Primate Societies Research Articles

Neural signatures of natural behaviour in socializing macaques.

Our understanding of the neurobiology of primate behaviour largely derives from artificial tasks in highly controlled laboratory settings, overlooking most natural behaviours that primate brains evolved to produce1-3. How primates navigate the multidimensional social relationships that structure daily life4 and shape survival and reproductive success5 remains largely unclear at the single-neuron level. Here we combine ethological analysis, computer vision and wireless recording technologies to identify neural signatures of natural behaviour in unrestrained, socially interacting pairs of rhesus macaques. Single-neuron and population activity in the prefrontal and temporal cortex robustly encoded 24 species-typical behaviours, as well as social context. Male-female partners demonstrated near-perfect reciprocity in grooming, a key behavioural mechanism supporting friendships and alliances6, and neural activity maintained a running account of these social investments. Confronted with an aggressive intruder, behavioural and neural population responses reflected empathy and were buffered by the presence of a partner. Our findings reveal a highly distributed neurophysiological ledger of social dynamics, a potential computational foundation supporting communal life in primate societies, including our own.

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.

Aging in Non-Human Primate Society: What Relevance for Social Gerontology?

Wild animals were once thought not to age, as their deaths were viewed as the consequences of constant exposure to the perennial risks of nature. Studies of non-human aging were largely confined to biological investigations, focusing upon short-lived species such as fruit flies, mice and nematodes. Over recent decades, this has changed, and studies of non-human aging have begun to investigate aging taking place in social contexts. The present paper reviews such work on social aging in non-human primate societies. Four themes were evident in seeking potential parallels between human and non-human social aging. These were social disengagement, social bonds or social capital, status rank and dominance, and kinship ties. No studies were found that had explored parent caregiving. The lack of clear evidence that agedness is perceived and recognised within non-human primate groups suggests that most age-associated behavioral changes are at best demi-regularities that map quite imprecisely upon social aging in human societies. However as non-human primate societies are becoming gradually confined to areas and environments established through human agency and human institutions, it is possible to speculate that non-human primate old age will become more common if less natural and as a result, perhaps more akin to social aging in human societies.

Mental health and well-being in primatology: Breaking the taboos.

We hope to raise awareness of mental health and well-being among primatologists. With this aim in mind, we organized a workshop on mental health as part of the main program of the Winter meeting of the Primate Society of Great Britain in December 2021. The workshop was very well received. Here, we review the main issues raised in the workshop, and supplement them with our own observations, reflections, and reading. The information we gathered during the workshop reveals clear hazards to mental health and suggests that we must collectively acknowledge and better manage both the hazards themselves and our ability to cope with them if we are to avert disaster. We call on institutions and learned societies to lead in seeking solutions for the benefit of primatologists and primatology.

Anti-predator strategies of adult male Central Himalayan Langurs (Semnopithecus schistaceus) in response to domestic dogs in a human-dominated landscape.

The evolution of predator-prey relationships is an important topic in primatology. Many aspects of primate society have been explained as a response to predation pressure. While predation has been discussed in broad theoretical terms, few systematically collected data exist on the subject. Furthermore, little information exists regarding the inter-male variation in responses to predators. To address this data gap, predatory dog-primate interactions were studied in a 78-member group of habituated, individually recognized Central Himalayan Langurs (CHL) (Semnopithecus schistaceus) living in a high-altitude subsistence agricultural landscape of northern India. We recorded 312 langur-dog interactions over 2 years. These predation events resulted in 15 serious attacks on adult females, infants, juveniles and sub-adults, in eight of which the prey was killed and consumed on the spot. In response to dog predation, adult males performed three types of anti-predator response behaviors: direct fighting with a predator, emitting alarm calls, fleeing and/or freezing. Differences were noted in each male's response to village dogs. The results showed that the likelihood of CHL adult males engaging in more costly counterattacks or attention getting alarm calls were better predicted by the level of investment in the group (genetic relatedness, duration of residency, social relationships), but not rank and mating rate. Long-duration resident adult males performed high and/or intermediate cost behaviors to protect vulnerable members of the group; their potential offspring, maternal siblings or cousins, and adult female social partners. Short-term residents or recent immigrant males exhibited two less energetically costly, more self-preserving behaviors, depending on their rank: (1) high-ranking short-tenure duration males, with high mating frequencies, performed flee and freeze responses; (2) low-ranking, low-mating-frequency males performed more alarm calls. Counterattacks and alarm calls were performed by adult males with relatively more experience with village dogs and were directed towards dogs with predatory histories significantly more often than dogs with non-predatory histories. Natural selection and kin selection have both contributed to the evolution of CHL anti-predator tactics.

A novel methodological approach for group classification during fission of a semi-free-ranging group of Japanese macaques (Macaca fuscata).

