Is there a species spectrum within the world-wide leaf economics spectrum? Major variations in leaf functional traits in the Mediterranean sclerophyll Quercus ilex.

The leaf economics spectrum is a general concept describing coordinated variation in foliage structural, chemical and physiological traits across resource gradients. Yet, within this concept,the role of within-species variation, including ecotypic and plastic variation components, has been largely neglected. This study hypothesized that there is a within-species economics spectrum within the general spectrum in the evergreen sclerophyll Quercus ilex which dominates low resource ecosystems over an exceptionally wide range. An extensive database of foliage traits covering the full species range was constructed, and improved filtering algorithms were developed. Standardized data filtering was deemed absolutely essential as additional variation sources can result in trait variation of 10–300%,blurring the broad relationships. Strong trait variation, c. two-fold for most traits to up to almost an order of magnitude, was uncovered.Although the Q. ilex spectrum is part of the general spectrum, within-species trait and climatic relationships in this species partly differed from the overall spectrum. Contrary to world-wide trends, Q. ilex does not necessarily have a low nitrogen content per mass and can increase photosynthetic capacity with increasing foliage robustness. This study argues that the within-species economics spectrum needs to be considered in regional- to biome-level analyses.

[1]  Ü. Niinemets Within-Canopy Variations in Functional Leaf Traits: Structural, Chemical and Ecological Controls and Diversity of Responses , 2016 .

[2]  J. Flexas,et al.  Photosynthetic limitations in Mediterranean plants: A review , 2014 .

[3]  Ü. Niinemets,et al.  Photosynthetic responses to stress in Mediterranean evergreens: Mechanisms and models , 2014 .

[4]  J. Peñuelas,et al.  Physiological and antioxidant responses of Quercus ilex to drought in two different seasons , 2014 .

[5]  Guirui Yu,et al.  Effects of Plant Functional Types, Climate and Soil Nitrogen on Leaf Nitrogen along the North-South Transect of Eastern China , 2013 .

[6]  B. Enquist,et al.  Assessing the causes and scales of the leaf economics spectrum using venation networks in Populus tremuloides , 2013 .

[7]  Distribution of leaf characteristics in relation to orientation within the canopy of woody species , 2013 .

[8]  Ian J. Wright,et al.  Impacts of trait variation through observed trait–climate relationships on performance of an Earth system model: a conceptual analysis , 2012 .

[9]  J. Fridley,et al.  Biogeographic constraints on the world‐wide leaf economics spectrum , 2012 .

[10]  B. Enquist,et al.  A common genetic basis to the origin of the leaf economics spectrum and metabolic scaling allometry. , 2012, Ecology letters.

[11]  Markus Neteler,et al.  A landscape genetics approach reveals ecological‐based differentiation in populations of holm oak (Quercus ilex L.) at the northern limit of its range , 2012 .

[12]  J. García-Plazaola,et al.  Photoprotection mechanisms in Quercus ilex under contrasting climatic conditions , 2012 .

[13]  Markus Reichstein,et al.  Gap Filling in the Plant Kingdom - Trait Prediction Using Hierarchical Probabilistic Matrix Factorization , 2012, ICML.

[14]  Jan-Philip M. Witte,et al.  Going beyond limitations of plant functional types when predicting global ecosystem–atmosphere fluxes: exploring the merits of traits‐based approaches , 2012 .

[15]  E. Andivia,et al.  Seasonal evolution of water status after outplanting of two provenances of Holm oak nursery seedlings , 2012, New Forests.

[16]  D. Royer,et al.  Roles of climate and functional traits in controlling toothed vs. untoothed leaf margins. , 2012, American journal of botany.

[17]  Miguel B. Araújo,et al.  Global patterns in the shape of species geographical ranges reveal range determinants , 2012 .

[18]  Cyrille Violle,et al.  The return of the variance: intraspecific variability in community ecology. , 2012, Trends in ecology & evolution.

