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.

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.

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.

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.

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).

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.

Modelling persistence over generations in biological and cultural evolution based on differential paces of change.

Paces of change are faster in cultural evolution than in biological evolution due to different levels of stability in information storage. This study develops mathematical models to investigate the consequences of differential mutation rates on the ability of groups of information units to survive over many generations. We examined the ability of groups composed of connected units to live on despite the occurrence of deleterious mutations that occur at probabilities ranging from 10-1 to 10-6. It appears that the degree of connection between units should be high enough for groups to persist across generations, but this alone did not ensure their survival; when groups of units were limited in size and subjected to high mutation rates, they did not survive for very long. By contrast, a significant proportion of groups were able to survive numerous generations if mutation rates were low and/or group size was large. The results revealed that the mean number of surviving generations was minimized for certain sizes of groups. When allowing information units to duplicate at each generation, simulation showed that a great number of groups avoided extinction even when mutating at the rate of cultural change if the initial group size was large and the duplication rate was high enough to counteract the consequences of environmental perturbations. The modelling described in this study sets out the conditions under which groups of units can survive along generations. It should serve as a basis for further investigations about the links between processes of biological and cultural changes.

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

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

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

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

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

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

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.

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.

DNA barcoding of reef brittle stars (Ophiuroidea, Echinodermata) from the southwestern Indian Ocean evolutionary hot spot of biodiversity.

In anticipation of the current biodiversity crisis, it has become critical to rapidly and accurately assess biodiversity. DNA barcoding has proved efficient in facilitating the discovery and description of thousands of species and also provides insight into the dynamics of biodiversity. Here, we sequenced a portion of the mitochondrial cytochrome c oxidase subunit I (COI) gene from all morphospecies of reef brittle stars collected during a large-scale biodiversity survey in the southwestern Indian Ocean (SWIO). Three methods of species delineation (Automatic Barcode Gap Discovery, Generalized Mixed Yule Coalescent model, and Bayesian Poisson Tree Processes) showed concordant results and revealed 51 shallow reef species in the region. Mean intraspecific genetic distances (0.005-0.064) and mean interspecific genetic distances within genera (0.056-0.316) were concordant with previous echinoderm studies. This study revealed that brittle-star biodiversity is underestimated by 20% within SWIO and by >40% when including specimens from the Pacific Ocean. Results are discussed in terms of endemism, diversification processes, and conservation implications for the Indo-West Pacific marine biodiversity. We emphasize the need to further our knowledge on biodiversity of invertebrate groups in peripheral areas.

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

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

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.