The production and turnover of extramatrical mycelium of ectomycorrhizal fungi in forest soils: Role in carbon cycling

Plant and Soil

Volumn 366, Issue 1-2, 2013, Pages 1-27

  Ekblad, A ^a   Wallander, H ^b   Godbold, D L ^c   Cruz, C ^d   Johnson, D ^e   Baldrian, P ^f   Bjork R G ^a,g   Epron, D ^h   Kieliszewska Rokicka, B ⁱ   Kjoller R ^j   Kraigher, H ^k   Matzner, E ^l   Neumann, J ^l   Plassard, C ^m  

^a ÖREBRO UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^d UNIVERSITY OF LISBON   (Portugal)

^e UNIVERSITY OF ABERDEEN   (United Kingdom)

^f INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^g UNIVERSITY OF GOTHENBURG   (Sweden)

^h UNIVERSITÉ DE LORRAINE   (France)

ⁱ KAZIMIERZ WIELKI UNIVERSITY   (Poland)

^j UNIVERSITY OF COPENHAGEN   (Denmark)

^k SLOVENIAN FORESTRY INSTITUTE   (Slovenia)

^l UNIVERSITY OF BAYREUTH   (Germany)

^m UMR ECO SOLS   (France)

more..

Author keywords

Decomposition; Exploration type; Extramatrical mycelium; In growth bag; Minirhizotron; Rhizomorphs; Soil organic matter; Turnover rates

Indexed keywords

BIOMASS; CARBON CYCLE; ECTOMYCORRHIZA; FOREST SOIL; FUNGUS; SOIL BIOTA; SOIL ORGANIC MATTER;

SCANDINAVIA;

FUNGI; PICEA ABIES;

EID: 84874034964     PISSN: 0032079X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11104-013-1630-3     Document Type: Review

References (218)

1. Abuzinadah RA, Read DJ (1986) The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. I. Utilization of proteins and peptides by ectomycorrhizal fungi. New Phytol 103: 481-493.
2. Agerer R (2001) Exploration types of ectomycorrhizae. A proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11: 107-114.
3. Agerer R, Rambold G (2004-2011) [first posted on 2004-06-01; most recent update: 2011-01-10]. DEEMY - An Information System for Characterization and Determination of Ectomycorrhizae. www. deemy. de - München, Germany.
4. Alberton O, Kuyper TW (2009) Ectomycorrhizal fungi associated with Pinus sylvestris seedlings respond differently to increased carbon and nitrogen availability: implications for ecosystem responses to global change. Glob Change Biol 15: 166-175.
5. 2. New Phytol 167: 859-868.
6. Allen MF (2007) Mycorrhizal Fungi: highways for water and nutrients in arid soils. Vadose Zone J 6: 291-297.
7. Alvarez M, Gieseke A, Godoy R, Hartel S (2006) Surface-bound phosphatase activity in ectomycorrhizal fungi: a comparative study between a colorimetric and a microscope-based method. Biol Fertil Soils 42: 561-568.
8. Arnebrant K (1994) Nitrogen amendments reduce the growth of ectramatrical mycelium. Mycorrhiza 5: 7-15.
9. Bååth E, Nilsson LO, Göransson H, Wallander H (2004) Can the extent of degradation of soil fungal mycelium during soil incubation be used to estimate ectomycorrhizal biomass in soil? Soil Biol Biochem 36: 2105-2109.
10. Bakker MR, Jolicoeur E, Trichet P, Augusto L, Plassard C, Guinberteau J, Loustau D (2009) Adaptation of fine roots to annual fertilization and irrigation in a 13-year-old Pinus pinaster stand. Tree Physiol 29: 229-238.
11. Baldrian P (2009) Ectomycorrhizal fungi and their enzymes in soils: is there enough evidence for their role as facultative soil saprotrophs? Oecologia 161: 657-660.
12. Bending GD, Read DJ (1995) The structure and function of the vegetative mycelium of ectomycorrhizal plants V. Foraging behaviour and translocation of nutrients from exploited litter. New Phytol 130: 401-409.
13. Bengtsson G, Erlandsson A, Rundgren S (1988) Fungal odour attracts soil Collembola. Soil Biol Biochem 20: 25-30.
14. Bengtsson G, Hedlund K, Rundgren S (1991) Selective odor perception in the soil Collembola Onychiurus armatus. J Chem Ecol 17: 2113-2125.
15. Berg B, Lindberg T (1980) Is litter decomposition retarded in the presence of mycorrhizal roots in forest soil? Swedish Coniferous Forest Project, Department of Ecology and Environmental Research, Swedish University of Agricultural Sciences. Internal Rep 95: 10 pp.
16. Berggren Kleja D, Svensson M, Majdi H, Jansson P-E, Langvall O, Bergkvist B, Johansson MB, Weslien P, Truusb L, Lindroth A, Ågren GI (2008) Pools and fluxes of carbon in three Norway spruce ecosystems along a climatic gradient in Sweden. Biogeochem 89: 7-25.
17. Bhupinderpal-Singh NA, Ottosson-Löfvenius M, Högberg MN, Mellander P-E, Högberg P (2003) Tree root and soil heterotrophic respiration as revealed by girdling of boreal Scots pine forest: extending observations beyond the first year. Plant Cell Environ 26: 1287-1296.
18. Bidartondo MI, Ek H, Wallander H, Söderström B (2001) Do nutrient additions alter carbon sink strength of ectomycorrhizal fungi? New Phytol 151: 543-550.
19. Böllmann J, Elmer M, Wöllecke J, Raidl S, Hüttl RF (2010) Defensive strategies of soil fungi to prevent grazing by Folsomia candida (Collembola). Pedobiol 53: 107-114.
20. 13C enrichment in soil profiles during the decomposition of soil organic matter. Oecologia 153: 89-98.
21. Brunner I, Bakker M, Björk R, Hirano Y, Lukac M, Aranda X, Børja I, Eldhuset T, Helmisaari H, Jourdan C, Konôpka B, López B, Miguel Pérez C, Persson H, Ostonen I (2012) Fine-root turnover rates of European forests revisited: an analysis of data from sequential coring and ingrowth cores. Plant Soil. doi: 10. 1007/s11104-012-1313-5.
22. Cairney JWG (2011) Ectomycorrhizal fungi: the symbiotic route to the root for phosphorus in forest soils. Plant Soil 344: 51-71.
23. Cairney JWG (2012) Extramatrical mycelia of ectomycorrhizal fungi as moderators of carbon dynamics in forest soil. Soil Biol Biochem 47: 198-208.
24. Caldwell MM, Dawson TE, Richards JH (1998) Hydraulic lift: consequences of water efflux from the roots of plants. Oecologia 113: 151-161.
25. Chapin FS III, McFarland J, McGuire AD, Euskirchen ES, Ruess RW, Kielland K (2009) The changing global carbon cycle: linking plant-soil carbon dynamics to global consequences. J Ecol 97: 840-850.
26. Clemmensen KE, Michelsen A, Jonasson S, Shaver GR (2006) Increased ectomycorrhizal fungal abundance after long-term fertilization and warming of two arctic tundra ecosystems. New Phytol 171: 391-404.
27. Colpaert JV, van Laere A, van Assche JA (1996) Carbon and nitrogen allocation in ectomycorrhizal and non-mycorrhizal Pinus sylvestris L. seedlings. Tree Physiol 16: 787-793.
28. Courty P-E, Bréda N, Garbaye J (2007) Relation between oak tree phenology and the secretion of organic matter degrading enzymes by Lactarius quietus ectomycorrhizas before and during bud break. Soil Biol Biochem 39: 1655-1663.
29. Courty P-E, Buée M, Diedhiou AG, Frey-Klett P, Le Tacon F, Rineau F, Turpault M-P, Uroz S, Garbaye J (2010) The role of ectomycorrhizal communities in forest ecosystem processes: New perspectives and emerging concepts. Soil Biol Biochem 42: 679-698.
30. Coutts MP, Nicholl BC (1990) Growth and survival of shoots, roots and mycorrhizal mycelium in clonal Sitka spruce during the first growing season after planting. Can J For Res 20: 861-868.
31. Cromack K Jr, Sollins P, Grausttein WC, Speidel K, Todd AW, Spycher G, Li CY, Todd RL (1979) Calcium oxalate accumulation and soil weathering in mats of the hypogeous fungus Hysterangium crassum. Soil Biol Biochem 11: 463-468.
32. Cullings K, Courty P-E (2009) Saprotrophic capabilities as functional traits to study functional diversity and resilience of ectomycorrhizal community. Oecologia 161: 661-664.
33. Cullings K, Vogler DR, Parker VT, Makhija S (2001) Defoliation effects on the community of a mixed Pinus contorta/Picea engelmannii stand in Yellowstone Park. Oecologia 127: 533-539.
34. Cullings K, Ishkhanova G, Henson J (2008) Defoliation effects on enzyme activities of the ectomycorrhizal fungus Suillus granulatus in a Pinus contorta (lodgepole pine) stand in Yellowstone National Park. Oecologia 158: 77-83.
35. Dahlberg A (2001) Community ecology of ectomycorrhizal fungi: an advancing interdisciplinary field. New Phytol 150: 555-562.
36. Dahlberg A, Stenlid J (1994) Size, distribution and biomass of genets in populations of Suillus bovinus (L.: Fr.) Roussel revealed by somatic incompatibility. New Phytol 128: 225-234.
37. 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: 795-811.
38. De Grandcourt A, Epron D, Montpied P, Louisanna E, Béreau M, Garbaye J, Guehl J-M (2004) Contrasting responses to mycorrhizal inoculation and phosphorus availability in seedlings of two tropical rainforest tree species. New Phytol 161: 865-875.
39. Dickie IA, Xu W, Koide RT (2002) Vertical niche differentiation of ectomycorrhizal hyphae in soils as shown by T-RFLP analysis. New Phytol 156: 527-535.
40. Donnelly DP, Boddy L, Leake JR (2004) Development, persistence and regeneration of foraging ectomycorrhizal mycelial systems in soil microcosms. Mycorrhiza 14: 37-45.
41. Duddridge JA, Malibari A, Read DJ (1980) Structure and function of mycorrhizal rhizomorphs with special reference to their role in water transport. Nature 287: 834-836.
42. Ehleringer JR, Buchmann N, Flanagan LB (2000) Carbon isotope ratios in belowground carbon cycle processes. Ecol Appl 10: 412-422.
43. Ek H (1997) The influence of nitrogen fertilization on the carbon economy of Paxillus involutus in ectomycorrhizal association with Betula pendula. New Phytol 135: 133-142.
44. Ek H, Sjögren M, Arnebtant K, Söderström B (1994) Extramatrical mycelial growth, biomass allocation and nitrogen uptake in ectomycorrhizal systems in response to collembolan grazing. Appl Soil Ecol 1: 155-169.
45. Ekblad A, Näsholm T (1996) Determination of chitin in fungi and mycorrhizal roots by an improved HPLC analysis of glucosamine. Plant Soil 178: 29-35.
46. Ekblad A, Wallander H, Carlsson R, HussDanell K (1995) Fungal biomass in roots and extramatrical mycelium in relation to macronutrients and plant biomass of ectomycorrhizal Pinus sylvestris and Alnus incana. New Phytol 131: 443-451.
47. Ekblad A, Wallander H, Näsholm T (1998) Chitin and ergosterol combined to measure total and living fungal biomass in ectomycorrhizas. New Phytol 138: 143-149.
48. 2 pulse labelling of trees. Biogeosci Discuss 8: 885-919.
49. Fernandez CW, Koide RT (2012) The role of chitin in the decomposition of ectomycorrhizal fungal litter. Ecology 93: 24-28.
50. Finér L, Ohashi M, Noguchi K, Hirano Y (2011) Fine root production and turnover in forest ecosystems in relation to stand and environmental characteristics. For Ecol Manage 262: 2008-2023.
51. Finlay RD (2008) Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot 59: 1115-1126.
52. 14C-labelled carbon between plants interconnected by a common mycelium. New Phytol 103: 143-156.
53. Finlay R, Söderström B (1992) Mycorrhiza and carbon flow to the soil. In: Allen MF (ed) Mycorrhizal functioning: an integrative plant-fungal process. Chapman and Hall, Routledge, pp 134-162.
54. Fitter AH (1991) Costs and benefits of mycorrhizas: implications for functioning under natural conditions. Experientia 47: 350-355.
55. Fitter AH, Sanders IR (1992) Interactions with the soil fauna. In: Allen MF (ed) Mycorrhizal functioning: an integrative plant-fungal process. Chapman and Hall, Routledge, pp 333-354.
56. Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35: 837-843.
57. 2 alters root symbiont community structure in forest trees. New Phytol 152: 431-442.
58. 2. Mycorrhiza 15: 25-31.
59. Frey-Klett P, Chavatte M, Clausse ML, Courrier S, Le Roux C, Raaijmakers J, Martinotti MG, Pierrat JC, Garbaye J (2005) Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads. New Phytol 165: 317-328.
60. Gadgil RL, Gadgil PD (1975) Suppression of litter decomposition by mycorrhizal roots of Pinus radiata. New Zealand J For Sci 5: 33-41.
61. 2 and nitrogen fertilization in a warm temperate forest. Plant Soil 303: 301-310.
62. Gebauer G, Schulze ED (1991) Carbon and nitrogen isotope ratios in different compartments of a healthy and a declining Picea-abies forest in the Fichtelgebirge, Ne Bavaria. Oecologia 87: 198-207.
63. Gehring CA, Whitham TG (2002) Mycorrhizae-Herbivore interactions: population and community consequences. In: van der Heijden MGA, Sanders I (eds) Mycorrhizal ecology, ecological studies, Vol. 157. Springer, pp 295-320.
64. Genney DR, Anderson IC, Alexander IJ (2006) Fine-scale distribution of pine ectomycorrhizas and their extramatrical mycelium. New Phytol 170: 381-390.
65. Giesler R, Högberg MN, Strobel BW, Richter A, Nordgren A, Högberg P (2007) Production of dissolved organic carbon and low-molecular weight organic acids in soil solution driven by recent tree photosynthate. Biogeochem 84: 1-12.
66. Gill RA, Jackson RB (2000) Global patterns of root turnover for terrestrial ecosystems. New Phytol 147: 13-31.
67. Gleixner G (2005) Stable isotope composition of soil organic matter. In: Flanagan LB, Ehleringer JR, Pataki DE (eds) Stable isotopes and biosphere-atmosphere interactions: processes and biological controls. Academic, London, pp 29-46.
68. Gleixner G, Bol R, Balesdent J (1999) Molecular insight into soil carbon turnover. Rapid Commun Mass Spectrom 13: 1278-1283.
69. Gleixner G, Poirier N, Bol R, Balesdent J (2002) Molecular dynamics of organic matter in a cultivated soil. Org Geochem 33: 357-366.
70. 2. New Phytol 137: 433-440.
71. Godbold DL, Hoosbeek MR, Lukac M, Cotrufo MF, Janssens IA, Ceulemans R, Polle A, Velthorst EJ, Scarascia-Mugnozza G, De Angelis P, Miglietta F, Peressotti A (2006) Mycorrhizal turnover as a dominant process for carbon input into soil organic matter. Plant Soil 281: 15-24.
72. 2]. New Phytol 146: 163-168.
73. Grebenc T, Kraigher H (2007) Changes in the community of ectomycorrhizal fungi and increased fine root number under adult beech trees chronically fumigated with double ambient ozone concentration. Plant Biol (Stuttg) 9: 279-287.
74. Griffiths RP, Baham JE, Caldwell BA (1994) Soil solution chemistry of ectomycorrhizal mats in forest soil. Soil Biol Biochem 26: 331-337.
75. Hagerberg D, Wallander H (2002) The impact of forest residue removal and wood ash amendment on the growth of the ectomycorrhizal external mycelium. FEMS Microbiol Ecol 39: 139-146.
76. Hagerberg D, Thelin G, Wallander H (2003) The production of ectomycorrhizal mycelium in forests: Relation between forest nutrient status and local mineral sources. Plant Soil 252: 279-290.
77. Harley JL (1989) The significance of mycorrhizal. Mycol Res 92: 129-139.
78. 2 flux: uncovering the contribution and environmental responses of ectomycorrhizas. Glob Chang Biol 13: 1786-1797.
79. 2 fluxes and individual mycorrhizosphere components to photosynthesis. Biogeosciences Discuss 8: 3155-3201.
80. Hendricks JJ, Mitchell RJ, Kuehn KA, Pecot SD, Sims SE (2006) Measuring external mycelia production of ectomycorrhizal fungi in the field: the soil matrix matters. New Phytol 171: 179-186.
81. Hobbie EA (2006) Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology 87: 563-569.
82. Hobbie EA, Agerer R (2010) Nitrogen isotopes in ectomycorrhizal mushrooms correspond to belowground exploration types. Plant Soil 327: 71-83.
83. Hodge A, Fitter AH (2010) Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc Natl Acad Sci USA 107: 13754-13759.
84. Hodge A, Alexander IJ, Gooday GW (1995) Chitinolytic enzymes of pathogenic and ectomycorrhizal fungi. Mycol Res 99: 935-941.
85. Hodge A, Helgason T, Fitter AH (2010) Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecol 3: 267-273.
86. Högberg MN, Högberg P (2002) Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phytol 154: 791-795.
87. 15N abundance of surface soils, roots and mycorrhizas in profiles of European forest soils. Oecologia 108: 207-214.
88. Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Löfvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411: 789-792.
89. Högberg MN, Bååth E, Nordgren A, Arnebrant K, Högberg P (2003) Contrasting effects of nitrogen availability on plant carbon supply to mycorrhizal fungi and saprotrophs - a hypothesis based on field observations in boreal forests. New Phytol 160: 225-238.
90. Högberg MN, Briones MJI, Keel SG, Metcalfe DB, Campbell C, Midwood AJ, Thornton B, Hurry V, Linder S, Näsholm T, Högberg P (2010) Quantification of effects of season and nitrogen supply on tree below-ground carbon transfer to ectomycorrhizal fungi and other soil organisms in a boreal pine forest. New Phytol 187: 485-493.
91. Högberg P, Johannisson C, Yarwood S, Callesen I, Näsholm T, Myrold DD, Högberg M (2011) Recovery of ectomycorrhiza after 'nitrogen saturation' of a conifer forest. New Phytol 189: 515-525.
92. Hopkin SP (1997) Biology of the Springtails: (Insecta: Collembola). Oxford Univ. Press, Oxford.
93. Hughes JK, Hodge A, Fitter AH, Atkin OK (2008) Mycorrhizal respiration: implications for global scaling relationships. Trends Plant Sci 13: 583-588.
94. Ingham ER, Griffiths RP, Cromack K, Entry JA (1991) Comparison of direct vs fumigation incubation microbial biomass estimates from ectomycorrhizal mat and non-mat soils. Soil Biol Biochem 23: 465-471.
95. Jaatinen K, Laiho R, Vuorenmaa A, del Castillo U, Minkkinen K, Pennanen T, Penttila T, Fritze H (2008) Responses of aerobic microbial communities and soil respiration to water-level drawdown in a northern boreal fen. Environ Microbiol 10: 339-353.
96. Jentschke G, Godbold DL, Brandes B (2001) Nitrogen limitation in mycorrhizal Norway spruce (Picea abies) seedlings induced mycelial foraging for ammonium: implications for Ca and Mg uptake. Plant Soil 234: 109-117.
97. 2. Soil Biol Biochem 41: 1111-1116.
98. Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185: 631-647.
99. 2 pulse labelling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhizal mycelia to the soil. New Phytol 153: 327-334.
100. Johnson D, Krsek M, Wellington EMH, Stott AW, Cole L, Bardgett RD, Read DJ, Leake JR (2005) Soil invertebrates disrupt carbon flow through fungal networks. Science 309: 1047.
101. Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163: 459-480.
102. Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321: 5-33.
103. Kalbitz K, Solinger S, Park J-H, Michalzik B, Matzner E (2000) Controls on the dynamics of dissolved organic matter in soils: A review. Soil Sci 165: 277-304.
104. Kalliokoski T, Pennanen T, Nygren P, Sievänen R, Helmisaari H-S (2010) Belowground interspecific competition in mixed boreal forests: fine root and ectomycorrhiza characteristics along stand developmental stage and soil fertility gradients. Plant Soil 330: 73-89.
105. Kaneda S, Kaneko N (2004) The feeding preference of a collembolan (Folsomia candida Willem) on ectomycorrhiza (Pisolithus tinctorius (Pers.)) varies with mycelial growth condition and vitality. Appl Soil Ecol 27: 1-5.
106. Kårén O, Nylund J-E (1997) Effects of ammonium sulphate on the community structure and biomass of ectomycorrhizal fungi in a Norway spruce stand in southwestern Sweden. Can J Bot 75: 1628-1642.
107. 3 levels during three growing seasons. Glob Chang Biol 11: 1167-1179.
108. Kimmins JP (2004) Forest Ecology, a foundation for sustainable forest management and environmental ethics in forestry. Prentice Hall, Upper Saddle River.
109. Kjöller R (2006) Disproportionate abundance between ectomycorrhizal root tips and their associated mycelia. FEMS Microbiol Ecol 58: 214-224.
110. Klironomos JN, Hart MM (2001) Animal nitrogen swap for plant carbon. Nature 410: 651-652.
111. Kluber LA, Tinnesand KM, Caldwell BA, Dunhamd SM, Yarwood RR, Bottomley PJ, Myrold DD (2010) Ectomycorrhizal mats alter forest soil biogeochemistry. Soil Biol Biochem 42: 1607-1613.
112. Koide RT, Malcolm GM (2009) N concentration controls decomposition rates of different strains of ectomycorrhizal fungi. Fungal Ecol 2: 197-202.
113. Koide RT, Wu T (2003) Ectomycorrhizas and retarded decomposition in a Pinus resinosa plantation. New Phytol 158: 401-407.
114. Koide RT, Fernandez CW, Peoples MS (2011) Can ectomycorrhizal colonization of Pinus resinosa roots affect their decomposition? New Phytol 191: 508-514.
115. Korkama T, Fritze H, Pakkanen A, Pennanen T (2007) Interactions between extraradical ectomycorrhizal mycelia, microbes associated with the mycelia and growth rate of Norway spruce (Picea abies) clones. New Phytol 173: 798-807.
116. Kraigher H, Grebenc T, Hanke DE (2008) Ozone stress and ectomycorrhizal root-shoot signalling. In: Varma A (ed) Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematic, 3rd edn. Springer, Berlin, pp 337-357.
117. Krauss J, Funke W (1999) Extraordinary high density of Protura in a windfall area of young spruce stands. Pedobiol 43: 44-46.
118. Kuzyakov Y, Friedel JK, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32: 1485-1498.
119. Landeweert R, Hoffland E, Finlay RD, Kuyper TW, van Breemen N (2001) Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals. Trends Ecol Evol 16: 248-254.
120. Landeweert R, Leeflang P, Kuyper TW, Hoffland E, Rosling A, Wernars K, Smit E (2003) Molecular identification of ectomycorrhizal mycelium in soil horizons. Appl Environ Microbiol 69: 327-333.
121. Langley JA, Hungate BA (2003) Mycorrhizal controls on belowground litter quality. Ecology 84: 2302-2312.
122. Langley JA, Chapman SK, Hungate BA (2006) Ectomycorrhizal colonization slows root decomposition, the post-mortem fungal legacy. Ecol Lett 9: 955-959.
123. Last FT, Dighton J, Mason PA (1987) Successions of sheathing mycorrhizal fungi. Trends Ecol Evol 2: 157-161.
124. Lawrynowicz M, Falinski JB, Bober J (2006) Interactions among hypogeous fungi wild boars in the subcontinental pine forest. Biodivers Res Conserv 1-2: 102-106.
125. 14C pulse labeling of Pinus sylvestris seedlings: effects of litter patches and interaction with a wood-decomposer fungus. Tree Physiol 21: 71-82.
126. Leake J, Johnson D, Donnelly D, Muckle G, Boddy L, Read D (2004) Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can J Bot 82: 1016-1045.
127. 2 pulse-labelling in an upland grassland. Appl Soil Ecol 33: 152-175.
128. Lilleskov EA, Bruns TD, Dawson TE, Camacho FJ (2009) Water sources and controls on water-loss rates of epigeous ectomycorrhizal fungal sporocarps during summer drought. New Phytol 182: 483-494.
129. Lindahl BD, Taylor AFS (2004) Occurrence of N-acetylhexosaminidase-encoding genes in ectomycorrhizal basidiomycetes. New Phytol 164: 193-199.
130. Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173: 611-620.
131. Lindahl BD, de Boer W, Finlay RD (2010) Disruption of root carbon transport into forest humus stimulates fungal opportunists at the expense of mycorrhizal fungi. ISME J 4: 872-881.
132. Litton CM, Raich JW, Ryan MG (2007) Carbon allocation in forest ecosystems. Glob Chang Biol 13: 2089-2109.
133. Lussenhop J, Fogel R (1999) Seasonal change in phosphorus content of Pinus strobus - Cenococcum geophilum ectomycorrhizae. Mycologia 91: 742-746.
134. MacArthur RH, Pianka ER (1966) On optimal use of a patchy environment. Am Nat 100: 603-609.
135. Majdi H, Truus L, Johansson U, Nylund JE, Wallander H (2008) Effects of slash retention and wood ash addition on fine root biomass and production and ectomycorrhizal mycelium in a Norway spruce stand in SW Sweden. For Ecol Manage 255: 2109-2117.
136. Malmström A, Persson T (2011) Responses of Collembola and Protura to tree girdling - some support for ectomycorrhizal feeding. Soil Org 83: 279-285.
137. Markkola A, Kuikka K, Rautio P, Härmä E, Roitto M, Tuomi J (2004) Defoliation increases carbon limitation in ectomycorrhizal symbiosis of Betula pubescens. Oecologia 140: 234-240.
138. Martin F, Selosse MA (2008) The Laccaria genome: a symbiont blueprint decoded. New Phytol 180: 296-310.
139. Massei G, Genov PV (2004) The environmental impact of wild boar. Galemys 16: 135-145.
140. Meyer A, Grote R, Polle A, Butterbach-Bahl K (2010) Simulating mycorrhiza contribution to forest C- and N cycling-the MYCOFON model. Plant Soil 327: 493-517.
141. Moyano FE, Kutsch WL, Rebmann C (2008) Soil respiration fluxes in relation to photosynthetic activity in broad-leaf and needle-leaf forest stands. Agr For Meteorol 148: 135-143.
142. Nadelhoffer KJ (2000) The potential effects of nitrogen deposition on fine-root production in forest ecosystems. New Phytol 147: 131-139.
143. Näsholm T, Nordin A, Edfast A-B, Högberg P (1997) Identification of coniferous forests with incipient nitrogen saturation through analysis of arginine and nitrogen-15 abundance of trees. J Environ Qual 26: 302-309.
144. Nilsson LO, Wallander H (2003) The production of external mycelium by ectomycorrhizal fungi in a Norway spruce forest was reduced in response to nitrogen fertilization. New Phytol 158: 409-416.
145. Nilsson LO, Giesler R, Bååth E, Wallander H (2005) Growth and biomass of mycorrhizal mycelia in coniferous forests along short natural nutrient gradients. New Phytol 165: 613-622.
146. Nilsson LO, Bååth E, Falkengren-Grerup U, Wallander H (2007) Growth of ectomycorrhizal mycelia and composition of soil microbial communities in oak forest soils along a nitrogen deposition gradient. Oecologia 153: 375-384.
147. Nilsson LO, Wallander H, Gundersen P (2012) Changes in microbial activities and biomasses over a forest floor gradient in C-to-N ratio. Plant Soil 355: 75-86.
148. Nygren CMR, Edqvist J, Elfstrand M, Heller G, Taylor AFS (2007) Detection of extracellular protease activity in different species and genera of ectomycorrhizal fungi. Mycorrhiza 17: 241-248.
149. Nylund J-E, Wallander H (1992) Ergosterol analysis as a means of quantifying mycorrhizal biomass. In: Norris JR, Read DJ, Varma AK (eds) Methods in microbiology vol 24. Academic, London, pp 77-88.
150. 2 and nitrogen fertilization. New Phytol 176: 164-174.
151. 2-enrichment and nutrient availability alter ectomycorrhizal fungal communities. Ecology 87: 2278-2287.
152. Pass G, Szucsich NU (2011) 100 years of research on the Protura: many secrets still retained. Soil Organisms 83: 309-334.
153. Pastor J, Naiman RJ (1992) Selective foraging and ecosystem processes in boreal forests. Am Nat 139: 690-705.
154. Perez-Moreno J, Read DJ (2000) Mobilization and transfer of nutrients from litter to tree seedlings via the vegetative mycelium of ectomycorrhizal plants. New Phytol 145: 301-309.
155. Persson T (1989) Role of soil animals in C and N mineralisation. Plant Soil 115: 241-245.
156. Persson I-L, Danell K, Bergström R (2000) Disturbance by large herbivores in boreal forests with special reference to moose. Ann Zool Fenn 37: 251-263.
157. Plassard C, Louche J, Ali MA, Duchemin M, Legname E, Cloutier-Hurteau B (2011) Diversity in phosphorus mobilisation and uptake in ectomycorrhizal fungi. Ann For Sci 68: 33-43.
158. Potila H, Wallander H, Sarjala T (2009) Growth of ectomycorrhizal fungi in drained peatland forests with variable P and K availability. Plant Soil 316: 139-150.
159. 2-enrichment. Glob Chang Biol 14: 1-13.
160. Querejeta JI, Egerton WLM, Allen MF (2003) Direct nocturnal water transfer from oaks to their mycorrhizal symbionts during severe soil drying. Oecologia 134: 55-64.
161. Querejeta JI, Egerton-Warbrton LM, Allen MF (2007) Hydraulic lift may buffer rhizosphere hyphae against the negative effects of severe soil drying in a California Oak savanna. Soil Biol Biochem 39: 409-417.
162. Read DJ (1992) The mycorrhizal mycelium. In: Allen MF (ed) Mycorrhizal functioning. Chapman and Hall, London, pp 102-133.
163. Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance? New Phytol 157: 475-492.
164. Remén C, Persson T, Finlay R, Ahlström K (2008) Responses of oribatid mites to tree girdling and nutrient addition in boreal coniferous forests. Soil Biol Biochem 40: 2881-2890.
165. Remén C, Fransson P, Persson T (2010) Population responses of oribatids and enchytraeids to ectomycorrhizal and saprotrophic fungi in plant-soil microcosms. Soil Biol Biochem 42: 978-985.
166. Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171: 41-53.
167. Rosling A (2009) Trees, mycorrhiza and minerals - field relevance of in vitro experiments. Geomicrobiol J 26: 389-401.
168. Rosling A, Landeweert R, Lindahl BD, Larsson K-H, Kuyper TW, Taylor AFS, Finlay RD (2003) Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile. New Phytol 159: 775-783.
169. Rosling A, Lindahl BD, Finlay RD (2004) Carbon allocation to ectomycorrhizal roots and mycelium colonising different mineral substrates. New Phytol 162: 795-802.
170. Rousseau JVD, Sylvia DM, Fox AJ (1994) Contribution of ectomycorrhiza to the potential nutrient-absorbing surface of pine. New Phytol 128: 639-644.
171. Saikkonen K, Ahonen-Jonnarth U, Markkola AM, Helander M, Tuomi J, Roitto M, Ranta H (1999) Defoliation and mycorrhizal symbiosis: a functional balance between carbon sources and below-ground sinks. Ecol Lett 2: 19-26.
172. Saravesi K, Markkola AM, Rautio P, Roitto M, Tuomi J (2008) Defoliation causes parallel temporal responses in a host tree and its fungal symbionts. Oecologia 156: 117-123.
173. Schmalholz M, Hylander K (2009) Succession of bryophyte assemblages following clear-cut logging in boreal southern-central Sweden - Does retrogressive succession occur? Can J For Res 39: 1871-1880.
174. Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478: 49-56.
175. Setälä H (1995) Growth of birch and pine seedlings in relation to grazing by soil fauna on ectomycorrhizal fungi. Ecology 76: 1844-1851.
176. Setälä H (2000) Reciprocal interactions between Scots pine and soil food web structure in the presence and absence of ectomycorrhiza. Oecologia 125: 109-118.
177. Setälä H, Kulmala P, Mikola J, Makkola AM (1999) Influence of ectomycorrhiza on the structrue of detrital food webs in pine rhizosphere. Oikos 87: 113-122.
178. Shaw PJA (1988) Aconsistent hierarchy in the fungal feeding preferences of the Collembola Onychiurus armatus. Pedobiol 31: 3-4.
179. Simard SW (2009) The foundational role of mycorrhizal networks in self-organization of interior Douglas-fir forests. For Ecol Manage 258: 95-107.
180. Sims SE, Hendricks JJ, Mitchell RJ, Kuehn KA, Pecot SD (2007) Nitrogen decreases and precipitation increases ectomycorrhizal extramatrical mycelia production in a longleaf pine forest. Mycorrhiza 17: 299-309.
181. Smith SE, Read DJ (2008) Mycorrhizal Symbiosis 3rd edn. Academic, London.
182. Söderström B (1979) Seasonal fluctuations of active fungal biomass in horizons of a podzolized pine-forest soil in central Sweden. Soil Biol Biochem 11: 149-154.
183. Söderström B, Read DJ (1987) Respiratory activity of intact and excised ectomycorrhizal mycelial systems growing in unsterilized soil. Soil Biol Biochem 19: 231-236.
184. Spiteller P (2008) Chemical defence strategies of higher fungi. Chem Eur J 14: 9100-9110.
185. Stadler M, Sterner O (1998) Production of bioactive secondary metabolites in the fruit bodies of macrofungi as a response to injury. Phytochem 49: 1013-1019.
186. Steinman K, Siegwolf RTW, Saurer M, Körner C (2004) Carbon fluxes to the soil in a mature temperate forest assessed by 13C isotope tracing. Oecologia 141: 489-501.
187. Stenström E (1991) The effects of flooding on the formation of ectomycorrhizae in Pinus sylvestris seedlings. Plant Soil 131: 247-250.
188. Talbot JM, Allison SD, Treseder KK (2008) Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct Ecology 22: 955-963.
189. Tamm C-O (1991) Nitrogen in terrestrial ecosystems. Springer, Berlin.
