Environmental Science and Pollution Research

, Volume 26, Issue 31, pp 32374–32384 | Cite as

Suitable habitat prediction of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) and its implications for conservation in Baihe Nature Reserve, Sichuan, China

  • Xin DongEmail author
  • Yuan-meng-ran Chu
  • Xiaodong Gu
  • Qiongyu Huang
  • Jindong Zhang
  • Wenke BaiEmail author
Research Article


As an endemic primate species with one of the highest priorities in wildlife conservation in China, Sichuan snub-nosed monkeys (Rhinopithecus roxellana) have undergone a sharp decline and range reduction in recent centuries. Here, we used maximum entropy modelling (MaxEnt) integrated with four types of environmental variables, including three biological climate variables (Bio17, precipitation of the driest quarter; Bio6, min. temperature of the coldest month; and Bio2, mean diurnal range), three topographic variables (altitude, slope, and aspect), two anthropogenic variables (Human Footprint Index and human disturbance), and three vegetation-related variables (enhanced vegetation index, normalized difference vegetation index, and Wet Index) to identify the spatial distribution of suitable habitats for Sichuan snub-nosed monkeys in Baihe Nature Reserve (BNR), which is located in the Minshan Mountains. The average training AUC of our model performance is 0.929 ± 0.003. The model predicted 9.6 km2 of high suitability habitats and 14.1 km2 of moderate suitability habitats for Sichuan snub-nosed monkeys, adding up to only 11.7% of the total area of concern for the study in the BNR. The top four variables ranked in the model (altitude, Human Footprint Index, human disturbance, and Bio17) accounted for relative gain contributions of 23.3%, 19.3%, 14.2%, and 13.4%, respectively. The predicted suitable habitats were confined to an altitude range of 1971–3198 m, Human Footprint Index of mainly 3–5 values, low human disturbance (mainly livestock), and precipitation of the driest (or coldest) quarter of 9–22 mm. Additionally, the suitable habitats were mainly distributed in the core zone (36.1%), buffer zone (26.8%), and experimental zone (29.5%). The remaining habitats (7.6%) were distributed in the 0.5-km buffer zone of the reserve border. The predicted suitable habitats indicated limited suitable habitat space for the Sichuan snub-nosed monkeys, with most of the suitable habitat distributed outside the core zone in the BNR. Our findings highlighted that human activities in all three functional zones could be the most negative factor on suitable habitat distribution of Sichuan snub-nosed monkeys in the BNR.


Sichuan snub-nosed monkeys Habitat suitability MaxEnt Baihe Nature Reserve Zoning Human disturbance 



We would like to thank the staff of the BNR Management Bureau for their assistance with field data collection. We especially thank all workers contributing to data collection for the 4th National Census of the Giant Panda.

Funding information

This work was supported by the Habitat Restoration Programme for Sichuan snub-nosed monkeys in the Baihe Nature Reserve (BNR) programmes by the State Forestry Administration of China (Grant No. 401295). We also acknowledge the following sources of funding: the National Natural Science Foundation of China (41571517; 31572293) and the Key Laboratory of Southwest China Wildlife Resources Conservation (China West Normal University), Ministry of Education, China (XNYB17-2).

Supplementary material

11356_2019_6369_MOESM1_ESM.docx (101 kb)
ESM 1 (DOCX 100 kb)


