Biodiversity Science ›› 2019, Vol. 27 ›› Issue (3): 314-326.doi: 10.17520/biods.2018339

• Original Papers • Previous Article     Next Article

Structural features of root-associated fungus-plant interaction networks in the tropical montane rain forest of Jianfengling, China

Yang Siqi1, Zhang Qi1, Song Xiqiang1, Wang Jian1, Li Yide2, Xu Han2, Guo Shouyu3, Ding Qiong1, *()   

  1. 1 Research Center for Terrestrial Biodiversity of the South China Sea, Institute of Tropical Agriculture and Forestry, Hainan University, Haikou 570228
    2 Research Institute of Tropical Forestry, Chinese Academy of Forestry, Guangzhou 510520
    3 State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101
  • Received:2018-12-25 Accepted:2019-02-27 Online:2019-04-09
  • Ding Qiong E-mail:dingqiong@hainu.edu.cn

Functionally diverse root-associated fungi may differentially interact with host plants, potentially affecting the assembly processes of belowground plant and fungi communities. Here, we applied the Illumina Miseq sequencing technique to identify root-associated fungi of plants which were co-dominant in a tropical montane rain forest on Hainan Island, China. Structural features of bipartite networks were compared among the whole root-associated, arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) fungus-plant interactions. A total of 297,831 fungal ITS1 sequences were obtained from eight families including Aceraceae, Annonaceae, Apocynaceae, Aquifoliaceae, Arecaceae, Fagaceae, Lauraceae, and Oleaceae. Fungal sequences were assigned to 1,279 OTUs comprised of Ascomycota (748 OTUs), Basidiomycota (354), Glomeromycota (80), and unidentified fungi (97). At least three functional groups of fungi i.e. putatively ECM (40 OTUs, represented 23.4% of the total fungal reads), AM (40, 13.9%) and saprophyte (83, 19.8%) were prevalent in the core root-associated fungal community (420 OTUs) of the tropical montane rain forest. Network analysis indicated that AM, ECM and root-associated fungus-plant interaction network showed structural features which cannot be predicate by null models assuming species interact randomly. Community level indices behaved differently among different ecotypes of fungus-plant interactions. Specifically, the degree of nestedness (NODF) and connectance were higher, while specialization was lower in the AM interaction network than the expected values from null models. In contrast, the ECM interaction network had a significantly higher degree of specialization and lower nestedness and connectance than the null models. At guild levels, plant niche overlap of AM and ECM interactions are higher and lower than the null model, respectively. Niche breadth of ECM fungi was narrower than that of AM fungi. Co-occurrence patterns of plant and fungus further confirmed competition for resources was intense in ECM interaction network (high C-score of both plants and fungi) and weak in the AM interaction network (low C-score). These findings suggest that at least two modes of interspecific interactions are critical for the assembly and coexistence of root-associated fungal communities, i.e. redundancy (nestedness) of AM interactions, and niche differentiation (specialization) of ECM interactions. Here we provide a comprehensive exploration of the interactions among functionally diverse root-associated fungal guild within a forest, which is key to understand the mechanisms maintaining species coexistence in tropical forests.

Key words: root-associated fungi, tropical montane rain forest, interaction network, nestedness, specialization

Fig. 1

Rarefaction curves of root-associated fungi of eight plant families in the tropical montane rain forest of Jianfengling"

Table 1

Species diversity and richness of root-associated fungal community of eight plant families in the tropical montane rain forest of Jianfengling"

宿主植物
Host plant
根样品数
No. of root samples
真菌物种数 / reads
No. of fungal species/reads
核心真菌物种数 / reads
No. of core fungal species/reads
Shannon多样性指数
Shannon diversity index
槭树科 Aceraceae 34 701 / 31,589 328 / 29,817 3.97
番荔枝科 Annonaceae 32 440 / 31,588 256 / 30,846 2.88
夹竹桃科 Apocynaceae 41 434 / 31,589 277 / 31,134 2.58
冬青科 Aquifoliaceae 39 675 / 31,588 334 / 29,932 4.05
棕榈科 Arecaceae 21 436 / 31,589 264 / 30,894 3.12
壳斗科 Fagaceae 31 359 / 31,589 217 / 30,983 2.58
樟科 Lauraceae 35 463 / 31,589 261 / 30,508 4.04
木犀科 Oleaceae 34 546 / 31,589 302 / 30,527 3.72

Fig. 2

Compositional differences of root-associated fungi by order among the eight plant families in the tropical montane rain forest of Jianfengling. For each plant family, left and right column are percentage of OTUs and reads, respectively."

