Population and conservation status of a transboundary group of black snub-nosed monkeys (Rhinopithecus strykeri) between China and Myanmar

Population and conservation status of a transboundary group of black snub-nosed monkeys(Rhinopithecus strykeri)between China and Myanmar

The responses of nonhuman primates towards conspecific deaths in the wild, and the activities of carnivores scavenging the corpses, are different but interconnected thanatological and ecological aspects of wildlife mortality. We report the first thanatological events observed in a wild, multilevel group of Myanmar or black snub-nosed monkeys (Rhinopithecus strykeri [R. strykeri]) and mesocarnivores scavenging on a monkey carcass in the Pianma region, near the China-Myanmar border. We detected two freshly deceased carcasses during field surveys. The group members visited the location of their recently deceased conspecific twice and variously looked down at the carcass, emitted alarm calls and unusual contact calls, hugged social partners and prevented approaches by individuals from other social units. These behaviors suggest strong bonds and emotional reactions to the death of a companion in R. strykeri. Infrared camera trapping revealed the Siberian weasel (Mustela sibirica) as the principal scavenger on the carcass, followed by the yellow-throated marten (Martes flavigula). Siberian weasels showed greater activity levels and time spent feeding on the R. strykeri carcass when it was fresh, while remaining vigilant for potential competitors and predators. After the carcass was largely consumed and decayed, both frequency and duration of feeding and vigilance behaviors decreased.

Hybridization is widely recognized as promoting both species and phenotypic diversity. However, its role in mammalian evolution is rarely examined. We report historical hybridization among a group of snub-nosed monkeys (Rhinopithecus) that resulted in the origin of a hybrid species. The geographically isolated gray snub-nosed monkey Rhinopithecus brelichi shows a stable mixed genomic ancestry derived from the golden snub-nosed monkey (Rhinopithecus roxellana) and the ancestor of black-white (Rhinopithecus bieti) and black snub-nosed monkeys (Rhinopithecus strykeri). We further identified key genes derived from the parental lineages, respectively, that may have contributed to the mosaic coat coloration of R. brelichi, which likely promoted premating reproductive isolation of the hybrid from parental lineages. Our study highlights the underappreciated role of hybridization in generating species and phenotypic diversity in mammals.

Colobines are a unique group of Old World monkeys that principally eat leaves and seeds rather than fruits and insects. We report the sequencing at 146× coverage, de novo assembly and analyses of the genome of a male golden snub-nosed monkey (Rhinopithecus roxellana) and resequencing at 30× coverage of three related species (Rhinopithecus bieti, Rhinopithecus brelichi and Rhinopithecus strykeri). Comparative analyses showed that Asian colobines have an enhanced ability to derive energy from fatty acids and to degrade xenobiotics. We found evidence for functional evolution in the colobine RNASE1 gene, encoding a key secretory RNase that digests the high concentrations of bacterial RNA derived from symbiotic microflora. Demographic reconstructions indicated that the profile of ancient effective population sizes for R. roxellana more closely resembles that of giant panda rather than its congeners. These findings offer new insights into the dietary adaptations and evolutionary history of colobine primates.

