Ecological Research

, Volume 30, Issue 2, pp 247–266 | Cite as

Phenology of leaf morphological, photosynthetic, and nitrogen use characteristics of canopy trees in a cool-temperate deciduous broadleaf forest at Takayama, central Japan

  • Hibiki M. NodaEmail author
  • Hiroyuki Muraoka
  • Kenlo Nishida Nasahara
  • Nobuko Saigusa
  • Shohei Murayama
  • Hiroshi Koizumi
Special Feature Long-term and interdisciplinary research on forest ecosystem functions: Challenges at Takayama site since 1993


We studied interannual variations in single-leaf phenology, i.e., temporal changes in leaf ecophysiological parameters that are responsible for forest canopy function, in a cool-temperate deciduous broadleaf forest at Takayama, central Japan. We conducted long-term in situ research from 2003 to 2010 (excluding 2008). We measured leaf mass per unit area (LMA), leaf chlorophyll and nitrogen contents, and leaf photosynthetic and respiratory characteristics [dark respiration, light-saturated photosynthetic rate (A max), maximum carboxylation rate (V cmax), and electron transport rate (J max)] of leaves of mature canopy trees of Betula ermanii Cham. and Quercus crispula Blume, from leaf expansion to senescence. All leaf characteristics changed markedly from leaf expansion (late May) through senescence (mid–late October). The photosynthetic capacity of B. ermanii leaves rapidly increased during leaf expansion and decreased during senescence, while that of Q. crispula leaves changed gradually. The relationships among LMA, photosynthetic capacity, and nitrogen content changed throughout the season. The timings (calendar dates) of leaf expansion, maturity, and senescence differed among the 7 years, indicating that interannual variations in micrometeorological conditions strongly affected leaf phenological events. We examined the seasonal changes as a function of the date or cumulative air temperatures. From leaf expansion to maturity, the increases in chlorophyll content, A max, V cmax, J max, and LMA were explained well by the growing-degree days, and their decreases in autumn were explained well by chilling-degree days. Our findings will be useful for predicting the effects of current variations in climatic conditions and future climate change on forest canopy structure and function.


Carbon cycle Forest canopy Phenology model Photosynthesis Respiration 



We thank K. Kurumado, M. Ohno, Y. Miyamoto, and Y. Hiomo of the Takayama field station, Gifu University, and the “Takayama Community” members, especially S. Yamamoto and H. Kondo of the National Institute of Advanced Industrial Science and Technology, A. Ito of the National Institute for Environmental Studies, T. Akiyama of Gifu University, T. Hiura of Hokkaido University, and J. D. Tenhunen of the University of Bayreuth, for their support during our field measurements and for encouragement during this long-term research. We also thank S. Kinoshita, Center for Environmental Measurement and Analysis, National Institute for Environmental Studies, for leaf nitrogen analyses. We thank the anonymous reviewers for their constructive comments on this manuscript. This long-term ecological research was supported by the Ministry of the Environment, Japan, as a Global Environment Research Fund project (S-1, PI: T. Oikawa). This work was also supported by the Japan Society for the Promotion of Science (JSPS) 21st Century COE Program (Satellite Ecology) at Gifu University, KAKENHI (JSPS grant no. 18710006 to HM), the JSPS-NRF-NSFC A3 Foresight Program (PI: H. Muraoka), the Environment Research and Technology Development Fund of the Ministry of Environment, Japan (D-0909, PI: T. Hiura), the Global Change Observation Mission of the Japan Aerospace Exploration Agency (PI#102), and the JSPS Funding Program for Next Generation World-Leading Researchers (to HM).


