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Facilitation promotes changes in leaf economics traits of a perennial forb

Abstract

Optimal allocation of resources is crucial to maximize plant success. Plants modify their economic strategies by adjusting functional traits in response to shifts in environmental conditions. Facilitation has been recognized as a major biotic filter of trait distribution in communities, although the effect of facilitation on intraspecific variability has been scarcely explored. We evaluated intraspecific shifts in leaf functional traits of a perennial forb (Helleborus foetidus) in relation to the presence of a nurse plant (Juniperus sabina) in two sites with contrasting abiotic stress levels. The effects of abiotic (site) and biotic (juniper presence, microsite) environments on specific leaf area (SLA), leaf area (LA), lamina/petiole length ratio (LPR), intrinsic water use efficiency (iWUE) and leaf nutrient content (N, P and N:P) per mass were evaluated. Alleviation of drought stress associated with nurse plant presence was reflected in SLA, LA, LPR and iWUE at the high-stress site. Individuals growing in open areas showed more resource-conservative traits, supporting the argument that this strategy is advantageous in environments that limit opportunities for rapid carbon gain. Leaf nutrients were unrelated to other traits. The large amount of intraspecific variation in leaf functional traits related to facilitative processes highlights the importance of facilitation as a major source of plant trait variation. Both positive and negative biotic interactions, as well as intraspecific trait variability, should be considered in mechanistic models of plant communities’ functional responses to environmental changes.

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References

  1. Ackerly DD, Dudley SA, Sultan SE, Schmitt J, Coleman JS, Linder CR, Sandquist DR, Geber MA, Evans AS, Dawson TE, Lechowicz MJ (2000) The evolution of plant ecophysiological traits: recent advances and future directions. Bioscience 50:979–995. doi:10.1641/0006-3568(2000)050[0979:TEOPET]2.0.CO;2

  2. Adler D (2005) vioplot: violin plot. R package version 0.2

  3. Adler PB, Fajardo A, Kleinhesselink AR, Kraft NJB (2013) Trait-based tests of coexistence mechanisms. Ecol Lett 16:1294–1306. doi:10.1111/ele.12157

  4. Aerts R, Chapin FSIII (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67. doi:10.1016/S0065-2504(08)60016-1

  5. Albert CH, Thuiller W, Yoccoz NG, Douzet R, Aubert S, Lavorel S (2010a) A multi-trait approach reveals the structure and the relative importance of intra- vs. interspecific variability in plant traits. Funct Ecol 24:1192–1201. doi:10.1111/j.1365-2435.2010.01727.x

  6. Albert CH, Thuiller W, Yoccoz NG, Soudant A, Boucher F, Saccone P, Lavorel S (2010b) Intraspecific functional variability: extent, structure and sources of variation. J Ecol 98:604–613. doi:10.1111/j.1365-2745.2010.01651.x

  7. Auger S, Shipley B (2013) Inter-specific and intra-specific trait variation along short environmental gradients in an old-growth temperate forest. J Veg Sci 24:419–428. doi:10.1111/j.1654-1103.2012.01473.x

  8. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300. doi:10.2307/2346101

  9. Bertness MD, Callaway RM (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193. doi:10.1016/0169-5347(94)90088-4

  10. Bloom AJ, Chapin FSIII, Mooney HA (1985) Resource limitation in plants—an economic analogy. Annu Rev Ecol Syst 16:363–392. doi:10.1146/annurev.es.16.110185.002051

  11. Boucher FC, Thuiller W, Arnoldi C, Albert CH, Lavergne S (2013) Unravelling the architecture of functional variability in wild populations of Polygonum viviparum L. Funct Ecol 27:382–391. doi:10.1111/1365-2435.12034

  12. Brooker RW, Callaghan TV (1998) The balance between positive and negative plant interactions and its relationship to environmental gradients: a model. Oikos 81:196–207. doi:10.2307/3546481

  13. Brooker RW, Maestre FT, Callaway RM, Lortie CL, Cavieres LA, Kunstler G, Liancourt P, Tielbörger K, Travis JMJ, Anthelme F, Armas C, Coll L, Corcket E, Delzon S, Forey E, Kikvidze Z, Olofsson J, Pugnaire F, Quiroz CL, Saccone P, Schiffers K, Seifan M, Touzard B, Michalet R (2008) Facilitation in plant communities: the past, the present, and the future. J Ecol 96:18–34. doi:10.1111/j.1365-2745.2007.01295.x

