Chin J Plan Ecolo ›› 2018, Vol. 42 ›› Issue (9): 946-954.doi: 10.17521/cjpe.2018.0066

• Review • Previous Articles     Next Articles

Modeling the potential suitable habitat of Impatiens hainanensis, a limestone-endemic plant

NING Yao1,LEI Jin-Rui2,SONG Xi-Qiang1,3,*(),HAN Shu-Mei1,3,ZHONG Yun-Fang1,*()   

  1. 1Tropical Agriculture and Forestry College, Hainan University, Haikou 570228, China
    2Forestry Institute of Hainan Province, Haikou 571100, China
    3Research Center for Terrestrial Biodiversity of the South China Sea, Hainan University, Haikou 570228, China
  • Received:2018-03-28 Revised:2018-09-11 Online:2018-09-26 Published:2018-09-20
  • Contact: Xi-Qiang SONG,Yun-Fang ZHONG E-mail:songstrong@hainu.edu.cn;zhongzyf@163.com
  • Supported by:
    Supported by the Hainan Provincial Innovative Research Team Program.(2018CXTD334);the National Natural Science Foundation of China.(31560229)

Abstract:

Aims Modelling potential distribution ranges of threatened species is of great significance for their conservation. In this paper, the distribution of potential suitable habitat of Impatiens hainanensis,a limestone-endemic and endangered plant in Hainan Island, was studied to provide scientific basis for their effective in situ conservation and re-introduction of I. hainanensis.

Methods Based on eight occurrence sites and 12 environmental variables, the Maximum Entropy (MaxEnt) algorithm and GIS technology were used to create a model linking the distribution ranges of I. hainanensis with environments. With data on five actual distribution sites and five non-occurrence sites, four model evaluation metrics (area under the receiver operating characteristic curve (AUC), kappa coefficient, true skill statistic (TSS), overall accuracy) were used to evaluate the predictive performance and accuracy of this model.

Important findings The results indicated that the indicative value of all four evaluation metrics were above 0.9, indicating that the MaxEnt model can effectively predict the potential suitable habitats of I. hainanensis.Slope, precipitation of the driest quarter and coefficients of precipitation variation were the three main environmental factors influencing the distribution of I. hainanensis. At present, the most suitable habitat includes western and southern parts of Baisha County, the central and southern parts of Changjiang County, the eastern part of the Dongfang City and northeastern Ledong County, accounting for 1.8% of land area on Hainan Island. Since the potential suitable habitat of I. hainanensis is rare and severely fragmented, the protection of this species is urgent. We suggest to collect the seeds of various geographic populations of I. hainanensis to establish a germplasm resource bank. The most suitable habitat of the species, including Tian’an Village and Jiangbian Village in Dongfang City, northeast of Ledong County (Jiaxi Reserve), should be selected as the priority places for future extensive field surveys and re-introduction.

Key words: local adaption, habitat suitability, Maximum Entropy, GIS, Hainan, endemic plant

Fig. 1

Actual geographic distribution maps of Impatiens hainanensis."

Supplement I

Basic information for the 13 Impatiens hainanensis populations investigated in the field"

地点 Sites 种群编码 Populations code 经度 Longitude 纬度 Latitude 海拔 Altitude (m)
俄贤岭
Exian Moutain
Pop1 109.094° E 19.013° N 945
Pop 2 109.098° E 19.010° N 890
Pop 3 109.097° E 19.007° N 1 000
Pop 4 109.109° E 19.104° N 490
Pop 5 109.112° E 19.013° N 1 050
王下乡
Wangxia Village
Pop6 109.117° E 19.024° N 450
Pop7 109.109° E 19.019° N 590
Pop8 109.128° E 19.018° N 350
Pop9 109.129° E 19.019° N 460
皇帝洞 Huangdidong Pop10 109.137° E 18.960° N 250
猕猴岭保护区
Mihouling Reserve
Pop11 109.065° E 18.929° N 480
Pop12 109.065° E 18.928° N 400
Pop13 109.063° E 18.927° N 340

Table 1

Data information of habitat evaluation"

