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Potential habitat corridors and restoration areas for the black-and-white snub-nosed monkey Rhinopithecus bieti in Yunnan, China
Abstract and Figures
The black-and-white snub-nosed monkey
Rhinopithecus bieti
is endemic to China, where its population is fragmented into 15 isolated groups and threatened despite efforts to protect the species. Here we analyse possible habitat connectivity between the groups reported in Yunnan, using genetic, least-cost path and Euclidean distances. We detect genetic isolation between the northern and southern groups but not among the northern groups. We show that genetic distance is better explained by human disturbance and land-cover least-cost paths than by Euclidian distance. High-quality habitats were found to be more fragmented in the southern part of the study area and interspersed with human-influenced areas unsuitable for black-and-white snub-nosed monkeys, which may explain the genetic isolation of the southern groups. Potential corridors are identified based on the least-cost path analysis, and seven sensitive areas are proposed for restoration. We recommend (1) that restoration is focused on the current range of the monkeys, with efforts to reduce human disturbance and human population pressure and increase public awareness, and (2) the development of a long-term plan for habitat restoration and corridor design in the areas between groups.
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... Previous studies on the habitat quality of the Yunnan snub-nosed monkey only carried out preliminary discrimination and analysis based on monkey colony corridors and potential suitable habitats due to the particularity of species distribution and the limitation of data acquisition [5,[36][37][38][39][40]. Previous research using the InVEST model to statically model habitat quality studied the impact of villages on monkey habitat quality [12]. ...
... Each land cover type was assigned a Habitat Suitability rating for Yunnan snub-nosed monkeys. These ratings are: most suitable (with a value of 1.0), suitable (0.8), less suitable (0.6), unsuitable (0.2), and obstructive (0.0) [12,37]. ...
... Each land cover type was assigned a Habitat Suitability rating for Yunnan snub-nosed monkeys. These ratings are: most suitable (with a value of 1.0), suitable (0.8), less suitable (0.6), unsuitable (0.2), and obstructive (0.0) [12,37]. The habitat quality score is determined using the following equations: Q xj indicates the quality of habitat in parcel x that is in LULC j; H j is the habitat suitability of LULC type j; z is a scaling parameter set at 2.5; k is the half-saturation constant set at 0.5; D xj indexes the total threat level in grid cell x with LULC type j [37,43]. ...
The reduction in habitat quality (as shown, in part, by the increase in habitat rarity) is an important challenge when protecting the Yunnan snub-nosed monkey. We used the InVEST model to quantitatively analyze the dynamic changes in the habitat of the Yunnan snub-nosed monkey from 1975 to 2022. The results show that in the study period, the degree of habitat degradation increased, with the degradation range at its widest in the south, and the degradation intensity highest in the north, especially along a center “spine” area in the north. Over the latter part of the study period, the habitat quality of most monkey groups improved, which is conducive to the survival and reproduction of the population. However, the habitat quality and monkey populations are still at significant risk. The results provide the basis for formulating the protection of the Yunnan snub-nosed monkey and provide research cases for the protection of other endangered species.
... All data were geo-corrected in ERDAS 9.2 with a root-mean-square (RMS) error < 1. LULC types (such as Armand pine and hemlock) were assigned one of five habitat categories, based on the Yunnan vegetation classification system and the monkey's habitat preferences. These five habitat categories, in declining quality, were optimal habitat, suboptimal habitat, suitable habitat, unfavorable habitat, and highly unfavorable habitat [5]. ...
... We should enhance habitat connectivity and build up ecological corridors to promote gene exchange and conserve genetic diversity in these areas where connectivity with other monkey groups is impeded by agriculture and grazing land, roads, and villages. This is especially true for the isolated monkey groups (C3, C6, and C14) [4][5][6]44]. ...
... The study area and locations of monkey groups in Yunnan Province (China). The numbers labeling each green area represent the monkey group number(1)(2)(3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15). ...
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.