The black or Myanmar snub-nosed monkey (Rhinopithecus strykeri) was discovered in the Gaoligong Mountains of northeastern Kachin state, Myanmar in 2010, and was subsequently found in the mountains of northwestern Yunnan, China in 2011. Across these regions, there were an estimated 14-15 groups with approximately 950 individuals in total. However, teams of people conducting field surveys and camera trap studies, of which I was part, only confirmed five sub-populations with 400 individuals on the Sino-Myanmar border from data collected 2012-2017. Based on approximately two years field searching, I and my colleagues discovered one population (Luoma group) in the Gaoligong Mountains and conducted another 203 days of field observation to collect dietary data. I also conducted cafeteria feeding trials with 600 wild plant species on two captive individuals housed at Yaojiaping Wildlife Rescue Centre in the Gaoligong Mountains National Nature Reserve. I found that black snub-nosed monkeys can consume 593 items from more than 170 food plants of trees, bushes, and herbs representing 76 genera and 41 plant families, as well as 15 species of lichen. Among these food items and species, 14 plant species and four lichen species also are consumed by the wild monkeys as well. The food plants mainly distribute in intact sub-tropical evergreen broadleaf forests and hemlock-broadleaf mixed forests at an altitude of 2200-3000 m. Based on interview surveys, camera trap records, and habitat distribution modelling, I confirm this is the main elevational range used by the black snub-nosed monkey species. Nutritional studies and comparisons of 100 leaf samples the monkeys selectively consumed (70 species) with the nutrient content of 54 leaf samples (48 plant species) the monkeys' avoided in spring and autumn reveal that black snub-nosed monkey preferentially select leaves higher in free water content, crude protein, and phosphorus , and avoid leaves with a higher neutral detergent fibre content, which is similar to other snub-nosed monkeys. Using interview-based survey data and MAXENT modelling of black snub-nosed monkey along the Sino-Myanmar border, I found that black snub-nosed monkey inhabit high-quality habitat at 1420 km2, medium-quality habitat at 750 km2, and low-quality habitats at 1410 km2. Only 13.9% of the highly suitable habitat (medium + core habitat) for black snub-nosed monkey falls within protected areas in China. Approximately 2.6% of the entire habitat has been lost in the past 15 years, 96% of which has been in Myanmar. Two national parks (Imawbum NP in Myanmar and Nujiang Grand Canyon NP in China) are therefore proposed for saving this species. Lastly, for structuring a systematic transboundary conservation network in the highly-biodiverse but poorly-studied Gaoligong Mountains region, I used interview-based survey results (on animal distribution data) of three taxa (Primates, Pheasants and Mishmi Takin) and identified five flagship species (R. strykeri, Hoolock tianxing, Trachypithecus shortridgei, Lophophorus sclateri, Budorcas taxicolor) as surrogates of community biodiversity in the Gaoligong Mountains. After confirming the reliability of species distribution data via selective field surveys, I applied multicriteria decision analysis techniques along with data on habitat suitability (MAXENT Model) to highlight areas for transboundary conservation efforts. My results indicate that approximately 83.4% (10,398.7 km2) of remaining habitat with high conservation value for each of the five flagship species is unprotected. This includes six large zones separated by rivers and human settlements that should be designated as transboundary World Nature Heritage, National Parks, or Wildlife sanctuaries along the northern Sino-Myanmar border. Accordingly, I propose related conservation actions and policies for transboundary conservation in the Gaoligong Mountains.

Since its initial discovery in 2010 in the Gaoligong Mountains on the Sino-Myanmar border, there remains no direct information on the feeding habits of the black snub-nosed monkey (Rhinopithecus strykeri). This species is on the verge of extinction, with an estimated remaining population of < 400 individuals. Due to difficulties in following these monkeys across steep mountainous terrain, during 203 observation days (September 2015-January 2017) we recorded 80h of behavioral records of a wild population (Luoma group). Our preliminary results identified 14 plant species and four lichen species consumed by the monkeys. In addition, we provided the only two captive individuals of this species with a cafeteria diet composed of > 600 wild-collected plant species that were gathered from known R. strykeri habitats to determine which plant species and food items were considered palatable. Our results indicate that the captive monkeys freely consumed young and mature leaves, fruits/seeds, buds, flowers, twigs, and bark from 170 different species of trees, bushes, and herbs representing 76 genera and 41 plant families, as well as 15 species of lichen. All foods consumed by the wild monkeys were also consumed by the captive individuals. Food plants consumed by R. strykeri were found principally in intact subtropical evergreen broadleaf forests and hemlock-broadleaf mixed forests at an altitude of 2200-3000m. Strict enforcement of habitat protection and access to resources across this elevation zone appear to be essential for the conservation and survivorship of this critically endangered primate.

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.

The Gaoligong Mountains, located in the southeastern Tibetan Plateau, is one of the world's biodiversity hotspots and provides a refugium for many endangered endemic animals. In this study, we reported a population genetic study on black snub-nosed monkey (Rhinopithecus strykeri), a critically endangered primate endemic to the Gaoligong Mountains, yet their large-scale population genetic study remains underexplored. Here, we performed population genetic analyses from two geographical populations (Pianma and Luoma) based on targeted genomic single-nucleotide polymorphism (SNP) data (37.7 K) and mitochondrial DNA (mtDNA) control region (842 bp). Both nuclear SNP data and mtDNA revealed relatively low levels of genetic variation in both populations compared to other reported primates, which is most likely to be explained by loss of historical genetic diversity due to inbreeding and long-term small effective population size, thus potentially aggravating the effects of inbreeding and genetic depression. Phylogenetic and population structure analyses for mtDNA revealed two deep lineages (approximately 0.69 million years ago), but limited genetic differentiation in nuclear data, which might have been caused by the Late Cenozoic uplift of the Tibetan Plateau and glacial refuge, and subsequent secondary contact as a result of historically high and bidirectional gene flow between populations. Ecological niche modeling and landscape connectivity analyses also showed historical and recent connectivity between two geographical populations. The demographic history inferred from both mtDNA and nuclear data revealed at least two continuous declines in the effective population size occurring around 43 Kya and 8-10 Kya, respectively, probably due to Pleistocene glaciations and subsequent human activities. Our results provide the first detailed and comprehensive genetic insights into the genetic diversity, population structure, and demographic history of a critically endangered species, and provide essential baseline information to guide conservation efforts.

