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.

The influence of phylogeny, social style, and sociodemographic factors on macaque social network structure.

Among nonhuman primates, the evolutionary underpinnings of variation in social structure remain debated, with both ancestral relationships and adaptation to current conditions hypothesized to play determining roles. Here we assess whether interspecific variation in higher-order aspects of female macaque (genus: Macaca) dominance and grooming social structure show phylogenetic signals, that is, greater similarity among more closely-related species. We use a social network approach to describe higher-order characteristics of social structure, based on both direct interactions and secondary pathways that connect group members. We also ask whether network traits covary with each other, with species-typical social style grades, and/or with sociodemographic characteristics, specifically group size, sex-ratio, and current living condition (captive vs. free-living). We assembled 34-38 datasets of female-female dyadic aggression and allogrooming among captive and free-living macaques representing 10 species. We calculated dominance (transitivity, certainty), and grooming (centrality coefficient, Newman's modularity, clustering coefficient) network traits as aspects of social structure. Computations of K statistics and randomization tests on multiple phylogenies revealed moderate-strong phylogenetic signals in dominance traits, but moderate-weak signals in grooming traits. GLMMs showed that grooming traits did not covary with dominance traits and/or social style grade. Rather, modularity and clustering coefficient, but not centrality coefficient, were strongly predicted by group size and current living condition. Specifically, larger groups showed more modular networks with sparsely-connected clusters than smaller groups. Further, this effect was independent of variation in living condition, and/or sampling effort. In summary, our results reveal that female dominance networks were more phylogenetically conserved across macaque species than grooming networks, which were more labile to sociodemographic factors. Such findings narrow down the processes that influence interspecific variation in two core aspects of macaque social structure. Future directions should include using phylogeographic approaches, and addressing challenges in examining the effects of socioecological factors on primate social structure.

Comparing physical and social cognitive skills in macaque species with different degrees of social tolerance.

Contemporary evolutionary theories propose that living in groups drives the selection of enhanced cognitive skills to face competition and facilitate cooperation between individuals. Being able to coordinate both in space and time with others and make strategic decisions are essential skills for cooperating within groups. Social tolerance and an egalitarian social structure have been proposed as one specific driver of cooperation. Therefore, social tolerance is predicted to be associated with enhanced cognitive skills that underpin communication and coordination. Social tolerance should also be associated with enhanced inhibition, which is crucial for suppressing automatic responses and permitting delayed gratification in cooperative contexts. We tested the performance of four closely related non-human primate species (genus Macaca) characterized by different degrees of social tolerance on a large battery of cognitive tasks covering physical and social cognition, and on an inhibitory control task. All species performed at a comparable level on the physical cognition tasks but the more tolerant species outperformed the less tolerant species at a social cognition task relevant to cooperation and in the inhibitory control task. These findings support the hypothesis that social tolerance is associated with the evolution of sophisticated cognitive skills relevant for cooperative social living.

Lack of evidence that Tonkean macaques understand what others can hear.

By distinguishing the attentional cues of their mates, animals can learn what part of their environment is of potential interest. However, recognizing the attentional states of others through auditory perception appears to be difficult, since these states are generally not accompanied by ostensive signals liable to reveal them. In this context, one study found that rhesus macaques withhold their action when unobserved, then concluding that they know what others can hear. We replicated this study by testing 18 Tonkean macaques in an experimental setting where subjects had to choose between two boxes containing a food reward. One box made a noise when opened, and the other opened silently. An experimenter was present and could either have her back to subjects or be facing them. If subjects aimed to avoid attracting the experimenter's attention, they were expected to select the silent box while the experimenter's back was turned. Results showed that subjects did not discriminate between boxes, whatever the experimenter's position. We thus found no evidence that Tonkean macaques are able to take the auditory attentional states of a human into account. It is therefore premature to conclude that monkeys can establish a link between hearing and knowing.

Inferences about food location in three cercopithecine species: an insight into the socioecological cognition of primates.

