Plant functional traits have globally consistent effects on competition

Nature

Volumn 529, Issue 7585, 2016, Pages 204-207

  Kunstler, Georges ^a,b,c   Falster, Daniel ^c   Coomes, David A ^d   Hui, Francis ^e   Kooyman, Robert M ^c,f   Laughlin, Daniel C ^g   Poorter, Lourens ^h   Vanderwel, Mark ⁱ   Vieilledent, Ghislain ^j   Wright, S Joseph ^k   Aiba, Masahiro ^l   Baraloto, Christopher ^m,n   Caspersen, John ^o,p   Cornelissen, J Hans C ^q   Gourlet Fleury, Sylvie ^j   Hanewinkel, Marc ^p,r   Herault, Bruno ^j   Kattge, Jens ^s,t   Kurokawa, Hiroko ^l,ai   Onoda, Yusuke ^u   Peñuelas, Josep ^v,w   Poorter, Hendrik ^x   Uriarte, Maria ^y   Richardson, Sarah ^z   Ruiz Benito, Paloma ^aa,ab   Sun, I Fang ^ac   Ståhl, Göran ^ad   Swenson, Nathan G ^ae   Thompson, Jill ^af,ag   Westerlund, Bertil ^ad   Wirth, Christian ^t,ah   Zavala, Miguel A ^ab   Zeng, Hongcheng ^o   Zimmerman, Jess K ^ag   Zimmermann, Niklaus E ^p   Westoby, Mark ^c   more..

^a Cemagref   (France)

^b UNIV GRENOBLE ALPES   (France)

^c MACQUARIE UNIVERSITY   (Australia)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^f ROYAL BOTANIC GARDENS AND DOMAIN TRUST   (Australia)

^g UNIVERSITY OF WAIKATO   (New Zealand)

^h WAGENINGEN UNIVERSITY   (Netherlands)

ⁱ UNIVERSITY OF REGINA   (Canada)

^j CIRAD   (France)

^k SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^l TOHOKU UNIVERSITY   (Japan)

^m Campus Agronomique   (France)

ⁿ FLORIDA INTERNATIONAL UNIVERSITY   (United States)

^o UNIVERSITY OF TORONTO   (Canada)

^p SWISS FEDERAL RESEARCH INSTITUTE WSL   (Switzerland)

^q VU UNIVERSITY AMSTERDAM   (Netherlands)

^r UNIVERSITY OF FREIBURG   (Germany)

^s MAX PLANCK INSTITUTE FOR BIOGEOCHEMISTRY   (Germany)

^t GERMAN CENTRE FOR INTEGRATIVE BIODIVERSITY RESEARCH IDIV HALLE JENA LEIPZIG   (Germany)

^u KYOTO UNIVERSITY   (Japan)

^v CSIC   (Spain)

^w CREAF   (Spain)

^x FORSCHUNGSZENTRUM JÜLICH   (Germany)

^y Och Spine at New York Presbyterian Hospitals   (United States)

^z LANDCARE RESEARCH   (New Zealand)

^aa UNIVERSITY OF STIRLING   (United Kingdom)

^ab UNIVERSITY OF ALCALÁ   (Spain)

^ac NATIONAL DONG HWA UNIVERSITY   (Taiwan)

^ad SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^ae Bldg 142   (United States)

^af CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

^ag UNIVERSITY OF PUERTO RICO   (Puerto Rico)

^ah UNIVERSITY OF LEIPZIG   (Germany)

^ai FORESTRY AND FOREST PRODUCTS RESEARCH INSTITUTE   (Japan)

more..

