, Volume 22, Issue 4, pp 437–447 | Cite as

Photosynthetic responses of birch and alder saplings grown in a free air CO2 enrichment system in northern Japan

  • Norikazu Eguchi
  • Kazuki Karatsu
  • Tatsushiro Ueda
  • Ryo Funada
  • Kentaro Takagi
  • Tsutom Hiura
  • Kaichiro Sasa
  • Takayoshi KoikeEmail author
Original Paper


Though birch and alder are the common pioneer tree species which dominate in northeast Asia, little is known about the effects of the predicted increase in atmospheric CO2 concentrations ([CO2]) upon their photosynthesis in field conditions. To investigate this, we grew 2-year-old saplings of three Betulaceae species (Betula platyphylla var. japonica Hara, Betula maximowicziana Regel, and Alnus hirsuta Turcz) for 2 years in a free air CO2 enrichment system in northern Japan. Since the effect of high [CO2] is known to depend on soil conditions, we evaluated the responses in two soils which are widely distributed in northern Japan: infertile and immature volcanic ash (VA) soil, and fertile brown forest (BF) soil. For B. platyphylla, photosynthetic down-regulation occurred in both soils, but for B. maximowicziana, down-regulation occurred only in VA soil. The explanation is reduced nitrogen and Rubisco content in the leaf. For A. hirsuta, down-regulation occurred only in BF soil because of the accumulation of starch in foliage, which restricts CO2 diffusion inside the chloroplast. The higher photosynthetic rate of A. hirsuta in infertile VA soil could be due to the sink for photosynthates in the N2-fixing symbiont. These three species are all able to down-regulate at high [CO2]. However, it is possible that A. hirsuta would dominate in VA soil and B. maximowicziana in BF soil in the early stages of forest succession in a CO2-enhanced world.


Alnus Betula East-Asia FACE Photosynthetic down-regulation 



This study was supported partly by the Research Revolution 2002 project of the Ministry of Education, Sport, Culture, Science and Technology of Japan; by Japan Society for the Promotion of Science (JSPS) Research Fellowships for Young Scientists to N.E.; and by a JSPS Basic Research A grant to T.K. We thank Prof. Ch. Körner, Prof. R. Oren, and Dr. R. Häsler for advice in constructing the FACE system. We also thank Dr. D.T. Tissue, Dr. R.F. Sage, Dr. R.J. Norby, Dr. S. Linder, and Dr. U. Lüttke for valuable comments on a previous draft.


