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Spatial and temporal variations in photosynthetic capacity of a temperate deciduous-evergreen forest

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The understory evergreen trees showed maximal photosynthetic capacity in winter, while the overstory deciduous trees showed this capacity in spring. The time lag in productive ecophysiologically active periods between deciduous overstory and evergreen understory trees in a common temperate forest was clearly related to the amount of overstory foliage.

Abstract

In temperate forests, where deciduous canopy trees and evergreen understory trees coexist, understory trees experience great variation in incident radiation corresponding to canopy dynamics represented by leaf-fall and leaf-out. It is generally thought that changes in the light environment affect understory plants’ ecophysiological traits. Thus, to project and estimate annual energy, water, and carbon exchange between forests and the atmosphere, it is necessary to investigate seasonal variation in the ecophysiological activities of both evergreen trees in the understory and deciduous trees that make up the canopy/overstory. We conducted leaf-scale gas-exchange measurements and nitrogen content analyses for six tree species along their heights throughout a complete year. Photosynthetic capacity as represented by the maximum carboxylation rate (V cmax25) and photosynthetic nitrogen use efficiency (PNUE) of deciduous canopy trees peaked immediately after leaf-out in late May, declined and stabilised during the mid-growing season, and drastically decreased just before leaf-fall. On the other hand, the timing of lowest V cmax25 and PNUE for evergreen understory trees coincided with that of the highest values for canopy trees. Furthermore, understory trees’ highest values appeared just before canopy tree leaf-out, when incident radiation in the understory was highest. This implies that failing to consider seasonal variation in leaf ecophysiological traits for both canopy and understory trees could lead to serious errors in estimating ecosystem productivity and energy balance for temperate forests.

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References

  • Adams WWIII, Zarter CR, Ebbert V, Demmig-Adams B (2004) Photoprotective strategies of overwintering evergreens. Bioscience 54:41–49. doi:10.2307/1314584

    Article  Google Scholar 

  • Anten NPR, Miyazawa K, Hikosaka K, Nagashima H, Hirose T (1998) Leaf nitrogen distribution in relation to leaf age and photon flux density in dominant and subordinate plants in dense stands of a dicotyledonous herb. Oecologia 113:314–324

    Article  Google Scholar 

  • 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. Agric For Meteorol 90:1–25

    Article  Google Scholar 

  • Baldocchi D, Matt DR, Hutchison BA, McMillen RT (1984) Solar radiation within an oak-hickory forest: an evaluation of the extinction coefficients for several radiation components during fully leafed and leafless periods. Agric For Meteorol 32:307–322

    Article  Google Scholar 

  • Breckle SW, Walter H (2002) Walter’s vegetation of the earth: the ecological systems of the geo-biosphere, 4th edn. Springer, Berlin

    Book  Google Scholar 

  • Carswell FE, Meir P, Wandelli EV, Bonates LCM, Kruijt B, Barbosa EM, Nobre AD, Grace L, Jarvis PG (2000) Photosynthetic capacity in a central Amazonian rain forest. Tree Physiol 20:179–186. doi:10.1093/treephys/20.3.179

    Article  PubMed  Google Scholar 

  • Collatz GJ, Ball JT, Grivet C, Berry JA (1991) Physiological and environmental regulation of stomatal conductance, photo-synthesis and transpiration: a model that includes a laminar boundary layer. Agric For Meteorol 54:107–136. doi:10.1016/0168-1923(91),90002-8

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90

    Article  CAS  PubMed  Google Scholar 

  • Gill DS, Amthor JS, Bormann FH (1998) Leaf phenology, photosynthesis, and the persistence of saplings and shrubs in a mature northern hardwood forest. Tree Physiol 18:281–289

    Article  PubMed  Google Scholar 

  • Grassi G, Vicinelli E, Ponti F, Cantoni L, Magnani F (2005) Seasonal and interannual variability of photosynthetic capacity in relation to leaf nitrogen in a deciduous forest plantation in northern Italy. Tree Physiol 25:349–360

    Article  PubMed  Google Scholar 

  • Harley PC, Baldocchi DD (1995) Scaling carbon dioxide and water vapour exchange from leaf to canopy in a deciduous forest. I. Leaf model parametrization. Plant Cell Environ 18:1146–1156. doi:10.1111/j.1365-3040.1995.tb00625.x

