Global patterns of leaf mechanical properties.

Leaf mechanical properties strongly influence leaf lifespan, plant-herbivore interactions, litter decomposition and nutrient cycling, but global patterns in their interspecific variation and underlying mechanisms remain poorly understood. We synthesize data across the three major measurement methods, permitting the first global analyses of leaf mechanics and associated traits, for 2819 species from 90 sites worldwide. Key measures of leaf mechanical resistance varied c. 500-800-fold among species. Contrary to a long-standing hypothesis, tropical leaves were not mechanically more resistant than temperate leaves. Leaf mechanical resistance was modestly related to rainfall and local light environment. By partitioning leaf mechanical resistance into three different components we discovered that toughness per density contributed a surprisingly large fraction to variation in mechanical resistance, larger than the fractions contributed by lamina thickness and tissue density. Higher toughness per density was associated with long leaf lifespan especially in forest understory. Seldom appreciated in the past, toughness per density is a key factor in leaf mechanical resistance, which itself influences plant-animal interactions and ecosystem functions across the globe.

[1]  A. Schimper,et al.  Plant-geography upon a physiological basis , 2022 .

[2]  A. Loveless A Nutritional Interpretation of Sclerophylly Based on Differences in the Chemical Composition of Sclerophyllous and Mesophytic Leaves , 1961 .

[3]  N. Beadle Soil Phosphate and Its Role in Molding Segments of the Australian Flora and Vegetation, with Special Reference to Xeromorphy and Sclerophylly , 1966 .

[4]  Veva Elwell,et al.  Toxicity and Anti-Inflammatory Activity of Phenolic-Rich Extract from Nopalea cochenillifera (Cactaceae): A Preclinical Study on the Prevention of Inflammatory Bowel Diseases , 2023, Plants.

[5]  J. M. Cherrett A Simple Penetrometer for Measuring Leaf Toughness in Insect Feeding Studies , 1968 .

[6]  P. Feeny SEASONAL CHANGES IN OAK LEAF TANNINS AND NUTRIENTS AS A CAUSE OF SPRING FEEDING BY WINTER MOTH CATERPILLARS , 1970 .

[7]  R. Whittaker Communities and Ecosystems , 1975 .

[8]  Robert H. Smith The analysis of intra-generation change in animal populations. , 1973 .

[9]  D. Levin The Chemical Defenses of Plants to Pathogens and Herbivores , 1976 .

[10]  D. Levin,et al.  The toxicity of plant alkaloids: an Ecogeographic perspective , 1978 .

[11]  Yiu-Wing Mai,et al.  On the guillotining of materials , 1979 .

[12]  T. Givnish On the Adaptive Significance of Leaf Form , 1979 .

[13]  David J. Hicks,et al.  The Ecology of Leaf Life Spans , 1982 .

[14]  P. Coley,et al.  HERBIVORY AND DEFENSIVE CHARACTERISTICS OF TREE SPECIES IN A LOWLAND TROPICAL FOREST , 1983 .

[15]  A. Atkins,et al.  Elastic and Plastic Fracture: Metals, Polymers, Ceramics, Composites, Biological Materials , 1985 .

[16]  J. Felsenstein Phylogenies and the Comparative Method , 1985, The American Naturalist.

[17]  Thomas J. Givnish,et al.  Adaptation to Sun and Shade: a Whole-Plant Perspective , 1988 .

[18]  P. Lucas,et al.  Estimation of the fracture toughness of leaves , 1990 .

[19]  P. Lucas,et al.  The Fracture Toughness of the Leaf of the Dicotyledon Calophyllum inophyllum L. (Guttiferae) , 1991 .

[20]  O. Pellmyr Plant-Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions , 1991 .

[21]  P. Lucas,et al.  Leaf fracture toughness and sclerophylly: their correlations and ecological implications , 1992 .

[22]  M. Pagel A method for the analysis of comparative data , 1992 .

[23]  P. Coley,et al.  Delayed greening in tropical leaves: an antiherbivore defense? , 1992 .

