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.

Eyeblink rate as an indicator of concentration on grooming in Japanese macaques (Macaca fuscata).

In primates, social relationships with a high frequency of social grooming are referred to as "affiliate relationships," "friendship," "bonding," and are described as involving positive emotion. However, the psychological state during social grooming has not been fully understood. In this study, I focused on blinking as a behavior that reflects psychological state during grooming in Macaca fuscata, a nonhuman wild primate, and examined for the first time whether the blink rate reflects concentration on social grooming. To test this hypothesis, I focused on ectoparasite removals during social grooming with the following three predictions: (1) blinks are synchronized with breakpoints (when monkeys can release visual attention) of mouthing ectoparasites during grooming, (2) the blink rate is lower during grooming (when requiring visual concentration) than during resting (when no visual concentration is required), and (3) the lower the blink rate during grooming (supposedly in high concentration), the higher the frequency of ectoparasites removals (outputs of the task). I recorded the faces of 10 wild female Japanese macaques on Kinkazan Island, Miyagi Prefecture, with video, while they were resting and grooming, and recorded the timing and frequency of eyeblink and ectoparasite removals. All three predictions were supported, suggesting that the blink rate during grooming can be an indicator of concentration on grooming in nonhuman primates. Whether grooming concentration is associated with an affiliative relationship with the grooming partner is an issue that should be carefully examined in future studies, but eyeblink studies may provide new perspectives for understanding the psychological state of individuals during grooming in a noninvasive manner.

Association between stress and bilateral symmetrical alopecia in free-ranging Formosan macaques in Mt. Longevity, Taiwan.

Since 2013, a high incidence of bilateral symmetrical alopecia has been observed in free-ranging Formosan macaques (Macaca cyclopis) in Mt. Longevity, Taiwan. We hypothesized that stress induces alopecia in this population. To verify our hypothesis, we evaluated the histopathological characteristics of skin biopsy and used a validated enzyme immunoassay (EIA) for fecal glucocorticoid metabolite (FGM) analysis, which act as an indicator of stress experienced by the individual. Follicular densities were lower (2.1-3.0 mm2) in individuals with symmetrical alopecia than in those with normal hair conditions (4.7 mm2). Furthermore, anagen to catagen/telogen ratios were lower in individuals with alopecia (0-1.4) than in those with normal hair (4.0). The histopathological characteristics of alopecia were similar to those of telogen effluvium, which indicates that stress is one of the possible etiologies. On the basis of the analytical and biological validation of EIAs for FGM analysis, 11ß-hydroxyetiocholanolone was considered suitable for monitoring adrenocortical activity in both sexes of Formosan macaques. The mean concentrations (standard error; sample size) of 11ß-hydroxyetiocholanolone were 2.02 (0.17; n = 10) and 1.41 (0.10; n = 31) µg/g for individuals with and without alopecia, respectively. Furthermore, the results of logistic regression analysis show that 11ß-hydroxyetiocholanolone (p = 0.012) concentration was positively associated with alopecia. Thus, stress was the most likely to trigger symmetrical alopecia in Formosan macaques in Mt. Longevity. Although stress can decrease the fitness of an individual, considering the population status of Formosan macaques in Taiwan is stable and alopecia was only observed in our study area, which is isolated from other populations, the impact on the total population of Formosan macaque in Taiwan is limited. Nonetheless, stress-induced immunosuppression and alopecia might affect the local abundance and increase zoonosis risk due to frequent human-macaque contact in Mt. Longevity. Future studies are suggested to focus on the causative factor of stress and the effects of stress and alopecia on the health and welfare in the Formosan macaques.

The adaptive value of probability distortion and risk-seeking in macaques' decision-making.

