Microbial Ecology

, Volume 69, Issue 4, pp 733–747 | Cite as

Responses of Soil Fungi to Logging and Oil Palm Agriculture in Southeast Asian Tropical Forests

  • K. L. McGuire
  • H. D’Angelo
  • F. Q. Brearley
  • S. M. Gedallovich
  • N. Babar
  • N. Yang
  • C. M. Gillikin
  • R. Gradoville
  • C. Bateman
  • B. L. Turner
  • P. Mansor
  • J. W. Leff
  • N. Fierer
Fungal Microbiology

Abstract

Human land use alters soil microbial composition and function in a variety of systems, although few comparable studies have been done in tropical forests and tropical agricultural production areas. Logging and the expansion of oil palm agriculture are two of the most significant drivers of tropical deforestation, and the latter is most prevalent in Southeast Asia. The aim of this study was to compare soil fungal communities from three sites in Malaysia that represent three of the most dominant land-use types in the Southeast Asia tropics: a primary forest, a regenerating forest that had been selectively logged 50 years previously, and a 25-year-old oil palm plantation. Soil cores were collected from three replicate plots at each site, and fungal communities were sequenced using the Illumina platform. Extracellular enzyme assays were assessed as a proxy for soil microbial function. We found that fungal communities were distinct across all sites, although fungal composition in the regenerating forest was more similar to the primary forest than either forest community was to the oil palm site. Ectomycorrhizal fungi, which are important associates of the dominant Dipterocarpaceae tree family in this region, were compositionally distinct across forests, but were nearly absent from oil palm soils. Extracellular enzyme assays indicated that the soil ecosystem in oil palm plantations experienced altered nutrient cycling dynamics, but there were few differences between regenerating and primary forest soils. Together, these results show that logging and the replacement of primary forest with oil palm plantations alter fungal community and function, although forests regenerating from logging had more similarities with primary forests in terms of fungal composition and nutrient cycling potential. Since oil palm agriculture is currently the mostly rapidly expanding equatorial crop and logging is pervasive across tropical ecosystems, these findings may have broad applicability.

References

  1. 1.
    Brooks TM, Mittermeier RA, Mittermeier CG (2002) Habitat loss and extinction in the hotspots of biodiversity. Conserv Biol 16:909–923CrossRefGoogle Scholar
  2. 2.
    Gardner TA, Barlow J, Chazdon R, Ewers RM, Harvey CA, Peres CA, Sodhi NS (2009) Prospects for tropical forest biodiversity in a human-modified world. Ecol Lett 12:561–582CrossRefPubMedGoogle Scholar
  3. 3.
    Dirzo R, Raven PH (2003) Global state of biodiversity and loss. Annu Rev Environ Resour 28:137–167CrossRefGoogle Scholar
  4. 4.
    Asner GP, Rudel TK, Aide TM, Defries R, Emerson R (2009) A contemporary assessment of change in humid tropical forests. Conserv Biol 23:1386–1395CrossRefPubMedGoogle Scholar
  5. 5.
    Gibbs HK, Ruesch AS, Achard F, Clayton MK, Holmgren P, Ramankutty N, Foley JA (2010) Tropical forests were the primary sources of new agricultural land in the 1980s and 1990. Proc Natl Acad Sci U S A 107:16732–16737CrossRefPubMedCentralPubMedGoogle Scholar
  6. 6.
    Tilman D, Fargione J, Wolff B, D’Antonio C, Dobson A, Howarth R, Schindler D, Schlesinger WH, Simberloff D, Swackhamer D (2001) Forecasting agriculturally driven global environmental change. Science 292:281–284CrossRefPubMedGoogle Scholar
  7. 7.
    Perfecto I, Vandermeer J (2008) Biodiversity conservation in tropical agroecosystems—a new conservation paradigm. Ann N Y Acad Sci 1134:173–200CrossRefPubMedGoogle Scholar
  8. 8.
    Uriarte M, Schneider L, Rudel TK (2010) Synthesis: land transitions in the tropics. Biotropica 42:59–62CrossRefGoogle Scholar
  9. 9.
