Global trends in phenotypic plasticity of plants.
climate change
climatic variability
latitude
meta-analysis
phenotypic plasticity
Journal
Ecology letters
ISSN: 1461-0248
Titre abrégé: Ecol Lett
Pays: England
ID NLM: 101121949
Informations de publication
Date de publication:
Oct 2021
Oct 2021
Historique:
revised:
26
01
2021
revised:
12
05
2021
received:
14
12
2020
accepted:
21
05
2021
pubmed:
4
7
2021
medline:
11
9
2021
entrez:
3
7
2021
Statut:
ppublish
Résumé
Predicting plastic responses is crucial to assess plant species potential to adapt to climate change, but little is known about which factors drive the biogeographical patterns of phenotypic plasticity in plants. Theory predicts that climatic variability would select for increased phenotypic plasticity, whereas evidence indicates that stressful conditions can limit phenotypic plasticity. Using a meta-analytic, phylogeny-corrected approach to global data on plant phenotypic plasticity, we tested whether latitude, climate, climatic variability and/or stressful conditions are predictors of plastic responses at a biogeographical scale. We found support for a positive association between phenotypic plasticity and climatic variability only for plasticity in allocation. Plasticity in leaf morphology, size and physiology were positively associated with mean annual temperature. We also found evidence that phenotypic plasticity in physiology is limited by cold stress. Overall, plant plastic responses to non-climatic factors were stronger than responses to climatic factors. However, while climatic conditions were associated with plant plastic responses to climatic factors, they generally did not relate to plastic responses to other abiotic or biotic factors. Our study highlights the need to consider those factors that favour and limit phenotypic plasticity in order to improve predictive frameworks addressing plant species' potential to adapt to climate change.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
2267-2281Informations de copyright
© 2021 John Wiley & Sons Ltd.
Références
Addo-Bediako, A., Chown, S.L. & Gaston, K.J. (2000) Thermal tolerance, climatic variability and latitude. Proceedings of the Royal Society of London. Series B: Biological Sciences, 267, 739-745.
Alpert, P. & Simms, E.L. (2002) The relative advantages of plasticity and fixity in different environments: when is it good for a plant to adjust? Evolutionary Ecology, 16, 285-297.
Araújo, M.B., Ferri-Yáñez, F., Bozinovic, F., Marquet, P.A., Valladares, F. & Chown, S.L. (2013) Heat freezes niche evolution. Ecology Letters, 16, 1206-1219.
Arnold, P.A., Nicotra, A.B. & Kruuk, L.E.B. (2019) Sparse evidence for selection on phenotypic plasticity in response to temperature. Philosophical Transactions of the Royal Society B: Biological Sciences, 374, 20180185.
Atkin, O.K., Loveys, B.R., Atkinson, L.J. & Pons, T.L. (2006a) Phenotypic plasticity and growth temperature: understanding interspecific variability. Journal of Experimental Botany, 57, 267-281.
Atkin, O.K., Scheurwater, I. & Pons, T.L. (2006b) High thermal acclimation potential of both photosynthesis and respiration in two lowland Plantago species in contrast to an alpine congeneric. Global Change Biology 12, 500-515.
Auld, J.R., Agrawal, A.A. & Relyea, R.A. (2010) Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proceedings of the Royal Society B: Biological Sciences, 277, 503-511.
Ballaré, C.L. (1999) Keeping up with the neighbours: phytochrome sensing and other signalling mechanisms. Trends in Plant Science, 4, 97-102.
Baythavong, B.S. (2011) Linking the spatial scale of environmental variation and the evolution of phenotypic plasticity: selection favors adaptive plasticity in fine-grained environments. The American Naturalist, 178, 75-87.
Berry, J. & Bjorkman, O. (1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology, 31, 491-543.
Blomberg, S.P., Garland, T. & Ives, A.R. (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution, 57, 717-745.
Borenstein, M., Hedges, L.V., Higgins, J.P.T. & Rothstein, H.R. (2009) Introduction to meta-analysis. John Wiley & Sons, Ltd, Chichester, West sussex, United Kingdom.
