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Intraspecific phenotypic variability of plant functional traits in contrasting mountain grasslands habitats

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Abstract

Empirical studies that link plants intraspecific variation to environmental conditions are almost lacking, despite their relevance in understanding mechanisms of plant adaptation, in predicting the outcome of environmental change and in conservation. Here, we investigate intraspecific trait variation of four grassland species along with abiotic environmental variation at high spatial resolution (n = 30 samples per species trait and environmental factor per site) in two contrasting grassland habitats in Central Apennines (Italy). We test for phenotypic adaptation between habitats, intraspecific trait-environment relationships within habitats, and the extent of trait and environmental variation. We considered whole plant, clonal, leaf, and seed traits. Differences between habitats were tested using ANOVA and ANCOVA. Trait-environment relationships were assessed using multiple regression models and hierarchical variance partitioning. The extent of variation was calculated using the coefficient of variation. Significant intraspecific differences in trait attributes between the contrasting habitats indicate phenotypic adaptation to in situ environmental conditions. Within habitats, light, soil temperature, and the availability of nitrate, ammonium, magnesium and potassium were the most important factors driving intraspecific trait-environment relationships. Leaf traits and height growth show lower variability than environment being probably more regulated by plants than clonal traits which show much higher variability. We show the adaptive significance of key plant traits leading to intraspecific adaptation of strategies providing insights for conservation of extant grassland communities. We argue that protecting habitats with considerable medium- and small-scale environmental heterogeneity is important to maintain large intraspecific variability within local populations that finally can buffer against uncertainty of future climate and land use scenarios.

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Abbreviations

SLA:

Specific leaf area

LDMC:

Leaf dry matter content

References

  • 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Al Haj Khaled R, Duru M, Theau JP, Plantureux S, Cruz P (2005) Variation in leaf traits through seasons and N-availability levels and its consequences for ranking grassland species. J Veg Sci 16:391–398

    Article  Google Scholar 

  • Badyaev AV (2009) Evolutionary significance of phenotypic accommodation in novel environments: an empirical test of the Baldwin effect. Phil Trans R Soc B 364:1125–1141

    Google Scholar 

  • Barriopedro D, Fischer EM, Luterbacher J, Trigo RM, Garcia-Herrera R (2011) The hot summer of 2010: redrawing the temperature record map of Europe. Science 332:220–224

    Article  PubMed  CAS  Google Scholar 

  • Barker G, Grant A, Beavitt P, Christie N, Giorgi J, Hoare P, Leggio T, Migliavacca M (1991) Ancient and Modern Pastoralism in Central Italy: an Interdisciplinary Study in the Cicolano Mountains. Papers of the British School at Rome 59:15–88

    Google Scholar 

  • Baskin CC, Baskin JM (1998) Seeds: Ecology, biogeography, and evolution of dormancy and germination. Academic Press, San Diego

    Google Scholar 

  • Beier P, Brost B (2010) Use of land facets to plan for climate change: conserving the arenas, not the actors. Conserv Biol 24:701–710

    Article  PubMed  Google Scholar 

  • Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28

    Article  PubMed  Google Scholar 

  • Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologists. Ecol Lett 11:106–115

    PubMed  Google Scholar 

  • Branch NP (2012) Early-Middle Holocene vegetation history, climate change and human activities at Lago Riane (Ligurian Apennines, NW Italy). Veg Hist Archeobot. Published online 21 November 2012

  • Buckley RC (1982) Seed size and seedling establishment in tropical arid dunecrest plants. Biotropica 14:314–315

    Article  Google Scholar 

  • Burdon JJ (1987) Phenotypic and genetic patterns of resistance to the pathogen Phakopsora pachyrhizi in populations of Glycine canescens. Oecologia 73:257–267

    Article  Google Scholar 

  • Carter EB, Theodorou MK, Morris P (1997) Responses of Lotus corniculatus to environmental change. New Phytol 36:245–253

    Article  Google Scholar 

  • Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide; in. Aust J Bot 51:335–380

    Article  Google Scholar 

  • Garnier E, Laurent G, Bellmann A, Debain S, Berthelier P, Ducout B, Roumet C, Navas ML (2001) Consistency of species ranking based on functional leaf traits. New Phytol 152:69–83

