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.

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.

Both sheep and goats can solve inferential by exclusion tasks.

Despite the domestication of sheep and goats by humans for several millennia, we still lack comparative data on their cognitive capacity. Comparing the cognitive skills of farm animals can help understand the evolution of cognition. In this study, we compared the performances of sheep and goats in inference by exclusion tasks. We implemented two tasks, namely a cup task and a tube task, to identify whether success in solving the task could be attributed to either low-level mechanisms (avoiding the empty location strategy) or to deductive reasoning (if two possibilities A and B, but not A, then it must be B). In contrast to a previous study comparing goats and sheep in a cup task, we showed that both species solved the inferential condition with high success rates. In the tube task, performances could not be explained by alternative strategies such as avoiding the empty tube or preferring the bent tube. When applying a strict set of criteria concerning responses in all conditions and controlling for the potential effects of experience, we demonstrate that two individuals, a goat and a sheep, fulfil these criteria. This suggests that sheep and goats are able to make inferences based on deductive reasoning.

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.

Characterization of genome-wide microsatellite markers in rabbitfishes, an important resource for artisanal fisheries in the Indo-West Pacific.

Rabbitfishes are reef-associated fishes that support local fisheries throughout the Indo-West Pacific region. Sound management of the resource requires the development of molecular tools for appropriate stock delimitation of the different species in the family. Microsatellite markers were developed for the cordonnier, Siganus sutor, and their potential for cross-amplification was investigated in 12 congeneric species. A library of 792 repeat-containing sequences was built. Nineteen sets of newly developed primers, and 14 universal finfish microsatellites were tested in S. sutor. Amplification success of the 19 Siganus-specific markers ranged from 32 to 79% in the 12 other Siganus species, slightly decreasing when the genetic distance of the target species to S. sutor increased. Seventeen of these markers were polymorphic in S. sutor and were further assayed in S. luridus, S. rivulatus, and S. spinus, of which respectively 9, 10 and 8 were polymorphic. Statistical power analysis and an analysis of molecular variance showed that subtle genetic differentiation can be detected using these markers, highlighting their utility for the study of genetic diversity and population genetic structure in rabbitfishes.

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.

Rovers minimize human disturbance in research on wild animals.

Investigating wild animals while minimizing human disturbance remains an important methodological challenge. When approached by a remote-operated vehicle (rover) which can be equipped to make radio-frequency identifications, wild penguins had significantly lower and shorter stress responses (determined by heart rate and behavior) than when approached by humans. Upon immobilization, the rover-unlike humans-did not disorganize colony structure, and stress rapidly ceased. Thus, rovers can reduce human disturbance of wild animals and the resulting scientific bias.

Resource partitioning in tolerant and intolerant macaques.

The clumped distribution of food resources promotes food defensibility and can lead to the monopolizing of resources by high-ranking individuals. However, the balance of power is set at different levels according to societies, meaning that resource partitioning should vary between them. This study investigates whether dominance asymmetry and resource partitioning are related in non-human primates by comparing two species with contrasting social styles, namely rhesus macaques (Macaca mulatta) which display strong social intolerance and a steep gradient of dominance, and Tonkean macaques (Macaca tonkeana), which exhibit higher levels of tolerance and more balanced dominance relationships. Study groups were kept in semi-free ranging conditions. Animals were provided with fruit in three different clumped conditions during 30-min trials. We found that higher-ranking rhesus macaques had priority for the access to fruit: these individuals spent longer in the feeding area in the first 10-min period of trials, while lower-ranking individuals had diminished access to fruit under the most clumped condition; this was associated with sustained agonistic interactions. Dominance effects were weaker in Tonkean macaques. They exhibited co-feeding between high- and low-ranking individuals in the first period; there was no significant effect of dominance even in the most clumped condition; and frequencies of agonistic interactions remained moderate relative to the number of individuals present in the feeding area. These results show that food resources were more equitably distributed among group members in tolerant macaques than in their intolerant counterparts. Dominance gradient and social tolerance may be considered as two aspects of the same phenomenon.

Informed horses are influential in group movements, but they may avoid leading.

