Of the importance to reconsider individual variability in infant studies: Family traits do impact turn-taking perception in 6-month-olds.

Turn-taking is a universal pattern of human conversations characterized by a fast exchange of turns between speakers and an avoidance of overlaps. Language is embedded in this conversational skill acquired well before it during infancy, through everyday interactions with caregivers. The earliness of this skill and its link with language allows us to test whether social environment shapes early language development. We therefore study turn-taking perception of 6-month-old infants by measuring their gazes during video presentation of three different conversational situations where the turn is explicitly given, normally taken or taken with an overlap. We studied 51 infants to cover several family and infant characteristics: infants' sex, presence of siblings, and family socioeconomic status (SES). We found that infants looked more at the second speaker when she overlapped the first speaker than in the other situations, but not all infants were equally sensitive. Indeed, infants from high-SES families reacted differently to the three situations, while infants from the two lower SES categories did not. Also, only singletons reacted differently by looking more at the second speaker after the overlapping and turn-giving situations, and not after the turn-taking situation. Our results emphasize the importance of early social experiences on language development.

Social factors drive vocal exchanges in red-capped mangabeys (Cercocebus torquatus).

Of all the calls made by non-human primates, the function of short-distance contact calls has largely remained to be determined. These calls are the most frequent in the repertoire and are most often exchanged between individuals in a non-random way. To our knowledge, no study has ever examined how vocal exchanges are structured in red-capped mangabeys (Cercocebus torquatus), a semi-terrestrial monkey living in the African forest with a complex semi-tolerant/semi-despotic social system. Our goal was to assess the organization of contact call exchanges in this species and their relationship with individual and social factors such as age, affinity, and hierarchy. Therefore, we observed several captive groups of red-capped mangabeys and collected data on vocal behavior, as well as grooming, agonistic behavior, and spatial proximity. We defined a vocal exchange in this species as a series of contact calls made by two or more individuals within a maximum inter-caller interval of 2 s. At the individual level, the higher the individual's hierarchical rank, the less they initiated exchanges. Furthermore, the most socially integrated individuals had a longer average response time than the less integrated ones. At the dyadic level, preferred exchange partners were individuals often observed near one other or individuals most distant in age. Also, the further apart two individuals were in the dominance hierarchy, the shorter the response time. Our results support both the social bonding hypothesis and a modulating key role of the dominance hierarchy on the social use of contact calls, which is in line with the social style of this species.

Study of repertoire use reveals unexpected context-dependent vocalizations in bottlenose dolphins (Tursiops truncatus).

Dolphins are known for their complex vocal communication, not least because of their capacity for acoustic plasticity. Paradoxically, we know little about their capacity for flexible vocal use. The difficulty in describing the behaviours performed underwater while vocalizing makes it difficult to analyse the contexts of emissions. Dolphins' main vocal categories are typically considered to be used for scanning the environment (clicks), agonistic encounters (burst pulses) and socio-affiliative interactions (whistles). Dolphins can also combine these categories in mixed vocal emissions, whose use remains unclear. To better understand how vocalizations are used, we simultaneously recorded vocal production and the associated behaviours by conducting underwater observations (N = 479 events) on a group of 7 bottlenose dolphins under human care. Our results showed a non-random association between vocal categories and behavioural contexts. Precisely, clicks were preferentially emitted during affiliative interactions and not during other social/solitary contexts, supporting a possible complementary communicative function. Burst pulses were associated to high arousal contexts (agonistic and social play), pinpointing on their use as an "emotively charged" signal. Whistles were related to solitary swimming and not preferentially produced in any social context. This questions whistles' functions and supports their potential role as a distant contact call. Finally, mixed vocalizations were especially found associated with sexual (bust pulse-whistle-click), solitary play (burst pulse-whistle) and affiliative (click-whistle) behaviours. Depending on the case, their emission seems to confirm, modify or refine the functions of their simple counterparts. These results open up new avenues of research into the contextual use of dolphin acoustic signals.

Intentional gestural communication amongst red-capped mangabeys (Cercocebus torquatus).

