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.

The 10th anniversary of the scientific description of the black snub-nosed monkey (Rhinopithecus strykeri): It is time to initiate a set of new management strategies to save this critically endangered primate from extinction.

Traditionally, the genus Rhinopithecus (Milne-Edwards, 1872, Primates, Colobinae) included four allopatric species, restricted in their distributions to China and Vietnam. In 2010, a fifth species, the black snub-nosed monkey (Rhinopithecus strykeri) was discovered in the Gaoligong Mountains located on the border between China and Myanmar. Despite the remoteness, complex mountainous terrain, dense fog, and armed conflict that characterizes this region, over this past decade Chinese and Myanmar scientists have begun to collect quantitative data on the ecology, behavior and conservation requirements of R. strykeri. In this article, we review the existing data and present new information on the life history, ecology, and population size of R. strykeri. We discuss these data in the context of past and current conservation challenges faced by R. strykeri, and propose a series of both short-term and long-term management actions to ensure the survival of this Critically Endangered primate species. Specifically, we recommend that the governments and stakeholders in China and Myanmar formulate a transboundary conservation agreement that includes a consensus on bilateral exchange mechanisms, scientific research and monitoring goals, local community development, cooperation to prevent the hunting of endangered species and cross-border forest fires. These actions will contribute to the long-term conservation and survival of this Critically Endangered species.

Corrigendum: A Severe Lack of Evidence Limits Effective Conservation of the World's Primates.

[This corrects the article DOI: 10.1093/biosci/biaa082.].

Do we need to reclassify the social systems of gregarious apes?

Decades of research have led to a solid understanding of the social systems of gregarious apes: chimpanzees, bonobos, gorillas, and gibbons. As field studies have increasingly collected data from multiple neighboring habituated groups, genetic and social interconnections have been revealed. These findings provide a more nuanced picture of intergroup relations in apes, and have led to claims in the literature that some ape taxa have multilevel societies. A multilevel society is defined as a nested collection of social entities comprising at least two discernible levels of social integration between the individual and the population. We argue that the evidence for multilevel sociality sensu stricto in apes is currently inconclusive and that it is premature to abandon the traditional classification of ape social systems. However, available findings appear to be consistent with the existence of some degree of higher social grouping patterns. We propose the term supra-group organization which may adequately capture ape social systems when viewed from a top-down perspective.

Fermented food consumption in wild nonhuman primates and its ecological drivers.

OBJECTIVES: Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late-stage fermented foods, the ability of primates to detect them, and potential nutritional benefits. MATERIALS AND METHODS: We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed-effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates. RESULTS: Late-stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%-3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, late-stage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures. DISCUSSION: We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods.

A Severe Lack of Evidence Limits Effective Conservation of the World's Primates.

Threats to biodiversity are well documented. However, to effectively conserve species and their habitats, we need to know which conservation interventions do (or do not) work. Evidence-based conservation evaluates interventions within a scientific framework. The Conservation Evidence project has summarized thousands of studies testing conservation interventions and compiled these as synopses for various habitats and taxa. In the present article, we analyzed the interventions assessed in the primate synopsis and compared these with other taxa. We found that despite intensive efforts to study primates and the extensive threats they face, less than 1% of primate studies evaluated conservation effectiveness. The studies often lacked quantitative data, failed to undertake postimplementation monitoring of populations or individuals, or implemented several interventions at once. Furthermore, the studies were biased toward specific taxa, geographic regions, and interventions. We describe barriers for testing primate conservation interventions and propose actions to improve the conservation evidence base to protect this endangered and globally important taxon.

Male social rank and food competition in a primate multi-level society.

