Volume 41 Issue 4
Jul.  2020
Turn off MathJax
Article Contents
Chi Ma, Wei-Guo Xiong, Li Yang, Lu Zhang, Peter Robert Tomlin, Wu Chen, Peng-Fei Fan. Living in forests: strata use by Indo-Chinese gray langurs (Trachypithecus crepusculus) and the effect of forest cover on Trachypithecus terrestriality. Zoological Research, 2020, 41(4): 373-380. doi: 10.24272/j.issn.2095-8137.2020.047
Citation: Chi Ma, Wei-Guo Xiong, Li Yang, Lu Zhang, Peter Robert Tomlin, Wu Chen, Peng-Fei Fan. Living in forests: strata use by Indo-Chinese gray langurs (Trachypithecus crepusculus) and the effect of forest cover on Trachypithecus terrestriality. Zoological Research, 2020, 41(4): 373-380. doi: 10.24272/j.issn.2095-8137.2020.047

Living in forests: strata use by Indo-Chinese gray langurs (Trachypithecus crepusculus) and the effect of forest cover on Trachypithecus terrestriality

doi: 10.24272/j.issn.2095-8137.2020.047
Funds:  This study was supported by the National Natural Science Foundation of China (31372216, 31822049)
More Information
  • Studies on behavioral flexibility in response to habitat differences and degradation are crucial for developing conservation strategies for endangered species. Trachypithecus species inhabit various habitats and display different patterns of strata use; however, the effect of habitat structure on strata use remains poorly studied. Here, we investigated strata use patterns of Indo-Chinese gray langurs (Trachypithecus crepusculus) in a primary evergreen forest in Mt. Wuliang, southwest China, from June 2012 to January 2016. In addition, we compared T. crepusculus strata use and terrestriality with five other Trachypithecus species from previous studies. Unlike langurs living in karst forests, our study group was typically arboreal and spent only 2.9% of time on the ground. The group showed a preference for higher strata when resting and lower strata (<20 m) when moving. The langurs primarily used time on the ground for geophagy, but otherwise avoided the ground during feeding. These strata use patterns are similar to those of limestone langurs (T. francoisi) when using continuous forests. At the genus level (n=6 species), we found a negative relationship between habitat forest cover and terrestriality. This negative relationship was also true for the five limestone langur species, implying limestone langurs increase territoriality in response to decreased forest cover. Our results document behavioral flexibility in strata use of Trachypithecus langurs and highlight the importance of the protection of continuous forests to promote langur conservation.

  • loading
  • [1]
    Aggimarangsee N. 2004. Behavior and Ecology of Isolated Dusky Langur (Trachypithecus Obscurus) Population at Khao Lommuak, Prachuap Khiri Khan Province, Thailand. Ph.D. dissertation, Chiang Mai University, Chiang Mai.
    [2]
    Altmann J. 1974. Observational study of behavior: sampling methods. Behaviour, 49(3–4): 227−267.
    [3]
    Bennett EL, Davies AG. 1994. The ecology of Asian colobines. In: Davies AG, Oates JF. Colobine Monkeys. Cambridge: Cambridge University Press, 129–171.
    [4]
    Borries C, Primeau ZM, Ossi-Lupo K, Dtubpraserit S, Koenig A. 2014. Possible predation attempt by a marbled cat on a juvenile Phayre’s leaf monkey. Raffles Bulletin of Zoology, 62: 561−565.
    [5]
    Campbell CJ, Aureli F, Chapman CA, Ramos-Fernández G, Matthews K, Russo SE, Suarez S, Vick L. 2005. Terrestrial behavior of Ateles spp. International Journal of Primatology, 26(5): 1039−1051. doi:  10.1007/s10764-005-6457-1
    [6]
    Chapman CA. 2018. A road for a promising future for China’s primates: the potential for restoration. Zoological Research, 39(4): 244−248. doi:  10.24272/j.issn.2095-8137.2018.032
    [7]
    Fan PF. 2007. The Ecology and Behavior of Black Crested Gibbon (Nomascus Concolor Jingdongensis) at Dazhaizi, Wuliang Mountain, Yunnan, China. Ph.D. dissertation, Chinese Academy of Sciences, Kunming.
