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Temperature but not moisture response of germination shows phylogenetic constraints while both interact with seed mass and lifespan

Published online by Cambridge University Press:  24 April 2017

Fabien Arène ,
Laurence Affre ,
Aggeliki Doxa  and
Arne Saatkamp
Fabien Arène
Affiliation:
Institut Méditerranéen de Biodiversité et d'Ecologie (IMBE), Aix Marseille Université, Centre National de la Recherche Scientifique (CNRS), Institut pour la Recherche et le Développement (IRD), Université Avignon, Faculté St-Jérôme Case 421, 13397 Marseille cedex 20, France
Laurence Affre
Affiliation:
Institut Méditerranéen de Biodiversité et d'Ecologie (IMBE), Aix Marseille Université, Centre National de la Recherche Scientifique (CNRS), Institut pour la Recherche et le Développement (IRD), Université Avignon, Faculté St-Jérôme Case 421, 13397 Marseille cedex 20, France
Aggeliki Doxa
Affiliation:
Institut Méditerranéen de Biodiversité et d'Ecologie (IMBE), Aix Marseille Université, Centre National de la Recherche Scientifique (CNRS), Institut pour la Recherche et le Développement (IRD), Université Avignon, Faculté St-Jérôme Case 421, 13397 Marseille cedex 20, France
Arne Saatkamp*
Affiliation:
Institut Méditerranéen de Biodiversité et d'Ecologie (IMBE), Aix Marseille Université, Centre National de la Recherche Scientifique (CNRS), Institut pour la Recherche et le Développement (IRD), Université Avignon, Faculté St-Jérôme Case 421, 13397 Marseille cedex 20, France
*
*Correspondence Email: arne.saatkamp@imbe.fr
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Abstract

Understanding how plant traits interact with climate to determine plant niches is decisive for predicting climate change impacts. While lifespan and seed size modify the importance of germination timing, germination traits such as base temperature and base water potential directly translate climatic conditions into germination timing, impacting performance in later life stages. Yet we do not know how base temperature, base water potential, seed mass, lifespan and climate are related. We tested the relationships between base temperature and base water potential for germination, seed size and lifespan while controlling for bioclimatic regions. We also quantified the phylogenetic signal in germination traits and seed size using Pagel's λ. We used a worldwide data set of germination responses to temperature and moisture, seed size and lifespan of 240 seed plants from 49 families. Both germination temperature and moisture are negatively related to seed size. Annual plants show a negative relation between seed size and base water potential, whereas perennials display a negative relation between base temperature and seed mass. Pagel's λ highlighted the slow evolution of base temperature for germination, comparable to seed mass while base water potential was revealed to be labile. In the future, base water potential and seed mass can be used when moisture niches of plants are to be predicted. Lifespan, seed size and base temperature should be taken into account when analysing thermal limits of species distributions.

Keywords

base temperaturebase water potentialgermination traitshydrotimelifespanphylogenetic signalseed sizeseed–plantthermal time
Type
Research Papers
Information
Seed Science Research , Volume 27 , Special Issue 2: Seed Ecology , June 2017 , pp. 110 - 120
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Copyright © Cambridge University Press 2017 

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References

Agrawal, A.A., Johnson, M.T.J., Hastings, A.P. and Maron, J.L. (2013) A field experiment demonstrating plant life-history evolution and its eco-evolutionary feedback to seed predator populations. American Naturalist 181, 35–45.Google Scholar
