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Plant Biol (Stuttg) 2002; 4(4): 523-534
DOI: 10.1055/s-2002-34132
Original Paper
Georg Thieme Verlag Stuttgart ·New York

Leaf Biomechanics and Biomass Investment in Support in Relation to Long-Term Irradiance in Fagus

Ü. Niinemets 1 , S. Fleck 2
  • 1 Department of Plant Physiology, Institute of Molecular and Cell Biology, University of Tartu, Tartu, Estonia
  • 2 Department of Plant Ecology, University of Bayreuth, 95440 Bayreuth, Germany
Further Information

Publication History

Received: March 28, 2002

Accepted: June 19, 2002

Publication Date:
18 September 2002 (online)

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Abstract

We investigated biomass investment in support and assimilative leaf biomass in Fagus orientalis Lipsky and F. sylvatica L., and foliar biomechanical characteristics in F. orientalis to gain mechanistic insight into the determinants of leaf inclination in Fagus along the canopy light gradient. Because the leaf laminas of Fagus are elliptical, with petioles comprising only ca. 8 % of total leaf length, a leaf was approximated as a continuous sine load. Lamina load increased with increasing seasonal integrated quantum flux density in the canopy (Q int), but leaf length was independent of irradiance. Despite greater load, leaf deflection under leaf own weight was lower for leaves at higher Q int, indicating that foliage flexural stiffness (EI), that is a variable characterizing the resistance of beam-like structures to bending, scaled positively with irradiance. The components of EI - the leaf apparent Young's modulus of elasticity (E), which is a measure of leaf material properties, and lamina second moment of area (I), which characterizes the distribution of mass around the axis of bending - were also related to irradiance, with E decreasing, but I increasing with Q int. The positive scaling of I with Q int was associated with increases in leaf thickness and, in particular, with increases in the degree of leaf rolling, allowing the distribution of leaf mass further away from the neutral axis. Decreases in E were correlated with decreased leaf biomass investments in the midrib at higher irradiance. Both lamina and midrib nitrogen concentrations decreased with increasing Q int, suggesting that foliage dry mass based physiological activity was lower at higher irradiance, possibly because of an interaction of Q int with water stress in the canopy. Given that the veins also provide a pathway for water and nutrient transport to the leaf cells, as well as for carbon translocation from the leaf, lower leaf physiological activity in high light may provide an explanation for the lower biomass investment in major veins in high light. We conclude that foliage biomechanical characteristics and leaf inclination in the canopy are significantly affected by irradiance, and that the light effects may be modified by the reverse correlation between light and water availabilities in the canopy.

Key words

Carbon content - elastic modulus - flexural stiffness - light interception - nitrogen content - support costs

