Biodiversity Science ›› 2020, Vol. 28 ›› Issue (1): 99-106.doi: 10.17520/biods.2019158

• Editorial • Previous Article    

Incorporating species distribution model into the red list assessment and conservation of macrofungi: A case study with Ophiocordyceps sinensis

Yi Li1, 2, Zhiyao Tang3, Yujing Yan3, 4, Ke Wang2, 5, Lei Cai2, Jinsheng He3, Song Gu6, Yijian Yao2, *()   

  1. 1. College of Food Science and Engineering, Yangzhou University, Yangzhou, Jiangsu 225127
    2. State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101
    3. College of Urban and Environmental Sciences, Peking University, Beijing 100871
    4. Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark, University of Copenhagen, Denmark
    5. University of Chinese Academy of Sciences, Beijing 100049
  • Received:2019-05-08 Accepted:2019-08-01 Online:2019-12-24
  • Yijian Yao

China is rich in macrofungal biodiversity. However, many species have been threatened in recent years by human activity and climate change. Red list assessment is the first step towards species conservation. To protect this group of fungi, the Ministry of Ecology and Environment of the People’s Republic of China and the Chinese Academy of Sciences launched the Red List Assessment of Macrofungi in China in 2016. A reasonable assessment largely relies on the sufficient information of species’ geographic information, population numbers and sizes and population dynamics, which is lacked in most of macrofungal species. It is therefore necessary to employ new approaches to find and utilize more information for the assessment. Among the assessed species, Ophiocordyceps sinensis, which is an edible and medicinal fungus endemic to the Tibetan Plateau and its surrounding regions, has relatively abundant information. This species gained attention worldwide due to its obvious economic value and its importance to local societies. A species distribution modeling has also been an important component of its red list assessment. Here, we call on a previous study that aimed to predict the current potential distribution and to project the future distribution of Ophiocordyceps sinensis, and then we discuss how this modeling method can be employed in red list assessments to predict the current potential distribution and the range shifts of other macrofungal species in response to climate change. Challenges of using the model and possible solutions are also discussed. The species distribution modeling method is considered to have great potential for red list assessments and the subsequent conservation of macrofungi.

Key words: species distribution models, Ophiocordyceps sinensis, fungal conservation, biodiversity

Table 1

Assessment information of Ophiocordyceps sinensis"

