非人灵长类种群数量调查方法综述

doi:10.16829/j.slxb.150656

摘要/Abstract

摘要：

监测估算野生动物的种群数量是保护的核心工作。由于气候变化和人类活动的影响，野生动物种群常处于不稳定的状态。非人灵长类是动物界的高等类群，具有复杂的社会行为、丰富的物种多样性，全球有701种 (含亚种)，生活在多种类型的栖息地中，包括热带雨林、沼泽森林、红树林、次生林、落叶林、季雨林、山地森林，和包含孤存林、长廊森林、热带旱生林、山地草甸、地中海灌木林的稀树草原和干草原，以及荒漠、干旱的山地，甚至是雪地。绝大多数非人灵长类处于濒危的状态，长期有效的监测对于灵长类的保护十分重要。物种多样性和栖息地类型的多样性使得灵长类种群数量的调查方法多种多样。本文归纳总结了目前常用的非人灵长类种群数量调查方法的类型、基本原理、适用场景和局限性，并以研究实例加以分析；介绍了无人机、热成像、计算机学习系统等新技术应用在调查方法中的进展，希望为今后的非人灵长类野外数量调查、种群监测提供参考和启发。

关键词: 灵长类, 直接计数法, 样线法, 样点法, 红外相机调查法, 遗传调查法, 无人机调查法

Abstract:

Monitoring and estimating wildlife population size is essential to conservation. Affected by global climate change and human activities, wildlife populations could be relatively unstable. Primates are a group of highly evolved taxa in the animal kingdom and are among the most social of animals. As many as 701 species or subspecies of primates are recognized globally, forming a rich diversity. They could be found in various types of habitats, including rain forests, swamp forests, mangroves, secondary forests, deciduous forests, monsoon forests and montane forests, as well as in grasslands (savannah and steppe) including forest outliers, gallery forests, wooded steppes, thorn forests, Mediterranean scrubs and montane meadows, and even in deserts, dry uplands or permanent snow. Most primate species are endangered from different causes, and therefore effective long-term monitoring is of significant value to primate conservation. Species and habitat diversity have contributed to the numerous methods of censusing primate populations. This article offers a summary of widely-used non-human primate population censusing methods, including the classifications, the fundamentals, the various scenarios for application, and their limitations. The methods are analyzed with case studies and research. Furthermore, we introduce the latest applications of drones, thermal imaging and computer deep learning in primate population surveys, hoping to offer some insights into future non-human primate censusing and population monitoring.

Key words: Primates, Total count, Line transect sampling, Point census, Infra-red camera trap survey, Genetic methods of surveying, Survey by unmanned aerial vehicle

中图分类号:

Q958

陈熙尔, 殷丽洁, 秦大公, 姚锦仙, 李小雨, 潘文石. 非人灵长类种群数量调查方法综述[J]. 兽类学报, 2022, 42(6): 716-727.

Xier CHEN, Lijie YIN, Dagong QIN, Jinxian YAO, Xiaoyu LI, Wenshi PAN. An overview of population survey methods of non-human primates[J]. ACTA THERIOLOGICA SINICA, 2022, 42(6): 716-727.