    Dickie IA, Reich PB (2005) Ectomycorrhizal fungal communities at forest edges. J Ecol 93:244–255CrossRefGoogle Scholar
  10. 10.
    Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay RD, Wardle DA, Lindahl BD (2013) Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339:1615–1618CrossRefPubMedGoogle Scholar
  11. 11.
    Waring BG, Averill C, Hawkes CV (2013) Differences in fungal and bacterial physiology alter soil carbon and nitrogen cycling: insights from meta-analysis and theoretical models. Ecol Lett 16:887–894CrossRefPubMedGoogle Scholar
  12. 12.
    Hartmann M, Niklaus PA, Zimmermann S, Schmutz S, Kremer J, Abarenkov K, Luscher P, Widmer F, Frey B (2014) Resistance and resilience of the forest soil microbiome to logging-associated compaction. ISME J 8:226–244CrossRefPubMedCentralPubMedGoogle Scholar
  13. 13.
    Brearley FQ, Thomas AD (in press) Land-use change impacts on soil processes. CABI, WallingfordGoogle Scholar
  14. 14.
    Rodrigues JLM, Pellizari VH, Mueller R, Baek K, Jesus ED, Paula FS, Mirza B, Hamaoui GS, Tsai SM, Feigl B, Tiedje JM, Bohannan BJM, Nusslein K (2013) Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities. Proc Natl Acad Sci U S A 110:988–993CrossRefPubMedCentralPubMedGoogle Scholar
  15. 15.
    Trivedi P, Anderson IC, Singh BK (2013) Microbial modulators of soil carbon storage: integrating genomic and metabolic knowledge for global prediction. Trends Microbiol 21:641–651CrossRefPubMedGoogle Scholar
  16. 16.
    Bridge P, Spooner B (2001) Soil fungi: diversity and detection. Plant Soil 232:147–154CrossRefGoogle Scholar
  17. 17.
    Allen MF, Swenson W, Querejeta JI, Egerton-Warburton LM, Treseder KK (2003) Ecology of mycorrhizae: a conceptual framework for complex interactions among plants and fungi. Annu Rev Phytopathol 41:271–303CrossRefPubMedGoogle Scholar
  18. 18.
    Bell T, Freckleton RP, Lewis OT (2006) Plant pathogens drive density-dependent seedling mortality in a tropical tree. Ecol Lett 9:569–574CrossRefPubMedGoogle Scholar
  19. 19.
    Aime MC, Brearley FQ (2012) Tropical fungal diversity: closing the gap between species estimates and species discovery. Biodivers Conserv 21:2177–2180CrossRefGoogle Scholar
  20. 20.
    Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos J, Moora M, Rillig MC, Stock WD, Tibbett M, Zobel M (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 25:468–478CrossRefPubMedCentralPubMedGoogle Scholar
  21. 21.
    Setala H, McLean MA (2004) Decomposition rate of organic substrates in relation to the species diversity of soil saprophytic fungi. Oecologia 139:98–107CrossRefPubMedGoogle Scholar
  22. 22.
    McGuire KL, Zak DR, Edwards IP, Blackwood CB, Upchurch R (2010) Slowed decomposition is biotically mediated in an ectomycorrhizal, tropical rain forest. Oecologia 164:785–795CrossRefPubMedGoogle Scholar
  23. 23.
    Averill C, Turner BL, Finzi AC (2014) Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505:543-545CrossRefPubMedGoogle Scholar
  24. 24.
    Fierer N, Grandy AS, Six J, Paul EA (2009) Searching for unifying principles in soil ecology. Soil Biol Biochem 41:2249–2256CrossRefGoogle Scholar
  25. 25.
    Fierer N, Leff JW, Adams BJ, Nielsen UN, Bates ST, Lauber CL, Owens S, Gilbert JA, Wall DH, Caporaso JG (2012) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc Natl Acad Sci U S A 109:21390–21395CrossRefPubMedCentralPubMedGoogle Scholar
  26. 26.
    Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120CrossRefPubMedCentralPubMedGoogle Scholar
  27. 27.
    de Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811CrossRefPubMedGoogle Scholar
  28. 28.
