Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2009 Determinants of modular societies in snub-nosed monkeys (Rhinopithecus bieti) and other Asian colobines Grüter, Cyril C Abstract: Primates exhibit a variety of social systems, among which multilevel or modular societies are likely the most complex, the least understood and least investigated. Modular societies are structurally characterized by nuclear one-male units (OMUs) or harems which are habitually embedded within larger relatively coherent social bands. Within the order Primates, modular societies are uncommon, found in only a few species, e.g. hamadryas baboons, gelada baboons, proboscis monkeys, snub-nosed monkeys and humans (multifamily system). In an attempt to elucidate the evolution and functional determi- nants of modular societies in primates, I chose a twofold approach: First, I undertook a case study of the modular system of black-and-white snub-nosed monkeys (Rhinopithecus bieti), a highly endangered colobine whose socioecology has received only scant attention. The study was conducted over 20 months on a free-ranging, semi-habituated band in the montane Samage Forest (Baimaxueshan National Nature Reserve in Yunnan, PRC). The focal band was found to consist of 400 individuals, one of the largest groups of wild primates ever recorded. OMUs are cohesive entities within the band. Large all-male units (AMUs) composed of adult and sub-adult males as well as juveniles tended to follow the family units closely at all times. Such a large group likely confers costs of increased food competition, particularly with regard to spatially clumped and temporally restricted food items. However, the wide temporal and spatial availability of lichens - their staple fallback food - reduces the ecological costs of grouping, thus allowing for the formation of ‘super-groups’. Second, I conducted a comparative analysis focusing on Asian colobines (Presbytini) which form either autonomous and often territorial uni-male groups (e.g. Presbytis spp.) or modular associations (most odd- nosed colobines, i.e. Nasalis, Rhinopithecus, Py- gathrix), with the latter encompassing both tight bands composed of OMUs and loose neighborhoods of OMUs. I did a phylogenetic reconstruction of modularity in the Presbytini, revealing that the single OMU pattern is probably the ancestral state while the modular pattern is a derived feature. In order to answer the key question of why OMUs in some colobines have the propensity to congregate, I tested predictions of three socioecological hypotheses and evaluated other scenarios descriptively due to dif- ficulties of quantifying them. Odd-nosed monkeys in general and Rhinopithecus bieti in particular do not seem to accrue obvious ecological benefits from band formation such as thermoregulation, predation avoidance or enhanced efficiency of resource harvest. I found partial support for the bachelor threat hypothesis, i.e. that the number of non- reproductive bachelor males is a significant predictor variable of band formation. The threat posed by ‘gangs’ of bachelor males is thought to force OMUs to aggregate as a means of decreasing the amount of harassment and the risk of takeovers and infanticide, and thus may represent a salient force shaping the modular sociality. I also demonstrated via a comparative anal- ysis that modular species have significantly higher levels of sexual dimorphism in body weight thanthe non-modular ones, suggesting that living in a modular society intensifies the mating competition among males. Zu den am wenigsten bekannten und komplexesten sozialen Systemen bei Primaten gehören die modularen Gemeinschaften, die auf Einmanngruppen basieren, die sich regelmässig oder permanent zu höheren Banden zusammenschliessen. Solche Systeme wurden zum Beispiel bei Mantelpavianen (Papio hamadryas), Nasenaffen (Nasalis larvatus) und Stumpfnasenaffen (Rhinopithecus spp.) nachgewiesen. Um die Evolution und sozioökologischen Determinanten dieses Systems zu untersuchen, wurden ein- erseits wilde chinesische Stumpfnasenaffen (Rhinopithecus bieti) als Modellart während 20 Monaten im Freiland (Samage Forest, Baimaxueshan Nature Reserve, Yunnan, PRC) untersucht und andererseits eine taxa-übergreifende Metaanalyse an Langurenaffen durchgeführt. Mit einer phylogenetischen Analyse kon- nte demonstriert werden, dass Einmanngruppen bei Colobinen ancestral sind und modulare Banden ein abgeleitetes Merkmal darstellen. Die Ergebnisse der Freilandarbeit und vergleichenden Studie zeigen, dass solche Banden ökologische Kosten in Form erhöhter Nahrungskonkurrenz mit sich bringen. Die Tat- sache, dass sich modulare Arten wie Rhinopithecus bieti aber von reichlich vorhandenen Nahrungsquellen