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The Socioecology of Red-Shanked Doucs (Pygathrix Nemaeus) In THE SOCIOECOLOGY OF RED-SHANKED DOUCS (PYGATHRIX NEMAEUS) IN SON TRA NATURE RESERVE, VIETNAM by LARRY RAY ULIBARRI B.A., University of Northern Colorado, 2002 M.A., University of Colorado at Boulder, 2006 A thesis submitted to the faculty of the Graduate School of the University of Colorado in partial fulfillment of the requirement for the degree of Doctor of Philosophy Department of Anthropology 2013 This thesis entitled: The Socioecology of Red-shanked Doucs (Pygathrix nemaeus) in Son Tra Nature Reserve, Vietnam written by Larry Ray Ulibarri has been approved for the Department of Anthropology Professor Herbert Covert Professor Emeritus Dennis Van Gerven Professor Michelle Sauther Professor Emeritus David Armstrong Professor Barth Wright Date The final copy of this thesis has been examined by the signatories, and we find that both the content and form meet acceptable presentation standards of scholarly work in the above mentioned discipline. iii Ulibarri, Larry Ray (Ph.D., Anthropology) Title: The socioecology of red-shanked doucs in Son Tra Nature Reserve, Vietnam. Dissertation directed by Professor Herbert Covert Abstract This study aimed to gather socioecologic data on the red-shanked doucs (Pygathrix nemaeus) in Son Tra Nature Reserve, Vietnam, over 16 months for the purposes of assisting conservation initiatives of the government of Da Nang City. This included the study of social organization, structure, size, ranging behaviors, activity budget, food choice, selectivity, and dietary quality. These data were compared to transect phenology and weather data. The doucs live in modular societies with stable groups composed of stable units. The average group size was 18 individuals. Groups consisted of an average of 2.7 units with a daily pattern of fission-fusion. The degree of fission-fusion significantly correlates to daily activity budgets, leaf flush, and precipitation. Units always fused overnight. Average unit size was 6.5 individuals. Units were one-male/multi-female and multi-male/multi-female. Adult male to adult female sex ratio was 1:1.63 individuals, and young to adult ratio was 1:1.26 individuals. Home range was 36 ha with a core area of 8 ha. The average daily path length was 509 m, and path length was significantly and negatively correlated with precipitation. Social structures and organization are partly influenced by intergroup contest competition intensified by living in modular societies, ecological constraints including habitat quality and fragmentation, predation, and intragroup scramble competition. The activity budget of all individuals showed that inactivity was most common (35.3%), followed by moving (28.6%), socializing (21.7%), feeding (13.7%) and self-grooming (0.7%). There are a few significant differences in activity budgets between seasons and groups of iv individuals, but more compelling is the relationship between the daily activity budget and the daily pattern of fission-fusion between units. When units are fused they rest significantly more, and when fissioned they move, feed, vocalize, and are vigilant significantly more. This pattern appears to be an adaptation to avoiding intragroup scramble competition and for maintaining contact and coordination between dispersed foraging units. The need for inter-unit coordination may relate to intergroup contest competition and resource defense. The high degree of vocalizations also may relate to intragroup coordination and intergroup contest competition. The feeding budget of all individuals showed that leaves were most frequently selected (87.8%), followed by fruits and seeds (10.2%), flowers (1.6%) and bark/pith (0.4%). Young leaves were selected over mature leaves (68.6%), and whole leaf blades (86.5%) and petioles (13.1%) were more commonly selected leaf parts. Important food species on Son Tra include Parashorea stellata, Parsonsia laevigata, Ipomoea eberhardtii, Garcinia morella, Ficus variegata, Ficus depressa, and Ancistrocladus tectorius. Dietary diversity is low. Young leaves, and fruit and seeds, were not selected according to availability, suggesting that the doucs are selective foragers. Chemical and nutritional content of selected and non-selected leaves, and selected young and selected mature leaves, were not significantly different. The high quality of mature leaves might contribute to the high degree of folivory, suggesting a lack of dietary stresses. These data have been helpful in the planning and implementation of various exhibitions, reforestation efforts, and the building of canopy bridges for the doucs to cross between habitat fragments on Son Tra Nature Reserve. To Ulrike, my wife and Cheridee and Steve, my parents vi Acknowledgments This study was only possible thanks to the incredible support, patience, and dedication of my wife, Ulrike, who is a tremendous source of light and love, and passionate