The Behavioral Ecology of the Tibetan Macaque (Fascinating Life Sciences)

This open access book summarizes the multi-disciplinary results of one of China’s main primatological research projects on the endemic Tibetan macaque (__Macaca thibetana__), which had continued for over 30 years, but which had never been reported on systematically. Dedicated to this exceptional Old World monkey, this book makes the work of Chinese primatologists on the social behavior, cooperation, culture, cognition, group dynamics, and emerging technologies in primate research accessible to the international scientific community. __One of the most impressive Asian monkeys, and the largest member of its genus, the Tibetan macaque deserves to be better known. This volume goes a long way towards bringing this species into the spotlight with many excellent behavioral analyses from the field.__ - **Frans de Waal, Professor of Psychology, Emory University, USA**. __Macaques matter. To understand primate patterns and trends, and to gain important insight into humanity, we need to augment and expand our engagement with the most successful and widespread primate genus aside from Homo. This volume focuses on the Tibetan macaque, a fascinating species with much to tell us about social behavior, physiology, complexity and the macaque knack for interfacing with humans. This book is doubly important for primatology in that beyond containing core information on this macaque species, it also reflects an effective integrated collaboration between Chinese scholars and a range of international colleagues—exactly the type of collaborative engagement primatology needs. This volume is a critical contribution to a global primatology.__ - **Agustín Fuentes, Professor of Anthropology, University of Notre Dame, USA**. __I have many fond memories of my association with Mt. Huangshan research beginning in 1983, when together with Professor Qishan Wang we established this site. It is such a beautiful place and I miss it. It is gratifying to see how far research has progressed since we began work there, becoming more internationalized and very much a collaborative endeavor under the long-term direction of Professor Jin-Hua Li and colleagues. This book highlights the increased interest in this species, representing a variety of disciplines ranging from macro aspects of behavior, cognition and sociality, to micro aspects of microbes, parasites and disease, authored by a group of renowned Chinese and international primatologists. I applaud their efforts and expect more interesting work to come from this site in the years ahead.__ - **Kazuo Wada, Professor Emeritus, Kyoto University, Japan**. Foreword 7 Preface 9 Acknowledgments 11 Contents 12 List of Contributors 14 Part I: Introduction 16 Chapter 1: Recent Developments in Primatology and Their Relevance to the Study of Tibetan Macaques 17 1.1 Recent Trends and Developments in Primatology 18 1.2 Why Macaques, Especially Tibetan Macaques? 19 1.3 A Short History of Tibetan Macaque Research 21 1.4 Tibetan Macaques at Mt. Huangshan Research Site 22 References 24 Part II: Social Behavior and Dynamics in Tibetan Macaques 28 Chapter 2: Social and Life History Strategies of Tibetan Macaques at Mt. Huangshan 29 2.1 Introduction 29 2.2 Long-term Study of Tibetan Macaques at Mt. Huangshan 30 2.3 Social Life History Strategies 33 2.3.1 The Largest Macaca 33 2.3.2 Medium-Sized Group with Even Adult Sex Ratios 34 2.3.3 A Rich Repertoire of Affiliative and Ritualized Behaviors 34 2.3.4 Despotic Dominance Style 36 2.3.5 Reproductive Pattern with Year-Round Mating but Seasonal Births 37 2.4 Potential Contributions to Understanding Behavioral Mechanisms in Primate Societies 39 2.4.1 Bridge and Bond Role of Infant 39 2.4.2 Male-Female Friendships in a Promiscuous Mating System 40 2.4.3 Competitive and Cooperative Relationships Among Males 41 2.4.4 Behavioral Mechanism Promoting Genetic Diversity in a Small Group 41 2.5 Conclusions 42 Appendix I 43 Appendix II 44 References 56 Chapter 3: Size Matters in Primate Societies: How Social Mobility Relates to Social Stability in Tibetan and Japanese Macaques 59 3.1 Introduction 59 3.2 Social Mobility and Opportunity 61 3.3 Social Mobility and Social Stability 62 3.4 Measuring Social Mobility in Primate Societies 63 3.5 Results: Social Mobility in Tibetan and Japanese Macaques 65 3.6 Discussion 66 References 70 Chapter 4: Behavioral Exchange and Interchange as Strategies to Facilitate Social Relationships in Tibetan Macaques 72 4.1 Introduction 72 4.2 Exchange Between the Same