1932

Abstract

The niche is generally viewed in terms of species' intrinsic physiological potential and limitations due to competition. Although DNA sequencing has revealed the ubiquity of beneficial microbial symbioses, the role of mutualisms in shaping species niches is not broadly recognized. In this review, I use a widespread terrestrial mutualism, the ectomycorrhizal symbiosis, to help develop the mutualistic niche concept. Using contemporary niche theory, I show how mycorrhizal symbioses expand environmental ranges (requirement niche) and influence resource use (impact niche) for both plants and fungi. Simple niche models for competition between resource specialists and generalists also predict a range of ecological phenomena, from unexpected monodominance by some tropical trees to the functional biogeography of mycorrhizal symbiosis. A niche-based view of mutualism may also help explain stability of mutualisms even in the absence of clear benefits. The niche is a central concept in ecology, and better integration of mutualism will more accurately reflect the positive interactions experienced by nearly all species.

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2016-11-01
2024-03-29
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Literature Cited

  1. Aerts R. 2002. The role of various types of mycorrhizal fungi in nutrient cycling and plant competition. Mycorrhizal Ecology MGA van der Heijden, IR Sanders New York: Springer [Google Scholar]
  2. Afkhami ME, McIntyre PJ, Strauss SY. 2014. Mutualist-mediated effects on species' range limits across large geographic scales. Ecol. Lett. 17:1265–73 [Google Scholar]
  3. Anderson IC, Genney DR, Alexander IJ. 2014. Fine-scale diversity and distribution of ectomycorrhizal fungal mycelium in a Scots pine forest. New Phytol 201:1423–30 [Google Scholar]
  4. Averill C, Turner BL, Finzi AC. 2014. Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505:543–45 [Google Scholar]
  5. Baraloto C, Rabaud S, Molto Q, Blanc L, Fortunel C. et al. 2011. Disentangling stand and environmental correlates of aboveground biomass in Amazonian forests. Glob. Change Biol. 17:2677–88 [Google Scholar]
  6. Bertness MD, Callaway R. 1994. Positive interactions in communities. Trends Ecol. Evol. 9:191–93 [Google Scholar]
  7. Bever JD. 2002. Negative feedback within a mutualism: Host-specific growth of mycorrhizal fungi reduces plant benefit. Proc. R. Soc. B 269:2595–601 [Google Scholar]
  8. Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos J. et al. 2010. Rooting theories of plant community ecology in microbial interactions. Trends Ecol. Evol. 25:468–78 [Google Scholar]
  9. Boucher DH, James S, Keeler KH. 1982. The ecology of mutualism. Annu. Rev. Ecol. Syst. 13:315–47 [Google Scholar]
  10. Bougher NL, Grove TR, Malajczuk N. 1990. Growth and phosphorous acquisition of karri (Eucalyptus diversicolor F. Muell.) seedlings inoculated with ectomycorrhizal fungi in relation to phosphorous supply. New Phytol 114:77–85 [Google Scholar]
  11. Brundrett MC. 2009. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77 [Google Scholar]
  12. Bruno JF, Stachowicz JJ, Bertness MD. 2003. Inclusion of facilitation into ecological theory. Trends Ecol. Evol. 18:119–25 [Google Scholar]
  13. Bruns TD, Bidartondo MI, Taylor DL. 2002. Host specificity in ectomycorrhizal communities: What do the exceptions tell us. Integr. Comp. Biol. 42:352–59 [Google Scholar]
  14. Bruns TD, Peay KG, Boynton PJ, Grubisha LC, Hynson NA. et al. 2009. Inoculum potential of Rhizopogon spores increases with time over the first four years of a 99-year spore burial experiment. New Phytol 181:463–70 [Google Scholar]
  15. Bruns TD, Shefferson RP. 2004. Evolutionary studies of ectomycorrhizal fungi: recent advances and future directions. Can. J. Bot. 82:1122–32 [Google Scholar]
  16. Chase JM, Leibold MA. 2003. Ecological Niches: Linking Classical and Contemporary Approaches Chicago: Univ. Chicago Press
  17. Chase JM, Leibold MA, Simms E. 2000. Plant tolerance and resistance in food webs: community-level predictions and evolutionary implications. Evol. Ecol. 14:289–314 [Google Scholar]
  18. Chesson P. 2000. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31:343–66 [Google Scholar]
  19. Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A. et al. 2013. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339:1615–18 [Google Scholar]
  20. Collier FA, Bidartondo MI. 2009. Waiting for fungi: the ectomycorrhizal invasion of lowland heathlands. J. Ecol. 97:950–63 [Google Scholar]
  21. Connell JH, Lowman MD. 1989. Low-diversity tropical rainforests: some possible mechanisms for their existence. Am. Nat. 134:88–119 [Google Scholar]
  22. Corrales A, Mangan SA, Turner BL, Dalling JW. 2016. An ectomycorrhizal nitrogen economy facilitates monodominance in a neotropical forest. Ecol. Lett. 19:383–92 [Google Scholar]
  23. Courty PE, Buee M, Diedhiou AG, Frey-Klett P, Le Tacon F. et al. 2010. The role of ectomycorrhizal communities in forest ecosystem processes: new perspectives and emerging concepts. Soil Biol. Biochem. 42:679–98 [Google Scholar]
  24. Courty PE, Pritsch K, Schloter M, Hartmann A, Garbaye J. 2005. Activity profiling of ectomycorrhiza communities in two forest soils using multiple enzymatic tests. New Phytol 167:309–19 [Google Scholar]
  25. Cowles HC. 1899. The ecological relations of the vegetation on the sand dunes of Lake Michigan. Bot. Gaz. 27:95–117, 167–202, 281–308, 361–391 [Google Scholar]
  26. De Bary A. 1879. Die Erscheinung der Symbiose Strasburg: Karl J. Trubner
  27. de Mazancourt C, Schwartz MW. 2010. A resource ratio theory of cooperation. Ecol. Lett. 13:349–59 [Google Scholar]
  28. Dickie IA, Koele N, Blum JD, Gleason JD, McGlone MS. 2014. Mycorrhizas in changing ecosystems. Botany 92:149–60 [Google Scholar]
  29. Dickie IA, Koide RT, Fayish AC. 2001. Vesicular–arbuscular mycorrhizal infection of Quercus rubra seedlings. New Phytol 151:257–64 [Google Scholar]
  30. Dickie IA, Martínez-García LB, Koele N, Grelet GA, Tylianakis JM. et al. 2013. Mycorrhizas and mycorrhizal fungal communities throughout ecosystem development. Plant Soil 367:11–39 [Google Scholar]
  31. Dickie IA, Reich PB. 2005. Ectomycorrhizal fungal communities at forest edges. J. Ecol. 93:244–55 [Google Scholar]
  32. Dickie IA, Xu B, Koide RT. 2002. Vertical niche differentiation of ectomycorrhizal hyphae in soil as shown by T-RFLP analysis. New Phytol 156:527–35 [Google Scholar]
  33. Elias M, Gompert Z, Jiggins C, Willmott K. 2008. Mutualistic interactions drive ecological niche convergence in a diverse butterfly community. PLOS Biol 6:2642–49 [Google Scholar]
  34. Elton C. 1927. Animal Ecology London: Sidgwick & Jackson
  35. Falkowski PG, Fenchel T, Delong EF. 2008. The microbial engines that drive Earth's biogeochemical cycles. Science 320:1034–39 [Google Scholar]
  36. Fernandez CW, Kennedy PG. 2015. Revisiting the ‘Gadgil effect’: Do interguild fungal interactions control carbon cycling in forest soils. New Phytol 209:1382–94 [Google Scholar]
  37. Field KJ, Rimington WR, Bidartondo MI, Allinson KE, Beerling DJ. et al. 2015. First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO2. New Phytol 205:743–56 [Google Scholar]
  38. Finlay RD. 1989. Functional aspects of phosphorous uptake and carbon translocation in incompatible ectomycorrhizal associations between Pinussylvestris and Suillus grevillei and Boletinus cavipes. New Phytol 112:185–92 [Google Scholar]
  39. Frank A. 2005. On the nutritional dependence of certain trees on root symbiosis with belowground fungi (an English translation of A.B. Frank's classic paper of 1885). Mycorrhiza 15:267–75 [Google Scholar]
  40. Franklin O, Nasholm T, Hogberg P, Hogberg MN. 2014. Forests trapped in nitrogen limitation–an ecological market perspective on ectomycorrhizal symbiosis. New Phytol 203:657–66 [Google Scholar]
  41. Friesen ML, Porter SS, Stark SC, von Wettberg EJ, Sachs JL, Martinez-Romero E. 2011. Microbially mediated plant functional traits. Annu. Rev. Ecol. Evol. Syst. 42:23–46 [Google Scholar]
  42. Fukami T. 2015. Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu. Rev. Ecol. Evol. Syst. 46:1–23 [Google Scholar]
  43. Gadgil RL, Gadgil PD. 1971. Mycorrhiza and litter decomposition. Nature 233:133 [Google Scholar]
  44. Garcia K, Delaux PM, Cope KR, Ane JM. 2015. Molecular signals required for the establishment and maintenance of ectomycorrhizal symbioses. New Phytol 208:79–87 [Google Scholar]
  45. Grinnell J. 1917. The niche-relationships of the California thrasher. Auk 34:427–33 [Google Scholar]
  46. Güsewell S. 2004. N : P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–66 [Google Scholar]
  47. Hargreaves AL, Samis KE, Eckert CG. 2014. Are species' range limits simply niche limits writ large? A review of transplant experiments beyond the range. Am. Nat. 183:157–73 [Google Scholar]
  48. Hayward J, Horton TR, Pauchard A, Nunez MA. 2015. A single ectomycorrhizal fungal species can enable a Pinus invasion. Ecology 96:1438–44 [Google Scholar]
  49. Heil GW, Diemont WH. 1983. Raised nutrient levels change heathland into grassland. Vegetatio 53:113–20 [Google Scholar]
  50. Hodge A, Fitter AH, Robinson D. 2013. Microbial mediation of plant competition and community structure. Funct. Ecol. 27:865–75 [Google Scholar]
  51. Hoeksema JD, Chaudhary VB, Gehring C, Johnson NC, Karst J. et al. 2010. A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol. Lett. 13:394–407 [Google Scholar]
  52. Hoeksema JD, Piculell BJ, Thompson JN. 2009. Within-population genetic variability in mycorrhizal interactions. Commun. Integr. Biol. 2:110–12 [Google Scholar]
  53. Holland JN, Wang Y, Sun S, DeAngelis DL. 2013. Consumer–resource dynamics of indirect interactions in a mutualism–parasitism food web module. Theor. Ecol. 6:475–93 [Google Scholar]
  54. Holt RD. 2009. Bringing the Hutchinsonian niche into the 21st century: ecological and evolutionary perspectives. PNAS 106:Suppl 219659–65 [Google Scholar]
  55. Horton TR, Bruns TD. 2001. The molecular revolution in ectomycorrhizal ecology: peeking into the black-box. Mol. Ecol. 10:1855–71 [Google Scholar]
  56. Horton TR, Bruns TD, Parker VT. 1999. Ectomycorrhizal fungi associated with Arctostaphylos contribute to Pseudotsuga menziesii establishment. Can. J. Bot 77:93–102 [Google Scholar]
  57. Hutchinson GE. 1957. Concluding remarks. Cold Spring Harb. Symp. 22:415–27 [Google Scholar]
  58. Ishida TA, Nara K, Hogetsu T. 2007. Host effects on ectomycorrhizal fungal communities: insight from eight host species in mixed conifer-broadleaf forests. New Phytol 174:430–40 [Google Scholar]
  59. Janzen DH. 1970. Herbivores and the number of tree species in tropical forests. Am. Nat. 104:501–28 [Google Scholar]
  60. Johnson NC, Wilson GW, Bowker MA, Wilson JA, Miller RM. 2010. Resource limitation is a driver of local adaptation in mycorrhizal symbioses. PNAS 107:2093–98 [Google Scholar]
  61. Kazenel MR, Debban CL, Ranelli L, Hendricks WQ, Chung YA. et al. 2015. A mutualistic endophyte alters the niche dimensions of its host plant. AoB Plants 7:plv005 [Google Scholar]
  62. Kennedy P. 2010. Ectomycorrhizal fungi and interspecific competition: species interactions, community structure, coexistence mechanisms, and future research directions. New Phytol 187:895–910 [Google Scholar]
  63. Kennedy PG, Higgins LM, Rogers RH, Weber MG. 2011. Colonization-competition tradeoffs as a mechanism driving successional dynamics in ectomycorrhizal fungal communities. PLOS ONE 6:e25126 [Google Scholar]
  64. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O. et al. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–82 [Google Scholar]
  65. Klironomos JN. 2003. Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–301 [Google Scholar]
  66. Koele N, Dickie IA, Blum JD, Gleason JD, de Graaf L. 2014. Ecological significance of mineral weathering in ectomycorrhizal and arbuscular mycorrhizal ecosystems from a field-based comparison. Soil Biol. Biochem. 69:63–70 [Google Scholar]
  67. Kohler A, Kuo A, Nagy LG, Morin E, Barry KW. et al. 2015. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat. Genet. 47:410–15 [Google Scholar]
  68. Koide RT, Fernandez C, Malcolm G. 2014. Determining place and process: functional traits of ectomycorrhizal fungi that affect both community structure and ecosystem function. New Phytol 201:433–39 [Google Scholar]
  69. Koide RT, Kabir Z. 2001. Nutrient economy of red pine is affected by interactions between Pisolithus tinctorius and other forest-floor microbes. New Phytol 150:179–88 [Google Scholar]
  70. Koide RT, Shumway DL, Xu B, Sharda JN. 2007. On temporal partitioning of a community of ectomycorrhizal fungi. New Phytol 174:420–29 [Google Scholar]
  71. Koide RT, Wu T. 2003. Ectomycorrhizas and retarded decomposition in a Pinus resinosa plantation. New Phytol 158:401–7 [Google Scholar]
  72. Kummel M, Salant SW. 2006. The economics of mutualisms: optimal utilization of mycorrhizal mutualistic partners by plants. Ecology 87:892–902 [Google Scholar]
  73. Kuzyakov Y, Xu X. 2013. Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–69 [Google Scholar]
  74. Lankau RA, Keymer DP. 2016. Ectomycorrhizal fungal richness declines towards the host species' range edge. Mol. Ecol. 25:3224–41 [Google Scholar]
  75. Leake JR, Johnson D, Donnelly DP, Muckle GE, Boddy L, Read DJ. 2004. Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can. J. Bot. 82:1016–45 [Google Scholar]
  76. Lindahl BD, Tunlid A. 2015. Ectomycorrhizal fungi—potential organic matter decomposers, yet not saprotrophs. New Phytol 205:1443–47 [Google Scholar]
  77. MacArthur RH. 1958. Population ecology of some warblers of northeastern coniferous forests. Ecology 4:599–619 [Google Scholar]
  78. MacArthur RH. 1972. Geographical Ecology New York: Harper and Row
  79. Marquez LM, Redman RS, Rodriguez RJ, Roossinck MJ. 2007. A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315:513–15 [Google Scholar]
  80. McGuire K. 2007. Common ectomycorrhizal networks may maintain monodominance in a tropical rain forest. Ecology 88:567–74 [Google Scholar]
  81. McGuire KL, Henkel TW, de la Cerda IG, Villa G, Edmund F, Andrew C. 2008. Dual mycorrhizal colonization of forest-dominating tropical trees and the mycorrhizal status of non-dominant tree and liana species. Mycorrhiza 18:217–22 [Google Scholar]
  82. McKane RB, Johnson LC, Rastetter EB, Fry B, Giblin AE. et al. 2002. Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415:68–71 [Google Scholar]
  83. Miller TE, Burns JH, Munguia P, Walters EL, Kneitel JM. et al. 2005. A critical review of twenty years' use of the resource-ratio theory. Am. Nat. 165:439–48 [Google Scholar]
  84. Moeller HV, Neubert MG. 2016. Multiple friends with benefits: an optimal mutualist management strategy. Am. Nat. 187:E1–12 [Google Scholar]
  85. Mujic AB, Durall DM, Spatafora JW, Kennedy PG. 2016. Competitive avoidance not edaphic specialization drives vertical niche partitioning among sister species of ectomycorrhizal fungi. New Phytol 209:1174–83 [Google Scholar]
  86. Nara K, Hogetsu T. 2004. Ectomycorrhizal fungi on established shrubs facilitate subsequent seedling establishment of successional plant species. Ecology 85:1700–7 [Google Scholar]
  87. Nasholm T, Hogberg P, Franklin O, Metcalfe D, Keel SG. et al. 2013. Are ectomycorrhizal fungi alleviating or aggravating nitrogen limitation of tree growth in boreal forests. New Phytol 198:214–21 [Google Scholar]
  88. Nehls U, Grunze N, Willmann M, Reich M, Kuster H. 2007. Sugar for my honey: carbohydrate partitioning in ectomycorrhizal symbiosis. Phytochemistry 68:82–91 [Google Scholar]
  89. Nunez MA, Horton TR, Simberloff D. 2009. Lack of belowground mutualisms hinders Pinaceae invasions. Ecology 90:2352–59 [Google Scholar]
  90. Opik M, Metsis M, Daniell TJ, Zobel M, Moora M. 2009. Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest. New Phytol 184:424–37 [Google Scholar]
  91. Orwin KH, Kirschbaum MU, St John MG, Dickie IA. 2011. Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a model-based assessment. Ecol. Lett. 14:493–502 [Google Scholar]
  92. Partida-Martinez LP, Hertweck C. 2005. Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437:884–88 [Google Scholar]
  93. Parton WJ, Silver WL, Burke I, Grassens L, Harmon ME. et al. 2007. Global-scale similarities in nitrogen release patterns during long-term decomposition. Science 315:361–64 [Google Scholar]
  94. Peay KG, Bruns TD. 2014. Spore dispersal of basidiomycete fungi at the landscape scale is driven by stochastic and deterministic processes and generates variability in plant–fungal interactions. New Phytol 204:180–91 [Google Scholar]
  95. Peay KG, Bruns TD, Kennedy PG, Bergemann SE, Garbelotto M. 2007. A strong species–area relationship for eukaryotic soil microbes: Island size matters for ectomycorrhizal fungi. Ecol. Lett. 10:470–80 [Google Scholar]
  96. Peay KG, Garbelotto M, Bruns TD. 2010. Evidence of dispersal limitation in soil microorganisms: Isolation reduces species richness on mycorrhizal tree islands. Ecology 91:3631–40 [Google Scholar]
  97. Peay KG, Russo SE, McGuire KL, Lim Z, Chan JP. et al. 2015. Lack of host specificity leads to independent assortment of dipterocarps and ectomycorrhizal fungi across a soil fertility gradient. Ecol. Lett. 18:807–16 [Google Scholar]
  98. Peay KG, Schubert MG, Nguyen NH, Bruns TD. 2012. Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol. Ecol. 21:4122–36 [Google Scholar]
  99. Phillips RP, Brzostek E, Midgley MG. 2013. The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests. New Phytol 199:41–51 [Google Scholar]
  100. Potts MD, Ashton PS, Kaufman LS, Plotkin JB. 2002. Habitat patterns in tropical rain forests: a comparison of 105 plots in northwest Borneo. Ecology 83:2782–97 [Google Scholar]
  101. Pryor LD. 1956. Ectotrophic mycorrhiza in Reantherous species of Eucalyptus. Nature 177:587–88 [Google Scholar]
  102. Pulliam HR. 2000. On the relationship between niche and distribution. Ecol. Lett. 3:349–61 [Google Scholar]
  103. Querejeta JI, Egerton-Warburton LM, Allen MF. 2003. Direct nocturnal water transfer from oaks to their mycorrhizal symbionts during severe soil drying. Oecologia 134:55–64 [Google Scholar]
  104. Read DJ. 1991. Mycorrhizas in ecosystems. Experientia 47:376–91 [Google Scholar]
  105. Redecker D, Kodner R, Graham LE. 2000. Glomalean fungi from the Ordovician. Science 289:1920–21 [Google Scholar]
  106. 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 10:1025–34 [Google Scholar]
  107. Rich S, Boucher D. 1976. What ecologists look for. Bull. Ecol. Soc. Am. 57:8–9 [Google Scholar]
  108. Rineau F, Shah F, Smits MM, Persson P, Johansson T. et al. 2013. Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus. ISME J 7:2010–22 [Google Scholar]
  109. Robinson D, Fitter AH. 1999. The magnitude and control of carbon transfer between plants linked by a common mycorrhizal network. J. Exp. Bot. 50:9–13 [Google Scholar]
  110. Rusca TA, Kennedy PG, Bruns TD. 2006. The effect of different pine hosts on the sampling of Rhizopogon spore banks in five Eastern Sierra Nevada forests. New Phytol 170:551–60 [Google Scholar]
  111. Schwartz MW, Hoeksema JD. 1998. Specialization and resource trade: biological markets as a model of mutualisms. Ecology 79:1029–38 [Google Scholar]
  112. Shah F, Nicolas C, Bentzer J, Ellstrom M, Smits M. et al. 2016. Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors. New Phytol 209:1705–19 [Google Scholar]
  113. Simard SW, Perry DA, Jones MD, Myrold DD, Durall DM, Molina R. 1998. Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388:579–82 [Google Scholar]
  114. Smith SE, Read DJ. 2008. Mycorrhizal Symbiosis San Francisco: Elsevier
  115. Steidinger BS, Turner BL, Corrales A, Dalling JW, Briones MJ. 2014. Variability in potential to exploit different soil organic phosphorus compounds among tropical montane tree species. Funct. Ecol. 29:121–30 [Google Scholar]
  116. Talbot JM, Allison SD, Treseder KK. 2008. Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct. Ecol. 22:955–63 [Google Scholar]
  117. Talbot JM, Bruns TD, Taylor JW, Smith DP, Branco S. et al. 2014. Endemism and functional convergence across the North American soil mycobiome. PNAS 111:6431–46 [Google Scholar]
  118. Talbot JM, Martin F, Kohler A, Henrissat B, Peay KG. 2015. Functional guild classification predicts the enzymatic role of fungi in litter and soil biogeochemistry. Soil Biol. Biochem. 88:441–56 [Google Scholar]
  119. Taylor DL, Hollingsworth TN, McFarland JW, Lennon NJ, Nusbaum C, Ruess RW. 2014. A first comprehensive census of fungi in soil reveals both hyperdiversity and fine-scale niche partitioning. Ecol. Monogr. 84:3–20 [Google Scholar]
  120. Tedersoo L, Bahram M, Põlme S, Kõljalg U, Yorou NS. et al. 2014. Global diversity and geography of soil fungi. Science 346:1256688 [Google Scholar]
  121. 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 4:465–71 [Google Scholar]
  122. Terrer C, Vicca S, Hungate BA, Phillips RP, Prentice IC. 2016. Mycorrhizal association as a primary control of the CO2 fertilization effect. Science 353:6294–95 [Google Scholar]
  123. Tilman D. 1976. Ecological competition between algae: experimental confirmation of resource-based competition theory. Science 192:463–65 [Google Scholar]
  124. Tilman D. 1980. A graphical-mechanistic approach to competition and predation. Am. Nat. 116:362–93 [Google Scholar]
  125. Tilman D. 1982. Resource Competition and Community Structure Princeton, NJ: Princeton Univ. Press
