Macaca Tonkeana Research Articles

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.

Empathy versus parsimony in understanding post-conflict affiliation in monkeys: model and empirical data.

Post-conflict affiliation between former opponents and bystanders occurs in several species of non-human primates. It is classified in four categories of which affiliation received by the former victim, ‘consolation’, has received most attention. The hypotheses of cognitive constraint and social constraint are inadequate to explain its occurrence. The cognitive constraint hypothesis is contradicted by recent evidence of ‘consolation’ in monkeys and the social constraint hypothesis lacks information why ‘consolation’ actually happens. Here, we combine a computational model and an empirical study to investigate the minimum cognitive requirements for post-conflict affiliation. In the individual-based model, individuals are steered by cognitively simple behavioural rules. Individuals group and when nearby each other they fight if they are likely to win, otherwise, they may groom, especially when anxious. We parameterize the model after empirical data of a tolerant species, the Tonkean macaque (Macaca tonkeana). We find evidence for the four categories of post-conflict affiliation in the model and in the empirical data. We explain how in the model these patterns emerge from the combination of a weak hierarchy, social facilitation, risk-sensitive aggression, interactions with partners close-by and grooming as tension-reduction mechanism. We indicate how this may function as a new explanation for empirical data.

First case of peritoneal cysticercosis in a non-human primate host (Macaca tonkeana) due to Taenia martis

BackgroundInfections with larval stages (metacestodes) of a variety of taeniid species have been described in primates, including humans, with partial to severe clinical consequences. Taenia martis is a tapeworm of mustelids, and martens are mainly their definitive hosts in Central Europe. In the rodent intermediate host cysticerci develop in the pleural and peritoneal cavities. The present report describes a case of T. martis peritoneal cysticercosis in a Tonkean macaque.FindingsAn abdominal mass was detected in a 3-year-old male Tonkean macaque (Macaca tonkeana) born and raised in a primate colony in France. Examination of the mass after laparotomy showed numerous vesicles identified as cysticerci of T. martis, based on the morphology of scolex and hooks, with confirmation by PCR amplification and sequence analysis of the mitochondrial cytochrome c oxidase subunit 1 (cox1) and NADH dehydrogenase subunit 1 (nad1) genes. Exeresis of the lesion was not possible and praziquantel (5.7 mg/kg) was given twice at an interval of 3 days. The abdominal mass was greatly diminished upon examination 2 months later and no signs of recurrence were noticed during the following 4 years.ConclusionsThis is the first report of T. martis cysticercosis in a monkey. This record and the recent first description of an ocular T. martis cysticercosis in a human show the susceptibility of primates to T. martis and its zoonotic potential. This taeniid species must be considered in the differential diagnosis of cysticercosis in primates.

Hand preferences on unimanual and bimanual tasks in Tonkean macaques (Macaca tonkeana)

This is the first study to examine hand preferences in Tonkean macaques on a bimanual task. One of our objectives was to continue the move toward greater task standardization, in order to facilitate comparisons between species and studies on handedness. The main aim was to test and determine task robustness, by varying intra-task complexity. To this end, we administered several different tasks to the subjects: two unimanual tasks (grasping task featuring items of different sizes) and three coordinated bimanual tasks (tube task involving different materials, weights, and diameters). Although we found no significant hand preference in either task at the group level, the macaques were more strongly lateralized for small items than for large ones in the unimanual grasping task. Moreover, the absence of a correlation between these two versions of the unimanual task confirmed the weakness of this grasping task for assessing handedness. Regarding the bimanual tube task, no difference was found between the three versions in either the direction or the strength of hand preference. Moreover, the highly correlated hand preferences between these three versions suggest that the tube task provides a more robust means of measuring manual preferences.

