sugiura et al., 2006), socially-driven "phonological" dialects (Tanaka et al., 2006), and individual identity coding (Ceugniet and Izumi, 2004). In Campbell's monkeys, females produce several variants of their contact CH (combined harmonic) calls, some of which are shared by close affiliative partners (Lemasson and Hausberger, 2004). This remarkable phenomenon is dynamic (long term vocal convergence), as vocal sharing parallels the changes in social networks over time (Lemasson and Hausberger, 2004; Lemasson et al., 2011b). Interestingly, by screening the entire vocal repertoire of Campbell's monkeys and other Old World species (red-capped mangabeys and De Brazza's monkeys), identity coding has been found to be more reliable in calls mediating inter-individual social interactions (e.g. contact calls) than in socially less-targeted calls (e.g. food calls, alarm calls) (Lemasson and Hausberger, 2011; Bouchet et al., 2012b, 2013a). Identity coding is thus call type-dependent, but also varies with the context. For instance, Diana monkeys produce more stereotyped (individually distinctive) calls when travelling in dark compared with bright habitats, to facilitate spatial cohesion in the forest (Candiotti et al., 2012). An interesting parallel can be drawn with human language, as the amount of identity cues in speech is adjusted according to the audience design (vocal accommodation theory: Giles et al., 1991).

8The inter-individual (social interaction) level of analysis has also revealed some interesting parallels with human language. Vocal exchanges in nonhuman primates have been found to resemble primitive forms of conversations, as they follow a number of interaction rules that are universal across human cultures (Sugiura and Masataka, 1995; Henry et al., 2015). For example, Campbell's monkeys, Japanese macaques and marmosets respect a minimum and maximum inter-speech delay (to avoid calling simultaneously and ensure the continuance of the interaction) as well as a turn-taking principle (i.e. the two interlocutors alternate their calls) (Sugiura and Masataka, 1995; Lemasson et al., 2010a; see also Takahashi et al., 2013). Interestingly, social factors influence the organisation of vocal exchanges: in Campbell's monkeys, elders are more likely to receive a vocal response (Lemasson et al., 2010a; see also for marmosets: Chen et al., 2009), while in squirrel monkeys, closely-affiliated partners are preferred interlocutors (Biben et al., 1986). Nonhuman primates are even capable of elaboration and persistence (two markers of intentional communication in humans) to increase their chances of getting a vocal response (Koda, 2004). They are also able to acoustically copy (immediate vocal convergence) their partner during a vocal exchange, by producing a response call that structurally matches the one produced by their interlocutor (Sugiura, 1998); this phenomenon of "call matching" has also been observed in Diana monkeys and chimpanzees (Mitani and Brandt, 1994; Candiotti et al., 2012).

9The above-mentioned studies relate to adult plasticity, but human language is socially learnt at very early stages of development. Since the earliest works in the 1970s and 1980s, vocal development in nonhuman primates has been considered to be under strong genetic control. Social deprivation, deafening, hybridizing, and infant cross-fostering experiments revealed that nonhuman primates possess adult calls since birth and that they display little to no acoustic variability throughout their life (see Hammerschmidt and Fischer, 2008, for a review). But more recently, technical progress in acoustic analyses and a renewal of interest in vocal variability revealed some degree of acoustic variability during development (see Snowdon, 2009, for a review), and even a remarkable phenomenon of babbling in marmosets (Snowdon and Elowson, 2001).

10In addition to the ontogeny of acoustic structure, a growing number of studies have provided evidence for social learning of the appropriate context of calling (see Seyfarth and Cheney, 1997; or Snowdon, 2009, for a review). For instance, any kind of flying object elicits an alarm call in young vervet monkeys, but through observation of adults' behaviour, they learn to become more selective and to use this call type only if they have spotted real aerial predators (Seyfarth and Cheney, 1997). In Japanese macaques, the appropriate use of greeting calls, notably the choice of specific receivers, is acquired in the course of development, probably under the social influence of group members (Katsu et al., 2014). These studies have to some extent challenged the view of primate vocal behaviour as innate and inflexible, and they have highlighted the value of investigating vocal development in conjunction with the social environment.

11To have a complete understanding of the mechanisms and functions underlying primate communication, as well as vocal production and usage, another important dimension to study is auditory perception. For a message to be conveyed, receivers must be able to discriminate between the fine acoustic variations described above. Thus, the cognitive abilities and neuropsychological mechanisms underlying nonhuman primates' perceptual capacities are an important area of research. Studies have provided evidence that various species of primates are able to perceive contextual variants and individual differences. For example, playback experiments have shown that monkeys, notably Japanese macaques, are able to discriminate between contextual variants of coo calls (Le Prell and Moody, 2000), girneys (Masataka, 1989) and screams (Le Prell et al., 2002), and that they are capable of vocal recognition of individuals (intra-group: Ceugniet and Izumi, 2004b; Lemasson et al., 2008 – inter-group: Briseño-Jaramillo et al., 2015 – inter-species: Candiotti et al., 2013), including mother-offspring pairs (Masataka, 1985; Shizawa et al., 2005), and both maternal (Rendall et al., 1996) and even paternal kin (Pfefferle et al., 2014). Playback studies in different guenon species revealed that individual signatures are memorized for at least four years (Lemasson et al., 2005) and that referential alarm calls are decoded at both conspecific and heterospecific levels (Zuberbühler, 2000; Coye et al., 2015).