The self-initiated split of a social group, known as fission, is a challenge faced by many group-living animals. The study of group fission and the social restructuring process in real time provides insights into the mechanism of this biologically important process. Previous studies on fission in Japanese macaques (Macaca fuscata) assigned individuals to newly reorganized groups mainly using behavioral observations and group attendance records based on periods before or after fission itself. Here, we present a novel framework for group classification during the process of fission that uses quantifiable behavioral variables and statistical analyses. The framework was tested on a group fission process at Affenberg Landskron (Austria), a park that housed around 160 semi-free-ranging Japanese macaques. The behavioral data were collected for 26 days during fission. We analyzed three behavioral developments recurrent in fissions in Japanese macaques, that is, independence of behavior, participation in group movements, and separation of nomadic ranges. These analyses were combined to assign individuals to different groups. Our study resulted in one main group (N = 33), one subgroup (N = 36) and 56 individuals whose group membership was still undefined. The demographic characteristics of these newly formed groups were comparable with those of fissioned groups in wild populations. Furthermore, we found that these newly forming groups showed early social dynamics of fission five months before group level movements, that is: grouping based on spatial proximity and spatial withdrawal of the subgroup to the periphery. These results underline the validity of our novel framework to study social dynamics in Japanese macaques during the process of fission. It represents an important addition to existing methods, and we recommend testing its scope in other primate societies.

Fission-fusion dynamics in a wild group of Japanese macaques (Macaca fuscata) on Kinkazan Island caused by the repeated separation of an alpha male being followed by females.

The spatiotemporal cohesion of a group is an essential element of primate society. It is thus important to clarify the factors that influence the extent of variation in spatial cohesion and individual membership in a group over time, known as fission-fusion dynamics. During the mating season of 2019, the alpha male (TY) in a wild group of Japanese macaques on Kinkazan Island repeatedly disappeared from the group, and we observed fission-fusion dynamics caused by his movement. The group seemed to have split when TY left the group or its home range, and females who followed him had the most affiliative relationships with TY or were the relatives of those females. Although TY disappeared from the group in the post-mating season, these fission-fusion dynamics only occurred during the mating season probably because females had a more substantial need for protection against aggression from the other males during the mating season. These results indicate that, although rare, fission-fusion dynamics based on affiliative relationships between males and females can occur with the separation of alpha males from the group. More studies in other populations are needed to clarify the influence of group males on the spatial cohesion of groups.

Social complexity as a driving force of gut microbiota exchange among conspecific hosts in non-human primates.

The emergent concept of the social microbiome implies a view of a highly connected biological world, in which microbial interchange across organisms may be influenced by social and ecological connections occurring at different levels of biological organization. We explore this idea reviewing evidence of whether increasing social complexity in primate societies is associated with both higher diversity and greater similarity in the composition of the gut microbiota. By proposing a series of predictions regarding such relationship, we evaluate the existence of a link between gut microbiota and primate social behavior. Overall, we find that enough empirical evidence already supports these predictions. Nonetheless, we conclude that studies with the necessary, sufficient, explicit, and available evidence are still scarce. Therefore, we reflect on the benefit of founding future analyses on the utility of social complexity as a theoretical framework.

Female countertactics to male feticide and infanticide in a multilevel primate society

AbstractThe occurrence of male feticide and/or infanticide represents an extreme case of sexual conflict: an adaptive strategy of male reproduction at the expense of females. Females are predicted to develop numerous countertactics; however, it has remained unclear whether countertactics can effectively shift the balance which likely depends on the social and mating system. We conducted a 15-year, detailed observation of female and male behavior during male replacement in free-ranging golden snub-nosed monkeys (Rhinopithecus roxellana) of a multilevel society. We have identified several potential countertactics against feticide and/or infanticide, including pregnant or lactating females staying with ousted males or transferring to stay with the ousted male after being attacked, which lead to 2 of 11 fetuses succumbing to feticide, and extra-unit mating, female joint defense and transferring with their infants to other social units, which lead to 6 of 34 infants succumbing to infanticide. Female joint defenses crucially delay infanticide, providing mothers the opportunity to transfer with their vulnerable infants to another social unit where they have previously mated with the male leader or where they have female relatives. Importantly, in response to mothers starting to transfer, some males cease attacking infants, a change in behavior that is likely to be beneficial to males because during their tenures they can sire future offspring of the mothers who remain. Our findings show how dynamic interactions between males and females can be and how the conditions in multilevel societies can shift the outcome of intersexual conflict from males to females.

Social connections predict brain structure in a multidimensional free-ranging primate society.