Fig. 3

Compositional differences in reads of root-associated fungi by guilds and trophic modes of the eight plant families in the tropical montane rain forest of Jianfengling"

Fig. 4

Root-associated fungus-plant interaction networks (left) with density plots showing the distribution of nestedness (NODF) predicted by Patefiled’s null model (right) and observed nestedness (red vertical line) in tropical montane rain forest of Jianfenling Mountain Hainan Island. (A) and (B) are partial networks of AM and ECM interactions, and (C) is the whole root-associated fungus-plant interaction network. Acer, Aceraceae; Anno, Annoaceae; Apoc, Apocynaceae; Aqui, Aquifoliaceae; Arec, Arecaceae; Faga, Fagaceae; Laur, Lauraceae; Olea, Oleaceae. Interactions between plant and fungi are indicated by grey lines with thickness proportional to interaction strength."

Table 2

Structural features of root-associated fungus-plant interaction networks"

丛枝菌根网络
Arbuscular mycorrhizal network
外生菌根网络
Ectomycorrhizal network
根部真菌-植物互作网络
Root-associated fungus-plant network
观察值
Observed
零模型
Null model
观察值
Observed
零模型
Null model
观察值
Observed
零模型
Null model
网络嵌套性
Nestedness metric based on overlap and decreasing fill, NODF
68.39 60.70 26.06 58.36 32.59 9.40
网络加权嵌套性 Weighted NODF 45.12 53.76 18.04 48.44 20.46 7.69
网络专一性 Specialization (H°2) 0.31 0.01 0.81 0.01 0.54 0.01
网络连接性 Connectance 0.42 0.88 0.21 0.89 0.26 0.99
植物生态位重叠 Niche overlap of plants 0.46 0.99 0.11 0.99 0.25 0.99
真菌生态位重叠 Niche overlap of fungi 0.35 0.97 0.39 0.98 0.19 0.91
植物的伙伴多样性 Generality of plants 5.46 7.87 5.32 10.92 34.14 87.31
真菌的伙伴多样性 Vulnerability of fungi 3.41 4.84 1.28 2.74 3.16 7.95
植物Checkboard值 C-score of plants 0.17 0.28 0.62 0.48 0.38 0.96
真菌Checkboard值 C-score of fungi 0.24 0.02 0.52 0.43 0.62 0.85
1 Almario J, Jeena G, Wunder J, Langen G, Zuccaro A, Coupland G, Bucher M ( 2017) Root-associated fungal microbiota of nonmycorrhizal Arabis alpina and its contribution to plant phosphorus nutrition. Proceedings of the National Academy of Sciences, USA, 114, 9403-9412.
doi: 10.1073/pnas.1707410114 pmid: 28808032
2 Almeida-Neto M, Ulrich W ( 2011) A straightforward computational approach for measuring nestedness using quantitative matrices. Environmental Modelling and Software, 26, 173-178.
doi: 10.1016/j.envsoft.2010.08.003
3 Bahram M, Peay KG, Tedersoo L ( 2014) Local-scale biogeography and spatiotemporal variability in communities of mycorrhizal fungi. New Phytologist, 205, 1454-1463.
doi: 10.1111/nph.13206 pmid: 25767850
4 Bascompte J ( 2007) Networks in ecology. Basic and Applied Ecology, 8, 485-490.
doi: 10.1016/j.baae.2007.06.003
5 Bascompte J, Jordano P, Melián CJ, Olesen JM ( 2003) The nested assembly of plant-animal mutualistic networks. Proceedings of the National Academy of Sciences, USA, 100, 9383-9387.
doi: 10.1073/pnas.1633576100 pmid: 12881488
6 Bastolla U, Fortuna MA, Pascual-Garcia A, Ferrera A, Luque B, Bascompte J ( 2009) The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature, 458, 1018-1020.
doi: 10.1038/nature07950
7 Blaalid R, Davey ML, Kauserud H, Carlsen T, Halvorsen R, Hoiland K, Eidesen PB ( 2014) Arctic root-associated fungal community composition reflects environmental filtering. Molecular Ecology, 23, 649-659.