12The assessment of nonhuman primates' perceptual abilities can provide insights regarding the evolutionary origin of language processing. For example, although the left cerebral hemisphere is known to play an essential role in the processing of speech in humans, there is also evidence of some task-sharing between the two hemispheres, with the left hemisphere specializing in processing of syntactic and semantic activities, and the right hemisphere attending preferentially to the prosody or novelty of a signal (Friederici and Alter, 2004). No clear consensus about the phylogenetic origin of this hemispheric specialization has yet been reached, although there is some evidence for the importance of familiarity with the speaker as well as the emotional valence of the interaction on brain asymmetry in both human and nonhuman primates (Basile et al., 2009).

3 Contributions of the France-Japan collaboration: A further step toward understanding primate communication

3.1 Vocal flexibility under social influences

13To learn more about vocal flexibility in nonhuman primates, our teams have collaborated on two studies of the use of contact coo calls by adult Japanese macaques, with a special focus on the impact of the social characteristics of the caller and its interlocutor.

14First, Lemasson and Masataka investigated sex differences in usage style of contact calls (Lemasson et al., 2013a). They studied a group containing 8 adult males and 18 adult females, housed at the Primate Research Institute (University of Kyoto). Adult females were found to be more vocally active than males, and they also contributed more frequently to conversation-like vocal exchanges respecting the turn-taking rule. Interestingly, age was an important parameter: older females received increasingly more vocal responses from other group members. In males, however, dominance rank was the determining factor influencing call usage style, with lower-ranking males producing more repeated (juvenile-like) sequences than higher-ranking males.

15Sex differences in nonhuman primates’ calls can take the form of acoustic discrepancy (e.g. lower-pitched and longer calls in males) mostly related to differences in size and body weight (Ey et al., 2007). But differences in call usage (e.g. higher call rates, preferential usage of certain call types) are thought to be related to sex-specific social roles (Bouchet et al., 2010, 2012a). Females form the social core of the group in Japanese macaques, notably because they do not emigrate at puberty (Nakamichi and Yamada, 2010). They are thus often involved in mediation of intra-group social relationships, hence the frequent use of affiliative calls especially within socially ruled vocal exchanges. In addition, the order of participation within a vocal exchange is age-dependent, elders coming first, a pattern already known for other monkeys and in the conversations of most traditional oral, and some modern, human societies (Lemasson et al., 2010a). Age is socially important in Japanese macaques, with older matriarchs possessing a particular social status (Nakamichi and Yamada, 2010). Males, by contrast, are more socially peripheral, acting mostly as group protectors and playing a role in social vigilance and inter-group spacing, hence the lesser use of social calls. Their hierarchical rank is nevertheless a critical determinant of their position, with dominant males being more integrated within the troop (Horiuchi, 2005). Interestingly, conversely to females, whose dominance rank is stable as it is determined by age and kinship (Nakamichi and Yamada, 2010), male inter-troop transfers cause frequent rank changes among resident males (Suzuki et al., 1998).

16A subsequent study asked whether vocal exchanges might parallel the social network, given that affiliative calls are used in mediating social interactions (Arlet et al., 2015). Two captive groups of Japanese macaques were studied, including 17 and 28 adult females respectively, housed at the Primate Research Institute in two very different enclosures (one relatively small with open visibility, and one large and forested). We tested whether affiliative relationships (measured through dyadic spatial proximity and grooming scores), kinship, dominance rank and age differences could predict the distribution of dyadic vocal exchanges. We found that contact call rates between two given females correlated only with the time spent grooming each other, regardless of the group. Interestingly, contact calls were mostly exchanged between females when they were distant from each other. Lastly, dyads presenting a higher level of grooming reciprocity also initiated vocal exchanges in a more balanced way.

17These findings support the idea that social factors outweigh environmental factors in explaining flexibility in social call usage. Furthermore, this study provided empirical evidence for the predictions of the social bonding hypothesis developed by Dunbar (1996). This theory argues that vocal exchange rates evolved together with group size in primates, in order to facilitate the maintenance of cohesion between spatially-distant affiliated partners. Thus, once it became impossible to allocate enough time to physically interact with all affiliated group members, vocalizations replaced manual grooming as a form of "vocal grooming-at-a-distance", a step towards the emergence of conversations in the primate lineage.

3.2 Vocal development

18The existence of vocal flexibility in adult nonhuman primates raises questions about how this variability emerges during ontogeny; there is a need for more studies in this domain. Our teams have collaborated on four studies investigating various aspects of vocal development in three nonhuman primate species.

19One study, conducted at the Primate Research Institute, investigated the development of contact call use in Japanese macaques (Lemasson et al., 2013a). This study (already mentioned above) provided evidence of sex differences in vocal usage in adults. However, observations of 10 juveniles (5 males, 5 females, average age: 8–10 months old) revealed no sex differences at this early age. Overall, juveniles differed from adults by their higher overall vocal activity, and by their production of similar rates of isolated calls, repeated sequences (the same individual calls several times in a row) and exchange sequences (the individual responds vocally to or receives a response from a group member); adults, by contrast, called mostly within temporally ruled vocal exchanges. Also, when juveniles contributed to vocal exchanges, they respected the turn-taking rule far less than adults.

