Macaca Tonkeana Research Articles

Teeth Baring as a Model to Understand Complex Facial Signals in a Tolerant Macaque Species.

Facial communication regulates many aspects of social life in human and nonhuman primates. Empirically identifying distinct facial expressions and their underlying functions can help illuminate the evolution of species' communicative complexity. We focused on bared-teeth faces (BTFs), a highly versatile facial expression in the tolerant macaque Macaca tonkeana. By employing a diverse array of techniques (MaqFACS, unsupervised cluster analysis, Levenshtein distance, NetFACS), we quantitatively discriminated two distinct BTFs: bared-teeth (BT) and open mouth bared-teeth (OMBT), and evaluated their distribution across peaceful, playful, and agonistic contexts. Neither BT nor OMBT were context-specific, although BT frequently occurred during peaceful interactions and with low levels of stereotypy. OMBT was highly stereotyped during play, a context involving strong unpredictability. The presence of tongue-protrusion during OMBT was exclusive to peaceful contexts whereas the presence of glabella-lowering during BT and OMBT was specific to agonistic contexts. Hence, BT and OMBT per se are not context-specific, but their contextual relevance hinges on the inclusion of specific key elements. Moving forward, concurrent analyses of stereotypy and specificity should extend beyond our study to encompass other primate and non-primate species, facilitating direct comparisons and revealing how communicative and social complexity coevolve.

The Analysis of Habitat Suitability for Macaca Tonkeana in the Pangi Binangga Natural Reserve of West Toboli Village Using SIG and PCA Approach

The boti monkey, also known by its scientific name Macaca tonkeana, is a type of endemic primate found on Sulawesi Island. This study aims to determine the suitability of Macaca tonkeana habitat by using spatial analysis methods to determine the most suitable areas for survival. The study used a sample of locations conducted by observation method. The data collected was then spatially analysed by overlaying, classing, weighting, and scoring. PCA analysis was used to classify variables and assign weights to each parameter. Based on the habitat suitability model developed, the study sites were classified into three suitability levels: low, medium and high. Low suitability with an area of 9.475621 ha (0.374%). Medium suitability with an area of 461.777729 ha (18.184 %). High suitability with an area of 2065.896076 ha (81.442%). The model validation showed that most of the validation points were located within the high suitability class, with 92.59% of the total validation points. This indicates that the study site is likely to be a highly suitable habitat for Boti Monkeys.

Intestinal parasites infecting captive non-human primates in Italy.

Non-human primates (NHPs) living in captive conditions are susceptible to intestinal parasites that can contribute to mortality and morbidity, and cause zoonotic infections. Thus, parasite surveys on NHP populations under human care are relevant as part of the evaluation of NHPs welfare and in the zoonotic disease risk assessment, as well as in the exploration of parasite transmission pathways, according to the One-Health concept. This study aimed to identify intestinal parasites infecting NHPs living in two wildlife recovery centers and in a zoological garden, in Italy. Ninety-three fecal samples from Macaca tonkeana, Macaca fascicularis, Sapajus apella, Chlorocebus aethiops, Macaca fuscata, Macaca sylvanus, and Cebus capucinus were collected at Piano dell'Abatino Park (Lazio), and fecal smears and flotation were performed in order to identify parasites according to morphological keys. Additionally, one carcass of M. fuscata from the Bioparco Zoological Garden of Rome (Lazio) and one of M. fascicularis from the Center for the Recovery of Exotic and Maremma Wild Animals (Tuscany) were necropsied and intestinal adult nematodes were collected and characterized at morphological and molecular level, using the mitochondrial cox1 and rrnL markers. Protozoans (Entamoeba coli, Iodamoeba bütschlii, Dientamoeba fragilis-like, Giardia sp.), chromists (Balantidium/Buxtonella sp.) and nematodes (Capillaria sp., Trichuris sp., strongyliform larvae and Oesophagostomum sp.) were found through fecal smears and flotation. The collected adult nematodes from dead NHPs were morphologically identified as whipworms (genus Trichuris). Phylogenetic analyses grouped Trichuris specimens into the Trichuris trichiura complex of species, with specimens from M. fuscata clustering into a host-specific branch, and whipworms from M. fascicularis clustering within a clade formed by Trichuris infecting several primate species, including humans. The results here collected revealed the presence of potentially zoonotic parasites circulating in captive primates in Italy, providing useful information for the formulation of management and care plans for captive NHPs, and for the elaboration of safety measures for visitors and animal keepers.