分类地位 Taxonomy
界 Kingdom 门 Phylum 纲 Class 目 Order 科 Family
真菌界 Fungi 子囊菌门 Ascomycota 座囊菌纲 Sordariomycetes 肉座菌目 Hypocreales 线虫草科 Ophiocordycipitaceae
学名 Scientific name Ophiocordyceps sinensis
中文名 Chinese name 冬虫夏草
命名人 Species authority (Berk.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora
分类备注 Taxonomic notes Cordyceps sinensis (Berk.) Sacc.
Sphaeria sinensis Berk.
无性型名称 Hirsutella sinensis X.J. Liu, Y.L. Guo, Y.X. Yu & W. Zeng
anamorph: Hirsutella sinensis X.J. Liu, Y.L. Guo, Y.X. Yu & W. Zeng
评估信息 Assessment information
Red list category & criteria
易危 Vulnerable (VU), A2acd + 3cd
评估年份 Year published 2016
评估日期 Date assessed 2016/9/27
评定人 Assessor(s) 庄文颖, 李熠 Wen-Ying Zhuang, Yi Li
审定人 Reviewer(s) 吴兴亮, 李春如 Xing-Liang Wu, Chun-Ru Li
描述 Justification 相对于其他虫草类真菌, 冬虫夏草分布范围较广、种群密度和生物量更高, 由于受到人类过度采挖的影响, 其种群密度明显下降, 气候变化也影响了其分布范围。根据模型预测的结果, 气候变化导致的冬虫夏草分布区的丧失在未来的三、五十年内可能达到30%以上。
Ophiocordyceps sinensis has a wider distribution, higher population density and biomass comparing with other Cordyceps s. l. species. The population density was observed to decline due to over-harvesting, and its distribution was also reported to be affected by climate change. According to a study with species distribution modeling, over 30% of its current habitats will be lost in the next 30 to 50 years in response to future climate change.
地理分布 Geographic range
分布区 Range description 甘肃、青海、四川、云南、西藏 Gansu, Qinghai, Sichuan, Yunnan, Tibet
分布国家 Countries occurrence 中国、尼泊尔、印度、不丹 China, Nepal, India, Bhutan
分布图 Range map
种群 Population
种群数量 Population size
种群趋势 Current population trend 衰退 Decreasing
附件信息 Additional data
生境 Habitat
生境 Habitat 高寒草甸、高山灌丛 Alpine meadow, alpine shrub
生态系统 Ecosystems
世代年限 Generation length (years)
商业用途 Use and trade
商业用途 Use and trade 珍稀食药用菌 A precious edible and medicinal fungus
威胁因子 Threats
主要威胁因子 Major threat (s) 气候变化、过度采挖 Climate change and over harvesting
保护行动 Conservation actions
保护行动 Conservation actions 该物种1999年被原林业部和农业部列为国家二级保护物种, 其分布地部分被保护区覆盖。建议对物种的种群动态进行监测, 选择合适的地点建立保护地, 采取必要的保护措施, 尤其是防止过度采挖利用, 减少采挖活动对其生境的影响。
Ophiocordyceps sinensis has been listed as endangered species under the Chinese Second Class of State Protection by the State Forestry Administration and Ministry of Agriculture since 1999. Part of its distribution areas is now covered by nature reserves. Suggested conservation actions include monitoring the bacterial population dynamics, selecting suitable distribution sites as natural reserves, developing essential protection measures to reduce the influence of collecting activity to its natural habitats, especially to prevent over-harvesting.
[1] Aggarwal CC (2013) Outlier Analysis. Springer, New York.
[2] Allouche O, Tsoar A, Kadmon R (2006) Assessing the accuracy of species distribution models: Prevalence, kappa and the true skill statistic (TSS). Journal of Applied Ecology, 43, 1223-1232.
[3] Araújo MB, Guisan A (2006) Five (or so) challenges for species distribution modelling. Journal of Biogeography, 33, 1677-1688.
[4] Araújo MB, New M (2007) Ensemble forecasting of species distributions. Trends in Ecology and Evolution, 22, 42-47.
[5] Barrows CW, Rotenberry JT, Allen MF (2010) Assessing sensitivity to climate change and drought variability of a sand dune endemic lizard. Biological Conservation, 143, 731-736.
[6] Cannon PF (2011) The caterpillar fungus, a flagship species for conservation of fungi. Fungal Conservation, 1, 35-39.
