人为干扰对神农架川金丝猴连通性及遗传多样性的影响
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摘要
川金丝猴湖北种群是川金丝猴分布的最东缘,现主要分布于神农架国家公园和巴东自然保护区,其作为单独的管理单元,相对较低的遗传多样性、孤立的遗传状态和较小的种群数量,使得该种群面对环境变化脆弱性高。以神农架为研究区域,首先基于物种分布模型获得川金丝猴移动的阻力图层,利用电路理论分析适宜生境连接度;其次,设置道路和旅游两个人为干扰情景,运用最小费用距离模型与电路理论模型,分析道路和旅游活动对川金丝猴移动路径以及对不同亚群内和亚群间连通性的影响;最后,利用CDPOP软件模拟道路对川金丝猴遗传多样性的影响。结果表明:(1)神农架川金丝猴适宜生境分布较集中,生境斑块间存在多个潜在扩散区域;(2)道路改变了川金丝猴往来于南北生境间的最优路径,旅游干扰对川金丝猴移动路径无明显影响,其干扰主要在于川金丝猴对其具有回避性,回避距离为100 m;(3)道路显著降低金猴岭亚群内的连通性,并显著增加了所有亚群间的移动阻力,旅游活动对亚群内和亚群间的连通性无显著影响;(4)川金丝猴种群在150年内的遗传多样性呈下降趋势,道路的影响将加剧遗传多样性下降的程度。基于以上结果本文提出了针对性的保护建议,对于该物种的保护和其他濒危物种的类似研究具有较强的参考价值和借鉴意义。
The population of Sichuan snub-nosed monkey(Rhinopithecus roxellana) in Hubei Province occurs in the eastern most edge of species distribution; it has a small population size, genetic isolation, and low genetic diversity, which makes it more vulnerable to environmental changes. Focusing on the Shennongjia Area, we built a species distribution model to identify suitable habitat and achieve resistance surface for movement. We then used circuit theory to analyze landscape connectivity between suitable habitats. To investigate the influence of human disturbance on the moving path of the monkey and the connectivity between and within subpopulations, we combined scenario analysis, i.e., the scenario of road and tourism activity, with least cost model and circuit theory. Using the CDPOP software, we simulated the influence of road on the genetic diversity of monkey in 150 a. The suitable habitat aggregated in Shennongjia, and multiple potential dispersal areas between habitat patches were identified. The road changed the optimal route of monkey between the northern and southern suitable habitats. The tourism activity had no obvious influence on the moving path of the monkey, but resulted in a certain avoidance effect on the distribution of monkey with a distance of 100 m. The road significantly affected the connectivity within the Jinhoulin subpopulation and between all subpopulations, and the tourism activity had not significant effect on the connectivity of monkey. The genetic diversity of meta-population in 150 a exhibited a declining trend, and the roads will likely exacerbate the magnitude of the decline in genetic diversity. According to these results, we put forward some suggestions for the conservation of snub-nosed monkey. The results possess the reference value and the importance to protect this species and others.
The population of Sichuan snub-nosed monkey(Rhinopithecus roxellana) in Hubei Province occurs in the eastern most edge of species distribution; it has a small population size, genetic isolation, and low genetic diversity, which makes it more vulnerable to environmental changes. Focusing on the Shennongjia Area, we built a species distribution model to identify suitable habitat and achieve resistance surface for movement. We then used circuit theory to analyze landscape connectivity between suitable habitats. To investigate the influence of human disturbance on the moving path of the monkey and the connectivity between and within subpopulations, we combined scenario analysis, i.e., the scenario of road and tourism activity, with least cost model and circuit theory. Using the CDPOP software, we simulated the influence of road on the genetic diversity of monkey in 150 a. The suitable habitat aggregated in Shennongjia, and multiple potential dispersal areas between habitat patches were identified. The road changed the optimal route of monkey between the northern and southern suitable habitats. The tourism activity had no obvious influence on the moving path of the monkey, but resulted in a certain avoidance effect on the distribution of monkey with a distance of 100 m. The road significantly affected the connectivity within the Jinhoulin subpopulation and between all subpopulations, and the tourism activity had not significant effect on the connectivity of monkey. The genetic diversity of meta-population in 150 a exhibited a declining trend, and the roads will likely exacerbate the magnitude of the decline in genetic diversity. According to these results, we put forward some suggestions for the conservation of snub-nosed monkey. The results possess the reference value and the importance to protect this species and others.