  1. Anderson RP, Gonzalez I Jr (2011) Species-specific tuning increases robustness to sampling bias in models of species distributions: an implementation with Maxent. Ecol Model 222:2796–2811Google Scholar
  2. Aryal A, Shrestha UB, Ji W, Ale SB, Shrestha S, Ingty T, Maraseni T, Cockfield G, Raubenheimer D (2016) Predicting the distributions of predator (snow leopard) and prey (blue sheep) under climate change in the Himalaya. Ecol Evol 6:4065–4075Google Scholar
  3. Bai W, Connor T, Zhang J, Yang H, Dong X, Gu X, Zhou C (2018) Long-term distribution and habitat changes of protected wildlife: giant pandas in Wolong Nature Reserve, China. Environ Sci Pollut Res 25:11400–11408Google Scholar
  4. Bista M, Panthi S, Weiskopf SR (2018) Habitat overlap between Asiatic black bear Ursus thibetanus and red panda Ailurus fulgens in Himalaya. PLoS One 13:e0203697. CrossRefGoogle Scholar
  5. Boria RA, Olson LE, Goodman SM, Anderson RP (2014) Spatial filtering to reduce sampling bias can improve the performance of ecological niche models. Ecol Model 275:73–77Google Scholar
  6. Chang ZF, Luo MF, Liu ZJ, Yang JY, Xiang ZF, Li M, Vigilant L (2012) Human influence on the population decline and loss of genetic diversity in a small and isolated population of Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Genetica 140:105–114Google Scholar
  7. Chopra SK (1989) International trade in endangered species: a guide to CITES. Martinus Nijhoff Publishers, Sold and distributed in the U.S.A. and Canada by Kluwer Academic PublishersGoogle Scholar
  8. Chu YM, Sha JCM, Kawazoe T et al (2018) Sleeping site and tree selection by Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in Baihe Nature Reserve, Sichuan, China. Am J Primatol 80:e22936. CrossRefGoogle Scholar
  9. Cui S, Luo X, Li C, Hu H, Jiang Z (2018) Predicting the potential distribution of white-lipped deer using the MaxEnt model. Biodivers Sci 26:171–176 (in Chinese) Google Scholar
  10. Elith J et al (2010) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29:129–151Google Scholar
  11. Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57Google Scholar
  12. ESRI (2017) ArcGIS Desktop, 10.5 edn. Environmental systems research Redlands, California, USA Exelis ENVI, 5.3 edn., Boulder, ColoradoGoogle Scholar
  13. Fahrig L, Merriam G (1985) Habitat patch connectivity and population survival. Ecol Soc Am 66:1762–1768Google Scholar
  14. Fang G, Chen J, Pan RL, Qi XG, Li BG, Fang G, Chen J, Pan RL, Qi XG, Li BG (2018) Female choice impacts residential male takeover in golden snub-nosed monkey (Rhinopithecus roxellana). Zool Res 39:266–271Google Scholar
  15. Fick SE, Hijmans RJ (2017) Worldclim 2: new 1-km spatial resolution climate surfaces for global land areas. Int J ClimatolGoogle Scholar
  16. Geospatial Data Cloud Computer Network Information Center, Chinese Academy of Sciences (2018) Accessed 11 July
  17. Gu ZH (2011) Analysis on landscape pattern of habitat of Sichuan golden monkey in Baihe Nature Reserve. J Anhui Agric Sci 13:136Google Scholar
  18. Hof AR, Jansson R, Nilsson C (2012) The usefulness of elevation as a predictor variable in species distribution modelling. Ecol Model 246:86–90Google Scholar
  19. Hull V, Xu W, Liu W, Zhou S, Viña A, Zhang J, Tuanmu MN, Huang J, Linderman M, Chen X, Huang Y, Ouyang Z, Zhang H, Liu J (2011) Evaluating the efficacy of zoning designations for protected area management. Biol Conserv 144:3028–3037Google Scholar
  20. IUCN (2018) The IUCN red list of threatened species. Version 2018.2. IUCN, Gland, SwitzerlandGoogle Scholar
  21. Kirkpatrick RC, Gu HJ, Zhou XP (1999) A preliminary report on Sichuan snub-nosed monkeys (Rhinopithecus roxellana) at Baihe Nature Reserve. Folia Primatol 70:117–120Google Scholar
  22. Kumar S, Stohlgren TJ (2009) Maxent modeling for predicting suitable habitat for threatened and endangered tree Canacomyrica monticola in New Caledonia. Journal of Ecology and Natural Environment 1:094–098Google Scholar
  23. Li B, Jia Z, Pan R, Ren B (2003) Changes in distribution of the snub-nosed monkey in China. Primates in Fragments Ecology & ConservationGoogle Scholar