    Rousk J, Brookes PC, Baath E (2009) Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl Environ Microbiol 75:1589–1596CrossRefPubMedCentralPubMedGoogle Scholar
  29. 29.
    Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–569CrossRefGoogle Scholar
  30. 30.
    Qin H, Wang HL, Strong PJ, Li YC, Xu QF, Wu QF (2014) Rapid soil fungal community response to intensive management in a bamboo forest developed from rice paddies. Soil Biol Biochem 68:177–184CrossRefGoogle Scholar
  31. 31.
    Hartmann M, Howes CG, Vaninsberghe D, Yu H, Bachar D, Christen R, Henrik Nilsson R, Hallam SJ, Mohn WW (2012) Significant and persistent impact of timber harvesting on soil microbial communities in Northern coniferous forests. ISME J 6:2320–2218CrossRefPubMedCentralGoogle Scholar
  32. 32.
    Falkowski PG, Fenchel T, Delong EF (2008) The microbial engines that drive Earth’s biogeochemical cycles. Science 320:1034–1039CrossRefPubMedGoogle Scholar
  33. 33.
    Hansen MC, Potapov PV, Moore R, Hancher M, Turubanova SA, Tyukavina A, Thau D, Stehman SV, Goetz SJ, Loveland TR, Kommareddy A, Egorov A, Chini L, Justice CO, Townshend JRG (2013) High-resolution global maps of 21st-century forest cover change. Science 342:850–853CrossRefPubMedGoogle Scholar
  34. 34.
    Brearley FQ (2012) Ectomycorrhizal associations of the Dipterocarpaceae. Biotropica 44:637–648CrossRefGoogle Scholar
  35. 35.
    Lee SS, Alexander IJ (1996) The dynamics of ectomycorrhizal infection of Shorea leprosula seedlings in Malaysian rain forests. New Phytol 132:297–305CrossRefGoogle Scholar
  36. 36.
    Alexander I, Ahmad N, Lee SS (1992) The role of mycorrhizas in the regeneration of some Malaysian forest trees. Phil Trans R Soc Lond B Biol Sci 335:379–388CrossRefGoogle Scholar
  37. 37.
    Wilcove DS, Giam X, Edwards DP, Fisher B, Koh LP (2013) Navjot’s nightmare revisited: logging, agriculture, and biodiversity in Southeast Asia. Trends Ecol Evol 28:531–540CrossRefPubMedGoogle Scholar
  38. 38.
    Berry NJ, Phillips OL, Lewis SL, Hill JK, Edwards DP, Tawatao NB, Ahmad N, Magintan D, Khen CV, Maryati M, Ong RC, Hamer KC (2010) The high value of logged tropical forests: lessons from northern Borneo. Biodivers Conserv 19:985–997CrossRefGoogle Scholar
  39. 39.
    Putz FE, Zuidema PA, Synnott T, Pena-Claros M, Pinard MA, Sheil D, Vanclay JK, Sist P, Gourlet-Fleury S, Griscom B, Palmer J, Zagt R (2012) Sustaining conservation values in selectively logged tropical forests: the attained and the attainable. Conserv Lett 5:296–303CrossRefGoogle Scholar
  40. 40.
    Koh LP, Wilcove DS (2008) Is oil palm agriculture really destroying tropical biodiversity? Conserv Lett 1:60–64CrossRefGoogle Scholar
  41. 41.
    Fitzherbert EB, Struebig MJ, Morel A, Danielsen F, Bruhl CA, Donald PF, Phalan B (2008) How will oil palm expansion affect biodiversity? Trends Ecol Evol 23:538–545CrossRefPubMedGoogle Scholar
  42. 42.
    Sodhi NS, Koh LP, Clements R, Wanger TC, Hill JK, Hamer KC, Clough Y, Tscharntke T, Posa MRC, Lee TM (2010) Conserving Southeast Asian forest biodiversity in human-modified landscapes. Biol Conserv 143:2375–2384CrossRefGoogle Scholar
  43. 43.
    Basiron Y (2007) Palm oil production through sustainable plantations. Eur J Lipid Sci Technol 109:289–295CrossRefGoogle Scholar
  44. 44.