doi: 10.1111/mec.12622 pmid: 24320873
8 Blüthgen N, Fründ J, Vázquez DP, Menzel F ( 2008) What do interaction network metrics tell us about specialization and biological traits. Ecology, 89, 3387-3399.
doi: 10.1890/07-2121.1 pmid: 19137945
9 Burkle LA, Marlin JC, Knight TM ( 2013) Plant-pollinator interactions over 120 years: Loss of species, co-occurrence, and function. Science, 339, 1611-1615.
doi: 10.1126/science.1232728 pmid: 23449999
10 Cannon PF, Kirk PM ( 2007) Fungal Families of the World. CABI Bioscience, Wallingford.
11 Cardoso EJBN, Nogueira MA, Zangaro W ( 2017) Importance of mycorrhizae in tropical soils. In: Diversity and Benefits of Microorganisms from the Tropics (eds de Azevedo J, Quecine M), Springer, Cham.
doi: 10.1007/978-3-319-55804-2_11
12 Chagnon PL, Bradley RL, Klironomos JN ( 2012) Using ecological network theory to evaluate the causes and consequences of arbuscular mycorrhizal community structure. New Phytologist, 194, 307-312.
doi: 10.1111/j.1469-8137.2011.04044.x
13 Chen L, Zheng Y, Gao C, Mi XC, Ma KP, Wubet T, Guo LD ( 2017) Phylogenetic relatedness explains highly interconnected and nested symbiotic networks of woody plants and arbuscular mycorrhizal fungi in a Chinese subtropical forest. Molecular Ecology, 26, 2563-2575.
doi: 10.1111/mec.14061 pmid: 28207957
14 Corrales A, Henkel TW, Smith ME ( 2018) Ectomycorrhizal associations in the tropics—Biogeography, diversity patterns and ecosystem roles. New Phytologist, 220, 1076-1091.
doi: 10.1111/nph.15151 pmid: 29689121
15 Dickie KH, Cann C, Norman EC, Bamforth CW, Muller RE ( 2001) Foam-negative materials. Journal of the American Society of Brewing Chemists, 59, 17-23.
doi: 10.1094/ASBCJ-59-0017
16 Edgar RC ( 2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26, 2460-2461.
doi: 10.1093/bioinformatics/btq461
17 Edgar RC ( 2013) UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10, 996.
doi: 10.1038/NMETH.2604 pmid: 23955772
18 Edgar RC ( 2018) Accuracy of taxonomy prediction for 16S rRNA and fungal ITS sequences, PeerJ, 6, e4652.
doi: 10.7717/peerj.4652
19 Fang JY, Li YD, Zhu B, Liu GH, Zhou GY ( 2004) Community structures and species richness in the montane rain forest of Jianfengling, Hainan Island, China. Biodiversity Science, 12, 29-43. (in Chinese with English abstract)
doi: 10.3321/j.issn:1005-0094.2004.01.005
[ 方精云, 李意德, 朱彪, 刘国华, 周光益 ( 2004) 海南岛尖峰岭山地雨林的群落结构、物种多样性以及在世界雨林中的地位. 生物多样性, 12, 29-43.]
doi: 10.3321/j.issn:1005-0094.2004.01.005
20 Fortuna MA, Stouffer DB, Olesen JM, Jordano P, Mouillot D, Krasnov BR, Poulin R, Bascompte J ( 2010) Nestedness versus modularity in ecological networks: Two sides of the same coin? Journal of Animal Ecology, 79, 811-817.
doi: 10.1111/j.1365-2656.2010.01688.x pmid: 20374411
21 Gao C, Montoya L, Xu L, Madera M, Hollingsworth J, Purdom E, Hutmacher RB, Dahlberg JA, Coleman-Derr D, Lemaux PG, Taylor JW ( 2019) Strong succession in arbuscular mycorrhizal fungal communities. The ISME Journal, 13, 214-226.
doi: 10.1038/s41396-018-0264-0
22 Gotelli NJ, McCabe DJ ( 2002) Species co-occurrence: A meta-analysis of J. M. Diamond’s assembly rules model. Ecology, 83, 2091-2096.
