How do leaf veins influence the worldwide leaf economic spectrum? Review and synthesis

Journal of Experimental Botany

Volumn 64, Issue 13, 2013, Pages 4053-4080

  Sack, Lawren ^a   Scoffoni, Christine ^a   John, Grace P ^a   Poorter, Hendrik ^b   Mason, Chase M ^c   Mendez Alonzo, Rodrigo ^a   Donovan, Lisa A ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

Drought tolerance; functional traits; leaf hydraulics; leaf mass per area; leaf nutrient concentrations; photosynthetic rate; vasculature; vein patterning.

Indexed keywords

BIOLOGICAL MODEL; BIOMASS; CELL RESPIRATION; DROUGHT; DROUGHT TOLERANCE; EVAPOTRANSPIRATION; FUNCTIONAL TRAITS; GENETICS; HISTOLOGY; LEAF HYDRAULICS; LEAF MASS PER AREA; LEAF NUTRIENT CONCENTRATIONS; LIGHT; PHENOTYPE; PHOTOSYNTHESIS; PHOTOSYNTHETIC RATE; PHYSIOLOGY; PLANT; PLANT LEAF; PLANT STOMA; QUANTITATIVE TRAIT LOCUS; RADIATION EXPOSURE; REVIEW; VASCULAR BUNDLE (PLANT); VASCULARIZATION; VEIN PATTERNING.;

DROUGHT TOLERANCE; FUNCTIONAL TRAITS; LEAF HYDRAULICS; LEAF MASS PER AREA; LEAF NUTRIENT CONCENTRATIONS; PHOTOSYNTHETIC RATE; VASCULATURE; VEIN PATTERNING.;

BIOMASS; CELL RESPIRATION; DROUGHTS; LIGHT; MODELS, BIOLOGICAL; PHENOTYPE; PHOTOSYNTHESIS; PLANT LEAVES; PLANT STOMATA; PLANT TRANSPIRATION; PLANT VASCULAR BUNDLE; PLANTS; QUANTITATIVE TRAIT LOCI;

EID: 84885360288     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert316     Document Type: Review

References (134)

1. Aasamaa K, Sober A, Rahi M. 2001. Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. Australian Journal of Plant Physiology 28, 765-774.
2. Ackerly DD, Reich PB. 1999. Convergence and correlations among leaf size and function in seed plants: a comparative test using independent contrasts. American Journal of Botany 86, 1272-1281.
3. Arcand N, Kagawa AK, Sack L, Giambelluca TW. 2008. Scaling of frond form in Hawaiian tree fern Cibotium glaucum: compliance with global trends and application for field estimation. Biotropica 40, 686-691.
4. Beerling DJ, Franks PJ. 2010. Plant science: the hidden cost of transpiration. Nature 464, 495-496.
5. Blonder B, Violle C, Bentley LP, Enquist BJ. 2011. Venation networks and the origin of the leaf economics spectrum. Ecology Letters 14, 91-100.
6. Blonder B, Violle C, Enquist BJ. 2013. Assessing the causes and scales of the leaf economics spectrum using venation networks in Populus tremuloides. Journal of Ecology 101, 981-989.
7. Boyce CK, Brodribb TJ, Feild TS, Zwieniecki MA. 2009. Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proceedings of the Royal Society B 276, 1771-1776.
8. Boyce CK, Zwieniecki MA. 2012. Leaf fossil record suggests limited influence of atmospheric CO2 on terrestrial productivity prior to angiosperm evolution. Proceedings of the National Academy of Sciences, USA 109, 10403-10408.
9. Brodribb TJ, Feild TS. 2010. Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecology Letters 13, 175-183.
10. Brodribb TJ, Feild TS, Jordan GJ. 2007. Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology 144, 1890-1898.
11. Brodribb TJ, Feild TS, Sack L. 2010. Viewing leaf structure and evolution from a hydraulic perspective. Functional Plant Biology 37, 488-498.
12. Brodribb TJ, Jordan GJ. 2011. Water supply and demand remain balanced during leaf acclimation of Nothofagus cunninghamii trees. New Phytologist 192, 437-448.
13. Brodribb TJ, Jordan GJ, Carpenter RJ. 2013. Unified changes in cell size permit coordinated leaf evolution. New Phytologist 199, 559-570.
14. Buckley TN, Mott KA, Farquhar GD. 2003. A hydromechanical and biochemical model of stomatal conductance. Plant, Cell and Environment 26, 1767-1785.
15. Buckley TN, Sack L, Gilbert ME. 2011. The role of bundle sheath extensions and life form in stomatal responses to leaf water status. Plant Physiology 156, 962-973.
16. Castro-Diez P, Puyravaud JP, Cornelissen JHC. 2000. Leaf structure and anatomy as related to leaf mass per area variation in seedlings of a wide range of woody plant species and types. Oecologia 124, 476-486.
17. Cochard H, Nardini A, Coll L. 2004. Hydraulic architecture of leaf blades: where is the main resistance? Plant, Cell and Environment 27, 1257-1267.
18. Coomes DA, Sack L. 2009. Response to comment on Coomes et al. 'Scaling of xylem vessels and veins within the leaves of oak species'. Biology Letters 5, 381-382.
19. Cornelissen JHC, Lavorel S, Garnier E, et al. 2003. A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Australian Journal of Botany 51, 335-380.
20. Cowan IR. 1972. Electrical analog of evaporation from, and flow of water in plants. Planta 106, 221-226.
21. Cramer MD, Hawkins H-J, Verboom GA. 2009. The importance of nutritional regulation of plant water flux. Oecologia 161, 15-24.
22. Cramer MD, Hoffmann V, Verboom GA. 2008. Nutrient availability moderates transpiration in Ehrharta calycina. New Phytologist 179, 1048-1057.
23. de Boer HJ, Eppinga MB, Wassen MJ, Dekker SC. 2012. A critical transition in leaf evolution facilitated the Cretaceous angiosperm revolution. Nature Communications 3, 1221.
24. Diaz S, Hodgson JG, Thompson K, et al. 2004. The plant traits that drive ecosystems: evidence from three continents. Journal of Vegetation Science 15, 295-304.
25. Donovan LA, Maherali H, Caruso CM, Huber H, de Kroon H. 2011. The evolution of the worldwide leaf economics spectrum. Trends in Ecology and Evolution 26, 88-95.
26. Dunbar-Co S, Sporck MJ, Sack L. 2009. Leaf trait diversification and design in seven rare taxa of the Hawaiian Plantago radiation. International Journal of Plant Sciences 170, 61-75.
27. Edwards EJ. 2006. Correlated evolution of stem and leaf hydraulic traits in Pereskia (Cactaceae). New Phytologist 172, 479-489.
28. Ehleringer JR, Clark C. 1988. Evolution and adaptation in Encelia (Asteraceae) In: LD Gottlieb, SK Jain, eds, Plant evolutionary biology. New York: Chapman and Hall. pp. 221-248.
29. Evans GC. 1972. The quantitative analysis of plant growth. Oxford: Blackwell.