In humans, the attitude toward risk is not neutral and is dissimilar between bets involving gains and bets involving losses. The existence and prevalence of these decision features in non-human primates are unclear. In addition, only a few studies have tried to simulate the evolution of agents based on their attitude toward risk. Therefore, we still ignore to what extent Prospect theory's claims are evolutionarily rooted. To shed light on this issue, we collected data from nine macaques that performed bets involving gains or losses. We confirmed that their overall behaviour is coherent with Prospect theory's claims. In parallel, we used a genetic algorithm to simulate the evolution of a population of agents across several generations. We showed that the algorithm selects progressively agents that exhibit risk-seeking, and has an inverted S-shape distorted perception of probability. We compared these two results and found that monkeys' attitude toward risk is only congruent with the simulation when they are facing losses. This result is consistent with the idea that gambling in the loss domain is analogous to deciding in a context of life-threatening challenges where a certain level of risk-seeking behaviour and probability distortion may be adaptive. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

Non-human primate token use shows possibilities but also limitations for establishing a form of currency.

Non-human primates evaluate choices based on quantitative information and subjective valuation of options. Non-human primates can learn to value tokens as placeholders for primary rewards (such as food). With those tokens established as a potential form of 'currency', it is then possible to examine how they respond to opportunities to earn and use tokens in ways such as accumulating tokens or exchanging tokens with each other or with human experimenters to gain primary rewards. Sometimes, individuals make efficient and beneficial choices to obtain tokens and then exchange them at the right moments to gain optimal reward. Sometimes, they even accumulate such rewards through extended delay of gratification, or through other exchange-based interactions. Thus, non-human primates are capable of associating value to arbitrary tokens that may function as currency-like stimuli, but there also are strong limitations on how non-human primates can integrate such tokens into choice situations or use such tokens to fully 'symbolize' economic decision-making. These limitations are important to acknowledge when considering the evolutionary emergence of currency use in our species. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

Non-human primates use combined rules when deciding under ambiguity.

Decision outcomes in unpredictable environments may not have exact known probabilities. Yet the predictability level of outcomes matters in decisions, and animals, including humans, generally avoid ambiguous options. Managing ambiguity may be more challenging and requires stronger cognitive skills than decision-making under risk, where decisions involve known probabilities. Here we compare decision-making in capuchins, macaques, orangutans, gorillas, chimpanzees and bonobos in risky and ambiguous contexts. Subjects were shown lotteries (a tray of potential rewards, some large, some small) and could gamble a medium-sized food item to obtain one of the displayed rewards. The odds of winning and losing varied and were accessible in the risky context (all rewards were visible) or partially available in the ambiguous context (some rewards were covered). In the latter case, the level of information varied from fully ambiguous (individuals could not guess what was under the covers) to predictable (individuals could guess). None of the species avoided gambling in ambiguous lotteries and gambling rates were high if at least two large rewards were visible. Capuchins and bonobos ignored the covered items and gorillas and macaques took the presence of potential rewards into account, but only chimpanzees and orangutans could consistently build correct expectations about the size of the covered rewards. Chimpanzees and orangutans combined decision rules according to the number of large visible rewards and the level of predictability, a process resembling conditional probabilities assessment in humans. Despite a low sample size, this is the first evidence in non-human primates that a combination of several rules can underlie choices made in an unpredictable environment. Our finding that non-human primates can deal with the uncertainty of an outcome when exchanging one food item for another is a key element to the understanding of the evolutionary origins of economic behaviour. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

The identification of effective welfare indicators for laboratory-housed macaques using a Delphi consultation process.

Despite the importance for both animal welfare and scientific integrity of effective welfare assessment in non-human primates, there has been little or no consensus as what should be assessed. A Delphi consultation process was undertaken to identify the animal- and environment-based measures of welfare for laboratory-housed macaques and to determine their relative importance in on-site welfare assessments. One-hundred fifteen potential indictors were identified through a comprehensive literature search, followed by a two-round iterative electronic survey process to collect expert opinion. Stable group response and consensus about the validity, reliability, and feasibility of the proposed indicators (67.5% agreement) was achieved by the completion of Round Two. A substantially higher proportion of environment-based measures (72%: n = 44/61) were considered as valid, reliable, and feasible compared to the animal-based measures (22%: n = 12/54). The indicators that ranked most highly for assessing welfare were the presence of self-harm behaviours and the provision of social enrichment. This study provides an empirical basis upon which these indicators can be validated and then integrated into assessment tools developed for macaques and emphasises the need to include both animal- and environment-based indicators for accurate welfare monitoring.