    Lee-Cruz L, Edwards DP, Tripathi BM, Adams JM (2013) Impact of logging and forest conversion to oil palm plantations on soil bacterial communities in Borneo. Appl Environ Microbiol 79:7290–7297CrossRefPubMedCentralPubMedGoogle Scholar
  45. 45.
    Treu R (1998) Macrofungi in oil palm plantations of South East Asia. Mycologist 12:10–14CrossRefGoogle Scholar
  46. 46.
    Osemwegie OO, Okhuoya JA (2009) Diversity of macrofungi in oil palm agroforests of Edo State, Nigeria. J Biol Sci 9:584–593CrossRefGoogle Scholar
  47. 47.
    Wilcove DS, Koh LP (2010) Addressing the threats to biodiversity from oil-palm agriculture. Biodivers Conserv 19:999–1007CrossRefGoogle Scholar
  48. 48.
    Okuda T, Suzuki M, Adachi N, Quah ES, Hussein NA, Manokaran N (2003) Effect of selective logging on canopy and stand structure and tree species composition in a lowland dipterocarp forest in peninsular Malaysia. For Ecol Manag 175:297–320CrossRefGoogle Scholar
  49. 49.
    Manokaran N, Seng QE, Ashton PS, Lafrankie JV, Noor NSM, Ahmad WMSW, Okuda T (2004) Pasoh forest dynamics plot, peninsular Malaysia. In: Losos EC, Leigh EG (eds) Tropical forest diversity and dynamism: findings from a large-scale plot network. The University of Chicago Press, Chicago, pp 585–598Google Scholar
  50. 50.
    Adzmi Y, Suhaimi WC, Husni MSA, Ghazali HM, Amir SK, Baillie I (2010) Heterogeneity of soil morphology and hydrology on the 50 ha long-term ecological research plot at Pasoh, Peninsular Malaysia. J Trop For Sci 22:21–35Google Scholar
  51. 51.
    D’Angelo H, McGuire KL, Gillikin CM, Brearley, FQ, Merrer DC (in press) Evaluating the impact of oil palm agriculture and logging on soil microbial communities. In: Brearley, FQ, Thomas, AD (eds.) Land-use change impacts on soil processes. CABI, Wallingford.Google Scholar
  52. 52.
    McGuire KL, Payne SG, Palmer MI, Gillikin CM, Keefe D, Kim SJ, Gedallovich SM, Discenza J, Rangamannar R, Koshner JA, Massmann AL, Orazi G, Essene A, Leff JW, Fierer N (2013) Digging the New York City Skyline: soil fungal communities in green roofs and city parks. PLoS ONE 8(3):e58020CrossRefPubMedCentralPubMedGoogle Scholar
  53. 53.
    Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998Google Scholar
  54. 54.
    Kõljalg U, Larsson K-H, Abarenkov K, Nilsson RH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Vrålstad T, Ursing BM (2005) UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. 166: 1063–1068Google Scholar
  55. 55.
    Abarenkov K, Nilsson RH, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Hoiland K, Kjoller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Ursing BM, Vralstad T, Liimatainen K, Peintner U, Koljalg U (2010) The UNITE database for molecular identification of fungi—recent updates and future perspectives. New Phytol 186:281–285CrossRefPubMedGoogle Scholar
  56. 56.
    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267CrossRefPubMedCentralPubMedGoogle Scholar
  57. 57.
    Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20:217–263CrossRefPubMedGoogle Scholar
  58. 58.
    Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315CrossRefGoogle Scholar
  59. 59.
    German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397CrossRefGoogle Scholar
  60. 60.
    Bryan JE, Shearman PL, Asner GP, Knapp DE, Aoro G, Lokes B (2013) Extreme differences in forest degradation in Borneo: comparing practices in Sarawak, Sabah, and Brunei. PLoS One 8(7):e69679Google Scholar
  61. 61.
    Compton JE, Boone RD (2000) Long-term impacts of agriculture on soil carbon and nitrogen in New England forests. Ecology 81:2314–2330CrossRefGoogle Scholar
  62. 62.
    McLauchlan K (2006) The nature and longevity of agricultural impacts on soil carbon and nutrients: a review. Ecosystems 9:1364–1382CrossRefGoogle Scholar
  63. 63.
