Part I.Introduction1.Recent developments in primatology and their relevance for studies of Tibetan macaquesLixing Sun, Jin-Hua Li, Cédric Sueur, Paul A. Garber, Claudia Fichtel, and Peter M. KappelerPrimate research has expanded dramatically in many directions in recent decades, especially in exploring evolutionary continuities between nonhuman primates and humans, with major developments in the study of cooperation, culture, social cognition, social dynamics, behavioral economics, as well as with respect to integrating technological advances into routine field work. This chapter summarizes some of these frontiers in primate research to develop a context for the ensuing chapters.Part II.Social Behavior and Dynamics in Tibetan macaques2.The Tibetan macaque as a model for understanding primate behavior and evolutionJin-Hua Li, and Peter KappelerAs our closest relatives, non-human primates share many features with humans in body structure, physiology, genetic constitution, and behavior. Since most primates are long-lived, long-term studies are necessary for understanding their kinship, reproductive strategies, and evolutionary adaptations. Tibetan macaques (Macaca thibetana) are endemic to China. Little information about the species has been available until the 1980s. After a pilot study at Huangshan in 1983, we have investigated the life history, behavior, social relationships, and dynamics of a focus group of Tibetan macaques. We have set up a field station and collected longitudinal data with standard methods. Over the years, more than 150 researchers and students from Japan, the US, Germany, England and Canada have come and conducted their research projects with Chinese researchers. As a result, we now know that Tibetan macaques are the largest of all Macaca species with even sex ratios. Like other macaque species, Tibetan macaques live in a society consisting of multiple males, multiple females and their offspring. Males disperse from their natal groups, but females live within their natal group for life. A linear dominance hierarchy exists both among adult males and adult females. Different from most Macaca species, male Tibetan macaques delay their natal dispersal until early adulthood, and have intensive infant care. There are both competitive and cooperative relationship among group members, especially among males. Mature females do not show cycle changes of sex-skin. Mating occurs all around year, but ejaculation is limited to a period from July to January. Consortship is evident, typically lasting up to ten days. Many of these behavioral features make the Tibetan macaque an ideal model for exploring hypotheses connecting nonhuman primates and humans.3.How social mobility relates to societal stability: a new insight from Tibetan macaques and its implications in human societiesLixing Sun, Dong-Po Xia, and Jin-Hua LiOne of the most fundamental questions in behavioral biology is why societies can persist for a long period of time. While researchers in animal behavior have been hindered by a lack of an aggregate measure to quantify the dynamics of animal societies, researchers in social sciences have been challenged by the complexity and diversity of human societies. As a result, direct empirical evidence is still lacking for the hypothesized causal relationship between social mobility and social stability. Here we attempt to fill the void by examining a much simpler society in the Tibetan macaque (Macaca thibetana), which we have tracked for 30 consecutive years at Huangshan, China. By testing two group-level hypotheses based on benefit-cost analysis and social stratification, we show the first quantitative evidence that an annual 2-to-1 stay/change ratio in the hierarchy with a 3-to-1 upward/downward ratio in intragenerational social mobility provides a substantive expected benefit for adult members to stay in the group and wait for their chances to advance. Using a Markov transition matrix constructed from empirical data, we demonstrate that the current level of social mobility could lead to long-term structural stability in Tibetan macaque society. Furthermore, by zeroing in four group fission events observed during the 30 years, we found that males were far more incentivized than females in initiating group fission for social and sexual opportunities whereas females apparently readapted themselves to the chaotic process of group fission. These findings may shed new light on searching for answers about the biological root causes for such phenomena in human societies as chaos during the turnover of an organization or the balkanization in some regions of the world.4.Internal mechanism for group satiability in Tibetan macaques: behavioural exchange and biological marketsDong-Po Xia, Paul A. Garber, and Cédric SueurTo demonstrate the adaptive mechanisms behind gregariousness and sociality in non-human primates, we have to answer two questions: How gregariousness is shaped by external ecological factors (e.g., food and sleep sites) in natural environment and how to maintain group stability by complex behavioral interactions among individuals (e.g., grooming and copulation). Being highly social with frequent behavioral interactions, Tibetan macaques (Macaca thibetana) are