Many animal species use a variety of cognitive strategies to locate food resources. One strategy is to make inferences by exclusion, i.e., perceiving the absence of reward as a cue that another location should be investigated. The use of such advanced cognitive strategies may be more prominent in species that are known to frequently solve social challenges, and inferential reasoning has mainly been investigated in social species such as corvids, dogs, dolphins and non-human primates. In this paper, we investigate how far social intricacy may explain the disparity of reasoning performances observed in three cercopithecine species that differ in the density of their social network and the diversity of their social partners. We used standard reasoning tasks, testing the volume concept and inference by exclusion using visual and auditory modalities. We showed that Old World monkeys can infer the location of invisible food by exclusion. In addition, Tonkean macaques and olive baboons had greater performances in most tasks compared to rhesus macaques. These responses are consistent with the social complexity displayed by these three species. We suggest that the cognitive strategies required to navigate through a demanding social world are involved in the understanding of the physical domain.

The function of greetings in male Tonkean macaques.

Males living in multi-male groups are both strong rivals and potential allies. In several primate species they regularly interact through ritualized exchanges known as greetings. We studied five captive groups of Tonkean macaques (Macaca tonkeana) to test five hypotheses regarding the social function of greetings. We found that greetings were mostly reciprocal interactions, and that they often involved physical contact and facial displays. Although they were mostly initiated by the higher-ranking individual in each dyad, subordinates could initiate approximately one-third of greetings, which indicates that greetings do not serve as a formal acknowledgement of dominance relationships. Although greeting frequencies were negatively correlated to the frequency of supplantations and conflicts, they were not significantly influenced by age and dominance status, showing that greetings are not used to appease partners or decrease tension between males. Males most frequently greeted partners with whom they spent more time in proximity and body contact, and this is consistent with the hypothesis that greetings play a role in reinforcing social relationships. Lastly, greetings increased in frequency between individuals involved in challenges for rank, lending support to the hypothesis that males assess the state of their social relationships through greetings.

Collective arousal when reuniting after temporary separation in Tonkean macaques.

Celebrations and bursts of communal joy can occur spontaneously in human communities based on mechanisms of emotional contagion. Some examples of similar collective excitement have been reported in animals when they reunite or anticipate rewards, but little is known about the processes and meaning of these multiple interactions. We experimentally studied such collective arousals in two captive groups of Tonkean macaques (Macaca tonkeana) within the context of reunions following the temporary separation of two subgroups. We compared the behaviors of individuals after separation periods of 2 and 48 h with a control period with no separation. This study showed that it is possible to reproducibly induce bursts of friendly interactions in which groupmates run around over a period of several minutes, embracing and grasping one another while displaying numerous affiliative vocalizations and facial expressions. The longer the period of separation, the higher and longer-lasting the rates of affiliative interactions were. Individuals affiliated more frequently with groupmates from a previously separated subgroup than with those having stayed in their own subgroup. Collective arousal was followed by a quieter period characterized by high rates of contact-sitting and social grooming. These results point at the role of collective arousals in social cohesion; they could resolve social tension and renew social relationships. We propose that the emotional state experienced by Tonkean macaques during such events represents a disposition similar to that giving rise to what we humans call "shared joy."

Measuring complexity in organisms and organizations.

While there is no consensus about the definition of complexity, it is widely accepted that the ability to produce uncertainty is the most prominent characteristic of complex systems. We introduce new metrics that purport to quantify the complexity of living organisms and social organizations based on their levels of uncertainty. We consider three major dimensions regarding complexity: diversity based on the number of system elements and the number of categories of these elements; flexibility which bears upon variations in the elements; and combinability which refers to the patterns of connection between elements. These three dimensions are quantified using Shannon's uncertainty formula, and they can be integrated to provide a tripartite complexity index. We provide a calculation example that illustrates the use of these indices for comparing the complexity of different social systems. These indices distinguish themselves by a theoretical basis grounded on the amount of uncertainty, and the requirement that several aspects of the systems be accounted for to compare their degree of complexity. We expect that these new complexity indices will encourage research programmes aiming to compare the complexity levels of systems belonging to different realms.