OBJECTIVES: Social animals often have dominance hierarchies, with high rank conferring preferential access to resources. In primates, competition among males is often assumed to occur predominantly over reproductive opportunities. However, competition for food may occur during food shortages, such as in temperate species during winter. Higher-ranked males may thus gain preferential access to high-profitability food, which would enable them to spend longer engaged in activities other than feeding. MATERIALS AND METHODS: We performed a field experiment with a breeding band of golden snub-nosed monkeys, a species that lives in a multi-level society in high-altitude forests in central China. We provisioned monkey's high-profitability food during winter when natural foods are limited, and then recorded the times individual adult males spent engaged in different behaviors. RESULTS: Higher-ranking males spent less time feeding overall and fed on provisioned foods at a higher rate than lower-ranking males. Higher-ranking males therefore had more time to spend on alternative behaviors. We found no significant difference according to rank in times spent moving or resting. However, high-ranking males spend significantly longer on affiliative behaviors with other members of their social sub-units, especially grooming and being groomed, behaviors known to promote social cohesion in primates. DISCUSSION: We show that preferential access to high-profitability foods likely relaxes time-budget constraints to higher-ranking males. High-ranking males thus spend more time on non-feeding activities, especially grooming, which may enhance social cohesion within their social sub-unit. We discuss the potential direct and indirect benefits to high-ranking males associated with preferential access to high-value food during winter.

Chimpanzee ranging responses to fruit availability in a high-elevation environment.

Most primates experience seasonal fluctuations in the availability of food resources and face the challenge of balancing energy expenditure with energy gain during periods of resource scarcity. This is likely to be particularly challenging in rugged, montane environments, where available energy is relatively low and travel costs are high. Chimpanzees (Pan troglodytes) show extensive behavioral diversity across study sites. Yet, as most research has focused on low- and mid-elevation sites, little is known on how chimpanzees respond to periods of low fruit availability in harsh montane environments. We use focal follow and phenology data to investigate how fruit availability influences daily path length and monthly home range in chimpanzees living in Nyungwe National Park, a montane forest in Rwanda. Nyungwe chimpanzees decreased their daily travel distances during periods of fruit scarcity. However, this decrease in travel effort did not correspond with a decrease in foraging area. Instead, monthly homes ranges shifted location across the study period. Nyungwe chimpanzees occupy a relatively wide altitudinal range and the shifts in monthly home range location may reflect differences in the altitudinal distribution of food resources. Chimpanzee monthly diet was often dominated by one or two species and each of these species were confined to different elevation zones. One important species, Podocarpus latifolius, grew only at high elevations (2,600-2,950 m) and chimpanzees ranged at the altitudinal peak of their range for 2 consecutive months while feeding on this species. Thus, while high elevations are often thought to be harsh environments for primates, they can be an important part of a species' home range when they provide a refugium for densely distributed, important food species.

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.

Cafeteria-style feeding trials provide new insights into the diet and nutritional strategies of the black snub-nosed monkey (Rhinopithecus strykeri): Implications for conservation.

Anthropogenic changes and fragmentation of natural habitats often exert a negative effect on resource availability and distribution, and the nutritional ecology and feeding behavior of nonhuman primates. The goals of this study are to examine food choice and to identify the nutritional profile of foods consumed by the Critically Endangered black snub-nosed monkey (Rhinopithecus strykeri). To accomplish our study goals, we presented cafeteria-style feeding trials of fresh food items collected in the home range of wild black snub-nosed monkeys to the only two captive R. strykeri, and compared the nutritional profiles of the leafy foods (buds, young, and mature leaves, 100 i23tems from 70 plant species) selected with those avoided (54 items from 48 plant species). Overall, the results indicate that captive R. strykeri selected foods that were higher in moisture (Mo; 77.7%), crude protein (CP; 21.2%), total nonstructural carbohydrates (TNC; 34.9%), and phosphorus (P; 0.37%) while tending to avoid foods with a neutral detergent fiber (NDF) content of greater than 46.8%. Leaves collected in autumn and selected by the monkeys were characterized by a slightly higher amount of metabolizable energy (ME) than those rejected (1,350 kJ/100 g vs. 1,268 kJ/100 g). In contrast, the protein content of foods collected and consumed during the spring was greater (22.9%) than in autumn (16.4%). Random Forests modeling, an ensemble learning method, indicated that the proportion of Mo, NDF, ME, CP, P, and TNC were among the most important factors in predicting which items were consumed by the captive R. strykeri during spring and autumn. On the basis of the nutritional profile of foods consumed across the two seasons, we identified 18 nutrient-rich native plant species that we recommend for use in ex- and in-situ conservation management and reforestation programs to provide long-term access to a nutritionally adequate diet.