A causal role for frontal cortico-cortical coordination in social action monitoring.

Decision-making via monitoring others' actions is a cornerstone of interpersonal exchanges. Although the ventral premotor cortex (PMv) and the medial prefrontal cortex (MPFC) are cortical nodes in social brain networks, the two areas are rarely concurrently active in neuroimaging, inviting the hypothesis that they are functionally independent. Here we show in macaques that the ability of the MPFC to monitor others' actions depends on input from the PMv. We found that delta-band coherence between the two areas emerged during action execution and action observation. Information flow especially in the delta band increased from the PMv to the MPFC as the biological nature of observed actions increased. Furthermore, selective blockade of the PMv-to-MPFC pathway using a double viral vector infection technique impaired the processing of observed, but not executed, actions. These findings demonstrate that coordinated activity in the PMv-to-MPFC pathway has a causal role in social action monitoring.

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.

Recurrent circuit dynamics underlie persistent activity in the macaque frontoparietal network.

During delayed oculomotor response tasks, neurons in the lateral intraparietal area (LIP) and the frontal eye fields (FEF) exhibit persistent activity that reflects the active maintenance of behaviorally relevant information. Despite many computational models of the mechanisms of persistent activity, there is a lack of circuit-level data from the primate to inform the theories. To fill this gap, we simultaneously recorded ensembles of neurons in both LIP and FEF while macaques performed a memory-guided saccade task. A population encoding model revealed strong and symmetric long-timescale recurrent excitation between LIP and FEF. Unexpectedly, LIP exhibited stronger local functional connectivity than FEF, and many neurons in LIP had longer network and intrinsic timescales. The differences in connectivity could be explained by the strength of recurrent dynamics in attractor networks. These findings reveal reciprocal multi-area circuit dynamics in the frontoparietal network during persistent activity and lay the groundwork for quantitative comparisons to theoretical models.

The importance of first impression judgements in interspecies interactions.

Close human-wildlife interactions are rapidly growing, particularly due to wildlife tourism popularity. Using both laboratory and ecological observation studies we explored potential interspecies communication signalling mechanisms underpinning human-animal approach behaviour, which to date have been unclear. First impression ratings (n = 227) of Barbary macaques' social and health traits were related to the macaques' facial morphology and their observed behaviour supporting a shared facial signalling system in primates. These ratings significantly predicted intended approach to the macaques during hypothetical interactions. Finally, real-world interspecies proximity was observed and found to be best predicted by the interaction between human first impression perception and animal behaviour. Specifically, perceived macaque health in interaction with actual macaque dominance drives close interactions despite human proclivity to avoid dominant animals, raising safety concerns in interspecies interactions.

Complex patterns of grooming and sexual activity in Barbary macaques (Macaca sylvanus).

Grooming in primates is often considered a "currency" that can be exchanged for other "services" or "commodities" such as reciprocal grooming, coalitionary support, infant handling, tolerance around food sources, active food sharing, or mating opportunities. Previous studies on primate grooming-for-sex exchange viewed the males as the demanding class, with the females as suppliers of mating opportunities. In this study, we examine the broader context of grooming-for-mating exchange in Barbary macaques in Gibraltar. Our data show that Barbary macaque males groom females with whom they are mating more frequently and for longer periods than other females, and the relationship between grooming and mating remains significant in both sexual and nonsexual contexts. In addition, females groomed males with whom they were mating more frequently and for longer periods than other males. In both sexes, grooming was observed to be far more frequent and to occur for longer durations in sexual compared to nonsexual contexts. We did not find any difference in grooming behavior between presexual and postsexual contexts. Our data suggest that there is no simple model to describe Barbary macaque grooming patterns in sexual contexts. Although our results are partly consistent with male use of grooming as payment for mating, broadly assessed grooming-mating patterns cannot be solely explained by a male-driven grooming-for-mating exchange.

A connectional hub in the rostral anterior cingulate cortex links areas of emotion and cognitive control.

