Geophagy of Yunnan snub-nosed monkeys (Rhinopithecus bieti) at Xiangguqing in the Baimaxueshan Nature Reserve, China

Sleeping site locations are important to free-ranging primate groups. Sites are strategically selected by primates so as to optimize security, comfort and foraging efficiency. Data were collected on the distribution of sleeping sites of the Yunnan snub-nosed monkey (Rhinopithecus bieti) between Sep 2005 and Sep 2006 at Gehuaqing in Baimaxueshan Nature Reserve, China. We identified 54 sleeping sites, which were used 137 times during the study period. These sleeping sites were distributed throughout the monkey group's total home range. R. bieti preferred certain sleeping sites over others: 63% of the sleeping sites were used 2 or more times in 13 months. Groups reused locations in an unpredictable long-term pattern, but avoided using the same sleeping site on consecutive nights. To reduce the time and energetic costs of travel, monkeys preferred sleeping near commonly used feeding sites. We recorded 124 feeding sites in the home range, which were used 174 times. A total of 27 sleeping sites were also feeding sites, and all remaining sleeping sites were close to feeding sites. There was a positive correlation between the intensity of use of sleeping sites and feeding sites. The present study suggests that the availability and the location of immediate sources of food is a key factor in the choice of sleeping sites.

Natural disasters such as snow storms have far-reaching effects on variations in the habitat structure and ecological aspects of non-human primates. Yunnan snub-nosed monkeys (Rhinopithecus bieti) inhabit high-altitude forest and endure harsh winters. The effect of heavy snow-storms (January 19 to February 6, 2008) on two large groups of R. bieti (Gehuaqing group and Xiangguqing group) inhabiting Samage Forest in the Baimaxueshan Nature Reserve were assessed. Data on habitat damage were collected between March and May 2008 via field line sampling. The snow storms destroyed 237 big trees in the Samage Forest. The destroyed trees were mostly located along the mountain ridge and valley including Abies georgei, Tsuga dumosa, Pinus yunnanensis and Cyclobalanopsis oxyodon. These trees were important for R. bieti as they provide a dietary source of lichen that is a critical winter fallback food for this primate species, and consequently food availability for R. bieti was reduced. Our results also showed that two juveniles in the Gehuaqing group and three juveniles in the Xiangguqing group were found deceased following the storms. The fact indicates that R. bieti is well adapted to high altitude and strongly seasonal habitat might explain its resilience to heavy snow storms.

High-altitude dwelling primates have to optimize navigating a space that contains both a vertical and horizontal component. Black-and-white or Yunnan snub-nosed monkeys (Rhinopithecus bieti) are extreme by primate standards in inhabiting relatively cold subalpine temperate forests at very high altitudes where large seasonal variation in climate and food availability is expected to profoundly modulate their ranging strategies so as to ensure a positive energy balance. A “semi-nomadic” group ofR. bietiwas followed for 20 months in the montane Samage Forest, Baimaxueshan Nature Reserve, Yunnan, PRC, which consisted of evergreen conifers, oaks, and deciduous broadleaf trees. The aim of this study was to disentangle the effects of climate and phenology on patterns of altitudinal range use. Altitude used by the group ranged from a maximum of 3550 m in July 2007 to a minimum of 3060 m in April 2006. The proportional use of lichen, the monkeys’ staple fallback food, in the diet explained more variation in monthly use of altitudes than climatic factors and availability of flush and fruit. The abundance of lichens at high altitudes, the lack of alternative foods in winter, and the need to satisfy the monkey's basal energetic requirements explain the effect of lichenivory on use of altitudes.

The activity budgets of primates reflect their survival strategy. Despite existing data on the activity budgets of Yunnan snub-nosed monkeys (Rhinopithecus bieti), little is known about how activity budgets vary between age-sex classes. This study provides the first detailed activity budgets subdivided by age-sex class, based on observations of the largest habituated group of R. bieti at Xiangguqing in Baimaxueshan Nature Reserve. This study was conducted from June 2008 to May 2009. We found that adult females spent more time feeding (44.8%) than adult males (39.5%), juveniles (39.1%) and infants (14.2%). Females allocated significantly more time to feeding than to any other activity. Adult males allocated more time to miscellaneous activities (12.5%) than adult females (3.8%). Juveniles allocated less time to grooming than adults. Infants were being groomed 6.9% of the time, the highest proportion among all age-sex classes. Adults spent more time feeding, while immature individuals allocated more time to moving and other activities. There are several reasons why activity budgets can vary by age-sex class: (1) differential reproductive investment between males and females; (2) developmental differences among the age categories, and (3) social relationships between members of different age-sex classes, particularly dominance. These variations in activity budgets among the different age-sex classes may become a selective pressure in this species.