Botero, C.A., Weissing, F.J., Wright, J. & Rubenstein, D.R. (2015) Evolutionary tipping points in the capacity to adapt to environmental change. Proceedings of the National Academy of Sciences, 112, 184-189.
Bradshaw, A.D. & Hardwick, K. (1989) Evolution and stress-genotypic and phenotypic components. Biological Journal of the Linnean Society, 37, 137-155.
Callaway, R.M., Pennings, S.C. & Richards, C.L. (2003) Phenotypic plasticity and interactions among plants. Ecology, 84, 1115-1128.
Calosi, P., Bilton, D.T. & Spicer, J.I. (2008) Thermal tolerance, acclimatory capacity and vulnerability to global climate change. Biology Letters, 4, 99-102.
Campitelli, B.E., Des Marais, D.L. & Juenger, T.E. (2016) Ecological interactions and the fitness effect of water-use efficiency: competition and drought alter the impact of natural MPK12 alleles in Arabidopsis. Ecology Letters, 19, 424-434.
Carvajal, D.E., Loayza, A.P., Rios, R.S., Gianoli, E. & Squeo, F.A. (2017) Population variation in drought-resistance strategies in a desert shrub along an aridity gradient: Interplay between phenotypic plasticity and ecotypic differentiation. Perspectives in Plant Ecology, Evolution and Systematics, 29, 12-19.
Chagnon, P.-L., Brown, C., Stotz, G.C. & Cahill, J.F. (2018) Soil biotic quality lacks spatial structure and is positively associated with fertility in a northern grassland. Journal of Ecology, 106, 195-206.
Chapin, F.S. III, Autumn, K. & Pugnaire, F. (1993) Evolution of suites of traits in response to environmental stress. American Naturalist, 142, S78-S92.
Chevin, L.-M., Lande, R. & Mace, G.M. (2010) Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biology, 8, e1000357.
Crick, J.C. & Grime, J.P. (1987) Morphological plasticity and mineral nutrition capture in two herbaceous species of contrasted ecology. New Phytologist, 107, 403-414.
Davidson, A.M., Jennions, M. & Nicotra, A.B. (2011) Do invasive species show higher phenotypic plasticity than native species and if so, is it adaptive? A meta-analysis. Ecology Letters, 14, 419-431.
Davis, C.C., Willis, C.G., Primack, R.B. & Miller-Rushing, A.J. (2010) The importance of phylogeny to the study of phenological response to global climate change. Philosophical Transactions of the Royal Society B: Biological Sciences, 365, 3201-3213.
DeWitt, T.J., Sih, A. & Wilson, D.S. (1998) Costs and limits of phenotypic plasticity. Trends in Ecology & Evolution, 13, 77-81.
Dorn, L.A., Pyle, E.H. & Schmitt, J. (2000) Plasticity to light cues and resources in Arabidopsis thaliana: testing for adaptive value and costs. Evolution, 54, 1982-1994.
Dostál, P., Fischer, M. & Prati, D. (2016) Phenotypic plasticity is a negative, though weak, predictor of the commonness of 105 grassland species. Global Ecology and Biogeography, 25, 464-474.
Drake, J.E., Aspinwall, M.J., Pfautsch, S., Rymer, P.D., Reich, P.B., Smith, R.A. et al. (2015) The capacity to cope with climate warming declines from temperate to tropical latitudes in two widely distributed Eucalyptus species. Global Change Biology, 21, 459-472.
Easterling, D.R. (2000) Climate extremes: observations, modeling, and impacts. Science, 289, 2068-2074.
Emery, R.J.N., Chinnappa, C.C. & Chmielewski, J.G. (1994) Specialization, plant strategies, and phenotypic plasticity in populations of Stellaria longipes along an elevational gradient. International Journal of Plant Sciences, 155, 203-219.
Fick, S.E. & Hijmans, R.J. (2017) WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37, 4302-4315.
Frei, E.R., Ghazoul, J. & Pluess, A.R. (2014) Plastic responses to elevated temperature in low and high elevation populations of three grassland species. PLoS One, 9, e98677.