Aizen, M.A. and Woodcock, H. (1996) Effects of acorn size on seedling survival and growth in Quercus rubra following simulated spring freeze. Canadian Journal of Botany 74, 308–314.CrossRefGoogle Scholar
Allen, P.S., Meyer, S.E. and Khan, M.A. (2000) Hydrothermal time as a tool in comparative germination studies. In Black, M., Bradford, K.J. and Vázquez-Ramos, J. (eds), Seed Biology: Advances and applications, pp. 401–410. Proceedings of the Sixth International Workshop on Seeds, Merida, Mexico. Wallingford, UK: CABI Publishing.Google Scholar
Bair, N.B., Meyer, S.E. and Allen, P.S. (2006) A hydrothermal after-ripening time model for seed dormancy loss in Bromus tectorum L. Seed Science Research 16, 17–28.CrossRefGoogle Scholar
Baker, H.G. (1972) Seed weight in relation to environmental conditions in California. Ecology 53, 997–1010.Google Scholar
Baskin, C.C. and Baskin, J.M. (2014) Seeds: Ecology, Biogeography and Evolution of Dormancy and Germination. Burlington: Academic Press.Google Scholar
Baskin, J.M., Baskin, C.C. and Xiaojie, L. (2000) Taxonomy, anatomy and evolution of physical dormancy in seeds. Plant Species Biology 15, 139–152.Google Scholar
Batlla, D. and Benech-Arnold, R.L. (2003) A quantitative analysis of dormancy loss dynamics in Polygonum aviculare L. seeds: development of a thermal time model based on changes in seed population thermal parameters. Seed Science Research 13, 55–68.Google Scholar
Boulangeat, I., Lavergne, S., Van Es, J., Garraud, L. and Thuiller, W. (2011) Niche breadth, rarity and ecological characteristics within a regional flora spanning large environmental gradients. Journal of Biogeography 39, 204–214.Google Scholar
Bradford, K.J. (2002) Applications of hydrothermal time to quantifying and modeling seed germination and dormancy. Weed Science 50, 248–260.Google Scholar
Broennimann, O., Thuiller, W., Hughes, G., Midgley, G.F., Alkemade, J.M.R. and Guisan, A. (2006) Do geographic distribution, niche property and life form explain plants’ vulnerability to global change? Global Change Biology 12, 1079–1093.Google Scholar
Bykova, O., Chuine, I., Morin, X. and Higgins, S.I. (2012) Temperature dependence of the reproduction niche and its relevance for plant species distributions. Journal of Biogeography 39, 2191–2200.CrossRefGoogle Scholar
Canham, C.D., Kobe, R.K., Latty, E.F. and Chazdon, R.L. (1999) Interspecific and intraspecific variation in tree seedling survival: effects of allocation to roots versus carbohydrate reserves. Oecologia 121, 1–11.Google Scholar
Chave, J., Coomes, D., Jansen, S., Lewis, S.L., Swenson, N.G. and Zanne, A.E. (2009) Towards a worldwide wood economics spectrum. Ecology Letters 12, 351–c366.Google Scholar
Chuine, I. (2010) Why does phenology drive species distribution? Philosophical Transactions of the Royal Society B: Biological Sciences 365, 3149–3149.Google Scholar
Daniel, R.M. and Danson, M.J. (2010) A new understanding of how temperature affects the catalytic activity of enzymes. Trends in Biochemical Sciences 35, 584–591.CrossRefGoogle ScholarPubMed
Daws, M.I., Crabtree, L.M., Dalling, J.W., Mullins, C.E. and Burslem, D.F.R.P. (2008) Germination responses to water potential in neotropical pioneers suggest large-seeded species take more risks. Annals of Botany 102, 945–951.Google Scholar
Donoghue, M.J. and Edwards, E.J. (2014) Biome shifts and niche evolution in plants. Annual Review of Ecology, Evolutio, and Systematics 45, 547–572.Google Scholar
Donohue, K. (2002) Germination timing influences natural selection on life-history characters in Arabidopsis thaliana . Ecology 83, 1006–1016.Google Scholar
Donohue, K., Dorn, L., Griffith, C., Kim, E., Aguilera, A., Polisetty, C.R. and Schmitt, J. (2005) Environmental and genetic influences on the germination of Arabidopsis thaliana in the field. Evolution 59, 740–757.Google Scholar
Donohue, K., Rubio de Casas, R., Burghardt, L., Kovach, K. and Willis, C.G. (2010) Germination, postgermination adaptation, and species ecological ranges. Annual Reviews of Ecology, Evolution and Systematics 41, 293–319.Google Scholar
