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Acclimation of Fine Root Systems to Soil Warming: Comparison of an Experimental Setup and a Natural Soil Temperature Gradient

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Abstract

Global warming is predicted to impact high-latitude and high-altitude forests severely, jeopardizing their overall functioning and carbon storage, both of which depend on the warming response of tree fine root systems. This paper investigates the effect of soil warming on the biomass, morphology and colonizing ectomycorrhizal community of spruce fine and absorptive fine roots. We compare the responses of spruce roots growing at a man-made long-term soil warming (+ 4°C) experiment to results obtained from a geothermal soil temperature gradient (+ 1 to + 14°C) extending to the forest die-off edge, to shed light on the generalizability of the warming response and reveal any thresholds in acclimation ability. Trees in warmer soils formed longer and less-branched absorptive roots with higher specific root length and area, and lower root tissue density in both spruce stands, irrespective of warming method and location. Soil warming at the experimental warming site also supported the occurrence of a more varied EcM community and an increase in the abundance of Tomentella spp., indicating a shift in nutrient foraging. Fine and absorptive fine root biomass decreased toward warmer soil, with a sharp reduction occurring between + 4 and + 6°C from the ambient and leading to the collapse of the fine root system at the geothermal gradient. At the experimental warming site, the applied + 4°C warming had no effect on fine and absorptive fine root biomass. The similar fine root responses at the two warming sites suggest that the observations possibly reflect general acclimation patterns in spruce forests to global warming.

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References

  • Abarenkov K, Nilsson RH, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Ursing BM, Vralstad T, Liimatainen K, Peintner U, Kõljalg U. 2010. The UNITE database for molecular identification of fungi—recent updates and future perspectives. New Phytol 186:281–5.

    Article  Google Scholar 

  • Agerer R. 1991. Characterization of ectomycorrhiza. In: Norris JR, Read DJ, Varma AK, Eds. Techniques for the study of mycorrhiza. London: Academic Press. p 25–73.

    Chapter  Google Scholar 

  • 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 11:107–14.

    Article  Google Scholar 

  • Agerer R. 2006. Fungal relationships and structural identity of their ectomycorrhizae. Mycol Prog 5:67–107.

    Article  Google Scholar 

  • Anderson MJ. 2001. A new method for non parametric multivariate analysis of variance. Austral Ecology 26:32–46.

    Google Scholar 

  • Anderson MJ. 2004. PERMDISP: a FORTRAN computer program for permutational analysis of multivariate dispersions (for any two-factor ANOVA design) using permutation tests. Department of Statistics, University of Auckland, New Zealand.

  • Averill C, Turner BL, Finzi AC. 2014. Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505:543–5.

    Article  CAS  Google Scholar 

  • Beier C, Beierkuhnlein C, Wohlgemuth T, Penuelas J, Emmett B, Körner C, de Boeck H, Christensen JH, Leuzinger S, Janssens IA, Hansen K. 2012. Precipitation manipulation experiments—challenges and recommendations for the future. Ecol Lett 15:899–911.

    Article  Google Scholar 

  • Buée M, Courty PE, Mignot D, Garbaye J. 2007. Soil niche effect on species diversity and catabolic activities in an ectomycorrhizal fungal community. Soil Biol Biochem 39:1947–55.

    Article  CAS  Google Scholar 

  • Caudullo G, Tinner W, de Rigo D. 2016. Picea abies in Europe: distribution, habitat, usage and threats. In: San-Miguel-Ayanz J, de Rigo D, Caudullo G, Houston Durrant T, Mauri A, Eds. European atlas of forest tree species. Luxembourg: Publ. Off. EU. p e012300+.

  • Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay RD, Wardle DA, Lindahl BD. 2013. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339:1615–18.

    Article  CAS  Google Scholar 

  • Clemmensen KE, Finlay RD, Dahlberg A, Stenlid J, Wardle DA, Lindahl BD. 2015. Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests. New Phytol 205:1525–36.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Colwell RK. 2013. EstimateS, Version 9.1: statistical estimation of species richness and shared species from samples. http://viceroy.eeb.uconn.edu/EstimateS/.

