Social functions of relaxed open-mouth display in golden snub-nosed monkeys (Rhinopithecus roxellana).

Relaxed open-mouth display serves important social functions in relation to submission, reconciliation, affiliation and reassurance among non-human primate societies; however, quantitative evidence on this behavior remains insufficient among multi-level social groups. From July to November 2016, we examined four potential functions of the relaxed open-mouth display during pairwise, intra-unit social interactions among 18 free-ranging adult and sub-adult golden snub-nosed monkeys (Rhinopithecus roxellana) who belonged to three one-male, multi-female units (OMU) at Dalongtan, Shennongjia National Park, China. Results showed that: compared with no relaxed open-mouth display, (1) the occurrence of displacement by a dominant individual approaching a subordinate was lower and the distance of the subordinate to the approaching dominant was shorter when the subordinate showed open-mouth display; (2) relaxed open-mouth display reduced the probability of continued attack for victims of aggression and allowed victims to achieve closer proximity to the aggressor during post-conflict periods; (3) relaxed open-mouth display by dominant individuals allowed them to achieve closer proximity to subordinates; and (4) the exchange of relaxed open-mouth display had a greater impact on the outcome of interactions than one individual alone giving this signal. These findings suggest that relaxed open-mouth display serves important functions regarding submission, reconciliation, affiliation and reassurance in coordinating social interactions within OMUs in golden snub-nosed monkeys.

Black-and-white snub-nosed monkey (Rhinopithecus bieti) feeding behavior in a degraded forest fragment: clues to a stressed population.

Rapid global deforestation has forced many of the world's primates to live in fragmented habitats, making the understanding of their behavioral responses to degraded and fragmented habitats a key challenge for their future protection and management. The black-and-white snub-nosed monkey (Rhinopithecus bieti) is an endangered species endemic to southwest China. The forest habitat ranges from near-continuous to fragmented. In this study, we investigated the activity budget and diet of a R. bieti population that live in an isolated and degraded habitat patch at Mt. Lasha in Yunnan Province, near the current southern limit of the species. We used our data along with data from six other sites in more-continuous habitats across its range to model factors that predict stress, including feeding effort and time feeding on lichens against potential predictive parameters. Models showed feeding effort across all sites increased with increasing altitude and latitude, and with decreasing food species diversity. There was also a strong positive relationship between feeding effort and time feeding lichens. The Mt. Lasha R. bieti population exploited a total of 36 food species, spending 80.2% of feeding time feeding on lichens, Bryoria spp. and Usnea longissima. These figures are more comparable to those living in the north than those living in the mid- and southern part of the species' range. Given the models for feeding effort and time feeding on lichens, the unexpectedly high time spend feeding on lichens and feeding effort relative to latitude and elevation are suggestive of a stressed population at Mt. Lasha.

Birth seasonality and pattern in black-and-white snub-nosed monkeys (Rhinopithecus bieti) at Mt. Lasha, Yunnan.

Seasonal variation in environmental factors is vital to the regulation of seasonal reproduction in primates. Consequently, long-term systematic data is necessary to clarify the birth seasonality and pattern of primates in highly seasonal environments. This study indicated that black-and-white snub-nosed monkeys (Rhinopithecus bieti) at Mt. Lasha exhibited strict birth seasonality with a pulse model. Infants were born with a certain degree of synchronization. Birth distribution showed three birth peaks, and the birth pattern showed a "V" style in even-numbered years and a gradual increase in odd-numbered years. The beginning date, end date and median birth date were earlier in even-numbered years than those in odd-numbered years. The higher latitude of their habitats, earlier birth date, shorter birth period, fewer birth peaks and stronger birth synchrony might be adaptations for strongly seasonal variation in climate and food resources. After the summer solstice when daylight length began to gradually shorten, R. bieti at Mt. Lasha started to breed during the period with the highest environmental temperature and food availability, which implied that photoperiod may be the proximate factor triggering the onset of estrus and mating. It appears that R. bieti coincided conception and mid-lactation with the peak in staple foods, and weaning with the peak in high quality of foods. Thus, food availability was the ultimate factor regulating reproductive seasonality, and photoperiod was the proximate factor fine-turning the coordination between seasonal breeding and food availability.