[7] Cannon PF, Hywel-Jones NL, Maczey N, Norbu L, Tshitila , Samdup T, Lhendup P (2009) Steps towards sustainable harvest of Ophiocordyceps sinensis in Bhutan. Biodiversity and Conservation, 18, 2263-2281.
[8] Cui SP, Luo X, Li CW, Hu HJ, Jiang ZG (2018) Predicting the potential distribution of white-lipped deer using the MaxEnt model. Biodiversity Science, 26, 171-176. (in Chinese with English abstract)
[ 崔绍朋, 罗晓, 李春旺, 胡慧建, 蒋志刚 (2018) 基于MaxEnt模型预测白唇鹿的潜在分布区. 生物多样性, 26, 171-176.]
[9] Foody GM (2011) Impacts of imperfect reference data on the apparent accuracy of species presence-absence models and their predictions. Global Ecology and Biogeography, 20, 498-508.
[10] Guisan A, Tingley R, Baumgartner JB, Naujokaitis-Lewis I, Sutcliffe PR, Tulloch AI, Regan TJ, Brotons L, McDonald-Madden E, Mantyka-Pringle C, Martin TG, Rhodes JR, Maggini R, Setterfield SA, Elith J, Schwartz MW, Wintle BA, Broennimann O, Austin M, Ferrier S, Kearney MR, Possingham HP, Buckley YM (2013) Predicting species distributions for conservation decisions. Ecology Letters, 16, 1424-1435.
[11] Guo YL, Li X, Zhao ZF, Wei HY, Gao B, Gu W (2017) Prediction of the potential geographic distribution of the ectomycorrhizal mushroom Tricholoma matsutake under multiple climate change scenarios. Scientific Reports, 7, 46221.
[12] Guo YL, Li X, Zhao ZF, Nawaz Z (2019) Predicting the impacts of climate change, soils and vegetation types on the geographic distribution of Polyporus umbellatus in China. Science of the Total Environment, 648, 1-11.
[13] Hanley JA, McNeil BJ (1982) The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology, 143, 29-36.
[14] Hao JJ, Cheng Z, Liang HH, Yang XL, Li S, Zhou TS, Zhang WJ, Chen JK (2009) Genetic differentiation and distributing pattern of Cordyceps sinensis in China revealed by rDNA ITS sequences. Chinese Traditional and Herbal Drugs, 40, 112-116. (in Chinese with English abstract)
[ 郝剑瑾, 程舟, 梁洪卉, 杨晓伶, 李珊, 周铜水, 张文驹, 陈家宽 ( 2009) 基于rDNA ITS序列探讨我国冬虫夏草的遗传分化及分布格局. 中草药, 40, 112-116.]
[15] Hopping KA, Chignell SM, Lambin EF ( 2018) The demise of caterpillar fungus in the Himalayan region due to climate change and overharvesting. Proceedings of the National Academy of Sciences, USA, 115, 11489-11494.
[16] Kindt R (2018) Ensemble species distribution modelling with transformed suitability values. Environmental Modelling & Software, 100, 136-145.
[17] Li C, Liu XA, Wang J, Peng PH, Shao HY, Xian W ( 2018) Potential distribution and habitat suitability assessment of Taxus chinensis based on MaxEnt in Sichuan Province. Forest Inventory and Planning, 43(1), 22-29. (in Chinese with English abstract)
[ 李灿, 刘贤安, 王娟, 彭培好, 邵怀勇, 仙巍 ( 2018) 基于MaxEnt模型的四川省红豆杉潜在分布区分析及适宜性评价. 林业调查规划, 43(1), 22-29.]
[18] Li GQ, Liu CC, Liu YG, Yang J, Zhang XS, Guo K ( 2013) Advances in theoretical issues of species distribution models. Acta Ecologica Sinica, 33, 4827-4835. (in Chinese with English abstract)
[ 李国庆, 刘长成, 刘玉国, 杨军, 张新时, 郭柯 ( 2013) 物种分布模型理论研究进展. 生态学报, 33, 4827-4835.]
[19] Li Y, Wang XL, Jiao L, Jiang Y, Li H, Jiang SP, Lhosumtseiring N, Fu SZ, Dong CH, Zhan Y, Yao YJ ( 2011) A survey of the geographic distribution of Ophiocordyceps sinensis. The Journal of Microbiology, 49, 913-919.
[20] Li Y, Liu DM, Wang K, Wu HJ, Cai L, Cai L, Li JS, Yao YJ ( 2020) Red list assessment of macrofungi in China: Challenges and measures. Biodiversity Science, 28, 66-73. (in Chinese with English abstract)
