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The Behavioral Ecology of the Tibetan Macaque
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Their [Tibetan macaques’] flat, broad, bearded faces provide perhaps the most humanlike countenance I have ever seen in a monkey… . Apart from chimpanzees, I had never seen primate males so intensely involved with each other. In chimpanzees, too, males are at the same time rivals and friends, and I would argue the same for human males .
—Frans de Waal,The Ape and the Sushi Master (2001)
Mystery surrounded Tibetan macaques for a long time, even for experts. The species was not identified until the last third of the nineteenth century, and nothing more than its geographic distribution and external characters were known for the next hundred years. It was long referred to as Père David’s macaque, a rather odd name in reference to the French missionary and naturalist Father Armand David, who first collected the species. Moreover, the current name, Tibetan macaque, is misleading since the species is typically found in east-central China and not within the boundaries of Tibet. This is due to the fact that Père David initially located the species at a place close to the Sino-Tibetan border of his time.
We had to wait until the 1980s to see Mount Emei and Mount Huangshan come to light on the primatology map. This is where Qikun Zhao and Ziyun Deng from the Kunming Institute of Zoology and Qishan Wang and Jinhua Li from Anhui University began to study the behavior and life history of Tibetan macaques, definitively adding a new dimension to the macaque landscape. I still have the reprints of their publications in my bibliography, some written in Chinese. The works of Hideshi Ogawa, Carol Berman, and a new generation of primatologists soon followed. Now appears this multi-authored volume entirely devoted to the Tibetan macaque. This combined effort of two dozen scientists to review 40 years of research and present new findings about a single species should be viewed as a celebration of the species. It frees Tibetan macaques from the purgatory of scientific papers scattered across various journals and collections to join the small club of primate species that are honored with this attention. Many people would consider that brown monkeys like Tibetan macaques all look similar. Although they do not have the immediate visual appeal of more brightly colored primates, brown monkeys have different but equally attractive assets. With their fiery gaze and prominent beards, Tibetan macaques are no exception, and their adaptations and behaviors attract a great deal of research interest.
As scientists we are expected to test hypotheses and theories. Some of the contributors to this book do so, addressing broad issues such as cooperative strategies, social dynamics, collective decisions, feeding ecology, and pathogen transmission. They use Tibetan macaques as a model to investigate mainstream research questions in the field of behavioral ecology and evolution. Every animal species has its singularities, however, and deserves to be studied for itself. This is why other contributors seek to identify what makes Tibetan macaques special, investigating patterns such as social play, call types, or the fascinating “bridging” interactions in which infants play a role as buffers to reduce tension between adults. Science generally values the testing of general theories more than the humble seeking of what gives a species its own touch. In the end, however, both of these approaches are necessary. Years ago, I was struggling to rank the different species of macaque according to their levels of social tolerance. Quantitative measures were available in a limited number of species and I had to rely on qualitative data for others. I remember asking Qikun Zhao about the behaviors particular to Tibetan macaques at a conference held in Japan in 1996. I was trying to guess their social style, i.e., their own touch. This resulted in a tentative scaling of macaque species which would later be amended when quantitative data became available in Tibetan macaques. It should be emphasized that the story is far from over. As discussed in the book, why and to what extent the different behavioral traits constituting social styles may covary during the evolutionary process still remains to be elucidated. I am delighted to see how the study of the particular meets the general by yielding new perspectives and hypotheses to be tested.
As the editors point out, this book should not be considered an end, but rather a beginning. This highlighting of research into Tibetan macaques has the potential to strengthen Chinese primatology and favor its development at the national and international level. It may in turn help the Tibetan macaques. Like other species of non-human primates, their populations are threatened by the loss and fragmentation of their habitat. Admiring, knowledge, and conservation should go hand in hand to save the future of this unique species.
This book is mainly based on research papers presented in a spirited international primatology symposium held in the scenic area of Mt. Huangshan, China, in the summer of 2017. The chapters were grouped into five logical parts. Part I consists of a single chapter, which offers a brief introduction to recent developments in Chinese primatology and a short history of research on the primates of China in general and the Tibetan macaque in particular.