    [8]
    Fan PF, Garber P, Ma C, Ren GP, Liu CM, Chen XY, Yang JX. 2015. High dietary diversity supports large group size in Indo-Chinese gray langurs in Wuliangshan, Yunnan, China. American Journal of Primatology, 77(5): 479−491. doi:  10.1002/ajp.22361
    [9]
    Fan PF, Jiang XL. 2008. Effects of food and topography on ranging behavior of black crested gibbon (Nomascus concolor jingdongensis) in Wuliang mountain, Yunnan, China. American Journal of Primatology, 70(9): 871−878. doi:  10.1002/ajp.20577
    [10]
    Fan PF, Jiang XL, Tian CC. 2009. The critically endangered black crested gibbon Nomascus concolor on Wuliang Mountain, Yunnan, China: the role of forest types in the species' conservation. Oryx, 43(2): 203−208. doi:  10.1017/S0030605308001907
    [11]
    Fan PF, Liu CM, Luo WS, Jiang XL. 2007. Can a group elicit duets from its neighbours? A field study on the black-crested gibbon (Nomascus concolor jingdongensis) in Central Yunnan, China. Folia Primatologica, 78(3): 186−195. doi:  10.1159/000099139
    [12]
    Fan PF, Ma C. 2018. Extant primates and development of primatology in China: publications, student training, and funding. Zoological Research, 39(4): 249−254. doi:  10.24272/j.issn.2095-8137.2018.033
    [13]
    Fan PF, Ni QY, Sun GZ, Huang B, Jiang XL. 2008. Seasonal variations in the activity budget of Nomascus concolor jingdongensis at Mt. Wuliang, Central Yunnan, China: effects of diet and temperature. International Journal of Primatology, 29(4): 1047−1057. doi:  10.1007/s10764-008-9256-7
    [14]
    Fleagle JG. 1998. Primate Adaptation and Evolution. 2nd ed. San Diego: Academic Press.
    [15]
    Fruth B, McGrew WC. 1998. Resting and nesting in primates: behavioral ecology of inactivity. American Journal of Primatology, 46(1): 3−5. doi:  10.1002/(SICI)1098-2345(1998)46:1<3::AID-AJP2>3.0.CO;2-#
    [16]
    Galán-Acedo C, Arroyo-Rodríguez V, Cudney-Valenzuela SJ, Fahrig L. 2019. A global assessment of primate responses to landscape structure. Biological Reviews, 94(5): 1605−1618. doi:  10.1111/brv.12517
    [17]
    Gordon TAC, Harding HR, Wong KE, Merchant ND, Meekan MG, McCormick MI, Radford AN, Simpson SD. 2018. Habitat degradation negatively affects auditory settlement behavior of coral reef fishes. Proceedings of the National Academy of Sciences of the United States of America, 115(20): 5193−5198. doi:  10.1073/pnas.1719291115
    [18]
    Grueter CC, Li DY, Ren BP, Li M. 2013. Substrate use and postural behavior in free-ranging snub-nosed monkeys (Rhinopithecus bieti) in Yunnan. Integrative Zoology, 8(4): 335−345. doi:  10.1111/1749-4877.12023
    [19]
    Guan ZH. 2013. The Ecological and Social Behavior of Black-Crested Gibbon (Nomascus Concolor) at Dazhaizi, Wuliang Mountain, Central Yunnan, China. Ph.D. dissertation, University of Chinese Academy of Sciences, Beijing. (in Chinese)
    [20]
    He K, Hu NQ, Orkin JD, Nyein DT, Ma C, Xiao W, Fan PF, Jiang XL. 2012. Molecular phylogeny and divergence time of Trachypithecus: with implications for the taxonomy of T. phayrei. Zoological Research, 33(E3–E4): E104−E110.
    [21]
    Hendershott R, Rawson B, Behie A. 2018. Home Range Size and Habitat use by Cat Ba Langurs (Trachypithecus poliocephalus) in a Disturbed and Fragmented Habitat. International Journal of Primatology, 39(4): 547−566. doi:  10.1007/s10764-018-0051-9
    [22]
    Hendershott R. 2017. Socioecology of Cat Ba Langurs (Trachypithecus Poliocephalus): Implications for Conservation. Ph.D. dissertation, Australian National University, Australian.