Responses to a dead companion in a captive group of tufted capuchins (Sapajus apella).

The observation of specific reactions by animals to dead conspecifics raises questions about their capacity to understand death. We describe the behavior of a captive group of tufted capuchins in the hours following the death of an adult female. The behavior of 12 subjects was recorded over a 5-h period. Most group members displayed exploratory behaviors toward the corpse, peering at it, smelling, touching, lifting or pulling it at least once. Interactions with the corpse were particularly frequent in the first hour, then decreased in the following hours. The relatives of the deceased female were the most involved individuals, and her daughter spent more time near her body than the other members of the group. Rates of interaction with the body were especially high in subadult individuals. Most of the behaviors directed to the body of the deceased individual appeared to be investigative.

Monkeys (Sapajus apella and Macaca tonkeana) and great apes (Gorilla gorilla, Pongo abelii, Pan paniscus, and Pan troglodytes) play for the highest bid.

Many studies investigate the decisions made by animals by focusing on their attitudes toward risk, that is, risk-seeking, risk neutrality, or risk aversion. However, little attention has been paid to the extent to which individuals understand the different odds of outcomes. In a previous gambling task involving 18 different lotteries (Pelé, Broihanne, Thierry, Call, & Dufour, 2014), nonhuman primates used probabilities of gains and losses to make their decision. Although the use of complex mathematical calculation for decision-making seemed unlikely, we applied a gradual decrease in the chances to win throughout the experiment. This probably facilitated the extraction of information about odds. Here, we investigated whether individuals would still make efficient decisions if this facilitating factor was removed. To do so, we randomized the order of presentation of the 18 lotteries. Individuals from 4 ape and 2 monkey species were tested. Only capuchin monkeys differed from others, gambling even when there was nothing to win. Randomizing the lottery presentation order leads all species to predominantly use a maximax heuristic. Individuals gamble as soon as there is at least one chance to win more than they already possess, whatever the risk. Most species also gambled more as the frequency of larger rewards increased. These results suggest optimistic behavior. The maximax heuristic is sometimes observed in human managerial and financial decision-making, where risk is ignored for potential gains, however low they may be. This suggests a shared and strong propensity in primates to rely on heuristics whenever complexity in evaluation of outcome odds arises. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Prolonged transport and cannibalism of mummified infant remains by a Tonkean macaque mother.

Observations of animals' responses to dying or dead companions raise questions about their awareness of states of helplessness or death of other individuals. In this context, we report the case of a female Tonkean macaque (Macaca tonkeana) that transported the body of her dead infant for 25 days and cannibalized its mummified parts. The mother appeared agitated in the first 2 days after the birth. She then took care of her infant's corpse, which progressively dried and became mummified. In a third stage, the mother continued to transport the corpse as it started disintegrating, and she gnawed and consumed some parts of the remains. Our observations suggest that mummification of the body favored persistence of maternal behaviors by preserving the body's shape. The female gradually proceeded from strong attachment to the infant's body to decreased attachment, then finally full abandonment of the remains.

Relocation stress induces short-term fecal cortisol increase in Tonkean macaques (Macaca tonkeana).

The level of glucocorticoids, especially if obtained from noninvasive sampling, can be used as an index of animal well-being, allowing evaluation of the animal's response to environmental modifications. Despite evidence that these hormones play a relevant role in energy metabolism regulation in perceived or real stress events, little is known regarding the factors that could modify the capability of animals to cope with relocation events. The aim of this research was to assess fecal cortisol metabolite concentrations before, during and after acute stress (transfer and relocation event) in two well-established social groups of Tonkean macaques (Macaca tonkeana). The results showed that the fecal levels of cortisol increased in individuals of both groups in response to the stress event, with a similar trend in males and females. Hormone levels were back to baseline values in both groups a few days after transfer and relocation. The presence of known social partners could be one of the factors that possibly facilitated the adaptation process.

Growth rates in a captive population of Tonkean macaques.