变量及数据
Variable and data
代码
Code
来源
Source
原始坐标系
Original
coordinate system
昼夜温差月平均值
Mean diurnal range (Mean of monthly (max temperature - min temperature))
bio2 世界气候数据库
Worldclim
WGS84
等温性 Isothermality bio3
气温季节性变化标准偏差 Standard deviation of air temperature seasonality bio4
气温年较差 Air temperature annual range bio7
最冷季平均气温 Mean air temperature of coldest quarter bio11
年降水量 Annual precipitation bio12
降水量季节性变异系数 Coefficient of variation of precipitation seasonality bio15
最湿季降水量 Precipitation of wettest quarter bio16
最干季降水量 Precipitation of driest quarter bio17
海拔 Elevation ele 地理空间数据云
Geospatial data cloud (Computer network
information center of Chinese academy
of sciences)
WGS84
坡度 Slope slo
坡向 Aspect asp
海南凤仙花分布点 Distribution points of Impatiens hainanensis - 实地调查 Field survey WGS84
海南岛土地覆被类型图 Land cover type map of Hainan Island - 海南省林业厅 Forestry department of Hainan WGS84

Table 2

The criteria of the four evaluate indexes(area under the receiver operating characteristic curve (AUC), kappa coefficient, true skill statistic (TSS), overall accuracy)"

评估指标
Evaluate index
失败
Fail
很差
Very poor
一般
Common
较准确
Good
优秀
Excellent
本实验结果值(平均值±标准偏差)
Result value of this experiment
(mean ± SD)
AUC 0.50-0.60 0.60-0.70 0.70-0.80 0.80-0.90 0.90-1.00 0.98 ± 0.02
Kappa 0-0.40 0.40-0.55 0.55-0.70 0.70-0.85 0.85-1.00 0.96 ± 0.08
TSS 0-0.40 0.40-0.55 0.55-0.70 0.70-0.85 0.85-1.00 0.96 ± 0.08
Overall accuracy 0-0.40 0-0.55 0.55-0.70 0.70-0.85 0.85-1.00 0.98 ± 0.04

Fig. 2

The jackknife test result of environmental factor for Impatiens hainanensis. See Table 1 for the codes."

Fig. 3

The potential distribution of suitable habitat for Impatiens hainanensis in Hainan Island."