引文
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[12] Chang Z F,Liu Z J,Yang J Y,Li M,Vigilant L.Noninvasive genetic assessment of the population trend and sex ratio of the Shennongjia population of Sichuan snub-nosed monkeys (Rhinopithecus roxellana).Chinese Science Bulletin,2012,57(10):1135- 1141.
[13] Li B G,Pan R L,Oxnard C E.Extinction of snub-nosed Monkeys in China during the past 400 years.International Journal of Primatology,2002,23(6):1227- 1244.
[14] Li M,Liu Z J,Gou J X,Ren B P,Pan R L,Su Y J,Funk S M,Wei F W.Phylogeography and population structure of the golden monkeys (Rhinopithecus roxellana):inferred from mitochondrial DNA sequences.American Journal of Primatology,2007,69(11):1195- 1209.
[15] Luo M F,Liu Z J,Pan H J,Zhao L,Li M.Historical geographic dispersal of the golden snub-nosed monkey (Rhinopithecus roxellana) and the influence of climatic oscillations.American Journal of Primatology,2012,74(2):91- 101.
[16] Pan D,Hu H X,Meng S J,Men Z M,Fu Y X,Zhang Y P.A high polymorphism level in Rhinopithecus roxellana.International Journal of Primatology,2009,30(2):337- 351.
[17] 朱兆泉.神农架自然保护区金丝猴现状及保护.野生动物,1992,(3):16- 17,19- 19.
[18] 王翠玲,臧振华,邱月,邓舒雨,冯朝阳,谢宗强,徐文婷,刘蕾,陈全胜,申国珍.湖北神农架国家级自然保护区森林和川金丝猴栖息地的保护成效.生物多样性,2017,25(5):504- 512.
[19] 向左甫,禹洋,杨鹛,杨敬元,廖明尧,李明.神农架保护区的川金丝猴旗舰物种生态旅游有利于自然保护吗?科学通报,2011,56(22):1784- 1789.
[20] 杨敬元,廖明尧,余辉亮,姚辉.神农架金丝猴保护与研究现状.世界科技研究与发展,2008,30(4):418- 421.
[21] 苏化龙,马强,林英华,陈千明,乔云高,谭明凤.湖北省巴东县小神农架地区川金丝猴的种群调查.兽类学报,2004,24(1):84- 87,70- 70.
[22] Luo Z H,Zhou S R,Yu W D,Yu H L,Yang J Y,Tian Y H,Zhao M,Wu H.Impacts of climate change on the distribution of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in Shennongjia area,China.American Journal of Primatology,2015,77(2):135- 151.
[23] Elith J,Phillips S J,Hastie T,Dudík M,Chee Y E,Yates C J.A statistical explanation of MaxEnt for ecologists.Diversity and Distributions,2011,17(1):43- 57.
[24] Khatchikian C,Sangermano F,Kendell D,Livdahl T.Evaluation of species distribution model algorithms for fine-scale container-breeding mosquito risk prediction.Medical and Veterinary Entomology,2011,25(3):268- 275.
[25] Phillips S J,Anderson R P,Schapire R E.Maximum entropy modeling of species geographic distributions.Ecological Modelling,2006,190(3/4):231- 259.
[26] Searcy C A,Shaffer H B.Do ecological niche models accurately identify climatic determinants of species ranges?The American Naturalist,2016,187(4):423- 435.
[27] Songer M,Delion M,Biggs A,Huang Q Y.Modeling impacts of climate change on Giant Panda habitat.International Journal of Ecology,2012,2012:108752.
[28] Tan C L,Guo S,Li B G.Population structure and ranging patterns of Rhinopithecus roxellana in Zhouzhi National Nature reserve,Shaanxi,China.International Journal of Primatology,2007,28(3):577- 591.
[29] McRae B H,Shah V B,Mohapatra T K.2013.Circuitscape 4 User Guide.The Nature Conservancy.[2014-03- 28].http://www.circuitscape.org.
[30] Wang F,McShea W J,Wang D J,Li S,Zhao Q,Wang H,Lu Z.Evaluating landscape options for corridor restoration between Giant Panda reserves.PLoS One,2014,9(8):e105086.