doi: 10.1890/0012-9658(2002)083[2091:SCOAMA]2.0.CO;2
23 Huang CW, Liao YH, Ding Q ( 2017) Two sample pooling strategies revealed different root-associated fungal diversity of Rhododendron species. Acta Microbiologica Sinica, 57, 571-581. (in Chinese with English abstract)
doi: 10.13343/j.cnki.wsxb.20160337
[ 黄彩微, 廖映辉, 丁琼 ( 2017) 两种混合样品策略对揭示杜鹃花根部真菌多样性的影响. 微生物学报, 57, 571-581.]
doi: 10.13343/j.cnki.wsxb.20160337
24 James A, Pitchford JW, Plank MJ ( 2012) Disentangling nestedness from models of ecological complexity. Nature, 487, 227-230.
doi: 10.1038/nature11214 pmid: 22722863
25 Jiang YX, Lu JP ( 1991) Tropical Forest Ecosystem of Jianfengling, Hainan Island, China. Science Press, Beijing. (in Chinese)
[ 蒋有绪, 卢俊培 ( 1991) 中国海南岛尖峰岭热带林生态系统. 科学出版社, 北京.]
26 Kivlin SN, Winston GC, Goulden ML, Treseder KK ( 2014) Environmental filtering affects soil fungal community composition more than dispersal limitation at regional scales. Fungal Ecology, 12, 14-25.
doi: 10.1016/j.funeco.2014.04.004
27 Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lücking R, Martín MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüβler A, Scott JA, Senés C, Smith ME, Suija A, Taylor DL, Telleria MT, Weiss M, Larsson K-H ( 2013) Towards a unified paradigm for sequence-based identification of fungi. Molecular Ecology, 22, 5271-5277.
doi: 10.1111/mec.12481 pmid: 24112409
28 Kress WJ, Erickson DL, Jones FA, Swenson NG, Perez R, Sanjur O, Bermingham E ( 2009) Plant DNA barcodes and a community phylogeny of a tropical forest dynamics plot in Panama. Proceedings of the National Academy of Sciences, USA, 106, 18621-18626.
doi: 10.1073/pnas.0909820106
29 Merges D, Bálint M, Schmitt I, Böhning-Gaese K, Neuschulz EL ( 2018) Spatial patterns of pathogenic and mutualistic fungi across the elevational range of a host plant. Journal of Ecology, 106, 1545-1557.
doi: 10.1111/1365-2745.12942
30 Newsham KK ( 2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytologist, 190, 783-793.
doi: 10.1111/nph.2011.190.issue-3
31 Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG ( 2016) FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecology, 20, 241-248.
doi: 10.1016/j.funeco.2015.06.006
32 Patefield WM ( 1981) Algorithm AS 159: An efficient method of generating random R × C tables with given row and column totals. Journal of the Royal Statistical Society, Series C (Applied Statistics), 30, 91-97.
doi: 10.2307/2346669
33 Pianka ER ( 1974) Niche overlap and diffuse competition. Proceedings of the National Academy of Sciences, USA, 71, 2141-2145.
doi: 10.1073/pnas.71.5.2141 pmid: 4525324
34 Smith DP, Peay KG ( 2014) Sequence depth, not PCR replication, improves ecological inference from next generation DNA sequencing. PLoS ONE, 9, e90234.
35 Smith SE, Read DJ ( 2008) Mycorrhizal Symbiosis, 3rd edn. Academic Press, London.
36 Taudiere A, Munoz F, Lesne A, Monnet AC, Bellanger JM, Selosse MA, Moreau PA, Richard F ( 2015) Beyond ectomycorrhizal bipartite networks: Projected networks demonstrate contrasted patterns between early- and late-successional plants in Corsica. Frontiers in Plant Science, 6, 881.
doi: 10.3389/fpls.2015.00881 pmid: 4612159