  24. Li B, Pan R, Oxnard CE (2002) Extinction of snub-nosed monkey in China during the past 400 years. Int J Primatol 23:1227–1244Google Scholar
  25. Li YZ, Dong X, Liu XH (2016) Habitat pattern dynamics of the Golden snub-nosed monkey in Baihe Nature Reserve, Minshan Mountains, China over the past 40 years. Acta Ecol Sin 36:1803–1814Google Scholar
  26. Li Y, Jiang Z, Li C, Grueter CC (2010) Effects of seasonal folivory and frugivory on ranging patterns in Rhinopithecus roxellana. Int J Primatol 31:609–626Google Scholar
  27. Liu C, Newell G, White M (2016a) On the selection of thresholds for predicting species occurrence with presence-only data. Ecol Evol 6:337–348Google Scholar
  28. Liu C, White M, Newell G (2013) Selecting thresholds for the prediction of species occurrence with presence-only data. J Biogeogr 40:778–789Google Scholar
  29. Liu F, McShea WJ, Li D (2017) Correlating habitat suitability with landscape connectivity: a case study of Sichuan golden monkey in China. Ecol Model 353:37–46Google Scholar
  30. Liu G, Guan T, Dai Q, Li H, Gong M (2016b) Impacts of temperature on giant panda habitat in the north Minshan Mountains. Ecol Evol 6:987–996Google Scholar
  31. Merow C, Smith MJ, Silander JA Jr (2013) A practical guide to MaxEnt for modeling species’ distributions: what it does, and why inputs and settings matter. Ecography 36:1058–1069Google Scholar
  32. Nüchel J, Bøcher PK, Xiao W, Zhu AX, Svenning JC (2018) Snub-nosed monkey (Rhinopithecus): potential distribution and its implication for conservation. Biodivers Conserv 27:1517–1538Google Scholar
  33. O’Donnell MS, Ignizio DA (2012). Bioclimatic predictors for supporting ecological applications in the conterminous United States: U.S. Geological Survey Data Series 691:10.Google Scholar
  34. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259Google Scholar
  35. Phillips SJ, Dudík M (2008) Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31:161–175Google Scholar
  36. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, UKGoogle Scholar
  37. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  38. Ren B, Zhang S, Wang L, Liang B, Li B (2001) Vertical distribution of different age-sex classes in a foraging group of Sichuan golden monkeys (Rhinopithecus roxellana). Folia Primatol 72:96–99Google Scholar
  39. Schipper J, Chanson JS, Chiozza F, Cox NA, Hoffmann M, Katariya V, Lamoreux J, Rodrigues ASL, Stuart SN, Temple HJ, Baillie J, Boitani L, Lacher TE, Mittermeier RA, Smith AT, Absolon D, Aguiar JM, Amori G, Bakkour N, Baldi R, Berridge RJ, Bielby J, Black PA, Blanc JJ, Brooks TM, Burton JA, Butynski TM, Catullo G, Chapman R, Cokeliss Z, Collen B, Conroy J, Cooke JG, da Fonseca GAB, Derocher AE, Dublin HT, Duckworth JW, Emmons L, Emslie RH, Festa-Bianchet M, Foster M, Foster S, Garshelis DL, Gates C, Gimenez-Dixon M, Gonzalez S, Gonzalez-Maya JF, Good TC, Hammerson G, Hammond PS, Happold D, Happold M, Hare J, Harris RB, Hawkins CE, Haywood M, Heaney LR, Hedges S, Helgen KM, Hilton-Taylor C, Hussain SA, Ishii N, Jefferson TA, Jenkins RKB, Johnston CH, Keith M, Kingdon J, Knox DH, Kovacs KM, Langhammer P, Leus K, Lewison R, Lichtenstein G, Lowry LF, Macavoy Z, Mace GM, Mallon DP, Masi M, McKnight MW, Medellin RA, Medici P, Mills G, Moehlman PD, Molur S, Mora A, Nowell K, Oates JF, Olech W, Oliver WRL, Oprea M, Patterson BD, Perrin WF, Polidoro BA, Pollock C, Powel A, Protas Y, Racey P, Ragle J, Ramani P, Rathbun G, Reeves RR, Reilly SB, Reynolds JE, Rondinini C, Rosell-Ambal RG, Rulli M, Rylands AB, Savini S, Schank CJ, Sechrest W, Self-Sullivan C, Shoemaker A, Sillero-Zubiri C, de Silva N, Smith DE, Srinivasulu C, Stephenson PJ, van Strien N, Talukdar BK, Taylor BL, Timmins R, Tirira DG, Tognelli MF, Tsytsulina K, Veiga LM, Vie JC, Williamson EA, Wyatt SA, Xie Y, Young BE (2008) The status of the world's land and marine mammals: diversity, threat, and knowledge. Science 322:225–230Google Scholar