Apes, human's closest living relatives, are renowned for their intentional and highly flexible use of gestural communication. In stark contrast, evidence for flexible and intentional gestural communication in monkeys is scarce. Here, we investigated the intentionality and flexibility of spontaneous gesture use in red-capped mangabeys (Cercocebus torquatus). We applied established methods used in ape gesture research to analyse whether the body acts produced by a total of 17 individuals living in three different groups in captivity qualified as intentionally produced gesture instances. Results showed that signallers showed all hallmarks of intentionality during the production of 20 out of a total of 21 different types of body acts. These were only produced in the presence of other individuals, and the monkeys showed audience checking, sensitivity to the attentional states of recipients, adjustment of signal modality, and response waiting relative to their production. Moreover, in case of communication failure, the monkeys showed goal persistence, and regarding the production contexts they showed some signs of means-ends dissociation. Therefore, these monkeys are capable of flexible and intentional gestural communication and use this to communicate with conspecifics. Our results corroborate recent findings showing that intentional gestural communication was already present in the monkey lineage of catarrhine primates. We discuss our results in light of the comparative approach towards human language evolution and highlight our finding that these monkeys also showed flexible and intentional use of four 'free' manual gesture types.

Early life experience and sex influence acoustic repertoire use in wild-born, but hand-reared, captive cheetahs (Acinonyx jubatus).

Early deprivation of adult influence is known to have long-lasting effects on social abilities, notably communication skills, as adults play a key role in guiding and regulating the behavior of youngsters, including acoustic repertoire use in species in which vocal production is not learned. Cheetahs grow up alongside their mother for 18 months, thus maternal influences on the development of social skills are likely to be crucial. Here, we investigated the impact of early maternal deprivation on vocal production and use in 12 wild-born cheetahs, rescued and subsequently hand-reared either at an early (less than 2 months) or a later stage of development. We could distinguish 16 sound types, produced mostly singly but sometimes in repeated or multitype sound sequences. The repertoire of these cheetahs did not differ fundamentally from that described in other studies on adult cheetahs, but statistical analyses revealed a concurrent effect of both early experience and sex on repertoire use. More specifically, early-reared males were characterized by a high proportion of Purr, Meow, and Stutter; early-reared females Mew, Growl, Hoot, Sneeze, and Hiss; late-reared males Meow, Mew, Growl, and Howl; and late-reared females mostly Meow. Our study demonstrates therefore the long-term effects of maternal deprivation on communication skills in a limited-vocal learner and its differential effect according to sex, in line with known social differences and potential differential maternal investment. More generally, it emphasizes the critical importance to consider the past history of the subjects (e.g., captive/wild-born, mother/hand-reared, early/late-mother-deprived, etc.) when studying social behavior, notably acoustic communication.

Socially mediated overlap in vocal interactions between free-ranging black howler monkeys.

"Conversation rules" such as overlap avoidance and coordinated overlap have been reported in nonhuman animals, and seem to be adaptive responses to the requirements of social life. Some species display both patterns in an apparently flexible way, but the social factors mediating their respective usage remain poorly documented. We investigated the potential social factors guiding the usage of these temporal rules during collective howling in six free-ranging groups of black howler monkeys (Alouatta pigra). First, we found that adult males' vocalizations rarely overlap those of other callers while most adult females' calls overlap other members' calls, especially that of other females. Second, whereas some call types (notably affiliative calls) are typically emitted without overlap, roars (agonistic loud calls) overlap more frequently. Third, coordinated overlap is more frequent during intergroup competition. Our findings support the hypothesis that overlap avoidance and coordinated overlap are two different (here sex-related) vocal alliance social behaviors, at least for some nonhuman primates. More comparative investigations are now needed to explore further their evolutionary trajectories in this lineage.

When perceptual laterality vanishes with curiosity: A study in dolphins and starlings.

Sensory laterality is influenced by the individual's attentional state. There are variations in the way different individuals of a same species attend to stimuli. When confronted to novelty, some individuals are more explorative than others. Curiosity is composed of sensation and knowledge seeking in humans. In the present study, we hypothesized that more curious animals, i.e., showing more sensory exploration would be less lateralized than quietly attentive individuals, performing instead more gazing behaviours. In order to test this hypothesis and its possible generality, we performed two studies using two animal models (dolphins and starlings) and two modalities (visual and auditory) of presentation of species-specific and non-species-specific stimuli. Both dolphins and starlings presented more gazes for the species-specific stimuli and more exploratory components for the non-species-specific stimuli. Moreover, in both cases, the non-species-specific stimuli involved more lateralized responses whereas there was no or less clear laterality for the species-specific stimuli. The more exploratory dolphins and starlings also showed a decreased laterality: the more "curious" individuals showed no laterality. Further studies are needed on characterization of curiosity in relation to attention structure. The present study suggests that individual variations in sensory laterality may help disentangle the subtle differences between curiosity, attention and boldness.