Spot the odd one out: do snake pictures capture macaques' attention more than other predators?

Detecting and identifying predators quickly is key to survival. According to the Snake Detection Theory (SDT), snakes have been a substantive threat to primates for millions of years, so that dedicated visual skills were tuned to detect snakes in early primates. Past experiments confronted the SDT by measuring how fast primate subjects detected snake pictures among non-dangerous distractors (e.g., flowers), but did not include pictures of primates' other predators, such as carnivorans, raptors, and crocodilians. Here, we examined the detection abilities of N = 19 Tonkean macaques (Macaca tonkeana) and N = 6 rhesus macaques (Macaca mulatta) to spot different predators. By implementing an oddity task protocol, we recorded success rates and reaction times to locate a deviant picture among four pictures over more than 400,000 test trials. Pictures depicted a predator, a non-predator animal, or a simple geometric shape. The first task consisted of detecting a deviant picture among identical distractor pictures (discrimination) and the second task was designed to evaluate detection abilities of a deviant picture among different distractor pictures (categorization). The macaques detected pictures of geometric shapes better and faster than pictures of animals, and were better and faster at discriminating than categorizing. The macaques did not detect snakes better or faster than other animal categories. Overall, these results suggest that pictures of snakes do not capture visual attention more than other predators, questioning previous findings in favor of the SDT.

Is this worth the trouble? Strategic conflict management in Tonkean macaques

Conflict management entails preventing and repairing damages resulting from social conflicts. While previous research has emphasized post-conflict actions like reconciliation, the understanding of how primates weigh the costs and benefits of conflict remains limited. Uncovering this hidden but fundamental aspect of conflict management requires addressing actively avoided social conflicts. In a study involving semi-free ranging Tonkean macaques, individuals were presented with social dilemmas: displacing a peer to access a preferred juice reward or opting for a peer-free but less preferred one to avoid conflict. The results showed that subjects attributed a cost to the social conflict and did not demonstrate a systematic drive to dominate. Decision modeling revealed integration of peer hierarchy and reward subjective value, with subjects' own social rank impacting the balance between these social and economic dimensions. Overall, this research highlights how primates strategically address group cohesion and peacekeeping, sometimes at the expense of personal preferences.

Studying the Tonkean macaques of Strasbourg, a tale full of sound and fury.

In this paper, I chronicle the Strasbourg population of Tonkean macaques (Macaca tonkeana) over a period of half a century. In 1972, Tonkean macaques were imported from Sulawesi, Indonesia, to eastern France, leading to the establishment of two social groups in the Strasbourg region several years later. Our research team studied the social behavior and cognitive abilities of these Tonkean macaques for four decades. The species is characterized by a high degree of social tolerance. This has proven to be very informative in comparative studies of macaque social behavior, opening a new perspective on the evolution of primate societies. Over the years, the population has grown, and more social groups have been formed. However, the fact that some of the Tonkean macaques were healthy carriers of the herpes B virus led to disagreements over their management and eventually to the elimination of the positive individuals. Many individuals from the Strasbourg population are now kept in sanctuaries, and the number of captive breeding groups is limited. We still have much to learn about Tonkean macaques and there is a need for studies carried out in their native habitat in Sulawesi.

Hormonal responses to mating competition in male Tonkean macaques

Glucocorticoid and androgen hormones play a prominent role in male reproductive effort. Their production usually increases in non-human primates during mating competition, which may include rivalry for access to receptive females, struggles for high dominance rank, or social pressure on low-ranking individuals. It is generally assumed that glucocorticoids and androgens are associated with mating challenges rather than dominance status, but the involvement of multiple factors makes it difficult to disentangle the two. In this regard, Tonkean macaques provide a suitable model because they are characterized by relaxed dominance and year-round breeding, meaning that there is typically no more than one receptive female in a group, and thus first-ranking males can easily monopolize her. We studied two captive groups of Tonkean macaques over an 80-month period, recording the reproductive status of females, collecting urine from males and sampling behaviors in both sexes. Male urinary hormone concentrations could be affected by increased competition caused by the mating period, the number of males and the degree of female attractiveness. The highest increases in androgens were recorded in males performing female mate-guarding. Despite the importance of dominance status in determining which males can mate, we found no significant effect of male rank on glucocorticoids and only a marginal effect on androgens during mate-guarding. Both types of hormones were more directly involved in the mating effort of males than in their dominance status. Our results show that their function can be understood in light of the particular competitive needs generated by the species-specific social system.

