Abstract
China is facing an unprecedented set of challenges in balancing the effects of economic development and global climate change with environmental protection and maintaining biodiversity. Although positive steps have been undertaken to remedy this situation, currently 80% of China’s 25 extant primate species are threatened, 15–18 species have population sizes of less than 3000 individuals, and two species of gibbons and one species of langur have been extirpated over the past few decades. Today, virtually all species of primates in China inhabit fragmented landscapes and are distributed in small isolated subpopulations with limited opportunities to exchange individuals or genetic information. Here we present a historical framework examining how human-induced environmental changes, particularly since the second half of the 20th century, accelerated primate population decline in China. In addition, we modeled the expected spatial conflict between agricultural expansion and primate distributions over the next 25–75 years and assessed the current overlap between protected areas and primate distributions. Depending on the assumptions of the spatial conflict model, primate distributions are expected to decline by an additional 51–87% by the year 2100. Thus, unless large-scale conservation policies are implemented immediately the current trend of primate population decline, local extirpation, and species extinctions will accelerate. To mitigate against such extinction scenarios, we advocate the creation of a Chinese national agency and repository of environmental information focused on public awareness and education, the implementation of targeted programs of habitat restoration designed to return impacted forests to a more natural state especially within and at the boundaries of nature reserves, the establishment of additional protect areas, and the construction of a latticework of corridors connecting isolated primate subpopulations. This comprehensive approach offers the most effective way to protect China’s animal and plant biodiversity, including its endangered primate populations.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agoramoorthy G, Hsu M (1999) CITES implementation through the wildlife conservation law of Taiwan. J Int Wildl Law Policy 2:64–68
Ahn BJ (1975) The political economy of the People’s commune in China: changes and continuities. J Asian Stud 34:631–658. https://doi.org/10.2307/2052547
Ahrends A, Hollingsworth PM, Beckshafer P, Chen H, Zomer RJ, Zhang L et al (2017) China’s fight to halt tree cover loss. Proc R Soc B 284:20162559. https://doi.org/10.1098/rspb.2016.2559
Behal S (2014) Primate export: Ending the monkey business. India today. https://www.indiatoday.in/magazine/indiascope/story/19780228-government-bans-export-of-monkeys-us-forced-to-curtail-experiments-822869-2014-04-29. Accessed 29 April 2014
Bramall C (2004) Chinese land reform in long-run perspective and in the wider East Asian context. J Agrar Change 4:107–141. https://doi.org/10.1111/j.1471-0366.2004.00074.x
Bremer LL, Farley KA (2010) Does plantation forestry restore biodiversity or create green deserts? A synthesis of the effects of land-use transitions on plant species richness. Biodivers Conserv 19:3893–3915. https://doi.org/10.1007/s10531-010-9936-4
Bryant JV, Gottelli D, Zeng X, Hong X, Chan BP, Fellowes JR et al (2016) Assessing current genetic status of the Hainan gibbon using historical and demographic baselines: implications for conservation management of species of extreme rarity. Mol Ecol 25:3540–3556. https://doi.org/10.1111/mec.13716
Cao SX (2008) Why large-scale afforestation efforts in China have failed to solve the desertification problems. Environ Sci Technol 42:1826–1831. https://doi.org/10.1021/es0870597