Sexual ornaments but not weapons trade off against testes size in primates.

Males must partition their limited reproductive investments between traits that promote access to females (sexual ornaments and weapons) and traits that enhance fertilization success, such as testes and ejaculates. Recent studies show that if the most weaponized males can monopolize access to females through contest competition, thereby reducing the risk of sperm competition, they tend to invest less in sperm production. However, how males invest in sexual ornaments relative to sperm production remains less clear. If male ornaments serve as badges of status, with high-ranking males attaining near-exclusive access to females, similar to monopolizing females through combat, their expression should also covary negatively with investment in post-mating traits. In a comparative study across primates, which exhibit considerable diversification in sexual ornamentation, male weaponry and testes size, we found relative testes size to decrease with sexual ornaments but increase with canine size. These contrasting evolutionary trajectories might be driven by differential selection, functional constraints or temporal patterns of metabolic investment between the different types of sexual traits. Importantly, however, our results indicate that the theory of relative investments between weapons and testes in the context of monopolizing females can extend to male ornaments.

Individuality in coo calls of adult male golden snub-nosed monkeys (Rhinopithecus roxellana) living in a multilevel society.

Vocal individuality is a prerequisite for individual recognition, especially when visual and chemical cues are not available or effective. Vocalizations encoding information of individual identity have been reported in many social animals and should be particularly adaptive for species living in large and complexly organized societies. Here, we examined the individuality in coo calls of adult male golden snub-nosed monkeys (Rhinopithecus roxellana) living in a large and multilevel society. Coo calls are one of the most frequently occurring call types in R. roxellana and likely serve as the signals for contact maintenance or advertisement in various contexts including group movement, foraging, and resting. From April to October 2016, April to July 2017, and September to October 2017, we recorded a total of 721 coo calls from six adult males in a provisioned, free-ranging group and one adult male in captivity in Shennongjia National Park, China. We selected 162 high-quality recordings to extract 14 acoustic parameters based on the source-filter theory. Results showed that each of all parameters significantly differed among individuals, while pairwise comparisons failed to detect any parameter that was different between all pairs. Furthermore, a discriminant function analysis indicated that the correct assignment rate was 80.2% (cross-validation: 67.3%), greater than expected by chance (14.3%). In conclusion, we found evidence that coo calls of adult male R. roxellana allowed the reliable accuracy of individual discrimination complementarily enhanced by multiple acoustic parameters. The results of our study point to the selective pressures acting on individual discrimination via vocal signals in a highly gregarious forest-living primate.

Infant handling by female mountain gorillas: Establishing its frequency, function, and (ir)relevance for life history evolution.

OBJECTIVES: Infant handling describes cases in which youngsters are temporarily removed from the care of their mothers and "taken care of" (held, carried, etc.) by other conspecifics. Handlers may gain indirect fitness benefits from these actions and can practice mothering skills, thereby improving the odds of survival of their own infants. Great apes are notable for displaying little infant handling. Apart from anecdotal observations, no published data exist on infant handling in wild mountain gorillas. We tested two of the most pertinent explanations ("kin selection" and "learning to mother") in a wild population of mountain gorillas in Rwanda. We predicted that (a) nulliparous females would exhibit infant handling (i.e., carrying) more than parous females and (b) maternal kin would exhibit more infant handling than nonkin. METHODS: We collated 8 years of data on infant carrying behavior collected in 13 groups monitored by the Dian Fossey Gorilla Fund's Karisoke Research Center. RESULTS: Infant handling is an infrequent behavior (1,783 instances over 25,600 observation hours). A strong positive effect of relatedness and handler parity on the frequency of infant handling emerged. CONCLUSIONS: While the nature of handler-infant interactions (affiliative, abusive, etc.) remains unstudied, they could constitute alloparental care and could therefore attenuate maternal energetic burden and ultimately allow increased birth rates. However, the rarity of this behavior makes it an unlikely contributor to mountain gorillas' relatively short interbirth intervals.

