Biodiversity Science ›› 2014, Vol. 22 ›› Issue (5): 630-639.doi: 10.3724/SP.J.1003.2014.00109

Special Issue: Mangrove; Marine Biodiversity Special Feature

• Orginal Article • Previous Article     Next Article

Impact of Spartina alterniflora on benthic macro-invertebrates communities on mangrove wetland in Xicungang Estuary, Guangxi

Caiyun Zhao1, Xiaoyan Liu1, Jiade Bai2, Fengchun Lü1, Junsheng Li1, *()   

  1. 1 State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing 100012
    2 Beijing Milu Ecological Research Center, Beijing 100076
  • Received:2014-06-03 Accepted:2014-09-15 Online:2014-10-09
  • Li Junsheng E-mail:lijsh@craes.org.cn

In order to assess the ecological impacts of Spartina alterniflora on mangrove ecosystems, we investigated macro-invertebrate communities in S. alterniflora wetlands and a mangrove wetland between October 2012 and September 2013, in the Xicungang estuary, Guangxi Zhuang Autonomous Region. The species composition, biomass and diversity of macro-invertebrates were compared at different times between the mangrove habitat and S. alterniflora community. Sixteen species from Arthropoda, Mollusca, Annelida, Cnidadia and Sipuncula were collected from the two habitats. Twelve species were found in mangrove wetlands whereas 10 species were found in S. alterniflora wetlands. Perhaps due to the invasion of S. alterniflora, Glauconome chinensis became the predominant species, leading to a greater macro-invertebrate biomass in S. alterniflora wetlands than in mangrove wetland. On the other hand, the Margalef, Shannon-Wiener index, Simpson and Pieous diversity indices of macro-invertebrates were lower in S. alterniflora habitat than in mangrove habitat. Two-way ANOVA was used to analyze the effect of sampling periods and habitats on the number of species, biomass and diversity indices of macro-invertebrates. Our results showed that Shannon- Wiener index and Simpson diversity indices differed between the two habitats, the Margalef and Pieous diversity indices differed among sampling periods, number of species and biomass were affected by both habitats and sampling periods. Based on multiple linear regression analyses, macro-invertebrate biomass was related to the density of S. alterniflora, and Shannon-Wiener, Simpson diversity and species richness of macro-invertebrates were all related with the height of S. alterniflora. According to our NMDS (non-metric multidimensional scaling) analysis, macro-invertebrate communities in S. alterniflora habitat mainly differed from those of mangrove habitats due to sampling periods. In conclusion, the invasion of S. alterniflora in mangrove wetlands in Xicungang estuary increased the biomass of macro-invertebrates, while decreased the diversity of them, and also changed the community structure of macro-invertebrate assemblages.

Key words: macro-invertebrates, Spartina alterniflora, community structure, biodiversity biological invasion

Fig. 1

Locations of macro-invertebrates sampling sites in Xicungang, Beihai city, Guangxi Province. S represents Spartina alterniflora community, and M represents mangrove wetland."

Table 1

Species composition of macro-invertebrates in Spartina alterniflora and mangrove in Xicungang"