How a nonhuman primate mother responds to her dead infant is an indication of maternal behavior and perspectives on death. Here we describe three cases of a mother's response toward her dead infant in Yunnan snub-nosed monkeys (Rhinopithecus bieti) at Baimaxueshan Nature Reserve in Yunnan, China. The mother, whose infant died at 1month of age, showed strong maternal affection to the corpse and carried it for 4days. A mother with a stillborn infant showed similar maternal behavior to her dead offspring, but only held it for 1day. The mother of an aborted infant abandoned the carcass without carrying it or displaying other forms of maternal behavior. Our results suggest that the mother-infant bond in the Yunnan snub-nosed monkey is strongly influenced by the infants' age. Postdeath infant-carrying behavior could be affected by the combined action of reproductive hormones and the emotional response of the mother. This manuscript represents the first detailed report of a mother carrying her dead infant in this endangered monkey species.

The Yunnan snub-nosed monkey (Rhinopithecus bieti) is characterized by a larger home range and group size than other colobine species. We investigated variations in home range size of a free-ranging group of R. bieti from 1998 to 2007 in the Baimaxueshan National Nature Reserve in Yunnan, China. Group size increased from 160 to 450 over the 10 years. Results also showed a home range shift and yearly home range expansion, although this expansion was very limited. The study group covered a 33.78-km² area during the 10-year period, with some areas abandoned and others used repeatedly. The yearly home range increase stopped in 2004 and decreased thereafter. Despite increasing group size usually being coupled with larger yearly home range (>30 km²), the group confined itself within a relatively small and stable area (<18 km²) during 2005–2007, with a significant portion of their accessible home range discarded. Consequently, the study group showed the highest recorded population density among extant groups of R. bieti. Reasons why the group settled into a substantially smaller home range area remain unclear.

Ecological factors are known to influence the activity budgets of Yunnan snub-nosed monkeys (Rhinopithecus bieti). However, little is known about how activity budgets vary between age/sex classes, because the species is difficult to observe in the wild. This study provides the first detailed activity budgets subdivided by age/sex classes based on observations of the largest habituated group at Xiangguqing in Baimaxueshan Nature Reserve. This study was conducted from June 2008 to May 2009. We found that adult females spent more time feeding (44.8%) than adult males (39.5%), juveniles (39.1%), and infants (14.2%). Adult males allocated more time to miscellaneous activities (12.5%) than did adult females (3.8%). Infants were being groomed 6.9% of the time, which was the highest proportion among all age/sex classes. Adults spent more time feeding, while immature individuals allocated more time to moving and other activities. There are several reasons activity budgets may vary by age/sex class: 1) differential reproductive investment between males and females; 2) developmental differences among the age categories; 3) social relationships between members of different age/sex classes, particularly dominance. In addition, group size and adult sex ratio may also impact activity budgets. These variations in activity budgets among the different age/sex classes may become a selective pressure that shapes the development and growth pattern in this species. &lt;br&gt;&lt;br&gt;&lt;font color="red"&gt;&lt;b&gt; This article has been retracted. Link to the retraction &lt;u&gt;&lt;a href="http://dx.doi.org/10.2298/ABS160112009E"&gt;10.2298/ABS160112009E&lt;/a&gt;&lt;u&gt;&lt;/b&gt;&lt;/font&gt;

The appearance of tourists brings about behavioural changes in some primates. Primate behavioural responses to human activities can reflect their survival strategy. Little is known about how the behaviour of Rhinopithecus bieti changes in the presence of tourists. Here we provide the first detailed description of interactions between a provisioned group of R. bieti and tourists at Xiangguqing in Baimaxueshan Nature Reserve from July 2012 to June 2013. We found that R. bieti had different response rates to the 5 most common human actions (shout, photograph, offer food, clap, and wave). Results indicated that R. bieti expresses 10 behavioural reactions (threat, escape, vigilance, warning, panic, alliance, attack, foraging, approach, and staring) to tourists' actions. On the whole, most of the monkeys' responses were unfriendly or hostile; a small number were neutral and affiliative. Behavioural responses were also significantly different among the different age/sex classes. Immature individuals engaged in more affiliative behaviours than adult individuals, and adult males tended towards more hostile behaviours. The behaviour of R. bieti towards tourists showed both tension and adaptability. Scientific management of provisioned monkey groups and strict regulation of tourist behaviour is needed in order to protect the animals from the negative effects of tourism-related disturbance.