Dietary diversity of an ecological and macronutritional generalist primate in a harsh high-latitude habitat, the Taihangshan macaque (Macaca mulatta tcheliensis).

Recent advances in niche theory have stressed the importance of understanding dietary generalism at multiple levels, including the range of habitat and foods exploited by a species, foods exploited within populations, and patterns of nutrient intake. Here we apply this framework to examine the dietary strategy of the Macaca mulatta, a primate species that is second only to humans in their breadth of geographical distribution, and occupy diverse ecological habitats from cold temperate to tropical latitudes. A recent study showed that the Taihangshan subspecies ( M. mulatta tcheliensis) in China, which is found at the northern latitudinal limit of the species range, respond to ecologically constrained interannual variation in the macronutrient ratios of the spring diet in a way that theory predicts should be associated with ecological generalism. Here we further extend this study, examining the relationships between seasonal variation in food availability and the patterns of food selection across a full year. We found that, despite the ecological and macronutritional generalism of the species, Taihangshan macaques subsist on a relatively small range of foods (57 different foods, spread across 8 categories comprising seeds, fruits, buds, flowers, leaves, herbs, young bark, and twigs), but face considerable seasonal variation in the combinations available. In spring and summer, when seeds were scarce, leaves accounted for 60.3 ± 13.8% of their diet (dry matter [DM] %), and herbs contributed 31.7 ± 22.2%. However, in autumn and winter, when seeds were abundant, they contributed 68.5 ± 22.7% of the diet while herbs accounted for 18.9 ± 12.9% on a DM. Although young bark and twigs were available in all seasons, the macaques only fed on them in winter. We present comparative data from the literature on the diets of M. mulatta and other Macaca species, to interpret this pattern of resource use within the framework of multilevel niche theory.

Chimpanzee feeding ecology and fallback food use in the montane forest of Nyungwe National Park, Rwanda.

Almost all primates experience seasonal fluctuations in the availability of key food sources. However, the degree to which this fluctuation impacts foraging behavior varies considerably. Eastern chimpanzees (Pan troglodytes schweinfurthii) in Nyungwe National Park, Rwanda, live in a montane forest environment characterized by lower primary productivity and resource diversity than low-elevation forests. Little is known about chimpanzee feeding ecology in montane forests, and research to date predominantly relies on indirect methods such as fecal analyses. This study is the first to use mostly observational data to examine how seasonal food availability impacts the feeding ecology of montane forest chimpanzees. We examine seasonal changes in chimpanzee diet and fallback foods (FBFs) using instantaneous scan samples and fecal analyses, supported by inspection of feeding remains. Chimpanzee fruit abundance peaked during the major dry season, with a consequent change in chimpanzee diet reflecting the abundance and diversity of key fruit species. Terrestrial herbaceous vegetation was consumed throughout the year and is defined as a "filler" FBF. In contrast to studies conducted in lower-elevation chimpanzee sites, figs (especially Ficus lutea) were preferred resources, flowers were consumed at seasonally high rates and the proportion of non-fig fruits in the diet were relatively low in the current study. These divergences likely result from the comparatively low environmental diversity and productivity in higher-elevation environments.

Seasonal changes in social cohesion among males in a same-sex primate group.

