Biodiversity Science ›› 2013, Vol. 21 ›› Issue (4): 488-498.doi: 10.3724/SP.J.1003.2013.11055

Special Issue: Microbes Diversity

• Orginal Article • Previous Article     Next Article

Distribution pattern and maintenance of ectomycorrhizal fungus diversity

Cheng Gao1, 2, Liangdong Guo1, *()   

  1. 1 State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101
    2 University of Chinese Academy of Sciences, Beijing 100049
  • Received:2013-03-04 Accepted:2013-07-01 Online:2013-07-29
  • Guo Liangdong E-mail:guold@sun.im.ac.cn

Ectomycorrhiza (ECM) are symbionts formed between soil fungi and plant root systems, in which the fungus exchanges soil-derived nutrients for carbohydrates obtained from the host plant. As an important component of terrestrial ecosystems, ECM fungi can play an essential role in biodiversity maintenance and plant community succession. Understanding the distribution pattern and maintenance of ECM fungal diversity is therefore critical to the study of biodiversity and ecosystem functioning. An analysis of results of recent research indicates that ECM fungal diversity increases with increasing latitude, i.e. from tropical to subtropical and temperate regions. The role of dispersal in ECM fungal distribution is dependent on spatial scale. Thus, it has been found to be weak across global and local scales, but strong at regional and small scales. At the local scale, its influence has also been shown to be host-dominant dependent; thus, it is important in host non-dominant ecosystems, but not in host dominant ecosystems. Selection by plant, animal, microbe and abiotic factors can also affect the distribution pattern of ECM fungi, according to studies of temperate ecosystems. In contrast, studies of tropical ecosystems indicate that selection on ECM fungal distribution can be either strong or weak. ECM fungal diversity is also influenced by plant diversity and productivity. The plant diversity hypothesis at host genus-level fits well with ECM fungal diversity in temperate, subtropical and tropical forest ecosystems; in contrast, the productivity diversity hypothesis is only supported by some studies in temperate forest ecosystems. We propose that future studies should focus on the distribution pattern, maintenance mechanism and ecosystem function of ECM fungal diversity at a global scale, taking account of scenarios of global climate change.

Key words: selection, dispersal, spatial scale dependence, host dominant dependence, plant diversity hypothesis, productivity diversity hypothesis

Fig. 1

Ectomycorrhizal fungal (ECM) diversity in different climatic types. (A) ECM fungal species richness increased with host plant genus richness in both temperate (dots) and tropical (quadrates) forests. (B) ECM fungal species richness per plant species in temperate, subtropical and tropical forests, respectively. Different letters on bars denote significant difference at P < 0.05 level."

Fig. 2

The distribution pattern and maintenance mechanism of ectomycorrhizal fungal (ECM) diversity at different spatial scales and in different climatic types"

1 Amend AS, Seifert KA, Samson R, Bruns TD (2010) Indoor fungal composition is geographically patterned and more diverse in temperate zones than in the tropics. Proceedings of the National Academy of Sciences, USA, 107, 13748-13753.
2 Andrew C, Lilleskov EA (2009) Productivity and community structure of ectomycorrhizal fungal sporocarps under increased atmospheric CO2 and O3.Ecology Letters, 12, 813-822.
3 Aponte C, García LV, Marañón T, Gardes M (2010) Indirect host effect on ectomycorrhizal fungi: leaf fall and litter quality explain changes in fungal communities on the roots of co-occurring Mediterranean oaks.Soil Biology and Biochemistry, 42, 788-796.
4 Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology, 88, 541-549.
5 Aspray TJ, Jones EE, Davies MW, Shipman M, Bending GD (2013) Increased hyphal branching and growth of ectomycorrhizal fungus Lactarius rufus by the helper bacterium Paenibacillus sp.Mycorrhiza, 23, 403-410.
6 Bahram M, Põlme S, Kõljalg U, Zarre S, Tedersoo L (2012) Regional and local patterns of ectomycorrhizal fungal diversity and community structure along an altitudinal gradient in the Hyrcanian forests of northern Iran.New Phytologist, 193, 465-473.