  1. Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–372PubMedCrossRefGoogle Scholar
  2. Araki M (1999) Analysis of physical trait of soil with sampling cylinder. In: Arimitsu K, Sasa K, Takeda H, Tanimoto T, Ikuhara K, Hattori S, Yamamoto S, Yagi H (eds) Investigation approach in forest environment. Hakuyusya, Tokyo, pp 172–173 (In Japanese)Google Scholar
  3. Arp WJ (1991) Effects of source-sink relations on photosynthetic acclimation to elevated CO2. Plant Cell Environ 14:869–875CrossRefGoogle Scholar
  4. Beerling DJ (1999) Long-term responses of boreal vegetation to global change: an experimental and modeling investigation. Glob Chang Biol 5:55–74CrossRefGoogle Scholar
  5. Ceulemans R, Mousseau M (1994) Effects of elevated atmospheric CO2 on woody-plants. New Phytol 127:425–446CrossRefGoogle Scholar
  6. Coleman JS, McConnaughay KDM, Bazzaz FA (1993) Elevated CO2 and plant nitrogen-use: is reduced tissue nitrogen concentration size-dependent? Oecologia 93:195–200CrossRefGoogle Scholar
  7. Cushman SA, Wallin DO (2002) Separating the effects of environmental, spatial and disturbance factors on forest community structure in the Russian Far East. For Ecol Manage 168:201–215CrossRefGoogle Scholar
  8. Davey PA, Olcer H, Zakhleniuk O, Bernacchi CJ, Calfapietra C, Long SP, Raines CA (2006) Can fast-growing plantation trees escape biochemical down-regulation of photosynthesis when grown throughout their complete production cycle in the open air under elevated carbon dioxide? Plant Cell Environ 29:1235–1244PubMedCrossRefGoogle Scholar
  9. Drake BG, Gonzàles-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annu Rev Plant Physiol Plant Mol Biol 48:609–639PubMedCrossRefGoogle Scholar
  10. Eguchi N, Fukatsu E, Funada R, Tobita H, Kitao M, Maruyama Y, Koikes T (2004) Changes in morphology, anatomy, and photosynthetic capacity of needles of Japanese larch (Larix kaempferi) seedlings grown in high CO2 concentrations. Photosynthetica 42:173–178CrossRefGoogle Scholar
  11. Ehret DL, Jolliffe PA (1985) Leaf injury to bean-plants grown in carbon-dioxide enriched atmospheres. Can J Bot 63:2015–2020Google Scholar
  12. Faraway JJ (2006) Random Effects. In: Extending the linear model with R. Chapman Hall/CRC, Boca Raton, pp 153–183Google Scholar
  13. Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345CrossRefGoogle Scholar
  14. Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90CrossRefGoogle Scholar
  15. Fukui S (1990) Determination of sugar based on the sulfuric acid treatment. In: Determination of reducing sugar. 2nd edn. Gakkai Syuppan Center, Tokyo, pp 49–59 (In Japanese) Google Scholar
  16. Grishin SY (1995) The boreal forests of north-eastern Eurasia. Plant Ecol 121:11–21CrossRefGoogle Scholar
  17. Hacin JI, Bohlool BB, Singleton PW (1997) Partitioning of 14C-labeled photosynthate to developing nodules and roots of soybean (Glycine max). New Phytol 137:257–265CrossRefGoogle Scholar
  18. Hättenschwiler S, Hanada IT, Egli L, Asshoff R, Ammann W, Körner Ch (2002) Atmospheric CO2 enrichment of alpine treeline conifers. New Phytol 156:363–375CrossRefGoogle Scholar
  19. Hendry GR, Miglietta F (2006) FACE technology: past, present, and future. In: Nösberger J, Long SP, Norby RJ, Stitt M, Hendrey GR, Blum H (eds) Managed ecosystems and CO2. Springer, New York, pp 15–43Google Scholar
  20. Hibbs DE, Chan SS, Castellano M, Niu CH (1995) Response of red alder seedlings to CO2 enrichment and water-stress. New Phytol 129:569–577CrossRefGoogle Scholar
  21. Hyvönen R, Ågren GI, Linder S, Persson T, Cotrufo MF, Ekblad A, Freeman M, Grelle A, Janssens IA, Jarvis PG, Kellomäki S, Lindroth A, Loustau D, Lundmark T, Norby RJ, Oren R, Pilegaard K, Ryan MG, Sigurdsson BD, Strömgren M, van Oijen M, Wallin G (2007) The likely impact of elevated [CO2], nitrogen deposition, increased temperature and management on carbon sequestration in temperate and boreal forest ecosystems: a literature review. New Phytol 173:463–480PubMedCrossRefGoogle Scholar
  22. Kato Y (1983) Generation mechanism of volcanic ash soil. In: Takai Y (ed) Volcanic ash soil. Hakuyusha, Tokyo, pp 5–30 (In Japanese)Google Scholar
  23. Kikuzawa K (1982) Leaf survival and evolution in Betulaceae. Ann Bot 50:345–353Google Scholar
  24. Kimura W (1991) Revegetation process on a sub-alpine mudflow. Ecol Res 6:63–77CrossRefGoogle Scholar
  25. 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 troposphere O3. Oecologia 128:237–250CrossRefGoogle Scholar