  14. Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125. doi:10.1016/S0169-5347(02)00045-9

  15. Butterfield BJ, Briggs JM (2011) Regeneration niche differentiates functional strategies of desert woody plant species. Oecologia 165:477–487. doi:10.1007/s00442-010-1741-y

  16. Butterfield BJ, Callaway RM (2013) A functional comparative approach to facilitation and its context dependence. Funct Ecol 27:907–917. doi:10.1111/1365-2435.12019

  17. Callaway RM (1995) Positive interactions among plants. Bot Rev 61:306–349. doi:10.1007/BF02912621

  18. Callaway RM, Walker LR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78:1958–1965. doi:10.1890/0012-9658(1997)078[1958:CAFASA]2.0.CO;2

  19. Carlucci MB, Debastiani VJ, Pillar VD, Duarte LDS (2015) Between- and within-species trait variability and the assembly of sapling communities in forest patches. J Veg Sci 26:21–31. doi:10.1111/jvs.12223

  20. Cornwell WK, Ackerly DD (2009) Community assembly and shifts in plant trait distributions across an environmental gradient in coastal California. Ecol Monogr 79:109–126. doi:10.1890/07-1134.1

  21. Cornwell WK, Schwilk DW, Ackerly DD (2006) A trait-based test for habitat filtering: convex hull volume. Ecology 87:1465–1471. doi:10.1890/0012-9658(2006)87[1465:ATTFHF]2.0.CO;2

  22. Delgado-Baquerizo M, Maestre FT, Gallardo A, Bowker MA, Wallenstein M, Quero JL, Soliveres S, Ochoa V, Gozalo B, García-Gómez M, García-Palacios P, Berdugo M, Valencia E, Escolar C, Escudero A, Carreira JA, Arredondo T, Barraza-Zepeda C, Bran D, Chaieb M, Conceição AA, Contreras J, Derak M, Eldridge DJ, Espinosa CI, Florentino A, Gaitán J, Ghiloufi W, Gómez-González S, Gutiérrez JR, Hepper E, Hernández RM, Huber-Sannwald E, Jankju M, Liu J, Mau RL, Miriti M, Monerris J, Morici E, Muchane M, Naseri K, Ospina A, Polo V, Pucheta E, Quevedo-Robledo L, Ramírez E, Ramírez-Collantes DA, Romão R, Tighe M, Torres D, Torres-Díaz C, Ungar ED, Val J, Wamiti W, Wang D, Zaady E (2013) Decoupling of soil nutrient cycles as a function of aridity in global drylands. Nature 502:672–676. doi:10.1038/nature12670

  23. Díaz S, Hodgson JC, Thompson K, Cabido M, Cornelissen JHC, Jalili A, Montserrat-Martí G, Grime JP, Zarrinkamar F, Asri Y, Band SR, Basconcelo S, Castro-Díez P, Funes G, Hamzehee B, Khoshnevi M, Pérez-Harguindeguy N, Pérez-Rontomé MC, Shirvany FA, Vendramini F, Yazdani S, Abbas-Azimi R, Bogaard A, Boustani S, Charles M, Dehghan M, de Torres-Espuny L, Falczuk V, Guerrero-Campo J, Hynd A, Jones G, Kowsary E, Kazemi-Saeed F, Maestro-Martínez M, Romo-Díez A, Shaw S, Siavash B, Villar-Salvador P, Zak MR (2004) The plant traits that drive ecosystems. Evidence from three continents. J Veg Sci 15:295–304. doi:10.1111/j.1654-1103.2004.tb02266.x

  24. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19. doi:10.1007/BF00377192

  25. Fajardo A, McIntire EJB (2011) Under strong niche overlap conspecifics do not compete but help each other to survive: facilitation at the intraspecific level. J Ecol 99:642–650. doi:10.1111/j.1365-2745.2010.01771.x

