New Forests

, Volume 38, Issue 2, pp 157–175 | Cite as

Ectomycorrhizal communities within beech (Fagus sylvatica L.) forests that naturally regenerate from clear-cutting in northern Spain

  • Nieves Goicoechea
  • Iván Closa
  • Ana María de Miguel


The objectives of the work described here were to evaluate the diversity of ectomycorrhizal (ECM) fungi within Spanish beech (Fagus sylvatica L.) forests subjected to clear-cutting and natural regeneration and to elucidate the extent to which the carbohydrate concentration in roots of trees of different ages and sizes is related to ECM colonization. The study concerned an unmanaged forest, a stand clear-cut in 1996 and another clear-cut in 2001. ECM colonization of beech roots showed seasonal dynamics in the disturbed areas, but the percentage of roots colonized by ECM was not always related to the accumulation of non-structural carbohydrates. The composition of ECM communities differed between different stands and 40% of ECM morphotypes only occurred in disturbed ecosystems. However, comparable numbers of different ECM morphotypes (24, 25) were found in the three beech stands. This finding indicates that ECM diversity was quite high and similar within disturbed and unmanaged areas. This finding suggests that (1) ECM diversity was not affected by the size and age of trees and (2) the potential of ECM inocula remained high within clear-cut areas. Consequently, the introduction of ECM inocula by silvicultural practices would not be needed to improve the regeneration of clear-cut areas described in our study.


Beech forests Clear-cutting Ectomycorrhizal fungi Non-structural sugars 



Cenococcum geophilum


Ectomycorrhizal fungi








Tuber albidum







This research was supported by Fundación Universitaria de Navarra (FUNA, PIUNA) and Caja Navarra. Iván Closa was a recipient of a grant from Asociación de Amigos de la Universidad de Navarra (ADA). The authors are also grateful to Lorenzo Etxarri for assistance with logistics, site locations and history information on forest management and to Dr. Juan José Irigoyen and Amadeo Urdiain for technical assistance.


  1. Agerer R (1986) Studies on Ectomycorrhizae II. Introducing remarks on characterization and identification. Mycotaxon 26:473–492Google Scholar
  2. Agerer R (1987–2002) Colour atlas of ectomycorrhizae. Einhorn-Verlag, MunichGoogle Scholar
  3. Agerer R (1994) Characterization of ectomycorrhizas. In: Morris JR, Read D, Varma AK (eds) Techniques for mycorrhizal research. Methods in microbiology, vol 23. Academic Press, London, pp 25–73Google Scholar
  4. Agerer R (1999) Anatomical characteristics of identified Ectomycorrhizas: an attempt towards a natural classification. In: Varma A, Hock B (eds) Mycorrhiza. Structure, function, molecular biology and biotechnology, 2nd edn. Springer, Berlin, pp 633–682Google Scholar
  5. 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. doi: 10.1007/s005720100108 CrossRefGoogle Scholar
  6. Agerer R (2006) Fungal relationships and structural identity of their ectomycorrhizae. Mycol Prog 5:67–107. doi: 10.1007/s11557-006-0505-x CrossRefGoogle Scholar
  7. Agerer R, Gronbach E (1988) Cenococcum geophilum. In: Agerer R (ed) Colour atlas of ectomycorrhizae, plate 11. Einhorn Verlag, Schwäbisch GmündGoogle Scholar
  8. Avis PG, McLaughlin DJ, Dentinger BC, Reich PB (2003) Long-term increase in nitrogen supply alters above- and below-ground ectomycorrhizal communities and increases the dominance of Russula spp. in a temperate oak savanna. New Phytol 160:239–253. doi: 10.1046/j.1469-8137.2003.00865.x CrossRefGoogle Scholar
  9. Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–957. doi: 10.1104/pp.124.3.949 PubMedCrossRefGoogle Scholar
  10. Barbour MG, Burk JH, Pitts WD, William FS, Schwartz MW (1999) Terrestrial plant ecology, 3rd edn. Benjamin/Cummings, CAGoogle Scholar
  11. Bethlenfalvay GJ, Brown MS, Franson RL (1990) The Glycine-Glomus-Bradyrhizobium simbiosis. X. Relationships between leaf gas exchange and plant and soil water status in nodulated, mycorrhizal soybean under drought stress. Plant Physiol 94:723–728. doi: 10.1104/pp.94.2.723 PubMedCrossRefGoogle Scholar
  12. Bird C, McCleneghan C (2005) Morphological and functional diversity of ectomycorrhizal fungi on Roan Mountain (NC/TN). Southeast Nat 4:121–132. doi: 10.1656/1528-7092(2005)004[0121:MAFDOE]2.0.CO;2 CrossRefGoogle Scholar
  13. Blaise T, Garbaye J (1983) Effets de la fertilization minérale sur les ectomycorhizes d’une hêtraie. Acta Oecol 18:165–169Google Scholar
  14. Bradbury SM (1998) Ectomycorrhizas of lodgepole pine (Pinus contorta) seedlings originating from seed in southwestern Alberta cut blocks. Can J Bot 76:213–217. doi: 10.1139/cjb-76-2-213 CrossRefGoogle Scholar
  15. Bradbury SM, Danielson RM, Visser S (1998) Ectomycorrhizas of regenerating stands of lodgepole pine (Pinus contorta). Can J Bot 76:218–227. doi: 10.1139/cjb-76-2-218 CrossRefGoogle Scholar
  16. Brundrett M, Bougher N, Dell B, Grove T, Malajczuk N (1996) Working with mycorrhizas in forestry and agriculture. Australian Centre for International Agricultural Research, CanberraGoogle Scholar
  17. Buée M, Vairelles D, Garbaye J (2005) Year-round monitoring of diversity and potential metabolic activity of the ectomycorrhizal community in a beech (Fagus sylvatica) forest subjected to two thinning regimes. Mycorrhiza 15:235–245. doi: 10.1007/s00572-004-0313-6 PubMedCrossRefGoogle Scholar
  18. Clavería V, de Miguel A (2006) Análisis de la comunidad ectomicorrícica de un carrascal de Navarra (España). Bull Soc Hist Nat Toulouse 141:997–1001Google Scholar
  19. Coleman MD, Bledsoe CS, Lopushinsky W (1989) Pure culture response of ectomycorrhizal fungi to imposed water stress. Can J Bot 67:29–39. doi: 10.1139/b89-005 CrossRefGoogle Scholar
  20. Courty P-E, Pritsch K, Schloter M, Hartmann A, Garbaye J (2005) Activity profiling of ectomycorrhiza communities in two forest soils using multiple enzymatic tests. New Phytol 167:309–319. doi: 10.1111/j.1469-8137.2005.01401.x PubMedCrossRefGoogle Scholar
  21. de Román M, de Miguel AM (2005) Post-fire, seasonal and annual dynamics of the ectomycorrhizal community in a Quercus ilex L. forest over a 3-year period. Mycorrhiza 15:471–482. doi: 10.1007/s00572-005-0353-6 PubMedCrossRefGoogle Scholar
