Advertisement

The Leaf Economics Spectrum and its Underlying Physiological and Anatomical Principles

  • Yusuke Onoda
  • Ian J. WrightEmail author
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 44)

Summary

Large variations are found in leaf morphology and physiology across species in nature, reflecting diversity in carbon fixation and growth strategies. These variations in leaf traits are not random; rather, they are tightly coordinated with each other. Leaf traits can be expressed per leaf dry mass or per leaf area. A leaf-mass basis reflects leaf economics, i.e., revenues and expenditures per unit investment of biomass, while a leaf-area basis reflects fluxes in relation to surfaces. Leaf N and P concentrations, and photosynthetic and respiration rates – all considered on a mass basis, are negatively correlated with leaf mass per area (LMA) whilst leaf lifespan is positively correlated with LMA. These correlations are summarized into a single major axis called the “leaf economics spectrum” that runs from “quick-return” to “slow-return” species. On the other hand, correlations among area-based traits are less consistent and less understood in relation to leaf economy. LMA was positively correlated with leaf N content but mostly independent from photosynthetic rates per unit leaf area. Given that N is an essential element in photosynthetic proteins and thus photosynthesis, clarifying the mechanisms why the efficiency of photosynthesis (photosynthesis per unit N) decreases with LMA is a major concern in understanding the correlations among area-based traits in relation to leaf economy. Currently available data suggest that greater amounts of cell wall are required for long-lived leaves, which reduces the efficiency of photosynthesis by lowering (1) the fraction of leaf N invested in photosynthetic proteins and (2) CO2 diffusion rates through thicker and denser mesophyll cell walls. These physiological and structural constraints are a fundamental mechanism underpinning the general correlations among leaf economic traits.

Abbreviations

A

assimilation rate

Aarea

net assimilation rate per unit leaf area

Amass

net assimilation rate per unit leaf dry mass

C

carbon

Ca

ambient CO2 concentration

Cc

chloroplast CO2 concentration

Ci

intercellular CO2 concentration

CWarea

cell wall mass per unit leaf area

CWmass

cell wall mass per unit leaf mass

Dec

deciduous

DM

dry mass

Eve

evergreen

gm

mesophyll conductance for CO2

gs

stomatal conductance for CO2

LES

leaf economics spectrum

LL

leaf lifespan

LMA

leaf mass per area

N

nitrogen

Narea

leaf nitrogen (N) content per unit leaf area

Nmass

leaf N concentration

Np

photosynthetic N content per unit leaf area

NRub

rubisco N content per unit leaf area

P

phosphorus

PNUE

photosynthetic N use efficiency measured at saturating light intensity (=Aarea/Narea)

QR

quantile range

R

respiration rate in the dark

Rarea

dark respiration rate per unit leaf area

Rmass

dark respiration rate per unit leaf dry mass

Rubisco

ribulose bisphosphate carboxylase oxygenase

Sc

surface area of chloroplasts exposed to intercellular airspace per unit leaf area

Sm

surface area of mesophyll exposed to intercellular airspace per unit leaf area

SMA

standardized major axis

TCW

mesophyll cell wall thickness

Notes

Acknowledgments

This study is partly supported by grants from JSPS KAKENHI #26711025 (YO), and from the Australian Research Council (IW).