  26. Fajardo A, Piper F (2011) Intraspecific trait variation and covariation in a widespread tree species (Nothofagus pumilio) in southern Chile. New Phytol 189:259–271. doi:10.1111/j.1469-8137.2010.03468.x

  27. Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Aust J Plant Physiol 11:539–552. doi:10.1071/PP9840539

  28. Farquhar GD, O’Leary HM, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9:121–137

  29. Ferrio JP, Voltas J (2005) Carbon and oxygen isotope ratios in wood constituents of Pinus halepensis as indicators of precipitation, temperature and vapor pressure deficit. Tellus B 57:164–173. doi:10.1111/j.1600-0889.2005.00137.x

  30. Font Quer P (1993) Plantas medicinales: el dioscórides renovado, 10th edn. Peninsula, Barcelona

  31. Fortunel C, Fine PVA, Baraloto C (2012) Leaf, stem and root tissue strategies across 758 Neotropical tree species. Funct Ecol 26:1153–1161. doi:10.1111/j.1365-2435.2012.02020.x

  32. García-Cervigón AI, Olano JM, Eugenio M, Camarero JJ (2012) Arboreal and prostrate conifers coexisting in Mediterranean high mountains differ in their climatic responses. Dendrochronologia 30:279–286. doi:10.1016/j.dendro.2012.02.004

  33. García-Cervigón AI, Gazol A, Sanz V, Camarero JJ, Olano JM (2013) Intraspecific competition replaces interspecific facilitation as abiotic stress decreases: the shifting nature of plant-plant interactions. Perspect Plant Ecol Evol Syst 15:226–236. doi:10.1016/j.ppees.2013.04.001

  34. Gross N, Kunstler G, Liancourt P, de Bello F, Suding KN, Lavorel S (2009) Linking individual response to biotic interactions with community structure: a trait-based approach. Funct Ecol 23:1167–1178. doi:10.1111/j.1365-2435.2009.01591.x

  35. Gross N, Börger L, Soriano-Morales SI, Le Bagousse-Pinguet Y, Quero JL, García-Gómez M, Valencia-Gómez E, Maestre FT (2013) Uncovering multiscale effects of aridity and biotic interactions on the functional structure of Mediterranean shrublands. J Ecol 101:637–649. doi:10.1111/1365-2745.12063

  36. He Q, Bertness MD, Altieri AH (2013) Global shifts towards positive species interactions with increasing environmental stress. Ecol Lett 16:695–706. doi:10.1111/ele.12080

  37. Herrera CM, Medrano M, Rey PJ, Sánchez-Lafuente AM, García MB, Guitián J, Manzaneda AJ (2002) Interaction of pollinators and herbivores on plant fitness suggests a pathway for correlated evolution of mutualism- and antagonism-related traits. Proc Natl Acad Sci USA 99:16823–16828 10.1073ypnas.252362799

  38. Holmgren M, Scheffer M, Huston MA (1997) The interplay of facilitation and competition in plant communities. Ecology 78:1966–1975. doi:10.1890/0012-9658(1997)078[1966:TIOFAC]2.0.CO;2

  39. Hulshof CM, Swenson NG (2010) Variation in leaf functional trait values within and across individuals and species: an example from a Costa Rican dry forest. Funct Ecol 24:217–223. doi:10.1111/j.1365-2435.2009.01614.x

  40. Jackson BG, Peltzer DA, Wardle DA (2013) The within-species leaf economic spectrum does not predict leaf litter decomposability at either the within-species or whole community levels. J Ecol 101:1409–1419. doi:10.1111/1365-2745.12155

  41. Jacob L, Lawlor DW (1992) Dependence of photosynthesis of sunflower and maize leaves on phosphate supply, ribulose-l,5-biphosphate carboxylase/oxygenase activity, and ribulose-l,5-biphosphate pool size. Plant Physiol. 98:801–807. doi:10.1104/pp.98.3.801

  42. Jung V, Violle C, Mondy C, Hoffmann L, Muller S (2010) Intraspecific variability and trait-based community assembly. J Ecol 98:1134–1140. doi:10.1111/j.1365-2745.2010.01687.x

  43. Kichenin E, Wardle DA, Peltzer DA, Morse CW, Freschet GT (2013) Contrasting effects of plant inter- and intraspecific variation on community-level trait measures along an environmental gradient. Funct Ecol 27:1254–1261. doi:10.1111/1365-2435.12116

  44. Koch GW, Sillett SC, Jennings GM, Davis SD (2004) The limits to tree height. Nature 428:851–854. doi:10.1038/nature02417

  45. Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450. doi:10.2307/2404783

  46. Laforest-Lapointe I, Martínez-Vilalta J, Retana J (2014) Intraspecific variability in functional traits matters: case study of Scots pine. Oecologia 175:1337–1348. doi:10.1007/s00442-014-2967-x

  47. Lamont BB, Groom PK, Cowling RM (2002) High leaf mass per area of related species assemblages may reflect low rainfall and carbon isotope discrimination rather than low phosphorus and nitrogen concentrations. Funct Ecol 16:403–412. doi:10.1046/j.1365-2435.2002.00631.x

  48. Legendre P, Legendre L (2012) Numerical ecology, 3rd edn. Elsevier, Amsterdam

  49. Lenth RV, Hervé M (2014) lsmeans: least-squares means. R Package version 2:13

  50. Linares JC, Camarero JJ (2011) From pattern to process: linking intrinsic water use efficiency to drought-induced forest decline. Glob Chang Biol 18:1000–1015. doi:10.1111/j.1365-2486.2011.02566.x

  51. Linares JC, Covelo F, Carreira JA, Merino J (2012) Phenological and wáter-use patterns underlying maximum growing season length at the highest elevations: implications under climate change. Tree Physiol 32:161–170. doi:10.1093/treephys/tps003

  52. López González G (2004) Guía de los árboles y arbustos de la Península Ibérica y Baleares, 2nd edn. Mundi Prensa, Madrid

  53. Lortie CJ, Brooker RW, Choler P, Kikvidze Z, Michalet R, Pugnaire FI, Callaway RM (2004) Rethinking plant community theory. Oikos 107:433–438. doi:10.1111/j.0030-1299.2004.13250.x

  54. Maestre FT, Callaway RM, Valladares F, Lortie CJ (2009) Refining the stress gradient hypothesis for competition and facilitation in plant communities. J Ecol 97:199–205. doi:10.1111/j.1365-2745.2008.01476.x

  55. Martínez-Vilalta J, Mencuccini M, Vayreda J, Retana J (2010) Interspecific variation in functional traits, non climatic differences among species ranges, determines demographic rates across 44 temperate and Mediterranean tree species. J Ecol 98:1462–1475. doi:10.1111/j.1365-2745.2010.01718.x

  56. McCarroll D, Loader NJ (2004) Stable isotopes in tree rings. Quat Sci Rev 23:771–801. doi:10.1016/j.quascirev.2003.06.017

  57. McIntire EJB, Fajardo A (2014) Facilitation as a ubiquitous driver of biodiversity. New Phytol 201:403–416. doi:10.1111/nph.12478

  58. Messier J, McGill BJ, Lechowicz MJ (2010) How do traits vary across ecological scales? A case for trait-based ecology. Ecol Lett 13:838–848. doi:10.1111/j.1461-0248.2010.01476.x

  59. Miriti MN (2006) Ontogenetic shift from facilitation to competition in a desert shrub. J Ecol 94:973–979. doi:10.1111/j.1365-2745.2006.01138.x

  60. Montane F, Romanya J, Rovira P, Casals P (2010) Aboveground litter quality changes may drive soil organic carbon increase after shrub encroachment into mountain grasslands. Plant Soil 337:151–165. doi:10.1007/s11104-010-0512-1

  61. Moreno-Gutiérrez C, Dawson TE, Nicolás E, Querejeta JI (2012) Isotopes reveal contrasting water use strategies among coexisting plant species in a Mediterranean ecosystem. New Phytol 196:489–496. doi:10.1111/j.1469-8137.2012.04276.x

  62. Murphy KL, Klopatek JM, Klopatek CC (1998) The effects of litter quality and climate on decomposition along an elevational gradient. Ecol Appl 8:1061–1071. doi:10.1890/1051-0761(1998)008[1061:TEOLQA]2.0.CO;2