Male-male interactions in mixed-sex groups of social mammals are typically characterized by a mix of hostility and affiliation, as a result of inherent conflicts over mating opportunities, and the costs and benefits of social alliances, co-operative behaviors, and coalitionary defense. In species of nonhuman primates that form all-male groups, it is still unclear how the tradeoffs between the benefits of forming an all-male group and the cost of male-male competition in seeking mating opportunities with females in bisexual groups influence social cohesion in different seasons. Here, we used social network analysis to quantify the impact of reproductive seasonality on social cohesion and clique size of bachelor males residing in an all-male unit (AMU) in wild black-and-white snub-nosed monkeys (Rhinopithecus bieti). These primates are strict seasonal breeders and live in a modular social system composed of a number of one-male units (OMUs) and an associated peripheral AMU. We found that the AMU social network had a significantly lower density, centralization, clustering coefficient, and smaller clique size during the mating season compared to the non-mating period. However, aggression among AMU males during both mating and non-mating periods was low. Our results suggest that network structure topology in male same-sex social units is modulated by seasonal changes. Bachelor males engage in two types of competition to gain reproductive success: first, which is analogous to contest competition, in which bachelor males act aggressively and challenge OMU leader males in an attempt to take over an OMU; and second, which is more analogous to scramble competition, in which bachelor males avoid aggressive interactions and instead engage in sneaky copulations with fertile females. Our work adds to an understanding of the maintenance of all-male groups in species that form a multilevel society.

Male cooperation for breeding opportunities contributes to the evolution of multilevel societies.

A small number of primate species including snub-nosed monkeys (colobines), geladas (papionins) and humans live in multilevel societies (MLSs), in which multiple one-male polygamous units (OMUs) coexist to form a band, and non-breeding males associate in bachelor groups. Phylogenetic reconstructions indicate that the papionin MLS appears to have evolved through internal fissioning of large mixed-sex groups, whereas the colobine MLS evolved through the aggregation of small, isolated OMUs. However, how agonistic males maintain tolerance under intensive competition over limited breeding opportunities remains unclear. Using a combination of behavioural analysis, satellite telemetry and genetic data, we quantified the social network of males in a bachelor group of golden snub-nosed monkeys. The results show a strong effect of kinship on social bonds among bachelors. Their interactions ranged from cooperation to agonism, and were regulated by access to mating partners. We suggest that an 'arms race' between breeding males' collective defence against usurpation attempts by bachelor males and bachelor males' aggregative offence to obtain reproductive opportunities has selected for larger group size on both sides. The results provide insight into the role that kin selection plays in shaping inter-male cohesion which facilities the evolution of multilevel societies. These findings have implications for understanding human social evolution, as male-male bonds are a hallmark of small- and large-scale human societies.

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.

Aiming low: A resident male's rank predicts takeover success by challenging males in Yunnan snub-nosed monkeys.

In many primate species that form one-male breeding units (OMUs), the threat of a takeover by a bachelor male represents a major challenge to group stability and individual reproductive success. In the case of snub-nosed monkeys, which live in large multilevel or modular societies (MLS) comprising several OMUs that travel, feed and rest together and as well as one or more all male units (AMUs), the process by which rival males challenge resident OMU males for access to females is poorly understood. From September 2012 to October 2013, we recorded 48 cases in which rival males visited an OMU in a MLS of Yunnan snub-nosed monkeys (Rhinopithecus bieti) inhabiting the Baimaxueshan National Nature Reserve, Yunnan Province, China. In 40 cases, rival males engaged in mild agonistic interactions (approaching, staring, teeth-baring and chasing) but failed to take over the group; we counted these visits as failed takeovers, recognizing that they may nevertheless allow rival males to assess the competitive ability of residents. During eight successful takeovers, however, there was severe physical aggression between challenging and resident males, with serious injuries to participants. We found that neither the number of adult and subadult females in an OMU, the number of non-pregnant, non-lactating adult females in an OMU, nor the rank of a resident male relative to other resident males in the MLS predicted which OMU a challenging male targeted for takeover. However, a resident male's rank significantly predicted whether takeover attempts were successful. Specifically, challenging males were more successful in displacing a lower-ranking resident male than a higher-ranking male. Given that a Yunnan snub-nosed monkey MLS may contain as many as 40 resident and 36 bachelor males, continued research is required to determine the set of factors that enable resident males to maintain high social rank and successfully defend their harems. Am. J. Primatol. 78:974-982, 2016. © 2016 Wiley Periodicals, Inc.

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.