Chan BPL, Tan XF, Tan WJ (2008) Rediscovery of the critically endangered eastern black crested gibbon Nomascus nasutus (Hylobatidae) in China, with preliminary notes on population size, ecology, and conservation status. Asian Primates J 1:17–25
Crook FW (1978) The commune system in the People’s Republic of China, 1963–1974. Joint Economic Committee, Congress of the United States. Policy Perform 1:366–410
Cui LW, Li YC, Ma C, Scott MB, Li JF et al (2016) Distribution and conservation status of Shortridge’s capped langurs Trachypithecus shortridgei in China. Oryx 50:732–741. https://doi.org/10.1017/S0030605315000319
Cyranoski D (2016) Monkey Kingdom: China is positioning itself as a world leader in primate research. Nature 532:300–302. https://doi.org/10.1038/532300a
Dai LM, Zhao W, Shao GF, Lewis BJ, Yu DP, Zhou L et al (2013) The progress and challenges in sustainable forestry development in China. Int J Sust Dev World 20:394–403. https://doi.org/10.1080/13504509.2013.775193
Deng HQ, Zhou J (2017) Diet composition of Hainan gibbons (Nomascus hainanus) based on 13 years of observation. North-West J Zool e171703
Deng HQ, Zhou J, Yang YW (2014) Sound Spectrum Characteristics of Songs of Hainan Gibbon (Nomascus hainanus). Int J Primatol 35:547–556. https://doi.org/10.1007/s10764-014-9767-3
Dobrovolski R, Loyola RD, Guihaumon F, Gouveia SF, Diniz-Filho JAF (2013) Global agricultural expansion and carnivore conservation biogeography. Biol Conserv 165:162–170. https://doi.org/10.1016/j.biocon.2013.06.004
Dosen J, Raboy BE, Fortib MJ (2017) Restoration strategies to improve connectivity for golden-headed lion tamarins (Leontopithecus chrysomelas) in the Bahian Atlantic Forest, Brazil. Int J Primatol 38:962–983. https://doi.org/10.1007/s10764-017-9991-8
Economy EC (2007) The great leap backward? The cost of China’s environment. Foreign Aff 86:38–59. https://doi.org/10.2307/20032433
Estrada A, Garber PA, Rylands AB, Roos C, Fernandez-Duque E, Di Fiore A et al (2017) Impending extinction crisis of the world’s primates: why primates matter. Sci Adv 3:e1600946. https://doi.org/10.1126/sciadv.1600946
Estrada A, Garber PA, Mittermeier RA, Wich W, Goveia S et al (2018) Primates in peril: the significance of Brazil, Madagascar, Indonesia and the Democratic Republic of the Congo for global primate conservation. Peer J 6:e4869. https://doi.org/10.7717/peerj.4869
Fan PF (2017) The past, present, and future of gibbons in China. Biol Conserv 210:29–39. https://doi.org/10.1016/j.biocon.2016.02.024
Fan PF, Bartlett TQ (2017) Overlooked small apes need more attention! Am J Primatol. https://doi.org/10.1002/ajp.22658
Fan Z, Song YL (2003) Chinese primate status and primate captive breeding for biomedical research in China. In: Institute for Laboratory Animal Research (U.S.). International Perspectives: The Future of Nonhuman Primate Resources: Proceedings of the Workshop Held April 17–19, 2002. The National Academies Press, Washington DC, pp 36–45
Fan PF, Xiao W, Huo S, Ai HS, Wang TC, Lin RT (2011) Distribution and conservation status of Hoolock leuconedys in China. Oryx 45:129–134. https://doi.org/10.1017/s003060531000089x
Fan PF, Fei HL, Luo AD (2013) Ecological extinction of critically endangered northern white-cheeked gibbon (Nomascus leucogenys) in China. Oryx 48:52–55. https://doi.org/10.1017/s0030605312001305
Fan PF, Fei HL, Luo AD, Luo AD (2014a) Ecological extinction of the critically endangered northern white-cheeked gibbon Nomascus leucogenys in China. Oryx 48:52–55. https://doi.org/10.1017/s0030605312001305
Fan ZX, Zhao G, Li P, Osada N, Xing JC, Yi Y et al (2014b) Whole-genome sequencing of Tibetan macaque (Macaca thibetana) provides new insight into the macaque evolutionary history. Mol Biol Evol 31:1475–1489. https://doi.org/10.1093/molbev/msu104