García-Verdugo, C., Granado-Yela, C., Manrique, E., de Casas, R.R. & Balaguer, L. (2009) Phenotypic plasticity and integration across the canopy of Olea europaea subsp. guanchica (Oleaceae) in populations with different wind exposures. American Journal of Botany, 96, 1454-1461.
Gaston, K.J. & Chown, S.L. (1999) Why Rapoport’s rule does not generalise. Oikos, 84, 309-312.
Ghalambor, C.K. (2006) Are mountain passes higher in the tropics? Janzen’s hypothesis revisited. Integrative and Comparative Biology, 46, 5-17.
Gianoli, E. (2003) Phenotypic responses of the twining vine Ipomoea purpurea (Convolvulaceae) to physical support availability in sun and shade. Plant Ecology, 165, 21-26.
Gianoli, E. (2004) Plasticity of traits and correlations in two populations of Convolvulus arvensis (Convolvulaceae) differing in environmental heterogeneity. International Journal of Plant Sciences 165, 825-832.
Gianoli, E. & González-Teuber, M. (2005) Environmental heterogeneity and population differentiation in plasticity to drought in Convolvulus chilensis (Convolvulaceae). Evolutionary Ecology, 19, 603-613.
Gianoli, E., Molina-Montenegro, M.A. & Becerra, J. (2007) Interactive effects of leaf damage, light intensity and support availability on chemical defenses and morphology of a twining vine. Journal of Chemical Ecology, 33, 95-103.
Gianoli, E. & Palacio-López, K. (2009) Phenotypic integration may constrain phenotypic plasticity in plants. Oikos, 118, 1924-1928.
Gianoli, E., Quezada, I.M. & Suárez, L.H. (2009) Leaf damage decreases fitness and constrains phenotypic plasticity to drought of a perennial herb. Acta Oecologica, 35, 752-757.
Gianoli, E. & Valladares, F. (2012) Studying phenotypic plasticity: the advantages of a broad approach. Biological Journal of the Linnean Society, 105, 1-7.
Godoy, O., Valladares, F. & Castro-Díez, P. (2012) The relative importance for plant invasiveness of trait means, and their plasticity and integration in a multivariate framework. New Phytologist, 195, 912-922.
Grassein, F., Till-Bottraud, I. & Lavorel, S. (2010) Plant resource-use strategies: the importance of phenotypic plasticity in response to a productivity gradient for two subalpine species. Annals of Botany, 106, 637-645.
Grime, J.P. (1974) Vegetation classification by reference to strategies. Nature, 250, 26-31.
Grime, J.P. (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. The American Naturalist, 111, 1169-1194.
Grime, J.P. & Mackey, J.M.L. (2002) The role of plasticity in resource capture by plants. Evolutionary Ecology, 16, 299-307.
Gugger, S., Kesselring, H., Stöcklin, J. & Hamann, E. (2015) Lower plasticity exhibited by high- versus mid-elevation species in their phenological responses to manipulated temperature and drought. Annals of Botany, 116, 953-962.
Gurevitch, J. & Hedges, L.V. (1993) Meta-analysis: combining the results of independent experiments. New York, NY: Chapman & Hall.
Harrell, F.E. (2001) Regression modeling strategies: with applications to linear models, logistic regression, and survival analysis. Springer Series in Statistics. New York, NY: Springer New York.
Harrell, F.E. (2020) rms: Regression Modeling Strategies. R package version. 6.0-1.
Harris, I., Osborn, T.J., Jones, P. & Lister, D. (2020) Version 4 of the CRU TS monthly high-resolution gridded multivariate climate dataset. Scientific Data, 7, 109.
Harvey, P.H., Read, A.F. & Nee, S. (1995) Why ecologists need to be phylogenetically challenged. Journal of Ecology, 83, 535-536.
Henn, J.J., Buzzard, V., Enquist, B.J., Halbritter, A.H., Klanderud, K., Maitner, B.S. et al. (2018) Intraspecific trait variation and phenotypic plasticity mediate alpine plant species response to climate change. Frontiers in Plant Science, 9, 1548.
Hijmans, R.J. (2020) raster: Geographic data analysis and modeling. R package version 3.1-5. https://CRAN.R-project.org/package=raster.
Hoffmann, A.A. & Sgrò, C.M. (2011) Climate change and evolutionary adaptation. Nature, 470, 479-485.
Hulshof, C.M., Violle, C., Spasojevic, M.J., McGill, B., Damschen, E., Harrison, S. et al. (2013) Intra-specific and inter-specific variation in specific leaf area reveal the importance of abiotic and biotic drivers of species diversity across elevation and latitude. Journal of Vegetation Science, 24, 921-931.
IPCC (2019). Climate Change and Land: an IPCC special report on climate change, desertification, land degradation, sustainable land management, food security, and greenhouse gas fluxes in terrestrial ecosystems. [P.R. Shukla, J. Skea, E. Calvo Buendia, V. Masson-Delmotte, H.-O. Pörtner, D. C. Roberts, P. Zhai, R. Slade, S. Connors, R. van Diemen, M. Ferrat, E. Haughey, S. Luz, S. Neogi, M. Pathak, J. Petzold, J. Portugal Pereira, P. Vyas, E. Huntley, K. Kissick, M. Belkacemi, J. Malley, (eds.)].
Jentsch, A., Kreyling, J. & Beierkuhnlein, C. (2007) A new generation of climate-change experiments: events, not trends. Frontiers in Ecology and the Environment, 5, 365-374.
Jump, A.S. & Peñuelas, J. (2005) Running to stand still: adaptation and the response of plants to rapid climate change. Ecology Letters, 8, 1010-1020.
Kahl, S.M., Lenhard, M. & Joshi, J. (2019) Compensatory mechanisms to climate change in the widely distributed species Silene vulgaris. Journal of Ecology, 107, 1918-1930.
Kawano, S. & Hara, T. (1995) Optimal balance between propagule output, propagule size, and cost of propagule production in plants with special reference to its evolutionary-ecological implications. Plant Species Biology, 10, 119-125.
Kembel, S.W. & Cahill, J.F. (2005) Plant phenotypic plasticity belowground: a phylogenetic perspective on root foraging trade-offs. American Naturalist, 166, 216-230.
Koricheva, J., Gurevitch, J. & Mengersen, K. (2013) Handbook of meta-analysis in ecology and evolution. Princeton, NJ: Princeton University Press.
Krouk, G., Tranchina, D., Lejay, L., Cruikshank, A.A., Shasha, D., Coruzzi, G.M. et al. (2009) A systems approach uncovers restrictions for signal interactions regulating genome-wide responses to nutritional cues in Arabidopsis. PLoS Computational Biology, 5, e1000326.
Larigauderie, A. & Körner, C. (1995) Acclimation of leaf dark respiration to temperature in alpine and lowland plant species. Annals of Botany, 76, 245-252.
Lázaro-Nogal, A., Matesanz, S., Godoy, A., Pérez-Trautman, F., Gianoli, E. & Valladares, F. (2015) Environmental heterogeneity leads to higher plasticity in dry-edge populations of a semi-arid Chilean shrub: insights into climate change responses. Journal of Ecology, 103, 338-350.
Liefting, M., Hoffmann, A.A. & Ellers, J. (2009) Plasticity versus environmental canalization: population differences in thermal responses along a latitudinal gradient in Drosophila serrata. Evolution, 63, 1954-1963.
Lortie, C.J. & Aarssen, L.W. (1996) The specialization hypothesis for phenotypic plasticity in plants. International Journal of Plant Sciences, 157, 484-487.
Lorts, C.M. & Lasky, J.R. (2020) Competition × drought interactions change phenotypic plasticity and the direction of selection on Arabidopsis traits. New Phytologist, https://doi.org/10.1111/nph.16593.
Matesanz, S., Gianoli, E. & Valladares, F. (2010) Global change and the evolution of phenotypic plasticity in plants. Annals of the New York Academy of Sciences, 1206, 35-55.
McGill, B.J. (2019) The what, how and why of doing macroecology. Global Ecology and Biogeography, 28, 6-17.
McKitrick, M.C. (1993) Phylogenetic constraint in evolutionary theory: has it any explanatory power? Annual Review of Ecology Evolution and Systematics, 24, 307-330.
Moles, A.T., Perkins, S.E., Laffan, S.W., Flores-Moreno, H., Awasthy, M., Tindall, M.L. et al. (2014) Which is a better predictor of plant traits: temperature or precipitation? Journal of Vegetation Science, 25, 1167-1180.
Molina-Montenegro, M.A., Atala, C. & Gianoli, E. (2010) Phenotypic plasticity and performance of Taraxacum officinale (dandelion) in habitats of contrasting environmental heterogeneity. Biological Invasions, 12, 2277-2284.
Molina-Montenegro, M.A. & Naya, D.E. (2012) Latitudinal patterns in phenotypic plasticity and fitness-related traits: assessing the Climatic Variability Hypothesis (CVH) with an invasive plant species. PLoS One, 7, e47620.
Morel-Journel, T., Thuillier, V., Pennekamp, F., Laurent, E., Legrand, D., Chaine, A.S. et al. (2020) A multidimensional approach to the expression of phenotypic plasticity. Functional Ecology, 34, 2338-2349.
Murren, C.J., Auld, J.R., Callahan, H., Ghalambor, C.K., Handelsman, C.A., Heskel, M.A. et al. (2015) Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity. Heredity, 115, 293-301.
Naya, D.E., Spangenberg, L., Naya, H. & Bozinovic, F. (2012) Latitudinal patterns in rodent metabolic flexibility. American Naturalist, 179, E172-E179.
Nicotra, A.B., Atkin, O.K., Bonser, S.P., Davidson, A.M., Finnegan, E.J., Mathesius, U. et al. (2010) Plant phenotypic plasticity in a changing climate. Trends in Plant Science, 15, 684-692.
Nicotra, A.B., Segal, D.L., Hoyle, G.L., Schrey, A.W., Verhoeven, K.J.F. & Richards, C.L. (2015) Adaptive plasticity and epigenetic variation in response to warming in an Alpine plant. Ecology and Evolution, 5, 634-647.
Paradis, E. & Schliep, K. (2019) ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinfomatics, 35, 526-528.
Pierik, R., Cuppens, M.L.C., Voesenek, L.A.C.J. & Visser, E.J.W. (2004) Interactions between ethylene and gibberellins in phytochrome-mediated shade avoidance responses in Tobacco. Plant Physiology, 136, 2928-2936.
Pigliucci, M. (2001) Phenotypic plasticity: beyond nature and nurture. Baltimore, MD: The Johns Hopkins University Press.
Pigliucci, M., Cammell, K. & Schmitt, J. (1999) Evolution of phenotypic plasticity a comparative approach in the phylogenetic neighbourhood of Arabidopsis thaliana. Journal of Evolutionary Biology, 12, 779-791.
Portsmuth, A. & Niinemets, Ü. (2007) Structural and physiological plasticity in response to light and nutrients in five temperate deciduous woody species of contrasting shade tolerance. Functional Ecology, 21, 61-77.
Power, S.C., Verboom, G.A., Bond, W.J. & Cramer, M.D. (2019) Does a tradeoff between trait plasticity and resource conservatism contribute to the maintenance of alternative stable states? New Phytologist, 223, 1809-1819.
Pugnaire, F. & Valladares, F. (2007) Functional plant ecology, 2nd ed. Bocca Raton, USA: Taylor and Francis Group.
Qian, H. & Jin, Y. (2016) An updated megaphylogeny of plants, a tool for generating plant phylogenies and an analysis of phylogenetic community structure. Journal of Plant Ecology, 9, 233-239.
R Core Team (2019) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
Reed, T.E., Waples, R.S., Schindler, D.E., Hard, J.J. & Kinnison, M.T. (2010) Phenotypic plasticity and population viability: the importance of environmental predictability. Proceedings of the Royal Society B: Biological Sciences, 277, 3391-3400.
Reich, P.B. (2014) The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto. Journal of Ecology, 102, 275-301.
Reich, P.B. & Oleksyn, J. (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. PNAS, 101, 11001-11006.