... Although nearly 20 years has passed since the inception of landscape genetics, its application to primates is still in its infancy. 13 19,31,32,35 However, a few studies were new, applying landscape genetic analyses in combination with traditional population genetic tests for the first time in that species or population, 26,34,36 or taking an adaptive focus from previous neutral population genetics analyses. 29 While nearly all studies found evidence of restricted gene flow, the landscape barriers varied by taxon, geographic region, and the intensity of anthropogenic threat. ...
... gene flow (14 of 17 studies), 28,29,34 and well-known biogeographic dispersal barriers such as rivers and mountain ranges were characteristically identified as being difficult to traverse (that is, animals encountering these landscape features experienced high resistance to movement). 22,23,36,37 Moreover, deforestation, 19,24,26,27,[30][31][32][33]35 urbanization, 19,28,32,34 and high human population densities 33 and/or activity 26,27,[30][31][32]35 were typically identified as posing higher resistance to primate gene flow, than areas experiencing less anthropogenic disturbance. These patterns are not unique to primates and have been found to affect taxa at a global scale. ...
... gene flow (14 of 17 studies), 28,29,34 and well-known biogeographic dispersal barriers such as rivers and mountain ranges were characteristically identified as being difficult to traverse (that is, animals encountering these landscape features experienced high resistance to movement). 22,23,36,37 Moreover, deforestation, 19,24,26,27,[30][31][32][33]35 urbanization, 19,28,32,34 and high human population densities 33 and/or activity 26,27,[30][31][32]35 were typically identified as posing higher resistance to primate gene flow, than areas experiencing less anthropogenic disturbance. These patterns are not unique to primates and have been found to affect taxa at a global scale. ...
Landscape genetics is an emerging field that integrates population genetics, landscape ecology, and spatial statistics to investigate how geographical and environmental features and evolutionary processes such as gene flow, genetic drift, and selection structure genetic variation at both the population and individual levels, with implications for ecology, evolution, and conservation biology. Despite being particularly well suited for primatologists, this method is currently underutilized. Here, we synthesize the current state of research on landscape genetics in primates. We begin by outlining how landscape genetics has been used to disentangle the drivers of diversity, followed by a review of how landscape genetic methods have been applied to primates. This is followed by a section highlighting special considerations when applying the methods to primates, and a practical guide to facilitate further landscape genetics studies using both existing and de novo datasets. We conclude by exploring future avenues of inquiry that could be facilitated by recent developments as well as underdeveloped applications of landscape genetics to primates.
... Some studies have mapped the extent and distribution of suitable habitat of R. bieti and suggested habitat corridors to connect groups or subpopulations living in isolated pockets of suitable habitats [31,32]. However, these corridor conservation plans are impracticable because of excessive financial costs and high human resource requirements. ...
Habitat fragmentation affects the survival of wildlife and is a main threat to biodiversity. Corridors are frequently used to alleviate habitat fragmentation. However, corridors are costly and often ineffective in practice. Endangered species in montane regions are particularly affected by habitat fragmentation and therefore require economic and efficient conservation strategies. We propose a stepping stone strategy (SSS) to deal with habitat fragmentation threatening an endangered primate, the black-and-white snub-nosed monkeys (Rhinopithecus bieti). We selected the southern range of R. bieti as the study area, which covers 3,580 km2. We evaluated the habitat status and formulated an SSS based on the dispersal ability of an adult male R. bieti. Six sustainable habitat patches and 340 natural stepping stones were detected. Thirteen artificial stepping stones are needed to establish weak connectivity of habitats. Forty-four stepping stones are proposed as key stepping stones for attaining strong connectivity. The SSS is projected to incur substantially less pecuniary investment than the corridor strategy (0.06 million versus 5.65 million, USD). We conclude that 5 steps are needed for the SSS: (a) assessing the status of habitats to plan restorative intervention activities, (b) designing artificial stepping stones to weakly link sustainable habitats, (c) proposing corridors to allow for a stable connection between sustainable habitats, (d) identifying key stepping stones to establish small protected area, and (e) recovery of fragmented habitat and reinstatement of sustainable habitat. Our study suggests that SSS is a cost-effective and practical way for maintaining connectivity and supporting habitat recovery for endangered wildlife in montane regions.