7 Bending GD, Poole EJ, Whipps JM, Read DJ (2002) Characterisation of bacteria from Pinus sylvestris-Suillus luteus mycorrhizas and their effects on root-fungus interactions and plant growth.FEMS Microbiology Ecology, 39, 219-227.
8 Berner C, Johansson T, Wallander H (2012) Long-term effect of apatite on ectomycorrhizal growth and community structure.Mycorrhiza, 22, 615-621.
9 Bomberg M, Jurgens G, Saano A, Sen R, Timonen S (2003) Nested PCR detection of archaea in defined compartments of pine mycorrhizospheres developed in boreal forest humus microcosms.FEMS Microbiology Ecology, 43, 163-171.
10 Bomberg M, Timonen S (2009) Effect of tree species and mycorrhizal colonization on the archaeal population of boreal forest rhizospheres.Applied and Environmental Microbiology, 75, 308-315.
11 Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants.New Phytologist, 154, 275-304.
12 Bruns TD (1995) Thoughts on the processes that maintain local species-diversity of ectomycorrhizal fungi.Plant and Soil, 170, 63-73.
13 Cavender-Bares J, Izzo A, Robinson R, Lovelock CE (2009) Changes in ectomycorrhizal community structure on two containerized oak hosts across an experimental hydrologic gradient.Mycorrhiza, 19, 133-142.
14 Cox F, Barsoum N, Lilleskov EA, Bidartondo MI (2010) Nitrogen availability is a primary determinant of conifer mycorrhizas across complex environmental gradients.Ecology Letters, 13, 1103-1113.
15 Craig MacLean R, Dickson A, Bell G (2005) Resource competition and adaptive radiation in a microbial microcosm.Ecology Letters, 8, 38-46.
16 Crane S, Barkay T, Dighton J (2012) The effect of mercury on the establishment of Pinus rigida seedlings and the development of their ectomycorrhizal communities.Fungal Ecology, 5, 245-251.
17 Deslippe J, Hartmann M, Mohn W, Simard S (2011) Long-term experimental manipulation of climate alters the ectomycorrhizal community of Betula nana in Arctic tundra.Global Change Biology, 17, 1625-1636.
18 Dickie I, Xu B, Koide R (2002) Vertical niche differentiation of ectomycorrhizal hyphae in soil as shown by T-RFLP analysis.New Phytologist, 156, 527-535.
19 Dickie IA (2007) Host preference, niches and fungal diversity.New Phytologist, 174, 230-233.
20 Dickie IA, Dentinger BTM, Avis PG, McLaughlin DJ, Reich PB (2009) Ectomycorrhizal fungal communities of oak savanna are distinct from forest communities.Mycologia, 101, 473-483.
21 Dickie IA, Reich PB (2005) Ectomycorrhizal fungal comm- unities at forest edges.Journal of Ecology, 93, 244-255.
22 Ding Q, Liang Y, Legendre P, He XH, Pei KQ, Du XJ, Ma KP (2011) Diversity and composition of ectomycorrhizal community on seedling roots: the role of host preference and soil origin.Mycorrhiza, 21, 669-680.
23 Druebert C, Lang C, Valtanen K, Polle A (2009) Beech carbon productivity as driver of ectomycorrhizal abundance and diversity.Plant, Cell and Environment, 32, 992-1003.
24 Eisenhauer N, Milcu A, Sabais AC, Bessler H, Brenner J, Engels C, Klarner B, Maraun M, Partsch S, Roscher C, Schonert F, Temperton VM, Thomisch K, Weigelt A, Weisser WW, Scheu S (2011) Plant diversity surpasses plant functional groups and plant productivity as driver of soil biota in the long term.PLoS ONE, 6, e16055.
25 Facelli E, Smith SE, Facelli JM, Christophersen HM, Andrew Smith F (2010) Underground friends or enemies: model plants help to unravel direct and indirect effects of arbuscular mycorrhizal fungi on plant competition.New Phytologist, 185, 1050-1061.