  • Comas LH, Eissenstat DM. 2004. Linking fine root traits to maximum potential growth rate among 11 mature temperate tree species. Funct Ecol 18:388–97.

    Article  Google Scholar 

  • 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 42:679–98.

    Article  CAS  Google Scholar 

  • 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 167:309–19.

    Article  CAS  PubMed  Google Scholar 

  • Cox F, Barsoum N, Lilleskov EA, Bidartondo MI. 2010. Nitrogen availability is a primary determinant of conifer mycorrhizas across complex environmental gradients. Ecol Lett 13:1103–13.

    Article  PubMed  Google Scholar 

  • Deslippe JR, Hartmann M, Mohn WW, Simard SW. 2011. Long-term experimental manipulation of climate alters the ectomycorrhizal community of Betula nana in Arctic tundra. Glob Change Biol 17:1625–36.

    Article  Google Scholar 

  • Fernandez CW, Nguyen NH, Stefanski A, Han Y, Hobbie SE, Montgomery RA, Reich PB, Kennedy PG. 2017. Ectomycorrhizal fungal response to warming is linked to poor host performance at the boreal-temperate ecotone. Glob Change Biol 23:1598–609.

    Article  Google Scholar 

  • Finér L, Helmisaari H-S, Lõhmus K, Majdi H, Brunner I, Børja I, Eldhuset T, Godbold D, Grebenc T, Konôpka B, Kraigher H, Möttönen M-R, Ohashi M, Oleksyn J, Ostonen I, Uri V, Vanguelova E. 2007. Variation in fine root biomass of three European tree species: Beech (Fagus sylvatica L.), Norway spruce (Picea abies L. Karst.), and Scots pine (Pinus sylvestris L.). Plant Biosyst 141:394–405.

    Article  Google Scholar 

  • Frey-Klett P, Garbaye J, Tarkka M. 2007. The mycorrhiza helper bacteria revisited. New Phytol 176:22–36.

    Article  CAS  PubMed  Google Scholar 

  • Gill RA, Jackson RB. 2000. Global patterns of root turnover for terrestrial ecosystems. New Phytol 147:13–31.

    Article  Google Scholar 

  • Gorissen A, Kuyper TW. 2000. Fungal species-specific responses of ectomycorrhizal Scots pine (Pinus sylvestris) to elevated [CO2]. New Phytol 146:163–8.

    Article  CAS  Google Scholar 

  • Guo DL, Mitchell RJ, Hendricks JJ. 2004. Fine root branch orders respond differentially to carbon source-sink manipulations in a longleaf pine forest. Oecologia 140:450–7.

    Article  PubMed  Google Scholar 

  • Hajek P, Hertel D, Leuschner C. 2014. Root order- and root age-dependent response of two poplar species to belowground competition. Plant Soil 377:337–55.

    Article  CAS  Google Scholar 

  • Halldórsson B, Sigbjörnsson R. 2009. The Mw 6.3 Ölfus earthquake at 15:45 UTC on 29 May 2008 in South Iceland: ICEARRAY strong-motion recordings. Soil Dyn Earthq Eng 29:1073–83.

    Article  Google Scholar 

  • Hanson PJ, Riggs JS, Nettles WR, Phillips JR, Krassovski MB, Hook LA, Gu L, Richardson AD, Aubrecht DM, Ricciuto DM, Warren JM, Barbier C. 2017. Attaining whole-ecosystem warming using air and deep-soil heating methods with an elevated CO2 atmosphere. Biogeosciences 14:861–83.

    Article  CAS  Google Scholar 

  • Helmisaari H-S, Derome J, Nojd P, Kukkola M. 2007. Fine root biomass in relation to site and stand characteristics in Norway spruce and Scots pine stands. Tree Physiol 27:1493–504.

    Article  CAS  PubMed  Google Scholar 

  • Houston Durrant T, Mauri A, de Rigo D, Caudullo G. 2016. Picea sitchensis in Europe: distribution, habitat, usage and threats. In: San-Miguel-Ayanz J, de Rigo D, Caudullo G, Houston Durrant T, Mauri A, Eds. European atlas of forest tree species. Luxembourg: Publ. Off. EU. p e0137a1+.

  • IPCC. 2013. Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM, Eds. Cambridge, United Kingdom and New York, NY, USA: Cambridge University Press.

  • Jackson RB, Mooney HA, Schulze E-D. 1997. A global budget for fine root biomass, surface area, and nutrient contents. Proc Natl Acad Sci USA 94:7362–6.

    Article  CAS  PubMed  Google Scholar 

  • Jandl R, Schindlbacher A. 2014. Carbon sequestration in Central European forest ecosystems. In: CO2 sequestration and valorization.

  • Johnson MG, Rygiewicz PT, Tingey DT, Phillips DL. 2006. Elevated CO2 and elevated temperature have no effect on Douglas-fir fine-root dynamics in nitrogen-poor soil. New Phytol 170:345–56.

    Article  CAS  PubMed  Google Scholar 

  • King JS, Pregitzer KS, Zak DR. 1999. Clonal variation in above- and below-ground growth responses of Populus tremuloides Michaux: Influence of soil warming and nutrient availability. Plant Soil 217:119–30.

    Article  Google Scholar 

  • Kraigher H, Al Sayegh Petkovšek S, Grebenc T, Simončič P. 2007. Types of ectomycorrhiza as pollution stress indicators: case studies in Slovenia. Environ Monit Assess 128:31–45.

    Article  CAS  PubMed  Google Scholar 

  • Kramer-Walter KR, Bellingham PJ, Millar TR, Smissen RD, Richardson SJ, Laughlin DC. 2016. Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum. J Ecol 104:1299–310.

    Article  Google Scholar 

  • Kranabetter JM, Hawkins BJ, Jones MD, Robbins S, Dyer T, Li T. 2015. Species turnover (beta-diversity) in ectomycorrhizal fungi linked to NH4+ uptake capacity. Mol Ecol 24:5992–6005.

    Article  CAS  PubMed  Google Scholar 

  • Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lücking R, Martín MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüßler A, Scott JA, Senés C, Smith ME, Suija A, Taylor DL, Telleria MT, Weiss M, Larsson KH. 2013. Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–7.

    Article  CAS  Google Scholar 

  • Lal R. 2005. Forest soils and carbon sequestration. Forest Ecology and Management 220:242–58.

    Article  Google Scholar 

  • Leblans NIW. 2016. Natural gradients in temperature and nitrogen: Iceland represents a unique environment to clarify long-term global change effects on carbon dynamics.

  • Leblans NIW, Sigurdsson BD, Vicca S, Fu Y, Penuelas J, Janssens IA. 2017. Phenological responses of Icelandic subarctic grasslands to short-term and long-term natural soil warming. Glob Change Biol 23:4932–45.

    Article  Google Scholar 

  • Leppälammi-Kujansuu J, Ostonen I, Strömgren M, Nilsson LO, Kleja DB, Sah SP, Helmisaari HS. 2013. Effects of long-term temperature and nutrient manipulation on Norway spruce fine roots and mycelia production. Plant Soil 366:287–303.

    Article  CAS  Google Scholar 

  • Leppälammi-Kujansuu J, Salemaa M, Kleja DB, Linder S, Helmisaari HS. 2014. Fine root turnover and litter production of Norway spruce in a long-term temperature and nutrient manipulation experiment. Plant Soil 374:73–88.

    Article  CAS  Google Scholar 

  • Lilleskov EA, Hobbie EA, Fahey TJ. 2002. Ectomycorrhizal fungal taxa differing in response to nitrogen deposition also differ in pure culture organic nitrogen use and natural abundance of nitrogen isotopes. New Phytol 154:219–31.

    Article  CAS  Google Scholar 

  • Lilleskov EA, Hobbie EA, Horton TR. 2011. Conservation of ectomycorrhizal fungi: exploring the linkages between functional and taxonomic responses to anthropogenic N deposition. Fungal Ecol 4:174–83.

    Article  Google Scholar 

  • Liu D, Keiblinger KM, Schindlbacher A, Wegner U, Sun H, Fuchs S, Lassek C, Riedel K, Zechmeister-Boltenstern S. 2017. Microbial functionality as affected by experimental warming of a temperate mountain forest soil—a metaproteomics survey. Appl Soil Ecol 117–118:196–202.

    Article  Google Scholar 

  • Majdi H, Öhrvik J. 2004. Interactive effects of soil warming and fertilization on root production, mortality, and longevity in a Norway spruce stand in Northern Sweden. Glob Change Biol 10:182–8.

    Article  Google Scholar 

  • Makita N, Hirano Y, Yamanaka T, Yoshimura K, Kosugi Y. 2012. Ectomycorrhizal-fungal colonization induces physio-morphological changes in Quercus serrata leaves and roots. J Plant Nutr Soil Sci 175:900–6.

    Article  CAS  Google Scholar 

  • McCormack ML, Adams TS, Smithwick EAH, Eissenstat DM. 2012. Predicting fine root lifespan from plant functional traits in temperate trees. New Phytol 195:823–31.

    Article  Google Scholar 

  • McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB, Leppälammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M. 2015. Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–18.

    Article  PubMed  Google Scholar 

  • McCormack ML, Guo DL. 2014. Impacts of environmental factors on fine root lifespan. Front Plant Sci 5:1–11.

    Article  Google Scholar 

  • Melillo JM, Frey SD, DeAngelis KM, Werner WJ, Bernard MJ, Bowles FP, Pold G, Knorr MA, Grandy AS. 2017. Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world. Science 358:101–5.

    Article  CAS  PubMed  Google Scholar 

  • Nishar A, Bader MK, Gorman EJO, Deng J, Breen B, Leuzinger S. 2017. Temperature effects on biomass and regeneration of vegetation in a geothermal area. Front Plant Sci 8:1–11.

    Article  Google Scholar 

  • Niu S, Classen AT, Dukes JS, Kardol P, Liu L, Luo Y, Rustad L, Sun J, Tang J, Templer PH, Thomas RQ, Tian D, Vicca S, Wang YP, Xia J, Zaehle S. 2016. Global patterns and substrate-based mechanisms of the terrestrial nitrogen cycle. Ecol Lett 19:697–709.

    Article  PubMed  Google Scholar 

  • Norby RJ, Luo Y. 2004. Evaluating ecosystem responses to rising atmospheric CO2 and global warming in a multi-factor world. New Phytol 162:281–93.

    Article  Google Scholar 

  • O’Gorman EJ, Benstead JP, Cross WF, Friberg N, Hood JM, Johnson PW, Sigurdsson BD, Woodward G. 2014. Climate change and geothermal ecosystems: natural laboratories, sentinel systems, and future refugia. Glob Change Biol 20:3291–9.

    Article  Google Scholar 

  • Ostonen I, Helmisaari H-S, Borken W, Tedersoo L, Kukumägi M, Bahram M, Lindroos A-J, Nöjd P, Uri V, Merilä P, Asi E, Lõhmus K. 2011. Fine root foraging strategies in Norway spruce forests across a European climate gradient. Glob Change Biol 17:3620–32.

    Article  Google Scholar 

  • Ostonen I, Lõhmus K, Helmisaari H-S, Truu J, Meel S. 2007a. Fine root morphological adaptations in Scots pine, Norway spruce and silver birch along a latitudinal gradient in boreal forests. Tree Physiol 27:1627–34.

    Article  PubMed  Google Scholar 

  • Ostonen I, Lõhmus K, Lasn R. 1999. The role of soil conditions in fine root ecomorphology in Norway spruce (Picea abies (L.) Karst.). Plant Soil 208:283–92.

    Article  CAS  Google Scholar 

  • Ostonen I, Püttsepp Ü, Biel C, Alberton O, Bakker MR, Lõhmus K, Majdi H, Metcalfe D, Olsthoorn AFM, Pronk A, Vanguelova E, Weih M, Brunner I. 2007b. Specific root length as an indicator of environmental change. Plant Biosyst 141:426–42.

    Article  Google Scholar 

  • Ostonen I, Rosenvald K, Helmisaari H-S, Godbold D, Parts K, Uri V, Lõhmus K. 2013. Morphological plasticity of ectomycorrhizal short roots in Betula sp and Picea abies forests across climate and forest succession gradients: its role in changing environments. Front Plant Sci 4:335.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ostonen I, Tedersoo L, Suvi T, Lõhmus K. 2009. Does a fungal species drive ectomycorrhizal root traits in Alnus spp.? Can J For Res 39:1787–96.

    Article  CAS  Google Scholar 

  • Ostonen I, Truu M, Helmisaari H-S, Lukac M, Borken W, Vanguelova E, Godbold DL, Lõhmus K, Zang U, Tedersoo L, Preem J-K, Rosenvald K, Aosaar J, Armolaitis K, Frey J, Kabral N, Kukumägi M, Leppälammi-Kujansuu J, Lindroos A-J, Merilä P, Napa Ü, Nöjd P, Parts K, Uri V, Varik M, Truu J. 2017. Adaptive root foraging strategies along a boreal-temperate forest gradient. New Phytol 215:977–91.

    Article  CAS  PubMed  Google Scholar 

  • Parts K, Tedersoo L, Lõhmus K, Kupper P, Rosenvald K, Sõber A, Ostonen I. 2013. Increased air humidity and understory composition shape short root traits and the colonizing ectomycorrhizal fungal community in silver birch stands. For Ecol Manag 310:720–8.

    Article  Google Scholar 

  • Peñuelas J, Poulter B, Sardans J, Ciais P, Van Der Velde M, Bopp L, Boucher O, Godderis Y, Hinsinger P, Llusia J, Nardin E, Vicca S, Obersteiner M, Janssens IA. 2013. Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nat Commun 4:2934.

    Article  CAS  PubMed  Google Scholar 

  • Pold G, DeAngelis KM. 2013. Up against the wall: the effects of climate warming on soil microbial diversity and the potential for feedbacks to the carbon cycle. Diversity 5:409–25.

    Article  CAS  Google Scholar 

  • Prietzel J, Christophel D. 2014. Organic carbon stocks in forest soils of the German Alps. Geoderma 221–222:28–39.

    Article  CAS  Google Scholar 

  • Richardson AE, Barea J-M, McNeill AM, Prigent-Combaret C. 2009. Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–39.

    Article  CAS  Google Scholar 

  • Rinnan R, Michelsen A, Bååth E, Jonasson S. 2007. Fifteen years of climate change manipulations alter soil microbial communities in a subarctic heath ecosystem. Glob Change Biol 13:28–39.

    Article  Google Scholar 

  • Rosenstock NP, Ellström M, Oddsdottir E, Sigurdsson BD, Wallander H. 2018. Carbon sequestration and community composition of ectomycorrhizal fungi across a geothermal warming gradient in an Icelandic spruce forest. Fungal Ecol [Accepted].

  • Rosenvald K, Ostonen I, Truu M, Truu J, Uri V, Vares A, Lõhmus K. 2011. Fine-root rhizosphere and morphological adaptations to site conditions in interaction with tree mineral nutrition in young silver birch (Betula pendula Roth.) stands. Eur J For Res 130:1055–66.

    Article  Google Scholar 

  • Schindlbacher A, Rodler A, Kuffner M, Kitzler B, Sessitsch A, Zechmeister-Boltenstern S. 2011. Experimental warming effects on the microbial community of a temperate mountain forest soil. Soil Biol Biochem 43:1417–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schindlbacher A, Schnecker J, Takriti M, Borken W, Wanek W. 2015. Microbial physiology and soil CO2 efflux after 9 years of soil warming in a temperate forest—no indications for thermal adaptations. Glob Change Biol 21:4265–77.

    Article  Google Scholar 

  • Schindlbacher A, Zechmeister-Boltenstern S, Jandl R. 2009. Carbon losses due to soil warming: do autotrophic and heterotrophic soil respiration respond equally? Glob Change Biol 15:901–13.

    Article  Google Scholar 

  • Schnecker J, Borken W, Schindlbacher A, Wanek W. 2016. Little effects on soil organic matter chemistry of density fractions after seven years of forest soil warming. Soil Biol Biochem 103:300–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sigurdsson BD, Leblans NIW, Dauwe S, Guðmundsdóttir E, Gundersen P, Gunnarsdóttir GE, Holmstrup M, Ilieva-Makulec K, Kätterer T, Marteinsdóttir B, Maljanen M, Oddsdóttir ES, Ostonen I, Peñuelas J, Poeplau C, Richter A, Sigurðsson P, Van Bodegom P, Wallander H, Weedon J, Janssens I. 2016. Geothermal ecosystems as natural climate change experiments : the ForHot research site in Iceland as a case study. Icelandic Agric Sci 29:53–71.

    Article  Google Scholar 

  • Solly EF, Lindahl BD, Dawes MA, Peter M, Souza RC, Rixen C, Hagedorn F. 2017. Experimental soil warming shifts the fungal community composition at the alpine treeline. New Phytol 215:766–78.

    Article  CAS  PubMed  Google Scholar 

  • StatSoft I. 2005. STATISTICA (data analysis software system), version 7.1. www.statsoft.com.

  • Taylor LL, Leake JR, Quirk J, Hardy K, Banwart SA, Beerling DJ. 2009. Biological weathering and the long-term carbon cycle: integrating mycorrhizal evolution and function into the current paradigm. Geobiology 7:171–91.

    Article  CAS  PubMed  Google Scholar 

  • Tedersoo L, Kõljalg U, Hallenberg N, Larsson K. 2003. Fine scale distribution of ectomycorrhizal fungi and roots across substrate layers including coarse woody debris in a mixed forest. New Phytol 159:153–65.

    Article  CAS  Google Scholar 

  • Tedersoo L, Naadel T, Bahram M, Pritsch K, Buegger F, Leal M, Kõljalg U, Põldmaa K. 2012. Enzymatic activities and stable isotope patterns of ectomycorrhizal fungi in relation to phylogeny and exploration types in an afrotropical rain forest. New Phytol 195:832–43.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • ter Braak CJF, Šmilauer P. 2002. CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca, NY, USA. http: www.pri.wur.nl/uk/products/canoco/.

  • Þorbjörnsson D, Sæmundsson K, Kristinsson S, Kristjánsson B, Ágústsson K. 2009. Suðurlandsskjálftar 29. maí 2008. Áhrif á grunnvatnsborð, hveravirkni og sprungumyndun [The South Iceland earthquake on 29th of May 2008. Impacts on groundwater levels, activity of geothermal hot-spots and creation of seismic cracks]. Rep. No. ÍSOR-2009/0. Unnið fyrir Orkuveitu Reykjavíkur, Iceland Geosurvey, Reykjavik, Iceland.

  • Treseder KK, Marusenko Y, Romero-Olivares AL, Maltz MR. 2016. Experimental warming alters potential function of the fungal community in boreal forest. Glob Change Biol 22:3395–404.

    Article  Google Scholar 

  • Truu M, Ostonen I, Preem J-K, Lõhmus K, Nõlvak H, Ligi T, Rosenvald K, Parts K, Kupper P, Truu J. 2017. Elevated air humidity changes soil bacterial community structure in the silver birch stand. Front Microbiol 8:557.

    Article  PubMed  PubMed Central  Google Scholar 

  • Valverde-Barrantes OJ, Smemo KA, Feinstein LM, Kershner MW, Blackwood CB. 2015. Aggregated and complementary: symmetric proliferation, overyielding, and mass effects explain fine-root biomass in soil patches in a diverse temperate deciduous forest landscape. New Phytol 205:731–42.

    Article  Google Scholar 

  • van der Heijden EW, Kuyper TW. 2003. Ecological strategies of ectomycorrhizal fungi of Salix repens: root manipulation versus root replacement. Oikos 103:668–80.

    Article  Google Scholar 

  • Wahl S, Ryser P. 2000. Root tissue structure is linked to ecological strategies of grasses. New Phytol 148:459–71.