  1. Abrams MD, Mostoller SA (1995) Gas exchange, leaf structure and nitrogen in contrasting successional tree species growing in open and understory sites during a drought. Tree Physiol 15:361–370CrossRefPubMedGoogle Scholar
  2. Ahrends HE, Etzold S, Kutsch WL, Stoeckli R, Bruegger R, Jeanneret F, Wanner H, Buchmann N, Eugster W (2009) Tree phenology and carbon dioxide fluxes: use of digital photography for process-based interpretation at the ecosystem scale. Clim Res 39:261–274CrossRefGoogle Scholar
  3. Amthor JS (1989) Respiration and crop productivity. Springer, New YorkCrossRefGoogle Scholar
  4. Augspurger CK (2008) Early spring leaf out enhances growth and survival of saplings in a temperate deciduous forest. Oecologia 156:281–286CrossRefPubMedGoogle Scholar
  5. Baldocchi D, Meyers T (1998) On using eco-physiological, micrometeorological and biogeochemical theory to evaluate carbon dioxide, water vapor and trace gas fluxes over vegetation: a perspective. Agr Forest Meteorol 90:1–25CrossRefGoogle Scholar
  6. Baldocchi D, Falge E, Gu L, Olson R, Hollinger D, Running S, Anthoni P, Bernhofer C, Davis K, Evans R, Fuentes J, Goldstein A, Katul G, Law B, Lee X, Malhi Y, Meyers T, Munger W, Oechel W, Paw UKT, Pilegaard K, Schmid HP, Valentini R, Verma S, Vesala T, Wilson K, Wofsy S (2001) FLUXNET : a new tool to study the temporal and spatial variability of ecosystem-scale carbon dioxide, water vapor, and energy flux densities. B Am Meteorol Soc 82:2415–2434CrossRefGoogle Scholar
  7. Beer C, Reichstein M, Tomelleri E, Ciais P, Jung M, Carvalhais N, Rödenbeck R, Arain MF, Baldocchi D, Bonan GB, Bondeau A, Cescatti A, Lasslop G, Lindroth A, Lomas M, Luyssaert S, Margolis H, Oleson KW, Roupsard O, Veenendaal E, Viovy N, Williams C, Papale D (2010) Terrestrial gross carbon dioxide uptake: global distribution and covariation with climate. Science 329:834–838CrossRefPubMedGoogle Scholar
  8. Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR, Long SP (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ 24:253–259CrossRefGoogle Scholar
  9. Bernacchi CJ, Bagley JE, Serbin SP, Ruiz-Vera UM, Rosenthal DM, Vanloocke A (2013) Modelling C3 photosynthesis from the chloroplast to the ecosystem. Plant, Cell Environ 36:1641–1657CrossRefGoogle Scholar
  10. Bonan GB (1995) Land-atmosphere interactions for climate system models: coupling biophysical, biogeochemical, and ecosystem dynamical processes. Remote Sens Environ 51:57–73CrossRefGoogle Scholar
  11. Bonan GB (1996) A land surface model (LSM version 1.0) for ecological, hydrological, and atmospheric studies: technical description and user’s guide. National Center for Atmospheric Research, BoulderGoogle Scholar
  12. Canadell JG, Raupach MR (2008) Managing forests for climate change mitigation. Science 320:1456–1457CrossRefPubMedGoogle Scholar
  13. Canadell JG, Mooney HA, Baldocchi DD, Berry JA, Ehleringer JR, Field CB, Gower ST, Hollinger DY, Hunt JE, Jackson RB, Running SW, Shaver GR, Steffen W, Trumbore SE, Valentini R, Bond BY (2000) Carbon metabolism of the terrestrial biosphere: a multi technique approach for improved understanding. Ecosystems 3:115–130CrossRefGoogle Scholar
  14. Chmielewski F, Rötzer T (2002) Annual and spatial variability of the beginning of growing season in Europe in relation to air temperature changes. Clim Res 19:257–264CrossRefGoogle Scholar
  15. Chuine I, Kramer K, Hänninen H (2003) Plant development models. In: Schwartz MD (ed) PHENOLOGY: an integrative environmental science. Kluwer Academic Publishers, Dordrecht, pp 217–235CrossRefGoogle Scholar
  16. Chung H, Muraoka H, Nakamura M, Han S, Muller O, Son Y (2013) Experimental warming studies on tree species and forest ecosystems: a literature review. J Plant Res 126:447–460CrossRefPubMedGoogle Scholar
  17. Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD (2007) Shifting plant phenology in response to global change. Trends Ecol Evol 22:357–365CrossRefPubMedGoogle Scholar
  18. Evans J (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19CrossRefGoogle Scholar
  19. Fang J, Guo Z, Hu H, Kato T, Muraoka H, Son Y (2014) Forest biomass carbon sinks in East Asia, with special reference to the relative contributions of forest expansion and forest growth. Glob Change Biol 20:2019–2030CrossRefGoogle Scholar
  20. Farquhar G, von Caemmerer S, Berry J (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90CrossRefPubMedGoogle Scholar
  21. Gitelson AA, Merzlyak MN, Lichtenthaler HK (1996) Detection of red edge position and chlorophyll content by reflectance measurements near 700 nm. J Plant Physiol 148:501–508CrossRefGoogle Scholar
  22. Goulden ML, Munger JW, Fan SM, Daube BC, Wofsy SC (1996) Exchange of carbon dioxide by a deciduous forest: response to interannual climate variability. Science 271:1576–1578CrossRefGoogle Scholar
  23. Hänninen H, Tanino K (2011) Tree seasonality in a warming climate. Trends Plant Sci 16:412–416CrossRefPubMedGoogle Scholar
  24. Harley P, Baldocchi D (1995) Scaling carbon dioxide and water vapour exchange from leaf to canopy in a deciduous forest. I. Leaf model parameterization. Plant Cell Environ 18:1146–1156CrossRefGoogle Scholar
  25. Hikosaka K (2004) Interspecific difference in the photosynthesis-nitrogen relationship: patterns, physiological causes, and ecological importance. J Plant Res 117:481–494CrossRefPubMedGoogle Scholar
  26. Hikosaka K, Terashima I (1995) A model of the acclimation of photosynthesis in the leaves of C3 plants to sun and shade with respect to nitrogen use. Plant Cell Environ 18:605–618CrossRefGoogle Scholar
  27. Hikosaka K, Nabeshima E, Hiura T (2007) Seasonal changes in the temperature response of photosynthesis in canopy leaves of Quercus crispula in a cool-temperate forest. Tree Physiol 27:1035–1041CrossRefPubMedGoogle Scholar
  28. Ide R, Oguma H (2010) Use of digital cameras for phenological observations. Ecological Inform 5:339–347CrossRefGoogle Scholar
  29. Ito A (2008) The regional carbon budget of East Asia simulated with a terrestrial ecosystem model and validated using AsiaFlux data. Agr For Meteorol 148:738–747CrossRefGoogle Scholar
  30. Ito A, Oikawa T (2002) A simulation model of the carbon cycle in land ecosystems (Sim-CYCLE): a description based on dry-matter production theory and plot-scale validation. Ecol Model 151:143–176CrossRefGoogle Scholar
  31. Ito A, Muraoka H, Koizumi H, Saigusa N, Murayama S, Yamamoto S (2006) Seasonal variation in leaf properties and ecosystem carbon budget in a cool-temperate deciduous broad-leaved forest: simulation analysis at Takayama site, Japan. Ecol Res 21:137–149CrossRefGoogle Scholar
  32. Japan Meteorological Agency (2005) Report on abnormal weather 2005. (in Japanese; accessed May 31, 2014)
  33. Japan Meteorological Agency (2009) The climate in July. (in Japanese; accessed September 24, 2014)
  34. Japan Meteorological Agency (2014) The start and end date of the baiu from 1951: Tokai region. (in Japanese; accessed September 24, 2014)
  35. Keeling C, Chin J, Whorf T (1996) Increased activity of northern vegetation inferred from atmospheric CO2 measurements. Nature 382:146–149CrossRefGoogle Scholar
  36. Koike T (1988) Leaf structure and photosynthetic performance as related to the forest succession of deciduous broad-leaved trees. Plant Species Biol 3:77–87CrossRefGoogle Scholar
  37. Kosugi Y, Shibata S, Kobashi S (2003) Parameterization of the CO2 and H2O gas exchange of several temperate deciduous broad-leaved trees at the leaf scale considering seasonal changes. Plant, Cell Environ 26:285–301CrossRefGoogle Scholar
  38. Kramer K, Leinonen I, Loustau D (2000) The importance of phenology for the evaluation of impact of climate change on growth of boreal, temperate and Mediterranean forests ecosystems: an overview. Int J Biometeorol 44:67–75CrossRefPubMedGoogle Scholar
  39. Marshall B, Roberts JA (2000) Leaf development and canopy growth. Sheffield Academic Press, SheffieldGoogle Scholar
  40. Medlyn B, Dreyer E, Ellsworth D, Forstreuter M, Harley PC, Kirschbaum MUF, Le Roux X, Montpied P, Strassemeyer J, Walcroft A, Wang K, Loustau D (2002) Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data. Plant Cell Environ 25:1167–1179CrossRefGoogle Scholar
  41. Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, Alm-kübler K, Bissolli P, Braslavská O, Briede A, Chmielewski FM, Crepinsek Z, Curnel Y, Dahl Å, Defila C, Donnelly A, Filella Y, Jatczak K, Måge F, Mestre A, Nordli Ø, Peñuelas J, Pirinen P, Remišová V, Scheifinger H, Striz M, Susnik A, Van Vliet AJH, Wielgolaski F, Zach S, Zust A (2006) European phenological response to climate change matches the warming pattern. Glob Change Biol 12:1969–1976CrossRefGoogle Scholar
  42. Miyazawa S, Satomi S, Terashima I (1998) Slow leaf development of evergreen broad-leaved tree species in Japanese warm temperate forests. Ann Bot London 82:859–869CrossRefGoogle Scholar
  43. Mo W, Lee MS, Uchida M, Inatomi M, Saigusa N, Mariko S, Koizumi H (2005) Seasonal and annual variations in soil respiration in a cool-temperate deciduous broad-leaved forest in Japan. Agr For Meteorol 134:81–94CrossRefGoogle Scholar
  44. Morin X, Roy J, Sonié L, Chuine I (2010) Changes in leaf phenology of three European oak species in response to experimental climate change. New Phytol 186:900–910CrossRefPubMedGoogle Scholar
  45. Muraoka H, Koizumi H (2005) Photosynthetic and structural characteristics of canopy and shrub trees in a cool-temperate deciduous broadleaved forest: implication to the ecosystem carbon gain. Agr For Meteorol 134:39–59CrossRefGoogle Scholar
  46. Muraoka H, Koizumi H (2009) Satellite Ecology (SATECO)-linking ecology, remote sensing and micrometeorology, from plot to regional scale, for the study of ecosystem structure and function. J Plant Res 122:3–20CrossRefPubMedGoogle Scholar
  47. Muraoka H, Saigusa N, Nasahara KN, Noda H, Yoshino J, Saitoh TM, Nagai S, Koizumi H (2010) Effects of seasonal and interannual variations in leaf photosynthesis and canopy leaf area index on gross primary production of a cool-temperate deciduous broadleaf forest in Takayama, Japan. J Plant Res 123:563–576CrossRefPubMedGoogle Scholar
  48. Muraoka H, Noda HM, Nagai S, Motohka T, Saitoh TM, Nasahara KN, Saigusa N (2013) Spectral vegetation indices as the indicator of canopy photosynthetic productivity in a deciduous broadleaf forest. J Plant Ecol 6:393–407CrossRefGoogle Scholar
  49. Murayama S, Takamura C, Yamamoto S, Saigusa N, Morimoto S, Kondo H, Nakazawa T, Aoki S, Usami T, Kondo M (2010) Seasonal variations of atmospheric CO2, δ13C, and δ18 O at a cool temperate deciduous forest in Japan: influence of Asian monsoon. J Geophys Res 115(D17):D17304CrossRefGoogle Scholar
  50. Myneni R, Keeling C, Tucker C (1997) Increased plant growth in the northern high latitudes from 1981 to 1991. Nature 386:698–702CrossRefGoogle Scholar
  51. Nagai S, Nasahara KN, Muraoka H, Akiyama T, Tsuchida S (2010) Field experiments to test the use of the normalized difference vegetation index for phenology detection. Agr For Meteorol 150:152–160CrossRefGoogle Scholar
  52. Nagai S, Saitoh TM, Kurumado K, Tamagawa I, Kobayashi H, Inoue T, Suzuki R, Gamo M, Muraoka H, Nasahara NK (2013) Detection of bio-meteorological year-to-year variation by using digital canopy surface images of a deciduous broad-leaved forest. SOLA 9:106–110CrossRefGoogle Scholar
  53. Nakaji T, Ide R, Oguma H, Saigusa N, Fujinuma Y (2007) Utility of spectral vegetation index for estimation of gross CO2 flux under varied sky conditions. Remote Sens Environ 109:274–284CrossRefGoogle Scholar
  54. Nasahara KN, Muraoka H, Nagai S, Mikami H (2008) Vertical integration of leaf area index in a Japanese deciduous broad-leaved forest. Agr For Meteorol 148:1136–1146CrossRefGoogle Scholar
  55. Niinemets Ü, Tenhunen JD (1997) A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum. Plant Cell Environ 20:845–866CrossRefGoogle Scholar
  56. Niinemets Ü, Kull O, Tenhunen J (2004) Within-canopy variation in the rate of development of photosynthetic capacity is proportional to integrated quantum flux density in temperate deciduous trees. Plant Cell Environ 27:293–313CrossRefGoogle Scholar
  57. Nishida K (2007) Phenological eyes network (PEN)—A validation network for remote sensing of the terrestrial ecosystems. AsiaFlux Newslett 21:9–13Google Scholar
  58. Ohtsuka T, Akiyama T, Hashimoto Y, Inatomi M, Sakai T, Jia S, Mo W, Tsuda S, Koizumi H (2005) Biometric based estimates of net primary production (NPP) in a cool-temperate deciduous forest stand beneath a flux tower. Agr For Meteorol 134:27–38CrossRefGoogle Scholar
  59. Ohtsuka T, Mo W, Satomura T, Inatomi M, Koizumi H (2007) Biometric based carbon flux measurements and net ecosystem production (NEP) in a temperate deciduous broad-leaved forest beneath a flux tower. Ecosystems 10:324–334CrossRefGoogle Scholar
  60. Ohtsuka T, Saigusa N, Koizumi H (2009) On linking multiyear biometric measurements of tree growth with eddy covariance-based net ecosystem production. Glob Change Biol 15:1015–1024CrossRefGoogle Scholar
  61. Owen KE, Tenhunen J, Reichstein M, Wang Q, Falge E, Geyer R, Xiao X, Stoy P, Ammann C, Arain A, Aubinet M, Aurela M, Bernhofer C, Chojnicki BH, Granier A, Gruenwald T, Hadley J, Heinesch B, Hollinger D, Knoh A, Kutsch W, Lohila A, Meyers T, Moors E, Moureaux C, Pilegaard K, Saigusa N, Verma S, Vesala T, Vogel C (2007) Linking flux network measurements to continental scale simulations: ecosystem carbon dioxide exchange capacity under non-water-stressed conditions. Glob Change Biol 13:734–760CrossRefGoogle Scholar
  62. Peñuelas J, Rutishauser T, Filella I (2009) Phenology feedbacks on climate change. Science 324:887–888CrossRefPubMedGoogle Scholar
  63. Piao S, Fang J, Zhou L, Ciais P, Zhu B (2006) Variations in satellite-derived phenology in China’s temperate vegetation. Glob Change Biol 12:672–685CrossRefGoogle Scholar