Durka, W. and Michalski, S.G. (2012) Daphne: a dated phylogeny of a large European flora for phylogenetically informed ecological analyses. Ecology 93, 2297–2297.Google Scholar
Dürr, C., Dickie, J.B., Yang, X.Y. and Pritchard, H.W. (2015) Ranges of critical temperature and water potential values for the germination of species worldwide: contribution to a seed trait database. Agricultural and forest meteorology 200, 222–232.CrossRefGoogle Scholar
Evans, M.E.K., Hearn, D.J., Hahn, W.J., Spangle, J.M. and Venable, D.L. (2005) Climate and life-history evolution in evening primroses (Oenothera, Onagraceae): a phylogenetic comparative analysis. Evolution 59, 1914–1927.Google Scholar
Felsenstein, J. (1985) Phylogenies and the comparative method. American Naturalist 125, 1–15.Google Scholar
Finch-Savage, W.E. and Leubner-Metzger, G. (2006) Seed dormancy and the control of germination. New Phytologist 171, 501–523.Google Scholar
Forbis, T.A., Floyd, S.K. and Queiroz, A.D. (2002) The evolution of embryo size in angiosperms and other seed plants: implications for the evolution of seed dormancy. Evolution 56, 2112–2125.Google Scholar
Foster, S. and Janson, C.H. (1985) The relationship between seed size and establishment conditions in tropical woody plants. Ecology 66, 773–780.Google Scholar
Freckleton, R.P., Harvey, P.H. and Pagel, M. (2002) Phylogenetic analysis and comparative data: a test and review of evidence. American Naturalist 160, 712–726.Google Scholar
Gallagher, R.V., Beaumont, L.J., Hughes, L. and Leishman, M.R. (2010) Evidence for climatic niche and biome shifts between native and novel ranges in plant species introduced to Australia. Journal of Ecology 98, 790–799.Google Scholar
García-Baquero, G., Silvertown, J., Gowing, D.J. and Valle, C.J. (2015) Dissecting the hydrological niche: soil moisture, space and lifespan. Journal of Vegetation Science 27, 219–226.Google Scholar
Garnier, E. (1992) Growth analysis of congeneric annual and perennial grass species. Journal of Ecology 80, 665–675.Google Scholar
Grafen, A. (1989) The phylogenetic regression. Philosophical Transactions of the Royal Society Series B 326, 119–157.Google Scholar
Grubb, P.J. (1977) Maintenance of species-richness in plant communities: the importance of the regeneration niche. Biological Reviews of the Cambridge Philosophical Society 52, 107–145.Google Scholar
Hanspach, J., Kühn, I., Pompe, S. and Klotz, S. (2010) Predictive performance of plant species distribution models depends on species traits. Perspectives in Plant Ecology, Evolution and Systematics 12, 219–225.Google Scholar
Harper, J.L. (1977) Population Biology of Plants. London: Academic Press.Google Scholar
Harper, J.L., Williams, J.T. and Sagar, G.R. (1965) The behaviour of seeds in soil: I. The heterogeneity of soil surfaces and its role in determining the establishment of plants from seed. Journal of Ecology 53, 273–286.Google Scholar
Holdsworth, M.J., Finch-Savage, W.E., Grappin, P. and Job, D. (2008) Post-genomics dissection of seed dormancy and germination. Trends in Plant Science 13, 7–13.Google Scholar
Holt, G. and Chesson, P. (2014) Variation in moisture duration as a driver of coexistence by the storage effect in desert annual plants. Theoretical Population Biology 92, 36–50.Google Scholar
Huang, Z., Liu, S., Bradford, K.J., Huxman, T.E. and Venable, D.L. (2016) The contribution of germination functional traits to population dynamics of a desert plant community. Ecology 97, 250–261.Google Scholar
Jiménez-Alfaro, B., Silveira, F.A., Fidelis, A., Poschlod, P. and Commander, L.E. (2016) Seed germination traits can contribute better to plant community ecology. Journal of Vegetation Science 27, 637–645.Google Scholar
Jump, A.S. and Penuelas, J. (2005) Running to stand still: adaptation and the response of plants to rapid climate change. Ecology Letters 8, 1010–1020.Google Scholar