  126. Toju H, Yamamoto S, Sato H, Tanabe AS. 2013. Sharing of diverse mycorrhizal and root-endophytic fungi among plant species in an oak-dominated cool–temperate forest. PLOS ONE 8:e78248 [Google Scholar]
  127. Torti SD, Coley PD, Kursar TA. 2001. Causes and consequences of monodominance in tropical lowland forests. Am. Nat. 2:141–53 [Google Scholar]
  128. Turnbull MH, Goodall R, Stewart GR. 1995. The impact of mycorrhizal colonization upon nitrogen source utilization and metabolism in seedlings of Eucalyptus grandis Hill ex Maiden and Eucalyptus maculata Hook. Plant Cell Environ 18:1386–94 [Google Scholar]
  129. van der Heijden MGA. 2002. Arbuscular mycorrhizal fungi as a determinant of plant diversity: in search for underlying mechanisms and general principles. Mycorrhizal Ecology MGA van der Heijden, IR Sanders 243–65 New York: Springer [Google Scholar]
  130. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R. et al. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72 [Google Scholar]
  131. van der Heijden MGA, Martin FM, Selosse MA, Sanders IR. 2015. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–23 [Google Scholar]
  132. Voriskova J, Brabcova V, Cajthaml T, Baldrian P. 2014. Seasonal dynamics of fungal communities in a temperate oak forest soil. New Phytol 201:269–78 [Google Scholar]
  133. Vozzo JA, Hacskaylo E. 1974. Endo- and ectomycorrhizal associations in five Populus species. Bull. Torrey Bot. Club 101:182–86 [Google Scholar]
  134. Vralstad T, Schumacher T, Taylor AFS. 2002. Mycorrhizal synthesis between fungal strains of the Hymenoscyphus ericae aggregate and potential ectomycorrhizal and ericoid hosts. New Phytol 153:143–52 [Google Scholar]
  135. Wagg C, Jansa J, Stadler M, Schmid B, van der Heijden MGA. 2011. Mycorrhizal fungal identity and diversity relaxes plant-plant competition. Ecology 92:1303–13 [Google Scholar]
  136. Walker JK, Cohen H, Higgins LM, Kennedy PG. 2014. Testing the link between community structure and function for ectomycorrhizal fungi involved in a global tripartite symbiosis. New Phytol 202:287–96 [Google Scholar]
  137. Wallander H, Nilsson LO, Hagerberg D, Baath E. 2001. Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. New Phytol 151:753–60 [Google Scholar]
  138. Wallenda T, Read DJ. 1999. Kinetics of amino acid uptake by ectomycorrhizal roots. Plant Cell Environ 22:179–87 [Google Scholar]
  139. Waring BG, Adams R, Branco S, Powers JS. 2016. Scale-dependent variation in nitrogen cycling and soil fungal communities along gradients of forest composition and age in regenerating tropical dry forests. New Phytol 209:845–54 [Google Scholar]
  140. Warren RJ, Giladi I, Bradford MA. 2010. Ant-mediated seed dispersal does not facilitate niche expansion. J. Ecol. 98:1178–85 [Google Scholar]
  141. Warren RJ, Giladi I, Bradford MA, Flynn D. 2014. Competition as a mechanism structuring mutualisms. J. Ecol. 102:486–95 [Google Scholar]
  142. Weber A, Karst J, Gilbert B, Kimmins JP. 2005. Thuja plicata exclusion in ectomycorrhiza-dominated forests: testing the role of inoculum potential of arbuscular mycorrhizal fungi. Oecologia 143:148–56 [Google Scholar]
  143. Werner GD, Kiers ET. 2015. Order of arrival structures arbuscular mycorrhizal colonization of plants. New Phytol 205:1515–24 [Google Scholar]
  144. West SA, Griffin AS, Gardner A. 2007. Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J. Evol. Biol. 20:415–32 [Google Scholar]
  145. Whittaker RH. 1956. Vegetation of the Great Smoky Mountains. Ecol. Monogr. 26:1–80 [Google Scholar]
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