门 Phyla 纲 Class 科 Family 种 Species 互花米草Spartinar alterniflora 红树林Mangrove
节肢动物门
Arthropoda
甲壳纲 Crustacea 和尚蟹科 Mictyridae 短指和尚蟹 Mictyris brevidactylus + +
沙蟹科 Ocypodidae 沙蟹 Ocypodidae, sp. + +
弧边招潮蟹 Uca arcuata - +
藤壶科 Balanuidae 藤壶 Balanus sp. - +
软体动物门
Mollusca
腹足纲 Gastropoda 汇螺科 Potamididae 汇螺 Potamididae, sp. - +
滨螺科 Littorinidae 黑口拟滨螺 Littoraia melanostoma + +
蜑螺科 Neritidae 奥莱彩螺 Clithon oualaniensis + +
双壳纲 Bivalvia 满月蛤科 Lucinidae 满月蛤 Lucinidae, sp. + -
绿螂科 Glauconcomidae 中国绿螂 Glauconome chinensis ++ +
樱蛤科 Tellinidae 透明美丽蛤 Tellina diaphana - +
多板纲 Polyplacophora 锉石鳖科 Ischnochitonidae 锉石鳖 Ischnochitonidae, sp. - +
石鱉科 Chitonidae 石鳖 Chitonidae, sp. + +
多板纲 Polyplacophora 多板 Polyplacophora, sp. + -
环节动物门 Annelida 多毛纲 Polychaeta 沙蚕科 Nereididae 沙蚕 Nereididae, sp. + -
星虫动物门 Sipuncula 方格星虫纲 Sipunculidea 方格星虫科 Sipunculidae 裸体方格星虫 Sipunculus nudus - +
腔肠动物门 Cnidaria 珊瑚纲 Anthozoa 石珊瑚目 Madreporaria 石珊瑚 Madreporaria, sp. + -

Fig. 2

Comparison of the number of macro-invertebrates (A) and biomass (B) in Spartina alterniflora community and mangrove at different sampling time"

Table 2

Biomass of macro-invertebrates in different habitats and different seasons in Xicungang"

采样时间
Time
生境
Habitat
甲壳纲
Crustacea
腹足纲
Gastropoda
双壳纲
Bivalvia
多板纲
Polyplacophora
多毛纲
Polychaeta
方格星虫纲Sipunculidea 珊瑚纲 Anthozoa 合计
Sum
2012.10 互花米草 Spartina alterniflora 0.040 0.008 3.063 0.030 0.005 0.00 0.005 3.151
红树林 Mangrove 0.094 0.037 0.057 0.00 0.00 0.00 0.00 0.188
2012.12 互花米草 Spartina alterniflora 0.002 0.00 2.997 0.00 0.00 0.00 0.00 2.999
红树林 Mangrove 0.206 0.00 0.144 0.00 0.00 0.00 0.00 0.350
2013.5 互花米草 Spartina alterniflora 0.020 0.060 0.435 0.00 0.002 0.00 0.00 0.517
红树林 Mangrove 0.008 0.006 0.00 0.00 0.00 0.00 0.00 0.014
互花米草 Spartina alterniflora 0.028 0.043 15.747 0.032 0.00 0.00 0.00 15.850
2013.9 红树林 Mangrove 0.087 0.003 0.335 0.074 0.00 0.030 0.00 0.530
合计 Sum 0.486 0.157 22.778 0.136 0.006 0.030 0.005 23.598

Fig. 3

Diversity indices of macro-invertebrates across mangrove and Spartina alterniflora in Xicungang, Beihai"

Fig. 4

Non-metric multidimensional scaling (NMDS) plots for the benthic macro-invertebrates at Xicungang marshes at different sampling time"