Kleyer, M., Bekker, R.M., Knevel, I.C., Bakker, J.P., Thompson, K., Sonnenschein, M., Poschlod, P., van Groenendael, J.M., Klimeš, L., Klimešová, J., Klotz, S., Rusch, G.M., Hermy, M., Adriaens, D., Boedeltje, G., Bossuyt, B., Dannemann, A., Endels, P., Götzenberger, L., Hodgson, J.G., Jackel, A.K., Kühn, I., Kunzmann, D., Ozinga, W.A., Römermann, C., Stadler, M., Schlegelmilch, J., Steendam, H.J., Tackenberg, O., Wilmann, B., Cornelissen, J.H.C., Eriksson, O., Garnier, E. and Peco, B. (2008) The LEDA Traitbase: a database of life-history traits of the Northwest European flora. Journal of Ecology 96, 1266–1274.Google Scholar
Köchy, M. and Tielbörger, K. (2007) Hydrothermal time model of germination: parameters for 36 Mediterranean annual species based on a simplified approach. Basic and Applied Ecology 8, 171–182.Google Scholar
Kruk, B., Insausti, P., Razul, A. and Benech-Arnold, R.L. (2006) Light and thermal environments as modified by a wheat crop: effects on weed seed germination. Journal of Applied Ecology 43, 227–236.Google Scholar
Larcher, W. (2003) Physiological Plant Ecology: Ecophysiology and Stress Physiology of Functional Groups. Berlin, Heidelberg: Springer Verlag.Google Scholar
Leishman, M.R. and Westoby, M. (1994) The role of seed size in seedling establishment in dry soil conditions – experimental evidence from semi-arid species. Journal of Ecology 82, 249–258.Google Scholar
Leishman, M.R., Wright, I.J., Moles, A.T. and Westoby, M. (2000) The evolutionary ecology of seed size. In Fenner, M. (ed), Seeds – The Ecology of Regeneration in Plant Communities, pp. 31–57. Wallingford, UK: CABI Publishing.CrossRefGoogle Scholar
Lloret, F., Casanovas, C. and Penuelas, J. (1999) Seedling survival of Mediterranean shrubland species in relation to root:shoot ratio, seed size and water and nitrogen use. Functional Ecology 13, 210–216.Google Scholar
Lodge, G.M. and Whalley, R.D.B. (1981) Establishment of warm- and cool-season native perennial grasses on the north-west slopes of New South Wales. I. Dormancy and germination. Australian Journal of Botany 29, 111–119.Google Scholar
Losos, J.B. (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecology Letters 11, 995–1003.Google Scholar
Luis, M.D., Verdù, M. and Raventós, J. (2008) Early to rise makes a plant healthy, wealthy, and wise. Ecology 89, 3061–3071.Google Scholar
Marañón, T. and Grubb, P.J. (1993) Physiological basis and ecological significance of the seed size and relative growth rate relationship in Mediterranean annuals. Functional Ecology 7, 591–599.Google Scholar
Mazer, S.J. (1989) Ecological, taxonomic, and life history correlates of seed mass among Indiana dune angiosperms. Ecological Monographs 59, 153–175.Google Scholar
McGill, B.J., Enquist, B.J., Weiher, E. and Westoby, M. (2006) Rebuilding community ecology from functional traits. Trends in Ecology and Evolution 21, 178–185.Google Scholar
Metcalfe, D.J. and Grubb, P.J. (1995) Seed mass and light requirements for regeneration in Southeast Asian rain forest. Canadian Journal of Botany 73, 817–826.Google Scholar
Metz, J., Liancourt, P., Kigel, J., Harel, D., Sternberg, M. and Tielbörger, K. (2010) Plant survival in relation to seed size along environmental gradients: a long-term study from semi-arid and Mediterranean annual plant communities. Journal of Ecology 98, 697–704.Google Scholar
Moles, A.T., Ackerly, D.D., Tweddle, J.C., Dickie, J.B., Smith, R., Leishman, M.R., Mayfield, M.M., Pitman, A., Wood, J.T. and Westoby, M. (2007) Global patterns in seed size. Global Ecology and Biogeography 16, 109–116.Google Scholar
Moles, A.T., Ackerly, D.D., Webb, C.O., Tweddle, J.C., Dickie, J.B., Pitman, A.J. and Westoby, M. (2005) Factors that shape seed mass evolution. Proceedings of the National Academy of Sciences, USA 102, 10540–10540.Google Scholar