30. Evans JR, Schortemeyer M, McFarlane N, Atkin OK. 2000. Photosynthetic characteristics of ten Acacia species grown under ambient and elevated atmospheric CO2. Australian Journal of Plant Physiology 27, 13-25.
31. Farquhar GD, von Caemmerer S, Berry JA. 2001. Models of photosynthesis. Plant Physiology 125, 42-45.
32. Feild TS, Arens NC, Doyle JA, Dawson TE, Donoghue MJ. 2004. Dark and disturbed: a new image of early angiosperm ecology. Paleobiology 30, 82-107.
33. Feild TS, Brodribb TJ, Iglesias A, Chatelet DS, Baresch A, Upchurch GR, Gomez B, Mohr BAR, Coiffard C, Kvacek J, Jaramillo C. 2011a. Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution. Proceedings of the National Academy of Sciences, USA 108, 8363-8366.
34. Feild TS, Chatelet DS, Brodribb TJ. 2009. Ancestral xerophobia: a hypothesis on the whole plant ecophysiology of early angiosperms. Geobiology 7, 237-264.
35. Feild TS, Upchurch GR Jr, Chatelet DS, Brodribb TJ, Grubbs KC, Samain M-S, Wanke S. 2011b. Fossil evidence for low gas exchange capacities for Early Cretaceous angiosperm leaves. Paleobiology 37, 195-213.
36. Ferrio JP, Pou A, Florez-Sarasa I, Gessler A, Kodama N, Flexas J, Ribas-Carbo M. 2012. The Peclet effect on leaf water enrichment correlates with leaf hydraulic conductance and mesophyll conductance for CO2. Plant, Cell and Environment 35, 611-625.
37. Field CB, Mooney HA. 1986. The photosynthesis-nitrogen relationship in wild plants. In: TJ Givnish, ed, On the economy of plant form and function . Cambridge, UK: Cambridge University Press. pp. 25-55.
38. Flexas J, Barbour MM, Brendel O, et al. 2012. Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. Plant Science 193, 70-84.
39. Flexas J, Scoffoni C, Gago J, Sack L. 2013. Leaf mesophyll conductance and leaf hydraulic conductance: an introduction to their measurement and coordination. Journal of Experimental Botany 64, 3965-3981.
40. Franks PJ. 2004. Stomatal control and hydraulic conductance, with special reference to tall trees. Tree Physiology 24, 865-878.
41. Franks PJ, Farquhar GD. 2007. The mechanical diversity of stomata and its significance in gas exchange control. Plant Physiology 143, 78-87.
42. Fu Q, Cheng L, Guo Y, Turgeon R. 2011. Phloem loading strategies and water relations in trees and herbaceous plants. Plant Physiology 157, 1518-1527.
43. Garnier E, Laurent G. 1994. Leaf anatomy, specific mass and water content in congeneric annual and perennial grass species. New Phytologist 128, 725-736.
44. Gilliham M, Dayod M, Hocking BJ, Xu B, Conn SJ, Kaiser BN, Leigh RA, Tyerman SD. 2011. Calcium delivery and storage in plant leaves: exploring the link with water flow. Journal of Experimental Botany 62, 2233-2250.
45. Girardin P, Tollenaar M, Muldoon JF. 1985. Effect of temporary N starvation on leaf photosynthetic rate and chlorophyll content of maize. Canadian Journal of Plant Science 65, 491-500.
46. Givnish TJ. 1987. Comparative studies of leaf form: assessing the relative roles of selective pressures and phylogenetic constraints. New Phytologist 106 (Suppl), 131-160.
47. Givnish TJ, Pires JC, Graham SW, et al. 2005. Repeated evolution of net venation and fleshy fruits among monocots in shaded habitats confirms a priori predictions: evidence from an ndhF phylogeny. Proceedings of the Royal Society B 272, 1481-1490.
48. Grubb PJ. 1998. A reassessment of the strategies of plants which cope with shortages of resources. Perspectives in Plant Ecology, Evolution and Systematics 1, 3-31.
49. Guyot G, Scoffoni C, Sack L. 2012. Combined impacts of irradiance and dehydration on leaf hydraulic conductance: insights into vulnerability and stomatal control. Plant, Cell and Environment 35, 857-871.
50. Hao GY, Sack L, Wang AY, Cao KF, Goldstein G. 2010. Differentiation of leaf water flux and drought tolerance traits in hemiepiphytic and non-hemiepiphytic Ficus tree species. Functional Ecology 24, 731-740.
51. Heberling JM, Fridley JD. 2012. Biogeographic constraints on the world-wide leaf economics spectrum. Global Ecology and Biogeography 21, 1137-1146.
52. Hubbard RM, Ryan MG, Stiller V, Sperry JS. 2001. Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine. Plant, Cell and Environment 24, 113-121.
53. Jasienski M, Bazzaz FA. 1999. The fallacy of ratios and the testability of models in biology. Oikos 84, 321-326.
54. John GP, Scoffoni C, Sack L. 2013. Allometry of cells and tissues within leaves. American Journal of Botany.
55. Jordan GJ. 2011. A critical framework for the assessment of biological palaeoproxies: predicting past climate and levels of atmospheric CO2 from fossil leaves. New Phytologist 192, 29-44.