Author keywords

[No Author keywords available]

Indexed keywords

COMPETITION (ECOLOGY); FOREST ECOSYSTEM; PHENOTYPE; PHYSIOLOGY; PLANT;

ARTICLE; BIOME; COMPETITION; DENSITY; LEAF AREA; NONHUMAN; PLANT; PLANT GROWTH; PRIORITY JOURNAL; SPECIES; WOOD; ANALYSIS; ANATOMY AND HISTOLOGY; BIOLOGICAL MODEL; FOREST; GROWTH, DEVELOPMENT AND AGING; INTERNATIONAL COOPERATION; PHENOTYPE; PHYSIOLOGY; PLANT LEAF; TREE;

FORESTS; INTERNATIONALITY; MODELS, BIOLOGICAL; PHENOTYPE; PLANT LEAVES; TREES; WOOD;

EID: 84954129816     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature16476     Document Type: Article

References (134)

1. Westoby, M., Falster, D. S., Moles, A. T., Vesk, P. a. & Wright, I. J. Plant Ecological Strategies: some leading dimensions of variation between species. Annu. Rev. Ecol. Evol. Syst. 33, 125-159 (2002).
2. Wright, I. J. et al. The worldwide leaf economics spectrum. Nature 428, 821-827 (2004).
3. Chave, J. et al. Towards a worldwide wood economics spectrum. Ecol. Lett. 12, 351-366 (2009).
4. Keddy, P. A. Competition (Springer Netherlands, 1989).
5. Rees, M., Condit, R., Crawley, M., Pacala, S. W. & Tilman, D. Long-term studies of vegetation dynamics. Science 293, 650-655 (2001).
6. Adler, P. B., Fajardo, A., Kleinhesselink, A. R. & Kraft, N. J. B. Trait-based tests of coexistence mechanisms. Ecol. Lett. 16, 1294-1306 (2013).
7. MacArthur, R. & Levins, R. The limiting similarity, convergence, and divergence of coexisting species. Am. Nat. 101, 377-385 (1967).
8. Uriarte, M. et al. Trait similarity, shared ancestry and the structure of neighbourhood interactions in a subtropical wet forest: implications for community assembly. Ecol. Lett. 13, 1503-1514 (2010).
9. Kunstler, G. et al. Competitive interactions between forest trees are driven by species' trait hierarchy, not phylogenetic or functional similarity: implications for forest community assembly. Ecol. Lett. 15, 831-840 (2012).
10. HilleRisLambers, J., Adler, P., Harpole, W., Levine, J. & Mayfield, M. Rethinking community assembly through the lens of coexistence theory. Annu. Rev. Ecol. Evol. Syst. 43, 227-248 (2012).
11. Lasky, J. R., Uriarte, M., Boukili, V. K. & Chazdon, R. L. Trait-mediated assembly processes predict successional changes in community diversity of tropical forests. Proc. Natl Acad. Sci. USA 111, 5616-5621 (2014).
12. Kraft, N. J. B., Godoy, O. & Levine, J. M. Plant functional traits and the multidimensional nature of species coexistence. Proc. Natl Acad. Sci. USA 112, 797-802 (2015).
13. Mayfield, M. M. & Levine, J. M. Opposing effects of competitive exclusion on the phylogenetic structure of communities: phylogeny and coexistence. Ecol. Lett. 13, 1085-1093 (2010).
14. Kraft, N. J. B., Crutsinger, G. M., Forrestel, E. J. & Emery, N. C. Functional trait differences and the outcome of community assembly: an experimental test with vernal pool annual plants. Oikos 123, 1391-1399 (2014).
15. Wright, S. J. et al. Functional traits and the growth-mortality trade-off in tropical trees. Ecology 91, 3664-3674 (2010).
16. Goldberg, D. E. Competitive ability: definitions, contingency and correlated traits. Phil. Trans. R. Soc. Lond. B 351, 1377-1385 (1996).
17. Gaudet, C. L. & Keddy, P. A. A comparative approach to predicting competitive ability from plant traits. Nature 334, 242-243 (1988).
18. Kattge, J. et al. TRY - a global database of plant traits. Glob. Change Biol. 17, 2905-2935 (2011).
19. Uriarte, M., Canham, C. D., Thompson, J. & Zimmerman, J. K. A neighborhood analysis of tree growth and survival in a hurricane-driven tropical forest. Ecol. Monogr. 74, 591-614 (2004).