图/表 1

参考文献 0

	Aldrich B C, Molleson L, Nekaris K A I. 2008. Vocalizations as a conservation tool: an auditory survey of the Andean titi monkey Callicebus oenanthe Thomas, 1924 (Mammalia: Primates: Pitheciidae) at Tarangue, Northern Peru. Contributions to Zoology, 77 (1): 1-6.
	Arandjelovic M, Vigilant L. 2018. Non‑invasive genetic censusing and monitoring of primate populations. American Journal of Primatology, 80 (3): e22743.
	Bapureddy G, Santhosh K, Jayakumar S, Kumara H N. 2015. Estimate of primate density using distance sampling in the evergreen forests of the central Western Ghats, India. Current Science, 108 (1): 118-123.
	Buckland S T, Plumptre A J, Thomas L, Rexstad E A. 2010a. Design and analysis of line transect surveys for primates. International Journal of Primatology, 31 (5): 833-847.
	Buckland S T, Plumptre A J, Thomas L, Rexstad E A. 2010b. Line transect sampling of primates: can animal-to-observer distance methods work? International Journal of Primatology, 31 (3): 485-499.
	Chang Z F, Liu Z J, Yang J Y, Li M, Vigilant L. 2012. Noninvasive genetic assessment of the population trend and sex ratio of the Shennongjia population of Sichuan snub‑nosed monkeys (Rhinopithecus roxellana). Chinese Science Bulletin, 57 (10): 1135-1141.
	Cheyne S M, Thompson C J H, Phillis A C, Hill R M C, Limin S H. 2008. Density and population estimate of gibbons (Hylobates albibarbis) in the Sabangau catchment, Central Kalimantan, Indonesia. Primates, 49: 50-56.
	Chapman C A. 2018. A road for a promising future for China’s primates: The potential for restoration. Zoological Research, 39 (4): 244-248.
	Danielsen F, Burgess N D, Balmford A. 2005. Monitoring matters: examining the potential of locally‑bassed approaches. Biodiversity & Conservation, 14 (11): 2507-2542.
	Estrada A, Luecke L, van Belle S, Barrueta E, Meda M R. 2004. Survey of black howler (Alouatta pigra) and spider (Ateles geoffroyi) monkeys in the Mayan sites of Calakmul and Yaxchilan, Mexico and Tikal, Guatemala. Primates, 45: 33-39.
	Estrada A, Garber P A. 2022. Principal drivers and conservation solutions to the impending primate extinction crisis: introduction to the special issue. International Journal of Primatology, 43: 1-14.
	Fan P F, He K, Chen X, Ortiz A, Zhang B, Zhao C, Li Y Q, Zhang H B, Kimock C, Wang W Z, Groves C, Turvey S T, Roos C, Helgen K M, Jiang X L. 2017. Description of a new species of Hoolock gibbon (Primates: Hylobatidae) based on integrative taxonomy. American Journal of Primatology, 79 (5): e22631.
	Fan P F, Ma C. 2018. MaExtant primates and development of primatology in China: publications, student training, and funding. Zoological Research, 39 (4): 249-254.
	Fan P F, Zhang L, Yang L, Huang X, Shi K C, Liu G Q, Wang C H. 2022. Population recovery of the critically endangered western black crested gibbon (Nomascus concolor) in Mt. Wuliang, Yunnan, China. Zoological Research, 43 (2): 180-183.
	Gestich C C, Caselli C B, Nagy‑Reis M B, Setz E Z F, da Cunha R G T. 2016. Estimating primate population densities: the systematic use of playbacks along transects in population surveys. American Journal of Primatology, 79: e22586.
	Guo S T, Xu P F, Miao Q, Shao G F, Chapman C A, Chen X J, He G, Fang D Y, Zhang H, Sun Y W, Shi Z H, Li B G. 2020. Automatic identification of individual primates with deep learning techniques. iScience, 23 (8): 101412.
	Guo Y, Grueter C C, Lu J. 2022. Allomaternal care and ‘adoption’ in an edge-of-range population of Taihangshan macaques in northern China. Current Zoology.DOI: 10.1093/ac/zoac027