... These results suggest that the genetic diversity of R. bieti is negatively affected by habitat fragmentation due to anthropogenic landscape features. Li et al. [73] applied more models of landscape genetics to further investigate the effects of landscape configuration on gene flow among the local groups of R. bieti. They identified potential migration corridors among isolated local groups of R. bieti, with potentially higher connectivity in the northern part of the species range. ...
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.
... Studies of primate landscape genetics remain limited, though are increasing in number [38]. From these, it is clear that primate gene flow can be impeded by both natural (e.g., rivers: [39,40]) and anthropogenic barriers (e.g., highways: [41]), including anthropogenically-driven landcover change (e.g., agriculture and deforestation: [41][42][43][44][45]) and proximity to human settlements ([46,47]). Environmental variability can influence dispersal at multiple scales-from smaller-scale gene flow resulting from typical dispersal events to long-range dispersal and multigenerational gene flow-with implications ranging from driving local population genetic structure to influencing potential speciation events [3][4][5][6]. ...
Dispersal is a fundamental aspect of primates’ lives and influences both population and community structuring, as well as species evolution. Primates disperse within an environmental context, where both local and intervening environmental factors affect all phases of dispersal. To date, research has primarily focused on how the intervening landscape influences primate dispersal, with few assessing the effects of local habitat characteristics. Here, we use a landscape genetics approach to examine between- and within-site environmental drivers of short-range black-and-white ruffed lemur (Varecia variegata) dispersal in the Ranomafana region of southeastern Madagascar. We identified the most influential drivers of short-range ruffed lemur dispersal as being between-site terrain ruggedness and canopy height, more so than any within-site habitat characteristic evaluated. Our results suggest that ruffed lemurs disperse through the least rugged terrain that enables them to remain within their preferred tall-canopied forest habitat. Furthermore, we noted a scale-dependent environmental effect when comparing our results to earlier landscape characteristics identified as driving long-range ruffed lemur dispersal. We found that forest structure drives short-range dispersal events, whereas forest presence facilitates long-range dispersal and multigenerational gene flow. Together, our findings highlight the importance of retaining high-quality forests and forest continuity to facilitate dispersal and maintain functional connectivity in ruffed lemurs.
... The most widespread impacts on primates from road infrastructure were habitat loss and fragmentation. These can result in secondary direct and indirect impacts, including a reduction in access to resources and hence primates' abundance near roads and genetic exchange between populations (Li et al., 2015;Aquino et al., 2016). Roads open up previously undisturbed areas to numerous anthropogenic activities, namely, logging, hunting, agriculture, livestock grazing, and mining and drilling (e.g., Rawson et al., 2011). ...
Most primate populations are declining; 60% of species face extinction. The expansion of transportation and service corridors (T&S) (i.e., roads and railways and utility and service lines) poses a significant yet underappreciated threat. With the development of T&S corridors predicted to increase across primates' ranges, it is necessary to understand the current extent of its impacts on primates, the available options to mitigate these effectively, and recognize research and knowledge gaps. By employing a systematic search approach to identify literature that described the relationship between primates and T&S corridors, we extracted information from 327 studies published between 1980 and 2020. Our results revealed that 218 species and subspecies across 62 genera are affected, significantly more than the 92 listed by the IUCN Red List of Threatened Species. The majority of studies took place in Asia (45%), followed by mainland Africa (31%), the Neotropics (22%), and Madagascar (2%). Brazil, Indonesia, Equatorial Guinea, Vietnam, and Madagascar contained the greatest number of affected primate species. Asia featured the highest number of species affected by roads, electrical transmission lines, and pipelines and the only studies addressing the impact of rail and aerial tramways on primates. The impact of seismic lines only emerged in the literature from Africa and the Neotropics. Impacts are diverse and multifaceted, for example, animal–vehicle collisions, electrocutions, habitat loss and fragmentation, impeded movement and genetic exchange, behavioral changes, exposure to pollution, and mortality associated with hunting. Although several mitigation measures were recommended, only 41% of studies focused on their implementation, whereas only 29% evaluated their effectiveness. Finally, there was a clear bias in the species and regions benefiting from research on this topic. We recommend that government and conservation bodies recognize T&S corridors as a serious and mounting threat to primates and that further research in this area is encouraged.