20. Poorter, L. et al. Are functional traits good predictors of demographic rates? Evidence from five neotropical forests. Ecology 89, 1908-1920 (2008).
21. Poorter, L., Bongers, L. & Bongers, F. Architecture of 54 moist-forest tree species: traits, trade-offs, and functional groups. Ecology 87, 1289-1301 (2006).
22. Aiba, M. & Nakashizuka, T. Architectural differences associated with adult stature and wood density in 30 temperate tree species. Funct. Ecol. 23, 265-273 (2009).
23. Niinemets, Ü. A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance. Ecol. Res. 25, 693-714 (2010).
24. Adams, T. P., Purves, D. W. & Pacala, S. W. Understanding height-structured competition in forests: is there an R∗ for light? Proc. R. Soc. B 274, 3039-3047 (2007).
25. Sapijanskas, J., Paquette, A., Potvin, C., Kunert, N. & Loreau, M. Tropical tree diversity enhances light capture through crown plasticity and spatial and temporal niche differences. Ecology 95, 2479-2492 (2014).
26. Jucker, T., Bouriaud, O. & Coomes, D. A. Crown plasticity enables trees to optimize canopy packing in mixed-species forests. Funct. Ecol. 29, 1078-1086 (2015).
27. Bagchi, R. et al. Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature 506, 85-88 (2014).
28. Wang, P., Stieglitz, T., Zhou, D. W. & Cahill, J. F. Jr. Are competitive effect and response two sides of the same coin, or fundamentally different? Funct. Ecol. 24, 196-207 (2010).
29. Canham, C. D. et al. Neighborhood analyses of canopy tree competition along environmental gradients in New England forests. Ecol. Appl. 16, 540-554 (2006).
30. Rüger, N., Wirth, C., Wright, S. J. & Condit, R. Functional traits explain light and size response of growth rates in tropical tree species. Ecology 93, 2626-2636 (2012).
31. Schielzeth, H. Simple means to improve the interpretability of regression coefficients: Interpretation of regression coefficients. Methods Ecol. Evol. 1, 103-113 (2010).
32. Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Soft. 67, 1-48 (2014).
33. R Development Core Team. R: A Language and Environment for Statistical Computing http://www.R-project.org/ (R Foundation for Statistical Computing, 2014).
34. Kriticos, D. J. et al. CliMond: global high-resolution historical and future scenario climate surfaces for bioclimatic modelling. Methods Ecol. Evol. 3, 53-64 (2012).
35. Connell, J. H. On the prevalence and relative importance of interspecific competition: Evidence from field experiments. Am. Nat. 122, 661-696 (1983).
36. Chesson, P. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Evol. Syst. 31, 343-366 (2000).
37. Chesson, P. in Ecological Systems (ed. Leemans, R.) 223-256 (Springer, 2012).
38. Godoy, O. & Levine, J. M. Phenology effects on invasion success: insights from coupling field experiments to coexistence theory. Ecology 95, 726-736 (2014).
39. IGN Inventaire Forestier; http://inventaire-forestier.ign.fr/spip/spip.php?rubrique153.
40. Kooyman, R., Rossetto, M., Allen, C. & Cornwell, W. Australian tropical and subtropical rain forest community assembly: phylogeny, functional biogeography, and environmental gradients. Biotropica 44, 668-679 (2012).
41. New Zealand National Vegetation Survey Databank; https://nvs.landcareresearch.co.nz/.
42. Wiser, S. K., Bellingham, P. J. & Burrows, L. E. Managing biodiversity information: development of New Zealand's National Vegetation Survey databank. N. Z. J. Ecol. 25, 1-17 (2001).
43. Ministerio de Agricultura, Alimentación y Medio Ambiente. Inventario Forestal Nacional; http://www.magrama.gob.es/es/desarrollo-rural/temas/politica-forestal/inventario-cartografia/inventario-forestal-nacional/default.aspx.