    [23]
    Hrdy SB. 1977. Infanticide as a primate reproductive strategy. American Scientist, 65(1): 40−49.
    [24]
    Hu NQ, Guan ZH, Huang B, Ning WH, He K, Fan PF, Jiang XL. 2018. Dispersal and female philopatry in a long-term, stable, polygynous gibbon population: Evidence from 16 years field observation and genetics. American Journal of Primatology, 80(9): e22922. doi:  10.1002/ajp.22922
    [25]
    Huang C, Wei F, Li M, Li Y, Sun R. 2003. Sleeping cave selection, activity pattern and time budget of white-headed langurs. International Journal of Primatology, 24(4): 813−824. doi:  10.1023/A:1024628822271
    [26]
    Huang CM, Li YB. 2005. How does the white-headed langur (Trachypithecus leucocephalus) adapt locomotor behavior to its unique limestone hill habitat?. Primates, 46(4): 261−267. doi:  10.1007/s10329-005-0130-3
    [27]
    Huang CM, Wei FW, Li M, Quan GQ, Li HH. 2002. Current status and conservation of white-headed langur (Trachypithecus leucocephalus) in China. Biological Conservation, 104(2): 221−225. doi:  10.1016/S0006-3207(01)00168-9
    [28]
    Jiang XL, Ma SL, Wang YX, Sheeran LK, Poirier FE. 1994. Human encounter and predator avoidance behavior in black-crested gibbon, Hylobates concolor. Acta Anthropologica Sinica, 13(2): 181−188. (in Chinese)
    [29]
    Kirkpatrick RC. 2011. The asian colobines: diversity among leaf-eating monkeys. In: Campbell CJ, Fuentes A, MacKinnon KC, Bearder SK, Stumpf RM. Primates in Perspective. New York: Oxford University Press, 189–202.
    [30]
    Li ZY, Rogers ME. 2005. Are Limestone Hills a Refuge or Essential Habitat for White-Headed Langurs in Fusui, China?. International Journal of Primatology, 26(2): 437−452. doi:  10.1007/s10764-005-2932-y
    [31]
    Li ZY, Rogers ME. 2006. Food items consumed by white-headed langurs in Fusui, China. International Journal of Primatology, 27(6): 1551−1567. doi:  10.1007/s10764-006-9090-8
    [32]
    Liu GQ. 2017. Camera-trap pictures of over 20 wildlife species were captured in the Wuliang Mountain, Jingdong County. (2020-03-13). https://www.sohu.com/a/206694488_761010. (in Chinese)
    [33]
    Ma C, Fan PF, Zhang ZY, Li JH, Shi XC, Xiao W. 2017. Diet and feeding behavior of a group of 42 Phayre's langurs in a seasonal habitat in Mt. Gaoligong, Yunnan, China. American Journal of Primatology, 79(10): e22695. doi:  10.1002/ajp.22695
    [34]
    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. International Journal of Primatology, 36(4): 749−763. doi:  10.1007/s10764-015-9852-2
    [35]
    McGraw WS. 1996. Cercopithecid locomotion, support use, and support availability in the Tai Forest, Ivory Coast. American Journal of Physical Anthropology, 100(4): 507−522. doi:  10.1002/(SICI)1096-8644(199608)100:4<507::AID-AJPA5>3.0.CO;2-N
    [36]
    McGraw WS, Sciulli PW. 2011. Posture, ischial tuberosities, and tree zone use in West African Cercopithecids. In: D'Août K, Vereecke EE. Primate Locomotion: Linking Field and Laboratory Research. New York: Springer, 215–246.
    [37]
    Mekonnen A, Fashing PJ, Sargis EJ, Venkataraman VV, Bekele A, Hernandez-Aguilar RA, Rueness EK, Stenseth NC. 2018. Flexibility in positional behavior, strata use, and substrate utilization among Bale monkeys (Chlorocebus djamdjamensis) in response to habitat fragmentation and degradation. American Journal of Primatology, 80(5): e22760. doi:  10.1002/ajp.22760
    [38]
    Mittermeier RA, Rylands AB, Wilson DE. 2013. Handbook of the Mammals of the World. Vol. 3. Primates. Barcelona: Lynx Edicions.