A phased process to reintroduce a hand-reared infant Tonkean macaque to her natal group

Abstract Reintroduction of separated individuals into their social group is a major problem in the management of captive group of non-human primates. Here we report a case in captive Tonkean macaques in which a female infant was abandoned by her mother after birth, then removed, hand-reared, and reintroduced after weaning to her original group in several stages. After the initial phase of separation, a period of habituation to group members followed during which the infant was brought to the front of the group enclosure daily for two months. We then started a phased reintroduction process that lasted a year. Because the biological mother was the group member most attracted to the infant, the process began by allowing the two individuals to interact. In the next stages, we introduced the infant to the other individuals one after the other, starting with the females. Females then acted as protectors against potential male aggression. At the age of one year and two months, the introduced individual had fully integrated her original group. Two years later, she appeared to behave like the other group members. This report shows that a phased process can be used to reintroduce an infant to a macaque group containing several adult females and males.

Primate origins of corepresentation and cooperative flexibility: A comparative study with common marmosets (Callithrix jacchus), brown capuchins (Sapajus apella), and Tonkean macaques (Macaca tonkeana).

Human joint action is generally facilitated by the tendency to represent not only one's own task and behavior but also the partner's. Yet, under some conditions, such as in the joint Simon task, corepresentation can cause interference and hampers, rather than facilitates, joint performance. A competent cooperator should thus also be able to flexibly inhibit corepresentation if that is conducive to cooperation success. To investigate the evolutionary origin of corepresentation, as well as the cooperative flexibility to inhibit it when necessary, we tested brown capuchins and Tonkean macaques in the joint Simon task and compared them with the previously tested marmosets. Corepresentation was present in all 3 species, but its strength and the cooperation success varied substantially. The cooperatively breeding marmosets showed the weakest corepresentation effect and, therefore, highest cooperation success, and they were the only ones to use mutual gaze when coordination with the partner was necessary. Cooperative flexibility was therefore not correlated with brain size but with the prevalence of cooperation in nature. This conclusion was corroborated by species differences in gazing patterns and suggests that the drivers of cooperative flexibility in humans were not solely cognitive. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Come with me: experimental evidence for intentional recruitment in Tonkean macaques.

Recruitment is a process by which animals can initiate collective movements: the action of an individual prompts conspecifics to follow. Although it has been hypothesized that animals may be able to intentionally recruit others, there is no experimental evidence of this to date. We tested this hypothesis in two pairs of Tonkean macaques in a situation requiring the subjects to find a food site in a 2800 m2 area, and approach the site together to release rewards. Each subject was informed of the location of either highly or little-valued rewards. We recorded attention-action sequences in which an individual checked that his partner was attending to him before moving, and also simple departures (i.e., not preceded by eye contact). Analyses showed that sequences were more often followed by recruitment and leading the partner to a baited site than simple departures were. Moreover, subjects used attention-action sequences more frequently when informed of the location of the highly valued reward. This may be explained by the fact that the more motivated they were by the expected rewards, the more likely they were to actively recruit their partner. No such effect was found when subjects performed simple departures. We conclude that Tonkean macaques are capable of intentional recruitment because the subjects voluntarily behaved with the goal of influencing their partner's movement: they checked that the partner was paying attention to them and prompted him to follow by moving. Such performances can be accounted for either by associative learning or by intentional communication.