[1] Aguilar SV, Melgoza CA, Villarreal GF, Wehenkel C, Pinedo AC ( 2015). Modeling the potential distribution of Picea chihuahuana Martínez, an endangered species at the Sierra Madre Occidental, Mexico. Forests, 6, 692-707.
[2] Beaumont LJ, Hughes L, Poulsen M ( 2005). Predicting species distributions: Use of climatic parameters in BIOCLIM and its impact on predictions of species’ current and future distributions. Ecological Modelling, 186, 250-269.
doi: 10.1016/j.ecolmodel.2005.01.030
[3] Bennington CC, Mcgraw JB ( 1996). Environment-dependence of quantitative genetic parameters in Impatiens pallida. Evolution, 50, 1083-1097.
[4] Chu JM, Li YF, Zhang L, Li B, Gao MY, Tang XQ, Ni JW, Xu XQ ( 2017). Potential distribution range and conservation strategies for the endangered species Amygdalus pedunculata. Biodiversity Science, 25, 799-806.
doi: 10.17520/biods.2015218
[ 褚建民, 李毅夫, 张雷, 李斌, 高明远, 唐晓倩, 倪建伟, 许新桥 ( 2017). 濒危物种长柄扁桃的潜在分布与保护策略. 生物多样性, 25, 799-806.]
doi: 10.17520/biods.2015218
[5] Deb CR, Jamir NS, Kikon ZP ( 2017). Distribution prediction model of a rare orchid species ( Vanda bicolor Griff.) using small sample size. American Journal of Plant Sciences, 8, 1388-1398.
[6] Deng Y, Jiang ZC, Qin XM ( 2012). Water source partitioning among trees growing on carbonate rock in a subtropical region of Guangxi, China. Environmental Earth Sciences, 66, 635-640.
doi: 10.1007/s12665-011-1272-9
[7] Engler R, Guisan A, Rechsteiner L ( 2004). An improved approach for predicting the distribution of rare and endangered species from occurrence and pseudo-absence data. Journal of Applied Ecology, 41, 263-274.
doi: 10.1111/j.0021-8901.2004.00881.x
[8] Fois M, Fenu G, Lombra?a AC, Cogoni D, Bacchetta G ( 2015). A practical method to speed up the discovery of unknown populations using species distribution models. Journal for Nature Conservation, 24, 42-48.
doi: 10.1016/j.jnc.2015.02.001
[9] Francisco-Ortega J, Wang FG, Wang ZS, Xing FW, Liu H, Xu H, Xu WX, Luo YB, Song XQ, Gale S, Boufford DE, Maunder M, An SQ ( 2010). Endemic seed plant species from Hainan Island: A checklist. The Botanical Review, 76, 295-345.
doi: 10.1007/s12229-010-9054-8
[10] Gao FY ( 2012). A Study on Melica przewalskyi Population Spatial Pattern and Response to Soil Moisture in Degraded Alpine Grassland. Master degree dissertation, Northwest Normal University, Lanzhou.
[ 高福元 ( 2012). 高寒退化草地甘肃臭草种群空间分布格局对土壤水分的响应. 硕士学位论文, 西北师范大学, 兰州.]
[11] Hernandez PA, Graham CH, Master LL, Albert DL ( 2006). The effect of sample size and species characteristics on performance of different species distribution modeling methods. Ecography, 29, 773-785.
doi: 10.1111/j.0906-7590.2006.04700.x
[12] Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A ( 2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965-1978.
doi: 10.1002/(ISSN)1097-0088
[13] Hu QP, Guo ZH, Li CY, Ma L ( 2008). Advance at phenotypic plasticity in plant responses to abiotic factors. Scientia Silvae Cinicae, 44, 135-142.
doi: 10.3321/j.issn:1001-7488.2008.05.025
[ 胡启鹏, 郭志华, 李春燕, 马履 ( 2008). 植物表型可塑性对非生物环境因子的响应研究进展. 林业科学, 44, 135-142.]
doi: 10.3321/j.issn:1001-7488.2008.05.025
[14] Kumar S, Stohlgren TJ ( 2009). Maxent modeling for predicting suitable habitat for threatened and endangered tree Canacomyrica monticola in New Caledonia. Journal of Ecology & the Natural Environment, 1, 94-98.
[15] Lasky JR, Uriarte M, Muscarella R ( 2016). Synchrony, co-mpensatory dynamics, and the functional trait basis ofphonological diversity in a tropical dry forest tree co-mmunity: Effects of rainfall seasonality. EnvironmentalResearch Letters, 11, 115003. DOI: 10.1088/1748-9326/11/11/115003.