    [39]
    Newton P. 1992. Feeding and ranging patterns of forest hanuman langurs (Presbytis entellus). International Journal of Primatology, 13(3): 245−285. doi:  10.1007/BF02547816
    [40]
    Oates JF, Davies AG. 1994. What are the colobines?. In: Davies AG, Oates GF. Colobine Monkeys: Their Ecology, Behaviour and Evolution. Cambridge: Cambridge University Press, 1–10.
    [41]
    Pages G, Lloyd E, Suarez SA. 2005. The impact of geophagy on ranging behaviour in Phayre's leaf monkeys (Trachypithecus phayrei). Folia Primatologica, 76(6): 342−346. doi:  10.1159/000089532
    [42]
    Pebsworth PA, Huffman MA, Lambert JE, Young SL. 2019. Geophagy among nonhuman primates: a systematic review of current knowledge and suggestions for future directions. American Journal of Physical Anthropology, 168(567): 164−194.
    [43]
    Riley EP. 2008. Ranging patterns and habitat use of Sulawesi Tonkean macaques (Macaca tonkeana) in a human‐modified habitat. American Journal of Primatology, 70(7): 670−679. doi:  10.1002/ajp.20543
    [44]
    Rowe N, Myers M. 2016. All The World's Primates. Charlestown: Pogonias Press.
    [45]
    Roy D, Nagarajan R. 2018. Biology, ecology, and conservation of golden langur, Trachypithecus geei. In: Sivaperuman C, Venkataraman K. Indian Hotspots: Vertebrate Faunal Diversity, Conservation and Management Volume 1. Singapore: Springer, 251–283.
    [46]
    Srivastava KK, Bhardwaj AK, Abraham CJ, Zacharias VJ. 1996. Food habits of mammalian predators in Periyar Tiger Reserve, South India. Indian Forester, 122(10): 877−883.
    [47]
    Tian CC, Jiang XL, Peng H, Fan PF, Zhou SS. 2007. Tree species diversity and community structure characteristics in black crested gibbon (Nomascus concolor jingdongensis) habitats at Mt. Wuliang, central Yunnan, China. Acta Ecologica Sinica, 27(10): 4002−4010. (in Chinese) doi:  10.1016/S1872-2032(07)60089-4
    [48]
    Ware JV, Rode KD, Bromaghin JF, Douglas DC, Wilson RR, Regehr EV, Amstrup SC, Durner GM, Pagano AM, Olson J, Robbins CT, Jansen HT. 2017. Habitat degradation affects the summer activity of polar bears. Oecologia, 184(1): 87−99. doi:  10.1007/s00442-017-3839-y
    [49]
    Workman C. 2010. The Foraging Ecology of the Delacour's Langur (Trachypithecus Delacouri) in Van Long Nature Reserve, Vietnam. Ph.D. dissertation, Duke University, Durham.
    [50]
    Workman C, Schmitt D. 2012. Positional behavior of delacour's langurs (Trachypithecus delacouri) in northern Vietnam. International Journal of Primatology, 33(1): 19−37. doi:  10.1007/s10764-011-9547-2
    [51]
    Xiong JR, Gong SH, Qiu CG, Li ZY. 2009. Comparison of locomotor behaviour between white-headed langurs trachypithecus leucocephalus and francois' langurs T. francoisi in fusui, China. Current Zoology, 55(1): 9−19. doi:  10.1093/czoolo/55.1.9
    [52]
    Yu QG. 2004. Wuliangshan National Nature Reserve. Kunming: Yunnan Science and Technology Press. (in Chinese)
    [53]
    Zhang P, Li BG, Watanabe K. 2006. Use of forest strata by Sichuan snub-nosed monkeys Rhinopithecus roxellana in spring and winter in Qinling Mountains, China. Acta Zoologica Sinica, 52(3): 429−436.