    Mattingly WB, Orrock JL (2013) Historic land use influences contemporary establishment of invasive plant species. Oecologia 172:1147–1157CrossRefPubMedGoogle Scholar
  64. 64.
    Brudvig LA, Grman E, Habeck CW, Orrock JL, Ledvina JA (2013) Strong legacy of agricultural land use on soils and understory plant communities in longleaf pine woodlands. For Ecol Manag 310:944–955CrossRefGoogle Scholar
  65. 65.
    Dupouey JL, Dambrine E, Laffite JD, Moares C (2002) Irreversible impact of past land use on forest soils and biodiversity. Ecology 83:2978–2984CrossRefGoogle Scholar
  66. 66.
    Flinn KM, Vellend M (2005) Recovery of forest plant communities in post-agricultural landscapes. Front Ecol Environ 3:243–250CrossRefGoogle Scholar
  67. 67.
    Cleveland CC, Townsend AR, Schmidt SK, Constance BC (2003) Soil microbial dynamics and biogeochemistry in tropical forests and pastures, southwestern Costa Rica. Ecol Appl 13:314–326CrossRefGoogle Scholar
  68. 68.
    Fraterrigo JM, Balser TC, Turner MG (2006) Microbial community variation and its relationship with nitrogen mineralization in historically altered forests. Ecology 87:570–579CrossRefPubMedGoogle Scholar
  69. 69.
    van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, Van de Voorde TFJ, Wardle DA (2013) Plant-soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276CrossRefGoogle Scholar
  70. 70.
    Peay KG, Schubert MG, Nguyen NH, Bruns TD (2012) Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol Ecol 21:4122–4136CrossRefPubMedGoogle Scholar
  71. 71.
    Frankland JC (1998) Fungal succession—unravelling the unpredictable. Mycol Res 102:1–15CrossRefGoogle Scholar
  72. 72.
    Osono T (2007) Ecology of ligninolytic fungi associated with leaf litter decomposition. Ecol Res 22:955–974CrossRefGoogle Scholar
  73. 73.
    de Vries FT, Bloem J, Quirk H, Stevens CJ, Bol R, Bardgett RD (2012) Extensive management promotes plant and microbial nitrogen retention in temperate grassland. PLoS One 7(12):e51201Google Scholar
  74. 74.
    Simpson RJ, Oberson A, Culvenor RA, Ryan MH, Veneklaas EJ, Lambers H, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Richardson AE (2011) Strategies and agronomic interventions to improve the phosphorus-use efficiency of farming systems. Plant Soil 349:89–120CrossRefGoogle Scholar
  75. 75.
    Rosling A, Cox F, Cruz-Martinez K, Ihrmark K, Grelet GA, Lindahl BD, Menkis A, James TY (2011) Archaeorhizomycetes: unearthing an ancient class of ubiquitous soil fungi. Science 333:876–879CrossRefPubMedGoogle Scholar
  76. 76.
    Giam X, Clements GR, Aziz SA, Chong KY, Miettinen J (2011) Rethinking the ‘back to wilderness’ concept for Sundaland’s forests. Biol Conserv 144:3149–3152CrossRefGoogle Scholar
  77. 77.
    Schmidt SK, Wilson KL, Meyer AF, Gebauer MM, King AJ (2008) Phylogeny and ecophysiology of opportunistic “snow molds” from a subalpine forest ecosystem. Microb Ecol 56:681–687CrossRefPubMedGoogle Scholar
  78. 78.
    Neher DA, Weicht TR, Bates ST, Leff JW, Fierer N (2013) Changes in bacterial and fungal communities across compost recipes, preparation methods, and composting times. PLoS One 8(11):e79512Google Scholar
  79. 79.
    Smith ME, Gryganskyi A, Bonito G, Nouhra E, Moreno-Arroyo B, Benny G (2013) Phylogenetic analysis of the genus Modicella reveals an independent evolutionary origin of sporocarp-forming fungi in the Mortierellales. Fungal Genet Biol 61:61–68CrossRefPubMedGoogle Scholar
  80. 80.