Tonkean macaques communicate with their right hand

There are two conflicting hypotheses to explain the origins of language. Vocal origin theory states that language results from the gradual evolution of animals’ vocal communication, but gestural origin theory considers that language evolved from gestures, with the initial left-hemispheric control of manual gestures gradually encompassing vocalizations. To contribute to this debate, we investigated functional hemispheric specialization related to hand biases when grasping or showing an object through manual gesture in Tonkean macaques. The results of this study, the first quantitative study on Tonkean macaques’ handedness, showed a remarkable convergence of the Tonkean macaques’ handedness patterns with those of baboons and human infants, with hand preferences for manual communicative gestures significantly favoring the use of the right hand. Our findings support the hypothesis that left hemispheric lateralization for language is derived from a gestural communication system that was present in the common ancestor of macaques, baboons and humans.

Nutritional content explains the attractiveness of cacao to crop raiding Tonkean macaques

Abstract Nutritional ecology has been linked to crop raiding behavior in a number of wildlife taxa. Here our goal is to explore the role nutrition plays in cacao crop raiding by Tonkean macaques Macaca tonkeana in Sulawesi, Indonesia. From June – Sept. 2008 we collected fruit samples from 13 species known to be important Tonkean macaque foods and compared their nutritional value to that of cacao Theobroma cacao, an important cash crop in Sulawesi. Cacao pulp was significantly lower in protein, but lower in dietary fiber, and higher in digestible carbohydrates and energy content compared to forest fruits. These findings, combined with the fact that cacao fruits are spatially concentrated and available throughout the year, likely explain why Tonkean macaques are attracted to this cultivated resource. We use these data along with published feeding ecology data to propose strategies to minimize human-macaque conflict. Namely, we recommend the deliberate protection of Elmerillila tsiampaccca, Ficus spp. and Arenga pinnata, fruit species known to be regularly consumed and of considerable nutritional value. We also identify the A. pinnata palm as a potential buffer resource to curb cacao crop raiding by macaques. Cacao is a hard-to-process food because the pods have a thick outer skin that encases the seeds and pulp. Aren palm fruit, although lower in digestibility, is easier-to-process, higher in protein, and also available year round. In addition, because the palm has considerable cultural and economic significance for local people, the strategy of planting Aren palm in a buffer corridor is likely to garner local community support.

Social tolerance and adult play in macaque societies: a comparison with different human cultures

Differences in play behaviour often illuminate complex ecological parameters and social differences. In primate societies, including humans, individuals acquire information through play. It is adults in every community that are most committed to managing social practices. In tolerant species, adults often participate in play to reinforce social networks and cooperation. The 20 macaque species are all organized in multimale, multifemale groups but vary along a continuum from despotic/intolerant to egalitarian/tolerant social systems. These different social styles influence a wide range of behaviours including aggression and affiliation patterns, dominance relationships, and nepotism. We tested some hypotheses by comparing play patterns in two macaque societies at opposite ends of the continuum: despotic Japanese macaques, Macaca fuscata, and tolerant Tonkean macaques, Macaca tonkeana. Our results show that these two species have striking differences in the distribution of social play according to the age and sex of the players. Our findings strongly indicate that play, a highly plastic and versatile behaviour, is sensitive to the quality of interindividual relationships of a species, thus reflecting the nature of its social network. The different patterns of macaque play show striking parallels with those from comparisons of different human cultures including the distribution of social play according to the age and gender, partner preference according to age, and permissiveness of mothers. The adult play propensity of Tonkean compared to Japanese macaques indicates that adult–adult play is a good predictor for the polarity of changes in aggressiveness between different groups separated either genetically (taxa) or culturally (ethnies).

Are monkeys able to plan for future exchange?

Whether or not non-human animals can plan for the future is a hotly debated issue. We investigate this question further and use a planning-to-exchange task to study future planning in the cooperative domain in two species of monkeys: the brown capuchin (Cebus apella) and the Tonkean macaque (Macaca tonkeana). The rationale required subjects to plan for a future opportunity to exchange tokens for food by collecting tokens several minutes in advance. Subjects who successfully planned for the exchange task were expected to select suitable tokens during a collection period (5/10 min), save them for a fixed period of time (20/30 min), then take them into an adjacent compartment and exchange them for food with an experimenter. Monkeys mostly failed to transport tokens when entering the testing compartment; hence, they do not seem able to plan for a future exchange with a human partner. Three subjects did however manage to solve the task several times, albeit at very low rates. They brought the correct version of three possible token types, but rarely transported more than one suitable token at a time. Given that the frequency of token manipulation predicted transport, success might have occurred by chance. This was not the case, however, since in most cases subjects were not already holding the token in their hands before they entered the testing compartment. Instead, these results may reflect subjects' strengths and weaknesses in their time-related comprehension of the task.