We investigated afferent inputs from all areas in the frontal cortex (FC) to different subregions in the rostral anterior cingulate cortex (rACC). Using retrograde tracing in macaque monkeys, we quantified projection strength by counting retrogradely labeled cells in each FC area. The projection from different FC regions varied across injection sites in strength, following different spatial patterns. Importantly, a site at the rostral end of the cingulate sulcus stood out as having strong inputs from many areas in diverse FC regions. Moreover, it was at the integrative conjunction of three projection trends across sites. This site marks a connectional hub inside the rACC that integrates FC inputs across functional modalities. Tractography with monkey diffusion magnetic resonance imaging (dMRI) located a similar hub region comparable to the tracing result. Applying the same tractography method to human dMRI data, we demonstrated that a similar hub can be located in the human rACC.

Behavioral screening tools for identifying autism in macaques: existing and promising tests.

Autism is a behaviorally defined neurodevelopmental disease characterized by social communication and social interaction deficits, as well as repetitive behaviors and restricted interests. Although the causes of autism are extremely complex, involving genes, environments and gene-environment interactions, genetic mutations are the important risk factors. For this reason, preclinical research is now shifting into focusing on generating transgenic and knockout models, especially using macaques, which are the closest relatives to humans. In spite of unique advantages of macaques over rodents in both functionally specialized brain structures and highly sophisticated social behaviors, the limited availability of phenotype screening tools restricts their translational utility. Here, this review focuses specially on behavioral phenotyping assays for macaque models of autism. In the first part, the existing behavioral tests are discussed, and the second part is devoted to some few, in our view, very promising tests of new developments. In years to come, we should develop macaque models with high construct validity, improve face validity by designing more specialized behavioral screening tools, strengthen collaborative efforts between rodent and macaque models, and ultimately translate the results from animal models into human clinical trials.

Social networks predict immigration success in wild Japanese macaques.

Male migration is common in mammals and comes with associated benefits and costs. Male-male affiliative relationships are behavioural strategies that migrating males can adopt in order to maximise benefits and minimize costs. While we know that such strategies primarily serve to reduce tension, little is known about how they actually affect male immigration success. We investigated the influence of male-male affiliative relationships on immigration success in a group of wild Japanese macaques (Macaca fuscata). We used social network analysis to examine the distribution of male-male affiliative interactions and their association with immigration success. We found that visiting males with high eigenvector centralities and low weighted degree centralities were more likely to be integrated into the group. Other factors such as season, age-class, and dominance rank amongst visiting males did not affect male integration success. Our results suggest that strong male affiliative bonds and a centralized position within the male-male grooming network can predict future integration success of visiting males into a social group through promoting higher tolerance of resident males and reducing aggression risks.

Measuring personality in the field: An in situ comparison of personality quantification methods in wild Barbary macaques (Macaca sylvanus).

Three popular approaches exist for quantifying personality in animals: behavioral coding in unconstrained and experimental settings and trait assessment. Both behavioral coding in an unconstrained setting and trait assessment aim to identify an overview of personality structure by reducing the behavioral repertoire of a species into broad personality dimensions, whereas experimental assays quantify personality as reactive tendencies to particular stimuli. Criticisms of these methods include that they generate personality dimensions with low levels of cross-study or cross-species comparability (behavioral coding in unconstrained and experimental settings) or that the personality dimensions generated are not ecologically valid, that is, not reflecting naturally occurring behavior (trait assessment and experimental assays). Which method is best for comparative research is currently debated, and there is presently a paucity of personality research conducted in wild subjects. In our study, all three described methods are used to quantify personality in a wild animal subject, the Barbary macaque (Macaca sylvanus). Our results show that the structures generated by unconstrained behavioral coding and trait assessment were not equivalent. Personality dimensions derived from both trait assessments and experimental assays demonstrated low levels of ecological validity, with very limited correlation with behaviors observed in nonmanipulated circumstances. Our results reflect the methodological differences between these quantification methods. Based on these findings and the practical considerations of wild animal research, we suggest future comparative studies of quantification methods within similar methodological frameworks to best identify methods viable for future comparisons of personality structures in wild animals. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Bridging may help young female Tibetan macaques Macaca thibetana learn to be a mother.