Individual differences in co-representation in three monkey species (Callithrix jacchus, Sapajus apella and Macaca tonkeana) in the joint Simon task: the role of social factors and inhibitory control

Behavioral coordination is involved in many forms of primate interactions. Co-representation is the simultaneous mental representation of one’s own and the partner’s task and actions. It often underlies behavioral coordination and cooperation success. In humans, the dyadic social context can modulate co-representation. Here, we first investigated whether individual differences in co-representation in the joint Simon task in capuchin monkeys and Tonkean macaques can be explained by social factors, namely dyadic grooming and sociality index, rank difference and eigenvector centrality. These factors did not predict variation in co-representation. However, in this specific task, co-representation reduces rather than facilitates joint performance. Automatic co-representation therefore needs to be inhibited or suppressed to maximize cooperation success. We therefore also investigated whether general inhibitory control (detour-reaching) would predict co-representation in the joint Simon task in Tonkean macaques, brown capuchin and marmoset monkeys. Inhibitory control did neither explain individual differences nor species differences, since marmosets were most successful in their joint performance despite scoring lowest on inhibitory control. These results suggest that the animals’ ability to resolve conflicts between self and other representation to increase cooperation success in this task is gradually learned due to frequent exposure during shared infant care, rather than determined by strong general inhibitory control. Further, we conclude that the joint Simon task, while useful to detect co-representation non-invasively, is less suitable for identifying the factors explaining individual differences and thus a more fruitful approach to identify these factors is to design tasks in which co-representation favors, rather than hinders cooperation success.

Effects of social tolerance on stress: hair cortisol concentrations in the tolerant Tonkean macaques (Macaca tonkeana) and the despotic long-tailed macaques (Macaca fascicularis)

Group living is a source of stress and an individuals’ social environment has been shown to have a significant effect on its health and well-being. However, little is known about how different social organizations affect the stress levels of their members. Is living in a hierarchical society more or less stressful than living in a more tolerant structure? Here, we assess cortisol concentrations in the hair of two macaque species with radically different dominance styles: the egalitarian Tonkean macaque (Macaca Tonkeana) and the despotic long-tailed macaques (Macaca fascicularis). Hair was sampled in winter and again in late spring in two mixed-sex groups of 22 Tonkean macaques and 9 long-tailed macaques; Hair cortisol concentrations were significantly higher in the egalitarian Tonkean macaques than in the despotic long-tailed macaques, ranging from 161.13 to 938.8 pg/mg (mean ± SD 349.67 ± 126.22) and from 134.46 to 339.86 pg/mg (mean ± SD 231.2 ± 44.24), respectively. There was no difference between male and female cortisol concentrations, but hair cortisol increased with age in males. Dominance rank certainty was lower among female Tonkean macaques compared to long-tailed macaques. Our results suggest that species differences in dominance styles may translate into differences in long-term cortisol concentrations. We suggest that the higher cortisol concentrations in Tonkean macaques could be linked to the instability and lack of predictability and control around social relationships.

Public Perception on the Existence of Macaca hecki and Macaca tonkeana in Protected Forest and Pangi Binangga Nature Reserve of Central Sulawesi

Wildlife is one of the biological natural resources that can be use it sustainably and sustainably, because wildlife is a natural resource renewable or renewable biological (renewable resources). This study aims to determine public perception of the exixtence of Macaca hecki and Macaca tonkeana in Protected Forest and Pangi Binangga Nature Reserve of Central Sulawesi. This research was carried out along the Palu-Parigi trans road which is in the Protected Forest and Pangi Binangga Nature Reserve, Central Sulawesi Province in April - June 2021. The results showed that presence of endemic Sulawesi macaque (M. hecki and M. tonkeana) along the Palu-Parigi trans road which is in the Protected Forest and Pangi Binangga Nature Reserve area causes various problems such as people experiencing unpleasant events with the presence of macaque, stolen goods, enter into community plantations, and damage various types of agricultural crops (avocado, cloves, cocoa, and several other fruits).

Not all yawns tell the same story: The case of Tonkean macaques.

Here we show for the first time that the plasticity in morphology and duration of yawning in Macaca tonkeana can be associated with different functional contexts. Macaca tonkeana is classified as a tolerant macaque species characterized by social interactions minimally constrained by dominance rank or kinship. Tonkean macaques, as other egalitarian species, rely on a complex facial communicative system. We found that the degree of mouth opening (ranging from covered to uncovered tooth yawns) and the duration of yawning were not strictly dependent. The shortest uncovered tooth yawns were associated with an intense locomotor/physical activity and peaked immediately after stressful social events thus indicating an increase in arousal. In contrast, longer yawns, independently from teeth exposure, were primarily associated with a relaxed state of the subject. In conclusion, our study suggests that to explore the potential different functions of yawning, it is necessary to focus on the variability of its expression both in terms of morphology and duration, because not all yawns tell the same story.