NO MOM, NO PEACE FOR RHESUS MONKEYS

![Figure][1] Stress at an early age can have important consequences on the behaviour and brain development of an animal. For example, in their 2000 publication in Primates , Drago and Thierry found that when baby Tonkean Macaques were separated from their mothers they became aggressive and

Individual Analyses of Lévy Walk in Semi-Free Ranging Tonkean Macaques (Macaca tonkeana)

Animals adapt their movement patterns to their environment in order to maximize their efficiency when searching for food. The Lévy walk and the Brownian walk are two types of random movement found in different species. Studies have shown that these random movements can switch from a Brownian to a Lévy walk according to the size distribution of food patches. However no study to date has analysed how characteristics such as sex, age, dominance or body mass affect the movement patterns of an individual. In this study we used the maximum likelihood method to examine the nature of the distribution of step lengths and waiting times and assessed how these distributions are influenced by the age and the sex of group members in a semi free-ranging group of ten Tonkean macaques. Individuals highly differed in their activity budget and in their movement patterns. We found an effect of age and sex of individuals on the power distribution of their step lengths and of their waiting times. The males and old individuals displayed a higher proportion of longer trajectories than females and young ones. As regards waiting times, females and old individuals displayed higher rates of long stationary periods than males and young individuals. These movement patterns resembling random walks can probably be explained by the animals moving from one location to other known locations. The power distribution of step lengths might be due to a power distribution of food patches in the enclosure while the power distribution of waiting times might be due to the power distribution of the patch sizes.

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."

A comparative network analysis of social style in macaques

In group-living species, individuals gain significant advantages from establishing an extensive network of social relationships. This results in complex organizations that are difficult to quantify in a comprehensive manner. In this respect, network analyses are an ideal means to pinpoint the overall properties of social structures, and the place of each individual within these structures. We used network measurements to investigate cross-species variations in the social style of macaques, and studied 12 groups from four species. Two species (Macaca mulatta, Macaca fuscata) were characterized by a relatively weak social tolerance, a steep gradient of dominance and a strong preference for kin. The other two species (Macaca nigra, Macaca tonkeana) were known to display higher levels of tolerance, relaxed dominance and low kinship bias. We used a centrality index based on eigenvector centrality to show that in a comparison of intolerant and tolerant species, top-ranking individuals were more central than other group members in the former species than the latter. We also found that networks had higher modularity in intolerant species, indicating that kin-related partners interacted more frequently in subgroups of these species than in those of tolerant species. Consistently, the matrix of body contacts was more strongly correlated with the kinship matrix in intolerant species. This study demonstrates the efficiency of network methodology in detecting fine and overall contrasts in social structures, and also reveals novel dimensions in the social style of macaques.

Can Monkeys Make Investments Based on Maximized Pay-off?

Animals can maximize benefits but it is not known if they adjust their investment according to expected pay-offs. We investigated whether monkeys can use different investment strategies in an exchange task. We tested eight capuchin monkeys (Cebus apella) and thirteen macaques (Macaca fascicularis, Macaca tonkeana) in an experiment where they could adapt their investment to the food amounts proposed by two different experimenters. One, the doubling partner, returned a reward that was twice the amount given by the subject, whereas the other, the fixed partner, always returned a constant amount regardless of the amount given. To maximize pay-offs, subjects should invest a maximal amount with the first partner and a minimal amount with the second. When tested with the fixed partner only, one third of monkeys learned to remove a maximal amount of food for immediate consumption before investing a minimal one. With both partners, most subjects failed to maximize pay-offs by using different decision rules with each partner' quality. A single Tonkean macaque succeeded in investing a maximal amount to one experimenter and a minimal amount to the other. The fact that only one of over 21 subjects learned to maximize benefits in adapting investment according to experimenters' quality indicates that such a task is difficult for monkeys, albeit not impossible.

