Assessing the Impact of Village Development on the Habitat Quality of Yunnan Snub-Nosed Monkeys Using the INVEST Model.

The habitats of the already endangered Yunnan snub-nosed monkey (Rhinopithecus bieti) are degrading as village economies develop in and around these habitat areas, increasing the depopulation and biodiversity risk of the monkey. The paper aims to show the areas of these monkeys' high-quality habitats that are at highest risk of degradation by continued village development and hence be the focus of conservation efforts. Our analysis leveraged multiple tools, including primary component analysis, the InVEST Habitat-Quality model, and GIS spatial analysis. We enhanced our analysis by looking at habitat quality as it relates to the habitat suitability for the monkey specifically, instead of general habitat quality. We also focused on the impact of the smallest administrative scale in China-the village. These foci produced a clearer picture of the monkeys' and villages' situations, allowing for more targeted discussions on win-win solutions for both the monkeys and the village inhabitants. The results show that the northern habitat for the monkey is currently higher quality than the southern habitat, and correspondingly, the village development in the north is lower than in the south. Hence, we recommend conservation efforts be focused on the northern areas, though we also encourage the southern habitats to be protected from further degradation lest they degrade beyond the point of supporting any monkeys. We encourage developing a strategy that balances ecological protection and economic development in the northern region, a long-term plan for the southern region to reduce human disturbance, increase effective habitat restoration, and improve corridor design.

Impact of cost distance and habitat fragmentation on the daily path length of Rhinopithecus bieti.

An understanding of primate movement patterns in response to natural and anthropogenically induced changes in habitat heterogeneity, food availability, and plant species distribution is essential for developing effective management and conservation programs. Therefore, from July 2013 to June 2014, we examined the effects of landscape configuration on the ranging behavior (daily path length, DPL) of the Endangered Yunnan snub-nosed monkey (Rhinopithecus bieti) in the Baimaxueshan National Nature Reserve (27°34'N, 99°17'E) in Gehuaqing, China. Given the extreme difficulties in following the study group across high altitude mountainous terrain across an elevation of 2,500-4,000 m, we were only able to collect DPL using 3-4 GPS points per day on 21 individual days. We found that R. bieti traveled the shortest DPL in winter (1,141.31 m), followed by spring (2,034.06 m) and autumn (2,131.19 m). The cost distance, a statistical tool designed to estimate the difficulty of a species moving across its distributional range, was lowest in autumn (205.47), followed by spring (225.93) and winter (432.59) (one-way ANOVA: F = 3.852, P = 0.026, df = 2). The habitat fragmentation index (HFI), which measures the density of forest patches, indicated areas visited in the winter were more fragmented (HFI = 2.16) compared to spring (HFI = 1.83) or autumn (HFI = 1.3). Although our results should be considered preliminary, they suggest that both the availability of suitable travel routes and habitat fragmentation, driven by high-intensity human disturbance, constrain the movement of R. bieti. We found that undisturbed areas of the bands' range contained a high density of lichens, which represent a nutritious and abundant and year-round food source for Yunnan snub-nosed monkeys. In order to protect this Endangered species, we recommend that researchers construct detailed maps of landscape heterogeneity, particularly habitat connectivity, forest fragmentation, and seasonal variation in the location of major food patches in order to better understand and mitigate the effects of seasonal habitat change on patterns of R. bieti habitat utilization and population viability.

Preliminary report on Sichuan golden snub-nosed monkeys (Rhinopithecus roxellana roxellana) at Laohegou Nature Reserve, Sichuan, China.

Comparative studies of subspecies under different ecological environments offer insights into intraspecies evolutionary adaptive mechanisms. Golden snub-nosed monkeys (Rhinopithecus roxellana) include three subspecies in China classified mainly by their morphological variations: R. r. roxellana (Sichuan and Gansu province), R. r. qinlingensis (Shaanxi province) and R. r. hubeiensis (Hubei province). These three subspecies live in three isolated area with different environments. Past works focused on the last two subspecies, but little information of habitat and behaviors of the nominated subspecies (R. r. roxellana) is available to date. We conducted a two-year study on the diet, activity budget, home range and social organization of 4 herds of R. r. roxellana, based on a total of 106 days' observation in Laohegou (LHG) Nature Reserve, Sichuan province. By using scan sampling method, our results suggest that the R. r roxellana feeds predominantly on leaves (77.5%), and spends more time feeding (40.0%) and resting (27.0%) while compared to the other two subspecies. Kernel Density Estimation Method based on GPS technology confirms that R. r roxellana has relatively larger home ranges (49.1 km2). The unit size (8.3 ± 3.5 individuals) of R. r roxellana is also smaller. Therefore, it is possible that differences in food availability in relation to habitats have important impacts on the feeding strategy and social system of the golden snub-nosed monkey. These results provide data to further explore intraspecific adaptations of living 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 pattern-mixture model with nonfuture dependence and shift in current missing values.

For incomplete continuous longitudinal data with a monotone pattern, we study a pattern-mixture model which assumes that missingness only depends on observed data and the current missing value, and that the conditional distribution of the current missing value differ from that of the observed patterns by location and scale shifts. The shift parameters measure the departure from the missing at random mechanism. We show that a numerical or Monte Carlo approximation is needed to obtain the posterior draw of the mean at the final time point as a function of the posterior draw of the observed data model parameters and shift parameters, and that scale shifts have negligible impact on the estimated mean at the final time point. We use multiple imputation to avoid numerical integration and demonstrate that the usual multiple imputation variance estimator is valid for the estimated mean at the final time point when scale shifts are not considered. The multiple imputation method is applied to a clinical study of major depressive disorders.

Differences in the activity budgets of Yunnan snub-nosed monkeys (Rhinopithecus bieti) by age-sex class at Xiangguqing in Baimaxueshan Nature Reserve, China.

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.

Evidence of allomaternal nursing across one-male units in the Yunnan snub-nosed monkey (Rhinopithecus Bieti).

BACKGROUND: Allomaternal nursing, common in several species of social mammals, also has been reported in nonhuman primates. However, the function of this behavior in enhancing infant survivorship remains poorly understood. METHODOLOGY AND PRINCIPAL FINDINGS: The study was conducted on a free-ranging group of the Yunnan snub-nosed monkey (Rhinopithecus bieti) in the Baimaxueshan Natural Reserve. Direct observation and ad libitum sampling were used to record allocare behavior during a 20 month field study. R. bieti exhibits a multilevel social organization in which a large single troop, consisting of over 100 individuals, is divided into many one-male units (OMUs: 6∼41). These OMUs coordinate their daily activities, and feed, forage, travel, and rest together. Here we report on one case of infant temporary adoption in which an adult female from one OMU engaged in allomaternal nursing and cared for an infant from a different OMU of the same troop. This event began when the mother and her five-month-old infant were found to became separated accidentally. The victim infant was observed staying in another OMU. Over the next several days we observed a lactating female in the new OMU to care for and nurse both her infant and the immigrant infant, who also was tolerated by and cared for by the harem male. CONCLUSIONS AND SIGNIFICANCE: Our findings suggest that lactating primate females are primed to care for young infants and, that the misdirected parental care hypothesis may offer the strongest explanation for allomaternal nursing in R. bieti.

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.