  40. Su J, Aryal A, Nan Z, Ji W (2015) Climate change-induced range expansion of a subterranean rodent: implications for rangeland management in Qinghai-Tibetan Plateau. PLoS One 10:e0138969Google Scholar
  41. Thapa A, Wu R, Hu Y, Nie Y, Singh PB, Khatiwada JR, Yan L, Gu X, Wei F (2018) Predicting the potential distribution of the endangered red panda across its entire range using MaxEnt modeling. Ecol Evol 8:10542–10554. CrossRefGoogle Scholar
  42. Venter O et al. (2018) Last of the Wild Project, Version 3 (LWP-3): 1993 Human Footprint, 2018 Release. NASA Socioeconomic Data and Applications Center (SEDAC), Palisades, NYGoogle Scholar
  43. Wang B, Xu Y, Ran J (2017) Predicting suitable habitat of the Chinese monal (Lophophorus lhuysii) using ecological niche modeling in the Qionglai Mountains, China. Peer J 5:e3477. CrossRefGoogle Scholar
  44. Wang P, Teng M, He W, Tang C, Yang J, Yan Z (2018) Using habitat selection index for reserve planning and management for snub-nosed golden monkeys at landscape scale. Ecol Indic 93:838–846Google Scholar
  45. Wang S, Xie Y (2004) China species red list. Higher Education Press, Beijing, China (in Chinese) Google Scholar
  46. Wang W, Chu YM, Gang HU (2013) Habitat selection of golden snub-nosed monkey (Rhinopithecus roxellana) of Baihe Nature Reserve. Autumn Journal of China West Normal University 34:16–21Google Scholar
  47. Wei W, Swaisgood RR, Dai Q, Yang Z, Yuan S, Owen MA, Pilfold NW, Yang X, Gu X, Zhou H, Han H, Zhang J, Hong M, Zhang Z (2018) Giant panda distributional and habitat-use shifts in a changing landscape. Conserv Lett 11:e12575. CrossRefGoogle Scholar
  48. Wen H, Wen R (2006) The change of the plant and animal in China during different historical period. Chongqing Press, Chongqing (in Chinese) Google Scholar
  49. Wen R (2009) The distributions and changes of rare wild animals in China. Shandong Science and Technology Press, Jinan (in Chinese) Google Scholar
  50. Wu G, Wang H, Fu H, Zhao JZ, Yang YQ (2004) Habitat selection of Guizhou golden monkey (Phinopithecus roxellanae brelichi)in Fanjing Mountain Biosphere Reserve, China. J For Res 15:197–202Google Scholar
  51. Xu W, Li X, Pimm SL, Hull V, Zhang J, Zhang L, Xiao Y, Zheng H, Ouyang Z (2016) The effectiveness of the zoning of China's protected areas. Biol Conserv 204:231–236Google Scholar
  52. Yan Z, Teng M, He W, Wang Y, Yang J, Wang P (2018) Improving conservation effectiveness of nature reserve for golden snub-nosed monkey, a niche-based approach. Ecol Evol 8:9315–9325. CrossRefGoogle Scholar
  53. Zhang ZJ, Li LH, Li DY et al. (2013) Report on Comprehensive Scientific Survey in Baihe Nature Reserve of Sichuan. College of Life Science, China West Normal University; Baihe Nature Reserve Administration (in Chinese) Google Scholar
  54. Zhang Z et al (2014) Ecological scale and seasonal heterogeneity in the spatial behaviors of giant pandas. Integrative Zoology 9:46–60Google Scholar
  55. Zhao H et al (2016) Distribution and population of Rhinopithecus roxellana in Jiuzhaigou National Nature Reserve, Sichuan Province, China. Acta Ecol Sin 36:1797–1802Google Scholar
  56. Zhao X, Ren B, Garber PA, Li X, Li M (2018) Impacts of human activity and climate change on the distribution of snub-nosed monkey in China during the past 2000 years. Divers Distrib 24:92–102Google Scholar
  57. Zhao X, Ren B, Li D, Garber PA, Zhu P, Xiang Z, Grueter CC, Liu Z, Li M (2019) Climate change, grazing, and collecting accelerate habitat contraction in an endangered primate. Biol Conserv 231:88–97Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.College of Environmental Science and EngineeringChina West Normal UniversityNanchongChina
  2. 2.Key Laboratory of Southwest China Wildlife Resources ConservationChina West Normal UniversityNanchongChina
  3. 3.School of Sociology and AnthropologySun Yat-sen UniversityGuangzhouChina
  4. 4.Wildlife Resource Conservation and Management Station of Sichuan ProvinceChengduChina
  5. 5.Smithsonian Conservation Biology, InstituteFront RoyalUSA
  6. 6.Institute of EcologyChina West Normal UniversityNanchongChina

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