[ 李熠, 刘冬梅, 王科, 吴海军, 蔡蕾, 蔡磊, 李俊生, 姚一建 ( 2020) 中国大型真菌红色名录评估中存在的问题及今后的对策. 生物多样性, 28, 66-73.]
[21] Liu C, White M, Newell G ( 2018) Detecting outliers in species distribution data. Journal of Biogeography, 45, 164-176.
[22] Liu MM, Xing YM, Guo SX ( 2015) Habitat suitability assessment of medicinal Polyporus umbellatus in China based on MaxEnt modeling. China Journal of Chinese Meteria Medica, 40, 2792-2795. (in Chinese with English abstract)
[ 刘蒙蒙, 邢咏梅, 郭顺星 ( 2015) 基于MaxEnt生态位模型预测药用真菌猪苓在中国潜在适生区. 中国中药杂志, 40, 2792-2795.]
[23] Liu YP, Yu DY, Xun B, Sun Y, Hao RF ( 2014) The potential effects of climate change on the distribution and productivity of Cunninghamia lanceolata in China. Environmental Monitoring and Assessment, 186, 135-149.
[24] Luo ZH, Zhou SR, Yu WD, Yu HL, Yang JY, Tian YH, Zhao M, Wu H ( 2015) Impacts of climate change on the distribution of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in Shennongjia area, China. American Journal of Primatology, 77, 135-151.
[25] Marmion M, Parviainen M, Luoto M, Heikkinen RK, Thuiller W ( 2009) Evaluation of consensus methods in predictive species distribution modelling. Diversity and Distributions, 15, 59-69.
[26] Morán-Ordóñez A, Lahoz-Monfort JJ, Elith J, Wintle BA ( 2017) Evaluating 318 continental-scale species distribution models over a 60-year prediction horizon: What factors influence the reliability of predictions? Global Ecology and Biogeography, 26, 371-384.
[27] Negi CS, Koranga PR, Ghinga HS ( 2006) Yar tsa Gumba (Cordyceps sinensis): A call for its sustainable exploitation. International Journal of Sustainable Development & World Ecology, 13, 165-172.
[28] Pineda E, Lobo JM ( 2009) Assessing the accuracy of species distribution models to predict amphibian species richness patterns. Journal of Animal Ecology, 78, 182-190.
[29] Sharma S ( 2004) Trade of Cordyceps sinensis from high altitudes of the Indian Himalaya: Conservation and biotechnological priorities. Current Science, 86, 1614-1619.
[30] Shrestha UB, Bawa KS ( 2014) Impact of climate change on potential distribution of Chinese caterpillar fungus (Ophiocordyceps sinensis) in Nepal Himalaya. PLoS ONE, 9, e106405.
[31] Su F, Duan X, Chen D, Hao Z, Cuo L ( 2013) Evaluation of the global climate models in the CMIP5 over the Tibetan Plateau. Journal of Climate, 26, 3187-3208.
[32] Wang XL, Yao YJ ( 2011) Host insect species of Ophiocordyceps sinensis: A review. ZooKeys, 127, 43-59.
[33] Winkler D ( 2008) Yartsa Gunbu (Cordyceps sinensis) and the fungal commodification of Tibet’s rural economy. Economic Botany, 62, 291-306.
[34] Xu ZL, Peng HH, Peng SZ ( 2015) The development and evaluation of species distribution models. Acta Ecologica Sinica, 35, 557-567. (in Chinese with English abstract)
[ 许仲林, 彭焕华, 彭守璋 ( 2015) 物种分布模型的发展及评价方法. 生态学报, 35, 557-567.]
[35] Yan YJ, Li Y, Wang WJ, He JS, Yang RH, Wu HJ, Wang XL, Jiao L, Tang ZY, Yao YJ ( 2017) Range shifts in response to climate change of Ophiocordyceps sinensis, a fungus endemic to the Tibetan Plateau. Biological Conservation, 206, 143-150.
[36] Yao YJ, Wei JC, Zhuang WY, Cai L, Liu DM, Li JS, Wei TZ, Li Y, Wang K, Wu HJ ( 2020) Development of red list assessment of macrofungi in China. Biodiversity Science, 28, 4-10. (in Chinese with English abstract)
[ 姚一建, 魏江春, 庄文颖, 蔡蕾, 刘冬梅, 李俊生, 魏铁铮, 李熠, 王科, 吴海军 ( 2020) 中国大型真菌红色名录评估研究进展. 生物多样性, 28, 4-10.]