Males collectively defend their one-male units against bachelor males in a multi-level primate society.

Group-level male-male co-operation, which has been documented in several primate and non-primate societies, may be mutualistically advantageous to the participants when confronted with threats such as takeovers and cuckoldry by external males. Co-operation among members of distinct social units-while universal among humans-is extremely rare in non-human primates. We present the first observations of collective action or co-operation among males of different one-male units (OMU) in a multi-level society of Rhinopithecus roxellana. A total of 59 instances of male co-operation were recorded. Male co-operation included coordinated chasing, joint vigilance, and patrolling behavior directed at lone adult males trying to enter an OMU. Male co-operation was significantly more frequent during the mating season when the risk of incursions and extra-group paternity was higher. Paternity of infants born in the subsequent birth season and kin relationships among resident males were identified using microsatellite genotype. All infants were sired by OMU males, which we interpret as possible evidence for their success at thwarting mating attempts by satellite males. OMU males were principally unrelated suggesting that male co-operation is best understood in terms of the mutual direct benefits individuals obtain through collective action. Our findings lend support to the bachelor threat hypothesis in which the cooperative behavior of several individuals is more effective than the lone action of a single individual in providing mate defense. Our research has implications for understanding male bonding, higher-level collective action, and the evolution of social co-operation in human societies.

Female snub-nosed monkeys exchange grooming for sex and infant handling.

Allogrooming in primates has acquired an important social function beyond its original hygienic function and can be exchanged either for itself or used as a currency to obtain other benefits such as copulations, access to infants or agonistic support. We explore the strategic use of grooming as a social tool in semi-wild golden snub-nosed monkeys (Rhinopithecus roxellana) in central China, a species where two desirable resources, viz. reproductive males and infants, are restricted to the mating and birth season, respectively. We predict that females expend their grooming selectively to different individuals according to their "value". Our results show that in the mating season, females devoted more grooming to the resident male than in the birth season, and this effect was particularly strong in non-mothers (females without newborn infants). Moreover, females were more likely to groom the resident male after copulation than during baseline social conditions. In the birth season, females devoted more grooming to other females than in the mating season, and mothers (females with newborn infants) were the most valuable grooming partners. The mean rate of contact by non-mothers toward infants of other females was significantly higher after grooming the mothers than in baseline social conditions. In conclusion, our findings lend credence to the notion that primate females use grooming as a strategic tool to obtain limited resources such as males and infants and vary preference for particular individuals depending on the seasonal availability of valuable resources.

[Ecotourism disturbances to non-human primates].

In tandem with economic growth and rising living conditions, ecotourism has increasingly gained popularity among the Chinese public. Non-human primates, as charismatic animals and the closest relatives of human beings, have shown a strong affinity in attracting the general public and raising money, and for that reason a variety of monkey parks, valleys, and islands are becoming increasingly popular in China. Though successful in raising a substantial sum of money for the managing agency of a nature reserve, there may be negative impacts on monkey groups used in ecotourism. Here, to establish effective guards for non-human primates involved in ecotourism, we present a review on tourism disturbance and summarize the negative impacts on behavioral patterns, reproduction, and health condition of animals.

Sleeping tree selection of Cao Vit gibbon (Nomascus nasutus) living in degraded karst forest in Bangliang, Jingxi, China.

We studied the sleep-related behavior of two Cao Vit gibbon (Nomascus nasutus) groups in Bangliang Nature Reserve in Jingxi County, China between January 2008 and December 2009 to test four hypotheses related to sleeping tree selection (predation avoidance, thermoregulation, food access, and range defense). Gibbons entered sleeping trees 88 ± SD 37 min before sunset before their main potential nocturnal predator become active. They usually moved rapidly and straight to sleeping trees and kept silent once settled. Over the course of the study, gibbon groups used many (87 and 57 per group) sleeping trees and reused them irregularly. They also tended to sleep in relatively tall trees without lianas, choosing small branches close to the treetop. These behaviors would make it difficult for potential terrestrial predators to detect and approach the gibbons. Therefore, these results strongly support the predation avoidance hypothesis. Gibbons tended to sleep closer to ridges than to valley bottoms and they did not sleep at lower elevations in colder months. They thus appeared not to select sleeping trees to minimize thermoregulatory stress. Gibbons very rarely slept in feeding trees, instead generally sleeping more than 100 m away from the last feeding trees of the day or the first feeding tree of the next morning. These patterns led us to reject the food access hypothesis. Lastly, we did not find evidence to support the range defense hypothesis because gibbons did not sleep in overlap areas with neighbors more often than expected based on the proportion of overlap and exclusively used areas.