26 Frey-Klett P, Chavatte M, Clausse ML, Courrier S, Roux CL, Raaijmakers J, Martinotti MG, Pierrat JC, Garbaye J (2005) Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads.New Phytologist, 165, 317-328.
27 Gao C, Shi NN, Liu YX, Peay GK, Zheng Y, Ding Q, Mi XC, Ma KP, Wubet T, Buscot F, Guo LD (2013) Host plant genus level diversity is the best predictor of ectomycorrhizal fungal diversity in a Chinese subtropical forest.Molecular Ecology, 22, 3403-3414.
28 Gao Q, Yang ZL (2010) Ectomycorrhizal fungi associated with two species of Kobresia in an alpine meadow in the eastern Himalaya.Mycorrhiza, 20, 281-287.
29 Gebhardt S, Neubert K, Wollecke J, Munzenberger B, Huttl RF (2007) Ectomycorrhiza communities of red oak (Quercus rubra L.) of different age in the Lusatian lignite mining district, East Germany.Mycorrhiza, 17, 279-290.
30 Geml J, Timling I, Robinson CH, Lennon N, Nusbaum HC, Brochmann C, Noordeloos ME, Taylor DL (2012) An arctic community of symbiotic fungi assembled by long-distance dispersers: phylogenetic diversity of ectomycorrhizal basidiomycetes in Svalbard based on soil and sporocarp DNA.Journal of Biogeography, 39, 74-88.
31 Govindarajulu M, Pfeffer PE, Jin H, Abubaker J, Douds DD, Allen JW, Bücking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis.Nature, 435, 819-823.
32 Guo LD (郭良栋) (2012) Progress of microbial species diversity research in China.Biodiversity Science(生物多样性), 20, 572-580. (in Chinese with English abstract)
33 Guo LD (郭良栋), Tian CJ (田春杰) (2013) Progress of the function of mycorrhizal fungi in the cycle of carbon and nitrogen.Microbiology China(微生物学通报), 40, 158-171. (in Chinese with English abstract)
34 Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH (2012) Beyond biogeographic patterns: processes shaping the microbial landscape.Nature Reviews Microbiology, 10, 497-506.
35 Harrington TJ, Mitchell DT (2005) Ectomycorrhizas associated with a relict population of Dryas octopetala in the Burren, western Ireland. I. Distribution of ectomycorrhizas in relation to vegetation and soil characteristics.Mycorrhiza, 15, 425-433.
36 Hartley-Whitaker J, Cairney JWG, Meharg AA (2000) Toxic effects of cadmium and zinc on ectomycorrhizal colonization of Scots pine (Pinus sylvestris L.) from soil inoculum.Environmental Toxicology and Chemistry, 19, 694-699.
37 Hawksworth DL (2001) The magnitude of fungal diversity: the 1.5 million species estimate revisited.Mycological Research, 105, 1422-1432.
38 Hayward JA, Horton TR (2012) Edaphic factors do not govern the ectomycorrhizal specificity of Pisonia grandis (Nyctaginaceae).Mycorrhiza, 22, 647-652.
39 Hazard C, Gosling P, van der Gast CJ, Mitchell DT, Doohan FM, Bending GD (2013) The role of local environment and geographical distance in determining community composition of arbuscular mycorrhizal fungi at the landscape scale.The ISME Journal, 7, 498-508.
40 He XH, Duan YH, Chen YL, Xu MG (2010) A 60-year journey of mycorrhizal research in China: past, present and future directions.Science China-Life Sciences, 53, 1374-1398.
41 Hillebrand H (2004) On the generality of the latitudinal diversity gradient.The American Naturalist, 163, 192-211.
42 Hoeksema JD, Hernandez JV, Rogers DL, Mendoza LL, Thompson JN (2012) Geographic divergence in a species-rich symbiosis: interactions between monterey pines and ectomycorrhizal fungi.Ecology, 93, 2274-2285.
