, Volume 30, Issue 2, pp 363–374 | Cite as

Fine root turnover of Japanese white birch (Betula platyphylla var. japonica) grown under elevated CO2 in northern Japan

  • Xiaona WangEmail author
  • Saki Fujita
  • Tatsuro Nakaji
  • Makoto Watanabe
  • Fuyuki Satoh
  • Takayoshi KoikeEmail author
Original Paper


Key message

Elevated CO 2 reduced fine root dynamics (production and turnover) of white birch seedlings, especially grown in volcanic ash soil compared with brown forest soil.


Increased atmospheric CO2 usually enhances photosynthetic ability and growth of trees. To understand how increased CO2 affects below-ground part of trees under varied soil condition, we investigated the responses of the fine root (diameter <2 mm) dynamics of Japanese white birch (Betula platyphylla var. japonica) which was planted in 2010. The three-year-old birch seedlings were grown in four experimental treatments comprising two levels of CO2, i.e., ambient: 380–390 and elevated: 500 μmol mol−1, in combination with two kinds of soil: brown forest (BF) soil and volcanic ash (VA) soil which has few nutrients. The growth and turnover of fine roots were measured for 3 years (2011–2013) using the Mini-rhizotron. In the first observation year, live fine root length (standing crop) in BF soil was not affected by CO2 treatment, but it was reduced by the elevated CO2 from the second observation year. In VA soil, live fine root length was reduced by elevated CO2 for all 3 years. Fine root turnover tended to decrease under elevated CO2 compared with ambient in both soil types during the first and second observation years. Turnover of fine root production and mortality was also affected by the two factors, elevated CO2 and different soil types. Median longevity of fine root increased under elevated CO2, especially in VA soil at the beginning, and a shorter fine root lifespan appeared after 2 years of observation (2011–2012). These results suggest that elevated CO2 does not consistently stimulate fine root turnover, particularly during the plant seedlings stage, as it may depend on the costs and benefits of constructing and retaining roots. Therefore, despite the other uncontrollable environment factors, carbon sequestration to the root system may be varied by CO2 treatment period, soil type and plant age.


Elevated CO2 Fine root longevity Mini-rhizotron Survival analysis Volcanic ash soil 



We thank Mr. Ito Hirotaka for his contribution of the installation of the Mini-rhizotron system. We also thank Prof. Heljä-Sisko Helmisaari and Dr. Jaana Leppälammi-Kujansuu for their guidance on data analysis. Thanks are also given to Dr. Anthony Garrett of SCITEXT of Cambridge, UK and Ms. Amelie Vanderstock of Biological Institute of The University of Sydney, Australia for English improvement. This study was supported by the Japan Society for the Promotion of Science New field and Type B program (to T. Koike, 21114008 and 26660119).

Compliance with ethical standards

Conflict of interest

We declare that our research has no conflict of interest.


  1. Aber JD, Melillo JM (2001) Terrestrial ecosystems. Saunders College Publishers, PhiladelphiaGoogle Scholar
  2. Agathokleous E, Watanabe M, Nakaji T, Wang X, Satoh F, Koike T (2015) Impact of elevated CO2 on root traits of a sapling community of three birches and an oak: a free-air-CO2 enrichment (FACE) in northern Japan. Trees Struct Funct. doi: 10.1007/s00468-015-1272-6 Google Scholar
  3. Andersson P, Majdi H (2005) Estimating root longevity at sites with long periods of low root mortality. Plant Soil 276:9–14CrossRefGoogle Scholar
  4. Arnone JA, Zaller JG, Spehn EM, Niklaus PA, Wells CE, Korner C (2000) Dynamics of root systems in native grasslands: effects of elevated atmospheric CO2 (vol 147, pp 73, 2000). New Phytol 147:411CrossRefGoogle Scholar
  5. Bidartondo MI, Ek H, Wallander H, Soderstrom B (2001) Do nutrient additions alter carbon sink strength of ectomycorrhizal fungi? New Phytol 151:543–550CrossRefGoogle Scholar
  6. Bielenberg DG, Bassirirad H (2005) Nutrient acquisition of terrestrial plants in a changing climate. In: Bassirirad H (ed) Nutrient acquisition by plants—an ecological perspective, vol 181. Springer, Berlin, pp 311–330CrossRefGoogle Scholar
  7. Brunner I, Godbold DL (2007) Tree roots in a changing world. J Forest Res 12:78–82CrossRefGoogle Scholar
  8. Eguchi N, Karatsu K, Ueda T, Funada R, Takagi K, Hiura T, Sasa K, Koike T (2008) Photosynthetic responses of birch and alder saplings grown in a free air CO2 enrichment system in northern Japan. Trees Struct Funct 22:437–447CrossRefGoogle Scholar
  9. Eissenstat DM, Wells CE, Yanai RD, Whitbeck JL (2000) Building roots in a changing environment: implications for root longevity. New Phytol 147:33–42CrossRefGoogle Scholar
  10. Eshel A, Beeckman T (2013) Plant roots: the hidden half, 4th edn. CRC Press, New YorkGoogle Scholar
  11. Finzi AC, Moore DJP, DeLucia EH, Lichter J, Hofmockel KS, Jackson RB, Kim HS, Matamala R, McCarthy HR, Oren R, Pippen JS, Schlesinger WH (2006) Progressive nitrogen limitation of ecosystem processes under elevated CO2 in a warm-temperate forest. Ecology 87:15–25CrossRefPubMedGoogle Scholar
  12. Fitter AH (2005) Darkness visible: reflections on underground ecology. J Ecol 93:231–243CrossRefGoogle Scholar
  13. Gill RA, Jackson RB (2000) Global patterns of root turnover for terrestrial ecosystems. New Phytol 147:13–31CrossRefGoogle Scholar
  14. Gill RA, Burke IC, Lauenroth WK, Milchunas DG (2002) Longevity and turnover of roots in the shortgrass steppe: influence of diameter and depth. Plant Ecol 159:241–251CrossRefGoogle Scholar
  15. Green IJ, Dawson LA, Proctor J, Duff EI, Elston DA (2005) Fine root dynamics in a tropical rain forest is influenced by rainfall. Plant Soil 276:23–32CrossRefGoogle Scholar
  16. Guo DL, Mitchell RJ, Hendricks JJ (2004) Fine root branch orders respond differentially to carbon source-sink manipulations in a longleaf pine forest. Oecologia 140:450–457CrossRefPubMedGoogle Scholar
  17. Hara Y (2014) Time course of leaf area index of three birches grown under free air CO2 enrichment (FACE) system. Master thesis, Hokkaido University, p 46Google Scholar
  18. Heeraman DA, Juma NG (1993) A comparison of minirhizotron, core and monolith methods for quantifying barley (Hordeum vulgare L.) and faba bean (Vicia faba L.) root distribution. Plant Soil 148:29–41CrossRefGoogle Scholar
  19. Hendrick RL, Pregitzer KS (1992) The demography of fine roots in a Northern Hardwood forest. Ecology 73:1094–1104CrossRefGoogle Scholar
  20. Hendrick RL, Pregitzer KS (1996) Applications of minirhizotrons to understand root function in forests and other natural ecosystems. Plant Soil 185:293–304CrossRefGoogle Scholar
  21. Higgins PAT, Jackson RB, Des Rosiers JM, Field CB (2002) Root production and demography in a California annual grassland under elevated atmospheric carbon dioxide. Global Change Biol 8:841–850CrossRefGoogle Scholar
  22. Hogberg P, Read DJ (2006) Towards a more plant physiological perspective on soil ecology. Trends Ecol Evol 21:548–554CrossRefPubMedGoogle Scholar
  23. Housman DC, Naumburg E, Huxman TE, Charlet TN, Nowak RS, Smith SD (2006) Increases in desert shrub productivity under elevated carbon dioxide vary with water availability. Ecosystems 9:374–385CrossRefGoogle Scholar
  24. Johnson DW (2006) Progressive N limitation in forests: review and implications for long-term responses to elevated CO2. Ecology 87:64–75CrossRefPubMedGoogle Scholar
  25. Joslin JD, Wolfe MH (1999) Disturbances during minirhizotron installation can affect root observation data. Soil Sci Soc Am J 63:218–221CrossRefGoogle Scholar
  26. Kayama M, Makoto K, Nomura M, Satoh F, Koike T (2009) Nutrient dynamics and carbon partitioning in larch seedlings (Larix kaempferi) regenerated on serpentine soil in northern Japan. Landsc Ecol Eng 5:125–135CrossRefGoogle Scholar
  27. King JS, Pregitzer KS, Zak DR, Sober J, Isebrands JG, Dickson RE, Hendrey GR, Karnosky DF (2001) Fine-root biomass and fluxes of soil carbon in young stands of paper birch and trembling aspen as affected by elevated atmospheric CO2 and tropospheric O3. Oecologia 128:237–250CrossRefGoogle Scholar
  28. King JS, Albaugh TJ, Allen HL, Buford M, Strain BR, Dougherty P (2002) Below-ground carbon input to soil is controlled by nutrient availability and fine root dynamics in loblolly pine. New Phytol 154:389–398CrossRefGoogle Scholar
  29. Koike T (1995) Physiological ecology of the growth characteristics of Japanese mountain birch in northern Japan: a comparison with Japanese mountain white birch. In: Box EO et al (eds) Vegetation science in forestry: global perspective based on forest ecosystems of east and southeast Asia. Kluwer Academic Publishers, The Netherlands, pp 409–422Google Scholar
  30. Koike T, Yazaki K, Eguchi N, Kitaoka S, Funada R (2010) Effects of elevated CO2 on ecophysiological responses of larch species native to Northeast Eurasia. In: Osawa A et al (eds) Permafrost ecosystem. Springer, New York, pp 447–458CrossRefGoogle Scholar
  31. Koike T, Mao QZ, Inada N, Kawaguchi K, Hoshika Y, Kita K, Watanabe M (2012) Growth and photosynthetic responses of cuttings of a hybrid larch (Larix gmelinii var. japonica x L. kaempferi) to elevated ozone and/or carbon dioxide. Asian J Atmos Environ 6:104–110CrossRefGoogle Scholar
  32. Koike T, Watanabe M, Watanabe Y, Agathokleous E, Eguchi N, Takagi K, Satoh F, Kitaoka S, Funada R (2015) Ecophysiology of deciduous trees native to Northeast Asia grown under FACE (free air CO2 enrichment). J Agr Meteol 71:in printGoogle Scholar
  33. Lal R (2005) Forest soils and carbon sequestration. Forest Ecol Manag 220:242–258CrossRefGoogle Scholar
  34. Lichter J, Barron SH, Bevacqua CE, Finzi AC, Irving KE, Stemmler EA, Schlesinger WH (2005) Soil carbon sequestration and turnover in a pine forest after six years of atmospheric CO2 enrichment. Ecology 86:1835–1847CrossRefGoogle Scholar
  35. Lukac M, Calfapietra C, Godbold DL (2003) Production, turnover and mycorrhizal colonization of root systems of three Populus species grown under elevated CO2 (POPFACE). Global Change Biol 9:838–848CrossRefGoogle Scholar
  36. Luo Y, Su B, Currie WS, Dukes JS, Finzi AC, Hartwig U, Hungate B, McMurtrie RE, Oren R, Parton WJ, Pataki DE, Shaw MR, Zak DR, Field CB (2004a) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54:731–739CrossRefGoogle Scholar
  37. Luo YQ, White L, Hui DF (2004b) Comment on “Impacts of fine root turnover on forest NPP and soil C sequestration potential”. Science 304:1745CrossRefPubMedGoogle Scholar
  38. Maeght JL, Rewald B, Pierret A (2013) How to study deep roots—and why it matters. Front Plant Sci. doi: 10.3389/fpls.2013.00299 PubMedPubMedCentralGoogle Scholar
  39. Majdi H (1996) Root sampling methods—applications and limitations of the minirhizotron technique. Plant Soil 185:255–258CrossRefGoogle Scholar
  40. Majdi H, Andersson P (2005) Fine root production and turnover in a Norway spruce stand in northern Sweden: effects of nitrogen and water manipulation. Ecosystems 8:191–199CrossRefGoogle Scholar
  41. Majdi H, Pregitzer K, Moren AS, Nylund JE, Agren GI (2005) Measuring fine root turnover in forest ecosystems. Plant Soil 276:1–8CrossRefGoogle Scholar
  42. Mao QZ (2013) Ecophysiological study on the growth responses of larch species to changing environments-effects of elevated CO2, O3 and high nitrogen loading. PhD thesis, Hokkaido University, p 123Google Scholar
  43. Matamala R, Schlesinger WH (2000) Effects of elevated atmospheric CO2 on fine root production and activity in an intact temperate forest ecosystem. Global Change Biol 6:967–979CrossRefGoogle Scholar
  44. Matamala R, Gonzalez-Meler MA, Jastrow JD, Norby RJ, Schlesinger WH (2003) Impacts of fine root turnover on forest NPP and soil C sequestration potential. Science 302:1385–1387CrossRefPubMedGoogle Scholar
  45. McNear DH Jr (2013) The rhizosphere—roots, soil and everything in between. Nature Educ Knowl 4:1Google Scholar
  46. Meehl GA, Stocker TF, Collins WD, Friedlingstein P, Gaye AT, Gregory JM, Kitoh A, Knutti R, Murphy JM, Noda A, Raper SCB, Watterson IG, Weaver AJ, Zhao ZC (2007) Global climate projections. In: Solomon S et al (eds) Climate change: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge Univ Press, Cambridge and New York, pp 747–846Google Scholar
  47. Naumburg E, Ellsworth DS, Katul GG (2001) Modeling dynamic understory photosynthesis of contrasting species in ambient and elevated carbon dioxide. Oecologia 126:487–499CrossRefGoogle Scholar
  48. Noormets A, McDonald EP, Dickson RE, Kruger EL, Sober A, Isebrands JG, Karnosky DF (2001a) The effect of elevated carbon dioxide and ozone on leaf- and branch-level photosynthesis and potential plant-level carbon gain in aspen. Trees Struct Funct 15:262–270CrossRefGoogle Scholar
  49. Noormets A, Sober A, Pell EJ, Dickson RE, Podila GK, Sober J, Isebrands JG, Karnosky DF (2001b) Stomatal and non-stomatal limitation to photosynthesis in two trembling aspen (Populus tremuloides Michx.) clones exposed to elevated CO2 and/or O3. Plant Cell Environ 24:327–336CrossRefGoogle Scholar
  50. Norby RJ, Jackson RB (2000) Root dynamics and global change: seeking an ecosystem perspective. New Phytol 147:3–12CrossRefGoogle Scholar
  51. Norby RJ, Zak DR (2011) Ecological lessons from free-air CO2 enrichment (FACE) experiments. Annu Rev Ecol Evol S 42:181–203CrossRefGoogle Scholar
  52. Norby RJ, Wullschleger SD, Gunderson CA, Johnson DW, Ceulemans R (1999) Tree responses to rising CO2 in field experiments: implications for the future forest. Plant Cell Environ 22:683–714CrossRefGoogle Scholar
  53. Norby RJ, Ledford J, Reilly CD, Miller NE, O’Neill EG (2004) Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment. Pro Natl Acad Sci USA 101:9689–9693CrossRefGoogle Scholar
  54. Oren R, Ellsworth DS, Johnsen KH, Phillips N, Ewers BE, Maier C et al (2001) Soil fertility limits carbon sequestration by forest ecosystems in a CO2-enriched atmosphere. Nature 411:469–472CrossRefPubMedGoogle Scholar
  55. Pregitzer KS, Hendrick RL, Fogel R (1993) The demography of fine roots in response to patches of water and nitrogen. New Phytol 125:575–580CrossRefGoogle Scholar
  56. Pregitzer KS, Laskowski MJ, Burton AJ, Lessard VC, Zak DR (1998) Variation in sugar maple root respiration with root diameter and soil depth. Tree Physiol 18:665–670CrossRefPubMedGoogle Scholar
  57. Pregitzer KS, Zak DR, Maziasz J, DeForest J, Curtis PS, Lussenhop J (2000) Interactive effects of atmospheric CO2 and soil-N availability on fine roots of Populus tremuloides. Ecol Appl 10:18–33Google Scholar
  58. Pritchard SG, Rogers HH (2000) Spatial and temporal deployment of crop roots in CO2-enriched environments. New Phytol 147:55–71CrossRefGoogle Scholar
  59. Pritchard SG, Davis MA, Mitchell RJ, Prior SA, Boykin DL, Rogers HH, Runion GB (2001a) Root dynamics in an artificially constructed regenerating longleaf pine ecosystem are affected by atmospheric CO2 enrichment. Environ Exp Bot 46:55–69CrossRefPubMedGoogle Scholar
  60. Pritchard SG, Rogers HH, Davis MA, Van Santen E, Prior SA, Schlesinger WH (2001b) The influence of elevated atmospheric CO2 on fine root dynamics in an intact temperate forest. Global Change Biol 7:829–837CrossRefGoogle Scholar
