Social and economic interdependence as a basis for peaceful between-group relationships in nonhuman primates and humans.

Glowacki asserts that interdependent relationships beyond group boundaries are exceptionally rare among nonhuman mammals. However, rudimentary forms of interdependence can be seen in primate species that form multilevel societies, that is, core social units embedded within higher-level grouping categories. Studies of primate multilevel societies can enrich discussions about the evolutionary origins of peaceful between-group interactions in humans.

Correlated evolution of social organization and lifespan in mammals.

Discerning the relationship between sociality and longevity would permit a deeper understanding of how animal life history evolved. Here, we perform a phylogenetic comparative analysis of ~1000 mammalian species on three states of social organization (solitary, pair-living, and group-living) and longevity. We show that group-living species generally live longer than solitary species, and that the transition rate from a short-lived state to a long-lived state is higher in group-living than non-group-living species, altogether supporting the correlated evolution of social organization and longevity. The comparative brain transcriptomes of 94 mammalian species identify 31 genes, hormones and immunity-related pathways broadly involved in the association between social organization and longevity. Further selection features reveal twenty overlapping pathways under selection for both social organization and longevity. These results underscore a molecular basis for the influence of the social organization on longevity.

Chimpanzees Use Least-Cost Routes to Out-of-Sight Goals.

While the ability of naturally ranging animals to recall the location of food resources and use straight-line routes between them has been demonstrated in several studies [1, 2], it is not known whether animals can use knowledge of their landscape to walk least-cost routes [3]. This ability is likely to be particularly important for animals living in highly variable energy landscapes, where movement costs are exacerbated [4, 5]. Here, we used least-cost modeling, which determines the most efficient route assuming full knowledge of the environment, to investigate whether chimpanzees (Pan troglodytes) living in a rugged, montane environment walk least-cost routes to out-of-sight goals. We compared the "costs" and geometry of observed movements with predicted least-cost routes and local knowledge (agent-based) and straight-line null models. The least-cost model performed better than the local knowledge and straight-line models across all parameters, and linear mixed modeling showed a strong relationship between the cost of observed chimpanzee travel and least-cost routes. Our study provides the first example of the ability to take least-cost routes to out-of-sight goals by chimpanzees and suggests they have spatial memory of their home range landscape. This ability may be a key trait that has enabled chimpanzees to maintain their energy balance in a low-resource environment. Our findings provide a further example of how the advanced cognitive complexity of hominins may have facilitated their adaptation to a variety of environmental conditions and lead us to hypothesize that landscape complexity may play a role in shaping cognition.

Spatiotemporal association patterns in a supergroup of Rwenzori black-and-white colobus (Colobus angolensis ruwenzorii) are consistent with a multilevel society.

Primates display broad diversity in their social organization. The social groups of a few primate species are organized in a multilevel fashion, with large groups composed of multiple, core one-male units (OMUs). A characteristic of multilevel societies is that the higher levels can include hundreds of individuals. The Rwenzori black-and-white colobus (Colobus angolensis ruwenzorii) in the montane forests of Rwanda form supergroups and have been suspected to exhibit multilevel social organization. Here we present the first data on the "anatomy" of a supergroup numbering 500+ individuals. We identified subgroups within the supergroup based on progression data, extracting the social network structure from the time-stamped spatiotemporal distribution of passing individuals identified to age-sex class, and selecting an optimal time window for each network using the two-step approach developed by Uddin, Choudhury, Farhad, and Rahman (2017). We detail the existence of core units-multi-male units (MMUs) with a mean of 1.7 adult males and 3.1 adult females, as well as OMUs, all-female units and bachelor units composed of adult and sub-adult males. More than two-thirds of units are MMUs. These grouping patterns conform to a multilevel society with predominantly multi-male core units, a social system that has recently also been described for a population of the same taxon in Uganda. Individual identification will be required to corroborate these interpretations.

Quadratic relationships between group size and foraging efficiency in a herbivorous primate.

The effect of feeding competition on foraging efficiency is an important link between ecological factors and the social organization of gregarious species. We examined the effects of group size on daily travel distances, activity budgets, and energy intake of mountain gorillas in Rwanda. We measured daily travel distances of five groups, activity budgets of 79 gorillas in nine groups, and energy intake data for 23 adult females in three groups over a 16-month period. Travel distances and the proportion of time spent traveling increased with size for most groups, which would be expected if their foraging efficiency is limited by intragroup feeding competition. However, travel distances and times decreased for the largest group, which also had higher energy intake rates than intermediate sized groups. The improved foraging efficiency of the largest group may be explained by advantages in intergroup contest competition. The largest group had much lower home range overlap than the other study groups which may be due to groups avoiding one another as a result of male mating competition. Collectively, our results indicate that intermediate sized groups had the lowest foraging efficiency and provide a new twist on the growing evidence of non-linear relationships between group size and foraging efficiency in primates.

