A convergent interaction engine: vocal communication among marmoset monkeys.

To understand the primate origins of the human interaction engine, it is worthwhile to focus not only on great apes but also on callitrichid monkeys (marmosets and tamarins). Like humans, but unlike great apes, callitrichids are cooperative breeders, and thus habitually engage in coordinated joint actions, for instance when an infant is handed over from one group member to another. We first explore the hypothesis that these habitual cooperative interactions, the marmoset interactional ethology, are supported by the same key elements as found in the human interaction engine: mutual gaze (during joint action), turn-taking, volubility, as well as group-wide prosociality and trust. Marmosets show clear evidence of these features. We next examine the prediction that, if such an interaction engine can indeed give rise to more flexible communication, callitrichids may also possess elaborate communicative skills. A review of marmoset vocal communication confirms unusual abilities in these small primates: high volubility and large vocal repertoires, vocal learning and babbling in immatures, and voluntary usage and control. We end by discussing how the adoption of cooperative breeding during human evolution may have catalysed language evolution by adding these convergent consequences to the great ape-like cognitive system of our hominin ancestors. This article is part of the theme issue 'Revisiting the human 'interaction engine': comparative approaches to social action coordination'.

Do marmosets understand others' conversations? A thermography approach.

What information animals derive from eavesdropping on interactions between conspecifics, and whether they assign value to it, is difficult to assess because overt behavioral reactions are often lacking. An inside perspective of how observers perceive and process such interactions is thus paramount. Here, we investigate what happens in the mind of marmoset monkeys when they hear playbacks of positive or negative third-party vocal interactions, by combining thermography to assess physiological reactions and behavioral preference measures. The physiological reactions show that playbacks were perceived and processed holistically as interactions rather than as the sum of the separate elements. Subsequently, the animals preferred those individuals who had been simulated to engage in positive, cooperative vocal interactions during the playbacks. By using thermography to disentangle the mechanics of marmoset sociality, we thus find that marmosets eavesdrop on and socially evaluate vocal exchanges and use this information to distinguish between cooperative and noncooperative conspecifics.

The use of infrared thermography to investigate emotions in common marmosets.

Measuring body surface temperature changes with infrared thermography has recently been put forward as a non-invasive alternative measure of physiological correlates of emotional reactions. In particular, the nasal region seems to be highly sensitive to emotional reactions. Several studies suggest that nasal temperature is negatively correlated with the level of arousal in humans and other primates, but some studies provide inconsistent results. Our goal was to establish the use of infrared thermography to quantify emotional reactions in common marmosets (Callithrix jacchus), with a focus on the nasal region. To do so we exposed 17 common marmosets to a set of positive, negative and control stimuli (positive: preferred food, playback of food calls; negative: playback of aggressive vocalizations, teasing; control: no stimulus). We compared nasal temperature before and after the stimuli and expected that highly aroused emotional states would lead to a drop in nasal temperature. To validate the thermography measure, we coded piloerection of the tail as an independent measure of arousal and expected a negative correlation between the two measures. Finally, we coded physical activity to exclude its potential confounding impact on nasal temperature. Our results show that all predictions were met: the animals showed a strong decrease in nasal temperature after the presentation of negative arousing stimuli (teasing, playback of aggressive vocalizations). Furthermore, these changes in nasal temperature were correlated with piloerection of the tail and could not be explained by changes in physical activity. In the positive and the control conditions, we found systematic sex differences: in males, the preferred food, the playbacks of food calls, as well as the control stimulus led to an increase in nasal temperature, whereas in females the temperature remained stable (preferred food, control) or decreased (playback of food calls). Based on naturalistic observations that document higher food motivation and competition among female marmosets, as well as stronger reactions to separation from group members in male marmosets, these sex differences corroborate a negative correlation between arousal and nasal temperature. Overall, our results support that measuring nasal temperature by infrared thermography is a promising method to quantify emotional arousal in common marmosets in a fully non-invasive and highly objective way.

Reverse audience effects on helping in cooperatively breeding marmoset monkeys.

Cooperatively breeding common marmosets show substantial variation in the amount of help they provide. Pay-to-stay and social prestige models of helping attribute this variation to audience effects, i.e. that individuals help more if group members can witness their interactions with immatures, whereas models of kin selection, group augmentation or those stressing the need to gain parenting experience do not predict any audience effects. We quantified the readiness of adult marmosets to share food in the presence or absence of other group members. Contrary to both predictions, we found a reverse audience effect on food-sharing behaviour: marmosets would systematically share more food with immatures when no audience was present. Thus, helping in common marmosets, at least in related family groups, does not support the pay-to-stay or the social prestige model, and helpers do not take advantage of the opportunity to engage in reputation management. Rather, the results appear to reflect a genuine concern for the immatures' well-being, which seems particularly strong when solely responsible for the immatures.