    [54]
    Zhou QH, Huang CM, Li M, Wei FW. 2009. Sleeping site use by Trachypithecus francoisi at Nonggang Nature Reserve, China. International Journal of Primatology, 30(2): 353−365. doi:  10.1007/s10764-009-9348-z
    [55]
    Zhou QH, Luo B, Wei FW, Huang CM. 2013. Habitat use and locomotion of the Francois' langur (Trachypithecus francoisi) in limestone habitats of Nonggang, China. Integrative Zoology, 8(4): 346−355. doi:  10.1111/j.1749-4877.2012.00299.x
  • Relative Articles

    [1] Ying Geng, Jia-Fei He, Ying-Chun Li, Zhen-Hua Guan, Xiao-Yang He, Jun Sun, Zhi-Pang Huang, Yan-Peng Li, Fan Yong, Wen Xiao, Liang-Wei Cui. Preliminary study on dietary selection in Shortridge’s langurs (Trachypithecus shortridgei) from China. Zoological Research, 2020, 41(6): 715-720.  doi: 10.24272/j.issn.2095-8137.2020.123
    [2] Christian Roos, Kristofer M. Helgen, Roberto Portela Miguez, Naw May Lay Thant, Ngwe Lwin, Aung Ko Lin, Aung Lin, Khin Mar Yi, Paing Soe, Zin Mar Hein, Margaret Nyein Nyein Myint, Tanvir Ahmed, Dilip Chetry, Melina Urh, E. Grace Veatch, Neil Duncan, Pepijn Kamminga, Marcus A. H. Chua, Lu Yao, Christian Matauschek, Dirk Meyer, Zhi-Jin Liu, Ming Li, Tilo Nadler, Peng-Fei Fan, Le Khac Quyet, Michael Hofreiter, Dietmar Zinner, Frank Momberg. Mitogenomic phylogeny of the Asian colobine genus Trachypithecus with special focus on Trachypithecus phayrei (Blyth, 1847) and description of a new species. Zoological Research, 2020, 41(6): 656-669.  doi: 10.24272/j.issn.2095-8137.2020.254
    [3] Dong-Dong Qin, Shu-Fei Feng, Fei-Yu Zhang, Na Wang, Wen-Jie Sun, Yin Zhou, Teng-Fang Xiong, Xian-Lai Xu, Xiao-Ting Yang, Xiang Zhang, Xue Zhu, Xin-Tian Hu, Lei Xiong, Yun Liu, Yong-Chang Chen. Potential use of actigraphy to measure sleep in monkeys: comparison with behavioral analysis from videography. Zoological Research, 2020, 41(4): 437-443.  doi: 10.24272/j.issn.2095-8137.2020.056
    [4] Qi-Hai Zhou, Zhong-Hao Huang, Hua Wei, Cheng-Ming Huang. Variations in diet composition of sympatric Trachypithecus francoisi and Macaca assamensis in the limestone habitats of Nonggang, China. Zoological Research, 2018, 39(4): 284-290.  doi: 10.24272/j.issn.2095-8137.2018.046
    [5] Yong-Gang Yao. Creating animal models, why not use the Chinese tree shrew (Tupaia belangeri chinensis)?. Zoological Research, 2017, 38(3): 118-126.  doi: 10.24272/j.issn.2095-8137.2017.032
    [6] Yi-Ming Hu, Zhi-Xin Zhou, Zhi-Wen Huang, Ming Li, Zhi-Gang Jiang, Jian-Pu Wu, Wu-Lin Liu, Kun Jin, Hui-Jian Hu. A new record of the capped langur (Trachypithecus pileatus) in China. Zoological Research, 2017, 38(4): 203-205.  doi: 10.24272/j.issn.2095-8137.2017.038
    [7] Ying-Chun LI, Feng LIU, Xiao-Yang HE, Chi MA, Jun SUN, Dong-Hui LI, Wen XIAO, Liang-Wei CUI. Social organization of Shortridge's capped langur (Trachypithecus shortridgei) at the Dulongjiang Valley in Yunnan, China. Zoological Research, 2015, 36(3): 152-160.