Deciphering the Social Organization and Structure of Wild Yunnan Snub-Nosed Monkeys (Rhinopithecus bieti).

The social organization of natural groups of Rhinopithecus bieti (Yunnan snub-nosed monkey) is virtually unknown. We studied the demography and social structure of a free-ranging group at Samage Forest, China, for nearly 2 years. This study confirmed that R. bieti exhibits a multilevel social organization of core 1-male units (OMUs) that congregate in a band of >400 members. Even though the band appeared to be unified for the most part, we also witnessed occasional fission-fusion. OMUs were cohesive entities, and their members were spatially and socially isolated from members of other OMUs. Large all-male units associated with the band, and when they closely followed OMUs there was a tendency for elevated male aggression. Within OMUs, females associated preferentially with males and vice versa, resulting in a bisexually bonded society. Contrary to other Asian colobines, R. bieti were comparatively social, with grooming occupying 7.3% of the time. Social grooming was primarily a female affair, but males also participated in grooming networks. The integration of males into the social network of the OMU is thought to help to maintain OMU integrity and cohesion with other social units being in close proximity.

A new conservation strategy for China-A model starting with primates.

Although the evolutionary history of primates in China dates to the Eocene, and includes major radiations of lorisids, hominoids, cercopithecines, and colobines during the Miocene, Pliocene, and Pleistocene, extensive human-induced habitat change and deforestation over the past few centuries has resulted in 22 of 25 extant species listed as threatened or endangered, and two species of gibbons extirpated in the last few years. This commentary briefly reviews factors that have contributed to the decline of primates in China over the past 400 years, and in particular how major social events and economic development in modern China have resulted in unsustainable environmental change. In response, we describe our efforts to develop a strategic scientific, educational and conservation partnership in China, focusing on primates, in which GIS technology will be used to integrate geographical profiles, climatic information, and changes in land use patterns and human and nonhuman primate distributions to highlight issues of immediate concern and to develop priority-based conservation solutions. Our goal is to evaluate how human-induced environmental change has impacted primates over time and to predict the likelihood of primate population extinctions in the near future. This model represents an early warning system that will be widely available to the Chinese government, public, educational institutions, researchers, and NGOs through social media and educational videos in order to arouse public awareness and promote wildlife conservation. We encourage colleagues across a broad range of academic disciplines, political ideologies, and the public to help move this strategy into reality, the sooner the better. Am. J. Primatol. 78:1137-1148, 2016. © 2016 Wiley Periodicals, Inc.

Sexually selected lip colour indicates male group-holding status in the mating season in a multi-level primate society.

Sexual selection typically produces ornaments in response to mate choice, and armaments in response to male-male competition. Unusually among mammals, many primates exhibit colour signals that may be related to one or both processes. Here, we document for the first time correlates of facial coloration in one of the more brightly coloured primates, the black-and-white snub-nosed monkey (Rhinopithecus bieti). Snub-nosed monkeys have a one-male unit (OMU) based social organization, but these units aggregate semi-permanently into larger bands. This form of mating system causes many males to become associated with bachelor groups. We quantified redness of the prominent lower lip in 15 males (eight bachelors, seven OMU holders) in a group at Xiangguqing, China. Using mixed models, our results show that lip redness increases with age. More interestingly, there is a significant effect of the interaction of group-holding status and mating season on redness; that is, lip colour of OMU males undergoes reddening in the mating season, whereas the lips of subadult and juvenile bachelor males become paler at that time of year. These results indicate that lip coloration is a badge of (group-holding) status during the mating season, with non-adults undergoing facial differentiation, perhaps to avoid the costs of reproductive competition. Future research should investigate whether lip coloration is a product of male-male competition, and/or female mate choice.

Nocturnal sleeping habits of the Yunnan snub-nosed monkey in Xiangguqing, China.

Weather, predation, and social organization are hypothesized to influence sleeping habits of nonhuman primates at night. To investigate how the Yunnan snub-nosed monkey (Rhinopithecus bieti) prepares for and behaves during cold nights in their harsh alpine forest habitat (above 3,000 m), we studied the sleeping habits of the 171 one-male units (OMU) in one group for 12 months at Xiangguqing in the Baimaxueshan Nature Reserve, China. It took 20.2 min from the time the study group entered a sleeping site until they fell asleep. This duration was consistent over seasons. On average, sleeping time was 11.5 hr per night over the year. Seasonal mean lengths of sleeping time varied significantly, however, and ranged from 10 to 13 hr per night, correlating with night length. Two sleeping styles were distinguishable: solitary sleeping and huddled sleeping. That adult males in OMUs principally slept alone. This is likely to reflect night-time guarding behavior. Female-juvenile and female-infant dyadic huddles were the most prevalent sleeping unit (42% of all observed data), and the monkeys employed female-biased huddling during nocturnal sleep. Huddled sleeping group size showed significant seasonal variation, with the largest huddle (eight individuals) occurring in winter. Climate and social organization profoundly influence the nocturnal sleeping habits of R. bieti, while huddling behavior may help shield animals from cold nights and provide additional protection against predators.