43 Hooper D, Bignell D, Brown V, Brussard L, Mark Dangerfield J, Wall D, Wardle D, Coleman D, Giller K, Lavelle P (2000) Interactions between aboveground and belowground biodiversity in terrestrial ecosystems: patterns, mechanisms, and feedbacks.BioScience, 50, 1049-1061.
44 Horton TR, Bruns TD (1998) Multiple-host fungi are the most frequent and abundant ectomycorrhizal types in a mixed stand of Douglas fir (Pseudotsuga menziesii) and bishop pine (Pinus muricata).New Phytologist, 139, 331-339.
45 Hrynkiewicz K, Baum C, Niedojadlo J, Dahm H (2009) Promotion of mycorrhiza formation and growth of willows by the bacterial strain Sphingomonas sp. 23L on fly ash.Biology and Fertility of Soils, 45, 385-394.
46 Huang J, Nara K, Lian CL, Zong K, Peng KJ, Xue SG, Shen ZG (2012) Ectomycorrhizal fungal communities associated with Masson pine (Pinus massoniana Lamb.) in Pb-Zn mine sites of central south China.Mycorrhiza, 22, 589-602.
47 Ishida TA, Nara K, Hogetsu T (2007) Host effects on ectomycorrhizal fungal communities: insight from eight host species in mixed conifer-broadleaf forests.New Phytologist, 174, 430-440.
48 Iwanski M, Rudawska M (2007) Ectomycorrhizal colonization of naturally regenerating Pinus sylvestris L. seedlings growing in different micro-habitats in boreal forest.Mycorrhiza, 17, 461-467.
49 Izzo A, Canright M, Bruns TD (2006) The effects of heat treatments on ectomycorrhizal resistant propagules and their ability to colonize bioassay seedlings.Mycological Research, 110, 196-202.
50 Jarvis S, Woodward S, Alexander IJ, Taylor AFS (2013) Regional scale gradients of climate and nitrogen deposition drive variation in ectomycorrhizal fungal communities associated with native Scots pine.Global Change Biology, 19, 1688-1696.
51 Jonas JL, Wilson GWT, White PM, Joern A (2007) Consump- tion of mycorrhizal and saprophytic fungi by Collembola in grassland soils.Soil Biology and Biochemistry, 39, 2594-2602.
52 Jonsson L, Dahlberg A, Nilsson MC, Karen O, Zackrisson O (1999) Continuity of ectomycorrhizal fungi in self-regenerating boreal Pinus sylvestris forests studied by comparing mycobiont diversity on seedlings and mature trees.New Phytologist, 142, 151-162.
53 Kennedy PG, Hortal S, Bergemann SE, Bruns TD (2007) Competitive interactions among three ectomycorrhizal fungi and their relation to host plant performance.Journal of Ecology, 95, 1338-1345.
54 Kernaghan G, Widden P, Bergeron Y, Legare S, Pare D (2003) Biotic and abiotic factors affecting ectomycorrhizal diversity in boreal mixed-woods.Oikos, 102, 497-504.
55 Koide RT, Shumway DL, Xu B, Sharda JN (2007) On temporal partitioning of a community of ectomycorrhizal fungi.New Phytologist, 174, 420-429.
56 Koide RT, Xu B, Sharda J, Lekberg Y, Ostiguy N (2005) Evidence of species interactions within an ectomycorrhizal fungal community.New Phytologist, 165, 305-316.
57 Kranabetter JM, Durall DM, MacKenzie WH (2009) Diversity and species distribution of ectomycorrhizal fungi along productivity gradients of a southern boreal forest.Mycorrhiza, 19, 99-111.
58 Langenheder S, Prosser JI (2008) Resource availability influences the diversity of a functional group of hetero- trophic soil bacteria.Environmental Microbiology, 10, 2245-2256.
59 Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy.Nature Reviews Microbiology, 9, 119-130.
60 Liang Y (梁宇), Guo LD (郭良栋), Ma KP (马克平) (2002) The role of mycorrhizal fungi in ecosystems.Acta Phytoecologica Sinica(植物生态学报), 26, 739-745. (in Chinese with English abstract)
61 Lilleskov EA, Bruns TD, Horton TR, Taylor D, Grogan P (2004) Detection of forest stand-level spatial structure in ectomycorrhizal fungal communities.FEMS Microbiology Ecology, 49, 319-332.