44. Villaescusa, R. & Diaz, R. Segundo Inventario Forestal Nacional (1986-1996) (Ministerio de Medio Ambiente, 1998).
45. Villanueva, J. Tercer Inventario Forestal Nacional (1997-2007) (Ministerio de Medio Ambiente, 2004).
46. Fridman, J. & Stahl, G. A three-step approach for modelling tree mortality in swedish forests. Scand. J. For. Res. 16, 455-466 (2001).
47. Swiss National Forest Inventory (NFI); http://www.lfi.ch/index-en.php.
48. USDA Forest Inventory and Analysis National Program; http://www.fia.fs.fed.us/tools-data/.
49. Condit, R., Engelbrecht, B. M. J., Pino, D., Perez, R. & Turner, B. L. Species distributions in response to individual soil nutrients and seasonal drought across a community of tropical trees. Proc. Natl Acad. Sci. USA 110, 5064-5068 (2013).
50. Condit, R., Hubbell, S. P. & Foster, R. B. Mortality and growth of a commercial hardwood 'el cativo', Prioria copaifera, in Panama. For. Ecol. Manage. 62, 107-122 (1993).
51. Lasky, J. R., Sun, I., Su, S.-H., Chen, Z.-S. & Keitt, T. H. Trait-mediated effects of environmental filtering on tree community dynamics. J. Ecol. 101, 722-733 (2013).
52. Ishihara, M. I. et al. Forest stand structure, composition, and dynamics in 34 sites over japan. Ecol. Res. 26, 1007-1008 (2011).
53. Thompson, J. et al. Land use history, environment, and tree composition in a tropical forest. Ecol. Appl. 12, 1344-1363 (2002).
54. Ouédraogo, D.-Y., Mortier, F., Gourlet-Fleury, S., Freycon, V. & Picard, N. Slow-growing species cope best with drought: evidence from long-term measurements in a tropical semi-deciduous moist forest of Central Africa. J. Ecol. 101, 1459-1470 (2013).
55. Herault, B., Ouallet, J., Blanc, L., Wagner, F. & Baraloto, C. Growth responses of neotropical trees to logging gaps. J. Appl. Ecol. 47, 821-831 (2010).
56. Hérault, B. et al. Functional traits shape ontogenetic growth trajectories of rain forest tree species. J. Ecol. 99, 1431-1440 (2011).
57. Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965-1978 (2005).
58. Ricklefs, R. E. The Economy of Nature (WH Freeman, 2001).
59. Whittaker, R. H. Communities and Ecosystems (Macmillan, 1970).
60. Swenson, N. G. et al. Temporal turnover in the composition of tropical tree communities: functional determinism and phylogenetic stochasticity. Ecology 93, 490-499 (2012).
61. Gourlet-Fleury, S. et al. Environmental filtering of dense-wooded species controls above-ground biomass stored in African moist forests. J. Ecol. 99, 981-990 (2011).
62. Baraloto, C. et al. Decoupled leaf and stem economics in rain forest trees. Ecol. Lett. 13, 1338-1347 (2010).
63. Ackerly, D. D. & Cornwell, W. K. A trait-based approach to community assembly: partitioning of species trait values into within- and among-community components. Ecol. Lett. 10, 135-145 (2007).
64. Castro-Díez, P., Puyravaud, J., Cornelissen, J. & Villar-Salvador, P. Stem anatomy and relative growth rate in seedlings of a wide range of woody plant species and types. Oecologia 116, 57-66 (1998).
65. Cornelissen, J. An experimental comparison of leaf decomposition rates in a wide range of temperate plant species and types. J. Ecol. 84, 573-582 (1996).
66. Cornelissen, J., Diez, P. C. & Hunt, R. Seedling growth, allocation and leaf attributes in a wide range of woody plant species and types. J. Ecol. 84, 755-765 (1996).
67. Cornelissen, J., Werger, M., Castro-Diez, P., Van Rheenen, J. & Rowland, A. Foliar nutrients in relation to growth, allocation and leaf traits in seedlings of a wide range of woody plant species and types. Oecologia 111, 460-469 (1997).