    Article  Google Scholar 

  • Garnier E, Cortez J, Billes G, Navas ML, Roumet C, Debussche M, Laurent G, Blanchard A, Aubry D, Bellmann A, Neill C, Toussaint JP (2004) Plant functional markers capture ecosystem properties during secondary succession. Ecology 85:2630–2637

    Article  Google Scholar 

  • 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. Ann Bot 106:637–645

    Article  PubMed  Google Scholar 

  • Grime JP (1994) The role of plasticity in exploiting environmental heterogeneity. In: Caldwell MM, Pearcy R (eds) Exploitation of Environmental Heterogeneity in Plants. Academic press, San Diego, pp 1–18

    Chapter  Google Scholar 

  • Grime JP (2002) Plant strategies, vegetation processes, and ecosystem properties, 2nd edn. Wiley, Chichester

    Google Scholar 

  • Gross N, Suding KN, Lavorel S (2007) Leaf dry matter content and lateral spread predict response to land use change for six subalpine grassland species. J Veg Sci 18:289–300

    Article  Google Scholar 

  • Groves CR, Game ET, Anderson MG, Cross M, Enquist C, Ferdaña Z, Girvetz E, Gondor A, Hall KR, Higgins J, Marshall R, Popper K, Schill S, Shafer SL (2012) Incorporating climate change into systematic conservation planning. Biodivers Conserv 21:1651–1671

    Article  Google Scholar 

  • Grömping U (2006) Relative importance for linear regression in R: the package relaimpo. J Stat Softw 17:1–27

    Article  Google Scholar 

  • Halassy M, Campetella G, Canullo R, Mucina L (2005) Patterns of functional clonal traits and clonal growth modes in contrasting grasslands in the central Apennines, Italy. J Veg Sci 16:29–36

    Article  Google Scholar 

  • Hodgson JG, Mackey JML (1986) The ecological specialisation of dicotyledonous families within a local flora: some factors constraining optimization of seed size and their evolutionary significance. New Phytol 12:497–515

    Article  Google Scholar 

  • Hoffmann G (1991) Die Untersuchung von Böden – Methodenbuch 1. VDLUFA-Verlag, Darmstadt

    Google Scholar 

  • 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

    Article  Google Scholar 

  • IPCC (2012) Managing the risks of extreme events and disasters to advance climate change adaptation. A special report of working Groups I and II of the intergovernmental panel on climate change. In: Field CB, Barros V, Stocker TF et al (eds) Cambridge University Press, Cambridge, UK, and New York, NY, USA, 582 pp

  • ISTA (International Society of Testing Analysis) (1999) International rules for seed testing. Seed Sci Technol 27(supplement):201–244

    Google Scholar 

  • Kleyer M, Bekker RM, Knevel IC, Bakker JP, Thompson K, Sonnenschein M, Poschlod P, van Groenendael JM, Klimes L, Klimesová J, Klotz S, Rusch GM, Hermy M, Adriaens D, Boedeltje G, Bossuyt B, Endels P, Götzenberger L, Hodgson JG, Jackel A-K, Dannemann A, Kühn I, Kunzmann D, Ozinga WA, Römermann C, Stadler M, Schlegelmilch J, Steendam HJ, Tackenberg O, Wilmann B, Cornelissen JHC, Eriksson O, Garnier E, Fitter A, Peco B (2008) The LEDA Traitbase: a database of plant life-history traits of North West European Flora. J Ecol 96:1266–1274

    Article  Google Scholar 

  • Klimešová J, Klimeš L (2006) CLO-PLA3: a database of clonal growth architecture of Central-European plants. http://clopla.butbn.cas.cz

  • Knevel IC, Bekker RM, Kunzmann D, Stadler M, Thompson K (2005) The LEDA Traitbase collecting and measuring standards of life-history traits of the NW European flora. Published by the University of Groningen, Groningen

    Google Scholar 

  • Kwiatkowski W, Venanzoni R (1994) Carta dei suoli della riserva naturale di Torricchio. La Riserva Naturale di Torricchio 9:15–21

    Google Scholar 

  • Leishman MR, Westoby M (1994) The role of seed size in seedling establishment in dry soil conditions – experimental evidence from semi-arid species. J Ecol 82:249–258

    Article  Google Scholar 

  • Lemke I, Kolb A, Diekmann M (2012) Region and site conditions affect phenotypic trait variation in five forest herbs. Acta Oecol 39:18–24

    Article  Google Scholar 

  • Linhart YB (1988) Intra-population differentiation in annual plants. III. The contrasting effects of intra- and inter-specific competition. Evolution 42:1047–1064

    Article  Google Scholar 

  • Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. Annu Rev Ecol Syst 27:237–277

    Article  Google Scholar 

  • Mawdsley JR, O’Malley R, Ojima DS (2009) A Review of climate-change adaptation strategies for wildlife management and biodiversity conservation. Conserv Biol 2:1080–1089

    Article  Google Scholar 

  • Maillette C (1992) Seasonal model of modular growth in plants. J Ecol 80:123–130

    Article  Google Scholar 

  • Mazer SJ (1989) Ecological, taxonomic and life history correlates of seed mass among Indiana Dune angiosperms. Ecol Monogr 59:153–175

    Article  Google Scholar 

  • McCarthy MC, Enquist BJ (2007) Consistency between an allometric approach and optimal partitioning theory in global patterns of plant biomass allocation. Funct Ecol 21:713–720

    Article  Google Scholar 

  • Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20(12):685–692

    Article  PubMed  Google Scholar 

  • Moles AT, Westoby M (2006) Seed size and plant strategy across the whole life cycle. Oikos 113:91–105

    Article  Google Scholar 

  • Murray K, Conner MM (2009) Methods to quantify variable importance: implications for the analysis of noisy ecological data. Ecology 90:348–355

    Article  PubMed  Google Scholar 

  • 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 15:684–992

    Article  PubMed  CAS  Google Scholar 

  • Oborny B, Bartha S (1995) Clonality in plant communities – An overview. Abstracta Botanica 19:115–127

    Google Scholar 

  • Pakeman RJ, Garnier E, Lavorel S, Ansquer P, Castro H, Cruz P, Dolezal J, Eriksson O, Freitas H, Golodet C, Kigel J, Kleyer M, Leps J, Meier T, Papadimitriou M, Papanastasi VP, Quested H, Quetier F, Rusch G, Sternberg M, Theau JP, Thebault A, Vile D (2008) Impact of abundance weighting on the response of seed traits to climate and land use. J Ecol 96:355–366

    Article  Google Scholar 

  • Peat HJ, Fitter AH (1994) Comparative analyses of ecological characteristics of British angiosperms. Biol Rev 69:95–115

    Article  Google Scholar 

  • Pierce S, Luzzaro A, Caccianiga M, Ceriani RM, Cerabolini B (2007) Disturbance is the principal α-scale filter determining niche differentiation, coexistence and biodiversity in an alpine community. J Ecol 95:698–706

    Article  Google Scholar 

  • Pignatti S (1982) Flora d’Italia. Edagricole, Bologna

    Google Scholar 

  • Poorter H, Pepin S, Rijkers T, De Jong Y, Evans JR, Körner C (2006) Construction costs, chemical composition, and payback time of high and low irradiance leaves. J Exp Bot 57:355–371

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • R Development Core Team (2010) R: A language and environment for statistical computing. R version 2.13.1. Foundation for Statistical Computing. Vienna, Austria, http://www.R-project.org

  • Reich PB, Wright IJ, Cavender-Bares J, Craine JM, Oleksyn J, Westoby M, Walters MB (2003) The evolution of plant functional variation: traits, spectra and strategies. Int J Plant Sci 164:S143–S164

    Article  Google Scholar 

  • Ryser P, Urbas P (2000) Ecological significance of leaf life span among Central European grass species. Oikos 91:41–50

    Article  Google Scholar 

  • Schellenberg J, Pontes S (2012) Plant functional traits and nutrient gradients on grassland. Grass Forage Sci 67:305–319

    Article  Google Scholar 

  • Silvertown J (2004) Plant coexistence and the niche. Trends Ecol Evol 19:605–611

    Article  Google Scholar 

  • Simms EL (1990) Examining selection on the multivariate phenotype: plant resistance to herbivores. Evolution 44:1177–1188

    Article  Google Scholar 

  • Stanton ML (1984) Seed variation in wild radish: effect of seed size on components of seedlings and adult fitness. Ecology 65:1105–1112

    Article  Google Scholar 

  • Stöcklin J (1992) Umwelt, Morphologie und Wachstumsmuster klonaler Pflanzen - eine Übersicht. Bot Helv 102:3–21