Moles, A.T., Falster, D.S., Leishman, M.R. and Westoby, M. (2004) Small-seeded species produce more seeds per square metre of canopy per year, but not per individual per lifetime. Journal of Ecology 92, 384–396.Google Scholar
Moles, A.T. and Westoby, M. (2004) Seedling survival and seed size: a synthesis of the literature. Journal of Ecology 92, 372–383.Google Scholar
Mollard, F.P.O. and Naeth, M.A. (2015) Germination sensitivities to water potential among co-existing C3 and C4 grasses of cool semi-arid prairie grasslands. Plant Biology 17, 583–587.Google Scholar
Morin, X., Augspurger, C. and Chuine, I. (2007) Process-based modeling of species’ distributions: what limits temperature tree species’ range boundaries? Ecology 88, 2280–2291.Google Scholar
Münkemüller, T., Lavergne, S., Bzeznik, B., Dray, S., Jombart, T., Schiffers, K. and Thuiller, W. (2012) How to measure and test phylogenetic signal. Methods in Ecology and Evolution 3, 743–756.Google Scholar
Norden, N., Daws, M.I., Antoine, C., Gonzalez, M.A., Garwood, N.C. and Chave, J. (2009) The relationship between seed mass and mean time to germination for 1037 tree species across five tropical forests. Functional Ecology 23, 203–210.Google Scholar
Olano, J.M., Caballero, I. and Escudero, A. (2012) Soil seed bank recovery occurs more rapidly than expected in semi-arid Mediterranean gypsum vegetation. Annals of Botany 109, 299–307.Google Scholar
Orme, D. (2013) The caper package: comparative analysis of phylogenetics and evolution in R. R package, version 5. http://CRAN.R-project.org/package=caper Google Scholar
Pagel, M. (1999) Inferring the historical patterns of biological evolution. Nature 401, 877–884.Google Scholar
Parmesan, C., Gaines, S., Gonzalez, L., Kaufman, D.M., Kingsolver, J., Townsend Peterson, A. and Sagarin, R. (2005) Empirical perspectives on species borders: from traditional biogeography to global change. Oikos 108, 58–75.Google Scholar
Philippi, T. and Seger, J. (1989) Hedging one's evolutionary bets, revisited. Trends in Ecology and Evolution 4, 41–44.Google Scholar
Poorter, H. and Nagel, O. (2000) The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review. Functional Plant Biology 27, 1191–1191.Google Scholar
Poorter, L. (2007) Are species adapted to their regeneration niche, adult niche, or both? The American Naturalist 169, 433–442.Google Scholar
Primack, R.B. (1979) Reproductive effort in annual and perennial species of Plantago (Plantaginaceae). The American Naturalist 114, 51–62.Google Scholar
Prinzing, A., Durka, W., Klotz, S. and Brandl, R. (2001) The niche of higher plants: evidence for phylogenetic conservatism. Proceedings of the Royal Society B: Biological Sciences 268, 2383–2389.Google Scholar
Qian, H. and Ricklefs, R.E. (2004) Geographical distribution and ecological conservatism of disjunct genera of vascular plants in eastern Asia and eastern North America. Journal of Ecology 92, 253–265.Google Scholar
R Core Team (2014) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Revell, L.J. (2010) Phylogenetic signal and linear regression on species data. Methods in Ecology and Evolution 1, 319–329.CrossRefGoogle Scholar
Roche, P., Diaz-Burlinson, N. and Gachet, S. (2004) Congruency analysis of species ranking based on leaf traits: which traits are the more reliable? Plant Ecology 174, 37–48.Google Scholar
Rosbakh, S. and Poschlod, P. (2014) Initial temperature of seed germination as related to species occurrence along a temperature gradient. Functional Ecology 29, 5–14.Google Scholar
Roumet, C., Urcelay, C. and Diaz, S. (2006) Suites of root traits differ between annual and perennial species growing in the field. New Phytologist 170, 357–368.Google Scholar
Royal Botanic Gardens, Kew (2014) Seed information database – version 7.1.Google Scholar
Rustad, L., Campbell, J., Marion, G., Norby, R., Mitchell, M., Hartley, A., Cornelissen, J. and Gurevitch, J. (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126, 543–562.Google Scholar