  64. Piao S, Ciais P, Friedlingstein P, Peylin P, Reichstein M, Luyssaert S, Margolis H, Fang J, Barr A, Chen A, Grelle A, Hollinger DY, Laurila T, Lindroth A, Richardson AD, Vesala T (2008) Net carbon dioxide losses of northern ecosystems in response to autumn warming. Nature 451:49–52CrossRefPubMedGoogle Scholar
  65. Piao S, Ito A, Li S, Huang Y, Ciais P, Wang X, Peng S, Andres RJ, Fang J, Jeong S, Mao J, Mohammat A, Muraoka H, Nan H, Peng C, Peylin P, Shi X, Sitch S, Tao S, Tian H, Xu M, Yu G, Zeng N, Zhu B (2012) The carbon budget of terrestrial ecosystems in East Asia over the last two decades. Biogeosci Discuss 9:4025–4066CrossRefGoogle Scholar
  66. Porra R, Thompson W, Kriedemann P (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394CrossRefGoogle Scholar
  67. Reich PB, Walters MB, Ellsworth DS (1991) Leaf age and season influence the relationships between leaf nitrogen, leaf mass per area and photosynthesis in maple and oak trees. Plant Cell Environ 14:251–259CrossRefGoogle Scholar
  68. Reich PB, Walters MB, Ellsworth DS, Uhl C (1994) Photosynthesis-nitrogen relations in Amazonian tree species. Oecologia 97:62–72CrossRefGoogle Scholar
  69. Reich PB, Walters MB, Kloeppel BD, Ellsworth DS (1995) Different photosynthesis-nitrogen relations in deciduous hardwood and evergreen coniferous tree species. Oecologia 104:24–30CrossRefGoogle Scholar
  70. Reichstein M, Bahn M, Ciais P, Frank D, Mahecha MD, Seneviratne SI, Zscheischler J, Beer C, Buchmann N, Frank DC, Papale D, Rammig A, Smith P, Thonicke K, van der Velde K, Vicca S, Walz A, Wattenbach M (2013) Climate extremes and the carbon cycle. Nature 500:287–295CrossRefPubMedGoogle Scholar
  71. Richardson AD, Bailey AS, Denny EG, Martin CW, O’Keefe J (2006) Phenology of a northern hardwood forest canopy. Glob Change Biol 12:1174–1188CrossRefGoogle Scholar
  72. Richardson AD, Jenkins JP, Braswell BH, Hollinger DY, Ollinger SV, Smith ML (2007) Use of digital webcam images to track spring green-up in a deciduous broadleaf forest. Oecologia 152:323–334CrossRefPubMedGoogle Scholar
  73. Richardson AD, Black TA, Ciais P, Delbart N, Friedl MA, Gobron N, Hollinger DY, Kutsch WL, Longdoz B, Luyssaert S, Migliavacca M, Montagnani L, Munger JW, Moors E, Piao S, Rebmann C, Reichstein M, Saigusa N, Tomelleri E, Vargas R, Varlagin A (2010) Influence of spring and autumn phenological transitions on forest ecosystem productivity. Philos T R Soc B 365:3227–3246CrossRefGoogle Scholar
  74. Running S, Nemani R, Heinsch FA, Zhao M, Reeves M, Hashimoto H (2004) A continuous satellite-derived measure of global terrestrial primary production. Bioscience 54:547–560CrossRefGoogle Scholar
  75. Saigusa N, Yamamoto S, Murayama S, Kondo H (2005) Inter-annual variability of carbon budget components in an AsiaFlux forest site estimated by long-term flux measurements. Agr For Meteorol 134:4–16CrossRefGoogle Scholar
  76. Saigusa N, Yamamoto S, Hirata R, Ohtani Y, Ide R, Asanumae J, Gamoa M, Hirano T, Kondoa H, Kosugi Y, Li SG, Nakai Y, Takagi K, Tani M, Wanga H (2008) Temporal and spatial variations in the seasonal patterns of CO2 flux in boreal, temperate, and tropical forests in East Asia. Agr For Meteorol 148:700–713CrossRefGoogle Scholar
  77. Saitoh TM, Nagai S, Saigusa N, Kobayashi H, Suzuki R, Nasahara KN, Muraoka H (2012) Assessing the use of camera-based indices for characterizing canopy phenology in relation to gross primary production in a deciduous broad-leaved and an evergreen coniferous forest in Japan. Ecol Inform 11:45–54CrossRefGoogle Scholar