[24]  P. Lucas,et al.  How Tough are Sclerophylls , 1993 .

[25]  J. P. Grime,et al.  Methods in comparative plant ecology : a laboratory manual , 1993 .

[26]  J. P. Grime,et al.  Methods in Comparative Plant Ecology , 1993, Springer Netherlands.

[27]  P. V. Soest Nutritional Ecology of the Ruminant , 1994 .

[28]  I. Turner Sclerophylly: primarily protective? , 1994 .

[29]  W. Wright,et al.  A comparative study of the fracture properties of five grasses , 1995 .

[30]  D. Henry,et al.  Measurement of the shear and tensile fracture properties of leaves of pasture grasses , 1996 .

[31]  Brian W. Darvell,et al.  A portable fracture toughness tester for biological materials , 1996 .

[32]  M. F. Choong What makes a leaf tough and how this affects the pattern of Castanopsis fissa leaf consumption by caterpillars , 1996 .

[33]  J. Vincent,et al.  HERBIVORY AND THE MECHANICS OF FRACTURE IN PLANTS , 1996 .

[34]  J. A. Barone,et al.  HERBIVORY AND PLANT DEFENSES IN TROPICAL FORESTS , 1996 .

[35]  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.

[36]  J. Cornelissen,et al.  Functional leaf attributes predict litter decomposition rate in herbaceous plants. , 1997, The New phytologist.

[37]  Hendrik Poorter,et al.  Is inherent variation in RGR determined by LAR at low irradiance and by NAR at high irradiance? A review of herbaceous species , 1998 .

[38]  P. Jones,et al.  Representing Twentieth-Century Space–Time Climate Variability. Part I: Development of a 1961–90 Mean Monthly Terrestrial Climatology , 1999 .

[39]  N. Aranwela,et al.  Methods of assessing leaf‐fracture properties , 1999 .

[40]  J. Read,et al.  Characterising sclerophylly: some mechanical properties of leaves from heath and forest , 2000, Oecologia.

[41]  V. De Luca,et al.  The cell and developmental biology of alkaloid biosynthesis. , 2000, Trends in plant science.

[42]  Ian J. Wright,et al.  Relationships between leaf lifespan and structural defences in a low-nutrient, sclerophyll flora , 2001 .

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

[44]  V. Mosbrugger,et al.  Evolution and Function of Leaf Venation Architecture: A Review , 2001 .

[45]  S. Pennings,et al.  LATITUDINAL VARIATION IN PALATABILITY OF SALT-MARSH PLANTS: WHICH TRAITS ARE RESPONSIBLE? , 2002 .

[46]  M. Westoby,et al.  ECOLOGICAL STRATEGIES : Some Leading Dimensions of Variation Between Species , 2002 .

[47]  M. Westoby,et al.  Leaves at low versus high rainfall: coordination of structure, lifespan and physiology. , 2002, The New phytologist.

[48]  K. Thompson,et al.  Leaf traits as indicators of resource-use strategy in floras with succulent species , 2002 .

[49]  P. Reich,et al.  Least‐Cost Input Mixtures of Water and Nitrogen for Photosynthesis , 2002, The American Naturalist.

[50]  J. Read,et al.  Characterizing sclerophylly: the mechanical properties of a diverse range of leaf types. , 2003, The New phytologist.

[51]  Sandra Díaz,et al.  Leaf traits and herbivore selection in the field and in cafeteria experiments , 2003 .

[52]  P. Reich,et al.  A handbook of protocols for standardised and easy measurement of plant functional traits worldwide , 2003 .

[53]  I. Terashima Anatomy of non-uniform leaf photosynthesis , 1992, Photosynthesis Research.

[54]  P. Lucas Dental Functional Morphology: How Teeth Work , 2004 .

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

[56]  Tadaki Hirose,et al.  Allocation of nitrogen to cell walls decreases photosynthetic nitrogen‐use efficiency , 2004 .

[57]  P. Reich,et al.  Leaf lifespan as a determinant of leaf structure and function among 23 amazonian tree species , 1991, Oecologia.