Interactions Between Third Parties and Consortship Partners in Tonkean Macaques (Macaca tonkeana)

Sexual competition is potentially disruptive for the cohesion of social groups because stress and conflicts can extend to other group members. The displays and interactions of sexual partners are liable to influence the behavior of group-mates, which may need to observe them to anticipate possible consequences. We studied 2 captive groups of Tonkean macaques (Macaca tonkeana) to test whether group-mates pay more attention to consort partners, modify their activities and social interactions, and exhibit signs of stress during periods of sexual consortships. We found that group-mates approached the top-ranking male more frequently and were more frequently oriented toward the consort pair at the time of consortship than at other times. Group-mates spent less time sleeping, and devoted less time to manipulating the environment and more time to monitoring during consortship. This indicates that consortships may incur costs in individuals not involved in sexual competition. However, Tonkean macaques did not exhibit any signs of increased stress during consortship periods, as their rates of scratching and yawning did not differ between consortship and nonconsortship periods. This study shows that not only direct competitors but also other individuals monitor the behavior of sexual partners. It is likely that group-mates obtain information this way about ongoing action, and take decisions accordingly.

Land use in semi-free ranging Tonkean macaques Macaca tonkeana depends on environmental conditions: A geographical information system approach

Abstract Wild animals use their habitat according to ecological pressures such as predation, resource availability or temperature, yet little is known about how individuals use their environment in semi free-ranging conditions. We assessed whether a semi-free ranging group of Tonkean macaques Macaca tonkeana used its wooded parkland in a heterogeneous way. GIS and GPS were used to determine whether individuals adjusted their behaviors according to variation in environmental constraints over time of day and the course of a year. We demonstrated that social and resting activities occurred in high altitude areas and areas with a high density of bushes, whereas the group foraged in areas where the density of bushes and grass was low. In general, the animals used areas exposed to the sun that were not on a slope. Semi-free ranging Tonkean macaques seemed to behave like their wild counterparts in terms of activity budget, land use per activity and thermoregulation.

The use of the bared-teeth display during play fighting in Tonkean macaques (Macaca tonkeana): Sometimes it is all about oneself.

Play signals are viewed as important means by which animals inform each other that bites, strikes, and throws that occur during play fighting are indeed playful rather than serious. One such signal is the open mouth play face that is common in primates and many other mammals. Unfortunately, as most play fighting involves biting, it can be ambiguous as to whether any instance of opening the mouth is performed to communicate playful intent or is simply a preparation for biting. In this study, open mouths co-occurring with the bared-teeth display (teeth-baring) in Tonkean macaques were used to assess the context in which facial gestures only relevant for signaling (i.e., teeth-baring is not necessary for biting) are used during play. Two predictions arising from the hypothesis that play signals are used to facilitate playful contact were tested: that the open mouth with teeth-baring should (1) be most frequent preceding contact, and (2) that it should be performed most often when bites are directed at orientations that is visible to the recipient. The data only partially support these predictions. The open mouth with teeth-baring is also frequently used when a monkey withdraws from playful contact. Moreover, it is associated with bites to body targets, such as the rump, that offer little prospect for detection by the recipient; this supports the possibility that play signals may sometimes be emitted not to communicate with the partner but with the performer itself. Thus, play signals serve multiple functions during play fighting.

Are Monkeys Sensitive to the Regularity of Pay-off?

Animals commonly face fluctuations in their environment and resources. To maximize their benefits,they need to integrate the risks attached to potential pay-offs. We do not know, however, to what extent individuals account for irregularity in the latter. We tested the sensitivity of monkeys (Cebusapella, Macaca tonkeana, M. fascicularis) to the irregularity of pay-offs in two different tasks. In a first experiment, the subjects were given an exchange task where the reward probability varied between different conditions, but yielded the same average pay-off. There was no evidence of subjects favoring either condition, meaning that they behaved in accordance with the predictions ofthe classical decision theory (Expected Utility Theory). In a second experiment, we offered to subjects a choice between two options involving different pay-off regularity. In this case, a wide range of inter-individual variation was found in the choices of individuals. Whereas monkeys accepted irregular pay-off in a rational way, there were individual biases in their preferences. These results indicate that the preferences of animals in a risky situation were not unequivocally shaped by the environment in which species have evolved.