In species that move in cohesive groups, animals generally reach decisions through socially distributed processes, and individual knowledge is expected to influence collective decision making. Pooling of information should not be considered a general rule, however, since conflicts of interest may occur between group members. When resources are limited or highly attractive, higher-ranking individuals can prevent others from accessing food, and subordinates may have an interest in withholding information about its location. We investigated the role individual knowledge may play in recruitment processes in four groups of horses (Equus caballus). Animals were repeatedly released in a food search situation, in which one individual had been informed about the location of a preferred food, while another was a naïve control subject. Horses that were informed about the location of the feeding site were seen to approach the food source more steadily and were followed by a higher number of group members than their uninformed counterparts. Recruitment processes appeared mostly passive. Among the informed subjects, lower-ranking individuals were overall less followed than the higher-ranking ones. Most lower-ranking horses arrived alone at the feeding site. Non-followed informed subjects spent less time in active walk and used direct paths less frequently than followed animals, and they were joined by fewer partners at the attractive food source and spent more time feeding alone. This indicates that the influence of informed individuals on the behavior of other group members was a mixed process. Some horses brought nutritional benefits to their conspecifics by leading them to food supplies, whereas the behavior of others might be functionally deceptive.

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.

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.

Social tolerance in wild female crested macaques (Macaca nigra) in Tangkoko-Batuangus Nature Reserve, Sulawesi, Indonesia.

In primates, females typically drive the evolution of the social system and present a wide diversity of social structures. To understand this diversity, it is necessary to document the consistency and/or flexibility of female social structures across and within species, contexts, and environments. Macaques (Macaca sp.) are an ideal taxon for such comparative study, showing both consistency and variation in their social relations. Their social styles, constituting robust sets of social traits, can be classified in four grades, from despotic to tolerant. However, tolerant species are still understudied, especially in the wild. To foster our understanding of tolerant societies and to assess the validity of the concept of social style, we studied female crested macaques, Macaca nigra, under entirely natural conditions. We assessed their degree of social tolerance by analyzing the frequency, intensity, and distribution of agonistic and affiliative behaviors, their dominance gradient, their bared-teeth display, and their level of conciliatory tendency. We also analyzed previously undocumented behavioral patterns in grade 4 macaques: reaction upon approach and distribution of affiliative behavior across partners. We compared the observed patterns to data from other populations of grade 4 macaques and from species of other grades. Overall, female crested macaques expressed a tolerant social style, with low intensity, frequently bidirectional, and reconciled conflicts. Dominance asymmetry was moderate, associated with an affiliative bared-teeth display. Females greatly tolerated one another in close proximity. The observed patterns matched the profile of other tolerant macaques and were outside the range of patterns of more despotic species. This study is the first comprehensive analysis of females' social behavior in a tolerant macaque species under natural conditions and as such, contributes to a better understanding of macaque societies. It also highlights the relevance of the social style concept in the assessment of the degree of tolerance/despotism in social systems.

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.

Evolutionary history of a widespread Indo-Pacific goby: the role of Pleistocene sea-level changes on demographic contraction/expansion dynamics.

Compared to endemics, widespread species are of particular interest to retrace recent evolutionary history. These species have a large population size which provides a clearer genetic signature of past events. Moreover, their wide geographic range increases the potential occurrence of evolutionary events (expansion, divergence, etc.). Here, we used several coalescent-based methods to disentangle the evolutionary history of a widespread amphidromous goby (Sicyopterus lagocephalus), in the light of sea-level variations during the Pleistocene. Using 75 samples recovered from three biogeographic regions (Western Indian Ocean, Melanesia and Polynesia), we analysed a portion of the cytochromeb gene and confirmed three major haplogroups, each specific to a region. Furthermore, we found that: (1) the Melanesian haplogroup was the oldest while the two peripheral regions hosted daughter haplogroups; (2) two centrifugal colonisation events occurred from Melanesia to the periphery, each synchronised with periods of strong paleo-ENSO episodes; (3) the demographic contraction-expansion events were linked to Pleistocene sea-level changes; (4) Melanesia and Polynesia acted as efficient refuges during the Last Glacial Maximum. These results highlight the importance of studying widespread species to better understand the role of climate changes and paleo-oceanography on the evolution of biodiversity.

