Abstract
Although intraspecific trait variability is an important component of species ecological plasticity and niche breadth, its implications for community and functional ecology have not been thoroughly explored. We characterized the intraspecific functional trait variability of Scots pine (Pinus sylvestris) in Catalonia (NE Spain) in order to (1) compare it to the interspecific trait variability of trees in the same region, (2) explore the relationships among functional traits and the relationships between them and stand and climatic variables, and (3) study the role of functional trait variability as a determinant of radial growth. We considered five traits: wood density (WD), maximum tree height (H max), leaf nitrogen content (Nmass), specific leaf area (SLA), and leaf biomass-to-sapwood area ratio (B L:A S). A unique dataset was obtained from the Ecological and Forest Inventory of Catalonia (IEFC), including data from 406 plots. Intraspecific trait variation was substantial for all traits, with coefficients of variation ranging between 8 % for WD and 24 % for B L:A S. In some cases, correlations among functional traits differed from those reported across species (e.g., H max and WD were positively related, whereas SLA and Nmass were uncorrelated). Overall, our model accounted for 47 % of the spatial variability in Scots pine radial growth. Our study emphasizes the hierarchy of factors that determine intraspecific variations in functional traits in Scots pine and their strong association with spatial variability in radial growth. We claim that intraspecific trait variation is an important determinant of responses of plants to changes in climate and other environmental factors, and should be included in predictive models of vegetation dynamics.




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Ackerly DD, Cornwell WK (2007) A trait-based approach to community assembly: partitioning of species trait values into within- and among-community components. Ecol Lett 10:135–145
Albert CH, Thuiller W, Yoccoz NG, Soudant A, Boucher F, Saccone P, Lavorel S (2010a) Intraspecific functional variability: extent, structure and sources of variation. J Ecol 98:604–613
Albert CH, Thuiller W, Yoccoz NG, Douzet R, Aubert S, Lavorel S (2010b) A multi-trait approach reveals the structure and the relative importance of intra- vs. interspecific variability in plant traits. Funct Ecol 24:1192–1201
Alia R, Moro-serrano J, Notivol E (2001) Genetic variability of Scots pine (Pinus sylvestris). Growth traits and survivals. Silva Fenn 35:27–38
Allen CD, Macalad AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim JH, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manage 259:660–684
Baroloto C, Marcon E, Morneau F, Pavoine S, Roggy JC (2010) Integrating functional diversity into tropical forest plantation designs to study ecosystem processes. Ann For Sci 67:303
Barbéro M, Loisel R, Quézel P, Richardson DM, Romane F (1998) Pines of the Mediterranean basin. Cambridge University Press, Cambridge
de Bello F, Lavorel S, Diaz S, Harrington R, Cornelissen JHC, Bardgett RD, Berg MP, Cipriotti P, Feld CK, Hering D, Marins da Silva P, Potts SG, Sandin L, Sousa JP, Storkey J, Wardle DA, Harrison PA (2010) Towards an assessment of multiple ecosystem processes and services via functional traits. Biodivers Conserv 19:2873–2893
Benito Garzon M, Alia R, Robson TM, Zavala MA (2011) Intra-specific variability and plasticity influence potential tree species distribution under climate change. Glob Ecol Biogeogr 20:766–778
Bigler C, Bräker OU, Bugmann H, Dobbertin M, Rigling A (2006) Drought as an inciting mortality factor in Scots pine stands of the Valais, Switzerland. Ecosystems 9(3):330–343
Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forrister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28
Bolnick DI, Amarasekare P, Araujo MS, Bürger R, Levine J, Novak M, Rudolf VHW, Schreiber SJ, Urban MC, Vasseur DA (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26:183–192
Bolòs O, Vigo J (1984) Flora dels Països Catalans, vol I. Editorial Barcino, Barcelona
