The Evolution of Food Calls: Vocal Behaviour of Sooty Mangabeys in the Presence of Food.

The two main theories of food-associated calls in animals propose functions either in cooperative recruitment or competitive spacing. However, not all social animals produce food calls and it is largely unclear under what circumstances this call type evolves. Sooty mangabeys (Cercocebus atys) do not have food calls, but they frequently produce grunts during foraging, their most common vocalisation. We found that grunt rates were significantly higher when subjects were foraging in the group's periphery and with small audiences, in line with the cooperative recruitment hypothesis. In a subsequent field experiment we presented highly desired food items and found that discovering individuals called, unless harassed by competitors, but that the calls never attracted others, confirming that the grunts do not convey any information referential to food. Our data thus suggest that the evolution of cooperative food calling is a two-step process, starting with increased motivation to vocalise in the feeding context, followed by the evolution of acoustic variants derived from context-general contact calls. This evolutionary transition may only occur in species that feed on clumped, high-quality resources where social feeding is competitive, a condition not met in sooty mangabeys.

An Audience Effect in Sooty Mangabey Alarm Calling.

How does intentional communication evolve? Comparative studies can shed light on the evolutionary history of this relevant feature of human language and its distribution before modern humans. The current animal literature on intentional signaling consists mostly of ape gestural studies with evidence of subjects persisting and elaborating with sometimes arbitrary signals toward a desired outcome. Although vocalizations can also have such imperative qualities, they are typically produced in a functionally fixed manner, as if evolved for a specific purpose. Yet, intentionality can sometimes transpire even in functionally fixed calls, for example, if production is adapted to audience composition. In this study, we carried out field experiments to test whether free-ranging sooty mangabeys adjusted snake alarm call production to their audiences. We found a positive relation between alarm call production and naïve individuals arriving, suggesting that callers attempted to influence their behaviors relative to the snake. Subjects called more with smaller audiences, if they had not heard other calls before, and if socially important individuals were in the area. We concluded that sooty mangabeys alarm call production can be explained as an active attempt to refer to an external event, rather than a mere readout of an internal state.

Triiodothyronine and cortisol levels in the face of energetic challenges from reproduction, thermoregulation and food intake in female macaques.

Energy availability drives an individual's fitness and can be affected by diverse energetic challenges. The assessment of hormones involved in metabolic activity and energy mobilization provides a gateway to the study of physiological adaptations in response to changes in energy availability. Here, we investigated immunoreactive urinary total triiodothyronine (uTT3, thyroid hormone secreted through the hypothalamus-pituitary-thyroid axis and regulating the basal metabolic rate) alongside glucocorticoids (i.e. urinary cortisol, uCort, secreted through the hypothalamus-pituitary-adrenal axis and mediating energy mobilization) in wild female Assamese macaques (Macaca assamensis). Combining more than 2900; of behavioral data from 42 adult females with physiological data from 382 urine samples, we evaluated both uTT3 and uCort in relation to potential energetic challenges encountered by a female, namely fluctuations in energy intake, travel distance, reproductive state and minimum ambient temperature. As predicted, levels of both hormones changed in response to variation in energy intake with a tendency toward a positive effect on uTT3 and a significant negative effect on uCort levels. Unexpectedly, neither hormone was influenced by variation in travel distance. Reproductive state affected both hormones with higher levels of uTT3 and uCort in the second half of gestation. Finally, a decrease of minimum temperature triggered an increase in uCort but unexpectedly not in uTT3. Collectively, our results highlight the respective contribution of two endocrine axes when facing energetic challenges and the underlying metabolic strategies to cope with them. Overall, assessing thyroid hormones together with glucocorticoids provides an integrative picture in the evaluation of an individual's energy status.

Social bonding drives vocal exchanges in Bonobos.

The origin of human speech is still a hotly debated topic in science. Evidence of socially-guided acoustic flexibility and proto-conversational rules has been found in several monkey species, but is lacking in social and cooperative great apes. Here we investigated spontaneous vocal interactions within a peaceful context in captive bonobos to reveal that vocal interactions obey temporally and social rules. Dyadic vocal interactions were characterized by call overlap avoidance and short inter-call intervals. Bonobos preferentially responded to conspecifics with whom they maintained close bonds. We also found that vocal sharing rate (production rate of shared acoustic variants within each given dyad) was mostly explained by the age difference of callers, as other individual characteristics (sex, kinship) and social parameters (affinity in spatial proximity and in vocal interactions) were not. Our results show that great apes spontaneously display primitive conversation rules guided by social bonds. The demonstration that such coordinated vocal interactions are shared between monkeys, apes and humans fills a significant gap in our knowledge of vocal communication within the primate phylogeny and highlights the universal feature of social influence in vocal interactions.