  26. Kitaoka S, Koike T (2005) Seasonal and yearly variation in light use and nitrogen use by seedlings of four deciduous broad-leaved tree species invading larch plantations. Tree Physiol 25:467–475PubMedGoogle Scholar
  27. Koehler LH (1952) Differentiation of carbohydrates by anthrone reaction rate and color intensity. Anal Chem 24:1576–1579CrossRefGoogle Scholar
  28. Koike T (1988) Leaf structure and photosynthetic performance as related to the forest succession of deciduous broad-leaved trees. Plant Sp Biol 3:77–87CrossRefGoogle Scholar
  29. Koike T (1995) Effects of CO2 in interaction with temperature and soil fertility on the foliar phenology of alder, birch, and maple seedlings. Can J Bot 73:149–157CrossRefGoogle Scholar
  30. Koike T, Sakagami Y (1985) Comparison of the photosynthetic responses to temperature and light of Betula maximowicziana and Betula platyphylla var. japonica. Can J For Res 15:631–635CrossRefGoogle Scholar
  31. Koike T, Lei TT, Maximov R, Tabuchi R, Takahashi K, Ivanov BI (1996) Comparison of the photosynthetic capacity of Siberian and Japanese birch seedlings grown in elevated CO2 and temperature. Tree Physiol 16:381–385PubMedGoogle Scholar
  32. Koike T, Izuta T, Lei TT, Kitao M, Asanuma S (1997) Effects of high CO2 on nodule formation in roots of Japanese mountain alder seedling grown under two nutrient level. In: Ando T (ed) Plant nutrition—for sustainable food production and environment. Kluwer, Japan, pp 887–888Google Scholar
  33. Koike T, Kitao M, Quoreshi AM, Matsuura Y (2003) Growth characteristics of root-shoot relations of three birch seedlings raised under different water regimes. Plant Soil 255:303–310CrossRefGoogle Scholar
  34. Körner Ch (2000) Biosphere responses to elevated CO2 enrichment. Ecol Appl 10:1590–1619Google Scholar
  35. Körner Ch (2003) Carbon limitation in trees. J Ecol 91:4–17CrossRefGoogle Scholar
  36. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685PubMedCrossRefGoogle Scholar
  37. Levy PE, Lucas ME, Mckay HM, Escobar-Gutierres AJ, Rey A (2000) Testing process-based model of tree seedling growth by manipulating [CO2] and nutrient uptake. Tree Physiol 20:993–1005PubMedGoogle Scholar
  38. Liberloo M, Tulva I, Raïm O, Kull O, Ceulemans R (2007) Photosynthetic stimulation under long-term CO2 enrichment and fertilization is sustained across a closed Populus canopy profile (EUROFACE). New Phytol 173:537–549PubMedCrossRefGoogle Scholar
  39. Luo Y, Reynolds J, Wang Y, Wolfe D (1999) A search for predictive understanding of plant responses to elevated [CO2]. Glob Chang Biol 5:143–156CrossRefGoogle Scholar
  40. Makino A (1994) Biochemistry of C3-photosynthesis in high CO2. J Plant Res 107:79–84CrossRefGoogle Scholar
  41. Makino A, Mae T, Ohira K (1988) Differences between wheat and rice in the enzymic properties of ribrose-1,5-bisphosphate carboxylase/oxygenase and the relationship to photosynthetic gas exchange. Planta 174:30–38CrossRefGoogle Scholar
  42. Matsuda K, Shibuya M, Koike T (2002) Maintenance and rehabilitation of the mixed conifer-broadleaved forests in Hokkaido, northern Japan. Eurasian J For Res 5:119–130Google Scholar
  43. Matsui K (2001) Classification of soil production. In: Asami S (eds) University textbook of soil geography. Kokonshoin, Tokyo, pp 7–30. (In Japanese)Google Scholar
  44. Matsuki S (2003) Specific characteristics of anti-herbivore defense of deciduous broad-leaved trees in Betulaceae. PhD thesis, Hokkaido University, Japan (In Japanese)Google Scholar
  45. Melillo JM, McGuire AD, Kicklighter DW, Moore III B, Vorosmarty CJ, Schloss AL (1993) Global climate change and terrestrial net primary production. Nature 363:234–240CrossRefGoogle Scholar
  46. 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
  47. Nowak RS, Ellsworth DS, Smith SD (2004) Functional responses of plants to elevated atmospheric CO2—do photosynthetic and productivity data from FACE experiments support early predictions? New Phytol 162:253–280CrossRefGoogle Scholar
  48. Rey A, Jarvis PG (1998) Long-term photosynthetic acclimation to increased atmospheric CO2 concentration in young birch (Betula pendula) tree. Tree Physiol 18:441–450PubMedGoogle Scholar
  49. Rogers A, Ellsworth DS (2002) Photosynthetic acclimation of Pinus taeda (loblolly pine) to long-term growth in elevated pCO2 (FACE). Plant Cell Environ 25:851–858CrossRefGoogle Scholar