The golden snub‐nosed monkey, or golden monkey, inhabits the eastern Yangtze River. The black‐and‐white snub‐nosed monkey or Yunnan snub‐nosed monkey survives between the upper reaches of the Yangtze River and the Upper Mekong River. The bones, brains and other body parts of black‐and‐white snub‐nosed monkeys were then used to prepare medicinal remedies, which amounted to several dozen animals per year in the late 1970s and early 1980s. A spatial modeling of the ecological network of black‐and‐white snub‐nosed monkeys was then carried out in order to evaluate the degree of connectivity of its habitats and the impact of different development scenarios. Ecotourism responds to a demand for interaction with nature, while developing biodiversity conservation programs and increasing financial and educational benefits for local communities.
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.
Ecologists are concerned with the relationships between species composition and environmental factors, and with spatial structure within those relationships. A dissimilarity-based framework incorporating space explicitly is an extremely flexible tool for answering these questions. The R package ecodist brings together methods for working with dissimilarities, including some not available in other R packages. We present some of the features of ecodist, particularly simple and partial Mantel tests, and make recommendations for their effective use. Although the partial Mantel test is often used to account for the effects of space, the assumption of linearity greatly reduces its effectiveness for complex spatial patterns. We introduce a modification of the Mantel correlogram designed to overcome this restriction and allow consideration of complex nonlinear structures. This extension of the method allows the use of partial multivariate correlograms and tests of relationship between variables at different spatial scales. Some of the possibilities are demonstrated using both artificial data and data from an ongoing study of plant community composition in grazinglands of the northeastern United States.
We describe an extensive metapopulation study on the Glanville fritillary Melitaea cinxia, in a network of 1502 discrete habitat patches, comprising the entire distribution of this butterfly species in Finland. A thorough survey of the easily detected larval groups revealed a local population in 536 patches (dry meadows). We demonstrate that this system satisfies the four necessary conditions for a species to persist in a balance between stochastic local extinctions and recolonizations. Patterns of patch occupancy support several qualitative and quantitative model predictions. With decreasing regional density and average area of habitat patches, the butterfly occurs in a diminishing fraction of suitable habitat. To our knowledge, this is the first conclusive demonstration, based on a comparison of many conspecific metapopulations, of declining habitat occupancy and hence of increasing threat to survival caused by increasing habitat fragmentation.
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 of R. bieti was 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.
Abstract pathmatrixis a tool used to compute matrices of effective geographical distances among samples using a least-cost path algorithm. This program is dedicated to the study of the role of the environment on the spatial genetic structure of populations. Punctual locations (e.g. individuals) or zones encompassing sample data points (e.g. demes) are used in conjunction with a species-specific friction map representing the cost of movement through the landscape. Matrices of effective distances can then be exported to population genetic software to test, for example, for isolation by distance.pathmatrixis an extension to the geographical information system (GIS) softwarearcview3.x.
Landscape connectivity was defined by metrics to reflect landscape functional characteristic for it represents ' the degree to which the landscape facilitates or impedes movement among resource patches '. The theory and method of landscape connectivity is an important basis for landscape evaluation, management and ecological designing. It will also contribute to the regional sustainable development and biodiversity conservation. In this paper, the new progress of landscape connectivity research, including the concept, measurement and its ecological significationce were summarized, and the relationship between landscape connectivity and landscape elements, and its potential application perspectives were discussed. This review could serve as a guideline in further research and applications of the relationship between landscape pattern and ecological processes.