Human influence on the population decline and loss of genetic diversity in a small and isolated population of Sichuan snub-nosed monkeys (Rhinopithecus roxellana).

Human activities have caused worldwide loss and fragmentation of natural habitats, resulting in the decline and isolation of wild populations, consequently increasing their risks of extinctions. We investigated the genetic consequences of anthropogenic effects on the Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Shennongjia Nature Reserve (SNR), which is a small and isolated distribution of R. roxellana in China and would continue to be threatened by habitat degradation and loss, using extensive sampling and 16 microsatellite loci. High level of genetic variation was observed from 202 individuals collected from three R. roxellana populations (SNR population, Sichuan-Gansu population and Shaanxi population). However, R. roxellana in SNR showed the lowest genetic diversity. The likelihood analysis of migration/drift equilibrium indicated that the SNR population suffered much stronger effect of drift than the other two populations, indicating that small populations are prone to be affected by drift. The STRUCTURE analysis identified two clusters, separating the SNR population from the other two populations, suggesting an increasing drift-induced differentiation between SNR and the other two populations. Bottleneck tests revealed that R. roxellana in SNR experienced a severe population decline (37-fold) during the past 500 years as a consequence of human population expansion. The current effective population size (Ne) in SNR is less than 100 and the ratio of Ne to the census population size is approximately 0.08. Based on our findings, we suggest that the SNR population should be monitored systematically and considered as an important conservation and management unit.

Diet and feeding behavior of Rhinopithecus brelichi at Yangaoping, Guizhou.

Expectations of increases in human population growth and accelerated habitat loss, along with the realization that efforts to provide protection for ecosystems that sustain primates have met with limited success, make it critical that conservation plans are grounded firmly in scientific observation. Studies of the diet breadth and feeding behavior of endangered species, therefore, are critical for understanding ecological adaptations and developing a conservation strategy. The diet and feeding ecology of gray snub-nosed monkeys (Rhinopithecus brelichi) were studied in the Fanjingshan National Nature Reserve, Guizhou, China. The monkeys were found to consume 107 different species of trees, shrubs, and ground plants from 58 genera and 28 families. Food items included young leaves, mature leaves, flowers, fruits/seeds, buds, and insects. Among these food items, there were at least 13 evergreen species of tree and liana, 3 species of grasses, and at least 2 kinds of invertebrates collected from decayed wood. Diet varied markedly throughout different seasons. Overall, diet composition (based on feeding records) was 15.3% buds, 25.5% young leaves, 21.8% mature leaves, 9.4% flowers, 21.6% fruits/seeds, and 6.3% other items. The monkeys feed mainly on young leaves and flowers in spring, unripe fruits/seeds and young leaves in summer, ripe fruits/seeds in autumn, and mature leaves and buds in winter. We propose that when inhabiting forests of lower elevation and greater vegetation complexity, R. brelichi is characterized by expanded diet breadth and includes a greater diversity of food types and plant species in its diet. One food type that appears critical to the diet of this species, especially during the winter, are the buds of Magnolia sprengeri. To protect this resource we advocate working with local communities to limit the collection of M. sprengeri, which is used in traditional Chinese medicine and has high economic value for people in the reserve.

Habitat selection of black-and-white snub-nosed monkeys (Rhinopithecus bieti) in Tibet: implications for species conservation.