Ren, L., Guo, X., Liu, S., Yu, T., Guo, W., Wang, R. et al. (2020) Intraspecific variation in Phragmites australis: Clinal adaptation of functional traits and phenotypic plasticity vary with latitude of origin. Journal of Ecology, 108, 2531-2543.
Revell, L.J. (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217-223.
Reynolds, H.L. & D’Antonio, C. (1996) The ecological significance of plasticity in root weight ratio in response to nitrogen: Opinion. Plant and Soil, 185, 75-97.
Rezende, E.L., Bozinovic, F. & Garland, T. (2004) Climatic adaptation and the evolution of baal and maximum rates of metabolism in rodents. Evolution, 58, 1361-1374.
Richards, C.L., Bossdorf, O., Muth, N.Z., Gurevitch, J. & Pigliucci, M. (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecology Letters, 9, 981-993.
Rios, R.S., Salgado-Luarte, C. & Gianoli, E. (2014) Species divergence and phylogenetic variation of ecophysiological traits in lianas and trees. PLoS One, 9, e99871.
Salgado-Luarte, C. & Gianoli, E. (2011) Herbivory may modify functional responses to shade in seedlings of a light-demanding tree species. Functional Ecology, 25, 492-499.
Sánchez-Gómez, D., Valladares, F. & Zavala, M.A. (2006) Performance of seedlings of Mediterranean woody species under experimental gradients of irradiance and water availability: trade-offs and evidence for niche differentiation. New Phytologist, 170, 795-806.
Scheepens, J.F., Deng, Y. & Bossdorf, O. (2018) Phenotypic plasticity in response to temperature fluctuations is genetically variable, and relates to climatic variability of origin, in Arabidopsis thaliana. AoB Plants, 10, ply043.
Schlichting, C.D. (1986) The evolution of phenotypic plasticity in plants. Annual Review of Ecology Evolution and Systematics, 17, 667-693.
Schlichting, C.D. (1989) Phenotypic plasticity in Phlox. II. Plasticity of character correlations. Oecologia, 78, 496-501.
Schmid, S.F., Stöcklin, J., Hamann, E. & Kesselring, H. (2017) High-elevation plants have reduced plasticity in flowering time in response to warming compared to low-elevation congeners. Basic and Applied Ecology, 21, 1-12.
Schwartz, M.W. (2012) Using niche models with climate projections to inform conservation management decisions. Biological Conservation, 155, 149-156.
Seal, C.E., Daws, M.I., Flores, J., Ortega-Baes, P., Galíndez, G., León-Lobos, P. et al. (2017) Thermal buffering capacity of the germination phenotype across the environmental envelope of the Cactaceae. Global Change Biology, 23, 5309-5317.
Sentinella, A.T., Warton, D.I., Sherwin, W.B., Offord, C.A. & Moles, A.T. (2020) Tropical plants do not have narrower temperature tolerances, but are more at risk from warming because they are close to their upper thermal limits. Global Ecology and Biogeography, 29, 1387-1398.
Steinger, T., Roy, B.A. & Stanton, M.L. (2003) Evolution in stressful environments II: adaptive value and costs of plasticity in response to low light in Sinapis arvensis. Journal of Evolutionary Biology, 16, 313-323.
Stevens, G.C. (1989) The latitudinal gradient in geographical range: how so many species coexist in the tropics. American Naturalist, 133, 240-256.
Sultan, S.E. (2000) Phenotypic plasticity for plant development, function and life history. Trends in Plant Science, 5, 537-542.
Sultan, S.E. (2001) Phenotypic plasticity for fitness components in Polygonum species of contrasting ecological breadth. Ecology, 82, 328-343.
Sunday, J.M., Bates, A.E. & Dulvy, N.K. (2011) Global analysis of thermal tolerance and latitude in ectotherms. Proceedings of the Royal Society B: Biological Sciences, 278, 1823-1830.
Thompson, R.M., Beardall, J., Beringer, J., Grace, M. & Sardina, P. (2013) Means and extremes: building variability into community-level climate change experiments. Ecology Letters, 16, 799-806.