considered to fit well into addressing the later question. In the present study, we focused on the grooming and other social behaviors (e.g., aggression and copulation) to specifically answer the following three questions from the biological market perspective: (1) what kinds of behavioral exchanges are there in Tibetan macaques? (2) How do male and females select grooming partner? (3) What are the roles males and females play in group stability? This study could provide insights into the function of grooming on group stability and imply the behavioral adaptation for group stability and cohesiveness.5.Collective movement and decision making in Tibetan macaquesXi Wang, and Claudia FichtelCollective movement is a behavioral process that allows a group to adapt to its habitat in many social animals. It benefits the animals in many different ways including feeding, defense against predators, and reproduction. However, because the interests and needs of different members of a group are not necessarily the same, collective decisions that allow the group to coordinate their activities become vital. Otherwise, group stability will be weakened and the advantages associated with collective actions will diminish. Consensus decision is one of such mechanisms that allow all members of a social group to reach collective decisions to coordinate their group activities and enhance group stability. It is one of the newest foci in the study of animal behavior. Here we use the Tibetan macaque (Macaca thibetana) at Huangshan as our research subject to exam the interrelationship between its collective movements and decision making. Specifically, we propose to answer the following scientific questions: 1) how a collective decision is initiated, 2) what are the social factors that affect the consensus decision making, 3) how leadership, consensus decision, and group cohesion are interrelated. Therefore, the objectives of our study include elucidating the behavioral characteristics and evolutionary adaptation of consensus decision making in the Tibetan macaque. The results of our study can lead to new scientific findings for the protection and management of social animals. Our study also can provide insights into human social behavior and social coordination, which may be beneficial to improving the efficiency of human organizations and societies.6.Playing around: the significance of juvenile playJessica A. MayhewIn this chapter, I discuss previous work focused on play in captive juvenile gorillas (Gorilla gorilla gorilla) and present preliminary and ongoing play research on the juvenile Tibetan macaques (Macaca thibetana) at Valley of the Wild Monkeys, Mt. Huangshan, China. In primates, juvenile-hood is a prolonged, challenging period of life where juveniles learn to navigate a variety of social interactions and experience multiple contexts. For most species, play is the mechanism by which an individual repeatedly learns about its own physical and social capabilities, collects information about its peers, and refines its behavior. In this special context, relationships are formed, social bonds are strengthened, and mistakes can be made in relative safety. However, the structure and composition of play varies between species, and the costs and benefits (both short- and long-term) are still being deliberated. Because play is often a complex, multi-individual, fast-paced interaction, studying this suite of behaviors is challenging. Therefore, research has been slow to examine how play contributes to the development of socio-cognitive skills, facilitates social learning, or shapes future relationships between group members. Long-term research sites, such as the Valley of the Wild Monkeys, are optimal to study how these early social networks are established and change across the life course.7.The vocal repertoire of Tibetan macaques (Macaca thibetana) and congeneric comparisons Sofia K. BlueVocal repertoires are the essential foundation for studies on vocal communication. From this foundation researchers establish and promote the conformity of terminology, allow researchers to investigate certain calls in more detail, and aid comparative studies by serving as the infrastructure. The following results comprise the first systematic study on the vocalizations of Tibetan macaques (Macaca thibetana). A quantitative analysis was used to assess the vocal repertoire by extracting 30 acoustic parameters from 534 call recordings. Post hoc analyses classified eleven call types: coo, squawk, squeal, noisy scream, growl, bark, compound squeak, leap coo, weeping, modulated tonal scream, and pant. The copulation style of Tibetan macaques is specialized in comparison to the rest of the genus, and this study revealed an acoustically distinct female copulation call that is uncharacteristic of the genus. These calls are shrill undulating calls of a longer duration than the inhale exhale grunts typically observed in female macaques. Further congeneric comparisons revealed that, overall, the repertoires of macaques share a similar set of calls. The main differences are found in the calls emitted within the context of copulations. For Tibetan macaques, a derived female copulation call may be the result of the fact that females display behaviors that are considered rare in primates. For example, adult female Tibetan macaques harass copulatory dyads and show no proceptive behaviors indicative of estrus. Indeed, most of the derived vocalizations in the genus were the copulation calls of species with distinct copulation styles. It is likely that an interplay of phylogenetic, ecological, and social factors have shaped the vocal repertoires across the genus and the emergence of derived calls. 