20Higher levels of vocal activity and absence of sex differences in juveniles have also been observed in other species, for example De Brazza's monkeys (Bouchet et al., 2012a). This suggests that appropriate use of calls emerges through experience and social integration. As they grow older, individuals acquire more distinct social roles (Eaton et al., 1985) and their vocal activity evolves accordingly. This process is hypothesized to be based on social learning from same-sex adult models. Our findings add to the growing literature showing that juveniles learn appropriate contexts of call emission from adults (Seyfarth and Cheney, 1997; Snowdon, 1997; Roush and Snowdon, 2001).

21A second study focused on the turn-taking rule in another monkey species, again by comparing the appropriateness of call patterns between adults and juveniles, and also by testing the cognitive relevance of this rule in both age-classes (Lemasson et al., 2011a). Observations of 7 adult females and 7 youngsters, housed at the Station Biologique de Paimpont (University of Rennes 1), revealed that juveniles spontaneously break the turn-taking rule twelve times more often than adults. Furthermore, playback experiments showed that adult females discriminated between call exchanges that respected the turn-taking between callers and those that did not, whereas youngsters did not.

22In a third study, using similar playback experiments based on the violation-of-expectation paradigm, Bouchet et al. (2013b) tested whether adult and juvenile Japanese macaques equally paid attention to the call-matching rule. As mentioned earlier, during vocal exchanges, adult female Japanese macaques acoustically copy their partner's calls (Sugiura, 1998). Observations revealed that sub-adults (aged 3-5 years old) were less efficient than adults at respecting the call-matching rule (Sugiura, 1998; Masataka, 2003). Here, we tested the ability of 10 adult females and 10 one-year-old females, housed at the Primate Research Institute, to discriminate between vocal exchanges that respected the call-matching rule or not. Again, only adults displayed different levels of interest for the two types of stimuli.

23All of the above findings suggest that experience and social learning are involved in the emergence of different conversational rules. In fact, a recent study in marmosets provided empirical evidence that the turn-taking rule is learned during ontogeny under adult tutoring: adults reinforced their offspring by responding to calls that followed the species-typical temporal pattern, but remained silent following interrupted calls (Chow et al., 2015). Interestingly, in human infants too, turn-taking and vocal imitation improve within the first few months of life, supported by feedback from the mother during vocal interactions (Masataka, 1992, 1993, 2003).

24Finally, to better our understanding of maternal roles in monogamous primates, Koda and Lemasson investigated the development of wild gibbons' singing behaviour based on field data collected in Sumatra (Indonesia) (Koda et al., 2013b). Pairs of adult gibbons produce complex duets during which male and female sing synchronously. As part of those duets, adult females produce great calls which are individually distinctive (Oyakawa et al., 2007). Juveniles do not produce adult-like great calls, but sub-adult daughters are regularly involved in synchronized and overlapping great call interactions with their mother. We observed 6 female agile gibbons and their sub-adult daughters at different stages of development (inferred from co-singing rates). First, we found acoustic matching between mothers and daughters at the time of co-singing, which suggests abilities in immediate copying. Second, mothers were found to produce songs in a more stereotyped manner during mother-daughter interactions, especially at early stages of development, possibly to facilitate synchronization and their daughters’ learning of the appropriate acoustic structure. Lastly, during development, the degree of acoustic resemblance between mother (but not other adult females) and daughter increases, along with the precision of synchronization in the duet.

25This study provides evidence of a complex mechanism of song acquisition in sub-adult female gibbons, and highlights the maternal influence on offspring vocal development. Empirical evidence of social learning under parental influences and maternal tutoring is still very scarce. A recent study in marmosets demonstrated that infant calls undergo dramatic changes during the first two months of life, transforming from cries into mature adult-like phee calls. The timing of this transition was partly attributable to maturation but was also strongly influenced by contingent parental vocal feedback (Takahashi et al., 2015).

3.3 Perceptual abilities

26To know whether the acoustic variability observed is salient for the nonhuman primates themselves requires experiments. Playback experiments offer the possibility to investigate which characteristics of the acoustic stimuli subjects are sensitive to. Masataka's and Lemasson's teams have conducted two studies on the relevance of social and non-social acoustic stimuli in Japanese macaques and Campbell's monkeys, as well as a study testing for the pertinence of social visual stimuli in the same two species.

27One study was conducted to explore the effects of sound specificity and familiarity on auditory laterality in Japanese macaques (Lemasson et al., 2010b). Six adult females, housed at the Primate Research Institute, heard 10 categories of familiar and non-familiar nonhuman primate contact calls (familiar: calls of chimpanzees and gibbons housed at the same facility versus unfamiliar: calls of Campbell's monkeys, De Brazza's monkeys and red-capped mangabeys housed at the Station Biologique de Paimpont), bird calls (familiar: Japanese crows versus unfamiliar: French geese), and non-biological sounds (familiar: sound of pellets being poured into a bucket versus unfamiliar: piano melodies). Interestingly, familiarity, and not specificity, influenced auditory laterality but only for nonhuman primate calls, and not for other types of sounds. Experiments using the head-turn paradigm revealed a left-side head orientation (i.e. right cerebral hemisphere processing) bias at the group level for familiar nonhuman primates of the same or other species.