	Guschanski K, Vigilant L, McNeilage A, Gray M, Kagoda E, Robbins M M. 2009. Counting elusive animals: comparing field and genetic census of the entire mountain gorilla population of Bwindi Impenetrable National Park, Uganda. Biological Conservation, 142: 290-300.
	Hanya G, Yoshihiro S, Zamma K, Kubo R, Takahata Y. 2003. New method to census primate groups: estimating group density of Japanese macaques by point census. American Journal of Primatology, 60 (2): 43-56.
	He G, Yang H T, Pan R L, Sun Y W, Zheng P B, Wang J H, Jin X L, Zhang J J, Li B G, Guo S T. 2020. Using unmanned aerial vehicles with thermal‐image acquisition cameras for animal surveys: a case study on the Sichuan snub‑nosed monkey in the Qinling Mountains. Integrative Zoology, 15 (1): 79-86.
	Hulme D, Murphree M. 2001. African Wildlife and Livelihoods: The Promise and Performance of Community Conservation . Oxford: James Currey Ltd.
	Keeping D, Burger J H, Keitsile A O, Gielend M, Mudongo E, Wallgren M, Skarpe C, Lee Footea A. 2018. Can trackers count free-ranging wildlife as effectively and efficiently as conventional aerial survey and distance sampling? Implications for citizen science in the Kalahari, Botswana Derek. Biological Conservation, 223: 156-169.
	Li B G, Li M, Li J H, Fan P F, Ni Q Y, Lu J Q, Zhou X M, Long Y C, Jiang Z G, Zhang P, Huang Z P, Huang C M, Jiang X L, Pan R L, Gouveia S, Dobrovolski R, Grueter C C, Oxnard C, Groves C, Estrada A, Garber P A. 2018. The primate extinction crisis in China: immediate challenges and a way forward. Biodiversity and Conservation, 27: 3301-3327.
	Li C, Zhao C, Fan P F. 2015. White‑cheeked macaque (Macaca leucogenys): a new macaque species from Medog, southeastern Tibet. American Journal of Primatology, 77 (7): 753-766.
	Li X Y, Bleisch W V, Jiang X L. 2018. Using large spatial scale camera trap data and hierarchical occupancy models to evaluate species richness and occupancy of rare and elusive wildlife communities in southwest China. Diversity and Distributions, 24 (11): 1560-1572.
	Liu R, Amato K, Hou R, Gomez A, Dunn D W, Zhang J, Garber P A, Chapman C A, Righini N, He G, Fang G, Li Y H, Li B G, Guo S T. 2022. Specialized digestive adaptations within the hindgut of a colobine monkey. The Innovation, 3 (2): 100207.
	Ma C, Luo Z H, Liu C M, Orkin J D, Xiao W, Fan P F. 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.
	Napier J R, Napier P H. 1994. The Natural History of the Primates. Cambridge: The MIT Press, 10.
	Nekaris K A I, Blackham G V, Nijman V. 2008. Conservation implications of low encounter rates of five nocturnal primate species (Nycticebus spp.) in Asia. Biodiversity and Conservation, 17 (4): 733-747.
	Piel A K, Cohen N, Kamenya S, Ndimuligo S A, Pintea L, Stewart F A. 2015. Population status of chimpanzees in the Masito-Ugalla Ecosystem, Tanzania. American Journal of Primatology, 77 (10): 1027-1035.
	Plumptre A J, Cox D. 2006. Counting primates for conservation: primate surveys in Uganda. Primates, 47: 65-73.
	Plumptre A J, Sterling E J, Buckland S T. 2013. Primate Census and Survey Techniques. Primate Ecology and Conservation: A Handbook of Techniques . Oxford: Oxford University Press.
	Qi X G, Garber P A, Ji W H, Huang Z P, Huang K, Zhang P, Guo S T, Wang X W, He G, Zhang P, Li B G. 2014. Satellite telemetry and social modeling offer new insights into the origin of primate multilevel societies. Nature Communications, 5: 5296.
	Strier K B. 2017. Primate Behavioral Ecology. London and New York: Routledge.