[1] .Burnham KP, Anderson DR (1998) Model Selection and Inference: An Information-theoretic Approach. Springer, New York.
[2] .Chen GC (陈光程), Yu D (余丹), Ye Y (叶勇), Chen B (陈彬) (2013) Impacts of mangrove vegetation on macro-benthic faunal communities. Acta Ecologica Sinica(生态学报), 33, 327-336. (in Chinese with English abstract)
[3] .Chen HL, Li B, Hu JB, Chen JK, Wu JH (2007) Effects of Spartina alterniflora invasion on benthic nematode communities in the Yangtze Estuary. Marine Ecology Progress Series, 336, 99-110.
[4] .Chen ZB, Guo L, Jin BS, Wu JH, Zheng GH (2009) Effect of the exotic plant Spartina alterniflora on macrobenthos communities in salt marshes of the Yangtze River estuary, China. Estuarine, Coastal and Shelf Science, 82, 265-272.
[5] .Chen ZY (陈中义) (2004)Ecological Impacts of the Introduced Spartina alterniflora Invasion in the Coastal Ecosystems of Chongming Dongtan, the Yangtze River Estuary (互花米草入侵国际重要湿地崇明东滩的生态后果). PhD dissertation, Fudan University. (in Chinese with English abstract)
[6] .Chen ZY (陈中义), Fu CZ (傅萃长), Wang HY (王海毅), Li B (李博), Wu JH (吴纪华), Chen JK (陈家宽) (2005) Effects of Spartina alterniflora invasions on the benthic macro-invertebrates community at Dongtan of Chongming salt marsh, the Yangtze River estuary. Wetland Science(湿地科学), 3, 1-7. (in Chinese with English abstract)
[7] .Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology, 18, 117-143.
[8] .Davis HG, Taylor CM, Civille JC, Strong DR (2004) An Allee effect at the front of a plant invasion: Spartina in a Pacific estuary. Journal of Ecology, 92, 321-327.
[9] .Dong CY (董存有) (1993) Preliminary observation on Glaucomya chinensis in Zhujiang estuary. Sichuan Journal of Zoology(四川动物), 12(2), 32-33. (in Chinese)
[10] .Gao AG (高爱根), Chen QZ (陈全震), Zeng JN (曾江宁), Liao YB (廖一波), Yang JY (杨俊毅) (2005) Macrofauna community in the mangrove area of Xiamen Island, Zhejiang. Journal of Marine Sciences(海洋学研究), 23(2), 33-40. (in Chinese with English abstract)
[11] .Gao SH (高世和), Li FX (李复雪) (1985) Community ecology of ground-dwelling macrofauna of mangrove in the Jiulongjiang estuary, Fujian. Journal of Oceanography in Taiwan Strait(台湾海峡), 4, 179-191. (in Chinese with English abstract)
[12] .Gao Y (高阳), Cai LZ (蔡立哲), Ma L (马丽), Xu HL (徐华林), Wang YJ (王勇军), Zan QJ (昝启杰) (2004) Vertical distribution of macrobenthos of Futian mangrove mudflat in Shenzhen Bay. Journal of Oceanography in Taiwan Strait(台湾海峡), 23, 76-81. (in Chinese with English abstract)
[13] .Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4, 1-9.
[14] .He MH (何明海), Cai EX (蔡尔西), Xu HZ (徐惠州), Jiang JX (江锦祥), Zheng FW (郑凤武), Li RG (李荣冠) (1993) Studies on benthic ecology in mangrove in Jiulong River estuary, Fujian. Journal of Oceanography in Taiwan Strait(台湾海峡), 12, 61-68. (in Chinese with English abstract)
[15] .Hong RB (洪荣标), Lü XM (吕小梅), Chen L (陈岚), Fang SH (方少华) (2005) Benthos on mangrove wetland and smooth cordgrass (Spartina alterniflora) wetland in Jiulongjiang estuary. Journal of Oceanography in Taiwan Strait(台湾海峡), 24, 189-194. (in Chinese with English abstract)