References

  • 01 Bayerischer Klimaforschungsverbund . (1998) Klimakarte: Niederschläge 1961 - 1990. München; Karten Zur Wasserwirtschaft, Bayerisches Landesamt für Wasserwirtschaft
    Search in Google Scholar
  • 02 Chabot,  B. F.,, Jurik,  T. W.,, and Chabot,  J. F.. (1979);  Influence of instantaneous and integrated light-flux density on leaf anatomy and photosynthesis.  American Journal of Botany. 66 940-945
    Search in Google Scholar
  • 03 Charles-Edwards,  D. A.,, Charles-Edwards,  J.,, and Sant,  F. I.. (1974);  Leaf photosynthetic activity in six temperate grass varieties grown in contrasting light and temperature environments.  Journal of Experimental Botany. 25 715-724
    Search in Google Scholar
  • 04 Chiariello,  N.. (1984) Leaf energy balance in the wet lowland tropics. Physiological ecology of plants of the wet tropics. Proceedings of an international symposium held in Oxatepec and Los Tuxtlas, Mexico, June 29 to July 6, 1983. Medina, E., Mooney, H. A., and Vásquez-Yánes, C., eds. The Hague; Tasks for Vegetation Science, 12, Dr. W. Junk Publishers pp. 85-98
    Search in Google Scholar
  • 05 Cochard,  H.,, Pfeiffer,  M.,, Le Gall,  K.,, and Granier,  A.. (1997);  Developmental control of xylem hydraulic resistances and vulnerability to embolism in Fraxinus excelsior L.: impacts on water relations.  Journal of Experimental Botany. 48 655-663
    Search in Google Scholar
  • 06 Cochard,  H.,, Lemoine,  D.,, Dreyer,  E.,, and Winter,  K.. (1999);  The effects of acclimation to sunlight on the xylem vulnerability to embolism in Fagus sylvatica L.  Plant, Cell and Environment. 22 101-108
    Search in Google Scholar
  • 07 Dijkstra,  P., and Lambers,  H.. (1989);  Analysis of specific leaf area and photosynthesis of two inbred lines of Plantago major differing in relative growth rate.  The New Phytologist. 113 283-290
    Search in Google Scholar
  • 08 Ennos,  A. R.. (1997);  Wind as an ecological factor.  Trends in Ecology and Evolution. 12 108-111
    Search in Google Scholar
  • 09 Ennos,  A. R.,, Spatz,  H.-C.,, and Speck,  T.. (2000);  The functional morphology of the petioles of the banana, Musa textilis. .  Journal of Experimental Botany. 51 2085-2093
    Search in Google Scholar
  • 10 Field,  C., and Mooney,  H. A.. (1986) The photosynthesis - nitrogen relationship in wild plants. On the economy of plant form and function. Proceedings of the Sixth Maria Moors Cabot Symposium, “Evolutionary constraints on primary productivity: adaptive patterns of energy capture in plants”, Harvard Forest, August 1983. Givnish, T. J., ed. Cambridge; Cambridge University Press pp. 25-55
    Search in Google Scholar
  • 11 Fleck,  S.,, Niinemets,  Ü.,, Cescatti,  A.,, and Tenhunen,  J. D.. (2002);  Foliage light harvesting efficiency in relation to long-term irradiance in Fagus. .  Tree Physiology. in press
    PubMedSearch in Google Scholar
  • 12 Gere,  J. M., and Timoshenko,  S. P.. (1997) Mechanics of materials, 4th edn. Boston; PWS Publishing Company
    Search in Google Scholar
  • 13 Gibson,  L. J.,, Ashby,  M. F.,, and Easterling,  K. E.. (1988);  Structure and mechanics of the iris leaf.  Journal of Materials Science. 23 3041-3048
    CrossrefPubMedSearch in Google Scholar
  • 14 Givnish,  T. J.. (1978);  Ecological aspects of plant morphology: leaf form in relation to environment.  Acta Biotheoretica. 27 83-142
    PubMedSearch in Google Scholar
  • 15 Givnish,  T. J.. (1979) On the adaptive significance of leaf form. Topics in plant population biology. Solbrig, O. T., Jain, S., Johnson, G. B., and Raven, P. H., eds. New York; Columbia University Press pp. 375-407
    Search in Google Scholar
  • 16 Heilman,  P. E.,, Hinckley,  T. M.,, Roberts,  D. A.,, and Ceulemans,  R.. (1996) Production physiology. Biology of Populus and its implications for management and conservation. Stettler, R. F., Bradshaw, H. D., Heilman, P. E., and Hinckley, T. M., eds. Ottawa; National Research Council Canada pp. 459-489