28This finding confirms that the left-hemisphere dominance for communication processing in the primate lineage may have been over-emphasized, and that more studies investigating task-sharing between hemispheres are needed, "social" familiarity between interlocutors being an important factor to take into account. This finding also suggests that individual recognition is possible at the heterospecific level (see also Candiotti et al., 2013), a potentially important ability for primates that share habitats with other species.

29A second study asked whether there was a preference for consonant over dissonant sounds in Campbell's monkeys (Koda et al., 2013a). An earlier study showed that Japanese macaques were able to discriminate between consonant and dissonant chords (Izumi, 2000). The distribution of this perceptual ability across the primate lineage is particularly interesting for unravelling the phylogenetic origin of musicality in humans, who spontaneously prefer consonant over dissonant sounds from early infancy (Zentner and Kagan, 1998). Musical ability, and the underlying cognitive mechanisms, have been hypothesized to constitute an intermediate stage in the evolution of language in the order Primates (Masataka, 2007, 2009). In our study, 6 adult female Campbell's monkeys, housed at the Station Biologique de Paimpont, were tested in an experimental paradigm that enabled monkeys to express their auditory preferences. We applied a sensory reinforcement paradigm based on the spontaneous spatial positioning of the subject, free to move in its habitual enclosure, which was divided into two identical sections. As soon as the monkey moved to one side, the corresponding loudspeaker played one of the paired-comparison sounds until the monkey crossed the central line and moved to the other side, resulting in the other paired-comparison sound being immediately broadcast from the opposite speaker. Monkeys showed no preference for consonant over dissonant stimuli, even though the experimental paradigm was verified as monkeys displayed a preference for soft over loud white-noise control stimuli.

30In another study using the same experimental paradigm, tamarins did not show any preference for consonant chords (McDermott and Hauser, 2004). Only one human-reared infant chimpanzee has been reported to exhibit this preference (Sugimoto et al., 2010); enculturation and previous experience of hearing music may account for its peculiar sensitivity to consonance. As very few music-based studies have been conducted comparing human and nonhuman primates, at present it is possible to conclude only that sensitivity to musical harmony has not been established in the latter; further investigations are needed.

31Lastly, on a topic unrelated to the evolution of language but related to sensory and social preferences, our teams conducted a study of visual recognition of age-class and preference for infantile features in two species of Old World monkeys (Sato et al., 2012). In humans, infantile features are innately perceived as cute (Sanefuji et al., 2007); it is thought that attraction to "babyness" motivates caretaking behaviour. We tested 11 female Japanese macaques housed at the Primate Research Institute and 10 female Campbell's monkeys housed at the Station Biologique de Paimpont. Visual paired comparison tasks were conducted to test for the ability to discriminate between infant and adult images (of Japanese macaques) of their own species (Japanese macaque subjects) or of another species (Campbell's monkey subjects). Japanese macaques strongly discriminated, exhibiting a preference for infant over adult images. At the heterospecific level, Campbell's monkeys produced a weaker response, but still looked longer at infant versus adult images of Japanese macaques, suggesting that the attractiveness of infant images transcends species differences.

32Nonhuman primate societies, like human society, are based on complex interactions between individuals who differ in their social roles. Age is a key determinant of social status, thus visual recognition of age-class, as with the perception of identity cues in vocal signals, might be critical for social group functioning. Humans can perceive not only conspecific but also heterospecific "babyness" (Sanefuji et al., 2007). Our study provides evidence that this may also be the case in nonhuman primates, although additional studies in a wider range of species are needed.

4 Conclusion

33The France-Japan collaboration has enabled both our teams to share their knowledge of experimental paradigms and some methodological (e.g. acoustic analysis) tools, to get access to research facilities for primate behaviour studies in each country, and to conduct comparative studies on a wide range of socially varied primate species. Together, Masataka's and Lemasson's teams have contributed significantly to the current debate about vocal flexibility in nonhuman primates and the evolutionary origins of human language. Their studies highlight the critical influence of social factors on the emergence of acoustic variability in nonhuman primates with some key results as follows: 1) vocal activity is determined by the subject's social status within the group; 2) the network of vocal exchanges parallels the network of affiliative interactions; 3) the appropriate acoustic structure of calls and the appropriate context of calling are to some extent subject to social learning; 4) parental feedback shapes offspring vocal ontogeny; 5) perceptual abilities for discriminating between various social acoustic and visual stimuli are related to social functioning and experience.

34Over the years, our teams have gained extended knowledge, from both field and captive studies, about the communicative behaviour of two species notably: the Japanese macaque, a species endemic to Japan that lives in large multi-male multi-female groups, and the Campbell's monkey, an African guenon species that lives in harems. Comparative studies in these two, now well-known, key species whose social systems differ might allow us to further test the hypothesis of a co-evolution between social life and communicative abilities in the primate lineage (Dunbar, 1996; Masataka, 2008; Lemasson, 2011). This opens new lines of investigation regarding the factors which led to the emergence of the highly complex communication system that is human language (Zuberbühler et al., 2009; Lemasson et al., 2013b; Bouchet et al., 2016).