[16] .Hou SL (侯森林), Yu XY (余晓韵), Lu CH (鲁长虎) (2012) Effect of Spartina alterniflora invasion on the macrobenthic community in the Sheyang estuary. Transaction of Oceanology and Limnology(海洋湖沼通报), (1), 138-146. (in Chinese with English abstract)
[17] .Hu ZY (胡知渊), Bao YX (鲍毅新), Cheng HY (程宏毅), Zhang LL (张龙龙), Ge BM (葛宝明) (2009) Research progress on ecology of natural wetland zoobenthos in China. Chinese Journal of Ecology(生态学杂志), 28, 959-968. (in Chinese with English abstract)
[18] .Huang GM (黄冠闽), Zhang YH (张宜辉), Fang BZ (方柏州), Lin WS (林伟山) (2013) Effects of Spartina alterniflora on mangrove Kandelia candel seedlings regeneration. Journal of Fujian Forestry Science and Technology(福建林业科技), 40(4), 93-113. (in Chinese with English abstract)
[19] .Lana PC, Guiss C (1992) Macrofauna-plant-biomass interactions in a euhaline salt marsh in Paranagua Bay (Se Brazil). Marine Ecology Progress Series, 80, 57-64.
[20] .Levin LA, Talley TS (2000) Influences of vegetation and abiotic environmental factors on salt marsh invertebrates. In: Concepts and Controversies in Tidal Marsh Ecology (eds Weinstein MP, Kreeger DA), Kluwer, Dordrecht, pp. 661- 707. Springer, the Netherlands.
[21] .Lin XC (林秀春), Ren S (任帅), Gong Y (龚玉), Chen X (陈晓) (2010) Studies on macrobenthic community on Spartina alterniflora invaded area of Putian. Journal of Putian University(莆田高等专科学校学报), 17(2), 96-100. (in Chinese with English abstract)
[22] .Lu Q(陆强), Chen HL(陈慧丽), Shao XY(邵晓阳), Wang YY(王莹莹), Tao M(陶敏), He J(何京), Tang L(唐龙) (2013) Ecological characteristics of macrobenthic communities and its relationships with environmental factors in Hangzhou Xixi Wetland. Acta Ecologica Sinica(生态学报), 33(9), 2803-2815. (in Chinese with English abstract)Ludwig JA, Reynolds JF (1988) Statistical Ecology. John Wiley & Sons, New York.
[23] .Neira C, Levin LA, Grosholz ED, Mendoza G (2007) Influence of invasive Spartina growth stages on associated macrofaunal communities. Biological Invasions, 9, 975-993.
[24] .Netto SA, Lana PC (1997) Influence of Spartina alterniflora on superficial sediment characteristics of tidal flats in Paranagua Bay (south-eastern Brazil). Estuarine, Coastal and Shelf Science, 44, 641-648.
[25] .Pielou EC (1975) Ecological Diversity. Wiley, New York.
[26] .Posey MH, Alphin TD, Meyer DL, Johnson JM (2003) Benthic communities of common reed Phragmites australis and marsh cordgrass Spartina alterniflora marshes in Chesapeake Bay. Marine Ecology Progress Series, 261, 51-61.
[27] .Rangel TFLVB, Diniz-Filho JAF, Bini LM (2006) Towards an integrated computational tool for spatial analysis in macroecology and biogeography. Global Ecology and Biogeography, 15, 321-327.
[28] .Robertson TL, Weis JS (2005) A comparison of epifaunal communities associated with the stems of salt marsh grasses Phragmites australis and Spartina alterniflora. Wetlands, 25, 1-7.
[29] .Shen YM (沈永明), Wang YF (王艳芳), Chen SJ (陈寿军), Wu DL (吴德力), Yu WY (虞慰岩), Li ZH (李朝晖) (2013) The temporal and spatial distributions of the macrobenthos in Spartina alterniflora salt marsh. Geographical Research(地理研究), 32, 638-644. (in Chinese with English abstract)
