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Land use practices and ectomycorrhizal fungal communities from oak woodlands dominated by Quercus suber L. considering drought scenarios

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Abstract

Oak woodlands in the Mediterranean basin have been traditionally converted into agro-silvo-pastoral systems and exemplified sustainable land use in Europe. In Portugal, in line with the trend of other European countries, profound changes in management options during the twentieth century have led to landscape simplification. Landscapes are dynamic and the knowledge of future management planning combining biological conservation and soil productivity is needed, especially under the actual scenarios of drought and increasing evidence of heavy oak mortality. We examined the ectomycorrhizal (ECM) fungal community associated with cork oak in managed oak woodlands (called montado) under different land use practices, during summer. ECM fungal richness and abundance were assessed in 15 stands established in nine montados located in the Alentejo region (southern Portugal), using morphoty** and ITS rDNA analysis. Parameters related to the montados landscape characteristics, land use history over the last 25 years, climatic and edaphic conditions were taken into account. Fifty-five ECM fungal taxa corresponding to the most abundant fungal symbionts were distinguished on cork oak roots. Cenococcum geophilum and the families Russulaceae and Thelephoraceae explained 56% of the whole ECM fungal community; other groups were represented among the community: Cortinariaceae, Boletaceae, Amanita, Genea, Pisolithus, Scleroderma, and Tuber. There were pronounced differences in ECM fungal community structure among the 15 montados stands: C. geophilum was the only species common to all stands, tomentelloid and russuloid species were detected in 87–93% of the stands, Cortinariaceae was detected in 60% of the stands, and the other groups were more unequally distributed. Ordination analysis revealed that ECM fungal richness was positively correlated with the silvo-pastoral exploitation regime and low mortality of cork oak, while ECM fungal abundance was positively correlated with extensive agro-silvo-pastoral exploitation under a traditional 9-year rotation cultivation system and recent soil tillage. The effects of land use on the ECM fungal community and its implications in different scenarios of landscape management options, oak mortality, and global warming are discussed.

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References

  • Agerer R (1987–2008) Colour atlas of ectomycorrhizae. Einhorn-Verlag, Schwäbisch Gmünd, 1st–13th delivery.

  • Agerer R (2001) Exploration types of ectomycorrhizae. A proposal to classify ectomycorrhizal mycelial systems according to their pattern of differentiation and putative ecological importance. Mycorrhiza 11:107–114. doi:10.1007/s005720100108

    Article  Google Scholar 

  • Agerer R, Rambold G (2004–2007) [first posted on 2004-06-01; used update: 2007-05-01]. DEEMY—an information system for characterization and determination of ectomycorrhizae. www.deemy.de, München, Germany.

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Azul AM (2002) Diversidade de fungos ectomicorrízicos em ecossitemas de Montado. PhD Dissertation, University of Coimbra, Portugal

  • Azul AM, Agerer R, Freitas H (1999) “Quercirhiza nodulosomorpha” + Quercus suber L. Descr Ectomyc 4:103–108

    Google Scholar 

  • Azul AM, Agerer R, Freitas H (2001a) “Quercirhiza sclerotiigera” + Quercus suber L. Descr Ectomyc 5:99–105

    Google Scholar 

  • Azul AM, Agerer R, Freitas H (2001b) “Quercirhiza russulocystidiata” + Quercus suber L. Descr Ectomyc 5:93–98

    Google Scholar 

  • Azul AM, Agerer R, Freitas H (2001c) “Quercirhiza pedicae” + Quercus suber L. Descr Ectomyc 5:85–91

    Google Scholar 

  • Azul AM, Agerer R, Freitas H (2001d) “Quercirhiza internangularis” + Quercus suber L. Descr Ectomyc 5:79–83

    Google Scholar 

  • Azul AM, Agerer R, Freitas H (2001e) “Quercirhiza ectendotrophica” + Quercus suber L. Descr Ectomyc 5:67–72

    Google Scholar 

  • Azul AM, Agerer R, Freitas H (2006a) “Quercirhiza ateracusrugosa” + Quercus suber L. Descr Ectomyc 9/10:75–79

    Google Scholar 

  • Azul AM, Martín MP, Agerer R, Freitas H (2006b) “Quercirhiza auratercystidiata” + Quercus suber L. Descr Ectomyc 9/10:81–86

    Google Scholar 

  • Azul AM, Martín MP, Agerer R, Freitas H (2006c) “Quercirhiza flavocystidiata” + Quercus suber L. Descr Ectomyc 9/10:93–97

    Google Scholar 

  • Azul AM, Agerer R, Freitas H (2006d) “Quercirhiza lanatriangularis” + Quercus suber L. Descr Ectomyc 9/10:99–103

    Google Scholar 

  • Azul AM, Agerer R, Freitas H (2006e) “Quercirhiza summatriangularis” + Quercus suber L. Descr Ectomyc 9/10:111–114

    Google Scholar 

  • Azul AM, Agerer R, Freitas H (2006f) “Quercirhiza tomentellocystidiata” + Quercus suber L. Descr Ectomyc 9/10:115–119

    Google Scholar 

  • Azul AM, Agerer R, Freitas H (2006g) “Quercirhiza tomentelloflexuosa” + Quercus suber L. Descr Ectomyc 9/10:121–126

    Google Scholar 

  • Azul AM, Martín MP, Agerer R, Freitas H (2006h) “Quercirhiza tomentellofuniculosa” + Quercus suber L. Descr Ectomyc 9/10:127–134

    Google Scholar 

  • Azul AM, Martín MP, Agerer R, Freitas H (2008a) “Quercirhiza tomentellocumulata” + Quercus suber L. Descr Ectomyc 11/12:125–130

    Google Scholar 

  • Azul AM, Martín MP, Agerer R, Freitas H (2008b) “Quercirhiza tomentelloepidermoidea” + Quercus suber L. Descr Ectomyc 11/12:131–134

    Google Scholar 

  • Azul AM, Martín MP, Agerer R, Freitas H (2008c) “Quercirhiza tomentelloreticulata” + Quercus suber L. Descr Ectomyc 11/12:135–139

    Google Scholar 

  • Azul AM, Martín MP, Agerer R, Freitas H (2008d) “Quercirhiza tomentellostellata” + Quercus suber L. Descr Ectomyc 11/12:141–146

    Google Scholar 

  • Baddeley A, Watson CA (2005) Influences of root diameter, tree age, soil depth and season on fine root survivorship in Prunus avium. Plant Soil 276:15–22. doi:10.1007/s11104-005-0263-6

    Article  CAS  Google Scholar 

  • Baier R, Ingenhaag J, Blaschke H, Gottlein A, Agerer R (2006) Vertical distribution of an ectomycorrhizal community in upper soil horizons of a young Norway spruce (Picea abies [L.] Karst.) stand of the Bavarian Limestone Alps. Mycorrhiza 16:197–206. doi:10.1007/s00572-006-0035-z

    Article  PubMed  Google Scholar 

  • Brasier CM (1996) Phytophothora cinnamomi and oak decline in souther Europe. Environmental constraints including climate change. Ann Sci For 53:347–358

    Article  Google Scholar 

  • Brasier CM, Scott JK (2008) European oak decline and global warming: a theoretical assessment with special reference to the activity of Phytophthora cinnamomi. EPPO Bulletin 24:221–232. doi:10.1111/j.1365-2338.1994.tb01063.x

    Article  Google Scholar 

  • Byrd KB, Parker VT, Vogler DR, Cullings KW (2000) The influence of clear-cutting on ectomycorrhizal fungus diversity in a lodgepole pine (Pinus contorta) stand, Yellowstone National Park, Wyoming, and Gallatins National forest, Montana. Can J Bot 78:149–156. doi:10.1139/cjb-78-2-149

    Article  Google Scholar 

  • Chapman HD (1979) Total Exchangeable bases. In: Black CA, Evans DD, White JL, Ensminger LE, Clark FE (eds) Methods of soil analyses. Part 2. Chemical and microbiological properties, 5th edn. Agronomy 9, American Society of Agronomy, Madison

    Google Scholar 

  • Carreira JA, Lajtha K, Niell FX (1997) Phosphorous transformations along a soil/vegetation series of fire-prone, dolomitic, semi-arid shrublands of Southern Spain. Biogeochemistry 39:87–120

    Article  CAS  Google Scholar 

  • Courty P-E, Franc A, Pierrat J-C, Garbaye J (2008) Temporal changes in the ectomycorrhizal community in two soil horizons of a temperate Oak forest. Appl Environ Microbiol 74:5792–5801. doi:10.1128/AEM.01592-08

    Article  PubMed  CAS  Google Scholar 

  • Da Silva PM, Aguiar CAS, Niemelã SJP, Serrano ARM (2008) Diversity patterns of round-beetles (Coleoptera: Carabidae) along a gradient of land use disturbance. Agr Ecosyst Environ 124:270–274. doi:10.1016/j.agee.2007.10.007

    Article  Google Scholar 

  • Debussche M, Lepart J, Darvieux A (1999) Mediterranean landscapes changes: the ancient postcard evidence. Glob Ecol Biogeogr Lett 8:3–15. doi:10.1046/j.1365-2699.1999.00316.x

    Article  Google Scholar 

  • Decocq G, Aubert M, Dupont F, Alard Saguez DR, Wattez-Franger A, DeFoucault B, Delelis-Dusollier A, Bardat J (2004) Plant diversity in a managed temperate deciduous forest: understorey response to two silvicultural systems. J Appl Ecol 41:1065–1079. doi:10.1111/j.0021-8901.2004.00992.x

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • DGF (2003) Anuário Florestal 2003. Direcção Geral das Florestas, Lisboa

    Google Scholar 

  • Díaz-Delgado R, Lloret F, Pons X, Terradas J (2002) Satellite evidence of decreasing resilience in Mediterranean plant communities after recurrent wildfires. Ecology 83:2293–2303. doi:10.1890/0012-9658(2002)083[2293:SEODRI]2.0.CO;2

    Google Scholar 

  • Dickie IA, Guza RC, Krazewski SE, Reich PB (2004) Shared ectomycorrhizal fungi between a herbaceous perennial (Helianthemum bicknellii) and oak (Quercus) seedlings. New Phytol 64:375–382. doi:10.1111/j.1469-8137.2004.01177.x

    Article  Google Scholar 

  • European Environment Agency (2004) Impacts of Europe’s Changing Climate. An Indicator-Based Assessment. EEA Report No. 2/2004, European Environment Agency, Copenhagen

  • Gardes M, Bruns TD (1983) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  Google Scholar 

  • Gardes M, Bruns TD (1996) Community structure of ectomycorrhizal fungi in a Pinus muricata forest: above- and belowground views. Can J Bot 74:572–1583. doi:10.1139/b96-190

    Article  Google Scholar 

  • Hagerman SM, Durall DM (2004) Ectomycorrhizal colonization of greenhouse-grown Douglas-fir (Pseudotsuga menziesii) seedlings by inoculum associated with the roots of refuge plants sampled from a Douglas-fir forest in the southern interior of British Columbia. Can J Bot 82:742–751. doi:10.1139/b04-047

    Article  Google Scholar 

  • Hagerman SM, 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 For Res 29:124–134. doi:10.1139/cjfr-29-1-124

    Article  Google Scholar 

  • Hector A, Schmid B, Beierkuhnlein C, Caldeira MC, Diemer M, Dimitrakopoulos PG, Finn J, Freitas H, Giller PS, Good J, Harris R, Hogberg P, Huss-Danell K, Joshi J, Jumpponen A, Korner C, Leadley PW, Loreau M, Minns A, Mulder CPH, O’Donovan G, Otway SJ, Pereira JS, Prinz A, Read DJ, SchererLorenzen M, Schulze ED, Siamantziouras ASD, Spehn E, Terry AC, Troumbis AY, Woodward FI, Yachi S, Lawton JH (1999) Plant diversity and productivity in European grasslands. Science 286:1123–1127. doi:10.1126/science.286.5442.1123

    Article  PubMed  CAS  Google Scholar 

  • 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. doi:10.1046/j.1469-8137.2002.00417.x

    Article  Google Scholar 

  • Horton TR, Bruns TD (1998) Multiple host fungi are the most frequent and abundant ectomycorrhizal types in a mixed stand of Douglas fir (Pseudotsuga menziesii) and bishop pine (Pinus muricata). New Phytol 139:331–339. doi:10.1111/j.1469-8137.1998.00185.x

    Article  Google Scholar 

  • Joffre R, Rambal S, Ratte JP (1999) The dehesa systems of southern Spain and Portugal as a natural ecosystem mimic. Agrofor Syst 45:57–79. doi:10.1023/A:1006259402496

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Kennedy PG, Izzo AD, Bruns TD (2003) High potential for common mycorrhizal networks between understory and canopy trees in a mixed evergreen forest. J Ecol 91:1071–1080. doi:10.1046/j.1365-2745.2003.00848.x

    Article  Google Scholar 

  • Klaa K, Mill PJ, Incoll LD (2005) Distribution of small mammals in a silvoarable agroforestry system in Northern England. Agr Syst 63:101–110. doi:10.1007/s10457-004-1110-0

    Article  Google Scholar 

  • Lavergne S, Thuiller W, Molina J, Debussche M (2005) Environmental and human factors influencing rare plant local occurrence, extinction and persistence: a 115-year study in the Mediterranean region. J Biogeogr 32:799–811. doi:10.1111/j.1365-2699.2005.01207.x

    Article  Google Scholar 

  • Leake J, Johnson D, Donnelly D, Muckle G, Body 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. doi:10.1139/B04-060

    Article  Google Scholar 

  • 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 49:319–332. doi:10.1016/j.femsec.2004.04.004

    Article  PubMed  CAS  Google Scholar 

  • LQARS (1977) Sector de Fertilidade do Solo. DGSA—Ministério da Agricultura, Lisboa

    Google Scholar 

  • Magurran AE (1988) Ecological diversity and its measurement. Princeton University Press, New Jersey

    Google Scholar 

  • Mouillot F, Ratte J-P, Joffre R, Mouillot D, Rambal S (2005) Long-term forest dynamic after land abandonment in a fire prone Mediterranean landscape (central Corsica, France). Landscape Ecol 20:101–112. doi:10.1007/s10980-004-1297-5

    Article  Google Scholar 

  • Moreno G, Obrador JJ, Cubera E, Dupraz C (2005) Fine root distribution in Dehesas of Central-Western Spain. Plant Soil 277:153–162. doi:10.1007/s11104-005-6805-0

    Article  CAS  Google Scholar 

  • Nunes MCS, Vasconcelos MJ, Pereira JMC, Dasgupta N, Alldredge RJ, Rego FC (2005) Land cover type and fire in Portugal: do fires burn land cover selectively? Landscape Ecol 20:661–673. doi:10.1007/s10980-005-0070-8

    Article  Google Scholar 

  • 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. doi:10.1046/j.1469-8137.2000.00569.x

    Article  CAS  Google Scholar 

  • Pinto-Correia T (1993a) Land abandonment: Changes in the land use patterns around the Mediterranean basin. In: CIHEAM-IAMZ (ed) Etat de l’Agriculture en Méditerranée. Les sols dans la région méditerranéenne: utilisation, gestion et perspectives d’évolution. Zaragoza, Spain

  • Pinto-Correia T (1993b) Threatened Landscape in Alentejo, Portugal: the “montado” and other “agro-silvo pastoral” systems. Landscape Urban Plan 24:43–48. doi:10.1016/0169-2046(93)90081-N

    Article  Google Scholar 

  • Pinto-Correia T, Mascarenhas J (1999) Contribution to the extensification/intensification debate: new trends in the portuguese Montado. Landscape Urban Plan 46:125–131. doi:10.1016/S0169-2046(99)00036-5

    Article  Google Scholar 

  • Pinto-Correia T, Vos W (2004) Multifunctionality in Mediterranean landscapes—past and future. In: Jongman R (ed) The new dimensions of the European landscape. Wageningen EU Frontis Series, Springer

    Google Scholar 

  • Pulido FJ, Díaz M, Hidalgo SJ (2001) Size structure and regeneration of Spanish holm oak (Quercus ilex) forests and dehesas: effects of agroforestry use in their long-term sustainability. Forest Ecol Manag 146:1–13. doi:10.1016/S0378-1127(00)00443-6

    Article  Google Scholar 

  • Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems—a journeys towards relevance. New Phytol 157:475–492. doi:10.1046/j.1469-8137.2003.00704.x

    Article  Google Scholar 

  • Richard F, Millot S, Gardes M, Selosse M-A (2005) Diversity and specificity of ectomycorrhizal fungi retrieved from an old-growth Mediterranean forest dominated by Quercus ilex. New Phytol 166:1011–1023. doi:10.1111/j.1469-8137.2005.01382.x