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Bibliographie

Arlet M, Jubin R, Masataka N, Lemasson A (2015). Grooming-at-a-distance by exchanging calls in nonhuman primates. Biology Letters 11, 20150711. doi: 10.1098/rsbl.2015.0711

Basile M, Lemasson A, Blois-Heulin C (2009). Social and emotional values of sounds influence human (Homo sapiens) and non-human primate (Cercopithecus campbelli) auditory laterality. PLoS ONE 4, e6295. doi: 10.1371/journal.pone.0006295

Biben M, Symmes D, Masataka N (1986). Temporal and structural analysis of affiliative vocal exchanges in squirrel monkeys (Saimiri sciureus). Behaviour 98, 259–273. doi: 10.1163/156853986X00991

Bouchet H, Blois-Heulin C, Lemasson A (2012a). Age- and sex-specific patterns of vocal behavior in De Brazza’s monkeys (Cercopithecus neglectus). American Journal of Primatology 74, 12–28. doi: 10.1002/ajp.21002

Bouchet H, Blois-Heulin C, Lemasson A (2013a). Social complexity parallels vocal complexity: A comparison of three non-human primate species. Frontiers in Psychology 4, 390. doi: 10.3389/fpsyg.2013.00390

Bouchet H, Blois-Heulin C, Pellier A-S, Zuberbühler K, Lemasson A (2012b). Acoustic variability and individual distinctiveness in the vocal repertoire of red-capped mangabeys (Cercocebus torquatus). Journal of Comparative Psychology 126, 45–56. doi: 10.1037/a0025018

Bouchet H, Coye C, Lemasson A (2016). Le langage est-il le propre de l’homme? Apports des études sur les primates non humains. Tétralogiques 21, 87–133. http://www.ressources.univ-rennes2.fr/ciaphs/tetralogiques/spip.php?article30

Bouchet H, Koda H, Masataka N, Lemasson A (2013b). Do adults and youngsters equally pay attention to vocal exchange rules? The case of call matching in Japanese macaques. (oral communication at the 5th EFP congress). Folia Primatologica 84, 251. doi: 10.1159/000354129

Bouchet H, Pellier A-S, Blois-Heulin C, Lemasson A (2010). Sex differences in the vocal repertoire of adult red-capped mangabeys (Cercocebus torquatus): A multi-level acoustic analysis. American Journal of Primatology 72, 360–375. doi: 10.1002/ajp.20791

Breitenstein C, van Lancker D, Daum I (2010). The contribution of speech rate and pitch variation to the perception of vocal emotions in a German and an American sample. Cognition and Emotion 15, 57–79. doi: 10.1080/02699930126095

Briseño-Jaramillo M, Estrada A, Lemasson A (2015). Individual voice recognition and an auditory map of neighbours in free-ranging black howler monkeys (Alouatta pigra). Behavioral Ecology and Sociobiology 69, 13–25. doi: 10.1007/s00265-014-1813-9

Candiotti A, Zuberbühler K, Lemasson A (2012). Convergence and divergence in Diana monkey vocalisations. Biology Letters 8, 382–385. doi: 10.1098/rsbl.2011.1182

Candiotti A, Zuberbühler K, Lemasson A (2013). Voice discrimination in four primates. Behavioural Processes 99, 67–72. doi: 10.1016/j.beproc.2013.06.010

Ceugniet M, Izumi A (2004). Vocal individual discrimination in Japanese monkeys. Primates 45, 119–128. doi: 10.1007/s10329-003-0067-3

Chen HC, Kaplan G, Rogers LJ (2009). Contact calls of common marmosets (Callithrix jacchus): Influence of age of caller on antiphonal calling and other vocal responses. American Journal of Primatology 71, 165–170. doi: 10.1002/ajp.20636

Chow CP, Mitchell JF, Miller CT (2015). Vocal turn-taking in a non-human primate is learned during ontogeny. Proceedings of the Royal Society of London B 282, 20150069. doi: 10.1098/rspb.2015.0069

Coye C, Ouattara K, Zuberbühler K, Lemasson A (2015). Suffixation influences receivers’ behaviour in non-human primates. Proceedings of the Royal Society of London B 282, 20150265. doi: 10.1098/rspb.2015.0265

Dunbar RIM (1996). Grooming, gossip, and the evolution of language. Cambridge, MA: Harvard University Press.

Eaton GG, Johnson DF, Glick BB, Worlein JM (1985). Development in Japanese macaques (Macaca fuscata): Sexually dimorphic behavior during the first year of life. Primates 26, 238–247. doi: 10.1007/BF02382400

Ey E, Pfefferle D, Fischer J (2007). Do age- and sex-related variations reliably reflect body size in non-human primate vocalizations? A review. Primates 48, 253–267. doi: 10.1007/s10329-006-0033-y

Friederici AD, Alter K (2004). Lateralization of auditory language functions: A dynamic dual pathway model. Brain and Language 89, 267–276. doi: 10.1016/S0093-934X(03)00351-1

Giles H, Coupland N, Coupland J (1991). Accommodation theory: Communication, context, and consequence. In Contexts of Accommodation: Developments in Applied Sociolinguistics, Giles H, Coupland N, Coupland J (eds). Cambridge, UK: Cambridge University Press. pp. 1–68.

Hammerschmidt K, Fischer J (2008). Constraints in primate vocal production. In Evolution of Communicative Flexibility: Complexity, Creativity, and Adaptability in Human and Animal Communication, Oller DK, Griebel U (eds). Cambridge, MA: MIT Press. pp. 93–119.