37 Tedersoo L, Bahram M, Põlme S, Kõljalg U, Yorou NS, Wijesundera R, Ruiz LV, Vasco-Palacios AM, Thu PQ, Suija A, Smith ME, Sharp C, Saluveer E, Saitta A, Rosas M, Riit T, Ratkowsky D, Pritsch K, Põldmaa K, Piepenbring M, Phosri C, Peterson M, Parts K, Pärtel K, Otsing E, Nouhra E, Njouonkou AL, Nilsson RH, Morgado LN, Mayor J, May TW, Majuakim L, Lodge DJ, Lee SS, Larsson KH, Kohout P, Hosaka K, Hiiesalu I, Henkel TW, Harend H, Guo LD, Greslebin A, Grelet G, Geml J, Gates G, Dunstan W, Dunk C, Drenkhan R, Dearnaley J, Kesel AD, Dang T, Chen X, Buegger F, Brearley FQ, Bonito G, Anslan S, Abell S, Abarenkov K ( 2014) Global diversity and geography of soil fungi. Science, 346, 1078-1088.
38 Thebault E, Fontaine C ( 2010) Stability of ecological communities and the architecture of mutualistic and trophic Networks. Science, 329, 853-856.
doi: 10.1126/science.1188321 pmid: 20705861
39 Thiéry O, Vasar M, Jairus T, Davison J, Roux C, Kivistik PA, Metspalu A, Milani L, Saks ü, Moora M, Zobel M, Öpik M ( 2016) Sequence variation in nuclear ribosomal small subunit, internal transcribed spacer and large subunit regions of Rhizophagus irregularis and Gigaspora margarita is high and isolate-dependent. Molecular Ecology, 25, 2816-2832.
doi: 10.1111/mec.2016.25.issue-12
40 Toju H, Sato H, Yamamoto S, Kadowaki K, Tanabe AS, Yazawa S, Nishimura O, Agata K ( 2013 a) How are plant and fungal communities linked to each other in belowground ecosystems? A massively parallel pyrosequencing analysis of the association specificity of root-associated fungi and their host plants. Ecology and Evolution, 3, 3112-3124.
doi: 10.1002/ece3.706 pmid: 24101998
41 Toju H, Yamamoto S, Sato H, Tanabe AS, Gilbert GS, Kadowaki K ( 2013 b) Community composition of root-associated fungi in a Quercus-dominated temperate forest: “Codominance” of mycorrhizal and root-endophytic fungi. Ecology and Evolution, 3, 1281-1293.
doi: 10.1002/ece3.2013.3.issue-5
42 Tylianakis JM ( 2009) Warming up food webs. Science, 323, 1300-1301.
doi: 10.1126/science.1170909
43 Ulrich W, Gotelli NJ ( 2007) Null model analysis of species nestedness patterns. Ecology, 88, 1824-1831.
doi: 10.1890/06-1208.1 pmid: 17645028
44 Vázquez DP, Chacoff NP, Cagnolo L ( 2009) Evaluating multiple determinants of the structure of plant-animal mutualistic networks. Ecology, 90, 2039-2046.
doi: 10.1890/08-1837.1 pmid: 19739366
45 Xu H, Li YD, Lin MX, Wu JH, Luo TS, Zhou Z, Chen DX, Yang H, Li GJ, Liu SR ( 2015) Community characteristics of a 60 ha dynamics plot in the tropical montane rain forest in Jianfengling, Hainan Island. Biodiversity Science, 23, 192-201. (in Chinese with English abstract)
doi: 10.17520/biods.2014157
[ 许涵, 李意德, 林明献, 吴建辉, 骆土寿, 周璋, 陈德祥, 杨怀, 李广建, 刘世荣 ( 2015) 海南尖峰岭热带山地雨林60 ha动态监测样地群落结构特征. 生物多样性, 23, 192-201.]
doi: 10.17520/biods.2014157
46 Yamamoto S, Sato H, Tanabe AS, Hidaka A, Kadowaki K, Toju H ( 2014) Spatial segregation and aggregation of ectomycorrhizal and root-endophytic fungi in the seedlings of two Quercus species. PLoS ONE, 9, e96363.
doi: 10.1371/journal.pone.0096363 pmid: 24801150
47 Zhang J, Kobert K, Flouri T, Stamatakis A ( 2013) PEAR: A fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics, 30, 614-620.