56. Kattge J, Diaz S, Lavorel S, et al. 2011. TRY- A global database of plant traits. Global Change Biology 17, 2905-2935.
57. Kerton M, Newbury HJ, Hand D, Pritchard J. 2009. Accumulation of calcium in the centre of leaves of coriander (Coriandrum sativum L.) is due to an uncoupling of water and ion transport. Journal of Experimental Botany 60, 227-235.
58. Lambers H, Poorter H. 1992. Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Advances in Ecological Research 23, 187-261.
59. Lloyd J, Bloomfield K, Deomingues TF, Farquhar GD. 2013. Photosynthetically relevant foliar traits correlating better on a mass vs an area basis: of ecophysiological relevance or just a case of mathematical imperatives and statistical quicksand? New Phytologist 199, 311-321.
60. Manuel Perez-Perez J, Rubio-Diaz S, Dhondt S, Hernandez-Romero D, Sanchez-Soriano J, Beemster GTS, Rosa Ponce M, Micol JL. 2011. Whole organ, venation and epidermal cell morphological variations are correlated in the leaves of Arabidopsis mutants. Plant, Cell and Environment 34, 2200-2211.
61. Mason CM, McGaughey SE, Donovan LA. 2013. Ontogeny strongly and differentially alters leaf economic and other key traits in three diverse Helianthus species. Journal of Experimental Botany 64, 4091-4101.
62. McGill BJ, Enquist BJ, Weiher E, Westoby M. 2006. Rebuilding community ecology from functional traits. Trends in Ecology and Evolution 21, 178-185.
63. McKown AD, Cochard H, Sack L. 2010. Decoding leaf hydraulics with a spatially explicit model: principles of venation architecture and implications for its evolution. American Naturalist 175, 447-460.
64. Meidner H. 1983. Our understanding of plant water relations. Journal of Experimental Botany 34, 1606-1618.
65. Méndez-Alonzo R, Ewers FW, Sack L. 2013. Ecological variation in leaf biomechanics and its scaling with tissue structure across three mediterranean-climate plant communities Functional Ecology 27, 544-554.
66. Milla R, Reich PB. 2007. The scaling of leaf area and mass: the cost of light interception increases with leaf size. Proceedings of the Royal Society B 274, 2109-2114.
67. Murphy MRC, Jordan GJ, Brodribb TJ. 2012. Differential leaf expansion can enable hydraulic acclimation to sun and shade. Plant, Cell and Environment 35, 1407-1418.
68. Nardini A, Peda G, La Rocca N. 2012. Trade-offs between leaf hydraulic capacity and drought vulnerability: morpho-anatomical bases, carbon costs and ecological consequences. New Phytologist 196, 788-798.
69. Nee S, Colegrave N, West SA, Grafen A. 2005. The illusion of invariant quantities in life histories. Science 309, 1236-1239.
70. Niinemets Ü. 1999a. Components of leaf dry mass per area-thickness and density-alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytologist 144, 35-47.
71. Niinemets Ü. 1999b. Research review. Components of leaf dry mass per area-thickness and density-alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytologist 144, 35-47.
72. Niinemets Ü, Kull O, Tenhunen JD. 2004. Within-canopy variation in the rate of development of photosynthetic capacity is proportional to integrated quantum flux density in temperate deciduous trees. Plant, Cell and Environment 27, 293-313.
73. Niinemets Ü, Portsmuth A, Tena D, Tobias M, Matesanz S, Valladares F. 2007a. Do we underestimate the importance of leaf size in plant economics? Disproportional scaling of support costs within the spectrum of leaf physiognomy. Annals of Botany 100, 283-303.
74. Niinemets Ü, Portsmuth A, Tobias M. 2007b. Leaf shape and venation pattern alter the support investments within leaf lamina in temperate species: a neglected source of leaf physiological differentiation? Functional Ecology 21, 28-40.
75. Niinemets Ü, Sack L. 2006. Structural determinants of leaf light harvesting capacity and photosynthetic potentials. Progress in Botany 67, 385-419.
76. Nikinmaa E, Holtta T, Hari P, Kolari P, Makela A, Sevanto S, Vesala T. 2013. Assimilate transport in phloem sets conditions for leaf gas exchange. Plant, Cell and Environment 36, 655-669.
77. Niklas KJ, Cobb ED, Niinemets U, Reich PB, Sellin A, Shipley B, Wright IJ. 2007. 'Diminishing returns' in the scaling of functional leaf traits across and within species groups. Proceedings of the National Academy of Sciences, USA 104, 8891-8896.
78. Noblin X, Mahadevan L, Coomaraswamy IA, Weitz DA, Holbrook NM, Zwieniecki MA. 2008. Optimal vein density in artificial and real leaves. Proceedings of the National Academy of Sciences, USA 105, 9140-9144.
