Determinants of modular societies in snub-nosed monkeys (Rhinopithecus bieti) and other Asian colobines

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 determinants 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, Pygathrix), 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 difficulties 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 analysis that modular species have significantly higher levels of sexual dimorphism in body weight than the 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 gehoren die modularen Gemeinschaften, die auf Einmanngruppen basieren, die sich regelmassig oder permanent zu hoheren Banden zusammenschliessen. Solche Systeme wurden zum Beispiel bei Mantelpavianen (Papio hamadryas), Nasenaffen (Nasalis larvatus) und Stumpfnasenaffen (Rhinopithecus spp.) nachgewiesen. Um die Evolution und soziookologischen Determinanten dieses Systems zu untersuchen, wurden einerseits wilde chinesische Stumpfnasenaffen (Rhinopithecus bieti) als Modellart wahrend 20 Monaten im Freiland (Samage Forest, Baimaxueshan Nature Reserve, Yunnan, PRC) untersucht und andererseits eine taxa-ubergreifende Metaanalyse an Langurenaffen durchgefuhrt. Mit einer phylogenetischen Analyse konnte 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 okologische Kosten in Form erhohter Nahrungskonkurrenz mit sich bringen. Die Tatsache, dass sich modulare Arten wie Rhinopithecus bieti aber von reichlich vorhandenen Nahrungsquellen wie Baumflechten ernahren, verringert die Nahrungskonkurrenz allerdings betrachtlich. Modulare Arten weisen auch einen deutlich hoheren Geschlechtsdimorphismus im Korpergewicht auf, was auf verstarkte sexuelle Konkurrenz zwischen Mannchen hindeutet. Der Hauptnutzen des Zusammenschlusses in Banden scheint nicht okologischer Natur (Schutz vor Pradatoren, Thermoregulation, kollektives Lokalisieren von nicht-erschopften Ressourcen), sondern sozialer Natur zu sein und im effektiveren Schutz vor Angriffen durch Konkurrenten (vor allem „Junggesellen“) zu liegen: die Anzahl von nicht-reproduktiven Mannchen ausserhalb der Einmanngruppen (der „bachelor threat“) war signifikant hoher bei Arten mit modularen Sozietaten.