As anthropogenic habitat changes are often considered a threat to natural ecosystems and wildlife, a sound understanding of the effects of habitat alteration on endangered species is crucial when designing management strategies or performing conservation activities. Black-and-white snub-nosed monkeys (Rhinopithecus bieti) are categorized as endangered on the IUCN Red List and are endemic to the trans-Himalayas in China. At present, there are only 15 groups and 2,500 individuals remaining in the wild, and they are facing intense habitat degradation with selective logging for house building and firewood. Habitat deterioration through wood extraction is occurring at Xiaochangdu, Tibet, where one stable group of R. bieti lives in a marginal habitat in the northernmost part of the species' distribution. To understand the species' response to selective logging in an extremely marginal habitat, data on habitat preference and diet composition of a group of R. bieti were collected at Xiaochangdu from 2003 to 2005. The monkeys used different habitats nonrandomly during the year. The selection index for secondary conifer forest (SC), where selective logging has occurred, was the highest of all habitat types (>1), suggesting that the groups strongly preferred SC. The monkeys fed more on buds/leaves, more on flowers/fruit/seeds, and less on lichen in SC than in primary conifer forest (PC). Dietary diversity was significantly higher in SC than in PC. These results indicate that over the short term, low-intensity disturbances may result in increased foliage diversity that enable groups of R. bieti to survive in this marginal habitat.

Positive influence of traditional culture and socioeconomic activity on conservation: a case study from the black-and-white snub-nosed monkey (Rhinopithecus bieti) in Tibet.

Found in the Trans-Himalayas of north-west Yunnan and south-east Tibet, the black-and-white snub-nosed monkey (Rhinopithecus bieti) is one of the world's most endangered primates. A recent survey indicates that only 15 groups with 2500 individuals remain in the wild. However, the Tibetan Xiaochangdu group may be the only equilibrium group in the field since the last investigation in 1988. To evaluate the effects of traditional culture and socioeconomic activity on biodiversity conservation of R. bieti, we conducted a case study in the Honglaxueshan National Nature Reserve in southeast Tibet from June 2003 to May 2005. Interviews, direct observations, and analysis of socioeconomic data indicated major advantages to the conservation of R. bieti, which included that: 1) traditional culture mainly depended on raising livestock and collecting non-timber products rather than forest planting of Tibetan highland barley; 2) religious beliefs, against to kill any wildlife living on the sacred mountain, were mainly influenced by Tibetan Buddhism; and 3) bigger household numbers were induced by the polyandrous marriage system, which resulted in lower per capita resource consumption than smaller ones.

Male Allocare in Rhinopithecus bieti at Xiaochangdu, Tibet: Is It Related to Energetic Stress.

Male allocare among nonhuman primates has frequently been investigated from the perspective of the caretaker. Here we examined whether male allocare relates to environmental factors or the females' energetic stress. We researched the possible differences of allocare between sexes in free-ranging black-and-white snub-nosed monkeys (Rhinopithecus bieti) in Tibet. A combination of stepwise least squares regression analysis was used to identify the influence of ecological factors (temperature, rainfall, etc.) and infant age that best account for seasonal variation of allocare. The results indicate, except for the functions of infant age, however, that male allocare is a negative function of temperature and female allocare is a positive function of temperature. Specifically, we tested the energetic stress hypothesis, which predicts that the energetic burden of females in a severe environment favour an increased rate of male allocare during the seasons of high energetic stress. We analyzed the allocare difference between high energetic stress season (Mar - Apr), when temperature was low, food availability was scarce, and infants were young, and low energetic stress season (Jun - Aug), based on data obtained during June 2003 - June 2004. Our results supported the energetic stress hypothesis because male allocare in high energetic stress season was higher than that of in low energetic stress season and female allocare was reverse. Therefore, we propose it is the energetic stress on female that make male allocare possible. Male take these interests for other aims and meet some functional hypothesis, which are addressed from the perspective of the male.

Seasonality of mating and birth in wild black-and-white snub-nosed monkeys (Rhinopithecus bieti) at Xiaochangdu, Tibet.