[30] .Tan YY (覃盈盈), Liang SC (梁士楚) (2008) Current status and eradication strategy of invasive alien plants Spartina alterniflora in Guangxi. Wetland Science & Management(湿地科学与管理), 4(2), 47-50. (in Chinese with English abstract)
[31] .Wang AA (王安安), Sun X (孙雪), Cai JB (蔡景波), Chai XL (柴雪良), Liu J (刘健), Shang X (商栩) (2014) Effects of Spartina alterniflora invasions on the benthic macro-invertebrates community at mangrove wetland. Journal of Zhejiang Agricultural Sciences(浙江农业科学), (4), 572-577. (in Chinese with English abstract)
[32] .Wang RZ, Yuan L, Zhang LQ (2010) Impacts of Spartina alterniflora invasion on the benthic communities of salt marshes in the Yangtze Estuary, China. Ecological Engineering, 36, 799-806.
[33] .Wei DZ (魏德重), Xiang CY (项长友), Bao YX (鲍毅新), Li LF (李良峰), Zhang SS (章书声) (2012) Effect of mangrove planting on macrobenthic community structure and functional group. Journal of Zhejiang Normal University (Natural Sciences) (浙江师范大学学报(自然科学版)), 35, 195-202. (in Chinese with English abstract)
[34] .Wei SQ (韦受庆), Chen J (陈坚), Fan HQ (范航清) (1993) A study on the benthic macrofauna and its ecology in Shankou Mangrove Reserve area of Guangxi. Journal of the Guangxi Academy of Sciences(广西科学院学报), 9(2), 45-57. (in Chinese with English abstract)
[35] .Wu PQ (吴培强), Zhang J (张杰), Ma Y (马毅), Li XM (李晓敏) (2013) Remote sensing monitoring and analysis of the changes of mangrove in China in the past 20 years. Advances in Marine Science(海洋科学进展), 31, 406-414. (in Chinese with English abstract)
[36] .Xie WJ (谢文静), Gao S (高抒) (2009) Composition of the benthic macrofauna in the Spartina alterniflora salt marshes in the Wanggang area, central Jiangsu coast, eastern China. Journal of Nanjing University (Natural Sciences) (南京大学学报(自然科学版)), 45 , 553-561. (in Chinese with English abstract)
[37] .Xie ZF (谢志发), He WS (何文珊), Liu WL (刘文亮), Lu JJ (陆健健) (2008) Influence of Spartina alterniflora salt marsh at its different development stages on macrobenthos. Chinese Journal of Ecology(生态学杂志), 27, 63-67. (in Chinese with English abstract)
[38] .Xu XJ (徐晓军), Wang H (王华), You WH (由文辉), Liu BX (刘宝兴) (2006) A study on the fluctuation of zoobenthic community in Chongming Dongtan’s Spartina alterniflora Loisel. Transactions of Oceanology and Limnology(海洋湖沼通报), (2), 89-94. (in Chinese with English abstract)
[39] .Yu WY (虞蔚岩), Li ZH (李朝晖), Hua C (华春), Shen YM (沈永明), Ma L (马玲), Guo N (郭娜), Li ZX (李智星) (2009) The diversity analysis of macrobenthic fauna on the tidal flat with Spartina alterniflora in Dongtai, Yancheng in Jiangsu. Transactions of Oceanology and Limnology(海洋湖沼通报), (1), 123-128. (in Chinese with English abstract)
[40] .Zheng RQ (郑荣泉), Ge BM (葛宝明), Zhang YP (张永普), Zheng X (郑祥) (2006) The comparative study on the macrobenthic community ecology between the mangrove swamp and the naked tidal flat at the Yueqing Bay. Ecological Science(生态科学), 25, 299-302. (in Chinese with English abstract)
[41] .Zou FS (邹发生), Song XJ (宋晓军), Chen W (陈伟), Zheng XR (郑馨仁), Chen JH (陈建海) (1999) The diversity of benthic macrofauna on mud flat in Dongzhaigang Mangrove Reserve, Hainan. Chinese Biodiversity(生物多样性), 7, 175-180. (in Chinese with English abstract)