Fan PF, He K, Chen X, Ortiz A, Zhang B, Zhao C et al (2017a) Description of a new species of Hoolock gibbon (Primates: Hylobatidae) based on integrative taxonomy. Am J Primatol. https://doi.org/10.1002/ajp.22631
Fan PF, Liu Y, Zhang ZC, Zhao C, Li C, Liu WL et al (2017b) Phylogenetic position of the white-cheeked macaque (Macaca leucogenys), a newly described primate from southeastern Tibet. Mol Phylogenet Evol 107:80–89. https://doi.org/10.1016/j.ympev.2016.10.012
Fang J, Yu G, Liu L, Shuijin H, Chapin FS III (2018) Climate change human impacts, and carbon sequestration in China. Proc Natl Acad Sci USA 115:4015–4020
Fellowes JR, Chan BPL, Zhou J, Chen SH, Yang SB, Chit NS (2008) Current status of the Hainan gibbon (Nomascus hainanus): progress of population monitoring and other priority actions. Asian Primates J 1:2–8
Gale F, Hansen J, Jewison M (2015) China’s growing demand for agricultural imports. United States Department of Agriculture, EIB-138 Economic Research Service, February 2015
Geissmann T, Lwin N, Aung SS, Aung TN, Aung ZM, Hla TH et al (2011) A new species of snub-nosed monkey, genus Rhinopithecus Milne-Edwards, 1872 (Primates, Colobinae), from northern Kachin state, northeastern Myanmar. Am J Primatol 73:96–107. https://doi.org/10.1002/ajp.20894
Gray TNE, Hughes AC, Laurance WF, Long B, Lynam AJ, O’Kelly H, Ripple WJ, Seng T, Scotson L, Wilkinson NM (2018) The wildlife snaring cirisis” an insidious and pervasice threat to biodiversity in Southeast Asia. Biodivers Conserv 27:1031–1037
Grueter CC (2013) The biology of the snub-nosed monkeys, Douc langurs, proboscis monkeys and simakobu. Hauppauge, Nova Biomedical, New York
Grueter CC, Jiang XL, Konrad R, Fan PF, Guan ZH, Geissmann T (2009) Are Hylobates lar extirpated from China? Int J Primatol 30:553–567. https://doi.org/10.1007/s10764-009-9360-3
Guo YQ, Zhou J, Song XH, Den GHQ, Qiu Y, Shi L et al (2017) The population of Rhinopithecus brelichi in Fanjingshan National Nature Reserve, Guizhou, China. Acta Theriol Sin 37:104–108. https://doi.org/10.16829/j.slxb.201701009
Han ZX, Hu G, Wu SB, Cao CL, Dong X (2013) A census and status review of the Endangered François’ langur Trachypithecus francoisi in Chongqing, China. Oryx 47(1):128–133. https://doi.org/10.1017/S0030605311001396
Hao X (2007) Monkey research in China: developing a natural resource. Cell 129:1033–1036. https://doi.org/10.1016/j.cell.2007.05.051
Ho PT (1967) The significance of the Ch’ing period in Chinese history. J Asian Stud 26:189–195. https://doi.org/10.2307/2051924
Ho P (2003) Mao’s war against nature? The environmental impact of the Grain-First campaign in China. China J 50:37–59. https://doi.org/10.2307/3182245
Hong YY, Duo HR, Hong JY, Yang JY, Liu SM, Yu LH et al (2017) Resequencing and comparison of whole mitochondrial genome to gain insight into the evolutionary status of the Shennongjia golden snub-nosed monkey (SNJ R. roxellana). Ecol Evol 7:4456–4464. https://doi.org/10.1002/ece3.3011
Hsu MJ, Kao CC, Agoramoorthy G (2009) Interactions between visitors and Formosan macaques (Macaca cyclopis) at Shou-Shan Nature Park, Taiwan. Am J Primatol 71:214–222. https://doi.org/10.1002/ajp.20638
Hu HB, Liu WJ, Cao M (2008) Impact of land use and land cover changes on ecosystem services in Menglun, Xishuangbanna, Southwest China. Environ Monit Assess 146:147–156. https://doi.org/10.1007/s10661-007-0067-7
Huang PCC (1995) Rural class struggle in the Chinese revolution representational and objective realities from the land reform to the cultural revolution. Mod China 21:105–143. https://doi.org/10.1177/009770049502100105
Huang CM, Wei FW, Li M, Quan GQ, Li HH (2002) Current status and conservation of white-headed langur (Trachypithecus leucophalus) in China. Biol Conserv 104:221–225. https://doi.org/10.1016/s0006-3207(01)00168-9
