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Low light acclimation in five temperate broad-leaved tree species of different successional status: the significance of a shade canopy

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Abstract

Context

Tree species differ largely in their capability to produce characteristic shade leaves with effective morphological and physiological acclimation to low light.

Aims

By examining the sun/shade leaf differentiation in leaf morphology, foliar nitrogen and photosynthetic capacity in five temperate tree species of different successional status, we aimed at identifying those leaf traits that determine the development of a typical shade crown with low light-acclimated leaves.

Methods

Leaf morphology, foliar N content, photosynthetic capacity (V cmax, J max and A max) and leaf dark respiration (R d) were measured in the canopies of 26 adult trees of Fraxinus, Acer, Carpinus, Tilia and Fagus species.

Results

Six traits (the sun/shade leaf differentiation in specific leaf area, leaf size, A max per leaf area or per mass, photosynthetic N use efficiency and R d) were found to characterise best the degree of low light acclimation in shade leaves. All five species exhibited certain modifications in leaf morphology and/or physiology in response to low light; Fagus sylvatica showed the highest and Fraxinus excelsior the lowest shade leaf acclimation.

Conclusions

Our results indicate that the five early/mid- to late-successional species have developed species-specific low light acclimation strategies in their shade crowns which differ in terms of the relative importance of leaf morphological and physiological acclimation.

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References

  • Ball JT, Woodrow IE, Berry JA (1987) A model predicting stomatal conductance and its contribution to the control of photosynthesis under different environmental conditions. In: Biggins J (ed) Progress in photosynthesis research IV. Martinus Nijhof, Dordrecht, pp 221–234

    Chapter  Google Scholar 

  • Bassow SL, Bazzaz FA (1997) Intra- and inter-specific variation in canopy photosynthesis in a mixed deciduous forest. Oecologia 109:507–515

    Article  Google Scholar 

  • Bazzaz FA (1979) Physiological ecology of plant succession. Annu Rev Ecol Syst 10:351–371

    Article  Google Scholar 

  • 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—estimates from gas-exchange measurements on spinach. Planta 165:397–406

    Article  CAS  Google Scholar 

  • Coste S, Roggy J-C, Sonnier G, Dreyer E (2010) Similar irradiance-elicited plasticity of leaf traits in saplings of 12 tropical rainforest tree species with highly different leaf mass-to-area ratio. Funct Plant Biol 37:1–14

    Google Scholar 

  • dePury 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 

  • Ellenberg H, Leuschner C (2010) Vegetation Mitteleuropas mit den Alpen. UTB, Stuttgart

    Google Scholar 

  • Ellsworth DS, Reich PB (1993) Canopy structure and vertical patterns of photosynthesis and related leaf traits in a deciduous forest. Oecologia 96:169–178

    Article  Google Scholar 

  • Falster DS, Westoby M (2003) Leaf size and angle vary widely across species: what consequences for light interception? New Phytol 158:509–525

    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  Google Scholar 

  • Fay MP, Shaw PA (2010) Exact and asymptotic weighted logrank tests for interval censored data: the interval R package. J Stat Softw 36:1–34

    Google Scholar 

  • Fleck S (2002) Integrated analysis of relationships between 3D-structure, leaf photosynthesis, and branch transpiration of mature Fagus sylvatica and Quercus petraea trees in a mixed forest stand. PhD thesis, University of Bayreuth, Bayreuth, Germany

  • Frazer GW, Trofymow JA, Lertzman KP (1999) Canopy openness and leaf area in chronosequences of coastal temperate rainforests. Can J For Res 30:239–256

    Google Scholar 

  • Gregor T, Seidling W (1997) 50 years’ succession on a woodland clearing in the mountain area of eastern Hesse. Forstwiss Centrbl 116:218–231

    Article  Google Scholar 

  • Hallik L, Niinemets U, Wright IJ (2009) Are species shade and drought tolerance reflected in leaf-level structural and functional differentiation in Northern Hemisphere temperate woody flora? New Phytol 184:257–274

    Article  PubMed  CAS  Google Scholar 

  • Harley PC, Tenhunen JD (1991) Modeling the photosynthetic response of C3 leaves to environmental factors. In: Boote KJ, Loomis RS (eds) Modeling crop photosynthesis—from biochemistry to canopy. American Society of Agronomy and Crop Science Society of America, Madison, pp 17–39

    Google Scholar 

  • Hölscher D (2004) Leaf traits and photosynthetic parameters of saplings and adult trees of co-existing species in a temperate broad-leaved forest. Basic Appl Ecol 5:163–172

    Article  Google Scholar 

  • Jones TA, Thomas SC (2007) Leaf-level acclimation to gap creation in mature Acer saccharum trees. Tree Physiol 27:281–290

    Article  PubMed  CAS  Google Scholar 

  • Köcher P, Gebauer T, Horna V, Leuschner C (2009) Leaf water status and stem xylem flux in relation to soil drought in five temperate broad-leaved tree species with contrasting water use strategies. Ann For Sci 66:101

    Article  Google Scholar 

  • Kutsch WL, Herbst M, Vanselow R, Hummelshoj P, Jensen NO, Kappen L (2001) Stomatal acclimation influences water and carbon fluxes of a beech forest in northern Germany. Basic Appl Ecol 2:265–281

    Article  Google Scholar 

  • Larcher W (1994) Ökophysiologie der Pflanzen. UTB, Stuttgart

    Google Scholar 

  • Leuzinger S, Zotz G, Asshoff R, Körner C (2005) Responses of deciduous forest trees to severe drought in Central Europe. Tree Physiol 25:641–650