[42] .Zhou QQ (周青青), Chen ZL (陈志力), Xin K (辛琨) (2010) Research on the alien invasive status of mangrove in China. Journal of Anhui Agricultural Sciences(安徽农业科学), 38, 2662-2664. (in Chinese with English abstract)
[43] .Zhang JP (张景平), Huang XP (黄小平), Jiang ZJ (江志坚), Huang DJ (黄道建), Huang LM (黄良民) (2010) Assessment of the Pearl River estuary pollution by water comprehensive pollution index and biodiversity index. Journal of Tropical Oceanography(热带海洋学报), 29, 69-76. (in Chinese with English abstract)
[44] .Zhou HX (周虹霞), Liu JE (刘金娥), Qin P (钦佩) (2005) Effects of alien species (Spartina alterniflora) on soil microorganism diversity in salt marshes, Jiangsu coastal inter-tidal ecosystem. Acta Ecologica Sinica(生态学报), 25, 2304-2311. (in Chinese with English abstract)
[1] Xing Yuan, Wu Xiaoping, Ouyang Shan, Zhang Junqian, Xu Jing, Yin Senlu, Xie Zhicai. Assessment of macrobenthos biodiversity and potential human-induced stressors in the Ganjiang River system [J]. Biodiv Sci, 2019, 27(6): 648-657.
[2] Xie Fenglin, Zhou Quan, Shi Hang, Shu Xiao, Zhang Kerong, Li Tao, Feng Shuiyuan, Zhang Quanfa, Dang Haishan. Species composition and community characteristics of a 25 ha forest dynamics plot in deciduous broad-leaved forest, Qinling Mountains, north-central China [J]. Biodiv Sci, 2019, 27(4): 439-448.
[3] Yang Lufei, Chen Linlin, Li Xiaojing, Zhou Zhengquan, Liu Bo, Song Bo, Li Bingjun, Li Baoquan. Effect of seasonal hypoxia on macrobenthic communities in the Muping Marine Ranch, Yantai, China [J]. Biodiv Sci, 2019, 27(2): 200-210.
[4] Yunzhi Qin,Jiaxin Zhang,Jianming Liu,Mengting Liu,Dan Wan,Hao Wu,Yang Zhou,Hongjie Meng,Zhiqiang Xiao,Handong Huang,Yaozhan Xu,Zhijun Lu,Xiujuan Qiao,Mingxi Jiang. Community composition and spatial structure in the Badagongshan 25 ha Forest Dynamics Plot in Hunan Province [J]. Biodiv Sci, 2018, 26(9): 1016-1022.
[5] Wei Mo,Zhiliang Wang,You Li,Jianjun Guo,Runzhi Zhang. Faunal communities of deep soil layers in suburban Beijing [J]. Biodiv Sci, 2018, 26(3): 248-257.
[6] Yuhang Li, Wandong Chen, Houcai Cai, Zhongmin Sun, Kuidong Xu. Spatio-temporal variation of benthic diatom diversity and community structure in a sandy intertidal zone of the Nanji Islands, China [J]. Biodiv Sci, 2017, 25(9): 981-989.
[7] Ling-Zhao TAN, Chun-Yu FAN, Xiu-Hua FAN. Relationships between species diversity or community structure and productivity of woody-plants in a broad-leaved Korean pine forest in Jiaohe, Jilin, China [J]. Chin J Plan Ecolo, 2017, 41(11): 1149-1156.
[8] Hongying Zhou, Xuemei Yao, Li Li, Taonian Geng, Ying Zhang. Scleractinian coral community structure and distribution in the coastal waters surrounding Hainan Island [J]. Biodiv Sci, 2017, 25(10): 1123-1130.
[9] Quan FANG, Yi-Zhen LIU, Gang GE. Characteristics of plant communities containing rare conifers in Poyang Lake Basin, China [J]. Chin J Plan Ecolo, 2016, 40(9): 952-957.