Data on mating and birth seasonality were recorded in wild black-and-white snub-nosed monkeys (Rhinopithecus bieti) at Xiaochangdu in the Honglaxueshan National Nature Reserve, Tibet. This represents one of the harshest habitats utilized by any nonhuman primate. Variation in food availability, temperature, and photoperiod were examined to identify ecological influences on the timing of reproductive events. Mating was observed to occur mostly between July and October and to coincide with peak food availability and temperature, while births occurred between February and mid-March, the end of the period of lowest food availability. This pattern may be an adjustment to the extreme environmental conditions characteristic of this field site.

Social organization of black-and-white snub-nosed monkeys (Rhinopithecus bieti) at Deqin, China.

Data on social organization of two bands of black-and-white snub-nosed monkeys (Rhinopithecus bieti) were collected when the monkeys were crossing an open spot at Nanren and Bamei (northwest of Yunnan, China) using a sampling rule where individuals within one social unit are spatially closer to each other than individuals between social units. The typical pattern of social organization in this sample was multiple adult females (AFs) and their offspring with one adult male (AM) in a one-male unit (OMU), similar to that of many other colobines. In such units, on average one male is associated with 4.0 AFs and 2.5 of their offspring. Moreover, there are multimale/multifemale units and monogamous units besides OMUs. All bisexual units traveled together with at least one all-male unit as a cohesive band. In two bands of monkeys, 87% of AMs in bisexual units were within OMUs, 7.8% within monogamous units and 5.2% within multimale, multifemale units. In the Bamei band, 6.7% of AMs were in the all-male unit. The size of OMUs in the Nanren band was larger than that of the Bamei band, with more AFs and juveniles, which may be related to better conservation in the Nanren band's habitat. For the Nanren band, the average number of AFs in OMUs varied across time, increasing from 4.3 in 1994 to 5.1 in 2001, and then decreasing to 3.8 in 2005. This article suggests three possible explanations for this variation, but more data are needed for these hypotheses to be tested.

Diet and feeding behavior of Rhinopithecus bieti at Xiaochangdu, Tibet: adaptations to a marginal environment.

The diet and feeding ecology of a wild subpopulation of black-and-white snub-nosed monkeys (Rhinopithecus bieti) were studied at Xiaochangdu in Honglaxueshan Nature Reserve, Tibet. This region is climatologically harsher than any other inhabited by non-human primates. Black-and-white snub-nosed monkeys fed on 48 parts of 25 plant species, at least three species of lichens and seven species of invertebrates. The number of food items exploited varied markedly among seasons, with dietary diversity being greatest in spring and summer. In winter, black-and-white snub-nosed monkeys had to subsist on fallback foods such as dried grass and bark. Ubiquitous lichens formed a major dietary constituent throughout the year, contributing about 75% of feeding records. Even though lichens act as a staple, our findings signify that the monkeys at Xiaochangdu prefer feeding on foliage, which is higher in protein content than the former. We provide evidence that black-and-white snub-nosed monkeys are able to cope with an array of food items other than lichens and hence can be regarded as feeding generalists. We discuss the results with reference to previous studies on other subpopulations living in habitats that are floristically more diverse and offer more plant food items than the marginal habitat at Xiaochangdu.

First direct evidence of infanticide and cannibalism in wild snub-nosed monkeys (Rhinopithecus bieti).

Although infanticide has been witnessed in many species of Colobinae, and a case was observed in a captive group of golden snub-nosed monkeys (Rhinopithecus roxellana), observed cases of infanticide in wild snub-nosed monkeys (Rhinopithecus spp.) have not previously been recorded. Here we describe the killing of a 1-month-old infant by a male in a black-and-white snub-nosed monkey (R. bieti) group at Xiaochangdu in Tibet. The infanticidal attack was witnessed as part of a long-term observational study of ecology and behavior that began in June 2003. The male was observed killing and eating the infant. The literature proposes three main explanations for infanticide: two adaptive hypotheses (sexual selection and resource competition), and one nonadaptive hypothesis (social pathology). Individual cases of infanticide, such as this one, are important for comparative purposes, but when examined on their own they are difficult to interpret in relation to established theoretical frameworks. The cases we describe here show some consistency with the sexual selection hypothesis, but the lack of critical information (i.e., as to paternity) makes it impossible to draw a firm conclusion. This is also the first described case of cannibalism in snub-nosed monkeys.