Tolerant and intolerant macaques show different levels of structural complexity in their vocal communication.

We tested the social complexity hypothesis which posits that animals living in complex social environments should use complex communication systems. We focused on two components of vocal complexity: diversity (number of categories of calls) and flexibility (degree of gradation between categories of calls). We compared the acoustic structure of vocal signals in groups of macaques belonging to four species with varying levels of uncertainty (i.e. complexity) in social tolerance (the higher the degree of tolerance, the higher the degree of uncertainty): two intolerant species, Japanese and rhesus macaques, and two tolerant species, Tonkean and crested macaques. We recorded the vocalizations emitted by adult females in affiliative, agonistic and neutral contexts. We analysed several acoustic variables: call duration, entropy, time and frequency energy quantiles. The results showed that tolerant macaques displayed higher levels of vocal diversity and flexibility than intolerant macaques in situations with a greater number of options and consequences, i.e. in agonistic and affiliative contexts. We found no significant differences between tolerant and intolerant macaques in the neutral context where individuals are not directly involved in social interaction. This shows that species experiencing more uncertain social interactions displayed greater vocal diversity and flexibility, which supports the social complexity hypothesis.

A novel, short and easy-to-perform method to evaluate newborns' social olfactory preferences.

Humans' early olfactory perception has been studied mainly within the framework of mother-offspring interactions and only a few studies have focused on newborns' abilities to discriminate body odors per se. The aim of this study was to develop a method to evaluate olfactory social preferences of infants at term-equivalent age. Twenty dyads of infants (10 born preterm and 10 born at term) at term-equivalent age and their mothers were included. We analyzed the behavioral reactions of infants to their mother's upper-chest odor (that bears social, non-food related information). The two impregnated gauzes and a control gauze were presented to the infants for 10 s each, in a random order. We compared two durations of gauze impregnation: 30 min and 12 h. This study reveals that mothers' upper chest emits sufficient olfactory information to induce reactions in infants born full-term or born preterm and that a short impregnation is preferable to evaluate their perception of body odors, notably for those born preterm.

Maternal Care in Free-Ranging Arboreal Grey-Cheeked Mangabeys (Lophocebus albigena johnstoni) in Kibale National Park, Uganda.

Maternal styles have been intensively studied in a variety of terrestrial species of primates, but far less in arboreal species. However, to have a balanced view of the evolution of maternal care, it is necessary to investigate this behaviour in the context of habitat. Here, we investigate whether the mother's parity, age and dominance rank, as well as the infant's age and sex, influence maternal care and mother-infant proximity in arboreal grey-cheeked mangabeys (Lophocebus albigena). We observed 13 mother-infant dyads in four free-ranging groups for 6 months. Our main finding is that maternal care is a dynamic process affected by a mix of mothers' and infants' characteristics. We found that first-time mothers spent more time watching their infants than multiparous mothers, who carried, groomed and protected their infants more often. We also found that low-ranking mothers prevented their infants from leaving them more often than did high-ranking mothers. Moreover, mothers adjusted their care as infants became older. They groomed and protected female infants more than male infants, behaviours common in female-bonded species. Our study shows the ever-changing dynamics of maternal care related to infant age and highlights the role of the mother's parity and rank in this process.

Snort acoustic structure codes for positive emotions in horses.

While the vocal coding of human and animal internal states has been widely studied, the possible acoustic expression of "positive" emotions remains poorly known. Recent studies suggest that snorts (non-vocal sounds produced by the air expiration through the nostrils) appear to be reliable indicators of positive internal states in several ungulate species. Here, we hypothesised in horses that the acoustic structure of the snort could vary with the subjects' current emotional state. Indeed, a preliminary sound analysis of snorts let us suggest structure variations related to the presence of pulsations. We recorded snorts from 20 horses living in a riding center. Auditory playbacks run with 20 humans first confirmed the existence of two snort subtypes, i.e. one pulsed and one non-pulsed. Observations were then conducted to compare the distribution of these two subtypes according to the location (stall/pasture) of the signaller as a contextual determinant of its internal state and to its ears' position as a reflection of its emotional state. We found that both subtypes were preferentially observed in positive contexts, but that pulsed snorts were even more associated with highly appreciated situations (in pasture and with ears forward). This study is a step further in the identification of indicators of positive emotions in horses and more generally in the understanding of the acoustic emotions' coding.

Decision-making under risk of gain in young children and mangabey monkeys.