[37] Zhang XF, Wang D, Wang KX ( 1994) VORTEX model and its application on the management of Chinese river dolphin (Lipotes vexillifer) population. Chinese Biodiversity, 2, 133-139. (in Chinese with English abstract)
[ 张先锋, 王丁, 王克雄 ( 1994) 游涡模型及其在白暨豚种群管理中的应用. 生物多样性, 2, 133-139.]
[38] Zhang YJ, Li EW, Wang CS, Li YL, Liu XZ ( 2012) Ophiocordyceps sinensis, the flagship fungus of China: Terminology, life strategy and ecology. Mycology, 3, 2-10.
[1] Lintao Huang Hui Huang Lei Jiang. (2020) A revised taxonomy for Chinese hermatypic corals . Biodiv Sci, 28(4): 515-523.
[2] Xiongwei Yang,Ankang Wu,Qixian Zou,Guangrong Li,Mingming Zhang,Canshi Hu,Haijun Su. (2020) Field monitoring of mammals and birds using infrared cameras in Mayanghe National Nature Reserve, Guizhou, China . Biodiv Sci, 28(2): 219-225.
[3] Haiou Liu,Fengchun Zhang,Fuwei Zhao,Leshan Du,Dayuan Xue. (2020) Biodiversity sensitive issues from changes in the strategic objectives of the financial mechanism for the Convention on Biological Diversity . Biodiv Sci, 28(2): 244-252.
[4] Yisheng Ma,Qingqing Ma,Nianjun He,Dapeng Zhu,Kaihui Zhao,Hongcai Liu,Shuai Li,Liang Sun,Liubin Tang. (2020) Camera-trapping survey of mammals and birds in the Foping National Nature Reserve, China . Biodiv Sci, 28(2): 226-230.
[5] Kai Wang,Jinlong Ren,Hongman Chen,Zhitong Lyu,Xianguang Guo,Ke Jiang,Jinmin Chen,Jiatang Li,Peng Guo,Yingyong Wang,Jing Che. (2020) The updated checklists of amphibians and reptiles of China . Biodiv Sci, 28(2): 189-218.
[6] Yi Li,Dongmei Liu,Ke Wang,Haijun Wu,Lei Cai,Lei Cai,Junsheng Li,Yijian Yao. (2020) Red list assessment of macrofungi in China: Challenges and measures . Biodiv Sci, 28(1): 66-73.
[7] WANG Yu-Bing,SUN Yi-Han,DING Wei,ZHANG En-Tao,LI Wen-Huai,CHI Yong-Gang,ZHENG Shu-Xia. (2020) Effects and pathways of long-term nitrogen addition on plant diversity and primary productivity in a typical steppe . Chin J Plant Ecol, 44(1): 22-32.
[8] Wenying Zhuang,Yi Li,Huandi Zheng,Zhaoqing Zeng,Xincun Wang. (2020) Threat status of non-lichenized macro-ascomycetes in China and its threatening factors . Biodiv Sci, 28(1): 26-40.
[9] Shun Li,Liang Zou,Yinan Gong,Haitao Yang,Tianming Wang,Limin Feng,Jianping Ge. (2019) Advances in LiDAR technology in the field of animal ecology . Biodiv Sci, 27(9): 1021-1031.
[10] Xiaoyun Shi,Xiaogang Shi,Qiang Hu,Tianpei Guan,Qiang Fu,Jian Zhang,Meng Yao,Sheng Li. (2019) Evaluating the potential habitat overlap and predation risk between snow leopards and free-range yaks in the Qionglai Mountains, Sichuan . Biodiv Sci, 27(9): 951-959.
[11] Rui Yang,Qinyi Peng,Yue Cao,Le Zhong,Shuyu Hou,Zhicong Zhao,Cheng Huang. (2019) Transformative changes and paths toward biodiversity conservation in China . Biodiv Sci, 27(9): 1032-1040.
[12] Yongmin Li,Xiaobing Wu. (2019) A revised species list of amphibians and reptiles in the Anhui Province . Biodiv Sci, 27(9): 1002-1011.
[13] Junning Li, Tong Li, Yulian Wei. (2019) Relationship between diversity of wood-decaying fungi and their host wood in the Fenglin National Nature Reserve . Biodiv Sci, 27(8): 880-886.
[14] Yang Yunhui, Bai Keyu, Jarvis Devra, Long Chunlin. (2019) Xishuangbanna cucumber landraces and associated traditional knowledge . Biodiv Sci, 27(7): 743-748.
[15] Sun Beibei, Yu Cungen, Liu Hui, Yan Wenchao, Zhang Wenjun, Dai Dongxu. (2019) Spring and autumn shrimp and crab biodiversity in the east Nanji Islands . Biodiv Sci, 27(7): 787-795.
Full text