Burriel JA, Gracia C, Ibanez JJ, Mata T, Vayreda J (2000–2004) Inventari Ecologic i Forestal de Catalunya, 10 volumes. CREAF, Bellaterra
Campetella G, Botta-Dukát Z, Wellstein C, Canullo R, Gatto S, Chelli S, Mucina L, Bartha S (2011) Patterns of plant trait–environment relationships along a forest succession chronosequence. Agric Ecosyst Environ 145(1):38–48
Castroviejo S, Lainz M, López González G, Montserrat P, Muñoz Garmendia F, Paiva J, Villar L (eds) (1986) Flora ibérica: plantas vasculares de la Península Ibérica e Islas Baleares, vol 1. C.S.I.C, Madrid
Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE (2009) Towards a worldwide wood economics spectrum. Ecol Lett 12:351–366
Cianciaruso MV, Batalha MA, Gaston KJ, Petchey OL (2009) Including intraspecific variability in functional diversity. Ecology 90:81–89
Clausen J, Keck DD, Hiesey WM (1948) Experimental studies on the nature of species. III. Environmental responses of climatic races of Achillea. Carnegie Institution, Washington, DC
Cordell S, Goldstein G, Mueller-Dombois D, Webb D, Vitousek PM (1998) Physiological and morphological variation in Metrosideros polymorpha, a dominant Hawaiian tree species, along an altitudinal gradient: the role of phenotypic plasticity. Oecologia 113:188–196
Cornwell WK, Bhaskar R, Sack L, Cordell D, Lunch CK (2007) Adjustment of structure and function of Hawaiian Metrosideros polymorpha at high vs. low precipitation. Funct Ecol 21:1063–1071
Cornwell WK, Ackerly DD (2009) Community assembly and shifts in the distribution of functional trait values across an environmental gradient in coastal California. Ecol Monogr 79:109–126
DeLucia EH, Maherali H, Carey EV (2000) Climate-driven changes in biomass allocation in pines. Glob Change Biol 6:587–593
Díaz S, Cabido M, Casanoves F (1998) Plant functional traits and environmental filters at a regional scale. J Veg Sci 9(1):113–122
Fajardo A, Piper FI (2011) Intraspecific trait variation and covariation in a widespread tree species (Nothofagus pumilio) in southern Chile. New Phytol 189:259–271
Fox CW, Roff DA, Fairbairn DJ (2001) Evolutionary ecology: concepts and case studies. Oxford University Press, New York
Galiano L, Martínez-Vilalta J, Lloret F (2010) Drought-induced multifactor decline of Scots pine in the pyrenees and potential vegetation change by the expansion of co-occurring oak species. Ecosystems 13:978–991
Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA (2001) Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126:457–461
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
Hurme P, Repo T, Savolainen O, Pääkkönen T (1997) Climatic adaptation of bud set and frost hardiness in Scots pine (Pinus sylvestris). Can J For Res 27(5):716–723
Irvine J, Perks MP, Magnani F, Grace J (1998) The response of Pinus sylvestris to drought: stomatal control of transpiration and hydraulic conductance. Tree Physiol 18(6):393–402
Janse-Ten Klooster SH, Thomas EJ, Sterck FJ (2007) Explaining interspecific differences in sapling growth and shade tolerance in temperate forests. J Ecol 95(6):1250–1260
Kattge J, Díaz S, Lavorel S, Prentice IC, Leadley P, Bönisch G, Garnier E et al (2011) TRY—a global database of plant traits. Glob Change Biol 17(9):2905–2935. doi:10.1111/j.1365-2486.2011.02451.x
Keddy PA (1992) A pragmatic approach to functional ecology. Funct Ecol 6:621–626
King DA, Davies SJ, Nur Supardi MN, Tan S (2005) Tree growth is related to light interception and wood density in two mixed dipterocarp forests of Malaysia. Funct Ecol 19:445–453
King DA, Davies SJ, Nur Supardi MN (2006a) Growth and mortality are related to adult tree size in a Malaysian mixed dipterocarp forest. For Ecol Manage 223:152–158
King DA, Davies SJ, Tan S, Nur Supardi MN (2006b) The role of wood density and stem support costs in the growth and mortality of tropical trees. J Ecol 94:670–680
Kleinschmit J (1993) Intraspecific variation of growth and adaptive traits in European oak species. Ann For Sci 50(Supplement 1):166–185
Lambers H, Poorter H (1992) Inherent variation in growth-rate between higher-plants—a search for physiological causes and ecological consequences. Adv Ecol Res 23:187–261