doi: 10.1093/bioinformatics/btt593 pmid: 24142950
[1] LIN Li-Tao, MA Ke-Ming. (2019) Selection of null models in nestedness pattern detection of highly asymmetric mycorrhizal networks . Chin J Plant Ecol, 43(7): 611-623.
[2] Dong Zhang,Fengying Wan,Ling Chu,Yunzhi Yan. (2018) Longitudinal patterns in α and β diversity of the taxonomic and functional organizations of stream fish assemblages in the Qingyi River . Biodiv Sci, 26(1): 1-13.
[3] Xingfeng Si, Yuhao Zhao, Chuanwu Chen, Peng Ren, Di Zeng, Lingbing Wu, Ping Ding. (2017) Beta-diversity partitioning: methods, applications and perspectives . Biodiv Sci, 25(5): 464-480.
[4] Yan-Peng LI, Han XU, Yi-De LI, Tu-Shou LUO, De-Xiang CHEN, Zhang ZHOU, Ming-Xian LIN, Huai YANG. (2016) Scale-dependent spatial patterns of species diversity in the tropical montane rain forest in Jianfengling, Hainan Island, China . Chin J Plan Ecolo, 40(9): 861-870.
[5] Xuemei Zhang,Xufang Han,Liwei Liu,Aichun Xu. (2016) Influencing factors of the nested distribution of butterfly assemblages in the Zhoushan Archipelago, China . Biodiv Sci, 24(3): 321-331.
[6] Qiang Fang, Shuangquan Huang. (2012) Progress in pollination networks: network structure and dynamics . Biodiv Sci, 20(3): 300-307.
[7] Jingcheng Zhang, Yanping Wang, Pingping Jiang, Peng Li, Mingjian Yu, Ping Ding. (2008) Nested analysis of passeriform bird assemblages in the Thousand Island Lake region . Biodiv Sci, 16(4): 321-331.
[8] Wenjin Wang, Ming Zhang, Fude Liu, Jianwei Zheng, Zhongsheng Wang, Shiting Zhang, Wenjie Yang, Shu-qing An. (2007) Species association in tropical montane rain forest at two successional stages in Diaoluo Mountain of Hainan Island . Biodiv Sci, 15(3): 257-263.
[9] ZHU Hua. (2006) A DISCUSSION ON PLANT DIVERSITY OF TROPICAL MONTANE RAIN FORESTS IN XISHUANGBANNA, YUNNAN . Chin J Plan Ecolo, 30(1): 184-186.
[10] ZHENG Zheng, LI You-Rong, LIU Hong-Mao, FENG Zhi-Li, GAN Jian-Min, KONG Wei-Jing. (2005) LITTERFALL OF TROPICAL RAIN FORESTS AT DIFFERENT ALTITUDES,XISHUANGBANNA, SOUTHWEST CHINA . Chin J Plan Ecolo, 29(6): 884-893.
[11] LI Zong-Shan, TANG Jian-Wei, ZHENG Zheng, LI Qing-Jun, LUO Cheng-Kun, LIU Zheng-An, LI Zi-Neng, DUAN Wen-Yong, GUO Xian-Ming. (2004) A STUDY ON PLANT DIVERSITY OF TROPICAL MONTANE RAIN FORESTS IN XISHUANGBANNA, YUNNAN . Chin J Plan Ecolo, 28(6): 833-843.
[12] LIU Can-Ran, MA Ke-Ping, CHEN Ling-Zhi. (2002) NESTEDNESS: METHODS, MECHANISMS AND IMPLICATIONS FOR BIOLOGICAL CONSERVATION . Chin J Plan Ecolo, 26(增刊): 68-72.
[13] ZHANG Xiao-Ai, ZHAO Liang, KANG Ling. (2001) Evolutionary mechanisms of species coexistence in ecological communities . Biodiv Sci, 09(1): 8-17.
[14] HUANG Shi-Neng, LI Yi-De, LUO Tu-Shou, WANG Bo-Sun. (2000) Dynamics of Associations Between Tree Species During 10 Years of Succession in a Secondary-growth Tropical Montane Rainforest at Jianfengling on Hainan Island, China . Chin J Plan Ecolo, 24(5): 569-574.
[15] Yu Shixiao, Chong Guowei, Chen Zhaoying, Zang Runguo, Yang Yingcheng. (1998) Comparison of Ecological Entropy With Random and Systematic Sampling . Chin J Plan Ecolo, 22(5): 473-480.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed