Do we underestimate the importance of leaf size in plant economics? Disproportional scaling of support costs within the spectrum of leaf physiognomy.

BACKGROUND Broad scaling relationships between leaf size and function do not take into account that leaves of different size may contain different fractions of support in petiole and mid-rib. METHODS The fractions of leaf biomass in petiole, mid-rib and lamina, and the differences in chemistry and structure among mid-ribs, petioles and laminas were investigated in 122 species of contrasting leaf size, life form and climatic distribution to determine the extent to which differences in support modify whole-lamina and whole-leaf structural and chemical characteristics, and the extent to which size-dependent support investments are affected by plant life form and site climate. KEY RESULTS For the entire data set, leaf fresh mass varied over five orders of magnitude. The percentage of dry mass in mid-rib increased strongly with lamina size, reaching more than 40 % in the largest laminas. The whole-leaf percentage of mid-rib and petiole increased with leaf size, and the overall support investment was more than 60 % in the largest leaves. Fractional support investments were generally larger in herbaceous than in woody species and tended to be lower in Mediterranean than in cool temperate and tropical plants. Mid-ribs and petioles had lower N and C percentages, and lower dry to fresh mass ratio, but greater density (mass per unit volume) than laminas. N percentage of lamina without mid-rib was up to 40 % higher in the largest leaves than the total-lamina (lamina and mid-rib) N percentage, and up to 60 % higher than whole-leaf N percentage, while lamina density calculated without mid-rib was up to 80 % less than that with the mid-rib. For all leaf compartments, N percentage was negatively associated with density and dry to fresh mass ratio, while C percentage was positively linked to these characteristics, reflecting the overall inverse scaling between structural and physiological characteristics. However, the correlations between N and C percentages and structural characteristics differed among mid-ribs, petioles and laminas, implying that the mass-weighted average leaf N and C percentage, density, and dry to fresh mass ratio can have different functional values depending on the importance of within-leaf support investments. CONCLUSIONS These data demonstrate that variation in leaf size is associated with major changes in within-leaf support investments and in large modifications in integrated leaf chemical and structural characteristics. These size-dependent alterations can importantly affect general leaf structure vs. function scaling relationships. These data further demonstrate important life-form effects on and climatic differentiation in foliage support costs.

[1]  Thomas J. Givnish,et al.  COMPARATIVE STUDIES OF LEAF FORM: ASSESSING THE RELATIVE ROLES OF SELECTIVE PRESSURES AND PHYLOGENETIC CONSTRAINTS , 2008 .

[2]  Javrmila Solárová,et al.  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” , 1988, Biologia Plantarum.

[3]  M. Tobias,et al.  Leaf size modifies support biomass distribution among stems, petioles and mid-ribs in temperate plants. , 2006, The New phytologist.

[4]  M. Westoby,et al.  Cross‐species patterns in the coordination between leaf and stem traits, and their implications for plant hydraulics , 2006 .

[5]  Wenyun Zuo,et al.  A test of the generality of leaf trait relationships on the Tibetan Plateau. , 2006, The New phytologist.

[6]  M. Westoby,et al.  Bivariate line‐fitting methods for allometry , 2006, Biological reviews of the Cambridge Philosophical Society.

[7]  K. Niklas.  Plant allometry, leaf nitrogen and phosphorus stoichiometry, and interspecific trends in annual growth rates. , 2006, Annals of botany.

[8]  Mark G. Tjoelker,et al.  Universal scaling of respiratory metabolism, size and nitrogen in plants , 2006, Nature.

[9]  C. Körner,et al.  Construction costs, chemical composition and payback time of high- and low-irradiance leaves. , 2005, Journal of experimental botany.

[10]  A. Takenaka,et al.  Effects of leaf blade narrowness and petiole length on the light capture efficiency of a shoot , 1994, Ecological Research.

[11]  Ü. Niinemets,et al.  Structural determinants of leaf light-harvesting capacity and photosynthetic potentials , 2006 .

[12]  P. Shi,et al.  The leaf size-twig size spectrum of temperate woody species along an altitudinal gradient: an invariant allometric scaling relationship. , 2006, Annals of botany.

[13]  Dali Guo,et al.  Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. , 2005, The New phytologist.

[14]  P. Reich.  Global biogeography of plant chemistry: filling in the blanks. , 2005, The New phytologist.