79. Onoda Y, Westoby M, Adler PB, et al. 2011. Global patterns of leaf mechanical properties. Ecology Letters 14, 301-312.
80. Osnas JLD, Lichstein JW, Reich PB, Pacala SW. 2013. Global leaf trait relationships: mass, area, and the leaf economics spectrum. Science 340, 741-744.
81. Peak D, Mott KA. 2011. A new, vapour-phase mechanism for stomatal responses to humidity and temperature. Plant, Cell and Environment 34, 162-178.
82. Peppe DJ, Royer DL, Cariglino B, et al. 2011. Sensitivity of leaf size and shape to climate: global patterns and paleoclimatic applications. New Phytologist 190, 724-739.
83. Perez-Harguindeguy N, Diaz S, Garnier E, et al. 2013. New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 61, 167-234.
84. Philpott J. 1953. A blade tissue study of leaves of 47 species of Ficus. Botanical Gazette 115, 15-35.
85. Philpott J. 1956. Blade tissue organization of foliage leaves of some Carolina shrub-bog species as compared with their Appalachian mountain affinities. Botanical Gazette 118, 88-105.
86. Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R. 2009. Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist 182, 565-588.
87. Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L. 2012. Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytologist 193, 30-50.
88. Price CA, Enquist BJ. 2007. Scaling mass and morphology in leaves: an extension of the WBE model. Ecology 88, 1132-1141.
89. Pyankov VI, Kondratchuk AV, Shipley B. 1999. Leaf structure and specific leaf mass: the alpine desert plants of the Eastern Pamirs, Tadjikistan. New Phytologist 143, 131-142.
90. Quero JL, Villar R, Maranon T, Zamora R. 2006. Interactions of drought and shade effects on seedlings of four Quercus species: physiological and structural leaf responses. New Phytologist 170, 819-833.
91. Reich PB, Walters MB, Ellsworth DS. 1997. From tropics to tundra: global convergence in plant functioning. Proceedings of the National Academy of Sciences, USA 94, 13730-13734.
92. Reich PB, Wright IJ, Lusk CH. 2007. Predicting leaf physiology from simple plant and climate attributes: a global GLOPNET analysis. Ecological Applications 17, 1982-1988.
93. Roderick ML, Berry SL, Noble IR, Farquhar GD. 1999. A theoretical approach to linking the composition and morphology with the function of leaves. Functional Ecology 13, 683-695.
94. Royer DL, Miller IM, Peppe DJ, Hickey LJ. 2010. Leaf economic traits from fossils support a weedy habit for early angiosperms. American Journal of Botany 97, 438-445.
95. Sack L, Cowan PD, Jaikumar N, Holbrook NM. 2003. The 'hydrology' of leaves: co-ordination of structure and function in temperate woody species. Plant, Cell and Environment 26, 1343-1356.
96. Sack L, Dietrich EM, Streeter CM, Sanchez-Gomez D, Holbrook NM. 2008. Leaf palmate venation and vascular redundancy confer tolerance of hydraulic disruption. Proceedings of the National Academy of Sciences, USA 105, 1567-1572.
97. Sack L, Frole K. 2006. Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees. Ecology 87, 483-491.
98. Sack L, Holbrook NM. 2006. Leaf hydraulics. Annual Review of Plant Biology 57, 361-381.
99. Sack L, Scoffoni C. 2013. Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New Phytologist 198, 983-1000.
100. Sack L, Scoffoni C, McKown AD, Frole K, Rawls M, Havran JC, Tran H, Tran T. 2012. Developmentally based scaling of leaf venation architecture explains global ecological patterns. Nature Communications 3, 837.
101. Sack L, Streeter CM, Holbrook NM. 2004. Hydraulic analysis of water flow through leaves of sugar maple and red oak. Plant Physiology 134, 1824-1833.
102. Sack L, Tyree MT. 2005. Leaf hydraulics and its implications in plant structure and function. In: NM Holbrook, MA Zweiniecki, eds, Vascular transport in plants. Oxford: Elsevier/Academic Press.
103. Sack L, Tyree MT, Holbrook NM. 2005. Leaf hydraulic architecture correlates with regeneration irradiance in tropical rainforest trees. New Phytologist 167, 403-413.
104. Saltelli A, Chan K, Scott EM. 2009. Sensitivity analysis . New York: Wiley.
105. Scoffoni C, McKown AD, Rawls M, Sack L. 2012. Dynamics of leaf hydraulic conductance with water status: quantification and analysis of species differences under steady-state. Journal of Experimental Botany 63, 643-658.
106. Scoffoni C, Rawls M, McKown A, Cochard H, Sack L. 2011. Decline of leaf hydraulic conductance with dehydration: relationship to leaf size and venation architecture. Plant Physiology 156, 832-843.