IMAGE Team (2001) The IMAGE 2.2 implementation of the SRES Scenarios. A comprehensive analysis of emissions, climate change and impacts in the 21st century. Netherlands Environmental Assessment Agency (MNP) CD-ROM Publication 500110001, Bilthoven
IUCN (2017) http://www.iucnredlist.org/
Jiang ZG, Meng ZB, Zeng Y, Wu ZG, Zhou ZH (2008) CITES no-detrimental finding for exporting rhesus monkeys (Macaca mulatta) from China. NDF Workshop case study. WG5-Mammals 6:1–15
Jiang ZG, Ma Y, Wu Y, Wang YX, Zhou KY, Liu SY et al (2015) China’s mammal diversity and geographic distribution. Science Press, Beijing
Keenan RJ, Reams GA, Achard F, de Freitas JV, Grainger A, Lindquist E (2015) Dynamics of global forest area: results from the FAO global forest resources assessment. For Ecol Manag 352:9–20. https://doi.org/10.1016/j.foreco.2015.06.014
Kolleck J, Yang MY, Zinner D, Roos C (2013) Genetic diversity in endangered Guizhou snub-nosed monkeys (Rhinopithecus brelichi): contrasting results from microsatellite and mitochondrial DNA data. PLoS ONE 8:e73647. https://doi.org/10.1371/journal.pone.0073647
Kou WL, Xiao XG, Dong JW, Gan S, Zhai DL, Zhang GL et al (2015) Mapping deciduous rubber plantation areas and stand ages with PALSAR and landsat images. Remote Sens 7:1048–1073. https://doi.org/10.3390/rs70101048
Laurance W (2017) The dark legacy of China’s drive for global resources. Yale Environment 360. March 28 (http://e360.yale.edu/features/the-dark-legacy-of-china’s-drive-for-globalresources?from=timeline&isappinstalled=0. Accessed 28 March 2017
Lee J, Wang F (1999) Malthusian models and Chinese realities: the Chinese demographic system 1700–2000. Popul Dev Rev 25:33–65. https://doi.org/10.1111/j.1728-4457.1999.00033.x
Li W, Wang H (1999) Wildlife in Yunnan Province, China, at the border with Vietnam. Traffic B 18:21–30
Li BG, Pan RL, Oxnard CE (2002) Extinction of snub-nosed monkeys in China during the past 400 years. Int J Primatol 23:1227–1244. https://doi.org/10.1023/A:1021122819845
Li YB, Huang CM, Ding P, Tang Z, Wood C (2007) Dramatic decline of François’ langur Trachypithecus francoisi in Guangxi province, China. Oryx 41:38–43. https://doi.org/10.1017/s0030605307001500
Li XQ, Dodson J, Zhou J, Zhou XY (2009) Increases of population and expansion of rice agriculture in Asia, and anthropogenic methane emissions since 5000BP. Quat Int 202:41–50. https://doi.org/10.1016/j.quaint.2008.02.009
Li YC, Liu F, He XY, Ma C, Sun J, Li DH, Xiao W, Cui LW (2015a) Social organization of Shortridge’s capped langur (Trachypithecus shortridgei) at the Dulongjiang Valley in Yunnan, China. Zool Res 36:152–160
Li C, Zhao C, Fan PF (2015b) White-cheeked macaque (Macaca leucogenys): a new macaque species from Medog, southeastern Tibet. Am J Primatol 77:753–766. https://doi.org/10.1002/ajp.22394
Liedigk R, Yang M, Jablonski NG, Momberg F, Geissmann T, Lwin N et al (2012) Evolutionary history of the odd-nosed monkeys and the phylogenetic position of the newly described Myanmar snub-nosed monkey Rhinopithecus strykeri. PLoS ONE 7:e37418. https://doi.org/10.1371/journal.pone.0037418
Lin HB, Fan H, Zhang F, Huang XQ, Lin KQ, Shi L, Hu SN et al (2010) Genetic relationships of ethnic minorities in southwest China revealed by microsatellite markers. PLoS ONE 5:e9895. https://doi.org/10.1371/journal.pone.0009895
Liu J (2010) China’s road to sustainability. Science. https://doi.org/10.1126/science.1186234
Liu J (2013) Forest sustainability in China and implications for a telecoupled world. Asian Pac Policy Stud 1:230–250. https://doi.org/10.1002/app5.17
Liu L, Chen XC (2012) The archaeology of China: from the late paleolithic to the early bronze age. Cambridge University Press, Cambridge
