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Photosynthetically distinct responses of an early-successional tree, Betula ermanii, following a defoliating disturbance: observational results of a manipulated typhoon-mimic experiment

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Key message

The recovery of leaf photosynthetic rate of an early successional tree, Betula ermanii, to its pre-disturbance state following a defoliating disturbance was brought about by its fast leaf morphological response (LMA, leaf mass per area) but not physiological one (leaf N) as a resilience mechanism.

Abstract

Climate extremes possibly impair terrestrial vegetation and alter carbon cycles. Meanwhile, large uncertainty remains for evaluating the climatic impact on the vegetational function and structure and ecosystem CO2 exchange. We manipulated a defoliating disturbance experimentally in early September 2011 to simulate an extreme typhoon that actually hit a cool-temperate forest in Japan and ripped away a tremendous amount of foliage of early-successional B. ermanii trees in early September 2004, which corresponded to a decrease in plant area index (PAI) by 1.7 m2 m−2 from 3.3 m2 m−2 of the maximum PAI during the plant growth period. Over the 4-year observations in 2011–2016, we measured leaf-level photosynthesis following the manipulated disturbance. The highest maximum photosynthetic rate of leaves (Amax) occurred in 2014 among the observational period, which was the third year after the disturbance, and the subsequent Amax returned to the pre-disturbance state. We examined what biotic factors regulated Amax following the disturbance and found that the increase in the morphological attribute of leaf mass per area (LMA) enhanced Amax with a significant positive slope between LMA and Amax (R2 = 0.14 and p < 0.1). Meanwhile, Amax was hardly affected by the physiological attribute of leaf nitrogen (N) as indicated by a nonsignificant slope of the leaf N–Amax relationship (R2 = 0.04 and p = 0.281) throughout the observational period. This study would be a first challenge of a stand-scale defoliation experiment and provides a possible ecological inference regarding the functional and structural responses of early-successional trees following such disturbances.

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References

  • Baldocchi D, Chu H, Reichstein M (2018) Inter-annual variability of net and gross ecosystem carbon flux: a review. Agric For Meteorol 249:520–533

    Article  Google Scholar 

  • Chapin III, Matson PA, Vitousek P (2011) Principles of terrestrial ecosystem ecology, 2nd edn. Springer, New York

    Book  Google Scholar 

  • Ciais Ph, Reichstein M, Viovy N, Granier A, Ogée J, Allard V et al (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437:529–533

    Article  CAS  Google Scholar 

  • Edwards EJ, Chatelet DS, Sack L, Donoghue MJ (2014) Leaf life span and the leaf economic spectrum in the context of whole plant architecture. J Ecol 102:328–336

    Article  Google Scholar 

  • Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19

    Article  Google Scholar 

  • Foster DR, Aber JD (2004) Forests in time: the environmental consequences of 1000 years of change in New England. Yale University Press, United States, p 496

    Google Scholar 

  • Fukuzawa K, Shibata H, Takagi K, Satoh F, Koike T, Sasa K (2015) Roles of dominant understory Sasa bamboo in carbon and nitrogen dynamics following canopy tree removal in a cool-temperate forest in northern Japan. Plant Species Biol 30:104–115

    Article  Google Scholar 

  • Gough CM, Hardiman BS, Nave LE, Bohrer G, Maurer KD, Vogel CS, Nadelhoffer KJ, Curtis PS (2013) Sustained carbon uptake and storage following moderate disturbance in a Great Lakes forest. Ecol Appl 23:1202–11215

    Article  Google Scholar 

  • Hikosaka K, Nagamatsu D, Ishii HS, Hirose T (2002) Photosynthesis-nitrogen relationships in species at different altitudes on Mount Kinabalu, Malaysia. Ecol Res 17:305–313

    Article  Google Scholar 

  • Hufkens K, Friedl MA, Keenan TF, Sonnentag O, Bailey A, O’keefe J, Richardson AD (2012) Ecological impacts of a widespread frost event following early spring leaf out. Glob Change Biol 18:2365–2377

    Article  Google Scholar 

  • Ishii HT, Kobayashi T, Uemura S, Takahashi K, Hanba YT, Sumida A, Hara T (2008) Removal of understory dwarf bamboo (Sasa kurilensis) induces changes in water-relations characteristics of overstory Betula ermanii trees. J For Res 13:101–109

    Article  Google Scholar 

  • Jentsch A, Kreyling J, Beierkuhnlein C (2007) A new generaltion of climate-change experiments: events, not trends. Front Ecol Environ 5:365–374

    Article  Google Scholar 

  • Kattge J, Knorr W, Raddatz T, Wirth C (2009) Quantifying photosynthetic capacity and its relationship to leaf nitrogen content for global-scale terrestrial biosphere models. Glob Change Biol 15:976–991

    Article  Google Scholar 

  • Keenan TF, Darby B, Felts E, Sonnentag O, Friedl MA, Jufkens K, O’Keefe J, Klosterman S, Munger JW, Toomey M, Richardson AD (2014) Tracking forest phenology and seasonal physiology using digital repeat photography: a critical assessment. Ecol Appli 24:1478–1489

    Article  CAS  Google Scholar 

  • Kitaoka S, Koike T (2004) Invasion of broad-leaf tree species into a larch plantation: seasonal light environment, photosynthesis and nitrogen allocation. Physiol Plant 121:604–611

    Article  CAS  Google Scholar 

  • Knohl A, Kolle O, Minayeva TY, Milyukova IM, Vygodskaya NN, Foken T, Schulze E-D (2002) Carbon dioxide exchange of a Russian boreal forest after disturbance by wind throw. Glob Change Biol 8:231–246

    Article  Google Scholar 

  • Lasslop G, Reichstein M, Kattge J, Papale D (2008) Influences of observation errors in eddy flux data on inverse model parameter estimation. Biogeosciences 5:1311–1324

    Article  CAS  Google Scholar 

  • Lokhande S, Ogawa K, Tanaka A, Hara T (2003) Effect of temperature on ascorbate peroxidase activity and flowering of Arabidopsis thaliana ecotypes under different light conditions. J Plant Physiol 160:57–64

    Article  CAS  Google Scholar 

  • Macfarlane C (2011) Classification method of mixed pixels does not affect canopy metrics from digital images of forest overstory. Agric For Meteorol 151:833–840

    Article  Google Scholar 

  • Macfarlane C, Hoffman M, Eamus D, Kerp N, Higginson S, McMurtrie R, Adams M (2007) Estimation of leaf area index in eucalypt forest using digital photography. Agric For Meteorol 143:176–188

    Article  Google Scholar 

  • Nave LE, Gough CM, Maurer KD, Bohrer G, Hardiman BS, Moine JL, Munoz AB, Nadelhoffer KJ, Sparks JP, Strahm BD, Vogel CS, Curtis PS (2011) Disturbance and the resilience of coupled carbon and nitrogen cycling in a north temperate forest. J Geophys Res 116:G04016. https://doi.org/10.1029/2011JG001758

    Article  CAS  Google Scholar 

  • Noda HM, Muraoka H, Nasahara NK, Saigusa N, Murayama S, Koizumi H (2015) Phenology of leaf morphological, photosynthetic, and nitrogen use characteristics of canopy trees in a cool-temperate deciduous broadleaf forest at Takayama, central Japan. Ecol Res 30:247–266

    Article  CAS  Google Scholar 

  • Noguchi M, Yoshida T (2005) Factors influencing the distribution of two co-occurring dwarf bamboo species (Sasa kurilensis and S. senanensis) in a conifer-broadleaved mixed stand in northern Hokkaido. Ecol Res 20:25–30

    Article  Google Scholar 

  • Onoda Y, Hikosaka K, Hirose T (2004) Allocation of nitrogen to cell walls decreases photosynthetic nitrogen-use efficiency. Funct Ecol 18:419–425

    Article  Google Scholar 

  • Pregitzer KS, Euskirchen ES (2004) Carbon cycling and storage in world forests: biome patterns related to forest age. Glob Change Biol 10:2052–2077

    Article  Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/

  • Reichstein M, Falge E, Baldocchi D, Papale D, Aubinet M, Berbigier P et al (2005) On the separation of net ecosystem exchange into assimilation and ecosystem respiration: review and improved algorithm. Glob Change Biol 11:1424–1439

    Article  Google Scholar 

  • Reichstein M, Bahn M, Ciais P, Frank D, Mahecha MD, Seneviratne SI, Zxheischler J, Beer C, Buchmann N, Frank DC, Papale D, Rammig A, Smith P, Thonicke K, Walz VM, Wattenbach A M (2013) Climate extremes and the carbon cycle. Nature 500:287–295

    Article  CAS  Google Scholar 

  • Richardson AD, Klosterman S, Toomey M (2013) Near-surface sensor-derived phenology. In: Schwarts MD (ed) Phenology: an integrative environmental science. Springer, New York

    Google Scholar 

  • Ryu Y, Sonnentag O, Nilson T, Vargas R, Kobayashi H, Wenk R, Baldocchi DD (2010) How to quantify tree leaf area index in an open savanna ecosystem: a multi-instrument and multi-model approach. Agric For Meteorol 150:63–76

    Article  Google Scholar 

  • Seidl R, Thom D, Kautz M, Martin-Benito D, Peltoniemi M, Vacchiano G, Wild J, Ascoli D, Petr M, Honkaniemi J, Lexer MJ, Trotsiuk V, Mairota P, Svoboda M, Fabrika M, Nagel TA, Reyer CPO (2017) Forest disturbances under climate change. Nature Clim Change 7:395–402

    Article  Google Scholar 

  • Sippel S, Forkel M, Rammig A, Thonicke K, Flach M, Heimann M, Otto FEL, Reichstein M, Mahecha MD (2017) Contrasting and interacting changes in simulated spring and summer carbon cycle extremes in European ecosystems. Environ Res Lett 12:075006

    Article  Google Scholar 

  • Stuart-Haëntjens EJ, Curtis PS, Fahey RT, Vogel CS, Gough CM (2015) Net primary production of a temperate deciduous forest exhibits a threshold response to increasing disturbance severity. Ecology 96:2478–2487

    Article  Google Scholar 

  • Tabata A, Ono K, Sumida A, Hara T (2010) Effects of soil water conditions on the morphology, phenology and photosynthesis of Betula ermanii in the boreal forest. Ecol Res 25:823–835

    Article  Google Scholar 

  • Takashima T, Hikosaka K, Hirose T (2004) Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant Cell Environ 27:1047–1054

    Article  CAS  Google Scholar 

  • Toda M, Richardson AD (2018) Estimation of plant area index and phenological transition dates from digital repeat photography and radiometric approaches in a hardwood forest in the Northeastern United States. Agric For Meteorol 249:457–466

    Article  Google Scholar 

  • Toda M, Kolari P, Nakai T, Kodama Y, Shibata H, Yoshida T, Uemura S, Sumida A, Kato K, Ono K, Hara T (2011) Photosynthetic recovery of foliage after wind disturbance activates ecosystem CO2 uptake in cool-temperate forest of northern Japan. J Geophys Res Biogeosci 116:G02006. https://doi.org/10.1029/2010JG001611

    Article  Google Scholar 

  • Toda M, Nakai T, Kodama Y, Hara T (2018) Using digital repeat photography to track the canopy recovery process following a typhoon disturbance in a cool-temperate deciduous forest. Can J For Res. https://doi.org/10.1139/cjfr-2018-0005

    Article  Google Scholar 

  • Yi C, Pndall E, Ciais P (2015) Focus on extreme events and the carbon cycle. Environ Res Lett 10:070201

    Article  Google Scholar 

  • Yoshida T, Iga Y, Ozawa M, Noguchi M, Shibata H (2005) Factors influencing early vegetation establishment following soil scarification in a mixed forest in Northern Japan. Can J For Res 35:175–188

    Article  Google Scholar 

  • Zscheischler J, Mahecha MD, Harmeling S, Reichstein M (2013) Detection and attribution of large spatiotemporal extreme events in Earth observation data. Ecol Inf 15:66–73

    Article  Google Scholar 

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Acknowledgements

We thank Takashi Kohyama and Takayuki Nakatsubo for their observational support to the present research. We appreciate Moe Wakatsuchi for her helpful support for drawing a figure. We acknowledge Moshiri Experimental Forest staff for their support for operating the field observation.

Funding

Partial financial support was given by a Grant-in-Aid for Scientific Research (C) (16K00515) to one of the authors (MT) funded by the Ministry of Education, Culture, Sports, Science and Technology. This research was partly supported by the Integrated Research Program for Advancing Climate Models (TOUGOU program) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan.

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Correspondence to Motomu Toda.

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Communicated by van der Maaten.

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Toda, M., Fukuzawa, K., Nakamura, M. et al. Photosynthetically distinct responses of an early-successional tree, Betula ermanii, following a defoliating disturbance: observational results of a manipulated typhoon-mimic experiment. Trees 32, 1789–1799 (2018). https://doi.org/10.1007/s00468-018-1770-4

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