8.A review of Tibetan macaque social structure: female dominance styles, biological markets principles, and male-male social toleranceKrishna N. Balasubramaniam, Hideshi Ogawa, Jin-hua Li, and Carol M. BermanIn nonhuman primates, social structure refers to the patterning and distribution of competitive, cooperative, and conflict-managing interactions among group members. Assessing group social structure is vital since these aspects best capture how individuals realize the tradeoffs of group-living, i.e. maximize its benefits while minimizing its costs. In this chapter, we review our previous studies related to aspects of Tibetan macaque dominance and affiliative social structure, specifically (i) their dominance styles, (ii) market-based affiliative grooming exchange among females, and (iii) the emergence of male-male social tolerance and cooperation. Our research focused on a single group of Tibetan macaques in Mt. Huangshan, China. Our findings revealed that female Tibetan macaques showed many indications of a strict despotic dominance style, characterized by their high degrees of grooming kin bias, and low proportions of both bi-directional aggression and conciliatory tendencies. At the same time, males showed a few indications of a more tolerant style, including higher conciliatory tendencies and frequent ritualistic interactions. Market-based exchange of affiliative grooming behaviors also revealed evidence for a degree of tolerance. Specifically, grooming reciprocity was significant within each of six study-periods and, as predicted by markets frameworks, negatively correlated with the steepness of the dominance hierarchy across these periods. On the other hand, we detected no evidence for the interchange of grooming with a rank-related benefit -- agonistic support. Finally, findings on male-male social relationships revealed that, despite asymmetric dominance relationships and skewed mating success, high-ranking males exhibited certain forms of social tolerance. They did so specifically towards both low-rankers by tolerating them while feeding, and towards potential challengers by forming conservative coalitions. Taken together, these studies offer unique insights into the social structure of Tibetan macaques. While aspects of dominance social structure appear to place this species within the range of other despotic macaques, patterns of affiliative grooming and male-male cooperative exchanges reveal a somewhat more tolerant society. Such unlinked dominance and affiliative relationships indicates a possible influence of both past ancestral or phylogenetic links, and adaptation to current socioecological factors, on Tibetan macaque social structure.Part III. Evolution of rituals: insights from macaque bridging behaviour9.Female-female bridging behaviour in Tibetan macaquesLori K. Sheeran, and Dao ZhangBridging is an affiliative interaction in which two individuals lift an infant between them and lick and/or manipulate the infant's genitals, using the infant as a "bridge" to subsequent social interactions. Male-male bridging has been studied in several macaque (Macaca) species, but female-female bridging has received less focus. Male-male bridging is hypothesized to reduce social tension between bridging individuals, but it may function differently for females. We studied female-female bridging in Tibetan macaques (M. thibetana) from August-September 2014. We predicted that female-female bridging would show distinct patterns when compared to what has been reported for males. We recorded bridging behavior from an ethogram using all-occurrences and focal-animal sampling of eight adult and four subadult females. As has been observed for males, female-female bridges were never immediately followed by aggression, and females used infants as the "bridge" more often than they used juveniles. Unlike what has been reported for males, initiators of female-female bridging dyads were not subordinate to recipients. Female-female bridge initiation rates were correlated with social rank, but there was no significant relationship between bridge reception rates and social rank. Bridge receivers more frequently held infants in female-female bridges, which is significantly different from what has been reported in males. These preliminary results suggest that female-female bridging is related to female interest in infants rather than to the mediation of social tension between individuals, which is the likely function of bridging in adult males.10.Bridging behaviour and male-infant interactions in Macaca assamiensis in Nepal and Thailand: Comparison with those in M. thibetana in ChinaHideshi OgawaI studied social behaviors of Assamese macaques (Macaca assamensis) at Shivapuri-Nagarjun National Park, Kathmandu