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.

The snub-nosed monkey genus Rhinopithecus (Colobinae) comprises five species (Rhinopithecus roxellana, Rhinopithecus brelichi, Rhinopithecus bieti, Rhinopithecus strykeri, and Rhinopithecus avunculus). They are range-restricted species occurring only in small areas in China, Vietnam, and Myanmar. All extant species are listed as endangered or critically endangered by the International Union for Conservation of Nature (IUCN) Red List, all with decreasing populations. With the development of molecular genetics and the improvement and cost reduction in whole-genome sequencing, knowledge about evolutionary processes has improved largely in recent years. Here, we review recent major advances in snub-nosed monkey genetics and genomics and their impact on our understanding of the phylogeny, phylogeography, population genetic structure, landscape genetics, demographic history, and molecular mechanisms of adaptation to folivory and high altitudes in this primate genus. We further discuss future directions in this research field, in particular how genomic information can contribute to the conservation of snub-nosed monkeys.

Schneider and Ingram (1993) posited that society’s view of certain groups plays a powerful role in institutionalizing the level of power and status of those groups. While the theory was well developed by Schneider and Ingram, little is known empirically about how the public’s perceptions of the power and status of certain groups align with policies and elite messaging. We examine that link using a large sample from the Understanding America Study. We use this data to create “meta-constructions”, which are measures of how individuals perceive societal views of status and power of populations grouped by gender, race, and urbanicity. We first compare our findings with Schneider and Ingram’s quadrants of idealized population categorization. We then consider how views of gender, race, and urbanicity differ across individuals with different social characteristics, finding that more powerful groups are more likely to view society as being more equal than less powerful groups.

Studies on positional behavior and canopy use are essential for understanding how arboreal animals adapt their morphological characteristics and behaviors to the challenges of their environment. This study explores canopy and substrate use along with positional behavior in adult black snub-nosed monkeys Rhinopithecus strykeri, an endemic, critically endangered primate species in Gaoligong Mountains, southwest China. Using continuous focal animal sampling, we collected data over a 52-month period and found that R. strykeri is highly arboreal primarily using the high layers of the forest canopy (15–30 m), along with the terminal zone of tree crowns (52.9%), medium substrates (41.5%), and oblique substrates (56.8%). We also found sex differences in canopy and substrate use. Females use the terminal zones (56.7% versus 40.4%), small/medium (77.7% versus 60.1%), and oblique (59.9% versus 46.5%) substrates significantly more than males. On the other hand, males spend more time on large/very large (39.9% versus 22.3%) and horizontal (49.7% versus 35.2%) substrates. Whereas both sexes mainly sit (84.7%), and stand quadrupedally (9.1%), males stand quadrupedally (11.5% versus 8.3%), and bipedally (2.9% versus 0.8%) more often than females. Clamber, quadrupedalism, and leap/drop are the main locomotor modes for both sexes. Rhinopithecus strykeri populations never enter canopies of degenerated secondary forest and mainly use terminal branches in the middle and upper layers of canopies in intact mid-montane moist evergreen broadleaf forest and hemlock coniferous broadleaf mixed forests across their habitat.

The Myanmar snub-nosed monkey Rhinopithecus strykeri was discovered in 2010 on the western slopes of the Gaoligong Mountains in the Irrawaddy River basin in Myanmar and subsequently in the same river basin in China, in 2011. Based on 2 years of surveying the remote and little disturbed forest of the Gaoligong Mountains National Nature Reserve in China, with outline transect sampling and infrared camera monitoring, a breeding group comprising &gt; 70 individuals was found on the eastern slopes of the Gaoligong Mountains in the Salween River Basin. Given the Critically Endangered status of this primate (a total of &lt; 950 individuals are estimated to remain in the wild), efforts to protect the relatively undisturbed habitat of this newly discovered population and to prevent hunting are essential for the long-term survival of this species.

Habitat evaluation and conservation framework of the newly discovered and critically endangered black snub-nosed monkey

Identifying transboundary conservation priorities in a biodiversity hotspot of China and Myanmar: Implications for data poor mountainous regions