Biodiversity conservation is becoming more challenging and imminent due to rapid habitat loss and fragmentation under ever growing global demand for natural resource. Habitat loss and fragmentation can lower migration rate of a species populations, thereby reducing gene flow and genetic variability, leading to increased risk of extinction. Because of the relationship between genetic diversity and landscape characters, biodiversity conservation research should include study on landscape characteristics and their changes. Thus, conservation efforts should not only focus on a specific species itself, but also consider all components of its habitats. In this paper we discussed the relationship between landscape structure and genetic diversity using the Yunnan snub-nosed monkeys as an example. Landscape genetics is an interdisciplinary of population genetics, landscape ecology, and spatial statistics. It is used to quantify the effects of landscape characters on population genetic structures. Results from such studies may have great applications for biodiversity conservation and reserve management. There are five major research categories: (1) quantifying influence of landscape variables on genetic variation; (2) identifying barriers to gene flow; (3) identifying source-sink dynamics and movement corridors; (4) understanding the spatial and temporal scale of ecological processes; and (5) testing species-specific ecological hypotheses. Landscape genetics is becoming a popular research area, because it opens the possibility to investigate ecological processes through genetic data and to analyze how these processes operate in the real world. Landscape genetics have heuristic, as well as practical, values in encouraging landscape ecologists to think more about biological processes rather than spatial patterns, and in encouraging population geneticists to consider the quality of a landscape instead of mere spatial distance. The use of molecular genetic is a new research method in testing landscape ecological hypotheses. The habitat connectivity was studied using a least-cost model and genetic data of the Yunnan snub-nosed monkeys (Rhinopithecus bieti). We presented the connectivity and the habitat areas that were sensitive to overall connectivity. The Yunnan Snub-nosed Monkeys (Rhinopithecus bieti) is one of the rarest species in severe danger. Due to habitat loss and fragmentation, its gene communication was blocked and genetic diversity was threatened. The results show that only monkey groups in S3 were better connected, and other groups were poorly connected. The subpopulations north to S3 were affected by anthropogenic barriers less than the subpopulations south to S3. The potential dispersal corridor between populations was protracted and the important area to restore was located. The sensitive areas were concentrated in subpopulations among S3, S4 and S5 in central and south areas. These sensitive areas should be protect and restore preferential. Our paper also found that population geneticists could be investigated using landscape ecological data. We proposed that (1) a landscape approach should go beyond testing the effect of distance; (2) disturbance and landscape change could be incorporated into the study design; (3) simulation model might help establish a mechanistic link; (4) the spatial and temporal variability of site conditions was important to explaining quantitative traits and differences. Under the influence of social and economic development, natural ecosystems are increasingly threatened by disturbances such as habitat degradation, climatic changes, and invasive species etc. It is believed that landscape genetics would bridge researchers from micro-to macro-ecology. Our current focus of the research was landscape connectivity using genetic data, but interdisciplinary communication should be encouraged and facilitated for future study.
The Yunnan snub-nosed monkey is endemic to China and is one of the world's 25 most endangered of the snub-nosed monkey species. The Laojun Mountain Area (LMA) provides a significant habitat for the monkey and a "corridor" for the whole distribution area. However, the Yunnan snub-nosed monkey is facing habitat loss and a shrinking population size. The spatial distribution pattern of its potential habitats is very important for designing biological corridors. Despite its existence for many years, little is known about the potential habitat distribution in the study site. This study is based on the "3S" (GIS-Geography Information System, RS-Remote Sensing, GPS-Global Positioning System) techniques and multiple group discriminant analysis (MGDA) in SAS to develop a spatial model of the Laojun Mountain Area (about 7,231 km2) to simulate the Yunnan snub-nosed monkey's potential habitat conditions. The study results indicated that a significant difference was found when comparing the predicted potential habitat with the existing habitat. The predicted area was 6,226 km2, accounting for 86.59% of the total area, which was much greater than the existing one of 2,802 km2, accounting for 38.74% of the total area. Also, the connectivity of the predicted area was much stronger than current conditions.