190. Taylor AFS, Alexander I (2005) The ectomycorrhizal symbiosis: life in the real world. Mycologist 19: 102-112.
191. Tedersoo L, Kõljalg U, Hallenberg N, Larsson K-H (2003) Fine scale distribution of ectomycorrhizal fungi and roots across substrate layers including coarse woody debris in a mixed forest. New Phytol 159: 153-165.
192. Thelin G, Sverdrup H, Holmqvist J, Rosengren U, Lindén M (2002) Assessment of nutrient sustainability in Norway spruce and mixed Norway spruce-oak stands at Jämjö. In: Svedrup H, Stjernquist I (eds) Developing principles for sustainable forestry in southern Sweden. Kluwer, Dordrecht, pp 337-354.
193. 2 in field studies. New Phytol 164: 347-355.
194. Treseder KK, Allen MF (2000) Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition. New Phytol 147: 189-200.
195. Treseder KK, Allen MF, Ruess RW, Pregitzer KS, Hendrick RL (2005) Lifespans of fungal rhizomorphs under nitrogen fertilization in a pinyon-juniper woodland. Plant Soil 270: 249-255.
196. Treseder KK, Torn MS, Masiello CA (2006) An ecosystem-scale radiocarbon tracer to test use of litter carbon by ectomycorrhizal fungi. Soil Biol Biochem 38: 1077-1082.
197. 14C-labelled lignin, holocellulose and lignocellulose by mycorrhizal fungi. Archives Microbiol 139: 202-206.
198. Tsantrizos YS, Kope HH, Fortin JA, Ogilvie KK (1991) Antifungal antibiotics from Pisolithus tinctorius. Phytochem 30: 1113-1118.
199. Unestam T (1991) Water repellency, mat formation, and leaf stimulated growth of some ectomycorrhizal fungi. Mycorrhiza 1: 13-20.
200. Unestam T, Sun Y-P (1995) Extramatrical structures of hydrophobic and hydrophilic ectomycorrhizal fungi. Mycorrhiza 5: 301-311.
201. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 69-72.
202. van Schöll L, Kuyper T, Smits M, Landeweert R, Hoffland E, Breemen N (2008) Rock-eating mycorrhizas: their role in plant nutrition and biogeochemical cycles. Plant Soil 303: 35-47.
203. Vargas R, Allen MF (2008) Dynamics of fine root, fungal rhizomorphs, and soil respiration in a mixed temperate forest: integrating sensors and observations. Vadose Zone J 7: 1055-1064.
204. Wallander H (1995) A new hypothesis to explain allocation of dry matter between ectomycorrhizal fungi and pine seedlings. Plant Soil 168-169: 243-248.
205. Wallander H, Nylund J-E (1992) Effects of excess nitrogen and phosphorus starvation on the extramatrical mycelium of ectomycorrhizas of Pinus sylverstris L. New Phytol 120: 495-503.
206. Wallander H, Pallon J (2005) Temporal changes in the elemental composition of Rhizopogon rhizomorphs during colonization of patches with fresh organic matter or acid-washed sand. Mycologia 97: 295-303.
207. Wallander H, Thelin G (2008) The stimulating effect of apatite on ectomycorrhizal growth diminish after PK fertilization. Soil Biol Biochem 40: 2517-2522.
208. Wallander H, Nilsson LO, Hagerberg D, Bååth E (2001) Estimation of the biomass and production of external mycelium of ectomycorrhizal fungi in the field. New Phytol 151: 753-760.
209. Wallander H, Nilsson LO, Hagerberg D, Rosengren U (2003) Direct estimates of C: N ratios of ectomycorrhizal mycelia collected from Norway spruce forest soils. Soil Biol Biochem 35: 997-999.
210. 13C in ectomycorrhizal mycelia collected at different soil depths in two forest types. Oecologia 139: 89-97.
211. Wallander H, Johansson U, Sterkenburg E, Brandström M, Lindahl B (2010) Production of ectomycorrhizal mycelium peaks during canopy closure in Norway spruce forests. New Phytol 187: 1124-1134.
212. Wallander H, Ekblad A, Bergh J (2011) Growth and carbon sequestration by ectomycorrhizal fungi in intensively fertilized Norway spruce forests. For Ecol Manage 262: 999-1007.
213. Wallander H, Ekblad A, Godbold DL, Johnson D, Bahr A, Baldrian P, Björk RG, Kieliszewska-Rokicka B, Kjøller R, Kraigher H, Plassard C, Rudawska M (2013) Evaluation of methods to estimate production, biomass and turnover of ectomycorrhizal mycelium in forests soils - A review. Soil Biol Biochem 57: 1034-1042.
214. Warren JM, Brooks JR, Meinzer FC, Eberhart JL (2008) Hydraulic redistribution of water from Pinus ponderosa trees to seedlings: evidence for an ectomycorrhizal pathway. New Phytol 178: 382-394.
215. Weigt RB, Raidl S, Verma R, Rodenkirchen H, Göttlein A, Agerer R (2011) Effects of twice-ambient carbon dioxide and nitrogen amendment on biomass, nutrient contents and carbon costs of Norway spruce seedlings as influenced by mycorrhization with Piloderma croceum and Tomentellopsis submollis. Mycorrhiza 21: 375-391.
216. Wiklund K, Nilsson L-O, Jacobsson S (1995) Effect of irrigation, fertilization, and artificial drought on basidioma production in a Norway spruce stand. Can J Bot 73: 200-208.
217. 2 efflux under laboratory conditions. Soil Biol Biochem 43: 1355-1355.
218. Wu T (2011) Can ectomycorrhizal fungi circumvent the nitrogen mineralization for plant nutrition in temperate forest ecosystems? Soil Biol Biochem 43: 1109-1117.