Abstract
Revealing the seasonal and interannual variations in forest canopy photosynthesis is a critical issue in understanding the ecological mechanisms underlying the dynamics of carbon dioxide exchange between the atmosphere and deciduous forests. This study examined the effects of temporal variations of canopy leaf area index (LAI) and leaf photosynthetic capacity [the maximum velocity of carboxylation (V cmax)] on gross primary production (GPP) of a cool-temperate deciduous broadleaf forest for 5 years in Takayama AsiaFlux site, central Japan. We made two estimations to examine the effects of canopy properties on GPP; one is to incorporate the in situ observation of V cmax and LAI throughout the growing season, and another considers seasonality of LAI but constantly high V cmax. The simulations indicated that variation in V cmax and LAI, especially in the leaf expansion period, had remarkable effects on GPP, and if V cmax was assumed constant GPP will be overestimated by 15%. Monthly examination of air temperature, radiation, LAI and GPP suggested that spring temperature could affect canopy phenology, and also that GPP in summer was determined mainly by incoming radiation. However, the consequences among these factors responsible for interannual changes of GPP are not straightforward since leaf expansion and senescence patterns and summer meteorological conditions influence GPP independently. This simulation based on in situ ecophysiological research suggests the importance of intensive consideration and understanding of the phenology of leaf photosynthetic capacity and LAI to analyze and predict carbon fixation in forest ecosystems.
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References
Baldocchi DD (2008) ‘Breathing’ of the terrestrial biosphere: lessons learned from a global network of carbon dioxide flux measurement systems. Aust J Bot 56:1–26
Baldocchi DD, 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. Agric For Meteorol 90:1–25
Baldocchi DD, Wilson KB (2001) Modeling CO2 and water vapor exchange of a temperate broadleaved forest across hourly to decadal time scales. Ecol Model 142:155–184
Baldocchi DD, Wilson KB, Gu L (2002) How the environment, canopy structure and canopy physiological functioning influence carbon, water and energy fluxes of a temperate broad-leaved deciduous forest—an assessment with the biophysical model CANOAK. Tree Physiol 22:1065–1077
Ball JT, Woodrow IE, Berry JA (1987) A model predicting stomatal conductance and its contribution to the control of photosynthesis under different environmental conditions. Prog Photosynth Res 4:221–224
Barr A, Black TA, Hogg EH, Kljun N, Mogenstern K, Nesic Z (2004) Inter-annual variability in the leaf area index of boreal aspen-hazelnut forest in relation to net ecosystem production. Agric For Meteorol 126:237–255
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, Boulder
Bondeau A, Kicklighter DW, Kaduk J, The Participants of the Potsdam NPP Model Intercomparison (1999) Comparing global models of terrestrial net primary productivity (NPP): importance of vegetation structure on seasonal NPP estimates. Glob Chang Biol 5(Suppl 1):35–45
Brooks A, Farquhar GD (1985) Effect of temperature on the CO2/O2 specificity of ribulose-1, 5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light. Planta 165:397–406
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 multitechnique approach for improved understanding. Ecosystems 3:115–130
Chen WJ, Black TA, Yang PC, Barr AG, Neumann HH, Nesic Z, Blanken PD, Novak MD, Eley J, Ketler RJ, Cuenca R (1999) Effects of climatic variability on the annual carbon sequestration by a boreal aspen forest. Glob Chang Biol 5:41–53
Collatz GJ, Ball JT, Grivet C, Berry JA (1991) Physiological and environmental regulation of stomatal conductance, photosynthesis, and transpiration: a model that includes a laminar boundary layer. Agric For Meteorol 54:107–136
De Pury DGG, Farquhar GD (1997) Simple scaling of photosynthesis from leaves to canopies without the errors of big-leaf models. Plant Cell Environ 20:537–557
Falge E, Baldocchi D, Tenhunen J, Aubinet M, Bakwin P, Berbigier P, Bernhofer C, Burga G, Clement R, Davis KJ, Elbers JA, Goldstein AH, Grelle A, Granier A, Guðmindsson J, Hollinger D, Kowalski AS, Katul G, Law BE, Malhi Y, Meyers T, Monson RK, Munger JW, Oechel W, Paw U KT, Pilegaard K, Rannik Ü, Rebmann C, Suyker A, Valentini R, Wilson K, Wofsy S (2002) Seasonality of ecosystem respiration and gross primary production as derived from FLUXNET measurements. Agric For Meteorol 113:53–74
Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90