62 Mahmood S, Finlay RD, Fransson AM, Wallander H (2003) Effects of hardened wood ash on microbial activity, plant growth and nutrient uptake by ectomycorrhizal spruce seedlings.FEMS Microbiology Ecology, 43, 121-131.
63 Morris MH, Smith ME, Rizzo DM, Rejmanek M, Bledsoe CS (2008) Contrasting ectomycorrhizal fungal communities on the roots of co-occurring oaks (Quercus spp.) in a California woodland.New Phytologist, 178, 167-176.
64 Olsson PA, Wallander H (1998) Interactions between ectomycorrhizal fungi and the bacterial community in soils amended with various primary minerals.FEMS Microbiology Ecology, 27, 195-205.
65 Öpik M, Moora M, Liira J, Zobel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe.Journal of Ecology, 94, 778-790.
66 Parrent JL, Morris WF, Vilgalys R (2006) CO2 enrichment and nutrient availability alter ectomycorrhizal fungal communities.Ecology, 87, 2278-2287.
67 Peay KG, Garbelotto M, Bruns TD (2009) Spore heat resistance plays an important role in disturbance-mediated assemblage shift of ectomycorrhizal fungi colonizing Pinus muricata seedlings.Journal of Ecology, 97, 537-547.
68 Peay KG, Garbelotto M, Bruns TD (2010a) Evidence of dispersal limitation in soil microorganisms: isolation reduces species richness on mycorrhizal tree islands.Ecology, 91, 3631-3640.
69 Peay KG, Kennedy PG, Bruns TD (2011) Rethinking ectomycorrhizal succession: are root density and hyphal exploration types drivers of spatial and temporal zonation? Fungal Ecology, 4, 233-240.
70 Peay KG, Kennedy PG, Davies SJ, Tan S, Bruns TD (2010b) Potential link between plant and fungal distributions in a dipterocarp rainforest: community and phylogenetic structure of tropical ectomycorrhizal fungi across a plant and soil ecotone.New Phytologist, 185, 529-542.
71 Peay KG, Schubert MG, Nguyen NH, Bruns TD (2012) Measuring ectomycorrhizal fungal dispersal: macroecolo- gical patterns driven by microscopic propagules.Molecular Ecology, 21, 4122-4136.
72 Pennisi E (2004) The secret life of fungi.Science, 304, 1620-1622.
73 Pickles BJ, Genney DR, Anderson IC, Alexander IJ (2012) Spatial analysis of ectomycorrhizal fungi reveals that root tip communities are structured by competitive interactions.Molecular Ecology, 21, 5110-5123.
74 Pirozynski K, Malloch D (1975) The origin of land plants: a matter of mycotrophism.Biosystems, 6, 153-164.
75 Põlme S, Bahram M, Yamanaka T, Nara K, Dai YC, Grebenc T, Kraigher H, Toivonen M, Wang PH, Matsuda Y, Naadel T, Kennedy PG, Kõljalg U, Tedersoo L (2013) Biogeo- graphy of ectomycorrhizal fungi associated with alders (Alnus spp.) in relation to biotic and abiotic variables at the global scale.New Phytologist, 198, 1239-1249.
76 Pyare S, Longland WS (2001) Patterns of ectomycorrhizal- fungi consumption by small mammals in remnant old-growth forests of the Sierra Nevada.Journal of Mammalogy, 82, 681-689.
77 Richard F, Millot S, Gardes M, Selosse MA (2005) Diversity and specificity of ectomycorrhizal fungi retrieved from an old-growth Mediterranean forest dominated by Quercus ilex.New Phytologist, 166, 1011-1023.
78 Rinaldi AC, Commandini O, Kuyper TW (2009) Ectomycor- rhizal fungal diversity: separating the wheat from the chaff.Fungal Diversity, 33, 1-45.