Assessing the reliability of an automated method for measuring dominance hierarchy in non-human primates

Among animal societies, dominance is an important social factor that influences inter-individual relationships. However, assessing dominance hierarchy can be a time-consuming activity which is potentially impeded by environmental factors, difficulties in the recognition of animals, or disturbance of animals during data collection. Here we took advantage of novel devices, machines for automated learning and testing (MALT), designed primarily to study non-human primate cognition, to additionally measure the dominance hierarchy of a semi-free-ranging primate group. When working on a MALT, an animal can be replaced by another, which could reflect an asymmetric dominance relationship. To assess the reliability of our method, we analysed a sample of the automated conflicts with video scoring and found that 74% of these replacements included genuine forms of social displacements. In 10% of the cases, we did not identify social interactions and in the remaining 16% we observed affiliative contacts between the monkeys. We analysed months of daily use of MALT by up to 26 semi-free-ranging Tonkean macaques (Macaca tonkeana) and found that dominance relationships inferred from these interactions strongly correlated with the ones derived from observations of spontaneous agonistic interactions collected during the same time period. An optional filtering procedure designed to exclude chance-driven displacements or affiliative contacts suggests that the presence of 26% of these interactions in data sets did not impair the reliability of this new method. We demonstrate that this method can be used to assess the dynamics of both individual social status, and group-wide hierarchical stability longitudinally with minimal research labour. Further, it facilitates a continuous assessment of dominance hierarchies in captive groups, even during unpredictable environmental or challenging social events, which underlines the usefulness of this method for group management purposes. Altogether, this study supports the use of MALT as a reliable tool to automatically and dynamically assess dominance hierarchy within captive groups of non-human primates, including juveniles, under conditions in which such technology can be used.

Modeling social styles in macaque societies applied to a semi-free-ranging group of Macaca tonkeana

The covariation hypothesis (Thierry 2004) describes conflict management and variations in social structure observed in macaque societies and arranges these species in four dominance styles or grades ranging from egalitarian to despotic. Using an agent-based model (i.e., A-KinGDom), we obtained a set of measurements to quantitatively define the four social styles in captive or semi-free-ranging conditions. Results showed that intensity of aggression was an important parameter involved in the emergence of dominance styles and its level was critical to defining grade 2 (i.e., the second of the two despotic grades described in macaques). In our simulations, grade 2 only appeared using high-intensity aggression values that reflected the phylogenetic origin of despotic grades. Moreover, comparison between simulation results and the data obtained on a semi-free ranging group of Macaca tonkeana (classified as grade 4, or egalitarian) showed the presence of traits close to despotic societies (for example, an increase of gradient of hierarchy or a decrease of reconciliation behaviors). These results both support assigning grade 4 to this macaque species according to its phylogenetic origins and indicate the presence of intra-group variability in semi-free ranging groups of macaques, which in turn yields valuable information of their current social structure and facilitate the handling of these groups. We have developed an agent-based model that drives the emergence of social styles in macaque societies. The results of our simulations suggest that social style in macaques is an emergent behavior and that agent-based models are a good tool for exploring emergent behaviors in silico. Moreover, these models can be used to assess hypotheses on social structure in macaque in semi-free-ranging conditions and report useful knowledge about specific techniques for group handling.

Do primates flexibly use spatio-temporal cues when foraging?

Foraging in seasonal environments can be cognitively demanding. Comparative studies have associated large brain size with a frugivorous diet. We investigated the ability of three semi-free-ranging primate species with different degrees of frugivory (Ntrials: Macaca tonkeana = 419, Macaca fascicularis = 197, Sapajus apella = 346) in developing a mental representation of the spatio-temporal distribution of food using foraging experiments. Forty-two boxes were fixed on trees, and each week ("season"), some of them were filled with fruits which were either highly preferred, or less preferred. Spatial (geometrical panels) and temporal (peel skin of the available fruit) cues were present at each season to indicate where (food location), what (which food) was available, and when. To test the flexible use of the cues in primate foraging behaviour, we first removed the spatial and temporal cues one at a time, and then, we manipulated the "seasonal" order of the available fruit. We compared the foraging performances in the absence and the presence of the cues and during the usual and unusual seasonal order. The average proportion of baited boxes chosen by the subjects in presence of both cues was high (between 73% and 98%) for all species. The primates seemed to remember the spatio-temporal food availability (or used other cues) because no difference was found between trials with or without our spatial and temporal cues. When the usual seasonal pattern was changed, they flexibly adjusted the feeding choice by using the provided temporal cues. We discuss these results also in view of a possible experimental bias.