107. Shabala S, Schimanski LJ, Koutoulis A. 2002. Heterogeneity in bean leaf mesophyll tissue and ion flux profiles: leaf electrophysiological characteristics correlate with the anatomical structure. Annals of Botany 89, 221-226.
108. Sheriff DW. 1977. Evaporation sites and distillation in leaves. Annals of Botany 41, 1081.
109. Shipley B, Lechoweicz MJ, Wright I, Reich PB. 2006. Fundamental trade-offs generating the worldwide leaf economics spectrum. Ecology 87, 535-541.
110. Simonin KA, Limm EB, Dawson TE. 2012. Hydraulic conductance of leaves correlates with leaf lifespan: implications for lifetime carbon gain. New Phytologist 193, 939-947.
111. Small E. 1972. Photosynthetic rates in relation to nitrogen recycling as an adaptation to nutrient deficiency in peat bog plants. Canadian Journal of Botany 50, 2227-2233.
112. Sommerville KE, Sack L, Ball MC. 2012. Hydraulic conductance of Acacia phyllodes (foliage) is driven by primary nerve (vein) conductance and density. Plant, Cell and Environment 35, 158-168.
113. RDC Team. 2007. R: a language and environment for statistical computing . Vienna, Austria: R Foundation for Statistical Computing.
114. Tyree MT, Zimmermann MH. 2002. Xylem structure and the ascent of sap. Berlin: Springer.
115. Uhl D, Mosbrugger V. 1999. Leaf venation density as a climate and environmental proxy: a critical review and new data. Palaeogeography Palaeoclimatology Palaeoecology 149, 15-26.
116. Van Arendonk JJCM, Poorter H. 1994. The chemical composition and anatomical structure of leaves of grass species differing in relative growth rate. Plant, Cell and Environment 17, 963-970.
117. Villar R, Maranon T, Quero JL, Panadero P, Arenas F, Lambers H. 2005. Variation in relative growth rate of 20 Aegilops species (Poaceae) in the field: the importance of net assimilation rate or specific leaf area depends on the time scale. Plant and Soil 272, 11-27.
118. Villar R, Veneklaas EJ, Jordano P, Lambers H. 1998. Relative growth rate and biomass allocation in 20 Aegilops (Poaceae) species. New Phytologist 140, 425-437.
119. Violle C, Navas M-L, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E. 2007. Let the concept of trait be functional! Oikos 116, 882-892.
120. Walls RL. 2011. Angiosperm leaf vein patterns are linked to leaf functions in a global scale data set. American Journal of Botany 98, 244-253.
121. Walters MB, Reich PB. 1999. Low-light carbon balance and shade tolerance in the seedlings of woody plants: do winter deciduous and broad-leaved evergreen species differ? New Phytologist 143, 143-154.
122. Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ. 2002. Plant ecological strategies: some leading dimensions of variation between species. Annual Review of Ecology and Systematics 33, 125-159.
123. Westoby M, Reich PB, Wright IJ. 2013. Understanding ecological variation across species: area-based vs mass-based expression of leaf traits. New Phytologist 199, 322-323.
124. Witkowski ETF, Lamont BB. 1991. Leaf specific mass confounds leaf density and thickness. Oecologia 88, 486-493.
125. Wright IJ, Reich PB, Cornelissen JHC, et al. 2005a. Assessing the generality of global leaf trait relationships. New Phytologist 166, 485-496.
126. Wright IJ, Reich PB, Cornelissen JHC, et al. 2005b. Modulation of leaf economic traits and trait relationships by climate. Global Ecology and Biogeography 14, 411-421.
127. Wright IJ, Reich PB, Westoby M, et al. 2004. The worldwide leaf economics spectrum. Nature 428, 821-827.
128. Wright IJ, Westoby M. 2002. Leaves at low versus high rainfall: coordination of structure, lifespan and physiology. New Phytologist 155, 403-416.
129. Wylie RB. 1939. Relations between tissue organization and vein distribution in dicotyledon leaves. American Journal of Botany 26, 219-225.
130. Wylie RB. 1946. Relations between tissue organization and vascularization in leaves of certain tropical and subtropical dicotyledons. American Journal of Botany 33, 721-726.
131. Wylie RB. 1951. Principles of foliar organization shown by sun-shade leaves from ten species of deciduous dicotyledonous trees. American Journal of Botany 38, 355-361.
132. Wylie RB. 1952. The bundle sheath extension in leaves of dicotyledons. American Journal of Botany 39, 645-651.
133. Wylie RB. 1954. Leaf organization of some woody dicotyledons from New Zealand. American Journal of Botany 41, 186-191.
134. Zhang S-B, Guan Z-J, Sun M, Zhang J-J, Cao K-F, Hu H. 2012. Evolutionary association of stomatal traits with leaf vein density in Paphiopedilum, Orchidaceae. PLoS one 7, e40080.