79 Sato H, Tsujino R, Kurita K, Yokoyama K, Agata K (2012) Modelling the global distribution of fungal species: new insights into microbial cosmopolitanism.Molecular Ecology, 21, 5599-5612.
80 Scattolin L, Dal Maso E, Accordi SM, Sella L, Montecchio L (2012) Detecting asymptomatic ink-diseased chestnut trees by the composition of the ectomycorrhizal community.Forest Pathology, 42, 501-509.
81 Schickmann S, Urban A, Krautler K, Nopp-Mayr U, Hacklander K (2012) The interrelationship of mycophagous small mammals and ectomycorrhizal fungi in primeval, disturbed and managed Central European mountainous forests.Oecologia, 170, 395-409.
82 Schmit JP, Mueller GM, Leacock PR, Mata JL, Wu Q, Huang Y (2005) Assessment of tree species richness as a surrogate for macrofungal species richness.Biological Conservation, 121, 99-110.
83 Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Consortium FB (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proceedings of the National Academy of Sciences,USA, 109, 6241-6246.
84 Simon L, Bousquet J, Lévesque RC, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants.Nature, 363, 67-69.
85 Smith ME, Douhan GW, Fremier AK, Rizzo DM (2009) Are true multihost fungi the exception or the rule? Dominant ectomycorrhizal fungi on Pinus sabiniana differ from those on co-occurring Quercus species.New Phytologist, 182, 295-299.
86 Smith ME, Douhan GW, Rizzo DM (2007) Ectomycorrhizal community structure in a xeric Quercus woodland based on rDNA sequence analysis of sporocarps and pooled roots.New Phytologist, 174, 847-863.
87 Smith ME, Henkel TW, Catherine Aime M, Fremier AK, Vilgalys R (2011) Ectomycorrhizal fungal diversity and community structure on three co-occurring leguminous canopy tree species in a Neotropical rainforest.New Phytologist, 192, 699-712.
88 Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, 3rd edn. Academic Press, New York.
89 Stephan A, Meyer AH, Schmid B (2000) Plant diversity affects culturable soil bacteria in experimental grassland communities.Journal of Ecology, 88, 988-998.
90 Taniguchi T, Kanzaki N, Tamai S, Yamanaka N, Futai K (2007) Does ectomycorrhizal fungal community structure vary along a Japanese black pine (Pinus thunbergii) to black locust (Robinia pseudoacacia) gradient? New Phytologist, 173, 322-334.
91 Tedersoo L, Bahram M, Jairus T, Bechem E, Chinoya S, Mpumba R, Leal M, Randrianjohany E, Razafimandimbison S, Sadam A, Naadel T, Kõljalg U (2011) Spatial structure and the effects of host and soil environments on communities of ectomycorrhizal fungi in wooded savannas and rain forests of Continental Africa and Madagascar.Molecular Ecology, 20, 3071-3080.
92 Tedersoo L, Bahram M, Toots M, Diédhiou AG, Henkel TW, Kjøller R, Morris MH, Nara K, Nouhra E, Peay KG, Põlme S, Ryberg M, Smith ME, Kõljalg U (2012) Towards global patterns in the diversity and community structure of ectomycorrhizal fungi.Molecular Ecology, 21, 4160-4170.
93 Tedersoo L, Jairus T, Horton BM, Abarenkov K, Suvi T, Saar I, Kõljalg U (2008a) Strong host preference of ectomycorrhizal fungi in a Tasmanian wet sclerophyll forest as revealed by DNA barcoding and taxon-specific primers.New Phytologist, 180, 479-490.
94 Tedersoo L, Nara K (2010) General latitudinal gradient of biodiversity is reversed in ectomycorrhizal fungi.New Phytologist, 185, 351-354.
95 Tedersoo L, Partel K, Jairus T, Gates G, Poldmaa K, Tamm H (2009) Ascomycetes associated with ectomycorrhizas: molecular diversity and ecology with particular reference to the Helotiales.Environmental Microbiology, 11, 3166-3178.