    Summerbell RC (2005) Root endophyte and mycorrhizosphere fungi of black spruce, Picea mariana, in a boreal forest habitat: influence of site factors on fungal distributions. Studies in Mycology: 121–145Google Scholar
  81. 81.
    Tedersoo L, Arnold AE, Hansen K (2013) Novel aspects in the life cycle and biotrophic interactions in Pezizomycetes (Ascomycota, Fungi). Mol Ecol 22:1488–1493CrossRefPubMedGoogle Scholar
  82. 82.
    Lavorel S, Garnier E (2002) Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Funct Ecol 16:545–556CrossRefGoogle Scholar
  83. 83.
    Henle K, Davies KF, Kleyer M, Margules C, Settele J (2004) Predictors of species sensitivity to fragmentation. Biodivers Conserv 13:207–251CrossRefGoogle Scholar
  84. 84.
    Hawksworth DL (2012) Global species numbers of fungi: are tropical studies and molecular approaches contributing to a more robust estimate? Biodivers Conserv 21:2425–2433CrossRefGoogle Scholar
  85. 85.
    Ba AM, Duponnois R, Moyersoen B, Diedhiou AG (2012) Ectomycorrhizal symbiosis of tropical African trees. Mycorrhiza 22:1–29CrossRefPubMedGoogle Scholar
  86. 86.
    Smith ME, Henkel TW, Aime MC, Fremier AK, Vilgalys R (2011) Ectomycorrhizal fungal diversity and community structure on three co-occurring leguminous canopy tree species in a Neotropical rainforest. New Phytol 192:699–712CrossRefPubMedGoogle Scholar
  87. 87.
    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. ISME J 4:465–471CrossRefPubMedGoogle Scholar
  88. 88.
    Taylor DL, Bruns TD (1999) Community structure of ectomycorrhizal fungi in a Pinus muricata forest: minimal overlap between the mature forest and resistant propagule communities. Mol Ecol 8:1837–1850CrossRefPubMedGoogle Scholar
  89. 89.
    Peay KG, Kennedy PG, Davies SJ, Tan S, Bruns TD (2010) 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 Phytol 185:529–542CrossRefPubMedGoogle Scholar
  90. 90.
    Phosri C, Polme S, Taylor AFS, Koljalg U, Suwannasai N, Tedersoo L (2012) Diversity and community composition of ectomycorrhizal fungi in a dry deciduous dipterocarp forest in Thailand. Biodivers Conserv 21:2287–2298CrossRefGoogle Scholar
  91. 91.
    Tedersoo L, Smith ME (2013) Lineages of ectomycorrhizal fungi revisited: foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biol Rev 27:83–99CrossRefGoogle Scholar
  92. 92.
    Tedersoo L, Naadel T, Bahram M, Pritsch K, Buegger F, Leal M, Koljalg U, Poldmaa K (2012) Enzymatic activities and stable isotope patterns of ectomycorrhizal fungi in relation to phylogeny and exploration types in an afrotropical rain forest. New Phytol 195:832–843CrossRefPubMedGoogle Scholar
  93. 93.
    Dickie IA, Martinez-Garcia LB, Koele N, Grelet GA, Tylianakis JM, Peltzer DA, Richardson SJ (2013) Mycorrhizas and mycorrhizal fungal communities throughout ecosystem development. Plant Soil 367:11–39CrossRefGoogle Scholar
  94. 94.
    Last FT, Mason PA, Ingleby K, Fleming LV (1984) Succession of fruitbodies of sheathing mycorrhizal fungi associated with Betula pendula. For Ecol Manag 9:229–234CrossRefGoogle Scholar
  95. 95.
    Nara K, Nakaya H, Wu BY, Zhou ZH, Hogetsu T (2003) Underground primary succession of ectomycorrhizal fungi in a volcanic desert on Mount Fuji. New Phytol 159:743–756CrossRefGoogle Scholar
  96. 96.
    Kranabetter JM, Wylie T (1998) Ectomycorrhizal community structure across forest openings on naturally regenerated western hemlock seedlings. Can J Bot-Revue Canadienne De Botanique 76:189–196CrossRefGoogle Scholar
  97. 97.