Saatkamp, A., Affre, L., Baumberger, T., Dumas, P.J., Gasmi, A., Gachet, S. and Arène, F. (2011a) Soil depth detection by seeds and diurnally fluctuating temperatures: different dynamics in 10 annual plants. Plant and Soil 349, 331–340.Google Scholar
Saatkamp, A., Affre, L., Dutoit, T. and Poschlod, P. (2011b) Germination traits explain soil seed persistence across species: the case of Mediterranean annual plants in cereal fields. Annals of Botany 107, 415.Google Scholar
Saatkamp, A., Poschlod, P. and Venable, D.L. (2014) The functional role of soil seed banks in natural communities. In Gallagher, R.S. (ed), Seeds – The Ecology of Regeneration in Plant Communities, pp. 263–294. Wallingford, UK: CABI Publishing.Google Scholar
Sack, L., Scoffoni, C., John, G.P., Poorter, H., Mason, C.M., Mendez-Alonzo, R. and Donovan, L.A. (2013) How do leaf veins influence the worldwide leaf economic spectrum? Review and synthesis. Journal of Experimental Botany 64, 4053–4080.Google Scholar
Salisbury, E.J. (1942) The Reproductive Capacity of Plants. London: Bell.Google Scholar
Sarukhan, J. and Harper, J.L. (1973) Studies on plant demography: Ranunculus repens L., R. bulbosus L. and R. acris L.: I. Population flux and survivorship. Journal of Ecology 61, 675–716.Google Scholar
Saverimuttu, T. and Westoby, M. (1996) Seedling longevity under deep shade in relation to seed size. Journal of Ecology 84, 681–689.Google Scholar
Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Schölkopf, B., Weigel, D. and Lohmann, J.U. (2005) A gene expression map of Arabidopsis thaliana development. Nature Genetics 37, 501–506.Google Scholar
Schnitzler, J., Graham, C.H., Dormann, C.F., Schiffers, K. and Peter Linder, H. (2012) Climatic niche evolution and species diversification in the Cape flora, South Africa. Journal of Biogeography 39, 2201–2211.Google Scholar
Silvertown, J., Araya, Y. and Gowing, D. (2015) Hydrological niches in terrestrial plant communities: a review. Journal of Ecology 103, 93–108.Google Scholar
Steinmaus, S.J., Prather, T.S. and Holt, J.S. (2000) Estimation of base temperatures for nine weed species. Journal of Experimental Botany 51, 275–275.Google Scholar
Thomas, H. (1990) Osmotic adjustment in Lolium perenne; its heritability and the nature of solute accumulation. Annals of Botany 66, 521–530.Google Scholar
Thompson, P.A. (1970a) Changes in germination responses of Silene secundiflora in relation to the climate of its habitat. Physiologia Plantarum 23, 739–746.Google Scholar
Thompson, P.A. (1970b) Germination of species of Caryophyllaceae in relation to their geographical distribution in Europe. Annals of Botany 34, 427–449.Google Scholar
Trudgill, D.L., Honek, A., Li, D. and Straalen, N.M. (2005) Thermal time-concepts and utility. Annals of Applied Biology 146, 1–14.Google Scholar
Tutin, T.G., Heywood, V.H., Valentine, D.H., Walters, S.M. and Webb, D.A. (1964) Flora Europaea. Cambridge, UK: Cambridge University Press.Google Scholar
Venable, D.L. (2007) Bet hedging in a guild of desert annuals. Ecology 88, 1086–1090.Google Scholar
Venable, D.L. and Brown, J.S. (1988) The selective interaction of dispersal, dormancy and seed size as adaptations for reducing risks in variable environments. American Naturalist 131, 360–384.Google Scholar
Wright, I.J., Reich, P.B., Westoby, M., Ackerly, D.D., Baruch, Z., Bongers, F., Cavender-Bares, J., Chapin, T., Cornelissen, J.H.C., Diemer, M., Flexas, J., Garnier, E., Groom, P.K., Gulias, J., Hikosaka, K., Lamont, B.B., Lee, T., Lee, W., Lusk, C., Midgley, J.J., Navas, M.L., Niinemets, U., Oleksyn, J., Osada, N., Poorter, H., Poot, P., Prior, L., Pyankov, V.I., Roumet, C., Thomas, S.C., Tjoelker, M.G., Veneklaas, E.J. and Villar, R. (2004) The worldwide leaf economics spectrum. Nature 428, 821–827.CrossRefGoogle ScholarPubMed
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