[58]  Sandra Díaz,et al.  Chemistry and toughness predict leaf litter decomposition rates over a wide spectrum of functional types and taxa in central Argentina , 2004, Plant and Soil.

[59]  J. P. Grime,et al.  The plant traits that drive ecosystems: Evidence from three continents , 2004 .

[60]  K. Hikosaka,et al.  Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species , 2004 .

[61]  J. Read,et al.  Leaf Mechanical Properties in Sclerophyll Woodland and Shrubland on Contrasting Soils , 2005, Plant and Soil.

[62]  J. Read,et al.  Do tropical species invest more in anti-herbivore defence than temperate species? A test in Eucryphia (Cunoniaceae) in eastern Australia , 2005, Journal of Tropical Ecology.

[63]  S. Pennings,et al.  LINKING BIOGEOGRAPHY AND COMMUNITY ECOLOGY: LATITUDINAL VARIATION IN PLANT–HERBIVORE INTERACTION STRENGTH , 2005 .

[64]  G. Sanson,et al.  The biomechanics of browsing and grazing. , 2006, American journal of botany.

[65]  M Henry H Stevens,et al.  The growth-defense trade-off and habitat specialization by plants in Amazonian forests. , 2006, Ecology.

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

[67]  Alexia Stokes,et al.  Plant biomechanics in an ecological context. , 2006, American journal of botany.

[68]  P. Reich,et al.  Fundamental trade-offs generating the worldwide leaf economics spectrum. , 2006, Ecology.

[69]  J. Read,et al.  Leaf biomechanical properties and the densities of herbivorous insect guilds , 2007 .

[70]  F. Clissold The Biomechanics of Chewing and Plant Fracture: Mechanisms and Implications , 2007 .

[71]  Y. Onoda,et al.  Effects of light and nutrient availability on leaf mechanical properties of Plantago major: a conceptual approach. , 2008, Annals of botany.

[72]  Campbell O. Webb,et al.  Bioinformatics Applications Note Phylocom: Software for the Analysis of Phylogenetic Community Structure and Trait Evolution , 2022 .

[73]  N. Dominy,et al.  In tropical lowland rain forests monocots have tougher leaves than dicots, and include a new kind of tough leaf. , 2008, Annals of botany.

[74]  P. Reich,et al.  Why are evergreen leaves so contrary about shade? , 2008, Trends in ecology & evolution.

[75]  L. Williams THE FEEDING HABITS AND FOOD PREFERENCES OF ACRIDIDAE AND THE FACTORS WHICH DETERMINE THEM , 2009 .

[76]  L. Poorter,et al.  Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. , 2009, The New phytologist.

[77]  G. Mittelbach,et al.  Is There a Latitudinal Gradient in the Importance of Biotic Interactions , 2009 .

[78]  Yang-jian Zhang,et al.  Is there more insect folivory in warmer temperate climates? A latitudinal comparison of insect folivory in eastern North America , 2009 .

[79]  J. Read,et al.  Correlations between leaf toughness and phenolics among species in contrasting environments of Australia and New Caledonia. , 2009, Annals of botany.

[80]  Ichiro Terashima,et al.  Resistances along the CO2 diffusion pathway inside leaves. , 2009, Journal of experimental botany.

[81]  Kaoru Kitajima,et al.  Tissue-level leaf toughness, but not lamina thickness, predicts sapling leaf lifespan and shade tolerance of tropical tree species. , 2010, The New phytologist.

[82]  P. Sharma Mechanics of materials. , 2010, Technology and health care : official journal of the European Society for Engineering and Medicine.

[83]  J. Klomp,et al.  A review and synthesis , 2010 .

[84]  Y. Onoda,et al.  Reconciling species-level vs plastic responses of evergreen leaf structure to light gradients: shade leaves punch above their weight. , 2010, The New phytologist.

[85]  F. Woodward,et al.  Terrestrial Gross Carbon Dioxide Uptake: Global Distribution and Covariation with Climate , 2010, Science.