Liu ZH, Yu SM, Yuan XC (1984) Resources of the Hainan black gibbons and its present situation. Chin Wildl 6:1–4
Liu XN, Feng ZM, Jiang LU, Li P, Liao CH, Yang YZ et al (2013) Rubber plantation and its relationship with topographical factors in the border region of China, Laos and Myanmar. J Geogr Sci 23:1019–1040. https://doi.org/10.1007/s11442-013-1060-4
Long YC, and Richardson M (2008) Rhinopithecus roxellana. The IUCN Red List of Threatened Species 2008: e.T19596A8985735
Long YC, Kirkpatrick CR, Zhong T, Xiao L (1994) Report on distribution, population and ecology of the Yunnan snub-nosed monkey (Rhinopithecus bieti). Primates 35:241–250. https://doi.org/10.1007/bf02382060
Long YC, Momberg F, Ma J, Wang Y, Luo YM, Li HS et al (2012) Rhinopithecus strykeri found in China! Am J Primatol 74:871–873. https://doi.org/10.1002/ajp.22041
Lu JQ, Hou JH, Wang HF, Qu WY (2007) Current status of Macaca mulatta in Taihangshan Mountains Area, Jiyuan, Henan, China. Int J Primatol 28:1085–1091. https://doi.org/10.1007/s10764-007-9197-6
Lu JQ, Tian JD, Zhang P (2018) Advances in ecological research regarding rhesus macaques (Macaca mulatta) in China. Acta Theriol Sin 37:74–84
Ma C, Huang ZP, Zhao XF, Zhang LX, Sun WM, Scott MB et al (2014) Distribution and conservation status of Rhinopithecus strykeri in China. Primates 55:1–6. https://doi.org/10.1007/s10329-014-0425-3
Ma C, Luo ZH, Liu CM, Orkin JD, Xiao W, Fan PF (2015) Population and Conservation Status of Indochinese Gray Langurs (Trachypithecus crepusculus) in the Wuliang Mountains, Jingdong, Yunnan, China. Int J Primatol 36:749–763. https://doi.org/10.1007/s10764-015-9852-2
Meng QY (2015) The land revolution in China from an academic history perspective: changes of topics and paradigms. Chin J Sociol 1:419–446. https://doi.org/10.1177/2057150x15593713
Meyer D, Momberg F, Matauschek C, Oswald P, Lwin N, Aung SS et al (2017) Conservation status of the Myanmar or black snub-nosed monkey Rhinopithecus strykeri. Fauna & Flora International, Yangon, Myanmar and German Primate Center, Göttingen
Ministry of Forestry (1987) China’s forest zoning. China’s Forestry Publishing House, Beijing
Nadler T (2016a) Indochinese Gray Langur—Trachypithecus crepusculus. In: Rowe N, Myers M (eds) All the World’s Primates. Pogonias Press, Charlestown, p 592
Nadler T (2016b) White-headed langur—Trachypithecus leucocephalus. In: Rowe N, Myers M (eds) All the world’s primates. Pogonias Press, Charlestown, pp 604–605
New T, Xie ZQ (2008) Impacts of large dams on riparian vegetation: applying global experience to the case of China’s Three Gorges Dam. Biodivers Conserv 17:3149–3163. https://doi.org/10.1007/s10531-008-9416-2
Newmark WD, Jenkins CN, Pimm SL, McNeally PB, Halley JM (2017) Targeted habitat restoration can reduce extinction rates in fragmented forests. Proc Natl Acad Sci USA 114:9635–9640. https://doi.org/10.1073/pnas.1705834114
Nijman V (2010) An overview of international wildlife trade from southeast Asia. Biodivers Conserv 19:1101–1114. https://doi.org/10.1007/s10531-009-9758-4
Nijman V, Shepherd CR, Nekaris KAI (2014) Trade in Bengal slow lorises in Mong La, Myanmar, on the China border. Primate Conserv 28:139–142. https://doi.org/10.1896/052.028.0112
Pan RL (1986) Environmental changes at Menghai and other cultivated areas in Xishangbanna, Yunnan Province. Zool Res 7:190–202 (in Chinese)
Pan RL, Oxnard C, Grueter CC, Li BG, Qi XG, He G et al (2016) A new conservation strategy for China: a model starting with primates. Am J Primatol 78:1137–1148. https://doi.org/10.1002/ajp.22577
Piao SL, Ciais P, Huang Y, Shen ZH, Peng SS, Li JS et al (2010) The impacts of climate change on water resources and agriculture in China. Nature 467:43–51. https://doi.org/10.1038/nature09364