Food and Agriculture Organization of the United Nations (2005) Global forest resources assessment 2005. FAO Forestry Paper 147. http://www.fao.org
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 271:1576–1578
Heinsch FA, Zhao M, Running SWW, Kimball JS, Nemani RR, Davis KJ, Bolstad PV, Cook BD, Desai AR, Ricciuto DM, Law BE, Oechel WC, Kwon H, Luo H, Wpofsy SC, Dunn AL, Munger JW, Baldocchi DD, Xu L, Hollinger DY, Richardson AD, Stoy PC, Siqueria MBS, Monson RK, Burns SP, Flanagan LB (2006) Evaluation of remote sensing based terrestrial productivity from MODIS using regional tower eddy flux network observations. IEEE Trans Geosci Remote Sens 44:1908–1925
Ito A, Saigusa N, Murayama S, Yamamoto S (2005) Modeling of gross and net carbon dioxide exchange over a cool-temperate deciduous broad-leaved forest in Japan: analysis of seasonal and interannual change. Agric For Meteorol 134:122–134
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 21:137–149
Kapos V, Rhind J, Edwards M, Price MF, Ravilious C (2000) Developing a map of the world’s mountain forests. In: Price MF, Butt N (eds) Forests in sustainable mountain development: a state of knowledge report for 2000. CABI, Wallingford, pp 4–9
Kim J, Le D, Hong J, Kang S, Kim SJ, Moon SK, Kim JH, Son Y, Lee J, Kim S, Woo N, Kim K, Lee B, Lee BL, Kim S (2006) HydroKorea and CarboKorea: cross-scale studies of ecohydrology and biogeochemistry in a heterogeneous and complex forest catchment of Korea. Ecol Res 21:881–889
Kimura K, Ishida A, Uemura A, Matsumoto Y, Terashima I (1998) Effects of current-year and previous-year PPFDs on shoot gross morphology and leaf properties in Fagus japonica. Tree Physiol 18:459–466
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 44:67–75
Lambers H, Chapin FS III, Pons TL (1998) Plant physiological ecology. Springer, New York
Law BE, Sun OJ, Campbell J, van Tuyl S, Thornton PE (2003) Changes in carbon storage and fluxes in a chronosequence of ponderosa pine. Glob Chang Biol 9:510–524
Leuzinger S, Körner C (2007) Tree species diversity affects canopy leaf temperatures in a mature temperate forest. Agric For Meteorol 146:29–37
Markwell J, Osterman JC, Mitchell JL (1995) Calibration of the Minolta SPAD-502 leaf chlorophyll meter. Photosyn Res 46:467–472
Mo W, Lee M, 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. Agric For Meteorol 134:81–94
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. Agric For Meteorol 134:39–59
Muraoka H, Koizumi H (2006) Leaf and shoot ecophysiological properties and their role in photosynthetic carbon gain of cool-temperate deciduous forest trees. In: Kawatata H, Awaya Y (eds) Global climate change and response of carbon cycle in the Equatorial Pacific and Indian Oceans and adjacent landmasses. Elsevier oceanography series, vol 73. Elsevier, Amsterdam, pp 417–443
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 122:3–20
Myneni RB, Keeling CD, Tucker CJ, Asrar G, Nemani RR (1997) Increased plant growth in the northern high latitudes from 1981 to 1991. Nature 386:698–702
Nagai S, Saigusa N, Muraoka H, Nasahara KN (2009) What makes the satellite-based EVI-GPP relationship unclear? Ecol Res (in press)
Nasahara KN, Muraoka H, Nagai S, Mikami H (2008) Vertical integration of leaf area index in a Japanese deciduous broad-leaved forest. Agric For Meteorol 148:1136–1146
Niinemets Ü (2007) Photosynthesis and resource distribution through plant canopies. Plant Cell Environ 30:1052–1071
Niinemets Ü, Kull O, Tenhunen JD (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 27:293–313
Nishida K (2007) Phenological eyes network (PEN)—a validation network for remote sensing of the terrestrial ecosystems. AsiaFlux Newsl 21:9–13
Nishimura N, Matsui Y, Ueyama T, Mo W, Saijo Y, Tsuda S, Yamamoto S, Koizumi H (2004) Evaluation of carbon budgets of a forest floor Sasa senanensis community in a cool-temperate forest ecosystem, central Japan (in Japanese with English summary). Jpn J Ecol 54:143–158
Odum EP (1969) The strategy of ecosystem development. Science 164:262–270
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-leaves forest beneath a flux tower. Ecosystems 10:324–334
Ohtsuka T, Saigusa N, Koizumi H (2009) On linking multiyear biometric measurements of tree growth with eddy covariance-based net ecosystem production. Glob Chang Biol 15:1015–1024
Reichstein M, Ciais P, Papale D, Valentini R, Running S, Viovy N, Cramer W, Granier A, Ogee J, Allard V, Aubinet M, Bernhofer Chr, Buchmann N, Carrara A, Grünwald T, Heimann M, Heinesch B, Knohl A, Kutsch W, Loustau D, Manca G, Matteucci G, Miglietta F, Ourcival JM, Pilegaard K, Pumpanen J, Rambal S, Schaphoef S, Seufert G, Soussana J-F, Sanz M-J, Vesela T, Zhaop M (2006) Reduction of ecosystem productivity and respiration during the European summer 2003 climate anomaly: a joint flux tower, remote sensing and modelling analysis. Glob Chang Biol 12:1–18