Behaviors 75 4.2.1 Grooming for Itself 75 4.3 Exchange Between Different Behaviors 76 4.3.1 Grooming for Tolerance 76 4.3.2 Grooming for Infant Handling 81 4.3.3 Agonistic Support for Copulation 82 4.4 Conclusions 84 References 85 Chapter 5: Social Relationships Impact Collective Decision-Making in Tibetan Macaques 89 5.1 Introduction 89 5.2 Collective Decision-Making in Tibetan Macaques 92 5.2.1 A Macaque Species for Studying Decision-Making 92 5.2.2 Decision-Making During the Initiation Process of Group Movements 92 5.2.3 Decision-Making During the Joining Process of Group Movements 94 5.3 Social Relationship and Collective Decision-Making 97 5.4 Conclusions 99 References 99 Chapter 6: Considering Social Play in Primates: A Case Study in Juvenile Tibetan Macaques (Macaca thibetana) 103 6.1 Introduction 103 6.2 Play Behavior: An Overview 104 6.3 Macaque Play 107 6.4 Tibetan Macaques 108 6.5 Study Subjects and Data Collection 110 6.5.1 Maternal Allogrooming and Dominance Rank 110 6.5.2 Juvenile Play Behavior 111 6.5.3 Statistical Analyses 112 6.6 Results 113 6.6.1 Player Age 114 6.6.2 Number of Players 115 6.6.3 Player Composition 115 6.6.4 Matrilineal Relatedness and Rank 115 6.6.5 Maternal Social Relationships 115 6.6.6 Individual Playfulness 116 6.7 Discussion 118 6.7.1 Does Social Position Matter? 120 6.7.2 Future Considerations 122 References 124 Chapter 7: The Vocal Repertoire of Tibetan Macaques (Macaca thibetana) and Congeneric Comparisons 128 7.1 Introduction 128 7.2 Measuring Vocal Complexity 129 7.2.1 Vocal Repertoire Size 129 7.2.2 Identifying Homologous and Derived Calls 129 7.3 Understanding the Evolution of Vocal Complexity 130 7.4 Methods 131 7.4.1 Categories of Call Production 131 7.4.2 Exploring Vocal Homologs and Derived Calls in the Genus Macaca 132 7.4.3 Comparisons with Tibetan Macaques and Phylogenetic, Social, and Ecological Factors 133 7.5 Results 135 7.5.1 Homologous and Derived Calls in the Genus 135 7.5.2 Comparisons with the Vocal Repertoire of Tibetan Macaques 135 7.5.3 Potential Effects of Phylogeny, Sociality, and Ecology 139 7.6 Discussion 142 7.6.1 The Tibetan Macaque Vocal Repertoire 143 7.6.2 Phylogenetic, Social, and Ecological Factors Influencing Macaque Vocal Repertoires 144 7.7 Conclusions 145 References 146 Chapter 8: Tibetan Macaque Social Style: Covariant and Quasi-independent Evolution 149 8.1 Introduction: Primate Sociality and Social Structure 149 8.2 The Macaques and the Study of Variation in Social Structure 151 8.3 Tibetan Macaques and the YA1 Group 154 8.4 Evidence of Female Despotism Contradicts Earlier Studies 155 8.5 Males Exhibit Social Tolerance Despite Evidence for Despotism 157 8.6 Comparative Studies Provide Evidence for Both Covariation and Quasi-independent Evolution 159 8.7 Discussion and Future Directions 165 References 171 Part III: Evolution of Rituals: Insights from Bridging Behavior 178 Chapter 9: Preliminary Observations of Female-Female Bridging Behavior in Tibetan Macaques (Macaca thibetana) at Mt. Huangshan... 179 9.1 Introduction 179 9.2 Methods 181 9.3 Results 185 9.4 Discussion 190 References 192 Chapter 10: Bridging Behavior and Male-Infant Interactions in Macaca thibetana and M. assamensis: Insight into the Evolution o... 194 10.1 Introduction 194 10.2 Methods 195 10.2.1 Study Sites and Study Periods 195 10.2.1.1 Western Assamese Macaque (M. a. pelops) 195 10.2.1.2 Assamese macaque (M. a. assamensis or M. a. pelops) 196 10.2.1.3 Eastern Assamese Macaque (M. a. assamensis) 197 10.2.1.4 Tibetan Macaque (M. thibetana) 197 10.2.2 Sampling Methods 197 10.2.3 Definition of Behavior 198 10.3 Results 199 10.3.1 Bridging Behavior 199 10.3.2 Dyadic Male-Infant Interactions 201 10.3.3 Penis Sucking Between Adult Males 203 10.4 Discussion 203 10.5 Summary 206 References 206 Part IV: Living with Microbes, Parasites, and Diseases 209 Chapter 11: The Gut Microbiome of Tibetan Macaques: Composition, Influencing Factors and Function in Feeding Ecology 210 11.1 Introduction 210 11.2 Gut Microbiome of Tibetan Macaque 213 11.2.1 Composition of Gut Bacteria 213 11.2.2 Composition of Gut Fungi 214 11.3 Factors Affecting the Gut Microbiome in Tibetan Macaques 215 11.3.1 Affects of Age, Sex, and Season on Gut Bacterial Microbiome 215 11.3.2 Gut Fungal Microbiome Affected by Age, Sex, and Season 216 11.4 Functions of the Gut Microbiome in Tibetan Macaque Feeding Ecology 216 11.4.1 Gut Bacterial Microbiome and the Feeding Ecology of Tibetan Macaques 217 11.4.2 Gut Fungal Microbiome and Feeding Ecology of Tibetan Macaques 219 11.5 Conclusions and