    [8] Kai HE, Naiqing HU, Joseph D. ORKIN, Daw Thida NYEIN, Chi MA, Wen XIAO, Pengfei FAN, Xuelong JIANG. Molecular phylogeny and divergence time of Trachypithecus: with implications for the taxonomy of T. phayrei. Zoological Research, 2012, 33(E5-6): 104-110.  doi: 10.3724/SP.J.1141.2012.E05-06E104
    [9] Riaz Aziz Minhas, *, Khawaja Basharat Ahmed, Muhammad Siddique Awan, Naeem Iftikhar Dar. Habitat Utilization and Feeding Biology of Himalayan Grey Langur (Semnopithecus entellus ajex) in Machiara National Park, Azad Kashmir, Pakistan. Zoological Research, 2010, 31(2): 177-188.  doi: 10.3724/SP.J.1141.2010.02177
    [10] CAO Ming, ZHOU Wei, BAI Bing, ZHANG Qin, WANG Bin, CHEN Min-Yong. Habitat Use of Williamson’s Mouse deer (Tragulus williamsoni) in Mengla Area, Southern Yunnan. Zoological Research, 2010, 31(3): 303-309.  doi: 10.3724/SP.J.1141.2010.03311
    [11] ZHOU Qi-Hai, CAI Xiang-Wen, HUANG Cheng-Ming. Habitat Selection and Use of François's Langurs (Trachypithecus francoisi) in Guangxi Province, Fusui Area. Zoological Research, 2010, 31(4): 421-427.  doi: 10.3724/SP.J.1141.2010.04421
    [12] DAI Qiang, GU Hai-jun , WANG Yue-zhao. Theories and Models for Habitat Selection. Zoological Research, 2007, 28(6): 681-688.
    [13] BAI Bing, ZHOU Wei, *, AI Huai-sen, LI Zheng-bo, ZHANG Xing-yong, HU Cheng-gui. Habitat Use of the Hoolock Gibbon (Hoolock hoolock) at Nankang, Mt. Gaoligong in Spring. Zoological Research, 2007, 28(2): 179-185.
    [14] NING Jia-jia, HUANG Cheng-ming , * , YU Hai, DAI Dong-liang, WU Zheng-jun, ZHONG Yi-ming. Summer Habitat Characteristics of the Chinese Crocodile Lizard (Shinisaurus crocodilurus) in the Luokeng Nature Reserve, Guangdong. Zoological Research, 2006, 27(4): 419-426.
    [15] ZANG Qiang, ZHAO Ya-jun, LI Bao-ming, SHI Zheng-xiang, HAN Jing. Behavioral Differences of the Chinese Little Fat-tailed Sheep in Three Growth Phases in the Loose Housing System in Summer. Zoological Research, 2005, 26(3): 279-286.
    [16] ZHOU Jiang, XIE Jia-hua, DAI Qiang, ZENG Ya-jun, LIU Jian-xin, ZHANG Wen-gang, ZHANG Shu-yi. Feeding Behavioral Strategy of Rhinolophus pearsoni in Summer. Zoological Research, 2002, 23(2): 120-128.
    [17] ZHANG Hong-hai, MA Jian-zhang. Habitat Preference of Sables in Winter. Zoological Research, 1999, 20(5): 355-359.
    [18] XU Hong-fa, LU Hou-ji, LIU Xi-ping. The Current Status and Habitat Use of Chinese Water Deer in The Coast of Jiangsu Province. Zoological Research, 1996, 17(3): 217-224.
    [19] Zhao xiaofan, Wang jinxing, Li ming. The studies on the proteinases responsible for the degradation of the yolk proteins in Cyprinus carpio. Zoological Research, 1994, 15(zk): 119-123.
    [20] HUANG Gang, CHEN Qiao-yun, TANG Zhen-hua, CHIANG Chia-liang. Purification of Carboxylesterase and Enzymatic Degradation of 14C-Malathion in Multi-Organophosphate-Resistant Mosquito (Culex pipiens pallens Coq.). Zoological Research, 1982, 3(zk): 229-236.
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(4)  / Tables(1)

    Article Metrics

    Article views (1511) PDF downloads(159) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return