References

  1. Ackerly D (1999) Self-shading, carbon gain and leaf dynamics: a test of alternative optimality models. Oecologia 119:300–310PubMedCrossRefGoogle Scholar
  2. Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67Google Scholar
  3. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216CrossRefGoogle Scholar
  4. Björkman O (1981) Responses to different quantum flux densities. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Physiological plant ecology I, responses to the physical environment, encyclopedia of plant physiology, vol 12/A. Springer, Berlin, pp 57–107CrossRefGoogle Scholar
  5. Blonder B, Violle C, Bentley LP, Enquist BJ (2011) Venation networks and the origin of the leaf economics spectrum. Ecol Lett 14:91–100PubMedCrossRefGoogle Scholar
  6. Blonder B, Violle C, Enquist BJ (2013) Assessing the causes and scales of the leaf economics spectrum using venation networks in Populus tremuloides. J Ecol 101:981–989CrossRefGoogle Scholar
  7. Blonder B, Vasseur F, Violle C, Shipley B, Enquist BJ, Vile D (2015) Testing models for the leaf economics spectrum with leaf and whole–plant traits in Arabidopsis thaliana. AoB Plants 7:plv049PubMedPubMedCentralCrossRefGoogle Scholar
  8. Carpita NC, McCann MC (2000) The cell wall. In: Buchanan B, Gruissem W, Jones R (eds) Biochemistry & molecular biology of plants. American Society of Plant Physiologists, Rockville, pp 52–108Google Scholar
  9. Chabot BF, Hicks DJ (1982) The ecology of leaf life spans. Annu Rev Ecol Syst 13:229–259CrossRefGoogle Scholar
  10. Chapin FS III (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260CrossRefGoogle Scholar
  11. Chapin FS III, Kedrowski RA (1983) Seasonal changes in nitrogen and phosphorus fractions and autumn retranslocation in evergreen and deciduous taiga trees. Ecology 64:376–391CrossRefGoogle Scholar
  12. Clements ES (1905) The relation of leaf structure to physical factors. Trans Am Microsc Soc 26:19–98CrossRefGoogle Scholar
  13. Cowan IR, Farquhar GD (1977) Stomatal function in relation to leaf metabolism and environment. Symp Soc Exp Biol 31:471–505Google Scholar
  14. Díaz S, Kattge J, Cornelissen JH, Wright IJ, Lavorel S, Dray S, Prentice IC et al (2016) The global spectrum of plant form and function. Nature 529:167–171PubMedCrossRefPubMedCentralGoogle Scholar
  15. Erskine PD, Stewart GR, Schmidt S, Turnbull MH, Unkovich M, Pate JS (1996) Water availability – a physiological constraint on nitrate utilization in plants of Australian semi-arid Mulga woodlands. Plant Cell Environ 19:1149–1159CrossRefGoogle Scholar
  16. Ethier GJ, Livingston NJ (2004) On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar-von Caemmerer-Berry leaf photosynthesis model. Plant Cell Environ 27:137–153CrossRefGoogle Scholar
  17. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19CrossRefGoogle Scholar
  18. Evans JR, Poorter H (2001) Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant Cell Environ 24:755–767CrossRefGoogle Scholar
  19. Evans JR, Seemann JR (1989) The allocation of protein nitrogen in the photosynthetic apparatus: costs, consequences, and control. In: Briggs WR (ed) Photosynthesis. Alan R. Liss, Inc., New York, pp 183–205Google Scholar
  20. Evans JR, Terashima I (1987) Effects of nitrogen nutrition on electron transport components and photosynthesis in spinach. Aust J Plant Physiol 14: 59—68CrossRefGoogle Scholar
  21. Evans JR, Sharkey TD, Berry JA, Farquhar GD (1986) Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants. Funct Plant Biol 13:281–292Google Scholar
  22. Evans JR, von Caemmerer S, Setchell BA, Hudson GS (1994) The relationship between CO2 transfer conductance and leaf anatomy in transgenic tobacco with a reduced content of Rubisco. Funct Plant Biol 21:475–495Google Scholar
  23. Evans JR, Kaldenhoff R, Genty B, Terashima I (2009) Resistances along the CO2 diffusion pathway inside leaves. J Exp Bot 60:2235–2248PubMedCrossRefGoogle Scholar
  24. Field C, Mooney HA (1986) The photosynthesis-nitrogen relationship in wild plants. In: Givnish TJ (ed) On the economy of form and function. Cambridge University Press, Cambridge, pp 25–55Google Scholar
  25. Flexas J, Ribas-Carbó M, Diaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ 31:602–621PubMedPubMedCentralCrossRefGoogle Scholar
  26. Flexas J, Niinemets Ü, Galle A, Barbour MM, Centritto M, Diaz-Espejo A et al (2013) Diffusional conductances to CO2 as a target for increasing photosynthesis and photosynthetic water-use efficiency. Photosynth Res 117:45–59PubMedCrossRefGoogle Scholar
  27. Fry SC (1988) The growing plant cell wall. Longman Scientific & Technical Harlow, EssexGoogle Scholar
  28. Funk JL, Glenwinkel LA, Sack L (2013) Differential allocation to photosynthetic and non-photosynthetic nitrogen fractions among native and invasive species. PLoS One 8:e64502PubMedPubMedCentralCrossRefGoogle Scholar
  29. Givnish TJ (2002) Adaptive significance of evergreen vs. deciduous leaves: solving the triple paradox. Silva Fenn 36:703–743CrossRefGoogle Scholar
  30. Grime JP, Hodgson JG, Hunt R (1988) Comparative plant ecology: a functional approach to common British species. Springer, DordrechtCrossRefGoogle Scholar
  31. Grime JP, Thompson K, Hunt R, Hodgson JG, Cornelissen JHC, Rorison IH et al (1997) Integrated screening validates primary axes of specialisation in plants. Oikos 79(2):259–281CrossRefGoogle Scholar
  32. Grubb PJ (2016) Trade-offs in interspecific comparisons in plant ecology and how plants overcome proposed constraints. Plant Ecol Divers 9:3–33CrossRefGoogle Scholar
  33. Grubb PJ, Grubb EA, Miyata I (1975) Leaf structure and function in evergreen trees and shrubs of Japanese warm temperate rain forest I. The structure of the lamina. Bot Mag (Tokyo) 88:197–211CrossRefGoogle Scholar
  34. Harley PC, Loreto F, Di Marco G, Sharkey TD (1992) Theoretical considerations when estimating the mesophyll conductance to carbon dioxide flux by analysis of the response of photosynthesis to carbon dioxide. Plant Physiol 98:1429–1436PubMedPubMedCentralCrossRefGoogle Scholar
  35. Harrison MT, Edwards EJ, Farquhar GD, Nicotra AB, Evans JR (2009) Nitrogen in cell walls of sclerophyllous leaves accounts for little of the variation in photosynthetic nitrogen-use efficiency. Plant Cell Environ 32:259–270PubMedCrossRefPubMedCentralGoogle Scholar
  36. Held MA, Jiang N, Basu D, Showalter AM, Faik A (2015) Plant cell wall polysaccharides: structure and biosynthesis. In: Ramawat KG, Mérillon J-M (eds) Polysaccharides: bioactivity and biotechnology. Springer, Cham, pp 3–54CrossRefGoogle Scholar
  37. Hikosaka K (2004) Interspecific difference in the photosynthesis-nitrogen relationship: patterns, physiological causes, and ecological importance. J Plant Res 117:481–494PubMedCrossRefPubMedCentralGoogle Scholar
  38. Hikosaka K, Shigeno A (2009) The role of Rubisco and cell walls in the interspecific variation in photosynthetic capacity. Oecologia 160:443–451PubMedCrossRefPubMedCentralGoogle Scholar
  39. Hikosaka K, Terashima I (1995) A model of the acclimation of photosynthesis in the leaves of C-3 plants to sun and shade with respect to nitrogen use. Plant Cell Environ 18:605–618CrossRefGoogle Scholar
  40. Hikosaka K, Hanba YT, Hirose T, Terashima I (1998) Photosynthetic nitrogen-use efficiency in leaves of woody and herbaceous species. Funct Ecol 12:896–905CrossRefGoogle Scholar
  41. Kattge J, Díaz S, Lavorel S, Prentice IC, Leadley P, Bönisch G et al (2011) TRY – a global database of plant traits. Glob Chang Biol 17:2905–2935PubMedCentralCrossRefGoogle Scholar
  42. Kieliszewski MJ, Lamport DTA, Tan L, Cannon MC (2010) Hydroxyproline-rich glycoproteins: form and function. In: Ulvskov P (ed) Annual plant reviews: plant polysaccharides, biosynthesis and bioengineering. Wiley-Blackwell, Oxford, pp 321–342CrossRefGoogle Scholar
  43. Kikuzawa K (1991) A cost-benefit analysis of leaf habit and leaf longevity of trees and their geographical pattern. Am Nat 138:1250–1263CrossRefGoogle Scholar
  44. Kimmerer TW, Potter DA (1987) Nutritional quality of specific leaf tissues and selective feeding by a specialist leafminer. Oecologia 71:548–551PubMedCrossRefPubMedCentralGoogle Scholar
  45. Lambers H, Poorter H (1992) Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Adv Ecol Res 23:187–261CrossRefGoogle Scholar
  46. Lamport DTA (1965) The protein component of primary cell walls. Adv Bot Res 2:151–218CrossRefGoogle Scholar
  47. Maire V, Wright IJ, Prentice IC, Batjes NH, Bhaskar R, Bodegom PM et al (2015) Global effects of soil and climate on leaf photosynthetic traits and rates. Glob Ecol Biogeogr 24:706–717CrossRefGoogle Scholar
  48. Makino A, Osmond B (1991) Solubilization of ribulose-1 5-bisphosphate carboxylase from the membrane fraction of pea leaves. Photosynth Res 29:79–86PubMedCrossRefPubMedCentralGoogle Scholar
  49. Makino A, Mae T, Ohira K (1986) Colorimetric measurement of protein stained with Coomassie brilliant blue R on sodium dodecyl sulfate-polyacrylamide gel electrophoresis by eluting with formamide. Agric Biol Chem 50:1911–1912Google Scholar
  50. Mason CM, Goolsby EW, Humphreys DP, Donovan LA (2016) Phylogenetic structural equation modelling reveals no need for an ‘origin’ of the leaf economics spectrum. Ecology Letters 19:54–61PubMedCrossRefPubMedCentralGoogle Scholar
  51. Medlyn BE, Duursma RA, Eamus D, Ellsworth DS, Prentice IC, Barton CV et al (2011) Reconciling the optimal and empirical approaches to modelling stomatal conductance. Glob Chang Biol 17:2134–2144CrossRefGoogle Scholar
  52. Merino J, Field C, Mooney HA (1984) Construction and maintenance costs of Mediterranean evergreen and deciduous leaves. Acta Oecol 5:211–219Google Scholar
  53. Miller RE, Woodrow IE (2008) Resource availability and the abundance of an N-based defense in Australian tropical rain forests. Ecology 89:1503–1509PubMedCrossRefPubMedCentralGoogle Scholar
  54. Moorcroft PR, Hurtt G, Pacala SW (2001) A method for scaling vegetation dynamics: the ecosystem demography model (ED). Ecol Monogr 71:557–586CrossRefGoogle Scholar
  55. Moss RA, Loomis WE (1952) Absorption spectra of leaves. I. The visible spectrum. Plant Physiol 27:370–391PubMedPubMedCentralCrossRefGoogle Scholar
  56. Niinemets Ü (2001) Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82:453–469CrossRefGoogle Scholar
  57. Niinemets Ü, Reichstein M (2003) Controls on the emission of plant volatiles through stomata: differential sensitivity of emission rates to stomatal closure explained. J Geophys Res Atmos 108:4208CrossRefGoogle Scholar
  58. Niinemets Ü, Wright IJ, Evans JR (2009) Leaf mesophyll diffusion conductance in 35 Australian sclerophylls covering a broad range of foliage structural and physiological variation. J Exp Bot 60:2433–2449PubMedCrossRefPubMedCentralGoogle Scholar
  59. Niklas KJ, Cobb ED, Niinemets Ü, Reich PB, Sellin A, Shipley B, Wright IJ (2007) “Diminishing returns” in the scaling of functional leaf traits across and within species groups. Proc Natl Acad Sci U S A 104:8891–8896PubMedPubMedCentralCrossRefGoogle Scholar
  60. Nobel PS, Zaragoza LJ, Smith WK (1975) Relation between mesophyll surface area, photosynthetic rate, and illumination level during development for leaves of Plectranthus parviflorus Henckel. Plant Physiol 55:1067–1070PubMedPubMedCentralCrossRefGoogle Scholar
  61. Oguchi R, Hikosaka K, Hirose T (2003) Does the photosynthetic light-acclimation need change in leaf anatomy? Plant Cell Environ 26:505–512CrossRefGoogle Scholar
  62. Onoda Y, Hikosaka K, Hirose T (2004) Allocation of nitrogen to cell walls decreases photosynthetic nitrogen-use efficiency. Funct Ecol 18:419–425CrossRefGoogle Scholar
  63. Onoda Y, Westoby M, Adler PB, Choong AMF, Clissold FJ, Cornelissen JHC et al (2011) Global patterns of leaf mechanical properties. Ecol Lett 14:301–312PubMedCrossRefPubMedCentralGoogle Scholar
  64. Onoda Y, Wright IJ, Evans JR, Hikosaka K, Kitajima K, Niinemets Ü et al (2017) Physiological and structural tradeoffs underlying the leaf economics spectrum. New Phytol 214:1447–1463PubMedCrossRefPubMedCentralGoogle Scholar
  65. Osnas JL, Lichstein JW, Reich PB, Pacala SW (2013) Global leaf trait relationships: mass, area, and the leaf economics spectrum. Science 340:741–744PubMedCrossRefGoogle Scholar
  66. Peterson AG (1999) Reconciling the apparent difference between mass- and area-based expressions of the photosynthesis-nitrogen relationship. Oecologia 118:144–150PubMedCrossRefPubMedCentralGoogle Scholar
  67. Poorter H, Evans JR (1998) Photosynthetic nitrogen-use efficiency of species that differ inherently in specific leaf area. Oecologia 116:26–37PubMedCrossRefPubMedCentralGoogle Scholar
  68. Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588PubMedPubMedCentralCrossRefGoogle Scholar
  69. Read J, Sanson GD (2003) Characterizing sclerophylly: the mechanical properties of a diverse range of leaf types. New Phytol 160:81–99CrossRefGoogle Scholar
  70. Reich PB (2014) The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. J Ecol 102:275–301CrossRefGoogle Scholar
  71. Reich PB, Uhl C, Walters MB, Ellsworth DS (1991) Leaf lifespan as a determinant of leaf structure and function among 23 Amazonian tree species. Oecologia 86:16–24PubMedCrossRefPubMedCentralGoogle Scholar
  72. Reich PB, Walters MB, Ellsworth DS (1992) Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecol Monogr 62:365–392CrossRefGoogle Scholar
  73. Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proc Natl Acad Sci U S A 94:13730–13734PubMedPubMedCentralCrossRefGoogle Scholar
  74. Reich PB, Ellsworth DS, Walters MB (1998a) Leaf structure (specific leaf area) modulates photosynthesis-nitrogen relations: evidence from within and across species and functional groups. Funct Ecol 12:948–958CrossRefGoogle Scholar
  75. Reich PB, Walters MB, Ellsworth DS, Vose JM, Volin JC, Gresham C, Bowman WD (1998b) Relationships of leaf dark respiration to leaf nitrogen, specific leaf area and leaf life-span: a test across biomes and functional groups. Oecologia 114:471–482PubMedCrossRefPubMedCentralGoogle Scholar
  76. Reich PB, Wright IJ, Cavender-Bares J, Craine JM, Oleksyn J, Westoby M, Walters MB (2003) The evolution of plant functional variation: traits, spectra, and strategies. Int J Plant Sci 164:S143–S164CrossRefGoogle Scholar
  77. Reu B, Proulx R, Bohn K, Dyke JG, Kleidon A, Pavlick R, Schmidtlein S (2011) The role of climate and plant functional trade-offs in shaping global biome and biodiversity patterns. Glob Ecol Biogeogr 20:570–581CrossRefGoogle Scholar
  78. Sack L, Scoffoni C, John GP, Poorter H, Mason CM, Mendez-Alonzo R, Donovan LA (2013) How do leaf veins influence the worldwide leaf economic spectrum? Review and synthesis. J Exp Bot 64:4053–4080PubMedCrossRefGoogle Scholar
  79. Sage RF, Pearcy RW (1987) The nitrogen use efficiency of C3 and C4 plants. I. Leaf nitrogen growth and biomass partitioning in Chenopodium album (L.) and Amaranthus retroflexus (L.). Plant Physiol 84:954–958PubMedPubMedCentralCrossRefGoogle Scholar
  80. Schimper AFW (1903) Plant-geography upon a physiological basis. Clarendon Press, OxfordCrossRefGoogle Scholar
  81. Schulze E-D, Kelliher FM, Körner C, Lloyd J, Leuning R (1994) Relationships among maximum stomatal conductance, ecosystem surface conductance, carbon assimilation rate, and plant nitrogen nutrition: a global ecology scaling exercise. Annu Rev Ecol Syst 25:629–660CrossRefGoogle Scholar
  82. Shields LM (1950) Leaf xeromorphy as related to physiological and structural influences. Bot Rev 16:399–447CrossRefGoogle Scholar