Future Directions 220 References 221 Chapter 12: Medicinal Properties in the Diet of Tibetan Macaques at Mt. Huangshan: A Case for Self-Medication 226 12.1 Introduction 226 12.2 Materials and Methods 229 12.3 Results and Discussion 231 12.3.1 Plant Food Species and Their Relative Density (RD) Values 231 12.3.2 Medicinal Foods in the Diet 235 12.3.3 Seasonality of Medicinal Food Ingestion 238 12.3.4 Antiparasitic Properties 238 12.3.5 Reproductive Modulation 239 12.3.6 Stress Reduction 241 12.4 Future Research 243 Appendix: Plant Secondary Metabolites in Plant Items Ingested by Tibetan Macaques at Mt. Huangshan 245 References 245 Chapter 13: Primate Infectious Disease Ecology: Insights and Future Directions at the Human-Macaque Interface 252 13.1 Introduction 252 13.2 Primate Infectious Disease Ecology 254 13.3 Human-Macaque Interfaces 256 13.4 Parasites at Human-Macaque Interfaces 259 13.5 The Future of Human-Macaque Disease Ecology 267 13.6 Conclusions 276 References 277 Part V: Emerging Technologies in Primatology 288 Chapter 14: MRI Technology for Behavioral and Cognitive Studies in Macaques In Vivo 289 14.1 Introduction 289 14.2 Magnetic Resonance Imaging (MRI) 291 14.2.1 Background of MRI 291 14.2.2 The Advantages of MRI 292 14.2.3 State of the Art at High Field MRI 292 14.3 In Vivo MRI Study in Macaques 293 14.3.1 Structural MRI in Brain Imaging Study 294 14.3.2 Functional MRI in Brain Imaging Study 297 14.4 Conclusion 298 References 299 This open access book summarizes the multi-disciplinary results of one of China’s main primatological research projects on the endemic Tibetan macaque ( Macaca thibetana ), which had continued for over 30 years, but which had never been reported on systematically. Dedicated to this exceptional Old World monkey, this book makes the work of Chinese primatologists on the social behavior, cooperation, culture, cognition, group dynamics, and emerging technologies in primate research accessible to the international scientific community. One of the most impressive Asian monkeys, and the largest member of its genus, the Tibetan macaque deserves to be better known. This volume goes a long way towards bringing this species into the spotlight with many excellent behavioral analyses from the field. - Frans de Waal, Professor of Psychology, Emory University, USA . Macaques matter. To understand primate patterns and trends, and to gain important insight into humanity, we need to augment and expand our engagement with the most successful and widespread primate genus aside from Homo. This volume focuses on the Tibetan macaque, a fascinating species with much to tell us about social behavior, physiology, complexity and the macaque knack for interfacing with humans. This book is doubly important for primatology in that beyond containing core information on this macaque species, it also reflects an effective integrated collaboration between Chinese scholars and a range of international colleagues—exactly the type of collaborative engagement primatology needs. This volume is a critical contribution to a global primatology. - Agustín Fuentes, Professor of Anthropology, University of Notre Dame, USA . I have many fond memories of my association with Mt. Huangshan research beginning in 1983, when together with Professor Qishan Wang we established this site. It is such a beautiful place and I miss it. It is gratifying to see how far research has progressed since we began work there, becoming more internationalized and very much a collaborative endeavor under the long-term direction of Professor Jin-Hua Li and colleagues. This book highlights the increased interest in this species, representing a variety of disciplines ranging from macro aspects of behavior, cognition and sociality, to micro aspects of microbes, parasites and disease, authored by a group of renowned Chinese and international primatologists. I applaud their efforts and expect more interesting work to come from this site in the years ahead. - Kazuo Wada, Professor Emeritus, Kyoto University, Japan . This open access book summarizes the multi-disciplinary results of one of Chinas main primatological research projects on the endemic Tibetan macaque (Macaca thibetana), which had continued for over 30 years, but which had never been reported on systematically. Dedicated to this exceptional Old World monkey, this book makes the work of Chinese primatologists on the social behavior, cooperation, culture, cognition, group dynamics, and emerging technologies in primate research accessible to the international scientific community. One of the most impressive Asian monkeys, and the largest member of its genus, the Tibetan macaque deserves to be better known. This volume goes a long way towards bringing this species into the spotlight with many excellent behavioral analyses from the field.