Attraction to infants is a common feature of non-human primates. Frequent affiliative male-infant interactions have been observed in many multimale, multifemale groups of macaques, including a behaviour termed 'bridging' in which two male macaques simultaneously lift an infant. This behaviour has been suggested to serve as a positive affiliative interaction between the adult or subadult males. Female macaques display bridging in the same manner as males, but the function of this behaviour to females remains unknown. In this study, we examined evidence for the function and evolution of bridging in female Tibetan macaques within the framework of three hypotheses: the learning to mother, a side-effect of selection for appropriate maternal care, and alliance formation hypotheses. Our results showed that subadult females initiated more bridging than adult females. Females preferred to use infants for bridging when the infants were less than four weeks old. Female frequency of received bridging with higher-ranking females was not significantly different from their frequency of received bridging with lower-ranking females. Bridging frequency was not significantly different between dyads composed of related and unrelated females. Additionally, post-bridging grooming frequency was significantly higher than nonbridging grooming interactions, suggesting a social function for bridging. The results of our study supported the 'learning to mother' hypothesis, suggesting that bridging among female intrasexual dyads is a multi-functional, complex and differential evolutionary process.

Comparative Investigations of Social Context-Dependent Dominance in Captive Chimpanzees (Pan troglodytes) and Wild Tibetan Macaques (Macaca thibetana).

Theoretical definitions of dominance, how dominance is structured and organized in nature, and how dominance is measured have varied as investigators seek to classify and organize social systems in gregarious species. Given the variability in behavioral measures and statistical methods used to derive dominance rankings, we conducted a comparative analysis of dominance using existing statistical techniques to analyze dominance ranks, social context-dependent dominance structures, the reliability of statistical analyses, and rank predictability of dominance structures on other social behaviors. We investigated these topics using behavioral data from captive chimpanzees (Pan troglodytes) and wild Tibetan macaques (Macaca thibetana). We used a combination of all-occurrence, focal-animal, and instantaneous scan sampling to collect social, agonistic, and associative data from both species. We analyzed our data to derive dominance ranks, test rank reliability, and assess cross-context predictability using various statistical analyses. Our results indicate context-dependent dominance and individual social roles in the captive chimpanzee group, one broadly defined dominance structure in the Tibetan macaque group, and high within-context analysis reliability but little cross-context predictability. Overall, we suggest this approach is preferable over investigations of dominance where only a few behavioral metrics and statistical analyses are utilized with little consideration of rank reliability or cross-context predictability.

Playing it cool: Characterizing social play, bout termination, and candidate play signals of juvenile and infant Tibetan macaques (Macaca thibetana).

Play behaviors and signals during playful interactions with juvenile conspecifics are important for both the social and cognitive development of young animals. The social organization of a species can also influence juvenile social play. We examined the relationships among play behaviors, candidate play signals, and play bout termination in Tibetan macaques (Macaca thibetana) during juvenile and infant social play to characterize the species play style. As Tibetan macaques are despotic and live in groups with strict linear dominance hierarchies and infrequent reconciliation, we predicted that play would be at risk of misinterpretation by both the individuals engaged in the play bout and by those watching, possibly leading to injury of the players. Animals living in such societies might need to frequently and clearly signal playful intent to play partners and other group members to avoid aggressive outcomes. We gathered video data on 21 individually-identified juvenile and infant macaques (one month to five years of age) from the Valley of the Wild Monkeys, Mt. Huangshan, China. We used all-occurrence sampling to record play behaviors and candidate play signals based on an ethogram. We predicted that play groups would use multiple candidate play signals in a variety of contexts and in association with the number of audience members in proximity to the players and play bout length. In the 283 playful interactions we scored, juvenile and infant macaques used multiple body and facial candidate play signals. Our data showed that juvenile and infant Tibetan macaques use a versatile repertoire of play behaviors and signals to sustain play.