	Thomas L, Buckland S T, Rexstad E A, Laake J L, Strindberg S, Hedley S L, Bishop J R B, Marques T A, Burnham K P. 2010. Distance software: design and analysis of distance sampling surveys for estimating population size. Journal of Applied Ecology, 47 (1): 5-14.
	van Kuijk S M, García‑Suikkanen C, Tello‑Alvarado J C, Veermer J, Hill C M. 2016. Estimating population density of the san martin titi Monkey (Callicebus oenanthe) in Peru using vocalisations. Folia Primatologica, 86: 525-533.
	Xia D, Li J, Matheson M D, Sun L, Sun B, Zhou Y. 2012. First occurrence of twins in provisioned free‑ranging Tibetan macaques (Macaca thibetana) at Huangshan, China. Primates, 53: 1-5.
	Zhao X, Garber P A, Li M. 2021. Alleviating human poverty: a successful model promoting wildlife conservation in China. Conservation Science and Practice, 3 (10): e511.
	Zhou X M, Wang B S, Pan Q, Zhang J B, Kumar S, Sun X Q, Liu Z J, Pan H J, Lin Y, Liu G J, Zhan W, Li M Z, Ren B P, Ma X Y, Ruan H, Cheng C, Wang D W, Shi F L, Hui Y Y, Tao Y J, Zhang C L, Zhu P F, Xiang Z F, Jiang W K, Chang J, Wang H H, Cao Z S, Jiang Z, Li B G, Yang G, Roos C, Garber P A, Bruford M W, Li R Q, Li M. 2014. Whole‑genome sequencing of the snub‑nosed monkey provides insights into folivory and evolutionary history. Nature Genetics, 46: 1303-1310.
	王相龙, 彭东, 申剑, 张宏, 朱蒙恩, 潘炳锟, 郑红伟, 周江, 黎大勇. 2021. 雅鲁藏布江加查峡谷西藏猕猴的种群数量及保护现状研究. 普洱学院学报, 37 (6): 1-4.
	王振兴, 王爱龙, 黄恒连, 蒙育宁, 梁霁鹏, 农登攀, 蒋迎红, 李友邦. 2014. 广西崇左白头叶猴国家级自然保护区及周边区域黑叶猴种群数量与分布. 四川动物, 33 (4): 487-492.
	尹峰, 梦梦, 刘定震, 周岐海, 黄乘明. 2015. 我国非人灵长类野外生态学研究现状与展望. 林业资源管理, 4: 1-6.
	邓怀庆, 周江. 2018. 贵州野钟保护区黑叶猴种群数量、分布及夜宿洞穴调查. 兽类学报, 38 (4): 420-425.
	龙勇诚, 程斌, 谢建国, 梁霁鹏, 程远. 2016. 灵长类: 人类失联太久的表亲. 森林与人类, 7: 12-27.
	田军东. 2011. 野生太行山猕猴的种群生态和社会结构. 郑州: 郑州大学硕士学位论文.
	冉文忠. 2003. 野生白头叶猴的现状: 分布、数量、栖息地利用和种群生存力分析. 北京: 北京大学博士学位论文.
	付文, 任宝平, 林建忠, 栾科, 王朋程, 王宾, 黎大勇, 周岐海. 2021. 济源太行山猕猴种群数量和保护现状. 广西师范大学学报, 39 (1): 45-52.
	江海声, 刘振河, 袁喜才, 王韩生. 1988. 海南岛南湾半岛猕猴 (Macaca mulatta) 种群数量动态及分布. 生态学报, 1: 86-94.
	许龙, 张正旺, 丁长青. 2003. 样线法在鸟类数量调查中的运用. 生态学杂志, 22 (5): 127-130.
	李文华, 宋晴川, 黄蓉, 赵家新, 李友邦, 周岐海. 2019. 广西恩城保护区黑叶猴种群数量和保护现状. 兽类学报, 39 (6): 623-629.
	李光松, 陈奕欣, 孙文莫, 王新文, 黄志旁, 李延鹏, 向左甫, 丁伟, 肖文, 李明. 2014. 中国怒江片马地区怒江金丝猴种群动态及社会组织初探. 兽类学报, 34 (4): 323-328.
	李晟, 王大军, 肖治术, 李欣海, 王天明, 冯利民, 王云. 2014. 红外相机技术在我国野生动物研究与保护中的应用与前景. 生物多样性, 22 (6): 685-695.
	李晟, 王大军, 卜红亮, 刘小庚, 靳彤. 2016. 四川省老河沟自然保护区兽类多样性红外相机调查. 兽类学报, 36 (3): 282-291.
	李晟. 2020. 中国野生动物红外相机监测网络建设进展与展望. 生物多样性, 28 (9): 1045-1048.
	杨业勤, 雷孝平, 杨传东, 孙敦渊, 陈继顺, 何汝态, 谭长芬, 张维勇. 2001. 黔金丝猴种群数量的调查研究. 野生动物生态与管理学术讨论会.
	杨帆, 邵全琴, 郭兴健, 李愈哲, 王东亮, 张雅娴, 汪阳春, 刘纪远, 樊江文. 2018. 玛多县大型野生食草动物种群数量对草畜平衡的影响研究. 草业学报, 27 (7): 13.
	肖文宏, 胡力, 黄小群, 肖治术. 2019. 基于标记—重捕模型开展野生动物红外相机种群监测的方法及案例. 生物多样性, 27 (3): 9.
	吴飞, 杨晓君. 2008. 样点法在森林鸟类调查中的运用. 生态学杂志, 27 (12): 2240-2244.
	何丽. 2010. 川金丝猴 (Rhinopithecus roxellana) 遗传学与栖息地分析. 石河子: 石河子大学博士学位论文.
	余梁哥, 陈敏杰, 杨士剑, 李学友, 师蕾. 2013. 利用红外相机调查屏边县大围山倭蜂猴、蜂猴及同域兽类. 四川动物, 6: 814-818.
	张龙, 邓玥, 钟雪, 白文科, 周材权, 王彬. 2019. 基于红外相机技术的川金丝猴地面活动监测. 三峡生态环境监测, 4 (3): 68-73.
	陈立军, 肖文宏, 肖治术. 2019. 物种相对多度指数在红外相机数据分析中的应用及局限. 生物多样性, 27 (3): 6.
	陈华豪. 1989. 有蹄类数量调查方法的讨论. 野生动物学报, 6: 17-21.
	陈奕欣, 肖治术, 李明, 王新文, 何臣相, 李海曙, 施顺金, 向左甫. 2016. 利用红外相机对高黎贡山中段西坡兽类和鸟类多样性初步调查. 兽类学报, 36 (3): 302-312.
	赵海涛, 王程亮, 王晓卫, 李保国, 王开锋, 李庭春, 李俊峰, 高存劳. 2015. 陕西米仓山国家级自然保护区猕猴的分布及种群数量调查. 生态学报, 35 (17): 5632-5637.
	钟凌, 贾康胜, 王晓卫, 雷颖虎, 曹崇文, 王程亮, 任轶, 付卫伟, 赵海涛, 李保国. 2018. 陕西省楼观台实验林场川金丝猴的种群数量及分布. 四川动物, 37 (2): 219-223.
	施方勤. 2009. 白马雪山滇金丝猴种群数量分布调查研究. 内蒙古林业调查设计, 32 (5): 102-103.
	袁朝晖, 孙建存, 宁智刚, 时鉴. 2003. 长青保护区金丝猴种群数量与分布调查. 陕西师范大学学报 (自然科学版), S2: 173-176.
	徐会明, 和育超, 张利周, 黄志旁. 2015. 云南云龙天池自然保护区龙马山黑白仰鼻猴种群动态调查. 林业调查规划, 40 (3): 57-59.