Qiu J (2009) Where the rubber meets the garden. Nature 457:246–247. https://doi.org/10.1038/457246a
Qiu J (2010) China drought highlights future climate threats. Nature 465:142–143. https://doi.org/10.1038/465142a
Ren GP, Young SS, Wang L, Wang W, Long YC, Wu RD et al (2015) Effectiveness of China’s national forest protection program and nature reserves. Conserv Biol 29:1368–1377. https://doi.org/10.1111/cobi.12561
Rosen GE, Smith KF (2010) Summarizing the evidence on the international trade in illegal wildlife. EcoHealth 7:24–32. https://doi.org/10.1007/s10393-010-0317-y
Ruan GW, Huang ZY (2014) Preliminary study on population ecology of Macaca arctoides in Tiantang Mountain Nature Reserve, Yulin, Guangxi. J Yulin Norm Univ (Nat Sci) 35:64–67. https://doi.org/10.3969/j.issn.1004-4671.2014.02.016
Schwitzer C, Mittermeier RA, Rylands AB, Chiozza F, Williamson EA, Wallis J, Cotton A (2015) Primates in Peril: the world’s most endangered primates 2014–2016. Conservation International, Arlington
Struebig MJ, Fischer M, Gaveau DLA, Meijaard E, Wich SA, Gonner C et al (2015) Anticipated climate and land-cover changes reveal refuge areas for Borneo’s orang-utans. Glob Chang Biol 21:2891–2904. https://doi.org/10.1111/gcb.12814
Sun XF, Wang LQ, Gu ZB (2005) A brief overview of China’s timber market system. Int For Rev 6:221–226. https://doi.org/10.1505/ifor.6.3.221.59973
Sun BH, Li JH, Yong ZH, Xia DP (2010) Mitochondrial DNA variation in Tibetan macaques (Macaca thibetana). Folia Zool 59:301–307. https://doi.org/10.25225/fozo.v59.i4.a5.2010
Tang X, McLellan BC, Snowden S, Zhang BS, Höök M (2015) Dilemmas for China: energy, economy and environment. Sustainability 7:5508–5520. https://doi.org/10.3390/su7055508
Thang VN (2016) Eastern Black crested gibbon: Nomascus nasutus. In: Rowe N, Myers M (eds) All the World’s primates. Pogonias Press, Charlestown, pp 657–658
Townsend PA, Masters KL (2015) Lattice-work corridors for climate change: a conceptual framework for biodiversity conservation and social-ecological resilience in a tropical elevational gradient. Ecol Soc 20:1. https://doi.org/10.5751/es-07324-200201
Turvey ST, Grees JJ, Di Fonzo MMI (2015) Historical data as a baseline for conservation: reconstructing long-term faunal extinction dynamics in Late Imperial—modern China. Proc R Soc B. https://doi.org/10.1098/rspb.2015.1299
Turvey ST, Bryant JV, Duncan C, Wong MHG, Fei H, Ma C, Hong X, Nash HC, Chan BPL, Xu Y, Fan PF (2017) How many remnant gibbon populations are left on Hainan? Testing the use of local ecological knowledge to detect cryptic threatened primates. Am J Primatol 79:e22593. https://doi.org/10.1002/ajp.22593
UNEP-WCMC (2017) World database of protected areas, May 2017. www.protectedplanet.net
Vina A, McConell WJ, Yang HB, Xu ZC, Liu JG (2016) Effects of conservation policy on China’s forest recovery. Sci Adv 2:e1500965. https://doi.org/10.1126/sciadv.1500965
Viswanathan PK (2007) Critical issues facing China’s rubber industry in the era of market integration: an analysis in retrospect and prospect. Working Paper No. 177. Gujarat Institute of Development Research, Gota, India (ISBN 81-89023-35-7)
Waley-Cohen J (2004) Expansion and colonization in early modern Chinese history. Hist Compass 2:1–6. https://doi.org/10.1111/j.1478-0542.2004.00076.x
Wallis J, Lonsdorf EV (2010) Summary of recommendations for primate conservation education programs. Am J Primatol 72:441–444. https://doi.org/10.1002/ajp.20764
Wang WR, Yao M (2017) Fine-scale genetic structure analyses reveal dispersal patterns in a critically endangered primate, Trachypithecus leucocephalus. Am J Primatol 79:e22635. https://doi.org/10.1002/ajp.22635