68. Cornelissen, J. et al. Leaf digestibility and litter decomposability are related in a wide range of subarctic plant species and types. Funct. Ecol. 18, 779-786 (2004).
69. Cornelissen, J. et al. Functional traits of woody plants: correspondence of species rankings between field adults and laboratory-grown seedlings? J. Veg. Sci. 14, 311-322 (2003).
70. Cornwell, W. K. & Ackerly, D. D. Community assembly and shifts in plant trait distributions across an environmental gradient in coastal California. Ecol. Monogr. 79, 109-126 (2009).
71. Cornwell, W. K., Schwilk, L. D. W. & Ackerly, D. D. A trait-based test for habitat filtering: convex hull volume. Ecology 87, 1465-1471 (2006).
72. Cornwell, W., Bhaskar, R., Sack, L. & Cordell, S. Adjustment of structure and function of Hawaiian Metrosideros polymorpha at high vs. low precipitation. Funct. Ecol. 21, 1063-1071 (2007).
73. Cornwell, W. K. et al. Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol. Lett. 11, 1065-1071 (2008).
74. Diaz, S. et al. The plant traits that drive ecosystems: evidence from three continents. J. Veg. Sci. 15, 295-304 (2004).
75. Fonseca, C. R., Overton, J. M., Collins, B. & Westoby, M. Shifts in trait-combinations along rainfall and phosphorus gradients. J. Ecol. 88, 964-977 (2000).
76. Fortunel, C. et al. Leaf traits capture the effects of land use changes and climate on litter decomposability of grasslands across Europe. Ecology 90, 598-611 (2009).
77. Freschet, G. T., Cornelissen, J. H., Van Logtestijn, R. S. & Aerts, R. Evidence of the 'plant economics spectrum' in a subarctic flora. J. Ecol. 98, 362-373 (2010).
78. Freschet, G. T., Cornelissen, J. H., van Logtestijn, R. S. & Aerts, R. Substantial nutrient resorption from leaves, stems and roots in a subarctic flora: what is the link with other resource economics traits? New Phytol. 186, 879-889 (2010).
79. Garnier, E. et al. Assessing the effects of land-use change on plant traits, communities and ecosystem functioning in grasslands: a standardized methodology and lessons from an application to 11 European sites. Ann. Bot. (Lond.) 99, 967-985 (2007).
80. Green, W. USDA PLANTS compilation, version 1, 09-02-02; http://bricol.net/downloads/data/PLANTSdatabase/ (2009).
81. Han, W., Fang, J., Guo, D. & Zhang, Y. Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. New Phytol. 168, 377-385 (2005).
82. He, J.-S. et al. A test of the generality of leaf trait relationships on the Tibetan Plateau. New Phytol. 170, 835-848 (2006).
83. He, J.-S. et al. Leaf nitrogen: phosphorus stoichiometry across Chinese grassland biomes. Oecologia 155, 301-310 (2008).
84. Hoof, J., Sack, L., Webb, D. T. & Nilsen, E. T. Contrasting structure and function of pubescent and glabrous varieties of Hawaiian Metrosideros polymorpha (Myrtaceae) at high elevation. Biotropica 40, 113-118 (2008).
85. Kattge, J., Knorr, W., Raddatz, T. & Wirth, C. Quantifying photosynthetic capacity and its relationship to leaf nitrogen content for global-scale terrestrial biosphere models. Glob. Change Biol. 15, 976-991 (2009).
86. Kleyer, M. et al. The LEDA traitbase: a database of life-history traits of the Northwest European flora. J. Ecol. 96, 1266-1274 (2008).
87. Kurokawa, H. & Nakashizuka, T. Leaf herbivory and decomposability in a malaysian tropical rain forest. Ecology 89, 2645-2656 (2008).
88. Laughlin, D. C., Leppert, J. J., Moore, M. M. & Sieg, C. H. A multi-trait test of the leaf-height-seed plant strategy scheme with 133 species from a pine forest flora. Funct. Ecol. 24, 493-501 (2010).