We quantified the home range and explored the style of ranging of black-and-white snub-nosed monkeys (Rhinopithecus bieti) in the subtropical-temperate montane Samage Forest (part of Baimaxueshan Nature Reserve) in the vicinity of Gehuaqing. Over 14.5 mo, we took positional records of the study band via a GPS receiver at 30-min intervals, and found that they covered an area of 32 km2. Over a 10-yr period, the group even ranged in an area of 56 km2, which is among the largest home range estimates for any primate. The large home range was probably due to the combined effects of large group size (N > 400) and forest heterogeneity, with seasonally food-rich areas interspersed with less valuable areas. The subjects did not use their home range uniformly: 29% of the grid cells had more location records than expected based on a uniform distribution, thus representing a core area, albeit a disjunct one. A continuous 1-mo group follow in the fall revealed that the band traveled on average 1.62 km/d and that days of concentrated use of a particular forest block were followed by more extensive marches. Neither climate nor human disturbance parameters correlate significantly with monthly estimates of the group’s home range size. Even though there is no significant correlation between temporal availability of plant phenophases and range size, our observations implicate temporal and spatial availability of food as a determinant of home range use of the focal group. Winter, spring, and summer home ranges are equally large: 18.2, 17.8, and 18.6 km2, respectively. Home range decreased markedly in fall (9.3 km2), probably because the band obtained sufficient food resources (fruit) in a smaller area. The large winter range is best attributed to the exploitation of dispersed clumped patches of mature fruits.

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.

Here we provide a preliminary assessment of dietary and habitat requirements of two sympatric primate taxa, a "simple-stomached" and "complex-stomached" species (Rhinopithecus bieti Colobinae vs. Macaca mulatta Cercopithecinae), as a basis for illuminating how the two coexist. Of ca. 22 plant food species consumed by the macaques, at least 16 were also eaten by the snub-nosed monkeys. Both species showed a preference for fruits. While the snub-nosed monkeys did not utilize any resources associated with human communities, rhesus macaques did occasionally raid agricultural crops. The mean elevation of the snub-nosed monkey group was 3,218 m, while the mean elevation of the macaque group was 2,995 m. Macaques were also spotted on meadows whereas snub-nosed monkeys evidently avoided these. For both species, mixed deciduous broadleaf/conifer forest was the most frequently used ecotype, but whereas evergreen broadleaf forest (Cyclobalanopsis community) accounted for only 3% of the location records of the snub-nosed monkeys, it accounted for 36% of the location records of the macaques. Groups of the two species usually kept a considerable spatial distance from one another (mean 2.4 km). One close encounter and confrontation between groups of the two species resulted in the macaque group moving away. Our findings suggest that the coexistence of the two taxa is facilitated via differential macrohabitat use and spatial avoidance. Although divergent habitat-use strategies may reflect interspecific competition, they may also merely reflect different physiological or ecological requirements.

Individual dispersal trends, unquestionably important for species ecology and evolution, are affected by multiple factors. Understanding the factors that influence female dispersal strategies offers important insight into primate dispersal mechanisms and female choice. To investigate the proximate causes of dispersal in female Yunnan snub-nosed monkeys (Rhinopithecus bieti), we observed and analyzed nine years of detailed dispersal and demographic data from a population of R. bieti in Xiangguqing, Baimaxueshan Nature Reserve, Yunnan Province, China. Results showed that females who lived long-term in a one-male unit (OMU), without giving birth and with few or no relatives, were more likely to leave that OMU. In addition, an OMU led by an outgroup male and containing more female relatives was significantly more likely to be chosen for immigration. Conversely, greater male age, longer male tenure, and more potentially fertile females discouraged immigration into an OMU. These results suggest that reproduction, male quality, and kin cooperation play the largest roles in female Yunnan snub-nosed monkey dispersal.