  61. Pritchard SG, Strand AE, McCormack ML, Davis MA, Finzi AC, Jackson RB, Matamala R, Rogers HH, Oren RAM (2008) Fine root dynamics in a loblolly pine forest are influenced by free-air-CO2-enrichment: a six-year-minirhizotron study. Global Change Bio 14:588–602CrossRefGoogle Scholar
  62. Qu LY, Shinano T, Quoreshi AM, Tamai Y, Osaki M, Koike T (2004) Allocation of 14C-carbon in two species of larch seedlings infected with ectomycorrhizal fungi. Tree Physiol 24:1369–1376CrossRefPubMedGoogle Scholar
  63. Ruess RW, Hendrick RL, Burton AJ, Pregitzer KS, Sveinbjornsson B, Allen MF, Maurer GE (2003) Coupling fine root dynamics with ecosystem carbon cycling in black spruce forests of interior Alaska. Ecol Monogr 73:643–662CrossRefGoogle Scholar
  64. Ryser P (2006) The mysterious root length. Plant Soil 286:1–6CrossRefGoogle Scholar
  65. Satomura T, Fukuzawa C, Horikoshi T (2007) Considerations in the study of tree fine-root turnover with minirhizotrons. Plant Root 1:34–45CrossRefGoogle Scholar
  66. Scarascia-Mugnozza GE, Karnosky DF, Ceulemans R, Innes JL (2001) The impact of CO2 and other greenhouse gases on forest ecosystems: an introduction. CABI publishing, ViennaGoogle Scholar
  67. Shi F, Sasa K, Koike T (2010) Characteristics of larch forests in Daxingan Mountains, Northeast China. In: Osawa A et al. (eds) Permafrost ecosystem: siberian larch forests. Ecological Studies 209, Springer, New York, pp 367–384Google Scholar
  68. Shinano T, Yamamoto T, Tawaraya K, Tadokoro M, Koike T, Osaki M (2007) Effects of elevated atmospheric CO2 concentration on the nutrient uptake characteristics of Japanese larch (Larix kaempferi). Tree Physiol 27:97–104CrossRefPubMedGoogle Scholar
  69. Takeuchi Y, Kubiske ME, Isebrands JG, Pregtizer KS, Hendrey G, Karnosky DF (2001) Photosynthesis, light and nitrogen relationships in a, young deciduous forest canopy under open-air CO2 enrichment. Plant Cell Environ 24:1257–1268CrossRefGoogle Scholar
  70. Terazawa M (2005) Tree sap III. Hokkaido University Press, Sapporo, p 204Google Scholar
  71. Tingey DT, Phillips DL, Johnson MG (2000) Elevated CO2 and conifer roots: effects on growth, life span and turnover. New Phytol 147:87–103CrossRefGoogle Scholar
  72. Tissue DT, Lewis JD (2010) Photosynthetic responses of cottonwood seedlings grown in glacial through future atmospheric CO2 vary with phosphorus supply. Tree Physiol 30:1361–1372CrossRefPubMedGoogle Scholar
  73. Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15CrossRefPubMedGoogle Scholar
  74. Wang XN, Qu L, Mao Q, Watanabe M, Hoshika Y, Koyama A, Kawaguchi A, Tamai Y, Koike T (2015) Ectomycorrhizal colonization and growth of the hybrid larch F1 under elevated CO2 and O3. Environ Pollut 197:116–126CrossRefPubMedGoogle Scholar
  75. Watanabe Y, Tobita H, Kitao M, Maruyama Y, Choi D, Sasa K, Funada R, Koike T (2008) Effects of elevated CO2 and nitrogen on wood structure related to water transport in seedlings of two deciduous broad-leaved tree species. Trees Struct Funct 22:403–411CrossRefGoogle Scholar
  76. Watanabe M, Umemoto-Yamaguchi M, Koike T, Izuta T (2010) Growth and photosynthetic response of Fagus crenata seedlings to ozone and/or elevated carbon dioxide. Landsc Ecol Eng 6:181–190CrossRefGoogle Scholar
  77. Yuan ZY, Chen HYH (2010) Fine root biomass, production, turnover rates, and nutrient contents in boreal forest ecosystems in relation to species, climate, fertility, and stand age: literature review and meta-analyses. Crit Rev Plant Sci 29:204–221CrossRefGoogle Scholar
  78. Zyryanova OA, Terazawa M, Koike T, Zyryanov VI (2010) White birch trees as resource species of Russia : their distribution, ecophysiological features, multiple utilizations. Eurasian J For Res 13:25–40Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Silviculture and Forest Ecological StudiesHokkaido UniversitySapporoJapan
  2. 2.Hokkaido University ForestsSapporoJapan
  3. 3.Tokyo University of Agriculture and TechnologyFuchuJapan

Personalised recommendations