Tjoelker, M.G., Oleksyn, J., Lorenc-Plucinska, G. & Reich, P.B. (2009) Acclimation of respiratory temperature responses in northern and southern populations of Pinus banksiana. New Phytologist, 181, 218-229.
Valladares, F., Gianoli, E. & Gómez, J.M. (2007) Ecological limits to plant phenotypic plasticity. New Phytologist, 176, 749-763.
Valladares, F. & Guzmán, B. (2006) Canopy structure and spatial heterogeneity of understory light in an abandoned Holm oak woodland. Annals of Forest Science, 63, 749-761.
Valladares, F., Matesanz, S., Guilhaumon, F., Araújo, M.B., Balaguer, L., Benito-Garzón, M. et al. (2014) The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecology Letters, 17, 1351-1364.
Valladares, F., Wright, S.J., Lasso, E., Kitajima, K. & Pearcy, R.W. (2000) Plastic phenotypic response to light of 16 congeneric shrubs from a panamanian rainforest. Ecology, 81, 1925-1936.
Van Buskirk, J. & Steiner, U.K. (2009) The fitness costs of developmental canalization and plasticity. Journal of Evolutionary Biology, 22, 852-860.
van Kleunen, M. & Fischer, M. (2005) Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytologist, 166, 49-60.
van Kleunen, M., Fischer, M. & Schmid, B. (2000) Costs of plasticity in foraging characteristics of the clonal plant Ranunculus reptans. Evolution, 54, 1947-1955.
van Ommen Kloeke, A.E.E., Douma, J.C., Ordoñez, J.C., Reich, P.B. & van Bodegom, P.M. (2012) Global quantification of contrasting leaf life span strategies for deciduous and evergreen species in response to environmental conditions. Global Ecology and Biogeography, 21, 224-235.
Vázquez, D.P., Gianoli, E., Morris, W.F. & Bozinovic, F. (2017) Ecological and evolutionary impacts of changing climatic variability. Biological Reviews, 92, 22-42.
Vázquez, D.P. & Stevens, R.D. (2004) The latitudinal gradient in niche breadth: concepts and evidence. American Naturalist, 164, E1-E19.
Veihmeyer, F.J. & Hendrickson, A.H. (1950) Soil moisture in relation to plant growth. Annual Review of Plant Physiology, 1, 285-304.
Viechtbauer, W. (2010) Conducting meta-analyses in R with the metafor package. Journal of Statistical Software, 36, 1-48.
Visser, M.E. (2008) Keeping up with a warming world; assessing the rate of adaptation to climate change. Proceedings of the Royal Society B: Biological Sciences, 275, 649-659.
Vitasse, Y., Hoch, G., Randin, C.F., Lenz, A., Kollas, C., Scheepens, J.F. et al. (2013) Elevational adaptation and plasticity in seedling phenology of temperate deciduous tree species. Oecologia, 171, 663-678.
Voesenek, L.A.C.J., Rijnders, J.H.G.M., Peeters, A.J.M., van de Steeg, H.M. & de Kroon, H. (2004) Plant hormones regulate fast shoot elongation under water: from genes to communities. Ecology, 85, 16-27.
Waitt, D.E. & Levin, D.A. (1993) Phenotypic integration and plastic correlations in Phlox drummondii (Polemoniaceae). American Journal of Botany, 80, 1224-1233.
Wang, M.-Z., Bu, X.-Q., Li, L., Dong, B.-C., Li, H.-L. & Yu, F.-H. (2018) Constraints on the evolution of phenotypic plasticity in the clonal plant Hydrocotyle vulgaris. Journal of Evolutionary Biology, 31, 1006-1017.
Weinig, C. (2000) Limits to adaptive plasticity: temperature and photoperiod influence shade-avoidance responses. American Journal of Botany, 87, 1660-1668.
Went, F.W. (1953) The effect of temperature on plant growth. Annual Review of Plant Physiology, 4, 347-362.
Wright, I.J., Reich, P.B., Westoby, M., Ackerly, D.D., Baruch, Z., Bongers, F. et al. (2004) The worldwide leaf economics spectrum. Nature, 428, 821-827.