  83. Shipley B, Lechowicz MJ, Wright IJ, Reich PB (2006) Fundamental trade-offs generating the worldwide leaf economics spectrum. Ecology 87:535–541PubMedCrossRefGoogle Scholar
  84. Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5:9–23PubMedPubMedCentralCrossRefGoogle Scholar
  85. Sinclair RJ, Hughes L (2010) Leaf miners: the hidden herbivores. Austral Ecol 35:300–313CrossRefGoogle Scholar
  86. Syvertsen JP, Lloyd J, McConchie C, Kriedemann PE, Farquhar GD (1995) On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves. Plant Cell Environ 18:149–157CrossRefGoogle Scholar
  87. Takashima T, Hikosaka K, Hirose T (2004) Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant Cell Environ 27:1047–1054CrossRefGoogle Scholar
  88. Terashima I, Miyazawa SI, Hanba YT (2001) Why are sun leaves thicker than shade leaves? Consideration based on analyses of CO2 diffusion in the leaf. J Plant Res 114:93–105CrossRefGoogle Scholar
  89. Terashima I, Hanba YT, Tazoe Y, Vyas P, Yano S (2006) Irradiance and phenotype: comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion. J Exp Bot 57:343–354PubMedCrossRefPubMedCentralGoogle Scholar
  90. Terashima I, Hanba YT, Tholen D, Niinemets Ü (2011) Leaf functional anatomy in relation to photosynthesis. Plant Physiol 155:108–116PubMedCrossRefPubMedCentralGoogle Scholar
  91. Tosens T, Niinemets Ü, Westoby M, Wright IJ (2012) Anatomical basis of variation in mesophyll resistance in eastern Australian sclerophylls: news of a long and winding path. J Exp Bot 63:5105–5119PubMedPubMedCentralCrossRefGoogle Scholar
  92. Tosens T, Nishida K, Gago J, Coopman RE, Cabrera HM, Carriquí M et al (2016) The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO2 diffusion as a key trait. New Phytol 209:1576–1590PubMedCrossRefPubMedCentralGoogle Scholar
  93. Van Soest PJ (1994) Nutritional ecology of the ruminant. Comstock Publishing, IthacaGoogle Scholar
  94. Wang YP, Lu XJ, Wright IJ, Dai YJ, Rayner PJ, Reich PB (2012) Correlations among leaf traits provide a significant constraint on the estimate of global gross primary production. Geophys Res Lett 39:L19405Google Scholar
  95. Warming E (1909) Oecology of plants. Clarendon Press, OxfordGoogle Scholar
  96. Warren CR (2008) Stand aside stomata, another actor deserves centre stage: the forgotten role of the internal conductance to CO2 transfer. J Exp Bot 59:1475–1487CrossRefGoogle Scholar
  97. Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Bio Rev 81:259–291CrossRefGoogle Scholar
  98. Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Annu Rev Ecol Syst 33:125–159CrossRefGoogle Scholar
  99. Wong SC, Cowan IR, Farquhar GD (1979) Stomatal conductance correlates with photosynthetic capacity. Nature 282:424–426CrossRefGoogle Scholar
  100. Wright IJ, Westoby M (2002) Leaves at low versus high rainfall: coordination of structure, lifespan and physiology. New Phytol 155:403–416CrossRefGoogle Scholar
  101. Wright IJ, Reich PB, Westoby M (2003) Least-cost input mixtures of water and nitrogen for photosynthesis. Am Nat 161:98–111PubMedGoogle Scholar
  102. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827PubMedCrossRefPubMedCentralGoogle Scholar
  103. Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Garnier E, Hikosaka K et al (2005) Assessing the generality of global leaf trait relationships. New Phytol 166:485–496PubMedCrossRefPubMedCentralGoogle Scholar
  104. Wright IJ, Dong N, Maire V, Prentice IC, Westoby M, Díaz S et al (2017) Global climatic drivers of leaf size. Science 357:917–921PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Division of Environmental Science and Technology, Graduate School of AgricultureKyoto UniversityOiwake, KitashirakawaJapan
  2. 2.Department of Biological Sciences, Faculty of ScienceMacquarie UniversitySydneyAustralia

Personalised recommendations