[16] Leng X, Wang ZS, An SQ, Feng J, Liu YH, Wang GM ( 2005). ISSR analysis of genetic diversity of Ilex integra, an insular endemic plant. Biodiversity Science, 13, 546-554.
doi: 10.3321/j.issn:1005-0094.2005.06.008
[ 冷欣, 王中生, 安树青, 冯珏, 刘玉虹, 王国明 ( 2005). 岛屿特有种全缘冬青遗传多样性的ISSR分析. 生物多样性, 13, 546-554.]
doi: 10.3321/j.issn:1005-0094.2005.06.008
[17] Liu QL, Li Y, Fang SZ ( 2017). Identification of potential cultivation region for Cyclocarya paliurus in China based on MaxEnt model. Journal of Nanjing Forestry University (Natural Science), 41, 25-29.
doi: 10.3969/j.issn.1000-2006.201608010
[ 刘清亮, 李垚, 方升佐 ( 2017). 基于MaxEnt模型的青钱柳潜在适宜栽培区预测. 南京林业大学学报(自然科学版), 41, 25-29.]
doi: 10.3969/j.issn.1000-2006.201608010
[18] Ma SM, Nie YB, Geng QL, Wang RX ( 2014). Impact of climate change on suitable distribution range and spatial pattern in Amygdalus mongolica. Chinese Journal of Plant Ecology, 38, 262-269.
doi: 10.3724/SP.J.1258.2014.00023
[ 马松梅, 聂迎彬, 耿庆龙, 王荣学 ( 2014). 气候变化对蒙古扁桃适宜分布范围和空间格局的影响. 植物生态学报, 38, 262-269.]
doi: 10.3724/SP.J.1258.2014.00023
[19] Majid A, Ahmad H, Saqib Z, Ali H ( 2015). Potential distribution of endemic Scutellaria chamaedrifolia geographic information system and statistical model approach. Pakistan Journal of Botany, 47, 51-56.
[20] Merow C, Smith MJ, Silander JA ( 2013). A practical guide to MaxEnt for modeling species’ distributions: What it does, and why inputs and settings matter. Ecography, 36, 1058-1069.
doi: 10.1111/j.1600-0587.2013.07872.x
[21] Nie YP, Chen HS, Wang KL ( 2011). Seasonal variation of water sources for plants growing on continuous rock outcrops in limestone area of Southwest China. Chinese Journal of Plant Ecology, 35, 1029-1037.
doi: 10.3724/SP.J.1258.2011.01029
[ 聂云鹏, 陈洪松, 王克林 ( 2011). 石灰岩地区连片出露石丛生境植物水分来源的季节性差异. 植物生态学报, 35, 1029-1037.]
doi: 10.3724/SP.J.1258.2011.01029
[22] Qin XS, He KS, Liu LW, Sun JM, Qi XM, Shi H ( 2012). Floristic and ecological characteristics of the community with Impatiens hainanensis in exianling limestone moutain, Hainan. Journal of South China Agricultural University, 33, 361-367.
doi: 10.7671/j.issn.1001-411X.2012.03.018
[ 秦新生, 何科稣, 刘立武, 孙君梅, 齐旭明, 施浩 ( 2012). 海南俄贤岭石灰岩山地海南凤仙花所在群落植物区系及生态特征. 华南农业大学学报, 33, 361-367.]
doi: 10.7671/j.issn.1001-411X.2012.03.018
[23] Qin XS, Zhang RJ, Chen HF, Wang FG, Tian HZ, Xing FW ( 2005). The resource and conservation on the rare and endangered plants in limestone regions in Hainan Island. Acta Scientiarum Naturalium Universitatis Sunyatseni (Natural Science), 44, 291-298.
doi: 10.3321/j.issn:0529-6579.2005.z1.057
[ 秦新生, 张荣京, 陈红锋, 王发国, 田怀珍, 邢福武 ( 2005). 海南岛石灰岩地区珍稀濒危植物及其保护. 中山大学学报(自然科学版), 44, 291-298.]
doi: 10.3321/j.issn:0529-6579.2005.z1.057
[24] Qin XS, Zhang RJ, Xing FW ( 2014). Flora of seed plants in the limestone areas of Hainan. Journal of South China Agricultural University, 35, 90-99.
doi: 10.7671/j.issn.1001-411x.2014.03.017
[ 秦新生, 张荣京, 邢福武 ( 2014). 海南石灰岩地区的种子植物区系. 华南农业大学学报, 35, 90-99.]
doi: 10.7671/j.issn.1001-411x.2014.03.017
[25] Rushton SP, Ormerod SJ, Kerby G ( 2004). New paradigms for modelling species distributions? Journal of Applied Ecology, 41, 193-200.
doi: 10.1111/j.0021-8901.2004.00903.x
[26] Shi W ( 2013). Effects of Climate Change on Distribution of Larix gmelinii in Northeast China. Master degree dissertation, Beijing Forestry University, Beijing.
[ 石慰 ( 2013). 气候变化对中国东北兴安落叶松分布的影响. 硕士学位论文, 北京林业大学, 北京.]