District, Nepal (27 44'N, 85 17'E, 1300-2100m) from 2014 to 2015, Assamese macaques at Tham Pla Temple, ChiangRai Province, Thailand (20 19'N, 99 51'E, 843m) from 2008 to 2012, and Tibetan macaques (M. thibetana) at Huangshan, Anhui Province, China (30 29'N, 118 11'E, 700-800m) from 1989 to 1993. All study groups were composed of multi-males and multi-females. The macaques were originally wild and free ranging but were provisioned daily and habituated to observers. By focal animal sampling, I observed adult males for 10 hours each in the birth and mating seasons, respectively. During the study periods, males of all macaque groups held an infant in front of another male. However, males of Assamese macaques in Nepal did not show bridging behavior, while males of Assamese macaques in Thailand showed bridging behavior at the frequency of 0.67 (number of behaviors per hour) in the birth season and 0.36 in the mating season, and males of Tibetan macaques in China showed bridging behavior at the frequency of 1.52 in the birth season and 0.08 in the mating season. That is, two adult males of Assamese macaques in Thailand and Tibetan macaques in China lifted an infant together, and sometimes touched or sucked the infant's genitalia. Only adult males of Tibetan macaques in China sucked the penis of another adult male, though adult males of Assamese macaques in Thailand and Tibetan macaques in China sucked the penis of a male infant during bridging behavior and dyadic male-infant interactions. The inter-species and inter-subspecies differences in social behaviors may be affected by the divergence among Assamese macaques in Nepal, Assamese macaques in Thailand, and Tibetan macaques in China.Part IV.Living with microbes, parasites, and disease11.The gut microbiome diversity, sociality, and adaptive evolution in free-ranging Tibetan macaquesBinghua SunA major effort is underway to understand the factors that can influence the distribution of microbial taxa within and among individuals. In general, Individuals acquire gut microbes from their mothers, relatives, mates or close community members and food sources during their lives. However, numerous internal and external factors, such as host genotype, diet, geography, temperature and social interactions, can also influence the gut microbial communities. Despite the existence of numerous studies of the impact of the gut microbiota on human health and disease, much work remains to be done to further our understanding of the host-microbe relationship in wild mammals, particularly under the context of social living. In this study, we took a Tibetan macaque social group as our research subject to study the gut microbiome of these macaques at group level using high-throughput sequencing methods. We attempt to answer the following four questions: (1) what is the microbiome community in a Tibetan macaque's gut composed of? (2) Whether can the community structure (age, sex, and kinship) influence the composition of the gut microbiome community and the structure of a wild Tibetan macaque? (3) How is the gut microbiome influenced by social living? (4) How do the gut microbes respond to the dynamic changes of the food resource? This study may provide a new insight into the adaptive evolution of wild-living primates.12.The influences of ancestral, sociodemographic, and anthropogenic factors on macaque sociality and zoonotic infection riskKrishna N. BlasubramaniamAmong nonhuman primates, sociality may be impacted by both ancestry and various current socioecological factors. Assessing their relative/dynamic effects on the evolution of primate sociality has been a major challenge for researchers. Here I present aspects of my research that focus on examining the impact of phylogenetic relatedness, group size, resource competition, and most recently, anthropogenic factors on primate social structure and/or zoonotic infection risk. In this regard, macaques (genus: Macaca) are an ideal genus, with their similar social organizations and well-established phylogenies, but diverse (despotic-to-tolerant) social styles, geographic ranges, and degrees of overlap with human landscapes. First, I use a comparative approach to reveal that the structure of dominance relationships across macaques shows strong phylogenetic signals, i.e. members of the Sulawesi lineage show more shallow hierarchies and less transitivity/certainty in their dominance networks than those of the Arctoides and/or Fascicularis lineages. In contrast, grooming network structure seems more labile to the influence of group size, with larger groups showing more modular, less dense network connections than smaller groups. Second, I describe contrasting evidence that sociodemographic factors impact within-species differences in macaque sociality. Among free-ranging rhesus macaques, larger group size and/or intense resource competition appear to generate greater degrees of despotism, i.e. more asymmetry in dominance and lower rates of post-conflict affiliation. However, among wild Tibetan macaques, larger group size/severe rangerestriction appeared to lower degrees of despotism, i.e. shallow dominance hierarchies and greater reciprocity in grooming. Thus some aspects of social behavior may