Henry L, Craig AJFK, Lemasson A, Hausberger M (2015). Social coordination in animal vocal interactions. Is there any evidence of turn-taking? The starling as an animal model. Frontiers in Psychology 6, 1416. doi: 10.3389/fpsyg.2015.01416

Horiuchi S (2005). Affiliative relations among male Japanese macaques (Macaca fuscata yakui) within and outside a troop on Yakushima Island. Primates 46, 191–197. doi: 10.1007/s10329-005-0131-2

Izumi A (2000). Japanese monkeys perceive sensory consonance of chords. Journal of the Acoustical Society of America 108, 3073–3078. doi: 10.1121/1.1323461

Jürgens U (1995). Neuronal control of vocal production in nonhuman and human primates. In Current Topics in Primate Vocal Communication, Zimmermann E, Newman JD, Jürgens U (eds). New-York: Plenum Press. pp. 199–206.

Katsu N, Yamada K, Nakamichi M (2014). Development in the usage and comprehension of greeting calls in a free-ranging group of Japanese macaques (Macaca fuscata). Ethology 120, 1024–1034. doi: 10.1111/eth.12275

Koda H (2004). Flexibility and context-sensitivity during the vocal exchange of coo calls in wild Japanese macaques (Macaca fuscata yakui). Behaviour 141, 1279–1296. doi: 10.1163/1568539042729685

Koda H, Basile M, Olivier M, Remeuf K, Nagumo S, Blois-Heulin C, Lemasson A (2013a). Validation of an auditory sensory reinforcement paradigm: Campbell’s monkeys (Cercopithecus campbelli) do not prefer consonant over dissonant sounds. Journal of Comparative Psychology 127, 265–271. doi: 10.1037/a0031237

Koda H, Lemasson A, Oyakawa C, Rizaldi, Joko P, Masataka N (2013b). Possible role of mother-daughter vocal interactions on the development of species-specific song in gibbons. PLoS ONE 8, e71432. doi: 10.1371/journal.pone.0071432

Koda H, Nishimura T, Tokuda IT, Oyakawa C, Nihonmatsu T, Masataka N (2012). Soprano singing in gibbons. American Journal of Physical Anthropology 149, 347–355. doi: 10.1002/ajpa.22124

Koda H, Oyakawa C, Kato A, Masataka N (2007). Experimental evidence for the volitional control of vocal production in an immature gibbon. Behaviour 144, 681–692. doi: 10.1163/156853907781347817

Le Prell CG, Moody DB (2000). Factors influencing the salience of temporal cues in the discrimination of synthetic Japanese monkey (Macaca fuscata) coo calls. Animal Behavior Processes 26, 261–273. doi: 10.1037/0097-7403.26.3.261

Le Prell CG, Hauser MD, Moody DB (2002). Discrete or graded variation within rhesus monkey screams? Psychophysical experiments on classification. Animal Behaviour 63, 47–62. doi: 10.1006/anbe.2001.1888

Lemasson A (2011). What can forest guenons ‘tell’ us about the origin of language? In Primate Communication and Human Language: Vocalisation, Gestures, Imitation and Deixis in Humans and Non-Humans, Vilain A, Schwartz J-L, Abry C, Vauclair J (eds). Amsterdam: John Benjamins. pp. 39–70.

Lemasson A, Hausberger M (2004). Patterns of vocal sharing and social dynamics in a captive group of Campbell’s monkeys (Cercopithecus campbelli campbelli). Journal of Comparative Psychology 118, 347–359. doi: 10.1037/0735-7036.118.3.347

Lemasson A, Hausberger M (2011). Acoustic variability and social significance of calls in female Campbell’s monkeys (Cercopithecus campbelli campbelli). The Journal of the Acoustical Society of America 129, 3341–3352. doi: 10.1121/1.3569704

Lemasson A, Gandon E, Hausberger M (2010a). Attention to elders’ voice in non-human primates. Biology Letters 6, 325–328. doi: 10.1098/rsbl.2009.0875

Lemasson A, Glas L, Barbu S, Lacroix A, Guilloux M, Remeuf K, Koda H (2011a). Youngsters do not pay attention to conversational rules: Is this so for nonhuman primates? Scientific Reports 1, 22. doi: 10.1038/srep00022

Lemasson A, Guilloux M, Rizaldi, Barbu S, Lacroix A, Koda H (2013a). Age- and sex-dependent contact call usage in Japanese macaques. Primates 54, 283–291. doi: 10.1007/s10329-013-0347-5

Lemasson A, Hausberger M, Zuberbühler K (2005). Socially meaningful vocal plasticity in adult Campbell’s monkeys. Journal of Comparative Psychology 119, 220–229. doi: 10.1037/0735-7036.119.2.220

Lemasson A, Koda H, Kato A, Oyakawa C, Blois-Heulin C, Masataka N (2010b). Influence of sound specificity and familiarity on Japanese macaques’ (Macaca fuscata) auditory laterality. Behavioural Brain Research 208, 286–289. doi: 10.1016/j.bbr.2009.12.008

Lemasson A, Ouattara K, Bouchet H, Zuberbühler K (2010c). Speed of call delivery is related to context and caller identity in Campbell’s monkey males. Naturwissenschaften 97, 1–5. doi: 10.1007/s00114-010-0715-6

Lemasson A, Ouattara K, Petit E, Zuberbühler K (2011b). Social learning of vocal structure in a nonhuman primate? BMC Evolutionary Biology 11, 362. doi: 10.1186/1471-2148-11-362

Lemasson A, Ouattara K, Zuberbühler K (2013b). Exploring the gaps between primate calls and human language. In The Evolutionary Emergence of Language: Evidence and Inference, Botha R, Everaert M (eds). Utrecht: Oxford University Press. pp. 181–203.