89. Martin, R. E., Asner, G. P. & Sack, L. Genetic variation in leaf pigment, optical and photosynthetic function among diverse phenotypes of Metrosideros polymorpha grown in a common garden. Oecologia 151, 387-400 (2007).
90. McDonald, P., Fonseca, C., Overton, J. & Westoby, M. Leaf-size divergence along rainfall and soil-nutrient gradients: is the method of size reduction common among clades? Funct. Ecol. 17, 50-57 (2003).
91. 2] on photosynthesis in European forest species: a meta-analysis of model parameters. Plant Cell Environ. 22, 1475-1495 (1999).
92. 2] experiments. Ecol. Modell. 124, 69-83 (1999).
93. 2 concentration: a synthesis. New Phytol. 149, 247-264 (2001).
94. Messier, J., McGill, B. J. & Lechowicz, M. J. How do traits vary across ecological scales? A case for trait-based ecology. Ecol. Lett. 13, 838-848 (2010).
95. Moles, A. T. et al. Factors that shape seed mass evolution. Proc. Natl Acad. Sci. USA 102, 10540-10544 (2005).
96. Moles, A. T. et al. A brief history of seed size. Science 307, 576-580 (2005).
97. Moles, A. T., Falster, D. S., Leishman, M. R. & Westoby, M. Small-seeded species produce more seeds per square metre of canopy per year, but not per individual per lifetime. J. Ecol. 92, 384-396 (2004).
98. Niinemets, Ü. Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82, 453-469 (2001).
99. Niinemets, Ü. Research review. components of leaf dry mass per area-thickness and density-alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytol. 144, 35-47 (1999).
100. Ogaya, R. & Peñuelas, J. Experimental drought in a holm oak forest: different photosynthetic response of the two dominant species, Quercus ilex and Phillyrea latifolia. Environ. Exp. Bot. 50, 137-148 (2003).
101. Ogaya, R. & Penuelas, J. Contrasting foliar responses to drought in Quercus ilex and Phillyrea latifolia. Biol. Plant. 50, 373-382 (2006).
102. Ogaya, R. & Peñuelas, J. Tree growth, mortality, and above-ground biomass accumulation in a holm oak forest under a five-year experimental field drought. Plant Ecol. 189, 291-299 (2007).
103. Ogaya, R. & Peñuelas, J. Tree growth, mortality, and above-ground biomass accumulation in a holm oak forest under a five-year experimental field drought. Plant Ecol. 189, 291-299 (2007).
104. Onoda, Y. et al. Global patterns of leaf mechanical properties. Ecol. Lett. 14, 301-312 (2011).
105. Ordoñez, J. C. et al. Plant strategies in relation to resource supply in mesic to wet environments: does theory mirror nature? Am. Nat. 175, 225-239 (2010).
106. Ordoñez, J. C. et al. Leaf habit and woodiness regulate different leaf economy traits at a given nutrient supply. Ecology 91, 3218-3228 (2010).
107. Pakeman, R. J. et al. Impact of abundance weighting on the response of seed traits to climate and land use. J. Ecol. 96, 355-366 (2008).
108. Pakeman, R. J., Lepš, J., Kleyer, M., Lavorel, S. & Garnier, E. Relative climatic, edaphic and management controls of plant functional trait signatures. J. Veg. Sci. 20, 148-159 (2009).
109. Peñuelas, J. et al. Faster returns on 'leaf economics' and different biogeochemical niche in invasive compared with native plant species. Glob. Change Biol. 16, 2171-2185 (2010).
110. Peñuelas, J. et al. Higher allocation to low cost chemical defenses in invasive species of Hawaii. J. Chem. Ecol. 36, 1255-1270 (2010).
111. Poorter, L. & Bongers, F. Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology 87, 1733-1743 (2006).
112. Poorter, L. Leaf traits show different relationships with shade tolerance in moist versus dry tropical forests. New Phytol. 181, 890-900 (2009).