In contrast to human adults, risk proneness in the gain domain is usually observed in both young children and non-human primates. It is currently unclear what mechanism might be underlying such economic preferences. We investigated decision-making under risk of gain in toddlers and monkeys. The choices of 2.5-year-old children and red-capped mangabeys (Cercocebus torquatus torquatus) were examined in a gambling task for food reward in which participants have to choose between two options, a secure option and a risky option. In contrast to monkeys, toddlers showed a strong preference for the risky option over the safe option. In order to test the hypothesis that risky choices in participants reflect inhibitory control difficulties, toddlers and mangabeys were presented in Experiment 2 with a situation analogous to that used in Experiment 1 except for the fact that the opaque cover under which was placed the secure option was replaced by a transparent cover. In this second experiment, toddlers continued to show a preference for the risky option over the safe option. In contrast, mangabeys showed a preference for the safe option over the risky option in Trial 1 but they shifted their economic preferences in Trial 2. We argue that decision-making strategies under risk of gain in both toddlers and mangabeys (a) do not reflect poor behavioral control and (b) are not reducible to perception-action couplings.

Factors of influence and social correlates of parturition in captive Campbell's monkeys: Case study and breeding data.

How nonhuman primates deal with birth, at the moment of delivery, and during the following days, remains poorly explored because of the unpredictability of this event, particularly for forest-dwelling arboreal species. Available studies highlight intra- and interspecific variation which suggest flexibility of the timing of delivery, of behavior associated with labor contractions and parturition, and the social context and ambient noise surrounding delivery. Here, we present the findings of a two-decade survey of reproduction in a population of captive Campbell's monkeys. Analysis of 34 births (with a female-biased sex ratio) showed that deliveries occurred systematically at night and more frequently during week-ends and in fall (September-November). This suggests the existence of both circadian and infradian biological rhythms. We present the first detailed description of a birth for this species and its short-term social consequences. In line with previous findings for other monkeys and apes, labor (estimated by unusual stretching postures) and parturition were rapid, and delivery occurred in a clear social and vocal context. During the following days, the new mother became the center of attention of for young (kin and non-kin) females and rose through the hierarchy. We discuss socio-ecological factors, notably captivity conditions and the high degree of tolerance in the species' social system, and confirm the existence of both "rigidity" and "flexibility" in the primates' adaptive reproductive strategies.

Vocal repertoire of free-ranging black howler monkeys' (Alouatta pigra): Call types, contexts, and sex-related contributions.

Alouatta species utter the most powerful primate vocalizations in the Neotropics and are well-known for their loud and long-lasting male howling bouts. However, the diversity of acoustic structures used in these howling bouts, as well as in non-howling contexts, and the relative contribution of the different group members to the entire vocal repertoire, needed to be explored further. This report provides the first detailed description of the vocal repertoire of black howler monkeys (Alouatta pigra), focusing on acoustic structures and contexts of emission of both loud and soft calls as well as on the contribution rate of males and females to the different call types. Three free-ranging social groups of black howler monkeys living in Palenque National Park, Mexico were monitored. We identified twelve acoustically discriminable call types, eight described previously and four described here for the first time. A few call types were systematically emitted either isolated or during howling bouts, but most of them could be heard in both calling contexts. Three call types were emitted only by females and two only by males. Adult males' call rates (for the seven shared call types) were higher than those of females but only when considering calls emitted within howling bouts. Our contextual analysis enabled us to divide call types into potential functional categories, according to their degree of contribution, to intra-group versus inter-group interactions and to neutral-positive versus negative situations. We then discussed how socio-ecological factors, notably sex differences in social behaviors, may explain the variability found in the vocal repertoire of this species and compared our findings with the literature on other primate species.

Vocal activities reflect the temporal distribution of bottlenose dolphin social and non-social activity in a zoological park.

Under natural conditions bottlenose dolphins (Tursiops truncatus) spend their time mostly feeding and then travelling, socializing, or resting. These activities are not randomly distributed, with feeding being higher in early morning and late afternoon. Social activities and vocal behavior seem to be very important in dolphin daily activity. This study aimed to describe the activity time-budget and its relation to vocal behavior for dolphins in a zoological park. We recorded behaviors and vocalizations of six dolphins over 2 months. All subjects performed more non-agonistic social interactions and play in the morning than in the afternoon. The different categories of vocalizations were distributed non-randomly throughout the day, with more chirps in the afternoon, when the animals were "less social." The most striking result was the strong correlation between activities and the categories of vocalizations produced. The results confirm the association between burst pulses and whistles with social activities, but also reveal that both are also associated with solitary play. More chirps were produced when dolphins were engaged in socio-sexual behaviors, emphasizing the need for further questioning about the function of this vocal category. This study reveals that: (i) in a group kept in zoological management, social activities are mostly present in the morning; and (ii) the acoustic signals produced by dolphins may give a reliable representation of their current activities. While more studies on the context of signal production are needed, our findings provide a useful tool for understanding free ranging dolphin behavior when they are not visible.