[10] Hongyan Liu,Chaojie Yang,Peidong Zhang,Wentao Li,Xiaolong Yang,Xiumei Zhang. Demersal nekton community structure of artificial reef zones in Laoshan Bay, Qingdao [J]. Biodiv Sci, 2016, 24(8): 896-906.
[11] Deyi Wang,Jianfeng Hao,Yan Li,Jinqiu Qi,Zengli Pei,Yujia Huang,Qian Jiang,Ya Chen. Examination of edge effects in a Cryptomeria fortunei plantation in Zhougong Mountain, western Sichuan [J]. Biodiv Sci, 2016, 24(8): 940-947.
[12] Mei Yang,Xinzheng Li,Yong Xu,Hongfa Wang,Baolin Zhang. Seasonal variations in macrobenthic communities in the subtidal zones of Jiaozhou Bay [J]. Biodiv Sci, 2016, 24(7): 820-830.
[13] Chaofeng Wang,Haibo Li,Wuchang Zhang,Li Zhao,Yuan Zhao,Tian Xiao. Analyzing the tintinnid community structure and distribution in the surface waters southeast of Hawaii from a cruise in 2013 [J]. Biodiv Sci, 2016, 24(7): 831-837.
[14] Jun Sun,Bing Xue. Marine phytoplankton diversity and the impact of global climate change [J]. Biodiv Sci, 2016, 24(7): 739-747.
[15] Zhi-Gao WANG, Zhong-Xin ZHANG, Wen-Ge WANG, Jun CHU. Preliminary analysis of forest community structure of Yaoluoping National Nature Reserve in Yuexi County, Anhui Province, China [J]. Chin J Plan Ecolo, 2016, 40(6): 615-619.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] Qingfu Liu,Yang Liu,Xiaoli Sun,Xuefeng Zhang,Sarula Kang,Yong Ding,Qing Zhang,Jianming Niu. The explanation of climatic hypotheses to community species diversity patterns in Inner Mongolia grasslands[J]. Biodiv Sci, 2015, 23(4): 463 -470 .
[2] Yu Gao,Guanghui Lin. Algal diversity and their importance in ecological processes in typical mangrove ecosystems[J]. Biodiv Sci, 2018, 26(11): 1223 -1235 .
[3] Chunfa Zhou, Daqing Zhou, Xiangkun Kong, Wenhong Deng. Differentiating nest sites characteristics of four sympatric cavity-nesting birds[J]. Biodiv Sci, 2012, 20(6): 716 -724 .
[4] Chen Wei-Chiu. A Preliminary Study on the Genus Wendlandia in China[J]. J Syst Evol, 1983, 21(3): 277 -284 .
[5] Zhi-Cheng CHEN, Xian-Chong WAN. The relationship between the reduction of nonstructural carbohydrate induced by defoliator and the growth and mortality of trees[J]. Chin J Plan Ecolo, 2016, 40(9): 958 -968 .
[6] Ni Jian and Wu Ji-you. Prospection of Hidden Deposit Using Spectral Reflectance of Plant Leaves Surface[J]. Chin Bull Bot, 1997, 14(01): 36 -40 .
[7] MA Yang, WANG Xue-Qin, ZHANG Bo, LIU Jin-Hui, HAN Zhang-Yong, and TANG Gang-Liang. Effects of wind erosion and sand burial on water relations and photosynthesis in Alhagi sparsifolia in the southern edge of the Taklimakan Desert[J]. Chin J Plan Ecolo, 2014, 38(5): 491 -498 .
[8] . Evolution and of NCED family genes in Vitis vinifera[J]. Chin Bull Bot, 2019, 54(4): 0 .
[9] Fan Li,Huanjun Zhang,Zhenbo Lü,Bingqing Xu,Liang Zheng. Species composition and community diversity of nekton in Laizhou Bay, China[J]. Biodiv Sci, 2013, 21(5): 537 -546 .
[10] Zhi-Yong XIONG, Yong LIU, Yong-Gang HE, Yun-Chun SONG, Ke-Xiu LI and Guan-Yuan HE. Heterozygosity of Knob-Associated Tandem Repeats and Knob Instability in Mitotic Chromosomes of Zea (Zea mays L. and Z. diploperennis Iltis Doebley)[J]. J Integr Plant Biol, 2005, 47(11): 1345 -1351 .