    Article  Google Scholar 

  • Harley PC, Thomas RB, Reynolds JF, Strain BR (1992) Modeling photosynthesis of cotton grown in elevated CO2. Plant Cell Environ 15:271–282. doi:10.1111/j.1365-3040.1992.tb00974.x

    Article  CAS  Google Scholar 

  • Harrington RA, Brown BJ, Reich PB (1989) Ecophysiology of exotic and native shrubs in Southern Wisconsin. Oecologia 80:356–367

    Article  Google Scholar 

  • Hikosaka K (2005) Nitrogen partitioning in the photosynthetic apparatus of Plantago asiatica leaves grown under different temperature and light conditions: similarities and differences between temperature and light acclimation. Plant Cell Environ 46:1283–1290

    Article  CAS  Google Scholar 

  • Hikosaka K, Kato MC, Hirose T (2004) Photosynthetic rates and partitioning of absorbed light energy in photoinhibited leaves. Physiol Plant 121:699–708. doi:10.1111/j.1399-3054.2004.00364.x

    Article  CAS  Google Scholar 

  • Hikosaka K, Ishikawa K, Borjigidai A, Muller O, Onoda Y (2006) Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate. J Exp Bot 57:291–302

    Article  CAS  PubMed  Google Scholar 

  • Hiyama T, Kochi K, Kobayashi N, Sirisampan S (2005) Seasonal variation in stomatal conductance and physiological factors observed in a secondary warm-temperate forest. Ecol Res 20:333–346. doi:10.1007/s11284-005-0049-6

    Article  Google Scholar 

  • Holst T, Hauser S, Kirchqässner A, Matzarakis A, Mayer H, Schindler D (2004) Measuring and modeling plant area index in beech stands. Int J Biometeorol 48:192–201

    Article  CAS  PubMed  Google Scholar 

  • Igarashi Y, Kumagai T, Yoshifuji N, Sato T, Tanaka N, Tanaka K, Suzuki M, Tantasirin C (2015) Environmental control of canopy stomatal conductance in a tropical deciduous forest in northern Thailand. Agric For Meteorol 202:1–10

    Article  Google Scholar 

  • Iio A, Yokoyama A, Takano M, Nakamura T, Fukasawa H, Nose Y, Kakubari Y (2008) Interannual variation in leaf photosynthetic capacity during summer in relation to nitrogen, leaf mass per area and climate within a Fagus crenata crown on Naeba Mountain, Japan. Tree Physiol 28:1421–1429. doi:10.1093/treephys/28.9.1421

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1007/s11284-005-0100-7

    Article  CAS  Google Scholar 

  • Koike T, Kitao M, Maruyama Y, Mori S, Lei TT (2001) Leaf morphology and photosynthetic adjustments among deciduous broad-leaved trees within the vertical canopy profile. Tree Physiol 21:951–958

    Article  CAS  PubMed  Google Scholar 

  • 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 26:285–301. doi:10.1046/j.1365-3040.2003.00960.x

    Article  Google Scholar 

  • Kull O, Jarvis PG (1995) The role of nitrogen in a simple scheme to scale up photosynthesis from leaf to canopy. Plant, Cell Environ 18:1174–1182

    Article  Google Scholar 

  • Kumagai T, Kume T (2012) Influences of diurnal rainfall cycle on CO2 exchange over Bornean tropical rainforests. Ecol Modell 246:91–98

    Article  CAS  Google Scholar 

  • Kumagai T, Ichie T, Yoshimura M, Yamashita M, Kenzo T, Saitoh TM, Ohashi M, Suzuki M, Koike T, Komatsu H (2006) Modeling CO2 exchange over a Bornean tropical rain forest using measured vertical and horizontal variation in leaf-level physiological parameters and leaf area densities. J Geophys Res 111:D10107. doi:10.1029/2005JD006676

    Article  Google Scholar 

  • Kumagai T, Mudd RG, Miyazawa Y, Liu W, Giambelluca TW, Kobayashi N, Lim TK, Jomura M, Matsumoto K, Huang M, Chen Q, Ziegler A, Yin S (2013) Simulation of canopy CO2/H2O fluxes for a rubber (Hevea brasiliensis) plantation in central Cambodia: the effect of the regular spacing of planted trees. Ecol Modell 265:124–135