about protecting Son Tra. Very special thanks to my parents, Cheridee and Steve, who supported me throughout my University endeavors. Thanks also to my siblings, Alan, Kristy and Jason for their continued support and encouragement, and to Kristy for editing parts of this thesis. Enormous thanks and gratitude go to my advisor Bert Covert for all of his advice, friendship, and help throughout the years and in writing, and to Valerie McBride who has continued to support me and encourage me when I needed it most. Without the help and support of all of these people, this would not have been. Thanks to my committee members Herbert Covert, Dennis Van Gerven, Michelle Sauther, David Armstrong and Barth Wright for their edits and comments and their support. The study was possible thanks to the collaborative efforts of numerous people. My extended thanks to Tilo Nadler, Director of the Endangered Primate Rescue Center (EPRC), and Ha Thang Long, Frankfurt Zoological Society, Vietnam representative, for their support and advice during research; Huyen Phuoc, former Director of the Department of Science and Technology of Da Nang and current People’s Committee member for his continued support and encouragement; Le Quang Nam and Vu Thi Bich Hau, Director and Deputy Director of the Department of Science and Technology, for their long-time support of the project and continued efforts to protect Son Tra; Thu Minh, Department of Science and Technology staff for her support and friendship; Thai Van Quang, Chief of Technical Division of the Department of Agriculture and Rural Development of Da Nang for his long-time support; Tran Van Luong, Director of Da Nang Forest Protection Department for his efforts to protect Son Tra and support the project; Ho Minh Phuong and Dang Ngoc Kim Trang, Director and senior staff of Son Tra Ecotourism Management Board, for their support and continued conservation efforts; Le Van Nhi and Phan Van Mui, Director and former Vice Director of Son Tra Nature Reserve, and Le Phuoc Bay, FPD head ranger, for their support and efforts to protect Son Tra; Dinh Thi Phuong Anh and Vo Van Minh, Da Nang University Committee Chair and Dean of the Biology Department of Da Nang University for their support; Nguyen Thi Dao, Faculty of Biology at Da Nang University, and Tran Ngoc Toan, botanist, for identifying plant samples; Vu Long from the Institute of Tropical Biology, and Phung Vo Cam Hong from Nong Lam University for their help in testing plant samples; Hoang Minh Duc, Vice Director of the Center of Biodiversity and Development, Vietnam, Van Ngoc Thinh, Central Annamites Coordinator for WWF Vietnam, Vu Ngoc Thang, Faculty of Biology at Hanoi University of Science, Pietro Corsi, Professor, History of Science at University of Oxford, and Thierry Hoquet, Professor, Département de Philosophie at l’Université de Paris for their support and help in addressing parts of this thesis; Gao Nguyen, VTV and film producer, for his friendship and passion to protect Son Tra; Tran Huu Vy, Bui Van Tuan, Nguyen Thi Tinh, and Nguyen Ai Tam for their lively conversation and encouragement; and last but not least, a special thanks to Bui Huy Hoang and Nguyen Hong Chung for their help in field research, and their courage and friendship. The project was made possible thanks to generous contributions made by Margot Marsh Biodiversity Foundation, The Primate Society of Great Britain, the Endangered Primate Conservation Fund, Frankfurt Zoological Society, and private donations from the Streicher and the Ulibarri clans. vii Table of Contents Chapter 1. Introduction and research aims 1 1.1. Introduction 1 1.2. Research aims 6 1.2.1. Concerning social structure/organization 6 1.2.2. Concerning activity budget 8 1.2.3. Concerning feeding ecology 9 1.3. Research significance 10 1.4. Dissertation outline 10 Chapter 2. Review of Pygathrix nemaeus 12 2.1. Introduction 12 2.2. Phylogeny 12 2.2.1. Phylogeny of the Cercopithecidae 12 2.2.2. Phylogeny of the Colobinae 13 2.2.3. Phylogeny of the Presbytini 15 2.2.4. Phylogeny of the odd-nosed colobines 15 2.2.5. Phylogeny and classification of Pygathrix 16 2.3. Biogeography 18 2.4. Descriptions and characteristics 21 2.4.1. Descriptions of Pygathrix 21 2.4.2. Reproduction, development, and care 26 2.4.3. Locomotion 29 2.4.4. Dental morphology 29 2.4.5. Digestive anatomy 30 2.4.5.1. Colobines 30 2.4.5.2. Distinctions in the gut morphology of species of Pygathrix 33 2.5. Distribution, population, and status 33 2.5.1. Distribution 33 2.5.2. Population size and status 42 2.6. Socioecology 43 2.6.1. Approaches in understanding socioecology and feeding ecology 43 2.6.2. Protein, fiber, and tannins 45 2.6.2.1. Protein 46 2.6.2.2. Fiber 46 2.6.2.3. Phenolics and toxins 47 2.7. Diets of colobines 48 2.7.1. Diets of African colobines – general patterns 48 2.7.2. Diets of Asian colobines 50 2.7.2.1. General patterns 50 2.7.2.2. Odd-nosed colobines 51 2.7.2.2.1.
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