Wang C, Lu HY, Zhang JP, Gu ZY, He KY (2014) Prehistoric demographic fluctuations in China inferred from radiocarbon data and their linkage with climate change over the past 50,000 years. Quat Sci Rev 98:45–59. https://doi.org/10.1016/j.quascirev.2014.05.015
Wang HH, Liu ZH, Xu ZM, Ding W, Xiao W (2015) Primate species diversity and disturbed way in Lanping. J Fujian For Sci 42:154–160
Wang J, Xin L, Tan M, Wang Y (2016a) Spatial heterogeneity in Chinese forest area change in the early 21st century. Forests 7:232. https://doi.org/10.3390/f7100232
Wang HH, Zhang SX, Xu ZM, Xiao W, Ding W, Xu LY et al (2016b) The temporal and spatial dynamics change of primate population in Yunlong County. Sichuan J Zool 35:801–809
Wang YY, Wu GL, Deng L, Tang ZS, Wang KB, Sun WY, Shangguan ZP (2017) Prediction of aboveground grassland biomass on the Loess Plateau, China, using a random forest algorithm. Sci Rep 7:6940. https://doi.org/10.1038/s41598-017-07197-6
Wei FW, Swaisgood R, Hu YB, Nie YG, Yan L, Zhang ZJ et al (2015) Progress in ecology and conservation of giant pandas. Conserv Biol 29:1497–1507. https://doi.org/10.1111/cobi.12582
Wen Y (2016) China’s rapid rise from backward agrarian society to industrial powerhouse in just 35 years. Reg Econ 24:8–14
Wu MC, Wei ZY, He NL (1987) Distribution and ecology of black langur (Presbytis francoisi Pousargues) in Guangxi Province. Chin Wildl 4:12–13 (in Chinese)
Wu RD, Long YC, Malanson GP, Garber PA, Zhang S, Li DQ et al (2014) Optimized spatial priorities for biodiversity conservation in China: a systematic conservation planning perspective. PLoS ONE 9:e103783. https://doi.org/10.1371/journal.pone.0103783
Xiang ZF, Huo S, Wang L, Cui LW, Xiao W, Quan RC, Tai Z (2007) Distribution, status and conservation of the black-and-white snub-nosed monkey Rhinopithecus bieti in Tibet. Oryx 41:525–531. https://doi.org/10.1017/s0030605307012124
Xu JC (2011) China’s new forests aren’t as green as they seem. Nature 477:371. https://doi.org/10.1038/477371a
Xu WH, Xiao Y, Zhang JG, Yang W, Zhang L, Hull V et al (2017) Strengthening protected areas for biodiversity and ecosystem services in China. Proc Natl Acad Sci USA 114:1601–1606. https://doi.org/10.1073/pnas.1620503114
Yang Y, Groves C, Garber PA, Wang X, Li H, Long Y, Li G, Tian Y, Dong S, Yang S, Behie A, Xiao W (2018) First insights into the feeding habits of the Critically Endangered Rhinopithecus strykeri: dietary characteristics and food resource distribution patterns. Am J Primatol
Ye ZZ (1993) Biology of Langurs (Presbytis). Yunnan Science and Technology Press, Kunming
Zhang YQ (2000) Deforestation and forest transition: theory and evidence in China. In: Palo M, Vanhanen H (eds) World forests from deforestation to transition?. Kluwer Academic Publishers, Dordrecht
Zhang YR, Wang SN (2018) Top ten conservation projects for Chinese wild animals—maintaining the beauty of the world. China Green Time (in Chinese). April 3
Zhang RZ, Chen LW, Qu WY, Chris C (2002) The primates of China: biogeography and conservation status. China Forestry Publishing House, Beijing
Zhang T, Teng JR, Wang HX (2005) Ecological habits and resource status of Tibetan macaques in Baishuijiang Nature Reserve of Gansu province. Sichuan J Zool 24:165–167
Zhang L, Hua N, Sun S (2008a) Wildlife trade, consumption and conservation awareness in southwest China. Biodivers Conserv 17:1493–1516. https://doi.org/10.1007/s10531-008-9358-8
Zhang Q, Lan SJ, Hu DM, Yu XX, Gu HJ, Chen X et al (2008b) Activities of Tibetan macaque in Baishuihe National Nature Reserve, Sichuan province. Sichuan J Zool 27:131–135
Zhang MX, Fellowes JR, Jiang XL, Wang W, Bosco PLC, Ren GP, Zhu JG (2010) Degradation of tropical forest in Hainan, China, 1991–2008: conservation implications for Hainan gibbon (Nomascus hainanus). Biol Conserv 143:1397–1404. https://doi.org/10.1016/j.biocon.2010.03.014