Richardson AD, Bailey AS, Denny EG, Martin CW, O’Keefe J (2006) Phenology of a northern hardwood forest canopy. Glob Chang Biol 12:1174–1188
Running SW, Nemani RR, Heinsch FA, Zhao M, Reeves M, Hashimoto H (2004) A continuous satellite-derived measure of global terrestrial primary production. Bioscience 54:547–560
Saigusa N, Yamamoto S, Murayama S, Kondo H, Nishimura N (2002) Gross primary production and net ecosystem exchange of a cool-temperate deciduous forest estimated by the eddy covariance method. Agric For Meteorol 112:203–215
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. Agric For Meteorol 134:4–16
Saigusa N, Yamamoto S, Hirata R, Ohtani Y, Ide R, Asanuma J, Gamo M, Hirano T, Kondo H, Kosugi Y, Li S, Nakai Y, Takagi K, Tani M, Wang H (2008) Temporal and spatial variations in the seasonal patterns of CO2 flux in boreal, temperate, and tropical forests in East Asia. Agric For Meteorol 148:700–713
Sakai T, Jia S, Kawamura K, Akiyama T (2002) Estimation of aboveground biomass and LAI of understory plant (Sasa senanensis) using a hand-held spectro-radiometer. J Jpn Soc Photogramm Remote Sens 41:27–35
Sasai T, Okamoto K, Hiyama T, Yamaguchi Y (2007) Comparing terrestrial carbon fluxes from the scale of a flux tower to the global scale. Ecol Model 208:135–144
Spitters CJT, Toussaint HAJM, Goudriaan J (1986) Separating the diffuse and direct component of global radiation and its implications for modeling canopy photosynthesis. Part 1. Components of incoming radiation. Agric For Meteorol 38:217–229
Takagi K, Fukuzawa K, Liang N, Kayama M, Nomura M, Hojyo H, Sugata S, Shibata H, Fukuzawa T, Takahashi Y, Nakaji T, Oguma H, Mano M, Akibayashi Y, Murayama T, Koike T, Sasa K, Fujinuma Y (2009) Change in CO2 balance under a series of forestry activities in a cool-temperate mixed forest with dense undergrowth. Glob Chang Biol 15:1275–1288
Tenhunen JD, Lenz R, Hantschel R (2001) Ecosystem approaches to landscape management in central Europe. Springer, Berlin, p 652
Thornley JHM (1976) Mathematical models in plant physiology. Academic, London
Turner DP, Ritts WD, Cohen WB, Maeirsperger TK, Gower ST, Kirschbaum AA, Running SW, Zhao M, Wofsy SC, Dunn AL, Law BE, Campbell JL, Oechel WC, Kwon HJ, Meyers TP, Small EE, Kurc SA, Gamon JA (2005) Site-level evaluation of satellite-based global terrestrial gross primary production and net primary production monitoring. Glob Chang Biol 11:1–19
Wang Q, Iio A, Tenhunen J, Kakubari K (2008) Annual and seasonal variations in photosynthetic capacity of Fagus crenata along an elevation gradient in the Naeba Mountains, Japan. Tree Physiol 28:277–285
White MA, Running SW, Thornton PE (1999) The impact of growing-season length variability on carbon assimilation and evaporation over 88 years in the eastern US deciduous forest. Int J Biometeorol 42:139–145
Wilson KB, Baldocchi DD, Hanson P (2000) Spatial and seasonal variability of photosynthetic parameters and their relationship to leaf nitrogen in a deciduous forest. Tree Physiol 20:565–578
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 24:571–583
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 23:865–877
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:402–413
Acknowledgments
We thank K. Kurumado and Y. Miyamoto of Takayama field station of Gifu University for their support of field investigations, and also the PEN project (http://www.pheno-eye.org/) for the canopy photographs. Thanks are also due to S. Yamamoto of Okayama University, H. Kondo of AIST, J. D. Tenhunen of University of Bayreuth and R. W. Pearcy of UC Davis for discussion and encouragement. Also, we thank the anonymous reviewers who made valuable comments on the manuscript. This study was supported by the Ministry of Environment, Japan, as Global Environment Research Fund (S-1: Integrated Study for Terrestrial Carbon Management of Asia in the twenty-first Century Based on Scientific Advancement), JSPS twenty-first Century COE Program (Satellite Ecology), KAKENHI (JSPS, no. 18710006) to HM and JSPS-KOSEF-NSFC A3 Foresight Program (quantifying and predicting terrestrial carbon sinks in East Asia: toward a network of climate change research).
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Muraoka, H., Saigusa, N., Nasahara, K.N. et al. 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, 563–576 (2010). https://doi.org/10.1007/s10265-009-0270-4
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DOI: https://doi.org/10.1007/s10265-009-0270-4