Temperate forests are characterized by pronounced climatic and phenological seasonality. Primates inhabiting such environments experience prolonged resource scarcity and low ambient temperatures in winter and are expected to adjust time allocation and foraging behavior so as to maintain their energy balance. We analyzed the activity scheduling of a group of Yunnan snub-nosed monkeys (Rhinopithecus bieti) based on data collected over 20months in the high-altitude (>3000m) Samage Forest, Baimaxueshan Nature Reserve, PRC. The forest consists of evergreen conifers and oaks and deciduous broadleaf trees. The diet varied seasonally, with young leaves preferentially exploited in spring and fruits in summer. The monkeys subsisted on readily available fallback resources (mainly lichens) in winter [Grueter et al. in (Am J Phys Anthropol 140:700-715, 2009)]. We predicted that this switch to a relatively low-quality diet would prompt an increase in feeding effort and decrease in moving effort. We found that the monkeys spent significantly more time feeding in winter than in the other seasons. The monthly time devoted to feeding was also negatively correlated with temperature and positively with percentage of lichens in the diet. Time spent on moving did not vary among seasons or with temperature, but day-journey length was found to be longer on hotter days. Time spent resting was lower in winter and under colder conditions and was also negatively correlated with time spent feeding, indicating that resting time is converted into feeding time during times of ecological stress. These results indicate a strong effect of seasonality on time allocation patterns, constraints on inactivity phases, and the prevalence of an energy-conserving foraging strategy in winter, when costs of thermoregulation were high and the availability of preferred food was low.

Primate home range sizes can vary tremendously as a consequence of the analytical technique chosen to estimate home range. This is exemplified by a recent dataset on free ranging snub-nosed monkeys (Rhinopithecus bieti) in Northwest Yunnan, China. Our findings show that the grid cell method cannot substitute for the minimum convex polygon (MCP) method and vice versa. MCP-based estimates are far too large, especially when the form of the home range is irregular due to forays into peripheral areas. Here, we propose an adjusted polygon method, whereby unsuitable and never visited areas are clipped out from the polygon, thus producing more accurate results. Compared to the grid cell method, the adjusted MCP is much more robust when the number of group relocations is limited; MCP turned out to be the method of choice for calculation of monthly and seasonal home ranges. The grid cell method on the other hand yielded the most precise estimates for total or annual home ranges. The style of ranging exhibited by a given primate taxon or population determines which analytical procedures should be applied to estimate home range size, and we would stress the need for thorough evaluation of the pros and cons of home range estimators before conducting field work and analysing data.

An increasing number of studies have found that the implementation of feeding sites for wildlife-related tourism can affect animal health, behaviour and reproduction. Feeding sites can favour high densities, home range overlap, greater sedentary behaviour and increased interspecific contacts, all of which might promote parasite transmission. In the Yunnan snub-nosed monkey (Rhinopithecus bieti), human interventions via provisioning monkeys at specific feeding sites have led to the sub-structuring of a group into genetically differentiated sub-groups. The fed subgroup is located near human hamlets and interacts with domesticated animals. Using high-throughput sequencing, we investigated Entamoeba species diversity in a local host assemblage strongly influenced by provisioning for wildlife-related tourism. We identified 13 Entamoeba species or lineages in faeces of Yunnan snub-nosed monkeys, humans and domesticated animals (including pigs, cattle, and domestic chicken). In Yunnan snub-nosed monkeys, Entamoeba prevalence and OTU richness were higher in the fed than in the wild subgroup. Entamoeba polecki was found in monkeys, pigs and humans, suggesting that this parasite might circulates between the wild and domestic components of this local social–ecological system. The highest proportion of faeces positive for Entamoeba in monkeys geographically coincided with the presence of livestock and humans. These elements suggest that feeding sites might indirectly play a role on parasite transmission in the Yunnan snub-nosed monkey. The implementation of such sites should carefully consider the risk of creating hotspots of disease transmission, which should be prevented by maintaining a buffer zone between monkeys and livestock/humans. Regular screenings for pathogens in fed subgroup are necessary to monitor transmission risk in order to balance the economic development of human communities dependent on wildlife-related tourism, and the conservation of the endangered Yunnan snub-nosed monkey.