  63. Nieto G (1986) Helleborus foetidus. In: Castroviejo S, Lainz M, López González G, Montserrat P, Muñoz Garmendia F, Paiva J, Villar L (eds) Flora Iberica vol. I. Lycopodiaceae-Papaveraceae. Real Jardín Botánico-CSIC, Madrid, pp 217–218

  64. Ninyerola M, Pons X, Roure JM (2005) Atlas climático digital de la Península Iberica. Metodología y aplicaciones en bioclimatología y geobotánica, 1st edn. Universidad Autónoma de Barcelona, Bellaterra

  65. Núñez C, Raffaele E, Núñez MA, Cuassolo F (2009) When do nurse plants stop nursing? Temporal changes in water stress levels in Austrocedrus chilensis growing within and outside shrubs. J Veg Sci 20:1064–1071. doi:10.1111/j.1654-1103.2009.01107.x

  66. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2012) Vegan: community ecology package. R package version 2.0-9

  67. Olano JM, Almería I, Eugenio M, von Arx G (2013) Under pressure: how a Mediterranean high-mountain forb coordinates growth and hydraulic xylem anatomy in response to temperature and water constraints. Funct Ecol 27:1295–1303. doi:10.1111/1365-2435.12144

  68. Olano JM, Linares JC, García-Cervigón AI, Arzac A, Delgado A, Rozas V (2014) Drought-induced increase in water use efficiency reduces tree secondary growth and tracheid wall thickness in a Mediterranean conifer. Oecologia 176:273–283. doi:10.1007/s0042-014-2989-4

  69. Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circ 939:1–19

  70. Page AL (1982) Methods of soil analysis. Part 2. Chemical and microbiological properties, 2nd edn. American Society of Agronomy, Madison

  71. Pinheiro J, Bates D, DebRoy S, Sarkar D, the R Development Core Team (2011) nlme: linear and nonlinear mixed effects models. R package version 3.1-109

  72. Poorter L (2009) Leaf traits show different relationships with shade tolerance in moist versus dry tropical forests. New Phytol 181:890–900. doi:10.1111/j.1469-8137.2008.02715.x

  73. Poorter L, Bongers F (2006) Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology 87:1733–1743. doi:10.1890/0012-9658(2006)87[1733:LTAGPO]2.0.CO;2

  74. Poorter L, Wright SJ, Paz H, Ackerly DD, Condit R, Ibarra-Manríquez G, Harms KE, Licona JC, Martínez-Ramos M, Mazer SJ, Muller-Landau HC, Peña-Claros M, Webb CO, Wright IJ (2008) Are functional traits good predictors of demographic rates? Evidence from five Neotropical forests. Ecology 89:1908–1920. doi:10.1890/07-0207.1

  75. Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588. doi:10.1111/j.1469-8137.2009.02830.x

  76. Porta J, López-Acevedo M, Rodríguez R (1986) Técnicas y experimentos en edafología, 1st edn. Col legi Oficial d’Enginyers Agrònoms de Catalunya, Barcelona

  77. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  78. Reich PB, Ellsworth DS, Uhl C (1995) Leaf carbon and nutrient assimilation and conservation in species of differing successional status in an oligotrophic Amazonian forest. Funct Ecol 9:65–76. doi:10.2307/2390092

  79. Reich PB, Oleksyn J, Wright I (2009) Leaf phosphorous influences the photosynthesis-nitrogen relation: a cross-biome analysis of 314 species. Oecologia 160:207–212. doi:10.1007/s00442-009-1291-3

  80. Roche P, Díaz-Burlinson N, Gachet S (2004) Congruency analysis of species ranking based on leaf traits: which traits are the more reliable? Plant Ecol 174:37–48. doi:10.1023/B:VEGE.0000046056.94523.57

  81. Roy J, Albert CH, Choler P, Clément JC, Ibanez S, Lavergne S, Saccone P, Zinger L, Geremia RA (2013) Microbes on the cliff: alpine cushion plants structure bacterial and fungal communities. Front Microbiol 4:64. doi:10.3389/fmicb.2013.00064