[1]	李明文. 非人灵长类动物种质冷冻保存研究进展和展望[J]. 兽类学报, 2022, 42(6): 728-740.
[2]	路纪琪田军东. 灵长类学术语的规范化表述：以α-雄性更替为例[J]. 兽类学报, 2020, 40(1): 81-86.
[3]	赵翥陈巍汪寅. 灵长类镜像神经元系统起源及其争议研究进展[J]. 兽类学报, 2019, 39(5): 556-564.
[4]	朱遵燕黄天鹏姚辉杨万吉向左甫. 神农架川金丝猴捕食矛纹草鹛雏鸟简报[J]. 兽类学报, 2019, 39(5): 585-589.
[5]	张鹏段永江陈涛张杰. 海南南湾猴岛景区内猕猴与游客接触行为的研究[J]. 兽类学报, 2018, 38(3): 267-276.
[6]	周运辉张鹏. 近五百年来长臂猿在中国的分布变迁[J]. , 2013, 33(3): 258-266.
[7]	吴林林郭松涛齐晓光张培李保国. 非人灵长类的亲缘选择[J]. , 2013, 33(3): 267-273.
[8]	张鹏. 非人灵长类的杀婴行为及其适应意义[J]. , 2011, 31(2): 185-194.
[9]	张鹏,渡边邦夫. 饲养条件下非人灵长类的营养需求[J]. , 2010, 30(1): 87-98.
[10]	张鹏, 渡边邦夫. 日本‘猴灾’的形成与管理策略的研究进展—— 对中国的启迪[J]. , 2009, 29(1): 86-95.
[11]	赵迎春　苏彦捷. 非人灵长类动物的警报叫声[J]. , 2005, 25(1): 81-85.
[12]	李宏群　张育辉　李保国. 非人灵长类社会等级现象的研究进展[J]. , 2004, 24(1): 53-60.
[13]	Richard B.Harris, 刘永生, 蔡桂全，Bart W.O'Gara. 使用样线法进行马麝粪堆密度的测量[J]. , 1992, 12(4): 302-305.
[14]	俞发宏, 彭燕章, 叶智彰, 潘汝亮. 四种灵长类肘关节的生物力学研究[J]. , 1992, 12(2): 96-104.
[15]	马世来, 王应祥. 中国现代灵长类的分布、现状与保护[J]. , 1988, 8(4): 250-260.