    Redecker D, Szaro TM, Bowman RJ, Bruns TD (2001) Small genets of Lactarius xanthogalactus, Russula cremoricolor and Amanita francheti in late-stage ectomycorrhizal successions. Mol Ecol 10:1025–1034CrossRefPubMedGoogle Scholar
  98. 98.
    Twieg BD, Durall DM, Simard SW (2007) Ectomycorrhizal fungal succession in mixed temperate forests. New Phytol 176:437–447CrossRefPubMedGoogle Scholar
  99. 99.
    Pickles BJ, Genney DR, Potts JM, Lennon JJ, Anderson IC, Alexander IJ (2010) Spatial and temporal ecology of Scots pine ectomycorrhizas. New Phytol 186:755–768CrossRefPubMedGoogle Scholar
  100. 100.
    Lilleskov EA, Bruns TD, Horton TR, Taylor DL, Grogan P (2004) Detection of forest stand-level spatial structure in ectomycorrhizal fungal communities. FEMS Microbiol Ecol 49:319–332CrossRefPubMedGoogle Scholar
  101. 101.
    Sinsabaugh RL, Carreiro MM, Alvarez S (2002) Enzyme and microbial dynamics of litter dynamics. In: Burns RG, Dick RP (eds) Enzymes in the environment: activity, ecology, and applications. Marcel Dekker, New York 249–265Google Scholar
  102. 102.
    Sinsabaugh RL, Moorhead DL (1994) Resource-allocation to extracellular enzyme-production—a model for nitrogen and phosphorus control of litter decomposition. Soil Biol Biochem 26:1305–1311CrossRefGoogle Scholar
  103. 103.
    Courty PE, Buee M, Diedhiou AG, Frey-Klett P, Le Tacon F, Rineau F, Turpault MP, Uroz S, Garbaye J (2010) The role of ectomycorrhizal communities in forest ecosystem processes: new perspectives and emerging concepts. Soil Biol Biochem 42:679–698CrossRefGoogle Scholar
  104. 104.
    Hanson CA, Allison SD, Bradford MA, Wallenstein MD, Treseder KK (2008) Fungal taxa target different carbon sources in forest soil. Ecosystems 11:1157–1167CrossRefGoogle Scholar
  105. 105.
    McGuire KL, Bent E, Borneman J, Majumder A, Allison SD, Treseder KK (2010) Functional diversity in resource use by fungi. Ecology 91:2324–2332CrossRefPubMedGoogle Scholar
  106. 106.
    Allison SD, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci U S A 105:11512–11519CrossRefPubMedCentralPubMedGoogle Scholar
  107. 107.
    Sodhi NS, Lee TM, Koh LP, Brook BW (2009) A meta-analysis of the impact of anthropogenic forest disturbance on Southeast Asia’s biotas. Biotropica 41:103–109CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • K. L. McGuire
    • 1
    • 2
  • H. D’Angelo
    • 2
  • F. Q. Brearley
    • 3
  • S. M. Gedallovich
    • 1
  • N. Babar
    • 1
  • N. Yang
    • 1
  • C. M. Gillikin
    • 1
  • R. Gradoville
    • 4
  • C. Bateman
    • 1
  • B. L. Turner
    • 5
  • P. Mansor
    • 6
  • J. W. Leff
    • 7
  • N. Fierer
    • 7
    • 8
  1. 1.Department of BiologyBarnard College of Columbia UniversityNew YorkUSA
  2. 2.Department of Ecology, Evolution and Environmental BiologyColumbia UniversityNew YorkUSA
  3. 3.School of Science and the EnvironmentManchester Metropolitan UniversityManchesterUK
  4. 4.College of Earth, Ocean, and Atmospheric SciencesOregon State UniversityCorvallisUSA
  5. 5.Smithsonian Tropical Research InstituteBalboaRepublic of Panama
  6. 6.Forest Research Institute MalaysiaKuala LumpurMalaysia
  7. 7.Department of Ecology and Evolutionary BiologyUniversity of Colorado, BoulderBoulderUSA
  8. 8.Cooperative Institute for Research in Environmental SciencesUniversity of ColoradoBoulderUSA

Personalised recommendations