Zhao G (2006) Reinventing China imperial Qing ideology and the rise of modern Chinese National identity in the Early Twentieth Century. Mod China 32:3–30. https://doi.org/10.1177/0097700405282349
Zhao HT, Wang CL, Wang XW, Wang KF, Zhang BY, Li JF et al (2016) Discovery of Tibetan macaques (Macaca thibetana) in Shaanxi Micangshan National Nature Reserve. Chin J Zool 49:793–797. https://doi.org/10.13859/j.cjz.201406001
Zhao XM, Ren BP, Garber PA, Li XH, Li M (2018) Impacts of human activities and climate change on the distribution of snub-nosed monkeys in China during the past 2000 Years. Divers Distrib 24:92–102. https://doi.org/10.1111/ddi.12657
Zhou Y, Zhang P (2013) Distribution and vicissitude of gibbons (Hylobatidae) in China during the last 500 years. Acta Theriol Sin 33:258–266
Zhou J, Wei FW, Li M, Zhang JF, Wang DL, Pan RL (2005) Hainan Black-crested gibbon is headed for extinction. Int J Primatol 26:453–465. https://doi.org/10.1007/s10764-005-2933-x
Zhou XM, Wang BS, Pan Q, Zhang JB, Kumar S, Sun XQ et al (2014) Whole-genome sequencing of the snub-nosed monkey provides insights into folivory and evolutionary history. Nat Genet 46:1303–1310. https://doi.org/10.1038/ng.3137
Zhou XM, Meng XH, Liu ZZ, Chang J, Wang BS, Li MZ et al (2016) Population genomics reveals low genetic diversity and adaptation to hypoxia in snub-nosed monkeys. Mol Biol Evol 33:2670–2681. https://doi.org/10.1093/molbev/msw150
Zhu Q (2015) From the first five-year plan to the cultural revolution: the pre-reform urban transformation of Hangzhou. Plan Perspect 30:571–595. https://doi.org/10.1080/02665433.2014.995694
Ziegler AD, Fox JM, Xu JC (2009) The rubber juggernaut. Science 324:1024–1025. https://doi.org/10.1126/science.1173833
Acknowledgements
This project was sponsored by the following Grants: Baoguo Li, Key Project of Natural Science Foundation of China (31730104) and National Key Program of Research and Development, Ministry of Science and Technology (2016YFC0503200), Ming Li (National Key R&D Program of China, 2016YFC0503200 and Strategic Priority Research Program of the Chinese Academy of Sciences, XDPB0202), Pengfei Fan (National Program for Support of Top-notch Young Professionals in China, National Natural Science Foundation of China—NNSFC, 30900169; 31160424; 31372216). Jiqi Lu (NNSFC, 31472018 and 31672302) and Qingyong Ni (NNSFC, 31501873 and Kadoorie Conservation China, Kadoorie Farm & Botanic Garden Corporation). Jinhua Li (NSFC, No. 31672307 and 31372215). Sidney Gouveia (Brazilian CNPq Grants, Procs. #303180/2016-1 and 402469/2016-0); Zhipang Huang (Collaborative Innovation Center for Biodiversity and Conservation in the Three Parallel Rivers Region of China). Colin Groves unfortunately passed away during the final stage of this project, and we wish to highlight his contributions to this manuscript. We also wish to take this opportunity to celebrate his significant achievements in primatology, particularly those related to China through his cooperation with a great number of Chinese scholars. Ruliang Pan wishes to thank his wife, Aiqun Zhang, for her enthusiastic support, so that he was able to use spare time on the project. Paul A. Garber also wishes to thank Chrissie, Sara, and Jenni for their love, guidance, and support, which have inspired his work on primate conservation. Our final thanks is given to Rong Hou who assisted in manuscript preparation.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Communicated by Xiaoli Shen.
Rights and permissions
About this article
Cite this article
Li, B., Li, M., Li, J. et al. The primate extinction crisis in China: immediate challenges and a way forward. Biodivers Conserv 27, 3301–3327 (2018). https://doi.org/10.1007/s10531-018-1614-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-018-1614-y