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.

Hierarchical steepness, counter-aggression, and macaque social style scale.

Nonhuman primates show remarkable variation in several aspects of social structure. One way to characterize this variation in the genus Macaca is through the concept of social style, which is based on the observation that several social traits appear to covary with one another in a linear or at least continuous manner. In practice, macaques are more simply characterized as fitting a four-grade scale in which species range from extremely despotic (grade 1) to extremely tolerant (grade 4). Here, we examine the fit of three core measures of social style-two measures of dominance gradients (hierarchical steepness) and another closely related measure (counter-aggression)-to this scale, controlling for phylogenetic relationships. Although raw scores for both steepness and counter-aggression correlated with social scale in predicted directions, the distributions appeared to vary by measure. Counter-aggression appeared to vary dichotomously with scale, with grade 4 species being distinct from all other grades. Steepness measures appeared more continuous. Species in grades 1 and 4 were distinct from one another on all measures, but those in the intermediate grades varied inconsistently. This confirms previous indications that covariation is more readily observable when comparing species at the extreme ends of the scale than those in intermediate positions. When behavioral measures were mapped onto phylogenetic trees, independent contrasts showed no significant consistent directional changes at nodes below which there were evolutionary changes in scale. Further, contrasts were no greater at these nodes than at neutral nodes. This suggests that correlations with the scale can be attributed largely to species' phylogenetic relationships. This could be due in turn to a structural linkage of social traits based on adaptation to similar ecological conditions in the distant past, or simply to unlinked phylogenetic closeness.

Where do we stand with the covariation framework in primate societies?

Comparative study of the social systems of macaques has revealed correlated variations between species in multiple social traits such as the asymmetry of dominance relationships, preferential treatment of kin, patterns of aggression and reconciliation, modes of socialization, and access to food resources. Macaques can be classified on a scale of four categories of social styles, ranging from the least to the most tolerant species. This led to the development of the covariation framework, which addresses the constraints responsible for the linkages between social traits, and their consequences on the evolution of primate social systems. Decades of research have provided a wealth of information that supports, complements, expands, or challenges the covariation framework. In this article, I review this body of knowledge and consider covariation in its two aspects, that is, as a pattern and as a hypothesis. I first consider the extent to which social styles can be invariant, the strength of correlations between traits, and the possible extension of the framework to nonhuman primates other than macaques. I then discuss how to formulate hypotheses, identify sources of linkage between traits, make predictions about the effects of social constraints, assess the tolerance dimension of social styles, and consider the breaking of linkages between traits. Whereas socioecological studies aim to understand how adaptation to the ecological environment determines the shape of social systems, the covariation framework is a complementary research program that seeks to unravel the internal processes that restrict or channel change in social behavior.

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.

Studying animal innovation at the individual level: A ratings-based assessment in capuchin monkeys (Sapajus [Cebus] sp.).

Large-scale studies of individual differences in innovative behavior among nonhuman animals are rare because of logistical difficulties associated with obtaining observational data on a large number of innovative individuals across multiple locations. Here, we take a different approach, using observer ratings to study individual differences in innovative behavior in 127 brown capuchin monkeys (Sapajus [Cebus] sp.) from 15 social groups and 7 facilities. Capuchins were reliably rated by 1 to 7 raters (mean 3.2 ± 1.6 raters/monkey) on a 7-point Likert scale for levels of innovative behavior, task motivation, sociality, and dominance. In a subsample, we demonstrate these ratings are valid: Rated innovation predicted performance on a learning task, rated motivation predicted participation in the task, rated dominance predicted social rank based on win/loss aggressive outcomes, and rated sociality predicted the time that monkeys spent in proximity to others. Across all 127 capuchins, individuals that were rated as being more innovative were significantly younger, more social, and more motivated to engage in tasks. Age, sociality, and task motivation all had independent effects on innovativeness, whereas sex, dominance, and group size were nonsignificant. Our findings are consistent with long-term behavioral observations of innovation in wild white-faced capuchins. Observer ratings may, therefore, be a valid tool for studies of animal innovation. (PsycInfo Database Record (c) 2021 APA, all rights reserved).