Lusk CH, Reich PB, Montgomery RA, Ackerly DD, Cavender-Bares J (2008) Why are evergreen leaves so contrary about shade? Trends Ecol Evol 23(6):299–303
Magnani F, Grace J, Borghetti M (2002) Adjustment of tree structure in response to the environment under hydraulic constraints. Funct Ecol 16(3):385–393
Maherali H, Pockman WT, Jackson RB (2004) Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85:2184–2199
Martínez-Vilalta J, Piñol P (2002) Drought-induced mortality and hydraulic architecture in pine populations of the NE Iberian Peninsula. For Ecol Manag 161:247–256
Martínez-Vilalta J, López BC, Adell N, Badiella L, Ninyerola M (2008) Twentieth century increase of Scots pine radial growth in NE Spain shows strong climate interactions. Glob Change Biol 14(12):2868–2881
Martínez-Vilalta J, Cochard H, Mencuccini M, Sterck F, Herrero A, Korhonen JFJ, Llorens P, Nikinmaa E, Nolè A, Poyatos R, Ripullone F, Sass-Klaassen U, Zweifel R (2009) Hydraulic adjustment of Scots pine across Europe. New Phytol 184:353–364
Martínez-Vilalta J, Mencuccini M, Vayreda J, Retana J (2010) Interspecific variation in functional traits, not climatic differences among species ranges, determines demographic rates across 44 temperate and Mediterranean tree species. J Ecol 98:1462–1475
Martínez-Vilalta J, Lloret F, Breshears DD (2012) Drought-induced forest decline: causes, scope and implications. Biol Lett 8(5):689–691
McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185
Mencuccini M, Bonosi L (2001) Leaf/sapwood area ratios in Scots pine show acclimation across Europe. Can J For Res 31:442–456
Mencuccini M (2003) The ecological significance of long-distance water transport: short-term regulation, long-term acclimation and the hydraulic costs of stature across plant life forms. Plant Cell Environ 26:163–182
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
Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan MD, Richards CL, Valladares F, van Kleunen M (2010) Plant phenotypic plasticity in a changing climate. Trends Plant Sci 15:684
Niinemets U, Kull K (2003) Leaf structure vs. nutrient relationships vary with soil conditions in temperate shrubs and trees. Acta Oecol 24:209–219
van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128:137–142
Oleksyn J, Reich PB, Zytkowiak R, Karolewski P, Tjoelker MG (2003) Nutrient conservation increases with latitude of origin in European Pinus sylvestris populations. Oecologia 136(2):220–235
O’Neill GA, Nigh G (2011) Linking population genetics and tree growth models to predict impacts of climate change on species’ growth and distribution. J Appl Ecol 45:1040–1049
Palmroth S, Berninger F, Nikinmaa E, Lloyd J, Pulkkinen P, Hari P (1999) Structural adaptation rather than water conservation was observed in Scots pine over a range of wet to dry climates. Oecologia 121(3):302–309
Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Moomer L (2011) Biomass allocation to leaves stems and roots: meta-analysis of interspecific variation and environmental control. New Phytol 193:30–50. doi:10.1111/j.1469-8137.2011.03952.x
Poorter L, Bongers F (2006) Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology 87:1733–1743
Poorter L (2008) The relationships of wood-, gas-, and water fractions of tree stems to performance and life history variation in tropical trees. Ann Bot 102:367–375
Poorter L, Paz H, Wright SJ, 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 5 neotropical forests. Ecology 89:1908–1920
Poorter L, McDonald I, Alarcón A, Fichtler E, Licona J-C, Peña-Claros M, Sterck F, Villegas Z, Sass-Klaassen U (2010) The importance of wood traits and hydraulic conductance for the performance and life history strategies of 42 rainforest tree species. New Phytol 185:481–492
Poyatos R, Martínez-Vilalta J, Čermák J, Ceulemans R, Granier A, Irvine J, Köstner B, Lagergren F, Meiresonne L, Nadezhdina N, Zimmermann R, Llorens R, Mencuccini M (2007) Plasticity in hydraulic architecture of Scots pine across Eurasia. Oecologia 153(2):245–259
Poyatos R, Llorens P, Piñol J, Rubio C (2008) Response of Scots pine (Pinus sylvestris L.) and pubescent oak (Quercus pubescens Wild.) to soil and atmospheric water deficits under Mediterranean mountain climate. Ann For Sci 65(3):306
Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proc Natl Acad Sci USA 94:13730–13734
Reich PB, Oleksyn J (2008) Climate warming will reduce growth and survival of Scots pine except in the far north. Ecol Lett 11(6):588–597
Sterck FJ, Martínez-Vilalta J, Mencuccini M, Cochard H, Gerrits P, Zweifel R, Herrero A, Korhonen JFJ, Llorens P, Nikinmaa E, Nolè A, Poyatos R, Ripullone F, Sass-Klaassen U (2012) Understanding trait interactions and their impacts on growth in Scots pine branches across Europe. Funct Ecol 26(2):541–549
Sterck FJ, Duursma RA, Pearcy RW, Valladares F, Cieslak M, Weemstra M (2013) Plasticity influencing the light compensation point offsets the specialization for light niches across shrub species in a tropical forest understorey. J Ecol 101(4):971–980
Vilà-Cabrera A, Rodrigo A, Martínez-Vilalta J, Retana J (2011a) Lack of regeneration and climatic vulnerability to fire of Scots pine may induce vegetation shifts at the southern edge of its distribution. J Biogeogr 39:488–496
Vilà-Cabrera A, Martínez-Vilalta J, Vayreda J, Retana J (2011b) Structural and climatic determinants of demographic rates of Scots pine forests across the Iberian Peninsula. Ecol Appl 21:1162–1172
Vilà-Cabrera A, Martínez–Vilalta J, Retana J (2014) Variation in reproduction and growth in declining Scots pine populations. Perspect Plant Ecol Evol Syst (in press)
Violle C, Navas M-L, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos 116:882–892
Wang T, O’Neill GA, Aitken SN (2010) Integrating environmental and genetic effects to predict responses of tree populations to climate. Ecol Appl 20:153–163
Westoby M, Falster DS, Moles A, Vesk PA, Wright IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Annu Rev Ecol Syst 33:125–159
Westoby M, Wright IJ (2006) Land-plant ecology on the basis of functional traits. Trends Ecol Evol 21:261–268
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 U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The world-wide leaf economics spectrum. Nature 428:821–827
Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Groom PK, Hikosaka K, Lee W, Lusk CH, Niinemets U, Oleksyn J, Osada N, Poorter H, Warton DI, Westoby M (2005) Modulation of leaf economic traits and trait relationships by climate. Glob Ecol Biogeogr 14:411–421
Wright IJ, Ackerly DD, Bongers F, Harms KE, Ibarra-Manriquez G, Martinez-Ramos M, Mazer SJ, Muller-Landau HC, Paz H, Pitman NCA, Poorter L, Silman MR, Vriesendorp CF, Webb CO, Westoby M, Wright SJ (2007) Relationships among ecologically important dimensions of plant trait variation in 7 Neotropical forests. Ann Bot 99:1003–1015
Wright SJ, Kitajima K, Kraft NJB, Reich PB, Wright IJ, Bunker DE, Condit R, Dalling JW, Davies SJ, Diaz S, Engelbrecht BMJ, Harms KE, Hubbell SP, Marks CO, Ruiz-Jaen MC, Salvador CM, Zanne AE (2010) Functional traits and the growth–mortality tradeoff in tropical trees. Ecology 91:3664–3674
Wright JP, Sutton-Grier A (2012) Does the leaf economic spectrum hold within local species pools across varying environmental conditions? Funct Ecol 26:1390–1398
Zweifel R, Steppe K, Sterck FJ (2007) Stomatal regulation by microclimate and tree water relations: interpreting ecophysiological field data with a hydraulic plant model. J Exp Bot 58:2113–2131
Acknowledgments
We thank Jordi Vayreda for his help querying the IEFC database and the elaboration of Fig. 1. Financial support was obtained from the Spanish Ministry of Education and Sciences via competitive grants CGL2007-60120, CGL2010-16373, CSD2008-0004 (Consolider Program).
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Communicated by Peter B. Reich.
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Laforest-Lapointe, I., Martínez-Vilalta, J. & Retana, J. Intraspecific variability in functional traits matters: case study of Scots pine. Oecologia 175, 1337–1348 (2014). https://doi.org/10.1007/s00442-014-2967-x
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DOI: https://doi.org/10.1007/s00442-014-2967-x
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