  22. Douglas RB, Parker VT, Cullings KW (2005) Belowground ectomycorrhizal community structure of mature lodgepole pine and mixed conifer stands in Yellowstone National Park. For Ecol Manage 208:303–317. doi: 10.1016/j.foreco.2004.12.011 CrossRefGoogle Scholar
  23. Douhan GW, Rizzo DM (2005) Phylogenetic divergence in a local population of the ectomycorrhizal fungus Cenococcum geophilum. New Phytol 166:263–271. doi: 10.1111/j.1469-8137.2004.01305.x PubMedCrossRefGoogle Scholar
  24. Erice G, Irigoyen JJ, Sánchez-Díaz M, Avice JCH, Ourry A (2007) Effect of drought, elevated CO2 and temperature on accumulation of N and vegetative storage proteins (VSP) in taproot of nodulated alfalfa before and after cutting. Plant Sci 172:903–912. doi: 10.1016/j.plantsci.2006.12.013 CrossRefGoogle Scholar
  25. Frank K, Beegle D, Denning J (1998) Phosphorus. In: Brown (ed) Recommended chemical soil test procedures for the north central region. North Carolina Regional Research Publication No. 221 (revised). Missouri Agricultural Experiment Station SB 1001, Columbia, MO, pp 21–26Google Scholar
  26. Grebenc T, Kraigher H (2007) Types of ectomycorrhiza of mature beech and spruce at ozone-fumigated and control forest plots. Environ Monit Assess 128:47–59. doi: 10.1007/s10661-006-9414-3 PubMedCrossRefGoogle Scholar
  27. Hagerman SH, Jones MD, Bradfield GE, Gillespie M, Durall DM (1999) Effects of clear-cut logging on the diversity and persistence of ectomycorrhizae at a subalpine forest. Can J Res 29:124–134. doi: 10.1139/cjfr-29-1-124 CrossRefGoogle Scholar
  28. Halpern CB, Spies TA (1995) Plant species diversity in natural and managed forests of the Pacific Northwest. Ecol Appl 5:913–934. doi: 10.2307/2269343 CrossRefGoogle Scholar
  29. Ingleby K, Munro RC, Noor M, Mason PA, Clearwater MJ (1998) Ectomycorrhizal populations and growth of Shorea parvifolia (Dipterocarpaceae) seedlings regenerating under three different forest canopies following logging. For Ecol Manage 111:171–179. doi: 10.1016/S0378-1127(98)00324-7 CrossRefGoogle Scholar
  30. Iñiguez J, Sánchez-Carpintero I, Val RM, Vitoria G, Peralta FJ (1992) Mapa de suelos de Navarra. E: 1:50.000. Gobierno de Navarra, SpainGoogle Scholar
  31. Jakucs E, Agerer R (1999) Tomentella pilosa (Burt) Bourdot & Galzin + Populus alba L. Descr Ectomycorrhizae 4:135–140Google Scholar
  32. Jany J-L, Martin F, Garbaye J (2003) Respiration activity of ectomycorrhizas from Cenococcum geophilum and Lactarius sp. in relation to soil water potential in five beech forests. Plant Soil 255:487–494. doi: 10.1023/A:1026092714340 CrossRefGoogle Scholar
  33. Jarvis CE, Walker JRL (1993) Simultaneous, rapid, spectrophotometric determination of total starch, amylose and amylopectin. J Sci Food Agric 63:53–57. doi: 10.1002/jsfa.2740630109 CrossRefGoogle Scholar
  34. Jones MD, Durall DM, Harniman SMK, Classen DC, Simard SW (1997) Ectomycorrhizal diversity on Betula papyrifera and Pseudotsuga menziesii seedlings grown in the greenhouse or outplanted in single-species and mixed plots in southern British Columbia. Can J Res 27:1872–1889. doi: 10.1139/cjfr-27-11-1872 CrossRefGoogle Scholar
  35. Jones MD, Durall DM, Cairney JWG (2003) Ectomycorrhizal fungal communities in young forest stands regenerating after clear-cut logging. New Phytol 157:399–422. doi: 10.1046/j.1469-8137.2003.00698.x CrossRefGoogle Scholar
  36. Jonsson L, Dahlberg A, Nilsson M-C, Kårén O, Zackrisson O (1999) Continuity of ectomycorrhizal fungi in self-regenerating boreal Pinus sylvestris forests studied by comparing mycobiont diversity on seedlings and mature trees. New Phytol 142:151–162. doi: 10.1046/j.1469-8137.1999.00383.x CrossRefGoogle Scholar
  37. Kropp BR, Albee S (1996) The effects of silvicultural treatments on occurrence of mycorrhizal sporocarps in a Pinus contorta forest: a preliminary study. Biol Conserv 78:313–318. doi: 10.1016/S0006-3207(96)00140-1 CrossRefGoogle Scholar
  38. Kuikka K, Harma E, Markkola A, Rautio P, Roitto M, Saikkonen K, Ahonen-Jonnarth U, Finlay R, Tuomi J (2003) Severe defoliation of Scots pine reduces reproductive investment by ectomycorrhizal symbionts. Ecology 84:2051–2061. doi: 10.1890/02-0359 CrossRefGoogle Scholar