[19]  S. Rambal,et al.  Photosynthetic sensitivity to drought varies among populations of Quercus ilex along a rainfall gradient. , 2012, Functional plant biology : FPB.

[20]  Ü. Niinemets,et al.  Terrestrial Photosynthesis in a Changing Environment: Photosynthesis during leaf development and ageing , 2012 .

[21]  J. Flexas,et al.  Terrestrial Photosynthesis in a Changing Environment: Ecophysiology of photosynthesis in semi-arid environments , 2012 .

[22]  Ghislain Vieilledent,et al.  When and how should intraspecific variability be considered in trait-based plant ecology? , 2011 .

[23]  S. Higgins,et al.  TRY – a global database of plant traits , 2011, Global Change Biology.

[24]  A. Arneth,et al.  Estimations of isoprenoid emission capacity from enclosure studies: measurements, data processing, quality and standardized measurement protocols , 2011 .

[25]  L. Gratani,et al.  Quercus ilex L. carbon sequestration capability related to shrub size , 2011, Environmental monitoring and assessment.

[26]  J. Kattge,et al.  Improving assessment and modelling of climate change impacts on global terrestrial biodiversity. , 2011, Trends in ecology & evolution.

[27]  Nathan J B Kraft,et al.  Sensitivity of leaf size and shape to climate: global patterns and paleoclimatic applications. , 2011, The New phytologist.

[28]  J. Peñuelas,et al.  Evergreens favored by higher responsiveness to increased CO₂. , 2011, Trends in ecology & evolution.

[29]  Ü. Niinemets,et al.  Tree Size- and Age-Related Changes in Leaf Physiology and Their Influence on Carbon Gain , 2011 .

[30]  M. Martín,et al.  Annual Variation of Foliar Nitrogen and Chlorophyll Contents in Mature Holm Oak Trees as a Basis for the Estimation of Canopy Nitrogen in a Mediterranean Wooded Grassland Ecosystem , 2011 .

[31]  F. Piper,et al.  Intraspecific trait variation and covariation in a widespread tree species (Nothofagus pumilio) in southern Chile. , 2011, The New phytologist.

[32]  M. Vaz,et al.  Leaf-level responses to light in two co-occurring Quercus (Quercus ilex and Quercus suber): leaf structure, chemical composition and photosynthesis , 2011, Agroforestry Systems.

[33]  Michael A. Forster,et al.  The adaptive value of functional and life-history traits across fertility treatments in an annual plant. , 2010, Annals of botany.

[34]  J. Baltzer,et al.  A Second Dimension to the Leaf Economics Spectrum Predicts Edaphic Habitat Association in a Tropical Forest , 2010, PLoS ONE.

[35]  M. Vaz,et al.  Drought-induced photosynthetic inhibition and autumn recovery in two Mediterranean oak species (Quercus ilex and Quercus suber). , 2010, Tree physiology.

[36]  A. Testi,et al.  MICROCLIMATIC RESPONSES OF PLANT COMMUNITIES TO CLIMATIC CHANGES: A STUDY CASE IN THE MEDITERRANEAN COASTAL VEGETATION NEAR ROME , 2010 .

[37]  F. Carevic,et al.  Plant water relations and edaphoclimatic conditions affecting acorn production in a holm oak (Quercus ilex L. ssp. ballota) open woodland , 2010, Agroforestry Systems.

[38]  I. Wright,et al.  Are species shade and drought tolerance reflected in leaf-level structural and functional differentiation in Northern Hemisphere temperate woody flora? , 2009, The New phytologist.

[39]  S. Higgins,et al.  Impacts of climate change on the vegetation of Africa: an adaptive dynamic vegetation modelling approach , 2009 .

[40]  Antoine Guisan,et al.  Importance of abiotic stress as a range‐limit determinant for European plants: insights from species responses to climatic gradients , 2009 .