An understanding of third-party friendships in a tolerant macaque

Complex societies are shaped by social relationships between multiple individuals. The pressure to track these relationships has driven the evolution of social cognition in primates. Importantly, it can be adaptive to track not only personal relationships, but also those established between third-parties. Primates have knowledge about others’ dominance hierarchies and kinship, but we do not know to what extent they also understand friendships. In a playback experiment, Tonkean macaques were presented with simulated conflicts involving third-party female dyads who were established friends or non-friends. Hearing a conflict between friends elicited a stronger behavioural response in listeners (i.e. an increase in looking time) compared to hearing a conflict between non-friends. Conflicts between friends are likely to represent a greater disruption of the social group and structure of the network, and therefore this difference in response may represent an adaptive strategy employed by the macaques to selectively monitor important social interactions in the group. These findings provide evidence that Tonkean macaques (and potentially other primates) can classify the relationships of others based on their degree of friendship and additionally, confirms the important role friendships have within the societies of social primates.

Are monkeys able to discriminate appearance from reality?

The understanding that the perceptual appearance of the environment can differ in several ways from the reality underlies the ability to discriminate appearance from reality. Being able to realize when a misperception can lead us to behave in inappropriate ways confers an evolutionary advantage and may be a prerequisite to develop a Theory of Mind. Understanding that our own perception can differ from reality seems indeed necessary to attribute to others perceptions or beliefs different than ours. This appearance-reality discrimination ability has recently been demonstrated in great apes but no information is currently available regarding this ability in other nonhuman species. In a comparative study, we tested Tonkean macaques (Macaca tonkeana), an Old World primate species, and brown capuchins (Sapajus apella), a New World primate species. We provided monkeys with two experiments using visual illusions of size and quantity to test their ability to discriminate appearance from reality, with an experimental setup similar to the one developed by Krachun et al. (2016) on chimpanzees. A large number of brown capuchins, from different ages and both sexes, as well as two Tonkean macaques succeeded in the two experiments. By ruling out all alternative explanations (i.e. visual tracking or associative learning), our study brings the first evidence that some Old World and New World monkeys are able to discriminate appearance from reality. Our results suggest moving the evolutionary apparition of this cognitive ability earlier in time. Finally, it suggests that humans could share more Theory of Mind components with more nonhuman species than we previously thought.

Where and what? Frugivory is associated with more efficient foraging in three semi-free ranging primate species.

Foraging in seasonal environments can be cognitively challenging. Comparative studies have associated brain size with a frugivorous diet. We investigated how fruit distribution (where) and preference (what) affect foraging decisions in three semi-free ranging primate species with different degrees of frugivory: Macaca tonkeana (Nindiv = 5; Ntrials = 430), M. fascicularis (Nindiv = 3; Ntrials = 168) and Sapajus apella (Nindiv = 6; Ntrials = 288). We used 36 boxes fixed on trees and filled with highly and less preferred fruits with different (weekly) spatio-temporal distributions. Individuals were tested in two conditions: (1) same fruit provided concurrently in the same quantity but in a scattered and in a clumped distribution, (2) highly preferred fruit was scattered while the less preferred was clumped. Generally, primates preferred feeding first on the boxes of the clumped distribution in both conditions, with the more frugivorous species at a higher degree than the less frugivorous species in condition (1), but not (2). Therefore, what fruit was available changed the foraging decisions of the more frugivorous species who also engaged more in goal-directed travel. When feeding on preferred fruit, primates probably maximized foraging efficiency regardless of their degree of frugivory. Our findings emphasize that the food type and distribution may be a preponderant driver in cognitive evolution.