Call rates of mothers change with maternal experience and with infant characteristics in free-ranging gray-cheeked mangabeys.

Studies have shown that becoming a mother triggers important social changes within females, according to both social experience and infant characteristics, showing different maternal concerns. But how this impacts call usage has been far less studied. Based on 6 months of observations of five free-ranging groups of gray-cheeked mangabeys, we investigated variations in the production of three call types (contact, excitement, and alarm calls) in 29 females of different ages, dominance ranks, and infant rearing experiences: 15 females with infants of different ages and sexes, and 14 females without infants. We found that in females with infants-both maternal and infant characteristics influenced call production in a call type-dependent way. Females produced contact calls at a higher rate during the first month of infant age and after weaning when infants start to move away. Mothers of daughters produced more contact calls than mothers of sons. More excitement calls were recorded for first-time and young mothers and for females with young infants, while alarm call rates were not influenced by any of these factors. Increased mother-infant spatial separation enhanced only contact and excitement call rates. Finally, we found that females with infants vocalized much more than females without infants. Our results contribute to the current debate about the social factors responsible for the flexibility of call usage in nonhuman primates and open new lines for research on mothering behavior in forest-dwelling species. Am. J. Primatol. 78:983-991, 2016. © 2016 Wiley Periodicals, Inc.

Suffixation influences receivers' behaviour in non-human primates.

Compared to humans, non-human primates have very little control over their vocal production. Nonetheless, some primates produce various call combinations, which may partially offset their lack of acoustic flexibility. A relevant example is male Campbell's monkeys (Cercopithecus campbelli), which give one call type ('Krak') to leopards, while the suffixed version of the same call stem ('Krak-oo') is given to unspecific danger. To test whether recipients attend to this suffixation pattern, we carried out a playback experiment in which we broadcast naturally and artificially modified suffixed and unsuffixed 'Krak' calls of male Campbell's monkeys to 42 wild groups of Diana monkeys (Cercopithecus diana diana). The two species form mixed-species groups and respond to each other's vocalizations. We analysed the vocal response of male and female Diana monkeys and overall found significantly stronger vocal responses to unsuffixed (leopard) than suffixed (unspecific danger) calls. Although the acoustic structure of the 'Krak' stem of the calls has some additional effects, subject responses were mainly determined by the presence or the absence of the suffix. This study indicates that suffixation is an evolved function in primate communication in contexts where adaptive responses are particularly important.

Grooming-at-a-distance by exchanging calls in non-human primates.

The 'social bonding hypothesis' predicts that, in large social groups, functions of gestural grooming should be partially transferred to vocal interactions. Hence, vocal exchanges would have evolved in primates to play the role of grooming-at-a-distance in order to facilitate the maintenance of social cohesion. However, there are few empirical studies testing this hypothesis. To address this point, we compared the rate of contact call exchanges between females in two captive groups of Japanese macaques as a function of female age, dominance rank, genetic relatedness and social affinity measured by spatial proximity and grooming interactions. We found a significant positive relationship between the time spent on grooming by two females and the frequency with which they exchanged calls. Our results conform to the predictions of the social bonding hypothesis, i.e. vocal exchanges can be interpreted as grooming-at-a-distance.

Behavioural evidence of magnetoreception in dolphins: detection of experimental magnetic fields.

Magnetoreception, meaning the perception of magnetic fields, is supposed to play an important role for orientation/navigation in some terrestrial and aquatic species. Although some spatial observations of free-ranging cetaceans' migration routes and stranding sites led to the assumption that cetaceans may be sensitive to the geomagnetic field, experimental evidence is lacking. Here, we tested the spontaneous response of six captive bottlenose dolphins to the presentation of two magnetized and demagnetized controlled devices while they were swimming freely. Dolphins approached the device with shorter latency when it contained a strongly magnetized neodymium block compared to a control demagnetized block that was identical in form and density and therefore undistinguishable with echolocation. We conclude that dolphins are able to discriminate the two stimuli on the basis of their magnetic properties, a prerequisite for magnetoreception-based navigation.