Lemasson A, Palombit RA, Jubin R (2008). Friendships between males and lactating females in a free-ranging group of olive baboons (Papio hamadryas anubis): Evidence from playback experiments. Behavioral Ecology and Sociobiology 62, 1027–1035. doi: 10.1007/s00265-007-0530-z

Lemasson A, Remeuf K, Rossard A, Zimmermann E (2012). Cross-taxa similarities in affect-induced changes of vocal behavior and voice in arboreal monkeys. PLoS ONE 7, e45106. doi: 10.1371/journal.pone.0045106

Masataka N (1983). Categorical responses to natural and synthesized alarm calls in Goeldi’s monkey (Callimico goeldii). Primates 24, 40–51. doi: 10.1007/BF02381452

Masataka N (1985). Development of vocal recognition of mothers in infant japanese macaques. Developmental Psychobiology 18, 107–114. doi: 10.1002/dev.420180203

Masataka N (1989). Motivational referents of contact calls in Japanese monkeys. Ethology 80, 265–273. doi: 10.1111/j.1439-0310.1989.tb00745.x

Masataka N (1992). Early ontogeny of vocal behavior of Japanese infants in response to maternal speech. Child Development 63, 1177–1185. doi: 10.1111/j.1467-8624.1992.tb01687.x

Masataka N (1993). Effects of contingent and noncontingent maternal stimulation on the vocal behaviour of three- to four-month-old Japanese infants. Journal of Child Language 20, 303–312. doi: 10.1017/S0305000900008291

Masataka N (2003). The onset of language. Cambridge, UK: Cambridge University Press.

Masataka N (2007). Music, evolution and language. Developmental Science 10, 35–39. doi: 10.1111/j.1467-7687.2007.00561.x

Masataka N (2008). The origins of language. Unraveling evolutionary forces. Tokyo: Springer.

Masataka N (2009). The origins of language and the evolution of music: A comparative perspective. Physics of Life Reviews 6, 11–22. doi: 10.1016/j.plrev.2008.08.003

Masataka N, Symmes D (1986). Effect of separation distance on isolation call structure in squirrel monkeys (Saimiri sciureus). American Journal of Primatology 10, 271–278. doi: 10.1002/ajp.1350100307

McDermott J, Hauser M (2004). Are consonant intervals music to their ears? Spontaneous acoustic preferences in a nonhuman primate. Cognition 94, B11–B21. doi: 10.1016/j.cognition.2004.04.004

Mitani JC, Brandt KL (1994). Social factors influence the acoustic variability in the long-distance calls of male chimpanzees. Ethology 96, 233–252. doi: 10.1111/j.1439-0310.1994.tb01012.x

Nakamichi M, Yamada K (2010). Lifetime social development in female Japanese macaques. In The Japanese Macaques, Nakagawa N, Nakamichi M, Sugiura H (eds). Tokyo: Springer. pp. 241–270.

Ouattara K, Lemasson A, Zuberbühler K (2009a). Campbell’s monkeys concatenate vocalizations into context-specific call sequences. Proceedings of the National Academy of Sciences 106, 22026–22031. doi: 10.1073/pnas.0908118106

Ouattara K, Lemasson A, Zuberbühler K (2009b). Campbell’s monkeys use affixation to alter call meaning. PLoS ONE 4, e7808. doi: 10.1371/journal.pone.0007808

Oyakawa C, Koda H, Sugiura H (2007). Acoustic features contributing to the individuality of wild agile gibbon (Hylobates agilis agilis) songs. American Journal of Primatology 69, 777–790. doi: 10.1002/ajp.20390

Pfefferle D, Ruiz-Lambides AV, Widdig A (2014). Female rhesus macaques discriminate unfamiliar paternal sisters in playback experiments: Support for acoustic phenotype matching. Proceedings of the Royal Society of London B 281, 20131628. doi: 10.1098/rspb.2013.1628

Rendall D, Rodman PS, Emond RE (1996). Vocal recognition of individuals and kin in free-ranging rhesus monkeys. Animal Behaviour 51, 1007–1015. doi: 10.1006/anbe.1996.0103

Roush RS, Snowdon CT (2001). Food transfer and development of feeding behavior and food-associated vocalizations in cotton-top tamarins. Ethology 107, 415–429. doi: 10.1046/j.1439-0310.2001.00670.x

Sanefuji W, Ohgami H, Hashiya K (2007). Development of preference for baby faces across species in humans (Homo sapiens). Journal of Ethology 25, 249–254. doi: 10.1007/s10164-006-0018-8

Sato A, Koda H, Lemasson A, Nagumo S, Masataka N (2012). Visual recognition of age class and preference for infantile features: Implications for species-specific vs universal cognitive traits in primates. PLoS ONE 7, e38387. doi: 10.1371/journal.pone.0038387

Schlenker P, Chemla E, Arnold K, Lemasson A, Ouattara K, Keenan S, Stephan C, Ryder R, Zuberbühler K (2014). Monkey semantics: Two ‘dialects’ of Campbell’s monkey alarm calls. Linguistics and Philosophy 37, 439–501. doi: 10.1007/s10988-014-9155-7

Seyfarth RM, Cheney DL. (1997). Some general features of vocal development in nonhuman primates. In Social Influences on Vocal Development, Snowdon CT, Hausberger M (eds). Cambridge, UK: Cambridge University Press. pp. 249–273.