    Google Scholar 

  • Sultan SE (1987) Evolutionary implications of phenotypic plasticity in plants. In: Hecht MK, Wallace B, Prance GT (eds) Evolutionary Biology, Vol 21. Springer, New York, pp 127–178

  • Tissue DT, Nobel PS (1988) Parent-ramet connections in Agave desert: influences of carbohydrates on growth. Oecologia 75:266–271

    Article  Google Scholar 

  • Turkington R (1989) The growth, distribution, and neighbour relationships of Trifolium repens in a permanent pasture. V. The coevolution of competitors. J Ecol 77:717–733

    Article  Google Scholar 

  • Turkington R, Aarssen LW (1984) In: Dirzo R, Sarukhan J (eds) Local scale differentiation as a result of competitive interactions. Sunderland, MA, Perspectives in Plant Population Ecology. Sinauer, pp 107–127

    Google Scholar 

  • Venanzoni R, Kwiatkowski W (1995) Analisi integrata del paesaggio in un settore dell’Appennino Centrale (Riserva naturale Montagna di Torricchio). Colloq Phytosociol 24:187–201

    Google Scholar 

  • Violle C, Enquist BJ, McGill BJ, Jiang L, Albert CH, Hulshof C, Jung V, Messier J (2012) The return of the variance: intraspecific variability in community ecology. Trends Ecol Evol 27(4):244–252

    Article  PubMed  Google Scholar 

  • Walck JL, Hidayati SN, Dixon KW, Thompson K, Poschlod P (2011) Climate change and plant regeneration from seed. Glob Change Biol 17:2145–2161

    Google Scholar 

  • Webb CT, Hoeting JA, Ames GM, Pyne MI, Poff NL (2010) A structured and dynamic framework to advance traits-based theory and prediction in ecology. Ecol Lett 13:267–283

    Article  PubMed  Google Scholar 

  • Wellstein C (2012) Seed–litter–position drives seedling establishment in grassland species under recurrent drought. Plant Biol 14:1006–1010

    Google Scholar 

  • Wellstein C, Kuss P (2011) Diversity and frequency of clonal traits along natural and land-use gradients in grasslands of the Swiss Alps. Folia Geobot 46:255–270

    Article  Google Scholar 

  • Wellstein C, Schröder B, Reineking B, Zimmermann NE (2011) Understanding species and community response to environmental change – A functional trait perspective. Agr Ecosyst Environ 145:1–4

    Article  Google Scholar 

  • West-Eberhard MJ (2005) Phenotypic accommodation: adaptive innovation due to developmental plasticity. J Exp Zool B 304:610–618

    Google Scholar 

  • Westoby M (1998) A leaf-height-seed (LHS) plant ecology strategy scheme. Plant Soil 199:213–227

    Article  CAS  Google Scholar 

  • Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Annu Rev Ecol Syst 33:125–159

    Article  Google Scholar 

  • Wilson PJ, Thompson K, Hodgson JG (1999) Specific Leaf Area and Leaf Dry Matter Content as Alternative Predictors of Plant Strategies. New Phytol 143:155–162

    Article  Google Scholar 

  • Wright IJ, Westoby M (1999) Differences in seedling growth behaviour among species: trait correlations across species, and trait shifts along nutrient compared to rainfall gradients. J Ecol 87:85–97

    Article  Google Scholar 

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Acknowledgments

We thank the Analytical Chemistry of the Bayreuth Centre of Ecology and Environmental Research (BayCEER, Germany) for performing the analyses of soil chemical parameters. This research was partially supported by Montagna di Torricchio Nature Reserve. SB was supported by the Hungarian National Science Foundation (OTKA K 72561). CW was supported by the Bavarian State Ministry of Sciences, Research and the Arts within the FORKAST project. We thank Martin Hallinger (University of Greifswald, Germany) for help with the determination of age of A. sempervirens.

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Correspondence to Camilla Wellstein.

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Pignatti (1982) for taxa; Venanzoni & Kwiatkowski (1995) for the syntaxa mentioned in Table 1.

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Wellstein, C., Chelli, S., Campetella, G. et al. Intraspecific phenotypic variability of plant functional traits in contrasting mountain grasslands habitats. Biodivers Conserv 22, 2353–2374 (2013). https://doi.org/10.1007/s10531-013-0484-6

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