Measuring variations in body mass is necessary to gain a deeper understanding of the evolution of life-history patterns, and it provides information on the timing of sexual maturity and the development of sexual dimorphism. In this study, we collected longitudinal data on body mass from infancy to adulthood in a captive population of Tonkean macaques (Macaca tonkeana). Tests to evaluate whether social group, maternal age, and dominance rank influenced growth rates showed that they had no significant effect. We investigated the timing and magnitude of breaking points in the growth paths of males and females, and checked whether these breaking points could correspond to specific reproductive and morphological developmental events. We found that male and female Tonkean macaques have roughly equivalent body masses until around the age of four, when males go through an adolescent growth spurt and females continue to grow at a constant rate. Males not only grow faster than females, but they also continue to grow for nearly one and a half years after females have attained their full body mass. Growth rate differences account for approximately two-thirds of the body mass sexual dimorphism; only the remaining third results from continued male growth beyond the age where full body mass is reached in females. We also discovered remarkable correspondences between the timing of testicular enlargement and the adolescent growth spurt in males, and between dental development and slowdown breaking points in both sexes.

Evidence that monkeys (Macaca tonkeana and Sapajus apella) read moves, but no evidence that they read goals.

Whereas most experiments indicate that monkeys have no theory of mind, a study carried out by Wood and collaborators (2007) claimed that they can make inferences about the intentions of another individual. We applied the experimental procedure devised by these authors to investigate whether monkeys can recognize goal-directed actions. We tested 16 Tonkean macaques (Macaca tonkeana) and 12 tufted capuchin monkeys (Sapajus apella). Each subject was submitted to 24 trials in randomized order. The experimenter presented 2 containers, 1 of which was potentially baited with a food reward. After the experimenter had either intentionally or accidentally made an action on 1 of the containers, the subject was asked to select 1 of them. We found that individuals in both species failed to distinguish between accidental and intentional actions. However, they displayed a significant preference for the container touched by the experimenter in the hand conditions, and not in the elbow conditions. These results do not support those reported by Wood and collaborators, but they are consistent with other studies concluding that monkeys are not capable of mind reading.

Personality structure and social style in macaques.

Why regularities in personality can be described with particular dimensions is a basic question in differential psychology. Nonhuman primates can also be characterized in terms of personality structure. Comparative approaches can help reveal phylogenetic constraints and social and ecological patterns associated with the presence or absence of specific personality dimensions. We sought to determine how different personality structures are related to interspecific variation in social style. Specifically, we examined this question in 6 different species of macaques, because macaque social style is well characterized and can be categorized on a spectrum of despotic (Grade 1) versus tolerant (Grade 4) social styles. We derived personality structures from adjectival ratings of Japanese (Macaca fuscata; Grade 1), Assamese (M. assamensis; Grade 2), Barbary (M. sylvanus; Grade 3), Tonkean (M. tonkeana; Grade 4), and crested (M. nigra; Grade 4) macaques and compared these species with rhesus macaques (M. mulatta; Grade 1) whose personality was previously characterized. Using a nonparametric method, fuzzy set analysis, to identify commonalities in personality dimensions across species, we found that all but 1 species exhibited consistently defined Friendliness and Openness dimensions, but that similarities in personality dimensions capturing aggression and social competence reflect similarities in social styles. These findings suggest that social and phylogenetic relationships contribute to the origin, maintenance, and diversification of personality.

Facial displays in young tufted Capuchin monkeys (Cebus apella): appearance, meaning, context and target.

Facial displays are important for communication, and their ontogeny has been studied primarily in chimpanzees and macaques. We investigated the ontogeny, communicative function and target of facial displays in Cebus apella. Our results show that facial displays are absent at birth and develop as infants grow older. Lip-smacking appears first (at about 1 month of age), followed by scalp-lifting, relaxed open-mouth, silent bared-teeth, open-mouth silent bared-teeth displays and finally the open-mouth threat face. Infants perform most facial displays in the same contexts as adults, with the exception of the silent bared-teeth display that young capuchins use primarily, or exclusively, in affiliative contexts. Interestingly, facial displays are exchanged very often with peers, less frequently with adults and almost never with the mother.