  82. Rüger N, Wirth C, Wright SJ, Condit R (2012) Functional traits explain light and size response of growth rates in tropical tree species. Ecology 93:2626–2636. doi:10.1890/12-0622.1

  83. Schöb C, Butterfield BJ, Pugnaire FI (2012) Foundation species influence trait-based community assembly. New Phytol 196:835–844. doi:10.1111/j.1469-8137.2012.04306.x

  84. Shipley B, Vile D, Garnier E, Wright IJ, Poorter H (2005) Functional linkages between leaf traits and net photosynthetic rate: reconciling empirical and mechanistic models. Funct Ecol 19:602–615. doi:10.1111/j.1365-2435.2005.01008.x

  85. Soliveres S, Eldridge DJ, Maestre FT, Bowker MA, Tighe M, Escudero A (2011) Microhabitat amelioration and reduced competition among understorey plants as drivers of facilitation across environmental gradients: towards a unifying framework. Perspect Plant Ecol Evol Syst 13:247–258. doi:10.1016/j.ppees.2011.06.001

  86. Stachowicz JJ (2001) Mutualism, facilitation and the structure of ecological communities. Bioscience 51:235–246. doi:10.1641/0006-3568(2001)051[0235:MFATSO]2.0.CO;2

  87. Thuiller W, Albert CH, Dubuis A, Randin C, Guisan A (2010) Variation in habitat suitability does not always relate to variation in species’ plant functional traits. Biol Lett 6:120–123. doi:10.1098/rsbl.2009.0669

  88. Valladares F, Niinemets Ü (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annu Rev Ecol Evol Syst 39:237–257. doi:10.1146/annurev.ecolsys.39.110707.173506

  89. Vasseur F, Violle C, Enquist BJ, Granier C, Vile D (2012) A common genetic basis to the origin of the leaf economics spectrum and metabolic scaling allometry. Ecol Lett 15:1149–1157. doi:10.1111/j.1461-0248.2012.01839.x

  90. Verdú M, García-Fayos P (2003) Frugivorous birds mediated sex-biased facilitation in a dioecious nurse plant. J Veg Sci 14:35–42. doi:10.1111/j.1654-1103.2003.tb02125.x

  91. Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos 116:882–892. doi:10.1111/j.2007.0030-1299.15559.x

  92. Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Annu Rev Ecol Evol Syst 33:125–159. doi:10.1146/annurev.ecolsys.33.010802.150452

  93. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas E, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827. doi:10.1038/nature02403

  94. Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Garnier E, Hikosaka K, Lamont BB, Lee W, Oleksyn J, Osada N, Poorter H, Villar R, Warton DI, Westoby M (2005) Assessing the generality of global leaf trait relationships. New Phytol 166:485–496. doi:10.1111/j.1469-8137.2005.01349.x

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Acknowledgments

We are indebted to David Vera and Jose B. López-Quintanilla (Sierra de las Nieves Natural Park) and José A. Carreira (University of Jaén) for all the facilities provided during field work and especially to Maika Folch, Gonzalo Pérez Monforte, Erik Rodríguez, Gonzalo Juste and Enrique Marcos for intensive field and lab collaboration. Technical staff from Rey Juan Carlos University helped with laboratory analysis. Alex Fajardo very kindly reviewed a previous version of the manuscript, and three anonymous referees provided useful comments to improve it. David Brown edited the English. This work was supported by a FPI-MICINN grant to A. I. García-Cervigón; projects of the Spanish Ministry of Science and Innovation (CGL2009-13190-C03-0) and Spanish Ministry of Economy and Competitiveness (CGL2012-34209); and European Union FEDER 0087 TRANSHABITAT to J. C. Linares. The experiments comply with the current laws of the country (Spain) in which the experiments were performed.

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Correspondence to Ana I. García-Cervigón.

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Communicated by Daniel Laughlin.

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García-Cervigón, A.I., Linares, J.C., Aibar, P. et al. Facilitation promotes changes in leaf economics traits of a perennial forb. Oecologia 179, 103–116 (2015). https://doi.org/10.1007/s00442-015-3312-8

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Keywords

  • Functional traits
  • Intraspecific trait variation
  • Leaf economics spectrum
  • Mediterranean high mountains
  • Plant-plant interactions