    Article  PubMed  Google Scholar 

  • Liburnau, H. Ritter Lorenz v. Hrg (1908) Eckert-Lorenz Lehrbuch der Forstwirtschaft für Waldbau und Försterschulen Band 3, Verlag der k.u.k. Hofbuchndlung T.W. Frick, Wien

  • Lichtenthaler HK, Buschmann C, Döll M, Fietz H-J, Bach T, Kozel U, Meier D, Rahmsdorf U (1981) Photosynthetic activity, chloroplast ultrastructure, and leaf characteristics of high-light and low-light plants and of sun and shade leaves. Photosynth Res 2:115–141

    Google Scholar 

  • Masarovicova E, Stefancik L (1990) Some ecophysiological features in sun and shade leaves of tall beech trees. Biol Plant 32:374–387

    Article  Google Scholar 

  • Montpied P, Granier A, Dreyer E (2009) Seasonal time-course of gradients of photosynthetic capacity and mesophyll conductance to CO2 across a beech (Fagus sylvatica L.) canopy. J Exp Bot 60:2407–2418

    Google Scholar 

  • Niinemets U (2007) Photosynthesis and resource distribution through plant canopies. Plant Cell Environ 30:1052–1071

    Article  PubMed  CAS  Google Scholar 

  • Niinemets U (2010) A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance. Ecol Res 25:693–714

    Article  Google Scholar 

  • Niinemets U, Kull O, Tenhunen JD (1998) An analysis of light effects on foliar morphology, physiology, and light interception in temperate deciduous woody species of contrasting shade tolerance. Tree Physiol 18:681–696

    Article  PubMed  Google Scholar 

  • Ogren E, Evans JR (1993) Photosynthetic light-response curves. 1. The influence of CO2 partial-pressure and leaf inversion. Planta 189:182–190

    Article  Google Scholar 

  • Popma J, Bongers F, Werger MJA (1992) Gap-dependence and leaf characteristics of trees in a tropical lowland rain forest in Mexico. Oikos 63:207–214

    Article  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org. Accessed 15 May 2012

  • Schulze ED (1970) Der CO2-Gaswechsel der Buche (Fagus sylvatica L.) in Abhängigkeit von den Klimafaktoren im Freiland. Flora 159:177–232

    Google Scholar 

  • Sims DA, Gebauer RLE, Pearcy RW (1994) Scaling sun and shade photosynthetic acclimation of Alocasia macrorrhiza to whole-plant performance.2. Simulation of carbon balance and growth at different photon flux densities. Plant Cell Environ 17:889–900

    Article  CAS  Google Scholar 

  • Tholen D, Zhu XG (2011) The mechanistic basis of internal conductance: a theoretical analysis of mesophyll cell photosynthesis and CO2 diffusion. Plant Physiol 156:90–105

    Article  PubMed  CAS  Google Scholar 

  • Thornley JHM (2002) Instantaneous canopy photosynthesis: analytical expressions for sun and shade leaves based on exponential light decay down the canopy and an acclimated non-rectangular hyperbola for leaf photosynthesis. Ann Bot 89:451–458

    Article  PubMed  CAS  Google Scholar 

  • Urban O, Kosvancova M, Marek MV, Lichtenthaler HK (2007) Induction of photosynthesis and importance of limitations during the induction phase in sun and shade leaves of five ecologically contrasting tree species from the temperate zone. Tree Physiol 27:1207–1215

    Article  PubMed  Google Scholar 

  • Valladares F, Niinemets U (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annu Rev Ecol Evol Syst 39:237–257

    Article  Google Scholar 

  • Valladares F, Chico JM, Aranda I, Balaguer L, Dizengremel P, Manrique E, Dreyer E (2002) The greater seedling high-light tolerance of Quercus robur over Fagus sylvatica is linked to a greater physiological plasticity. Trees 16:395–403

    CAS  Google Scholar 

  • von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387

    Article  Google Scholar 

  • Wallenda T, Stober C, Hoegbom L, Schinkel H, Georg E, Hoegberg P, Read DJ (2000) Nitrogen uptake processes in roots and mycorrhizas. In: Schulze ED (ed) Carbon and nitrogen cycling in European forest ecosystems. Springer, Berlin, pp 122–143

    Chapter  Google Scholar 

  • Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56:435–447

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank all members of the Göttingen Experimental Botanical Garden (particularly Dirk Deilke and Ulrich Werder) and the student helpers for their support in operating the lifter in the forest. The authors thank the administration of Hainich National Park (especially Jens Wilhelm) for the collaboration and granting access to the forest sites, Paul Köcher for the fruitful cooperation, Professor Zucchini (University of Göttingen) for advice in the statistical analysis and Christina Langenbruch for comments on the manuscript.

Funding

This research was conducted in the framework of ‘Graduiertenkolleg 1086: The Role of Biodiversity for Biogeochemical Cycles and Biotic Interactions in Temperate Deciduous Forests’. The financial support granted by DFG is gratefully acknowledged.

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Correspondence to Christoph Leuschner.

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Handling Editor: Erwin Dreyer

Contribution of the co-authors

SF developed the study design, NL conducted the research, NL with support from SF conducted the analysis, and CL, NL and SF wrote the paper.

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Legner, N., Fleck, S. & Leuschner, C. Low light acclimation in five temperate broad-leaved tree species of different successional status: the significance of a shade canopy. Annals of Forest Science 70, 557–570 (2013). https://doi.org/10.1007/s13595-013-0298-4

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  • DOI: https://doi.org/10.1007/s13595-013-0298-4

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