[31] 刘刚,龚明昊,官天培,谌利民,李惠鑫,张翼,周天元.生态旅游对大熊猫影响评价方法研究——以四川唐家河国家级自然保护区为例.动物学杂志,2016,51(5):724- 733.
[32] 李佳,丛静,刘晓,周芸芸,王秀磊,李广良,李迪强.基于红外相机技术调查神农架旅游公路对兽类活动的影响.生态学杂志,2015,34(8):2195- 2200.
[33] Foltête J C,Clauzel C,Vuidel G.A software tool dedicated to the modelling of landscape networks.Environmental Modelling & Software,2012,38:316- 327.
[34] Landguth E L,Cushman S A.cdpop:a spatially explicit cost distance population genetics program.Molecular Ecology Resources,2010,10(1):156- 161.
[35] 周芸芸,薛亚东,张宇,余辉亮,杨林森,蒋军,张于光.基于微卫星DNA的神农架川金丝猴遗传结构研究.生态学报,2018,38(4):1401- 1410.
[36] 梁冰,戚汉君,张树义,任宝平.笼养川金丝猴不同年龄阶段的发育特征.动物学报,2001,47(4):381- 387.
[37] Qi X G,Li B G,Ji W H.Reproductive parameters of wild female Rhinopithecus roxellana.American Journal of Primatology,2008,70(4):311- 319.
[38] 肖文,霍晟,向左甫,崔亮伟.黑白仰鼻猴种群生存力初步分析.动物学研究,2005,26(1):9- 16.
[39] Chang Z F,Luo M F,Liu Z J,Yang J Y,Xiang Z F,Li M,Vigilant L.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,2012,140(4/6):105- 114.
[40] Zhou X M,Meng X H,Liu Z J,Chang J,Wang B S,Li M Z,Wengel P O,Tian S L,Wen C L,Wang Z M,Garber P A,Pan H J,Ye X P,Xiang Z F,Bruford M W,Edwards S V,Cao Y C,Yu S C,Gao L J,Cao Z S,Liu G J,Ren B P,Shi F L,Peterfi Z,Li D Y,Li B G,Jiang Z,Li J S,Gladyshev V N,Li R Q,Li M.Population genomics reveals low genetic diversity and adaptation to hypoxia in Snub-nosed monkeys.Molecular Biology and Evolution,2016,33(10):2670- 2681.
[41] Luo M F,Pan H J,Liu Z J,Li M.Balancing selection and genetic drift at major histocompatibility complex class II genes in isolated populations of golden snub-nosed monkey (Rhinopithecus roxellana).BMC Evolutionary Biology,2012,12:207.
[42] 王鹏程,滕明君,穆俊明,胡文杰,杨敬元,晏召贵.神农架自然保护区川金丝猴退化生境特征及恢复技术.华中农业大学学报,2017,36(5):1- 9.
[43] Manel S,Holderegger R.Ten years of landscape genetics.Trends in Ecology & Evolution,2013,28(10):614- 621.
[44] Balkenhol N,Gugerli F,Cushman S A,Waits L P,Coulon A,Arntzen J W,Holderegger R,Wagner H H.Identifying future research needs in landscape genetics:where to from here?Landscape Ecology,2009,24(4):455- 463.
[2] Frantz A C,Bertouille S,Eloy M C,Licoppe A,Chaumont F,Flamand M C.Comparative landscape genetic analyses show a Belgian motorway to be a gene flow barrier for red deer (Cervus elaphus),but not wild boars (Sus scrofa).Molecular Ecology,2012,21(14):3445- 3457.
[3] Pérez-Espona S,McLeod J E,Franks N R.Landscape genetics of a top neotropical predator.Molecular Ecology,2012,21(24):5969- 5985.
[4] Manel S,Schwartz M K,Luikart G,Taberlet P.Landscape genetics:combining landscape ecology and population genetics.Trends in Ecology & Evolution,2003,18(4):189- 197.
[5] Holderegger R,Wagner H H.A brief guide to landscape genetics.Landscape Ecology,2006,21(6):793- 796.
[6] Storfer A,Murphy M A,Evans J S,Goldberg C S,Robinson S,Spear S F,Dezzani R,Delmelle E,Vierling L,Waits L P.Putting the ‘landscape’ in landscape genetics.Heredity,2007,98(3):128- 142.