[15]  Sandra Díaz,et al.  Specific leaf area and dry matter content estimate thickness in laminar leaves. , 2005, Annals of botany.

[16]  William G. Lee,et al.  Modulation of leaf economic traits and trait relationships by climate , 2005 .

[17]  U. Niinemets,et al.  Species differences in timing of leaf fall and foliage chemistry modify nutrient resorption efficiency in deciduous temperate forest stands. , 2005, Tree physiology.

[18]  I. Wright,et al.  Functional linkages between leaf traits and net photosynthetic rate: reconciling empirical and mechanistic models , 2005 .

[19]  D. Royer,et al.  Correlations of climate and plant ecology to leaf size and shape: potential proxies for the fossil record. , 2005, American journal of botany.

[20]  Karl J. Niklas,et al.  Nitrogen/phosphorus leaf stoichiometry and the scaling of plant growth , 2005 .

[21]  Hiroyuki Muraoka,et al.  Crown architecture in sun and shade environments: assessing function and trade-offs with a three-dimensional simulation model. , 2005, The New phytologist.

[22]  Fernando Valladares,et al.  Implications of opposite phyllotaxis for light interception efficiency of Mediterranean woody plants , 2005, Trees.

[23]  M. Westoby,et al.  Dry mass costs of deploying leaf area in relation to leaf size , 2005 .

[24]  I. Terashima,et al.  Construction and maintenance of the optimal photosynthetic systems of the leaf, herbaceous plant and tree: an eco-developmental treatise. , 2004, Annals of botany.

[25]  M. Tyree,et al.  Leaf Hydraulics and Its Implications in Plant Structure and Function , 2005 .

[26]  Alessandro Cescatti,et al.  Light capture efficiency decreases with increasing tree age and size in the southern hemisphere gymnosperm Agathis australis , 2005, Trees.

[27]  N. Holbrook,et al.  Functional design space of single-veined leaves: role of tissue hydraulic properties in constraining leaf size and shape. , 2004, Annals of botany.

[28]  P. Reich,et al.  Global patterns of plant leaf N and P in relation to temperature and latitude. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Sean C. Thomas,et al.  The worldwide leaf economics spectrum , 2004, Nature.

[30]  N. Holbrook,et al.  Hydraulic limitations imposed by crown placement determine final size and shape of Quercus rubra L. leaves , 2004 .

[31]  Alessandro Cescatti,et al.  Petiole length and biomass investment in support modify light interception efficiency in dense poplar plantations. , 2004, Tree physiology.

[32]  Ian J. Wright,et al.  World-wide leaf economics spectrum , 2004 .

[33]  Ü. Niinemets.  Are compound-leaved woody species inherently shade-intolerant? An analysis of species ecological requirements and foliar support costs , 2004, Plant Ecology.

[34]  N. Holbrook,et al.  The ‘hydrology’ of leaves: co‐ordination of structure and function in temperate woody species , 2003 .

[35]  M. Westoby,et al.  C O M M U N I T Y E C O L O G Y , 2022 .

[36]  N. Holbrook,et al.  Hydraulic and photosynthetic co‐ordination in seasonally dry tropical forest trees , 2002 .

[37]  J. Flexas,et al.  Regulation of photosynthesis of C3 plants in response to progressive drought: stomatal conductance as a reference parameter. , 2002, Annals of botany.

[38]  J. Flexas,et al.  Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. , 2002, Annals of botany.

[39]  J. Hibberd,et al.  Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants , 2002, Nature.

[40]  Ülo Niinemets,et al.  GLOBAL-SCALE CLIMATIC CONTROLS OF LEAF DRY MASS PER AREA, DENSITY, AND THICKNESS IN TREES AND SHRUBS , 2001 .

[41]  Hardy Pfanz,et al.  Leaf and twig photosynthesis of young beech (Fagus sylvatica) and aspen (Populus tremula) trees grown under different light regime , 2001 .

[42]  Hardy Pfanz,et al.  Photosynthetic Performance of Leaves and Twigs of Evergreen Holly (Ilex aquifolium L.) , 2000 .

[43]  Ülo Niinemets,et al.  Research review. Components of leaf dry mass per area – thickness and density – alter leaf photosynthetic capacity in reverse directions in woody plants , 1999 .

[44]  I. Noble,et al.  A theoretical approach to linking the composition and morphology with the function of leaves , 1999 .