Reproduction and survival in most primate species reflects management of both competitive and cooperative relationships. Here, we investigated the links between neuroanatomy and sociality in free-ranging rhesus macaques. In adults, the number of social partners predicted the volume of the mid–superior temporal sulcus and ventral-dysgranular insula, implicated in social decision-making and empathy, respectively. We found no link between brain structure and other key social variables such as social status or indirect connectedness in adults, nor between maternal social networks or status and dependent infant brain structure. Our findings demonstrate that the size of specific brain structures varies with the number of direct affiliative social connections and suggest that this relationship may arise during development. These results reinforce proposed links between social network size, biological success, and the expansion of specific brain circuits.

Maternal caretaking behavior towards a dead juvenile in a wild, multi-level primate society

Maternal caretaking and transport of dead infants are widespread among nonhuman primates, having been reported in numerous species of monkeys and apes. By contrast, accounts of such behaviors toward dead juveniles are scarce. Here, we describe responses by the mother and other group members to the death of a juvenile in a wild, multi-level group of Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Following the juvenile’s fatal accident, his mother transported and cared for the corpse for four days. Immature monkeys belonging to the same one-male unit, and some individuals from other social units also showed interest in and tended the corpse. Comparisons of this case with those involving the deaths of infants and an adult female in the same population highlight possible effects of physiological, psychological and emotional factors in primate thanatological responses, and provide an additional perspective on the origin and evolution of compassionate acts.

Invasion and defense of the basic social unit in a nonhuman primate society leads to sexual differences in the gut microbiome.

Multilevel society is one of the most complex social systems in natural ecosystems and is a typical feature among some primates. Given the potential connection between social behavior and gut microbiome composition, the multilevel social system could affect the primate gut microbiome. Here, based on long‐term observation (e.g. social unit dynamics, transfer, and behavior), we investigated this potential integrating 16S rRNA gene amplicon sequencing and behavior data in Yunnan snub‐nosed monkeys (Rhinopithecus bieti), which possess a multilevel social group based on one male units (OMUs, each unit with several breeding females and their offspring) and all‐male unit (AMU, several bachelor males residing together). We found that the mean unweighted Unifrac distance between adult males from different OMUs was significantly lower than that between adult females from different OMUs (paired Wilcoxon test, P = 0.007). There was no significant difference in the mean unweighted Unifrac distance between females within the same OMU or between females from different OMUs. These findings indicated the potential connection between the defense and invasion of social units and the gut microbiome community in wild Yunnan snub‐nosed monkeys. We speculated that the resident males of OMUs displaying a significantly higher similarity in the gut microbial community than that of adult females in separate OMUs might be associated with the sexual differences in their interactions and from previously having cohabitated together in the AMU. Therefore, this study suggested that multilevel societies might have an effect on the gut microbial community in this wild nonhuman primate species.

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.

First report of a leopard (Panthera pardus)\u2013bonobo (Pan paniscus) encounter at the LuiKotale study site, Democratic Republic of the Congo

Predation is a major cause of mortality in non-human primates, and considered a selective force in the evolution of primate societies. Although larger body size is considered as protection against predation, evidence for predation on great apes by carnivores comes from chimpanzees (Pan troglodytes), gorillas (Gorilla gorilla), and orangutans (Pongo spp.). Here, we describe the first encounter between wild bonobos (Pan paniscus) and a leopard (Panthera pardus). A single leopard was confronted by a group of habituated bonobos for three hours. Two adult males and one adolescent female bonobo actively harassed the leopard, which remained still for most of the encounter and reacted only to close approaches by bonobos. While no predation was observed, their behaviours confirm that bonobos perceive leopards as potential predators. Our report adds novel information to descriptions from other African ape species, and sheds light on the behavioural repertoire of bonobos’ anti-predation strategies. For future investigations, we suggest tagging leopards to remotely monitor their movements and allow assessment of encounter rates as one of several factors influencing predation pressure.

Advocacy and Activism as Essential Tools in Primate Conservation.

Primates are facing a global extinction crisis driven by an expanding human population, environmental degradation, the conversion of tropical forests into monocultures for industrial agriculture and cattle ranching, unsustainable resource extraction, hunting, climate change, and the threat of emerging zoonotic diseases. And, although many primate scientists have dedicated their careers to conservation, 65% of primate species are listed as Vulnerable, Endangered, or Critically Endangered, and >75% are experiencing a population decline. Projections indicate that by the end of the century, an additional 75% of the area currently occupied by wild primates will be lost to agriculture. Clearly, we are losing the battle and must change business-as-usual if we are to protect wild primates and their habitats. This article is a call to action. Primate societies and their membership need to expand their engagement in scientific advocacy and scientific activism designed to educate, inspire, organize, and mobilize global citizens to join together, lobby business leaders and politicians in both primate habitat countries and in consumer nations, boycott forest-risk products, participate in demonstrations and letter writing campaigns, and use social media to effect transformational change. We are the experts, and the more we and our professional organizations drive the public policy debate on wildlife conservation and environmental justice, the more successful we will be in protecting the world’s primates from extinction. The time to act is now!