[7] Balkenhol N,Cushman S A,Storfer A T,Waits L P.Landscape Genetics:Concepts,Methods,Applications.Chichester,UK:Wiley-Blackwell,2015.
[8] Holderegger R,Wagner H H.Landscape genetics.Bioscience,2008,58(3):199- 207.
[9] Blair M E,Melnick D J.Scale-dependent effects of a heterogeneous landscape on genetic differentiation in the Central American Squirrel Monkey (Saimiri oerstedii).PLoS One,2012,7(8):e43027.
[10] Li Y M.The effect of forest clear-cutting on habitat use in Sichuan snub-nosed monkey (Rhinopithecus roxellana) in Shennongjia Nature Reserve,China.Primates,2004,45(1):69- 72.
[11] Long Y,Richardson.Rhinopithecus roxellana.The IUCN Red List of Threatened Species (2008):e.T19596A8985735.DOI:10.2305/IUCN.UK.2008.RLTS.T39830A10273894.en.[2017-08-08].http://www.iucnredlist.org/details/19596/0.
[12] Chang Z F,Liu Z J,Yang J Y,Li M,Vigilant L.Noninvasive genetic assessment of the population trend and sex ratio of the Shennongjia population of Sichuan snub-nosed monkeys (Rhinopithecus roxellana).Chinese Science Bulletin,2012,57(10):1135- 1141.
[13] Li B G,Pan R L,Oxnard C E.Extinction of snub-nosed Monkeys in China during the past 400 years.International Journal of Primatology,2002,23(6):1227- 1244.
[14] Li M,Liu Z J,Gou J X,Ren B P,Pan R L,Su Y J,Funk S M,Wei F W.Phylogeography and population structure of the golden monkeys (Rhinopithecus roxellana):inferred from mitochondrial DNA sequences.American Journal of Primatology,2007,69(11):1195- 1209.
[15] Luo M F,Liu Z J,Pan H J,Zhao L,Li M.Historical geographic dispersal of the golden snub-nosed monkey (Rhinopithecus roxellana) and the influence of climatic oscillations.American Journal of Primatology,2012,74(2):91- 101.
[16] Pan D,Hu H X,Meng S J,Men Z M,Fu Y X,Zhang Y P.A high polymorphism level in Rhinopithecus roxellana.International Journal of Primatology,2009,30(2):337- 351.
[17] 朱兆泉.神农架自然保护区金丝猴现状及保护.野生动物,1992,(3):16- 17,19- 19.
[18] 王翠玲,臧振华,邱月,邓舒雨,冯朝阳,谢宗强,徐文婷,刘蕾,陈全胜,申国珍.湖北神农架国家级自然保护区森林和川金丝猴栖息地的保护成效.生物多样性,2017,25(5):504- 512.
[19] 向左甫,禹洋,杨鹛,杨敬元,廖明尧,李明.神农架保护区的川金丝猴旗舰物种生态旅游有利于自然保护吗?科学通报,2011,56(22):1784- 1789.
[20] 杨敬元,廖明尧,余辉亮,姚辉.神农架金丝猴保护与研究现状.世界科技研究与发展,2008,30(4):418- 421.
[21] 苏化龙,马强,林英华,陈千明,乔云高,谭明凤.湖北省巴东县小神农架地区川金丝猴的种群调查.兽类学报,2004,24(1):84- 87,70- 70.
[22] Luo Z H,Zhou S R,Yu W D,Yu H L,Yang J Y,Tian Y H,Zhao M,Wu H.Impacts of climate change on the distribution of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in Shennongjia area,China.American Journal of Primatology,2015,77(2):135- 151.
[23] Elith J,Phillips S J,Hastie T,Dudík M,Chee Y E,Yates C J.A statistical explanation of MaxEnt for ecologists.Diversity and Distributions,2011,17(1):43- 57.
[24] Khatchikian C,Sangermano F,Kendell D,Livdahl T.Evaluation of species distribution model algorithms for fine-scale container-breeding mosquito risk prediction.Medical and Veterinary Entomology,2011,25(3):268- 275.
[25] Phillips S J,Anderson R P,Schapire R E.Maximum entropy modeling of species geographic distributions.Ecological Modelling,2006,190(3/4):231- 259.