[45]  I. Noble,et al.  On the relationship between the composition, morphology and function of leaves , 1999 .

[46]  P. Reich,et al.  Convergence and correlations among leaf size and function in seed plants: a comparative test using independent contrasts. , 1999, American journal of botany.

[47]  P. Reich,et al.  Generality of leaf trait relationships: a test across six biomes: Ecology , 1999 .

[48]  E. Garnier,et al.  Relationships between photosynthesis, nitrogen and leaf structure in 14 grass species and their dependence on the basis of expression , 1999 .

[49]  O. Kull,et al.  Biomass investment in leaf lamina versus lamina support in relation to growth irradiance and leaf size in temperate deciduous trees. , 1999, Tree physiology.

[50]  U. Niinemets.  Differences in chemical composition relative to functional differentiation between petioles and laminas of Fraxinus excelsior. , 1999, Tree physiology.

[51]  K. Hikosaka,et al.  Photosynthetic nitrogen‐use efficiency in leaves of woody and herbaceous species , 1998 .

[52]  John R. Evans,et al.  Photosynthetic nitrogen-use efficiency of species that differ inherently in specific leaf area , 1998, Oecologia.

[53]  Hendrik Poorter,et al.  Inherent variation in plant growth : physiological mechanisms and ecological consequences , 1998 .

[54]  P. Reich,et al.  From tropics to tundra: global convergence in plant functioning. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[55]  H. Poorter,et al.  The fate of acquired carbon in plants: chemical composition and construction costs , 1997 .

[56]  E. Garnier,et al.  Leaf anatomy, specific mass and water content in congeneric annual and perennial grass species , 1994 .

[57]  E. Schulze,et al.  Relationships among Maximum Stomatal Conductance, Ecosystem Surface Conductance, Carbon Assimilation Rate, and Plant Nitrogen Nutrition: A Global Ecology Scaling Exercise , 1994 .

[58]  Karl J. Niklas,et al.  Influence of Tissue Density-specific Mechanical Properties on the Scaling of Plant Height , 1993 .

[59]  K. Niklas.  BIOMECHANICAL RESPONSES OF CHAMAEDOREA AND SPATHIPHYLLUM PETIOLES TO TISSUE DEHYDRATION , 1991 .

[60]  H. Lambers,et al.  Carbon and nitrogen economy of 24 wild species differing in relative growth rate. , 1990, Plant physiology.

[61]  F. Chapin,et al.  The Cost of Tundra Plant Structures: Evaluation of Concepts and Currencies , 1989, The American Naturalist.

[62]  F.W.T. Penning de Vries,et al.  A rapid method for determining the efficiency of biosynthesis of plant biomass , 1987 .

[63]  E. Medina.  NUTRIENT BALANCE AND PHYSIOLOGICAL PROCESSES AT THE LEAF LEVEL. , 1984 .

[64]  Maurice Demarty,et al.  Calcium and the cell wall , 1984 .

[65]  T. Givnish.  Leaf and Canopy Adaptations in Tropical Forests , 1984 .

[66]  H. Mooney,et al.  Physiological ecology of plants of the wet tropics , 1984, Tasks for vegetation Science.

[67]  P. Larson,et al.  Structure of Leaf/Branch Gap Parenchyma and Associated Vascular Tissues in Populus deltoides , 1983, Botanical Gazette.

[68]  E. Tanner,et al.  STUDIES ON THE BIOMASS AND PRODUCTIVITY IN A SERIES OF MONTANE RAIN FORESTS IN JAMAICA , 1980 .

[69]  P. B. Tomlinson,et al.  Tropical trees as living systems: the proceedings of the fourth Cabot symposium held at Harvard Forest, Petersham, Massachusetts, on April 26-30, 1976 , 1978 .

[70]  P. Grubb.  Control of Forest Growth and Distribution on Wet Tropical Mountains: with Special Reference to Mineral Nutrition , 1977 .

[71]  Thomas J. Givnish,et al.  Sizes and Shapes of Liane Leaves , 1976, The American Naturalist.

[72]  H. Nimz.  Das Lignin der Buche — Entwurf eines Konstitutionsschemas , 1974 .

[73]  F. James Rohlf,et al.  Biometry: The Principles and Practice of Statistics in Biological Research , 1969 .