    Article  CAS  Google Scholar 

  • Lambers H, Chapin FS III, Pons TL (2008) Plant physiological ecology, 2nd edn. Springer, New York, pp 58–59

    Book  Google Scholar 

  • Malhi Y, Baldocchi DD, Jarvis PG (1999) The carbon balance of tropical, temperate and boreal forests. Plant Cell Environ 22:715–740

    Article  CAS  Google Scholar 

  • Millard P, Proe MF (1991) Leaf demography and the seasonal internal cycling of nitrogen in sycamore (Acer-Pseudoplatanus L.) seedlings in relation to nitrogen supply. New Phytol 117:587–596

    Article  CAS  Google Scholar 

  • Miyazawa Y, Kikuzawa K (2005) Winter photosynthesis by saplings of evergreen broad-leaved trees in a deciduous temperate forest. New Phytol 165:857–866

    Article  CAS  PubMed  Google Scholar 

  • Miyazawa Y, Kikuzawa K (2006a) Physiological basis of seasonal trend in leaf photosynthesis of five evergreen broad-leaved species in a temperate deciduous forest. Tree Physiol 26:249–256. doi:10.1093/treephys/26.2.249

    Article  CAS  PubMed  Google Scholar 

  • Miyazawa Y, Kikuzawa K (2006b) Photosynthesis and physiological traits of evergreen broadleaved saplings during winter under different light environments in a temperate forest. Can J Bot 84:60–69. doi:10.1139/b05-144

    Article  CAS  Google Scholar 

  • Miyazawa S, Satomi S, Terashima I (1998) Slow leaf development of evergreen broad-leaved tree species in Japanese warm temperate forests. Ann Bot-London 82:859–869

    Article  Google Scholar 

  • Miyazawa S, Suzuki AA, Sone K, Terashima I (2004) Relationships between light, leaf nitrogen and nitrogen remobilization in the crowns of mature evergreen Quercus glauca trees. Tree Physiol 24:1157–1164

    Article  PubMed  Google Scholar 

  • Miyazawa Y, Kikuzawa K, Otsuki K (2007) Decrease in the capacity for RuBP carboxylation and regeneration with the progression of cold-induced photoinhibition during winter in evergreen broadleaf tree species in a temperate forest. Funct Plant Biol 34:393–401

    Article  CAS  Google Scholar 

  • Muller O, Hikosaka K, Hirose T (2005) Seasonal changes in light and temperature affect the balance between light harvesting and light utilisation components of photosynthesis in an evergreen understory shrub. Oecologia 143:501–508. doi:10.1007/s00442-005-0024-5

    Article  PubMed  Google Scholar 

  • Muller O, Oguchi R, Hirose T, Werger MJ, Hikosaka K (2009) The leaf anatomy of a broad-leaved evergreen allows an increase in leaf nitrogen content in winter. Physiol Plant 136:299–309. doi:10.1111/j.1399-3054.2009.01224.x

    Article  CAS  PubMed  Google Scholar 

  • National Astronomical Observatory of Japan (2012) Rika Nenpyo (Chronological Scientific Tables). Maruzen publishing, Tokyo [In Japanese]

  • 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 20:845–866. doi:10.1046/j.1365-3040.1997.d01-133.x

    Article  Google Scholar 

  • Nilson T (1971) A theoretical analysis of the frequency of gaps in plant stands. Agric For Meteorol 8:25–38

    Article  Google Scholar 

  • Oguchi R, Hikosaka K, Hiura T, Hirose T (2008) Costs and benefits of photosynthetic light acclimation by tree seedlings in response to gap formation. Oecologia 155:665–675. doi:10.1007/s00442-007-0951-4

    Article  CAS  PubMed  Google Scholar 

  • Öquist G, Huner NPA (2003) Photosynthesis of overwintering evergreen plats. Annu Rev Plant Biol 54:329–355

    Article  PubMed  Google Scholar 

  • 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 14:251–259

    Article  Google Scholar 

  • Ridder RM (2007) Global forest resources assessment 2010: options and recommendations for a global remote sensing survey of forests. FAO For Resour Assess Progr Work, Pap 141

    Google Scholar 

  • Sakai T, Akiyama T, Saigusa N, Yamamoto S, Yasuoka Y (2006) The contribution of gross primary production of understory dwarf bamboo, Sasa senanensis, in a cool-temperate deciduous broadleaved forest in central Japan. For Ecol Manage 236:259–267

    Article  Google Scholar 

  • Sellers PJ, Berry JA, Collatz GJ, Field CB, Hall FG (1992) Canopy reflectance, photosynthesis, and transpiration. III. A reanalysis using improved leaf models and a new canopy integration scheme. Remote Sens Environ 42:187–216

    Article  Google Scholar 

  • Sharpe PJ, DeMichele DW (1977) Reaction kinetics of poikilotherm development. J Theor Biol 64:649–670

    Article  CAS  PubMed  Google Scholar 

  • Skillman JB, Strain BR, Osmond CB (1996) Contrasting patterns of photosynthetic acclimation and photoinhibition in two evergreen herbs from a winter deciduous forest. Oecologia 107:446–455

    Article  Google Scholar 

  • Takanashi S, Kosugi Y, Matsuo N, Tani M, Ohte N (2006) Patchy stomatal behavior in broad-leaved trees grown in different habitats. Tree Physiol 26:1565–1578. doi:10.1093/treephys/26.12.1565

    Article  PubMed  Google Scholar 

  • Tenhunen JD, Serra AS, Harley PC, Dougherty RL, Reynolds JF (1990) Factors influencing carbon fixation and water use by Mediterranean sclerophyll shrubs during summer drought. Oecologia 82:381–393

    Article  Google Scholar 

  • Wilson KB, Baldocchi D (2001) Comparing independent estimates of carbon dioxide exchange over 5 years at a deciduous forest in the southeastern United States. J Geophys Res 106:34167–34178. doi:10.1029/2001JD000624

    Article  CAS  Google Scholar 

  • Wilson KB, Baldocchi D, Hanson PJ (2000) Spatial and seasonal variability of photosynthetic parameters and their relationship to leaf nitrogen in a deciduous forest. Tree Physiol 20:565–578

    Article  PubMed  Google Scholar 

  • Xu L, Baldocchi D (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

    Article  PubMed  Google Scholar 

  • Yamamura Y, Kimura M (1992) Matter-economical roles of evergreen leaves in Aucuba japonica, an understory shrub in the warm-temperate region of Japan 2. Dynamics and budgets of nutrients. Bot Mag (Tokyo) 105:95–104

    Article  CAS  Google Scholar 

  • Yasumura Y, Hikosaka K, Hirose T (2006) Seasonal changes in photosynthesis, nitrogen content and nitrogen partitioning in Lindera umbellata leaves grown in high or low irradiance. Tree Physiol 26:1315–1323

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported in part by Grants-in-Aid for Scientific Research (Nos. 11213209, 11480130, and 25281005) from the Ministry of Education, Science and Culture, Japan.

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Authors and Affiliations

  1. Hydrospheric Atmospheric Research Center, Nagoya University, Chikusa-ku, Nagoya, 464-8601, Japan

    Shuko Hamada, Tomo’omi Kumagai, Kiyotaka Kochi, Nakako Kobayashi & Tetsuya Hiyama

  2. Academic Research and Industry-Academia-Government Collaboration, Nagoya University, Chikusa-ku, Nagoya, 464-8601, Japan

    Shuko Hamada

  3. Department of Geography, University of Hawai’i at Manoa, Honolulu, HI, 96822, USA

    Yoshiyuki Miyazawa

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  1. Shuko Hamada
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  2. Tomo’omi Kumagai
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  3. Kiyotaka Kochi
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  5. Tetsuya Hiyama
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  6. Yoshiyuki Miyazawa
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Correspondence to Shuko Hamada.

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Communicated by C. Lovelock.

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Hamada, S., Kumagai, T., Kochi, K. et al. Spatial and temporal variations in photosynthetic capacity of a temperate deciduous-evergreen forest. Trees 30, 1083–1093 (2016). https://doi.org/10.1007/s00468-015-1347-4

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  • DOI: https://doi.org/10.1007/s00468-015-1347-4

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