Correction to: Kin bias and male pair-bond status shape male-male relationships in a multilevel primate society

Correction to: Kin bias and male pair-bond status shape male-male relationships in a multilevel primate society

Kin bias and male pair-bond status shape male-male relationships in a multilevel primate society

Male-male social relationships in group-living mammals vary from fierce competition to the formation of opportunistic coalitions or the development of long-lasting bonds. We investigated male-male relationships in Guinea baboons (Papio papio), a species characterized by male-male tolerance and affiliation. Guinea baboons live in a multi-level society, with units of one reproductively active “primary” male, 1–6 females, and offspring at the core level. Together with “bachelor” males, several units form a party, and 2–3 parties constitute a gang. We aimed to clarify to which degree male relationship patterns varied with relatedness and pair-bond status, i.e., whether males had primary or bachelor status. Data were collected from 24 males in two parties of Guinea baboons near Simenti in the Niokolo-Koba National Park in Senegal. Males maintained differentiated and equitable affiliative relationships (“strong bonds”) with other males that were stable over a 4-year period, irrespective of their pair-bond status. Remarkably, most bachelor males maintained strong bonds with multiple primary males, indicating that bachelor males play an important role in the cohesion of the parties. A clear male dominance hierarchy could not be established due to the high degree of uncertainty in individual rank scores, yet bachelor males were more likely to be found at the low end of the dominance hierarchy. Average relatedness was significantly higher between strongly bonded males, suggesting that kin biases contribute to the social preferences of males. Long-term data will be needed to test how male bonds affect male tenure and ultimately reproductive success.Significance statementMales living in social groups may employ different strategies to increase their reproductive success, from fierce fighting to opportunistic alliance formation or the development of long-term bonds. To shed light on the factors that shape male strategies, we investigated male-male social relationships in the multilevel society of Guinea baboons (Papio papio) where “primary” males are associated with a small number of females and their offspring in “units” while other males are “bachelors.” Strong bonds occurred among and between primary and bachelor males and strongly bonded males were, on average, more closely related. Bachelor males typically had multiple bond partners and thus play an important role in the fabric of Guinea baboon societies. Across primate species, neither dispersal patterns nor social organization clearly map onto the presence of strong bonds in males, suggesting multiple routes to the evolution of male bonds.

COVID-19と学会大会の運営

COVID-19と学会大会の運営

Vocal convergence in a multi-level primate society: insights into the evolution of vocal learning.

The extent to which nonhuman primate vocalizations are amenable to modification through experience is relevant for understanding the substrate from which human speech evolved. We examined the vocal behaviour of Guinea baboons, Papio papio, ranging in the Niokolo Koba National Park in Senegal. Guinea baboons live in a multi-level society, with units nested within parties nested within gangs. We investigated whether the acoustic structure of grunts of 27 male baboons of two gangs varied with party/gang membership and genetic relatedness. Males in this species are philopatric, resulting in increased male relatedness within gangs and parties. Grunts of males that were members of the same social levels were more similar than those of males in different social levels (N = 351 dyads for comparison within and between gangs, and N = 169 dyads within and between parties), but the effect sizes were small. Yet, acoustic similarity did not correlate with genetic relatedness, suggesting that higher amounts of social interactions rather than genetic relatedness promote the observed vocal convergence. We consider this convergence a result of sensory–motor integration and suggest this to be an implicit form of vocal learning shared with humans, in contrast to the goal-directed and intentional explicit form of vocal learning unique to human speech acquisition.

Music as a coevolved system for social bonding.

Why do humans make music? Theories of the evolution of musicality have focused mainly on the value of music for specific adaptive contexts such as mate selection, parental care, coalition signaling, and group cohesion. Synthesizing and extending previous proposals, we argue that social bonding is an overarching function that unifies all of these theories, and that musicality enabled social bonding at larger scales than grooming and other bonding mechanisms available in ancestral primate societies. We combine cross-disciplinary evidence from archeology, anthropology, biology, musicology, psychology, and neuroscience into a unified framework that accounts for the biological and cultural evolution of music. We argue that the evolution of musicality involves gene-culture coevolution, through which proto-musical behaviors that initially arose and spread as cultural inventions had feedback effects on biological evolution because of their impact on social bonding. We emphasize the deep links between production, perception, prediction, and social reward arising from repetition, synchronization, and harmonization of rhythms and pitches, and summarize empirical evidence for these links at the levels of brain networks, physiological mechanisms, and behaviors across cultures and across species. Finally, we address potential criticisms and make testable predictions for future research, including neurobiological bases of musicality and relationships between human music, language, animal song, and other domains. The music and social bonding hypothesis provides the most comprehensive theory to date of the biological and cultural evolution of music.