Part II contains seven chapters (Chaps. 2 – 8 ) focusing on social behavior and social dynamics in Tibetan macaques. In Chap. 2 , Jin-Hua Li and Peter M. Kappeler provide a comprehensive review of three decades of field research in Tibetan macaques at the Valley of Monkeys, highlighting the significance of this species as a model for understanding broader questions in primate behavior and evolution. Lixing Sun, Dong-Po Xia, and Jin-Hua Li follow up in Chap. 3 by introducing a new way to analyze the dynamics of macaque social hierarchy from a social mobility perspective with new insights unveiled through comparing Tibetan macaques with Japanese macaques. In Chap. 4 , Dong-Po Xia, Paul A. Garber, Cédric Sueur, and Jin-Hua Li look into the internal behavioral mechanisms promoting group stability in Tibetan macaque from a behavioral exchange and biological market point of view. In Chap. 5 , Xi Wang, Claudia Fichtel, Lixing Sun, and Jin-Hua Li investigate how Tibetan macaques make collective decisions during group movements. In Chap. 6 , Jessica A. Mayhew, Jake A. Funkhouser, and Kaitlin R. Wright explore the significance of play behavior in the development of social cognition in juvenile Tibetan macaques. This chapter is followed by Sofia K. Blue’s analysis of vocal communication in Chap. 7 , which generates insights from comparing Tibetan macaques with other macaque species. In Chap. 8 , Krishna N. Balasubramaniam, Hideshi Ogawa, Jin-Hua Li, Consuel Ionica, and Carol M. Berman offer a comprehensive review of Tibetan macaque’s social structure, with insights from their previous work on social styles, comparative studies with other macaque species, and male–male social tolerance.
Part III contains two highly focused studies about ritualized behavior of Tibetan macaques with the implication about how culture evolves. In Chap. 9 , Grant J. Clifton, Lori K. Sheeran, R. Steven Wagner, Jake A. Funkhouser, and Jin-Hua Li examine how infants are used for the regularly observed behavior of bridging between adult females. This is further pursued in Chap. 10 , where Hideshi Ogawa compares bridging behavior in two populations ofMacaca assamensis , which are then compared with Tibetan macaques to explore the evolutionary origins of this highly ritualized behavior.
Part IV is composed of four chapters, focusing on how Tibetan macaques live with microbes, parasites, and diseases. In Chap. 11 , Binghua Sun, Michael A. Huffman, and Jin-Hua Li take us into the microbial world inside the gut of Tibetan macaques and show how microbes adapt to the social behavior of the species. Then, Michael A. Huffman, Binghua Sun, and Jin-Hua Li present data in Chap. 12 to test the hypothesis that the diet of Tibetan macaques may incorporate self-medicative aspects to better survive in their environment, a proposition that has never been examined in this species before. Broadening the scope in Chap. 13 , Krishna N. Balasubramaniam, Cédric Sueur, Michael A. Huffman, and Andrew J. J. MacIntosh review previous work on infectious agents at human–macaque interfaces and offer several key future directions for research in this area.
Many recent discoveries in primatology involve technological advancements in research, which is the content of Part V. In a single chapter (Chap. 14 ), Yong Zhu and Paul A. Garber explore the great potential of the high field MRI technology in the study of primate behavior and cognition. While promising, this new imaging technology has several obvious limitations at present.
All in all, the contributors of this volume examine a broad range of topics about the behavioral ecology of the Tibetan macaque. Although data are still far from adequate and some conclusions are tentative, we hope this volume will help remove the Tibetan macaque from the list of little known primate species. We expect that the information presented here can stimulate further comparative study of behavioral, ecological, and evolutionary questions about macaques and other primates and hope that this contribution will facilitate the integration of Chinese primatology into the mainstream field.
This volume is based mainly on the research papers presented during the 2017 International Primatological Symposium at Mt. Huangshan, China. The National Natural Science Foundation of China sponsored the meeting and also provided funding to support open access publication of this volume, as well as the publishing fund of Hefei Normal University. Hefei Normal University also provided a fund to defray the cost of publication including book purchase. We are grateful to all the contributors for sharing their work, without which the timely publication of this volume would have been impossible.
All the chapters in the volume were peer reviewed and benefited from the sharp comments and constructive suggestions by colleagues who generously donated their time and offered professional help. We are particularly thankful for the following external reviewers: Filippo Aureli, Louise Barrett, Fred Bercovitch, Marco Gamba, Andrew King, Daoying Lan, Bonaventura Majolo, Nadine Müller, Charles Nunn, Paula Pebsworth, Odile Petit, Gabriele Schino, Masaki Shimada, Wencheng Song, Bernhard Thierry, Kazuo Wada, Qi Wu, and Hongyi Yang. We also thank Rose Amrhein who offered language help for most of the chapters. We are lucky to have Srinivasan Manavalan as our in-house editor who oversaw the book project from the beginning to the end and answered all of our questions and inquiries throughout the process.
April 2019