[27] Wu J, Qin F, Wang W, Chen P, Gao SH, Xu HJ, Lin Q, Zhu CQ, Yu YC ( 2010). Research progress of soil and peculiar plants in limestone areas of China. Journal of Jiangsu Forestry Science & Technology, 37, 50-54.
doi: 10.3969/j.issn.1001-7380.2010.02.015
[ 吴静, 秦飞, 王维, 陈平, 高世虎, 徐辉筠, 林琴, 朱朝芹, 俞元春 ( 2010). 我国石灰岩地区特有植物研究进展. 江苏林业科技, 37, 50-54.]
doi: 10.3969/j.issn.1001-7380.2010.02.015
[28] Wu JG, Lü JJ, Zhou QF ( 2010). Potential effects of climate change on the distribution of six desert plants in China. Chinese Bulletin of Botany, 45, 723-738.
doi: 10.3969/j.issn.1674-3466.2010.06.010
[ 吴建国, 吕佳佳, 周巧富 ( 2010). 气候变化对6种荒漠植物分布的潜在影响. 植物学通报, 45, 723-738.]
doi: 10.3969/j.issn.1674-3466.2010.06.010
[29] Xu ZL, Peng HH, Peng SZ ( 2015). The development and evaluation of species distribution models. Acta Ecologica Sinica, 35, 557-567.
doi: 10.5846/stxb201304030600
[ 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.]
doi: 10.5846/stxb201304030600
[30] Ying LX, Liu Y, Chen ST, Shen ZH ( 2016). Simulation of the potential range of Pistacia weinmannifolia in Southwest China with climate change based on the maximum-entropy (Maxent) model. Biodiversity Science, 24, 453-461.
doi: 10.17520/biods.2015246
[ 应凌霄, 刘晔, 陈绍田, 沈泽昊 ( 2016). 气候变化情景下基于最大熵模型的中国西南地区清香木潜在分布格局模拟. 生物多样性, 24, 453-461.]
doi: 10.17520/biods.2015246
[31] Yuan TX, Zhang HP, Ou ZY, Tan YB ( 2014). Effects of topography on the diversity and distribution pattern of ground plants in karst montane forests in Southwest Guangxi, China. Chinese Journal of Applied Ecology, 25, 2803-2810.
[ 袁铁象, 张合平, 欧芷阳, 谭一波 ( 2014). 地形对桂西南喀斯特山地森林地表植物多样性及分布格局的影响. 应用生态学报, 25, 2803-2810.]
[32] Zhen JH ( 2008). Landscape Dynamics and Suitability Assessment of Endangered Plant Tetraena Mongolica’s Habitats. PhD dissertation, Inner Mongolian Agricultural University, Huhhot.
doi: 10.7666/d.y1307764
[ 甄江红 ( 2008). 濒危植物四合木生境的景观动态与适宜性评价研究. 博士学位论文, 内蒙古农业大学, 呼和浩特.]
doi: 10.7666/d.y1307764
[33] Zhong YF ( 2014). Conservation Ecology of Impatiens hainanensis (Balsaminaceae), Endemic Species in Hainan Island. PhD dissertation, Hainan University, Haikou.
[ 钟云芳 ( 2014). 海南凤仙花保育生态学研究. 博士学位论文, 海南大学, 海口.]
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[1] Yang Ying-gen;Zhang Li-jun and Li yu. Studies on the Postharvest Physiology properties of Peach Fruits[J]. Chin Bull Bot, 1995, 12(04): 47 -49 .
[2] Zhou Shi-gong. Applications of Lanthanum in Botanical Research[J]. Chin Bull Bot, 1992, 9(02): 26 -29 .
[3] . [J]. Chin Bull Bot, 1996, 13(专辑): 105 .
[4] 杜维广 王彬如 谭克辉 郝迺斌. An Approach to the Breeding of Soybean with High Photosynthetic Efficiency[J]. Chin Bull Bot, 1984, 2(23): 7 -11 .
[5] ZHAO Yun-Yun ZHOU Xiao-Mei YANG Cai. Production of Hybrid F1 Between Avena magna and Avena nuda and It''s Identification[J]. Chin Bull Bot, 2003, 20(03): 302 -306 .
[6] . Professor Jiayang Li, a Plant Molecular Genetist[J]. Chin Bull Bot, 2003, 20(03): 370 -372 .
[7] . [J]. Chin Bull Bot, 1996, 13(专辑): 100 -101 .
[8] Qiong Jiang, Youning Wang, Lixiang Wang, Zhengxi Sun, Xia Li. Validation of Reference Genes for Quantitative RT-PCR Analysis in Soybean Root Tissue under Salt Stress[J]. Chin Bull Bot, 2015, 50(6): 754 -764 .
[9] MA Ke-Ming. Advances of the Study on Species Abundance Pattern[J]. Chin J Plan Ecolo, 2003, 27(3): 412 -426 .
[10] ZHANG Zhi-Meng, WAN Shu-Bo, NING Tang-Yuan, DAI Liang-Xiang. EFFECTS OF NITROGEN LEVEL ON NITROGEN METABOLISM AND CORRELATING ENZYME ACTIVITY IN PEANUT[J]. Chin J Plan Ecolo, 2008, 32(6): 1407 -1416 .