Shizawa Y, Nakamichi M, Hinobayashi T, Minami T (2005). Playback experiment to test maternal responses of Japanese macaques (Macaca fuscata) to their own infant’s call when the infants were four to six months old. Behavioural Processes 68, 41–46. doi: 10.1016/j.beproc.2004.10.002

Snowdon CT (1997). Affiliative processes and vocal development. Annals of the New York Academy of Sciences 807, 340–351. doi: 10.1111/j.1749-6632.1997.tb51931.x

Snowdon CT (2009). Plasticity of communication in nonhuman primates. In Advances in the Study of Behavior, Volume 40, Naguib M, Clayton NS, Zuberbühler K, Janik VM (eds). San Diego: Elsevier Academic Press. pp. 239–276.

Snowdon CT, Elowson AM (2001). ‘Babbling’in pygmy marmosets: Development after infancy. Behaviour 138, 1235–1248. doi: 10.1163/15685390152822193

Sugimoto T, Kobayashi H, Nobuyoshi N, Kiriyama Y, Takeshita H, Nakamura T, Hashiya K (2010). Preference for consonant music over dissonant music by an infant chimpanzee. Primates 51, 7–12. doi: 10.1007/s10329-009-0160-3

Sugiura H. (1998). Matching of acoustic features during the vocal exchange of coo calls by Japanese macaques. Animal Behaviour 55, 673–687. doi: 10.1006/anbe.1997.0602

Sugiura H, Masataka N (1995). Temporal and acoustic flexibility in vocal exchanges of coo calls in Japanese macaques (Macaca fuscata). In Current Topics in Primate Vocal Communication, Zimmermann E, Newman JD, Jürgens U (eds). New-York: Plenum Press. pp. 121–140.

Sugiura H, Tanaka T, Masataka N (2006). Sound transmission in the habitats of Japanese macaques and its possible effect on population differences in coo calls. Behaviour 143, 993–1012. doi: 10.1163/156853906778623617

Suzuki S, Hill DA, Sprague DS (1998). Intertroop transfer and dominance rank structure of nonnatal male Japanese macaques in Yakushima, Japan. International Journal of Primatology 19, 703–722. doi: 10.1023/A:1020329010009

Takahashi DY, Fenley AR, Teramoto Y, Narayanan DZ, Borjon JI, Holmes P, Ghazanfar AA (2015). The developmental dynamics of marmoset monkey vocal production. Science 349, 734–738. doi: 10.1126/science.aab1058

Takahashi DY, Narayanan DZ, Ghazanfar AA (2013). Coupled oscillator dynamics of vocal turn-taking in monkeys. Current Biology 23, 2162–2168. doi: 10.1016/j.cub.2013.09.005

Tanaka T, Sugiura H, Masataka N (2006). Cross-sectional and longitudinal studies of the development of group differences in acoustic features of coo calls in two groups of Japanese macaques. Ethology 112, 7–21. doi: 10.1111/j.1439-0310.2006.01103.x

Zentner MR, Kagan J (1998). Infants’ perception of consonance and dissonance in music. Infant Behavior and Development 21, 483–492. doi: 10.1016/S0163-6383(98)90021-2

Zuberbühler K (2000). Interspecies semantic communication in two forest primates. Proceedings of the Royal Society of London B 267, 713–718. doi: 10.1098/rspb.2000.1061

Zuberbühler K, Lemasson A (2013). Primate communication: Meaning from strings of calls. In Language and Recursion, Lowenthal F, Lefebvre L (eds). New-York: Springer. pp. 115–125.

Zuberbühler K, Ouattara K, Bitty A, Lemasson A, Noë R (2009). The primate roots of human language. In Becoming Eloquent: Advances in the Emergence of Language, Human Cognition, and Modern Cultures, d’Errico F, Hombert J-M (eds). Amsterdam: John Benjamins. pp. 235–264.

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Hélène Bouchet, Hiroki Koda, Nobuo Masataka et Alban Lemasson, « Vocal flexibility in nonhuman primates and the origins of human language », Revue de primatologie [En ligne], 7 | 2016, mis en ligne le 19 décembre 2016, consulté le 21 février 2017. URL : http://primatologie.revues.org/2637 ; DOI : 10.4000/primatologie.2637

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Auteurs

Hélène Bouchet

Université de Lyon – Université Jean Monnet Saint-Etienne, UMR 9197 Neuro-PSI / ENES – CNRS, Saint-Etienne, France.
Author for correspondence : helene.bouchet@yahoo.fr

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Hiroki Koda

University of Kyoto, Primate Research Institute, Cognition and Learning Section, Japan.
Email: koda.hiroki.7a@kyoto-u.ac.jp

Nobuo Masataka

University of Kyoto, Primate Research Institute, Cognition and Learning Section, Japan.
Email: masataka.nobuo.7r@kyoto-u.ac.jp

Alban Lemasson

Université de Rennes 1, UMR 6552 EthoS – CNRS, Station Biologique de Paimpont, Rennes, France.
Email : alban.lemasson@univ-rennes1.fr

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