    Article  PubMed  CAS  Google Scholar 

  • Rios-Díaz M, Mosquera-Losada R, Rigueiro-Rodríguez A (2006) Biodiversity indicators on silvopastoralism across Europe. In EFI Technical Report 21, European Forest Institute

  • Selosse M-A, Richard F, He X, Simard SW (2006) Mycorrhizal networks: des liaisons dangereuses. Trends Ecol Evol 21:621–628. doi:10.1016/j.tree.2006.07.003

    Article  PubMed  Google Scholar 

  • Simard SW, Durall DM (2004) Mycorrhizal networks: a review of their extent, function, and importance. Can J Bot 82:1140–1165. doi:10.1139/b04-116

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London

    Google Scholar 

  • Smith JE, McKay D, Brenner G, McIver J, Spatafora JW (2005) Early impacts of forest restoration treatments on the ectomycorrhizal fungal community and fine root biomass in a mixed conifer forest. J Appl Ecol 42:526–535. doi:10.1111/j.1365-2664.2005.01047.x

    Article  Google Scholar 

  • Sousa JP, da Gama MM, Pinto P, Keating A, Calhoa F, Lemos M, Castro C, Luz T, Leitão P, Dias S (2004) Effects of land use on Collembola diversity patterns in a Mediterranean landscape. Pedobiologia 48:609–622. doi:10.1016/j.pedobi.2004.06.004

    Article  Google Scholar 

  • StatSoft, Inc (2001) STATISTICA (Data Analysis Software System), Version 6. Tulsa, OK, USA

  • Stoate C, Borralho R, Araújo M (2000) Factors affecting corn bunting Miliaria calandra abundance in a Portuguese agricultural landscape. Agr Ecosyst Environ 77:219–226. doi:10.1016/S0167-8809(99)00101-2

    Article  Google Scholar 

  • Suz LM, Azul AM, Melissa MH, Bledsoe CS, Martín MP (2008) Morphoty** and molecular methods to characterize ectomycorrhizal roots and hyphae in soil. In: Nautiyal CS, Dion P (eds) Soil biology: molecular mechanisms of plant and microbe coexistence. Springer, Berlin, pp 437–474. doi:10.1007/978-3-540-75575-3_18

    Chapter  Google Scholar 

  • 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. doi:10.1046/j.0028-646x.2003.00792.x

    Article  CAS  Google Scholar 

  • Ter Braak CJF, Smilauer P (2002) CANOCO Manual and CanoDraw for Windows User’s Guide: Software for Canonical Community Ordination (version 4.5). Microcomputer Power, Ithaca, NY

  • White TJ, Burns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for polygenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, New York, pp 315–322

    Google Scholar 

  • Winka K, Ahlberg C, Eriksson OE (1998) Are the lichenized ostropales? Lichenologist 30:455–462. doi:10.1017/S0024282992000446

    Google Scholar 

  • Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice Hall International, London

    Google Scholar 

Download references

Acknowledgments

The authors would like to thank Fernanda Azul and Lurdes Barrico for technical assistance in cleaning the root samples. We also thank two anonymous reviewers for improving the paper, Ana Fonseca and Teresa Pinto-Correia for the land use history data, farmers, land users and/or stakeholders for their active participation, and Escola Superior Agrária (Coimbra) for soil analysis. Our work was funded by FCT-MCTES (Portuguese Foundation for Science and Technology) and European fund FEDER, project Praxis/P/AGR/11165/1998 and the project Flora Micológica Ibérica (CGL2006-12732-CO2-01/BOS). AM Azul was supported by individual grants from FCT-MCTES (SFRH7BPD/5560/2001) and European fund (Biod-Iberia Program: ES-TAF-A69).

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Correspondence to Anabela Marisa Azul.

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Questionnaire used in the interviews to the farmers and stakeholders

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Table 3 Ectomycorrhizal material

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Azul, A.M., Sousa, J.P., Agerer, R. et al. Land use practices and ectomycorrhizal fungal communities from oak woodlands dominated by Quercus suber L. considering drought scenarios. Mycorrhiza 20, 73–88 (2010). https://doi.org/10.1007/s00572-009-0261-2

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