  50. Sage RF, Sharkey TD, Seemann JR (1989) Acclimation of photosynthesis to elevated CO2 in five C3 species. Plant Physiol 89:590–596PubMedCrossRefGoogle Scholar
  51. Saxe H, Ellsworth DS, Heath J (1998) Tree and forest functioning in an enriched CO2 atmosphere. New Phytol 139:395–436CrossRefGoogle Scholar
  52. Sigurdsson BD (2001) Elevated [CO2] and nutrient status modified leaf phenology and growth rhythm of young Populus trichocarpa trees in a 3-year field study. Trees 15:403–413CrossRefGoogle Scholar
  53. Sigurdsson BD, Roberntz P, Freeman M, Næss M, Saxe HS, Thorgeirsson H, Linder S (2002) Impact studies on Nordic forests: effects of elevated CO2 and fertilization on gas exchange. Can J For Res 32:770–788CrossRefGoogle Scholar
  54. Steel RGD, Torrie JH (1980) Principles and procedures of statistics: a biometrical approach. McGraw Hill, New YorkGoogle Scholar
  55. Stitt M (1991) Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. Plant Cell Environ 14:741–762CrossRefGoogle Scholar
  56. Tamm CO (1991) Nitrogen in terrestrial ecosystems. Ecological studies 81. Springer, Heidelberg, pp 115Google Scholar
  57. Takagi K, Eguchi N, Ueda T, Sasa K, Koike T (2004) CO2 control in a FACE system for tree saplings. J Agr Meteorol 56:9–16 (In Japanese)Google Scholar
  58. Temperton VM, Grayston SJ, Jackson G, Barton CVM, Millard P, Jarvis PG (2003) Effects of elevated carbon dioxide concentration on growth and nitrogen fixation in Alunus glutinosa in a long-term field experiment. Tree Physiol 23:1051–1059PubMedGoogle Scholar
  59. Tissue DT, Megonigal JP, Thomas RB (1997) Nitrogenase activity and N2 fixation are stimulated by elevated CO2 in a tropical N2-fixing tree. Oecologia 109:28–33CrossRefGoogle Scholar
  60. Tjepkema JD, Schwintzer CR, Benson DR (1986) Physiology of actinorhizal nodules. Annu Rev Plant Physiol 37:209–232CrossRefGoogle Scholar
  61. Tobita H, Kitao M, Koike T, Maruyama Y (2005) Effects of elevated CO2 and nitrogen availability on nodulation of Alnus hirsuta (Turcz.). Phyt Ann Rei Bot 45:25–131Google Scholar
  62. Usuda H (2004) Effects of growth under elevated CO2 on the capacity of photosynthesis in two radish cultivars differing in capacity of storage root. Plant Prod Sci 7:377–385CrossRefGoogle Scholar
  63. Urban O (2003) Physiological impacts of elevated CO2 concentration ranging from molecular to whole plant responses. Photosynthetica 41:9–20CrossRefGoogle Scholar
  64. Vogel CS, Curtis PS (1995) Leaf gas-exchange and nitrogen dynamics of N2-fixing field-grown Alnus glutinosa under elevated atmospheric CO2. Glob Chang Biol 1:55–61CrossRefGoogle Scholar
  65. Vogel CS, Curtis PS, Thomas RB (1997) Growth and nitrogen accretion of dinitrogen-fixing Alnus glutinosa (L.) Gaertn. under elevated carbon dioxide. Plant Ecol 130:63–70CrossRefGoogle Scholar
  66. von Caemmerer S, Evans JE, Hudson GS, Andrews TJ (1994) The kinetics of ribulose-1,5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco. Planta 195:88–97CrossRefGoogle Scholar
  67. Wang YP, Rey A, Jarvis PG (1998) Carbon balance of young birch trees grown in ambient and elevated atmospheric CO2 concentration. Glob Chang Biol 4:797–807CrossRefGoogle Scholar
  68. Yazaki K, Funada R, Mori S, Maruyama Y, Abaimov AP, Kayama M, Koike T (2001) Growth and annual ring structure of Larix sibirica grown at different carbon dioxide concentrations and nutrient supply rates. Tree Physiol 21:1223–1229PubMedGoogle Scholar
  69. Zanetti S, Hartwig UA, Nösberger J (1998) Elevated atmospheric CO2 does not affect per se the preference for symbiotic nitrogen as opposed to mineral nitrogen of Trifolium repens L. Plant Cell Environ 21:623–630CrossRefGoogle Scholar
  70. Zotz G, Pepin S, Körner Ch (2005) No down-regulation of leaf photosynthesis in mature forest trees after three years of exposure to elevated CO2. Plant Biol 7:369–374PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Norikazu Eguchi
    • 1
  • Kazuki Karatsu
    • 1
  • Tatsushiro Ueda
    • 2
  • Ryo Funada
    • 3
  • Kentaro Takagi
    • 4
  • Tsutom Hiura
    • 4
  • Kaichiro Sasa
    • 4
  • Takayoshi Koike
    • 1
    • 4
    Email author
  1. 1.Graduate School of AgricultureHokkaido UniversitySapporoJapan
  2. 2.Hokkaido DALTONSapporoJapan
  3. 3.Faculty of AgricultureTokyo University of Agriculture and TechnologyFuchu-TokyoJapan
  4. 4.Department of Forest ScienceHokkaido UniversitySapporoJapan

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