113. Poorter, H., Niinemets, Ü., Poorter, L., Wright, I. J. & Villar, R. Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol. 182, 565-588 (2009).
114. Preston, K. A., Cornwell, W. K. & DeNoyer, J. L. Wood density and vessel traits as distinct correlates of ecological strategy in 51 California coast range angiosperms. New Phytol. 170, 807-818 (2006).
115. Pyankov, V. I., Kondratchuk, A. V. & Shipley, B. Leaf structure and specific leaf mass: the alpine desert plants of the Eastern Pamirs, Tadjikistan. New Phytol. 143, 131-142 (1999).
116. Quested, H. M. et al. Decomposition of sub-arctic plants with differing nitrogen economies: a functional role for hemiparasites. Ecology 84, 3209-3221 (2003).
117. Reich, P. B. et al. Scaling of respiration to nitrogen in leaves, stems and roots of higher land plants. Ecol. Lett. 11, 793-801 (2008).
118. Reich, P. B., Oleksyn, J. & Wright, I. J. Leaf phosphorus influences the photosynthesis-nitrogen relation: a cross-biome analysis of 314 species. Oecologia 160, 207-212 (2009).
119. Sack, L. Responses of temperate woody seedlings to shade and drought: do trade-offs limit potential niche differentiation? Oikos 107, 110-127 (2004).
120. Sack, L., Tyree, M. T. & Holbrook, N. M. Leaf hydraulic architecture correlates with regeneration irradiance in tropical rainforest trees. New Phytol. 167, 403-413 (2005).
121. Sack, L., Melcher, P. J., Liu, W. H., Middleton, E. & Pardee, T. How strong is intracanopy leaf plasticity in temperate deciduous trees? Am. J. Bot. 93, 829-839 (2006).
122. Sardans, J., Peñuelas, J. & Ogaya, R. Drought-induced changes in C and N stoichiometry in a Quercus ilex Mediterranean forest. For. Sci. 54, 513-522 (2008).
123. Sardans, J., Peñuelas, J., Prieto, P. & Estiarte, M. Changes in Ca, Fe, Mg, Mo, Na, and S content in a Mediterranean shrubland under warming and drought. J. Geophys. Res. 113, G03039 (2008).
124. Shipley, B. & Vu, T.-T. Dry matter content as a measure of dry matter concentration in plants and their parts. New Phytol. 153, 359-364 (2002).
125. Soudzilovskaia, N. A. et al. Functional traits predict relationship between plant abundance dynamic and long-term climate warming. Proc. Natl Acad. Sci. USA 110, 18180-18184 (2013).
126. Willis, C. G. et al. Phylogenetic community structure in minnesota oak savanna is influenced by spatial extent and environmental variation. Ecography 33, 565-577 (2010).
127. Wilson, K. B., Baldocchi, D. D. & Hanson, P. J. Spatial and seasonal variability of photosynthetic parameters and their relationship to leaf nitrogen in a deciduous forest. Tree Physiol. 20, 565-578 (2000).
128. Wright, I. J. et al. Relationships among ecologically important dimensions of plant trait variation in seven neotropical forests. Ann. Bot. (Lond.) 99, 1003-1015 (2007).
129. Wright, I. J. et al. Irradiance, temperature and rainfall influence leaf dark respiration in woody plants: evidence from comparisons across 20 sites. New Phytol. 169, 309-319 (2006).
130. Zanne, A. E. et al. Angiosperm wood structure: global patterns in vessel anatomy and their relation to wood density and potential conductivity. Am. J. Bot. 97, 207-215 (2010).
131. South, A. rworldmap. a new r package for mapping global data. Rem. J. 3, 35-43 (2011).
132. Nakagawa, S. & Hanson, P. J. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4, 133-142 (2013).
133. Johnson, P. C. D. Extension of Nakagawa and Schielzeth's R2GLMM to random slopes models. Methods Ecol. Evol. 5, 944-946 (2014).
134. Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: a Practical Information-Theoretic Approach (Springer-Verlag, 2002).