wie Baumflechten ernähren, verringert die Nahrungskonkurrenz allerdings beträchtlich. Modulare Arten weisen auch einen deutlich höheren Geschlechtsdimorphismus im Körpergewicht auf, was auf verstärkte sexuelle Konkurrenz zwischen Männchen hindeutet. Der Hauptnutzen des Zusammenschlusses in Banden scheint nicht ökologischer Natur (Schutz vor Prädatoren, Thermoregulation, kollektives Lokalisieren von nicht-erschöpften Ressourcen), sondern sozialer Natur zu sein und im effektiveren Schutz vor Angriffen durch Konkurrenten (vor allem „Junggesellen“) zu liegen: die Anzahl von nicht-reproduktiven Männchen ausserhalb der Einmanngruppen (der „bachelor threat“) war signifikant höher bei Arten mit modularen Sozietäten. Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-95938 Dissertation Published Version Originally published at: Grüter, Cyril C. Determinants of modular societies in snub-nosed monkeys (Rhinopithecus bieti) and other Asian colobines. 2009, University of Zurich, Faculty of Science. 2 Determinants of Modular Societies in Snub-nosed Monkeys (Rhinopithecus bieti) and other Asian Colobines Dissertation zur Erlangung der naturwissenschaftlichen Doktorwürde (Dr. sc. nat.) vorgelegt der Mathematisch-naturwissenschaftlichen Fakultät der Universität Zürich von Cyril C. Grüter von Ruswil LU Promotionskomitee Prof. Dr. Carel P. van Schaik (Leitung der Dissertation) Prof. Dr. Barbara König Zürich, 2009 ii For My wife Carol Jin Grüter & My mother Jutta Porr-Gwildies ii Acknowledgments This study was made possible by grants from the following institutions to Cyril C. Grüter: Janggen-Pöhn-Stiftung, A. H. Schultz Stiftung, Zürcher Tierschutz, G. & A. Claraz- Schenkung, Goethe-Stiftung, Jane Goodall Institute Schweiz, Kommission für Reisestipendien der Schweizerischen Akademie der Naturwissenschaften SANW, one anonymous foundation, Jutta & Othmar Porr, Hermann Stern, Offield Family Foundation, Amerman Foundation, Primate Conservation, Inc., Zoological Society of San Diego, and the Primate Action Fund of Conservation International. Bischofszell Nahrungsmittel AG is thanked for providing me with a huge supply of instant mashed potatoes. The research conducted was noninvasive and abides by the legal requirements in the People’s Republic of China. Numerous people were involved in this research project: I wish to thank Carel van Schaik for his belief in the success of my project, his guidance as my mentor and scientific supervisor and his continuous feedback that improved this work considerably. I express thanks to Wei Fuwen at the Institute of Zoology in Beijing for making this research project possible in the first place, hosting me in China, applying for permits and examining my thesis. Li Dayong deserves special mention for being my friend, helper and assistant throughout my time in China. Li Dayong and I would have been unable to carry out the demanding field work without the help of our three highly skilled and trustworthy field assistants ‘Lao Feng’, Feng Xuesheng and Feng Xuewen who guided us long hours through difficult terrain, from impenetrable bamboo thickets to deep snow. We spent hundreds of unforgettable and life-enriching hours in those often cold, windy, misty, yet truly spectacular mountains. iv I thank all the people in Gehuaqing for their hospitality, ‘Xiao He’ and ‘Si Mei’, my two cooks and nannies, for running the research station while I was in the mounatins, and my two dogs ‘Apple’ and ‘Strudel’ for making the sometimes lonely days more varied. I am appreciative of Liu Sikang for permitting me to work at Baimaxueshan Nature Reserve. I also thank Long Yongcheng at The Nature Conservancy (TNC) in Kunming for introducing me to the research and conservation efforts on Yunnan snub-nosed monkeys in China and providing constant ideological support. Ren Baoping for his companionship, cooperation and advice on various matters. Ding Wei and Yang Shijian for helping me get started with my pilot study back in 2002/2003. Craig Kirkpatrick for inspiring me and for regular advice on all kinds of scientific aspects and sharing ideas. Barbara König for accepting to be part of my dissertation committee and providing advice. Sandy Harcourt for taking the time to provide a review of my thesis. Peter Fashing, Craig Kirkpatrick, Ken Sayers, Dietmar Zinner, Chia Tan and several anonymous reviewers for instructive comments on the content of various manuscripts and proof-reading of the text. Karin Isler for assistance with MacClade analyses. Zhuang Jiaoyan and Luo Yongmei for help with GIS analyses. iv v Hai Xian, Liu Jingxin, Fang Zhendong, Xiao Maorong at the Alpine Botanical Garden in Shangri-La, Sun Hang at the Herbaria of the Kunming Institute of Botany (KIB)