  39. Last FT, Pelham J, Mason PA, Ingleby K (1979) Influence of leaves on sporophore production by fungi forming sheathing mycorrhizas with Betula spp. Nature 280:168–169. doi: 10.1038/280168a0 CrossRefGoogle Scholar
  40. Lobuglio KF (1999) Cenococcum. In: Cairney JWG, Chambers SM (eds) Ectomycorrhizal fungi. Key genera in profile. Springer, Berlin, pp 287–310Google Scholar
  41. Moncalvo J-M, Vilgalys R, Redhead SA, Johnson JE, James TY, Aime MC, Hofstetter V, Verduin SJW, Larsson E, Baroni TJ, Thorn RG, Jacobsson S, Clémençon H, Miller OK (2002) One hundred and seventeen clades of euagarics. Mol Phylogenet Evol 23:357–400. doi: 10.1016/S1055-7903(02)00027-1 PubMedCrossRefGoogle Scholar
  42. Olsen CR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. US Department of Agriculture Circular 939. US Government Printing Office, Washington, DCGoogle Scholar
  43. Pennanen T, Heiskanen J, Korkama T (2005) Dynamics of ectomycorrhizal fungi and growth of Norway spruce seedlings after planting on a mounded forest clear-cut. For Ecol Manage 213:243–252. doi: 10.1016/j.foreco.2005.03.044 CrossRefGoogle Scholar
  44. Peter M, Ayer F, Cudlín P, Egli S (2008) Belowground ectomycorrhizal communities in three Norway spruce stands with different degrees of decline in the Czech Republic. Mycorrhiza 18:157–169. doi: 10.1007/s00572-008-0166-5 PubMedCrossRefGoogle Scholar
  45. Porta J, López-Acevedo M, Rodríguez R (1986) Técnicas y experimentos en Edafología. Collegi Oficial d’Enginyers Agrònoms de Catalunya, Barcelona (in Spanish)Google Scholar
  46. Read DJ (1999) Mycorrhiza—the state of the art. In: Varma A, Hock B (eds) Mycorrhiza: structure, function, molecular biology and biotechnology. Springer, Berlin, pp 3–34Google Scholar
  47. Rivas-Martínez S, Báscones JC, Díaz TE, Fernández-González F, Loidi J (1991) Vegetación del Pirineo occidental y Navarra. Itinera Geobot 5:5–456Google Scholar
  48. Selosse M-A, Bauer R, Moyersoen B (2002) Basal hymenomycetes belonging to the Sebacinaceae are ectomycorrhizal on temperate deciduous trees. New Phytol 155:183–195. doi: 10.1046/j.1469-8137.2002.00442.x CrossRefGoogle Scholar
  49. Simard SW, Jones MD, Durall DM, Hope GD, Stathers Sorensen NS, Zimonick BJ (2003) Chemical and mechanical site preparation: effects on Pinus contorta growth, physiology, and microsite quality on grassy, steep forest sites in British Columbia. Can J Res 33:1495–1515. doi: 10.1139/x03-072 CrossRefGoogle Scholar
  50. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic Press, San DiegoGoogle Scholar
  51. Sorensen TA (1948) A method for establishing groups of equal amplitude in plant sociology based on similarity of species content and its application to analyses of the vegetation on Danish commons. Det Kgl Danske Vidensk Selsk Skr 5:1–34Google Scholar
  52. Urban A, Weiss M, Bauer R (2003) Ectomycorrhizas involving sebacinoid mycobionts. Mycol Res 107(1):3–14. doi: 10.1017/S0953756202007116 PubMedCrossRefGoogle Scholar
  53. USDA (1999) Soil taxonomy—second edition. Agriculture handbook number 436. United States Department of Agriculture, WashingtonGoogle Scholar
  54. Van der Hout P (2000) Testing the applicability of reduced impact logging in greenheart forest in Guyana. Int Forest Rev 2:24–32Google Scholar
  55. Visser S, Parkinson D (1999) Wildfire vs. Clear-cutting: Impacts on ectomycorrhizal and Decomposer Fungi. In: Meurisse RT, Ypsilantis WG, Seybold C (eds) Proceedings Pacific Northwest forest and rangeland soil organism symposium. US Department of Agriculture, Forest Service, Pacific Northwest Research Station, Portland, pp 114–123Google Scholar
  56. Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Nieves Goicoechea
    • 1
  • Iván Closa
    • 1
  • Ana María de Miguel
    • 2
  1. 1.Departamento de Biología Vegetal, sección Biología Vegetal (Unidad Asociada al CSIC, EEAD, Zaragoza), Facultades de Ciencias y FarmaciaUniversidad de NavarraPamplonaSpain
  2. 2.Departamento de Biología Vegetal, sección Botánica, Facultades de Ciencias y FarmaciaUniversidad de NavarraPamplonaSpain

Personalised recommendations