[41]  J. Peñuelas,et al.  Process based inventory of isoprenoid emissions from European forests: model comparisons, current knowledge and uncertainties , 2009 .

[42]  J. Flexas,et al.  Differential photosynthetic performance and photoprotection mechanisms of three Mediterranean evergreen oaks under severe drought stress. , 2009, Functional plant biology : FPB.

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

[44]  P. Cox,et al.  Impact of changes in diffuse radiation on the global land carbon sink , 2009, Nature.

[45]  J. Flexas,et al.  Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. , 2009, Annals of botany.

[46]  D. Woodruff,et al.  Coordination of leaf structure and gas exchange along a height gradient in a tall conifer. , 2008, Tree physiology.

[47]  F. Valladares,et al.  Plasticity and stress tolerance override local adaptation in the responses of Mediterranean holm oak seedlings to drought and cold. , 2008, Tree physiology.

[48]  J. Flexas,et al.  Seasonal and inter-annual variations of gas exchange in thirteen woody species along a climatic gradient in the Mediterranean island of Mallorca , 2009 .

[49]  Benjamin Smith,et al.  Representation of vegetation dynamics in the modelling of terrestrial ecosystems: comparing two contrasting approaches within European climate space , 2008 .

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

[51]  C. François,et al.  Modelling leaf mass per area in forest canopy as affected by prevailing radiation conditions , 2008 .

[52]  Ontogenetic changes in stomatal and biochemical limitations to photosynthesis of two co-occurring Mediterranean oaks differing in leaf life span. , 2008, Tree physiology.

[53]  J. Peñuelas,et al.  Drought, warming and soil fertilization effects on leaf volatile terpene concentrations in Pinus halepensis and Quercus ilex , 2008, Acta Physiologiae Plantarum.

[54]  J. Lloyd,et al.  Climate‐dependent variations in leaf respiration in a dry‐land, low productivity Mediterranean forest: the importance of acclimation in both high‐light and shaded habitats , 2007 .

[55]  J. Peñuelas,et al.  Sensitivity of terpene emissions to drought and fertilization in terpene-storing Pinus halepensis and non-storing Quercus ilex. , 2007, Physiologia plantarum.

[56]  Peter B Reich,et al.  Predicting leaf physiology from simple plant and climate attributes: a global GLOPNET analysis. , 2007, Ecological applications : a publication of the Ecological Society of America.

[57]  U. Niinemets,et al.  Photosynthesis and resource distribution through plant canopies. , 2007, Plant, cell & environment.

[58]  F. Castillo,et al.  Drought tolerance in the Mediterranean species Quercus coccifera, Quercus ilex, Pinus halepensis, and Juniperus phoenicea , 2007, Photosynthetica.

[59]  Ian J. Wright,et al.  “Diminishing returns” in the scaling of functional leaf traits across and within species groups , 2007, Proceedings of the National Academy of Sciences.

[60]  J. Peñuelas,et al.  Seasonal soil VOC exchange rates in a Mediterranean holm oak forest and their responses to drought conditions , 2007 .

[61]  J. Peñuelas,et al.  Leaf mass per area ratio in Quercus ilex leaves under a wide range of climatic conditions. The importance of low temperatures , 2007 .

[62]  J. Peñuelas,et al.  Contrasting foliar responses to drought in Quercus ilex and Phillyrea latifolia , 2006, Biologia Plantarum.

[63]  M. Westoby,et al.  Interrelations among pressure–volume curve traits across species and water availability gradients , 2006 .

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

[65]  F. Covone,et al.  Leaf plasticity in response to light of three evergreen species of the Mediterranean maquis , 2006, Trees.

[66]  Alessandro Cescatti,et al.  Complex adjustments of photosynthetic potentials and internal diffusion conductance to current and previous light availabilities and leaf age in Mediterranean evergreen species Quercus ilex. , 2006, Plant, cell & environment.

[67]  Ü. Niinemets,et al.  Interacting controls by light availability and nutrient supply on biomass allocation and growth of Betula pendula and B. pubescens seedlings , 2006 .

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

[69]  Cassia F. Read,et al.  Gradients of light availability and leaf traits with leaf age and canopy position in 28 Australian shrubs and trees. , 2006, Functional plant biology : FPB.

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

[71]  J. Peñuelas,et al.  Plasticity of leaf morphological traits, leaf nutrient content, and water capture in the Mediterranean evergreen oak Quercus ilex subsp. ballota in response to fertilization and changes in competitive conditions , 2006 .

[72]  A. Cescatti,et al.  Leaf internal diffusion conductance limits photosynthesis more strongly in older leaves of Mediterranean evergreen broad‐leaved species , 2005 .

[73]  Ü. Niinemets,et al.  Biomass allocation and growth rates in Pinus sylvestris are interactively modified by nitrogen and phosphorus availabilities and by tree size and age , 2005 .

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

[75]  A. Abadı́a,et al.  Seasonal changes in photosynthesis and photoprotection in a Quercus ilex subsp. ballota woodland located in its upper altitudinal extreme in the Iberian Peninsula. , 2005, Tree physiology.

[76]  P. Reich,et al.  Assessing the generality of global leaf trait relationships. , 2005, The New phytologist.

[77]  N. Anten Optimal photosynthetic characteristics of individual plants in vegetation stands and implications for species coexistence. , 2004, Annals of botany.

[78]  J. Tenhunen,et al.  Spatial and age-dependent modifications of photosynthetic capacity in four Mediterranean oak species. , 2004, Functional plant biology : FPB.

[79]  F. Valladares,et al.  Winter photoinhibition in the field involves different processes in four co-occurring Mediterranean tree species. , 2004, Tree physiology.

[80]  Josep Cifre,et al.  Understanding down-regulation of photosynthesis under water stress: future prospects and searching for physiological tools for irrigation management , 2004 .

[81]  P. Reich,et al.  Short Communication: Leaf trait relationships in Australian plant species. , 2004, Functional plant biology : FPB.

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

[83]  A. Escudero,et al.  Relative growth rate of leaf biomass and leaf nitrogen content in several mediterranean woody species , 2003, Plant Ecology.

[84]  A. Bombelli,et al.  Leaf Anatomy, Inclination, and Gas Exchange Relationships in Evergreen Sclerophqldous and Drought Semideciduous Shrub Species , 2000, Photosynthetica.

[85]  A. Nardini,et al.  Different responses to drought and freeze stress of Quercus ilex L. growing along a latitudinal gradient , 2000, Plant Ecology.

[86]  L. Gratani Canopy structure, vertical radiation profile and photosynthetic function in a Quercus ilex evergreen forest , 1997, Photosynthetica.

[87]  J. Tenhunen,et al.  Canopy structure within a Quercus ilex forested watershed: variations due to location, phenological development, and water availability , 1994, Trees.

[88]  J. Canadell,et al.  Variation in tissue element concentrations in Quercus ilex L. over a range of different soils , 1992, Vegetatio.

[89]  M. Rapp,et al.  Productivity and nutrient uptake in a holm oak (Quercus ilex L.) stand and during regeneration after clearcut , 1992, Vegetatio.

[90]  L. Gratani,et al.  Morphological adaptions of Quercus ilex leaves in the Castelporziano forest , 1992, Vegetatio.

[91]  S. Rambal Quercus ilex facing water stress: a functional equilibrium hypothesis , 1992, Vegetatio.

[92]  J. Tenhunen,et al.  Seasonal changes in net photosynthesis rates and photosynthetic capacity in leaves of Cistus salvifolius, a European mediterranean semi-deciduous shrub , 1987, Oecologia.

[93]  J. Tenhunen,et al.  Midday stomatal closure in Mediterranean type sclerophylls under simulated habitat conditions in an environmental chamber , 1981, Oecologia.

[94]  S. Sabaté,et al.  Nutrient content in Quercus ilex canopies: Seasonal and spatial variation within a catchment , 2004, Plant and Soil.

[95]  A. Escudero,et al.  Decline in photosynthetic nitrogen use efficiency with leaf age and nitrogen resorption as determinants of leaf life span , 2003 .

[96]  Josep Peñuelas,et al.  Comparative field study of Quercus ilex and Phillyrea latifolia: photosynthetic response to experimental drought conditions , 2003 .

[97]  J. Flexas,et al.  Relationship between maximum leaf photosynthesis, nitrogen content and specific leaf area in balearic endemic and non-endemic mediterranean species. , 2003, Annals of botany.

[98]  L. Sack,et al.  Crossovers in seedling relative growth rates between low and high irradiance: analyses and ecological potential , 2003 .

[99]  Fernando Valladares,et al.  Plasticity, instability and canalization: is the phenotypic variation in seedlings of sclerophyll oaks consistent with the environmental unpredictability of Mediterranean ecosystems? , 2002, The New phytologist.

[100]  U. Niinemets Stomatal conductance alone does not explain the decline in foliar photosynthetic rates with increasing tree age and size in Picea abies and Pinus sylvestris. , 2002, Tree physiology.

[101]  G. Liakopoulos,et al.  The Relationship between Anatomy and Photosynthetic Performance of Heterobaric Leaves1 , 2002, Plant Physiology.

[102]  Antonio Donato Nobre,et al.  Acclimation of photosynthetic capacity to irradiance in tree canopies in relation to leaf nitrogen concentration and leaf mass per unit area , 2002 .

[103]  J. Tenhunen,et al.  Monoterpene emissions in relation to foliar photosynthetic and structural variables in Mediterranean evergreen Quercus species , 2002 .

[104]  J. Tenhunen,et al.  A model coupling foliar monoterpene emissions to leaf photosynthetic characteristics in Mediterranean evergreen Quercus species , 2002 .

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

[106]  A. Portsmuth,et al.  Leaf structural and photosynthetic characteristics, and biomass allocation to foliage in relation to foliar nitrogen content and tree size in three Betula species. , 2002, Annals of botany.

[107]  W. Larcher,et al.  Shoot growth efficiency and production of Quercus ilex L. in different climates , 2002 .

[108]  Filippo Bussotti,et al.  Structural and functional traits of Quercus ilex in response to water availability , 2002 .

[109]  E. Garnier,et al.  A standardized protocol for the determination of specific leaf area and leaf dry matter content , 2001 .

[110]  Eric Garnier,et al.  Consistency of species ranking based on functional leaf traits. , 2001, The New phytologist.

[111]  H. Heilmeier,et al.  Internal leaf anatomy and photosynthetic resource-use efficiency: interspecific and intraspecific comparisons. , 2001, Tree physiology.

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

[113]  F. Valladares,et al.  Population divergence in the plasticity of the response of Quercus coccifera to the light environment , 2001 .

[114]  A. Bombelli,et al.  Differences in leaf traits among Mediterranean broad-leaved evergreen shrubs , 2001 .

[115]  Miquel Ninyerola,et al.  A methodological approach of climatological modelling of air temperature and precipitation through GIS techniques , 2000 .

[116]  F. Valladares,et al.  Low leaf-level response to light and nutrients in Mediterranean evergreen oaks: a conservative resource-use strategy? , 2000, The New phytologist.

[117]  B. Bond Age-related changes in photosynthesis of woody plants. , 2000, Trends in plant science.

[118]  F. Bussotti,et al.  Leaf morphology and macronutrients in broadleaved trees in central Italy , 2000, Trees.

[119]  P. Reich,et al.  Variation in aboveground net primary production of diverse European Pinus sylvestris populations , 2000, Trees.

[120]  P. Reich,et al.  Genetic and environmental control of seasonal carbohydrate dynamics in trees of diverse Pinus sylvestris populations. , 2000, Tree physiology.

[121]  A. Bombelli,et al.  Correlation between leaf age and other leaf traits in three Mediterranean maquis shrub species: Quercus ilex, Phillyrea latifolia and Cistus incanus , 2000 .

[122]  W. Larcher,et al.  Photosynthesis as a temperature indicator in Quercus ilex L. , 2000 .

[123]  Leaf temperature effects on gas exchange in Quercus ilex L. growing under field conditions , 2000 .

[124]  F. Valladares,et al.  Energy dissipation in drought-avoiding and drought-tolerant tree species at midday during the Mediterranean summer. , 2000, Tree physiology.

[125]  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 .

[126]  Serge Rambal,et al.  Modelling leaf gas exchange in holm-oak trees in southern Spain , 1999 .

[127]  J. P. Grime,et al.  Interacting effects of herbivory and fertility on a synthesized plant community , 1999 .

[128]  O. Kull,et al.  Stoichiometry of foliar carbon constituents varies along light gradients in temperate woody canopies: implications for foliage morphological plasticity. , 1998, Tree physiology.

[129]  F. Bussotti,et al.  Morpho-anatomical aterations in leaves of Gagus vatica L. and Quercus ilex L. in different environmental stress condition , 1998 .

[130]  M. Tretiach,et al.  Photosynthetic activity of Quercus ilex at the extremes of a transect between Mediterranean and submediterranean vegetation (Trieste - NE Italy) , 1997 .

[131]  W. Cramer,et al.  Regional impacts of climatic change on forests in the state of Brandenburg, Germany , 1997 .

[132]  P. Castro-Díez,et al.  Leaf morphology and leaf chemical composition in three Quercus (Fagaceae) species along a rainfall gradient in NE Spain , 1997, Trees.

[133]  L. Gratani,et al.  Phenology and leaf adaptive strategies of Mediterranean maquis plants , 1997 .

[134]  I. C. Prentice,et al.  BIOME3: An equilibrium terrestrial biosphere model based on ecophysiological constraints, resource availability, and competition among plant functional types , 1996 .

[135]  L. Gratani Leaf and shoot growth dynamics of Quercus ilex L. , 1996 .

[136]  S. Rambal,et al.  Optimization of carbon gain in canopies of mediterranean evergreen oaks , 1996 .

[137]  L. Gratani Structural and ecophysiological plasticity of some evergreen species of the mediterranean maquis in response to climate , 1995 .

[138]  S. Sabaté,et al.  Canopy nutrient content of a Quercus ilex L. forest: fertilization and irrigation effects , 1994 .

[139]  J. Tenhunen,et al.  Site-specific water relations and stomatal response of Quercus ilex in a Mediterranean watershed. , 1994, Tree physiology.

[140]  L. Gratani Risposta fotosintetica ed adattamenti morfologici fogliari di alcune specie arbustive sempreverdi, a variazioni microclimatiche , 1994 .

[141]  Seasonal and year to year variation in performance of Gordonia acuminata seedlings in different light environments , 1992 .

[142]  N. Fetcher,et al.  The relationship between treefall gap size and light flux in a Neotropical rain forest in Costa Rica , 1989, Journal of Tropical Ecology.

[143]  L. Gratani,et al.  Variations in leaf characteristics of Quercus ilex L. over a microclimatic gradient , 1988 .

[144]  L. Gratani Variability in chlorophyll content along a gradient in a mediterranean ecosystem , 1985 .

[145]  J. Berry,et al.  Photosynthetic Response and Adaptation to Temperature in Higher Plants , 1980 .

[146]  T. Ingestad,et al.  Nitrogen stress in birch seedlings. II. N, K, P, Ca, and Mg nutrition , 1979 .

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

[148]  J. RUFILANCHAS SALCEDO [Growth and nutrition]. , 1957, Acta pediatrica espanola.