be linked to ancestry, whereas others are labile to socioecological and/or supply-and-demand biological markets conditions. My current research is implementing the conceptual framework of coupled-natural-and-human-systems to assess the impact of anthropogenic factors on spatiotemporal variation in macaque social networks. Further, this work is also revealing that human activity may impact the prevalence of zoonotic bacterial pathogens in free-living rhesus macaques, setting the stage for future investigation of the impact of zoonotic infection/transmission on animal social networks and vice versa.13.The medicinal diet of macaques as a parasite control strategy: is there a case for Tibetan macaques?Michael A. Huffman, Binghua Sun, and Jin-Hua LiParasites and pathogens cause a variety of diseases that can affect the behavior and reproductive fitness of an individual, and a variety of behavioral responses to parasitism have been reported. Because the need to counteract such pressure is great, anti-parasitic behaviors are expected to occur throughout the animal kingdom. Indeed, even insects utilize the chemical defenses of plants to protect themselves from parasitoid predators and parasites. A number of anti-parasitic adaptations have also been reported among mammals ranging from bats to bears. It should be no surprise then that primates also have the ability to act in ways that prevent or minimize transmission or control existing parasite infections, often in ways quite similar to other animals. At our current level of understanding, health maintenance and self-medicative behaviors can be classified into four basic levels: 1) optimal avoidance or reduction of the possibility for disease transmission (avoidance of feces contaminated food, water, substrates), 2) the dietary selection of items with a preventative or health maintenance affect (items eaten routinely in small amounts or on a limited basis), 3) ingestion of a substance for the curative treatment or control of a disease, and 5) application of a substance to the body or a living area for the control of disease transmission or a physical condition. In this chapter, we review the plants in the diet of Tibetan macaques and identify the parts that have known medicinal properties. We then compare the plant species and parts that have also been consumed by Japanese macaques and other primates to infer their potential use for self-medication in Tibetan macaques.14.Social network structure and infectious agent risk: insights from Japanese and rhesus macaquesKrishna N. Balasubramaniam, Cedric Sueur, and Andrew J. J. MacIntoshThe risk of acquisition of infectious diseases may be a major cost to social group living in animals. In this regard, social network analytical approaches have been highly useful in modeling the transmission and spread of infectious agents through animal groups and populations. In this chapter, we first we provide a brief overview of those aspects of network structure - e.g. individuals' betweenness- and/or eigenvector centrality in contact affiliation networks, and community sub-structuring or modularity of groups - that may influence infectious agent susceptibility and transmission. We then review findings from our work on both wild Japanese macaques (Macaca fuscata), and captive rhesus macaques (M. mulatta), that reveal how aspects of networks may co-evolve with infectious agent risk. First, possessing strong, central connections in contact-affiliation networks may be (i) detrimental by increasing the likelihood of nematode parasite transmission in wild Japanese macaques, but also (ii) beneficial by socially buffering captive rhesus macaques against susceptibility to infection from enteric bacterial pathogens. Further, in Japanese macaques, increased social grooming with a wider range of partners functions to reduce ectoparasite (lice) loads in winter and summer months. Finally, work on captive rhesus macaques comparing links between microbial phylogenies and social networks is revealing evidence for the contact-mediated sharing of commensal gut E. coli. Such sharing, more easily discernible at the community level, lends support to the recently proposed hypothesis that increased network sub-structuring may present "social bottlenecks" to the network-wide dissemination of parasites. We end by discussing a few avenues of future research, including (1) delineating the host- or parasite-specific factors that may favor social buffering versus contact-mediated transmission, and (2) assessments of the interaction between host biology and social network connections to affect infection risk.Part V. Emerging technologies in primatology 15.iPrimate : insights form technological advances in primatologyAmy R. Klegart, and Agustin FuentesTechnology is pervasive across the Anthropocene and global advances are occurring at a staggering rate. Simultaneously, the second decade of the 21st century finds nearly 60% of living primates threatened or endangered. These threats underscore the pressing need for increased research efficiency and efficacy as rapidly dwindling primate populations worldwide severely limits scientist's opportunities to gain further insight into the evolution of human behavior and society. As