[26] Searcy C A,Shaffer H B.Do ecological niche models accurately identify climatic determinants of species ranges?The American Naturalist,2016,187(4):423- 435.
[27] Songer M,Delion M,Biggs A,Huang Q Y.Modeling impacts of climate change on Giant Panda habitat.International Journal of Ecology,2012,2012:108752.
[28] Tan C L,Guo S,Li B G.Population structure and ranging patterns of Rhinopithecus roxellana in Zhouzhi National Nature reserve,Shaanxi,China.International Journal of Primatology,2007,28(3):577- 591.
[29] McRae B H,Shah V B,Mohapatra T K.2013.Circuitscape 4 User Guide.The Nature Conservancy.[2014-03- 28].http://www.circuitscape.org.
[30] Wang F,McShea W J,Wang D J,Li S,Zhao Q,Wang H,Lu Z.Evaluating landscape options for corridor restoration between Giant Panda reserves.PLoS One,2014,9(8):e105086.
[31] 刘刚,龚明昊,官天培,谌利民,李惠鑫,张翼,周天元.生态旅游对大熊猫影响评价方法研究——以四川唐家河国家级自然保护区为例.动物学杂志,2016,51(5):724- 733.
[32] 李佳,丛静,刘晓,周芸芸,王秀磊,李广良,李迪强.基于红外相机技术调查神农架旅游公路对兽类活动的影响.生态学杂志,2015,34(8):2195- 2200.
[33] Foltête J C,Clauzel C,Vuidel G.A software tool dedicated to the modelling of landscape networks.Environmental Modelling & Software,2012,38:316- 327.
[34] Landguth E L,Cushman S A.cdpop:a spatially explicit cost distance population genetics program.Molecular Ecology Resources,2010,10(1):156- 161.
[35] 周芸芸,薛亚东,张宇,余辉亮,杨林森,蒋军,张于光.基于微卫星DNA的神农架川金丝猴遗传结构研究.生态学报,2018,38(4):1401- 1410.
[36] 梁冰,戚汉君,张树义,任宝平.笼养川金丝猴不同年龄阶段的发育特征.动物学报,2001,47(4):381- 387.
[37] Qi X G,Li B G,Ji W H.Reproductive parameters of wild female Rhinopithecus roxellana.American Journal of Primatology,2008,70(4):311- 319.
[38] 肖文,霍晟,向左甫,崔亮伟.黑白仰鼻猴种群生存力初步分析.动物学研究,2005,26(1):9- 16.
[39] Chang Z F,Luo M F,Liu Z J,Yang J Y,Xiang Z F,Li M,Vigilant L.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,2012,140(4/6):105- 114.
[40] Zhou X M,Meng X H,Liu Z J,Chang J,Wang B S,Li M Z,Wengel P O,Tian S L,Wen C L,Wang Z M,Garber P A,Pan H J,Ye X P,Xiang Z F,Bruford M W,Edwards S V,Cao Y C,Yu S C,Gao L J,Cao Z S,Liu G J,Ren B P,Shi F L,Peterfi Z,Li D Y,Li B G,Jiang Z,Li J S,Gladyshev V N,Li R Q,Li M.Population genomics reveals low genetic diversity and adaptation to hypoxia in Snub-nosed monkeys.Molecular Biology and Evolution,2016,33(10):2670- 2681.
[41] Luo M F,Pan H J,Liu Z J,Li M.Balancing selection and genetic drift at major histocompatibility complex class II genes in isolated populations of golden snub-nosed monkey (Rhinopithecus roxellana).BMC Evolutionary Biology,2012,12:207.
[42] 王鹏程,滕明君,穆俊明,胡文杰,杨敬元,晏召贵.神农架自然保护区川金丝猴退化生境特征及恢复技术.华中农业大学学报,2017,36(5):1- 9.
[43] Manel S,Holderegger R.Ten years of landscape genetics.Trends in Ecology & Evolution,2013,28(10):614- 621.
[44] Balkenhol N,Gugerli F,Cushman S A,Waits L P,Coulon A,Arntzen J W,Holderegger R,Wagner H H.Identifying future research needs in landscape genetics:where to from here?Landscape Ecology,2009,24(4):455- 463.