- Frans de Waal, Professor of Psychology, Emory University, USA. Macaques matter. To understand primate patterns and trends, and to gain important insight into humanity, we need to augment and expand our engagement with the most successful and widespread primate genus aside from Homo. This volume focuses on the Tibetan macaque, a fascinating species with much to tell us about social behavior, physiology, complexity and the macaque knack for interfacing with humans. This book is doubly important for primatology in that beyond containing core information on this macaque species, it also reflects an effective integrated collaboration between Chinese scholars and a range of international colleagues--exactly the type of collaborative engagement primatology needs. This volume is a critical contribution to a global primatology. - Agustín Fuentes, Professor of Anthropology, University of Notre Dame, USA. I have many fond memories of my association with Mt. Huangshan research beginning in 1983, when together with Professor Qishan Wang we established this site. It is such a beautiful place and I miss it. It is gratifying to see how far research has progressed since we began work there, becomi ng more internationalized and very much a collaborative endeavor under the long-term direction of Professor Jin-Hua Li and colleagues. This book highlights the increased interest in this species, representing a variety of disciplines ranging from macro aspects of behavior, cognition and sociality, to micro aspects of microbes, parasites and disease, authored by a group of renowned Chinese and international primatologists. I applaud their efforts and expect more interesting work to come from this site in the years ahead.- Kazuo Wada, Professor Emeritus, Kyoto University, Japan Front Matter ....Pages i-xvi Front Matter ....Pages 1-1 Recent Developments in Primatology and Their Relevance to the Study of Tibetan Macaques (Lixing Sun, Jin-Hua Li, Cédric Sueur, Paul A. Garber, Claudia Fichtel, Peter M. Kappeler)....Pages 3-13 Front Matter ....Pages 15-15 Social and Life History Strategies of Tibetan Macaques at Mt. Huangshan (Jin-Hua Li, Peter M. Kappeler)....Pages 17-46 Size Matters in Primate Societies: How Social Mobility Relates to Social Stability in Tibetan and Japanese Macaques (Lixing Sun, Dong-Po Xia, Jin-Hua Li)....Pages 47-59 Behavioral Exchange and Interchange as Strategies to Facilitate Social Relationships in Tibetan Macaques (Dong-Po Xia, Paul A. Garber, Cédric Sueur, Jin-Hua Li)....Pages 61-77 Social Relationships Impact Collective Decision-Making in Tibetan Macaques (Xi Wang, Claudia Fichtel, Lixing Sun, Jin-Hua Li)....Pages 79-92 Considering Social Play in Primates: A Case Study in Juvenile Tibetan Macaques (Macaca thibetana) (Jessica A. Mayhew, Jake A. Funkhouser, Kaitlin R. Wright)....Pages 93-117 The Vocal Repertoire of Tibetan Macaques (Macaca thibetana) and Congeneric Comparisons (Sofia K. Blue)....Pages 119-139 Tibetan Macaque Social Style: Covariant and Quasi-independent Evolution (Krishna N. Balasubramaniam, Hideshi Ogawa, Jin-Hua Li, Consuel Ionica, Carol M. Berman)....Pages 141-169 Front Matter ....Pages 171-171 Preliminary Observations of Female-Female Bridging Behavior in Tibetan Macaques (Macaca thibetana) at Mt. Huangshan, China (Grant J. Clifton, Lori K. Sheeran, R. Steven Wagner, Jake A. Funkhouser, Jin-Hua Li)....Pages 173-187 Bridging Behavior and Male-Infant Interactions in Macaca thibetana and M. assamensis: Insight into the Evolution of Social Behavior in the sinica Species-Group of Macaques (Hideshi Ogawa)....Pages 189-203 Front Matter ....Pages 205-205 The Gut Microbiome of Tibetan Macaques: Composition, Influencing Factors and Function in Feeding Ecology (Binghua Sun, Michael A. Huffman, Jin-Hua Li)....Pages 207-222 Medicinal Properties in the Diet of Tibetan Macaques at Mt. Huangshan: A Case for Self-Medication (Michael A. Huffman, Bing-Hua Sun, Jin-Hua Li)....Pages 223-248 Primate Infectious Disease Ecology: Insights and Future Directions at the Human-Macaque Interface (Krishna N. Balasubramaniam, Cédric Sueur, Michael A. Huffman, Andrew J. J. MacIntosh)....Pages 249-284 Front Matter ....Pages 285-285 MRI Technology for Behavioral and Cognitive Studies in Macaques In Vivo (Yong Zhu, Paul A. Garber)....Pages 287-299