technological advances are made, primatologists are incorporating them into their research programs in a variety of ways, leading to emerging new methodologies and new possibilities for the study of both primate behavior as well as primate conservation and management. The technologically diverse toolkits now available to primatologists have 1) increased efficiency in data acquisition and analysis and 2) opened previously inaccessible avenues of inquiry. Such technology-facilitated or augmented approaches to primatology can be used to gain novel insights into both the sustainability and threats facing primates globally, in addition to uncovering patterns that underlie human behavior and society. Here we review some key emerging technologies and how they have already been incorporated into primate research as well as new horizons for those same technologies. Major foci include 1) how cellular and satellite connectivity, cloud-based storage systems, and portable technologies including phones, tablets, laptops, and their associated "apps" facilitate behavioral research, 2) how advances in genetics and genomics can lead to new insights into both primate evolution, behavior, and conservation, and 3) how remote monitoring devices such as GPS collars, video collars, and camera traps can be used to increase our understanding of primate behavior and societies in the light of the current conservation crisis. 16.New imaging technologies for behavioral, cognitive, and medical studies in primatesYong Zhu, and Paul A. GarberCerebral palsy (CP) is a non-progressive movement disorder that occurs in approximately 2-4 of every 1000 live births. Animal models have greatly assisted in understanding the mechanisms of brain injury underlying CP. Although there is no one model that appears to replicate all of the deficits seen in CP due to the many different potential symptoms and underlying causes, each model aims to answer an important aspect of CP. In this study, we created a rhesus macaque model of CP at 6 months of age (approx. 24 human months), and continuing behavior and neurodevelopmental follow-up testing for 20 months (approx. 80 human months). Over the 20 months, behavioral and developmental evaluations were recorded, and the change of cerebral imaging was detected by 9.4T MRI. The results showed that the models showed the change in many measurable behaviors including posture, muscle tension, and movement time. Brain MRI showed bilirubin deposition in the basal ganglia, which supported the pathological changes of the CP models. The results of our study indicate that accurate simulation of the model may provide a scientific platform for research on behavior, pathology, and clinical rehabilitation of human bilirubin CP. More importantly, the new, enhanced imaging technology may have a great potential to be used to study a wider range of primate behavior (especially those in relation to development), in addition to its uses in functional brain imaging.17.Genetic and epigenetics methods in primatology as illustrated in a case study of folate utilizationJian-Yuan ZhaoGenetic diversity is the total number of genetic characteristics in the genetic makeup of a species. It serves as a way for populations to adapt to changing environments. Therefore, describing the genetic diversity in Macaca tibetana is meaningful for us to guarantee the survival of the Tibetan macaque. Under the supervision of Prof. Li, I started my research life from investigating genetic diversity of Tibetan macaque using DNA extracted from fecal samples, and found Tibetan macaque in Huangshan had a very poor genetic diversity with a severe bottleneck effect in evolution. After graduation, I kept my research interest in genetic study and move my research field from genetic diversity in population to genetic variants in disease phenotype. Recently, we found the genetic variant in Fidgetin (FIGN) was associated with the risk of congenital heart disease (CHD), which is the most common human birth defect worldwide. In three independent case-control studies including a total of 1,489 CHD patients and 1,745 controls, we found the +94762G>C (rs2119289) variant in intron 4 of the FIGN gene was associated with significant reduction in CHD susceptibility. Analysis of combined samples indicated that CHD risks in individuals carrying heterozygous (GC) or homozygous (CC) genotypes were reduced by 44% and 66%, respectively, compared to those with the major GG genotype. Minor C allele carriers who had decreased plasma folate levels exhibited significantly increased FIGN expression because the transcription suppressor CREB1 did not bind the alternative promoter of FIGN isoform X3. Mechanistically, increased FIGN expression led to the accumulation of both reduced folate carrier 1 (RFC1) and dihydrofolate reductase (DHFR) via inhibition of their proteasomal degradation, which promoted folate absorption and metabolism. Our results may explain why circulating folate levels do not have a good diagnostic value. Based on our study, I discuss the potential uses of these genetic and epigenetic methods in the study of the behavior, physiology, and conservation of primates in the future.... Mehr
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