Conserving social–ecological systems in Indonesia: human–nonhuman primate interconnections in Bali and Sulawesi

An important question asked by primatologists and conservationists alike is: what is the relevance of primates and primate conservation for ecosystem conservation? The goal of this article is to contribute to this dialogue by advocating the use of a research perspective that focuses on the dynamics of human-nonhuman primate sympatry and interaction (i.e., ethnoprimatology) in order to better understand complex social-ecological systems and to inform their conservation management. This perspective/approach is based largely on the recognition that human primates are important components of all ecological systems and that niche construction is a fundamental feature of their adaptive success. To demonstrate the relevance of the human-nonhuman primate interface for ecosystem conservation, we provide examples from our research from two islands in the Indonesian archipelago: Bali and Sulawesi. In Bali, humans and long-tail macaques coexist in a system that creates favorable environments for the macaques. This anthropogenic landscape and the economic and ecological relationships between humans and monkeys on Bali provide insight into sustainable systems of human/nonhuman primate coexistence. In Lore Lindu National Park in Central Sulawesi, villagers and Tonkean macaques overlap in their use of both forest and cultivated resources. The finding that the Arenga pinnata palm is extremely important for both villagers and macaques points to a conservation management recommendation that may help protect the overall ecosystem; the cultivation and propagation of mutually important tree species at forest-agricultural ecotone as a means to curb crop raiding and to alleviate farmer's perceived need to clear additional forest.

From the first intention movement to the last joiner: macaques combine mimetic rules to optimize their collective decisions.

Mechanisms related to collective decision making have recently been found in almost all animal reigns from amoebae to worms, insects and vertebrates, including human beings. Decision-making mechanisms related to collective movements-including pre-departure and joining-have already been studied at different steps of the movement process, but these studies were always carried out separately. We therefore have no understanding of how these different processes are related when they underlie the same collective decision-making event. Here, we consider the whole departure process of two groups of Tonkean macaques (Macaca tonkeana), using a stochastic model. When several exclusive choices are proposed, macaques vote and choose the majority. Individuals then join the movement according to a mimetism based on affiliative relationships. The pre-departure quorum and the joining mimetic mechanism are probably linked, but we have not yet identified which transition mechanism is used. This study shows that decision-making related to macaque group movements is governed by a quorum rule combined with a selective mimetism at departure. This is the first time that transition mechanisms have been described in mammals, which consequently helps understand how a voting process leads to social amplification. Our study also provides the first complete proof that there is continuity in the decision-making processes underlying collective movements in mammals from the first intention movement right through to the last joiner.

Delay Maintenance in Tonkean Macaques (Macaca tonkeana) and Brown Capuchin Monkeys (Cebus apella)

Animals commonly face choices requiring them to wait and postpone action. The ability to delay gratification is a prerequisite for making future-oriented decisions. We investigated the ability of brown capuchins (Cebus apella) and Tonkean macaques (Macaca tonkeana) to delay benefits in several experiments. In exchange tasks, subjects had to return a piece of cookie after a given time lag to obtain a larger one from an experimenter. Capuchins could wait 10–40 s and macaques 20–80 s depending on subjects and the size of rewards. Both groups were able to anticipate delay durations, but unlike macaques, capuchins discounted all sizes of reward at the same speed, meaning that their delay-maintenance was not affected by the reward size. When the subjects could give the initial piece of cookie back immediately and then wait for the return, performances increased to 10–21 min for capuchins and 21–42 min for macaques, demonstrating the role of consumption inhibition in postponing gratification. In a further task, we presented subjects with an accumulation of food pieces added at short intervals until they seized them. On average, brown capuchins could wait 33–42 s and macaques 38–72 s before seizing the rewards. Our results confirmed that brown capuchins were more impulsive than Tonkean macaques in several tasks. We did not find significant differences between the waiting performances of the Tonkean macaques and those previously reported in long-tailed macaques. The contrasting performances of macaques and capuchins might be related to their different skills in the physical and social domains.