  78. Sasai T, Ichii K, Yamaguchi Y, Nemani R (2005) Simulating terrestrial carbon fluxes using the new biosphere model “biosphere model integrating eco-physiological and mechanistic approaches using satellite data” (BEAMS). J Geophys Res 110(G2):G02014CrossRefGoogle Scholar
  79. Schaber J, Badeck FW (2003) Physiology-based phenology models for forest tree species in Germany. Int J Biometeorol 4:193–201CrossRefGoogle Scholar
  80. Sims DA, Gamon JA (2002) Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages. Remote Sens Environ 81:337–354CrossRefGoogle Scholar
  81. Tenhunen JD, Kabat P (1999) Integrating hydrology, ecosystem dynamics, and biogeochemistry in complex landscapes. Wiley, New YorkGoogle Scholar
  82. Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395CrossRefPubMedGoogle Scholar
  83. Wang Q, Iio A, Tenhunen J, Kakubari Y (2008) Annual and seasonal variations in photosynthetic capacity of Fagus crenata along an elevation gradient in the Naeba Mountains, Japan. Tree Physiol 28:277–285CrossRefPubMedGoogle Scholar
  84. White M, Running S, Thornton P (1999) The impact of growing-season length variability on carbon assimilation and evapotranspiration over 88 years in the eastern US deciduous forest. Int J Biometeorol 42:139–145CrossRefPubMedGoogle Scholar
  85. Wilson KB, Baldocchi DD, Hanson PJ (2000) Spatial and seasonal variability of photosynthetic parameters and their relationship to leaf nitrogen in a deciduous forest. Tree Physiol 20:565–578CrossRefPubMedGoogle Scholar
  86. Wilson KB, Baldocchi DD, Hanson PJ (2001) Leaf age affects the seasonal pattern of photosynthetic capacity and net ecosystem exchange of carbon in a deciduous forest. Plant Cell Environ 24:571–583CrossRefGoogle Scholar
  87. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827CrossRefPubMedGoogle Scholar
  88. Xu L, Baldocchi DD (2003) Seasonal trends in photosynthetic parameters and stomatal conductance of blue oak (Quercus douglasii) under prolonged summer drought and high temperature. Tree Physiol 23:865–877CrossRefPubMedGoogle Scholar
  89. Yamamoto S, Koizumi H (2005) Long-term carbon exchange at Takayama site, a cool-temperature deciduous forest in Japan. Agr For Meteorol 134:1–3CrossRefGoogle Scholar
  90. Yamamoto S, Murayama S, Saigusa N, Kondo H (1999) Seasonal and inter-annual variation of CO2 flux between a temperate forest and the atmosphere in Japan. Tellus 51B:402–413CrossRefGoogle Scholar
  91. Yasumura Y, Ishida A (2011) Temporal variation in leaf nitrogen partitioning of a broad-leaved evergreen tree, Quercus myrsinaefolia. J Plant Res 124:115–123CrossRefPubMedGoogle Scholar
  92. Zhang X, Friedl MA, Schaaf CB, Strahler AH, Hodges JCF, Gao F, Reed BC, Huete A (2003) Monitoring vegetation phenology using MODIS. Remote Sens Environ 84:471–475CrossRefGoogle Scholar

Copyright information

© The Ecological Society of Japan 2014

Authors and Affiliations

  • Hibiki M. Noda
    • 1
    Email author
  • Hiroyuki Muraoka
    • 2
  • Kenlo Nishida Nasahara
    • 3
  • Nobuko Saigusa
    • 1
  • Shohei Murayama
    • 4
  • Hiroshi Koizumi
    • 5
  1. 1.Center for Global Environmental ResearchNational Institute for Environmental StudiesTsukubaJapan
  2. 2.Institute for Basin Ecosystem StudiesGifu UniversityGifuJapan
  3. 3.Faculty of Life and Environment SciencesUniversity of TsukubaTsukubaJapan
  4. 4.Research Institute for Environmental Management TechnologyNational Institute of Advanced Industrial Science and Technology (AIST)TsukubaJapan
  5. 5.Department of Biology, Faculty of EducationWaseda UniversityTokyoJapan

Personalised recommendations