96 Tedersoo L, Sadam A, Zambrano M, Valencia R, Bahram M (2010) Low diversity and high host preference of ectomycorrhizal fungi in western Amazonia, a neotropical biodiversity hotspot.The ISME Journal, 4, 465-471.
97 Tedersoo L, Suvi T, Jairus T, Kõljalg U (2008b) Forest microsite effects on community composition of ectomycorrhizal fungi on seedlings of Picea abies and Betula pendula.Environmental Microbiology, 10, 1189-1201.
98 Tilman D (1982) Resource Competition and Community Structure. Princeton University Press, Princeton.
99 Tilman D, Wedin D, Knops J (1996) Productivity and sustainability influenced by biodiversity in grassland ecosystems.Nature, 379, 718-720.
100 Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies.Ecology Letters, 11, 1111-1120.
101 Twieg BD, Durall DM, Simard SW (2007) Ectomycorrhizal fungal succession in mixed temperate forests.New Phytologist, 176, 437-447.
102 Uroz S, Calvaruso C, Turpaul MP, Pierrat JC, Mustin C, Frey-Klett P (2007) Effect of the mycorrhizosphere on the genotypic and metabolic diversity of the bacterial communities involved in mineral weathering in a forest soil.Applied and Environmental Microbiology, 73, 3019-3027.
103 van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems.Ecology Letters, 11, 296-310.
104 Vellend M (2010) Conceptual synthesis in community ecology.Quarterly Review of Biology, 85, 183-206.
105 Viketoft M, Bengtsson J, Sohlenius B, Berg MP, Petchey O, Palmborg C, Huss-Danell K (2009) Long-term effects of plant diversity and composition on soil nematode communities in model grasslands.Ecology, 90, 90-99.
106 Waldrop MP, Zak DR, Blackwood CB, Curtis CD, Tilman D (2006) Resource availability controls fungal diversity across a plant diversity gradient.Ecology Letters, 9, 1127-1135.
107 Walker JF, Miller OK, Horton JL (2005) Hyperdiversity of ectomycorrhizal fungus assemblages on oak seedlings in mixed forests in the southern Appalachian Mountains.Molecular Ecology, 14, 829-838.
108 Wang Q, Gao C, Guo LD (2011) Ectomycorrhizae associated with Castanopsis fargesii (Fagaceae) in a subtropical forest, China.Mycological Progress, 10, 323-332.
109 Wang Q, He XH, Guo LD (2012) Ectomycorrhizal fungus communities of Quercus liaotungensis Koidz of different ages in a northern China temperate forest.Mycorrhiza, 22, 461-470.
110 Wang ZH (王志恒), Tang ZY (唐志尧), Fang JY (方精云) (2009) The species-energy hypothesis as a mechanism for species richness patterns.Biodiversity Science(生物多样性), 17, 613-624. (in Chinese with English abstract)
111 Wubet T, Christ S, Schöning I, Boch S, Gawlich M, Schnabel B, Fischer M, Buscot F (2012) Differences in soil fungal communities between European beech (Fagus sylvatica L.) dominated forests are related to soil and understory vegetation.PLoS ONE, 7, e47500.
112 Zhang Y (张宇), Guo LD (郭良栋) (2012) Progress of fungal DNA barcode.Mycosystema(菌物学报), 31, 809-820. (in Chinese with English abstract)
113 Zhu BR (朱璧如), Zhang DY (张大勇) (2011) A process-based theoretical framework for community ecology.Biodiversity Science(生物多样性), 19, 389-399. (in Chinese with English abstract)
114 Zhu Y (祝燕), Mi XC (米湘成), Ma KP (马克平) (2009) A mechanism of plant species coexistence: the negative density-dependent hypothesis.Biodiversity Science(生物多样性), 17, 594-604. (in Chinese with English abstract)
115 Zobel M (1997) The relative of species pools in determining plant species richness: an alternative explanation of species coexistence? Trends in Ecology and Evolution, 12, 266-269.
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[2] . [J]. Chin Bull Bot, 1994, 11(专辑): 70 .
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