    Search in Google Scholar
  • 17 Hodánová,  D.. (1972);  Structure and development of sugar beet canopy. I. Leaf area - leaf angle relations.  Photosynthetica. 6 401-409
    PubMedSearch in Google Scholar
  • 18 Ishida,  A.,, Toma,  T.,, and Marjenah .. (1999);  Leaf gas exchange and chlorophyll fluorescence in relation to leaf angle, azimuth, and canopy position in the tropical pioneer tree, Macaranga conifera. .  Tree Physiology. 19 117-124
    PubMedSearch in Google Scholar
  • 19 Jurik,  T. W.,, Chabot,  J. F.,, and Chabot,  B. F.. (1982);  Effects of light and nutrients on leaf size, CO2 exchange, and anatomy in wild strawberry (Fragaria virginiana). .  Plant Physiology. 70 1044-1048
    PubMedSearch in Google Scholar
  • 20 Kim,  Y. T.,, Glerum,  C.,, Stoddart,  J.,, and Colombo,  S. J.. (1987);  Effect of fertilization on free amino acid concentrations in black spruce and jack pine containerized seedlings.  Canadian Journal of Forest Research. 17 27-30
    PubMedSearch in Google Scholar
  • 21 King,  M. J.,, Vincent,  J. F. V.,, and Harris,  W.. (1996);  Curling and folding of leaves of monocotyledons - a strategy for structural stiffness.  New Zealand Journal of Botany. 34 411-416
    PubMedSearch in Google Scholar
  • 22 Le Roux,  X.,, Walcroft,  A. S.,, Daudet,  F. A.,, Sinoquet,  H.,, Chaves,  M. M.,, Rodrigues,  A.,, and Osorio,  L.. (2001);  Photosynthetic light acclimation in peach leaves: importance of changes in mass : area ratio, nitrogen concentration, and leaf nitrogen partitioning.  Tree Physiology. 21 377-386
    PubMedSearch in Google Scholar
  • 23 Lovelock,  C. E., and Clough,  B. F.. (1992);  Influence of solar radiation and leaf angle on leaf xanthophyll concentrations in mangroves.  Oecologia. 91 518-525
    CrossrefPubMedSearch in Google Scholar
  • 24 Miller,  P. C.. (1967);  Leaf temperatures, leaf orientation and energy exchange in quaking aspen (Populus tremuloides) and Gambell's oak (Quercus gambellii) in central Colorado.  Acta Oecologica/Oecologia Plantarum. 2 241-270
    PubMedSearch in Google Scholar
  • 25 Morgan,  J., and Cannell,  M. G. R.. (1987);  Structural analysis of tree trunks and branches: tapered cantilever beams subject to large deflections under complex loading.  Tree Physiology. 3 365-374
    PubMedSearch in Google Scholar
  • 26 Moulia,  B., and Fournier,  M.. (1997);  Mechanics of the maize leaf: a composite beam model of the midrib.  Journal of Materials Science. 32 2771-2780
    CrossrefPubMedSearch in Google Scholar
  • 27 Moulia,  B.,, Fournier,  M.,, and Guitard,  D.. (1994);  Mechanics and form of the maize leaf: in vivo qualification of flexural behaviour.  Journal of Materials Science. 29 2359-2366
    CrossrefPubMedSearch in Google Scholar
  • 28 Näsholm,  T., and McDonald,  A. J. S.. (1990);  Dependence of amino acid composition upon nitrogen availability in birch (Betula pendula). .  Physiologia Plantarum. 80 507-514
    CrossrefPubMedSearch in Google Scholar
  • 29 Niinemets,  Ü.. (1995);  Distribution of foliar carbon and nitrogen across the canopy of Fagus sylvatica: adaptation to a vertical light gradient.  Acta Oecologica. 16 525-541
    PubMedSearch in Google Scholar
  • 30 Niinemets,  Ü.. (1998 a);  Adjustment of foliage structure and function to a canopy light gradient in two co-existing deciduous trees. Variability in leaf inclination angles in relation to petiole morphology.  Trees: Structure and Function. 12 446-451
    PubMedSearch in Google Scholar
  • 31 Niinemets,  Ü.. (1998 b);  Are compound-leaved woody species inherently shade-intolerant? An analysis of species ecological requirements and foliar support costs.  Plant Ecology. 134 1-11