    Article  Google Scholar 

  • Wan S, Norby RJ, Pregitzer KS, Ledford J, O’Neill EG. 2004. CO2 enrichment and warming of the atmosphere enhance both productivity and mortality of maple tree fine roots. New Phytol 162:437–46.

    Article  Google Scholar 

  • Weemstra M, Mommer L, Visser EJW, van Ruijven J, Kuyper TW, Mohren GMJ, Sterck FJ. 2016. Towards a multidimensional root trait framework: a tree root review. New Phytol 211:1159–69.

    Article  CAS  PubMed  Google Scholar 

  • Wells CE, Eissenstat DM. 2001. Marked differences in survivorship among apple roots of different diameters. Ecology 82:882–92.

    Article  Google Scholar 

  • Xu Z, Yin H, Xiong P, Wan C, Liu Q. 2012. Short-term responses of Picea asperata seedlings of different ages grown in two contrasting forest ecosystems to experimental warming. Environ Exp Botany 77:1–11.

    Article  Google Scholar 

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Acknowledgements

We thank Krista Lõhmus for valuable discussions, Kessy Abarenkov for guidance with uploading the EcM fungal sequences, and Aale Puri, Aulis Puri, Laura Soon and Marta Arula for assistance in the laboratory. We acknowledge the EU through the European Regional Development Fund (Center of Excellence ENVIRON and EcolChange), the Estonian Ministry of Education, Research projects IUT2-16, IUT34-9 and Lydia and Felix Krabi Scholarship Fund for financial support. We are very grateful to ExpeER for financing the field work of Kaarin Parts and analyses of EcM fungal community samples at the Achenkirch experimental area. This work contributes to the Icelandic ForHot-Forest Project (IRF Fund, No. 163272-051), the CAR-ES Nordic Network, the ClimMani (ES1308) and the Biolink COST Actions (FP1305).

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Authors and Affiliations

  1. Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51014, Tartu, Estonia

    Kaarin Parts & Ivika Ostonen

  2. Natural History Museum and Botanical Garden, University of Tartu, Ravila 14a, 50411, Tartu, Estonia

    Leho Tedersoo

  3. Department of Forest Ecology, Federal Research and Training Centre for Forests, Natural Hazards and Landscape – BFW, Vienna, Austria

    Andreas Schindlbacher

  4. Agricultural University of Iceland, 311, Hvanneyri, Borgarnes, Iceland

    Bjarni D. Sigurdsson

  5. CREAF, 08193, Cerdanyola del Vallés, Spain

    Bjarni D. Sigurdsson

  6. CSIC, Global Ecology Unit, CREAF-CSIC, Universitat Autònoma de Barcelona, 08193, Bellaterra, Catalonia, Spain

    Bjarni D. Sigurdsson

  7. Department of Biology, University of Antwerp, Antwerp, Belgium

    Niki I. W. Leblans

  8. Icelandic Forest Research Mógilsá, 162, Reykjavik, Iceland

    Edda S. Oddsdóttir

  9. Department of Soil Ecology, University of Bayreuth, Bayreuth, Germany

    Werner Borken

Authors
  1. Kaarin Parts
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  2. Leho Tedersoo
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  3. Andreas Schindlbacher
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  4. Bjarni D. Sigurdsson
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  5. Niki I. W. Leblans
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  6. Edda S. Oddsdóttir
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  7. Werner Borken
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  8. Ivika Ostonen
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Corresponding author

Correspondence to Kaarin Parts.

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Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Published database given in below link: https://doi.org/10.5281/zenodo.1299492.

Author Contributions

IO, AS, BDS and ESO conceived of or designed study, KP, IO, AS, BDS, WB and NIWL performed research, KP and IO analyzed data, IO, LT, BDS and AS contributed new methods or models, and KP wrote the paper.

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Parts, K., Tedersoo, L., Schindlbacher, A. et al. Acclimation of Fine Root Systems to Soil Warming: Comparison of an Experimental Setup and a Natural Soil Temperature Gradient. Ecosystems 22, 457–472 (2019). https://doi.org/10.1007/s10021-018-0280-y

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  • DOI: https://doi.org/10.1007/s10021-018-0280-y

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