Fallback foods of temperate-living primates: a case study on snub-nosed monkeys.

Only a few primate species thrive in temperate regions characterized by relatively low temperature, low rainfall, low species diversity, high elevation, and especially an extended season of food scarcity during which they suffer from dietary stress. We present data of a case study of dietary strategies and fallback foods in snub-nosed monkeys (Rhinopithecus bieti) in the Samage Forest, Northwest Yunnan, PRC. The snub-nosed monkeys adjusted intake of plant food items corresponding with changes in the phenology of deciduous trees in the forest and specifically showed a strong preference for young leaves in spring. A non-plant food, lichens (Parmeliaceae), featured prominently in the diet throughout the year (annual representation in the diet was about 67%) and became the dominant food item in winter when palatable plant resources were scarce. Additional highly sought winter foods were frost-resistant fruits and winter buds of deciduous hardwoods. The snub-nosed monkeys' choice of lichens as a staple fallback food is likely because of their spatiotemporal consistency in occurrence, nutritional and energetic properties, and the ease with which they can be harvested. Using lichens is a way to mediate effects of seasonal dearth in palatable plant foods and ultimately a key survival strategy. The snub-nosed monkeys' fallback strategy affects various aspects of their biology, e.g., two- and three-dimensional range use and social organization. The higher abundance of lichens at higher altitudes explains the monkeys' tendency to occupy relatively high altitudes in winter despite the prevailing cold. As to social organization, the wide temporal and spatial availability of lichens strongly reduces the ecological costs of grouping, thus allowing for the formation of "super-groups." Usnea lichens, the snub-nosed monkeys' primary dietary component, are known to be highly susceptible to human-induced environmental changes such as air pollution, and a decline of this critical resource base could have devastating effects on the last remaining populations. Within the order Primates, lichenivory is a rare strategy and only found in a few species or populations inhabiting montane areas, i.e., Macaca sylvanus, Colobus angolensis, and Rhinopithecus roxellana. Other temperate-dwelling primates rely mainly on buds and bark as winter fallback foods.

Characteristics of night-time sleeping places selected by golden monkeys (Rhinopithecus bieti) in the Samage Forest, Baima Snow Mountain Nature Reserve, China.

We examined the criteria for sleeping place selection in a social band of Rhinopithecus bieti (black-and-white snub-nosed or golden monkeys) living in the mountainous Samage Forest, Baima Snow Mountain Nature Reserve, Yunnan, China. We performed principal component analysis and found that slope aspect, tree height and trunk diameter were likely key variables influencing selection of sleeping places. Sleeping sites were preferentially located in mixed deciduous/conifer forest. The monkeys slept exclusively in evergreen trees, of which 82% were conifers (mostly Picea likiangensis and Tsuga dumosa) and 18% evergreen oaks (Cyclobalanopsis oxyodon and Quercus spp.). Sleeping trees were tall (mean 30.5 m), had high boles (mean 18.4 m), large diameters (mean 62.6 cm) and large crown areas (mean 57.9 m(2) ). A comparative analysis of phytological and architectural features between trees in "sleeping site plots" (n= 18) and trees in "non-sleeping-site plots" (n= 66) revealed that diameter, crown surface area and tree height were significantly (P < 0.01) larger in the former compared with the latter. All investigated roosting sites were situated on steep mountain slopes. Valleys and mountain ridges were avoided. We also detected re-use of roosting sites on several occasions, but not on consecutive nights. It is most likely that a mix of factors (stability of trees, access to food, unit cohesion, monitoring potential) explains the pattern of sleeping site preference, but predation at night seems to be only slightly important. Climate appears to have a profound influence on patterns of sleeping site selection in the monkeys' harsh temperate habitat. This is demonstrated by the monkeys' preference for mixed forest at medium elevations over montane fir forest at high elevations and slopes instead of ridges, with reduced exposure to wind and precipitation inherent in the former. We also emphasize the possibly substantial role that non-environmental factors (the nature of social organization and socio-behavioral strategies) play in determining sleeping site use in R. bieti and other primates.