    CrossrefPubMedSearch in Google Scholar
  • 32 Niinemets,  Ü.. (1999 a);  Differences in chemical composition relative to functional differentiation between petioles and laminas of Fraxinus excelsior. .  Tree Physiology. 19 39-45
    PubMedSearch in Google Scholar
  • 33 Niinemets,  Ü.. (1999 b);  Research review. Components of leaf dry mass per area - thickness and density - alter leaf photosynthetic capacity in reverse directions in woody plants.  The New Phytologist. 144 35-47
    CrossrefPubMedSearch in Google Scholar
  • 34 Niinemets,  Ü., and Fleck,  S.. (2002);  Petiole mechanics, leaf inclination, morphology, and investment in support in relation to light availability in the canopy of Liriodendron tulipifera. .  Oecologia. 132 21-33
    CrossrefPubMedSearch in Google Scholar
  • 35 Niinemets,  Ü., and Kull,  O.. (1998);  Stoichiometry of foliar carbon constituents varies along light gradients in temperate woody canopies: implications for foliage morphological plasticity.  Tree Physiology. 18 467-479
    PubMedSearch in Google Scholar
  • 36 Niinemets,  Ü., and Kull,  O.. (1999);  Biomass investment in leaf lamina versus lamina support in relation to growth irradiance and leaf size in temperate deciduous trees.  Tree Physiology. 19 349-358
    PubMedSearch in Google Scholar
  • 37 Niinemets,  Ü.,, Kull,  O.,, and Tenhunen,  J. D.. (1998);  An analysis of light effects on foliar morphology, physiology, and light interception in temperate deciduous woody species of contrasting shade tolerance.  Tree Physiology. 18 681-696
    PubMedSearch in Google Scholar
  • 38 Niinemets,  Ü.,, Kull,  O.,, and Tenhunen,  J. D.. (1999);  Variability in leaf morphology and chemical composition as a function of canopy light environment in co-existing trees.  International Journal of Plant Sciences. 160 837-848
    CrossrefPubMedSearch in Google Scholar
  • 39 Niklas,  K. J.. (1991 a);  Effects of tissue volume and location on the mechanical consequences of dehydration of petioles.  American Journal of Botany. 78 361-369
    PubMedSearch in Google Scholar
  • 40 Niklas,  K. J.. (1991 b);  The elastic moduli and mechanics of Populus tremuloides (Salicaceae) petioles in bending and torsion.  American Journal of Botany. 78 989-996
    PubMedSearch in Google Scholar
  • 41 Niklas,  K. J.. (1991 c);  Flexural stiffness allometries of angiosperm and fern petioles and rachises: evidence for biomechanical convergence.  Evolution. 45 734-750
    PubMedSearch in Google Scholar
  • 42 Niklas,  K. J.. (1992 a);  Gravity induced effects on material properties and size of leaves on horizontal shoots of Acer saccharum (Aceraceae). .  American Journal of Botany. 79 820-827
    PubMedSearch in Google Scholar
  • 43 Niklas,  K. J.. (1992 b);  Petiole mechanics, light interception by lamina, and “Economy in Design”.  Oecologia. 90 518-526
    PubMedSearch in Google Scholar
  • 44 Niklas,  K. J.. (1993);  Testing “economy in design” in plants: are the petioles and rachises of leaves “designed” according to the principle of uniform strength?.  Annals of Botany. 71 33-41
    CrossrefPubMedSearch in Google Scholar
  • 45 Niklas,  K. J.. (1996);  Differences between Acer saccharum leaves from open and wind-protected sites.  Annals of Botany. 78 61-66
    CrossrefPubMedSearch in Google Scholar
  • 46 Niklas,  K. J.. (1999);  Research review. A mechanical perspective on foliage leaf form and function.  The New Phytologist. 143 19-31
    CrossrefPubMedSearch in Google Scholar
  • 47 Paolillo,  D. J., Jr.,, and Niklas,  K. J.. (1996);  Effects of Rht-dosage on the breaking strength of wheat seedling leaves.  American Journal of Botany. 83 567-572
    PubMedSearch in Google Scholar
  • 48 Pearcy,  R. W., and Valladares,  F.. (1999) Resource acquisition by plants: the role of crown architecture. Physiological plant ecology. Press, M. C., Scholes, J. D., and Barker, M. G., eds. Cornwall; Blackwell Science - MPG Books Ltd. pp. 45-66
    Search in Google Scholar
  • 49 Peters,  R.. (1992) Ecology of beech forests in the northern hemisphere. Wageningen; Landbouwuniversiteit Wageningen, Ph.D. Dissertation
    Search in Google Scholar
  • 50 Peters,  R.. (1997) Beech forests, Geobotany 24. Dordrecht, Boston, London; Kluwer Academic Publishers
    Search in Google Scholar
  • 51 Planchais,  I., and Sinoquet,  H.. (1998);  Foliage determinants of light interception in sunny and shaded branches of Fagus sylvatica L.  Agricultural and Forest Meteorology. 89 241-253
    CrossrefPubMedSearch in Google Scholar
  • 52 Preston,  R. D.. (1974) The physical biology of plant cell walls. London; Chapman and Hall
    Search in Google Scholar
  • 53 Ross,  J., and Sulev,  M.. (2000);  Sources of errors in measurements of PAR.  Agricultural and Forest Meteorology. 100 103-125
    CrossrefPubMedSearch in Google Scholar
  • 54 Schultz,  H. R., and Matthews,  M. A.. (1993);  Xylem development and hydraulic conductance in sun and shade shoots of grapevine (Vitis vinifera L.): evidence that low light uncouples water transport capacity from leaf area.  Planta. 190 393-406
    PubMedSearch in Google Scholar
  • 55 Shen,  C. F.. (1992) A monograph of the genus Fagus Tourn ex L. (Fagaceae). City University of New York; Ph.D. Dissertation
    Search in Google Scholar
  • 56 Sims,  D. A., and Pearcy,  R. W.. (1994);  Scaling sun and shade photosynthetic acclimation of Alocasia macrorrhiza to whole-plant performance - I. Carbon balance and allocation at different daily photon flux densities.  Plant, Cell and Environment. 17 881-887
    PubMedSearch in Google Scholar
  • 57 Tuffers,  A. V.,, Naidoo,  G.,, and von Willert,  D. J.. (1999);  The contribution of leaf angle to photoprotection in the mangroves Avicennia marina (Forssk.) Vierh. and Bruguiera gymnorrhiza (L.) Lam. under field conditions in South Africa.  Flora. 194 267-275
    PubMedSearch in Google Scholar
  • 58 Tyree,  M. T.,, Cochard,  H.,, Cruiziat,  P.,, Sinclair,  B.,, and Ameglio,  T.. (1993);  Drought-induced leaf shedding in walnut: evidence for vulnerability segmentation.  Plant, Cell and Environment. 16 879-882
    PubMedSearch in Google Scholar
  • 59 Valladares,  F., and Pearcy,  R. W.. (2000);  The role of crown architecture for light harvesting and carbon gain in extreme light environments assessed with a realistic 3-D model.  Anales Jardin Botanico de Madrid. 58 3-16
    PubMedSearch in Google Scholar
  • 60 Vertregt,  N., and Penning de Vries,  F. W. T.. (1987);  A rapid method for determining the efficiency of biosynthesis of plant biomass.  Journal of Theoretical Biology. 128 109-119
    PubMedSearch in Google Scholar
  • 61 Vincent,  J. F. V.. (1982);  The mechanical design of grass.  Journal of Materials Science. 17 856-860
    CrossrefPubMedSearch in Google Scholar
  • 62 Vincent,  J. F. V.. (1983);  The influence of water content on the stiffness and fracture properties of grass leaves.  Grass and Forage Science. 38 107-114
    PubMedSearch in Google Scholar
  • 63 Vogel,  S.. (1989);  Drag and reconfiguration of broad leaves in high winds.  Journal of Experimental Botany. 40 941-948
    PubMedSearch in Google Scholar
  • 64 Wetherhold,  R. C.. (1997) Mechanics of laminated structures. Composites engineering handbook. Mallick, P. K., ed. New York; Materials Engineering, Marcel Dekker, Inc. pp. 203-248
    Search in Google Scholar
  • 65 Young,  W. C., and Roark,  R. J.. (1989) Roark's formulas for stress & strain, 6th edn. New York; McGraw Hill
    Search in Google Scholar

Ü. Niinemets

Department of Plant Physiology
Institute of Molecular and Cell Biology
University of Tartu

Riia 23
EE 51010 Tartu
Estonia

Email: ylo@zbi.ee

Section Editor: L. A. C. J. Voesenek