Skip to main content

Advertisement

SpringerLink
Log in

Tree species richness induces strong intraspecific variability of beech (Fagus sylvatica) leaf traits and alleviates edaphic stress

  • OriginalPaper
  • Published:
European Journal of Forest Research Aims and scope Submit manuscript

Abstract

Manipulating stand composition is an important management tool that foresters can use to affect the nature of forests and ecosystem processes. In mixed stands, interspecific interactions among trees can cause changes in tree performances. Nevertheless, these interactions are context dependent (cf. stress-gradient hypothesis, SGH). We thus investigated how intraspecific functional changes in leaf trait (19 traits) of European beech (Fagus sylvatica) were influenced by stand composition. We compared pure beech stands with four mixed stands containing from one to three additional tree species along a gradient of edaphic stress (gradient of soil water-holding capacity and rooting depth). First, we demonstrated that stand composition induced strong intraspecific leaf trait variation in beech for LDMC, LMA, phenolic compounds, leaf pH and magnesium concentration, suggesting higher nutrient acquisition by more diverse stands. Nevertheless, these results were modulated by edaphic stress. Mixed stands only conferred an advantage in relatively stressed sites (luvisol and leptosol). Besides, the addition of oak to beech stands had unexpected negative effects in sites with less severe stress (cambisol) as indicated by the null or positive LogRR of LMA, LDMC and phenolics. This study found that stand composition is an important though often-overlooked driver of intraspecific variability in leaf quality, and potentially reflects changes in beech tree physiology and productivity. Our results also suggest that positive interactions prevail in sites with stressful conditions. Such validation of the SGH is rare in natural or managed mature forests. Lastly, we strongly recommend that forest managers consider stand composition and abiotic factors when implementing forest growth models to improve their yield predictions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

LDMC:

Leaf dry matter content

LMA:

Leaf mass per area

LogRR:

Log response ratio

SGH:

Stress-gradient hypothesis

References

  • Adler PB, Fajardo A, Kleinhesselink AR, Kraft NJB (2013) Trait-based tests of coexistence mechanisms. Ecol Lett 16:1294–1306

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Albert CH, Thuiller W, Yoccoz NGDouzet, Aubert R, 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

    Article  Google Scholar 

  • Albert CH, Grassein F, Schurr FM, Vieilledent G, Violle C (2011) When and how should intraspecific variability be considered in trait-based plant ecology? Perspect Plant Ecol 13:217–225

    Article  Google Scholar 

  • Baize B (2000) Guide des analyses en pédologie. INRA Editions Paris

  • Bärlocher F, Graça M (2005) Total Phenolics. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide. Springer, Berlin, pp 97–100

    Chapter  Google Scholar 

  • Bates D, Sarkar D (2006) lme4: linear mixed-effects models using S4 classes In: http://CRANR-projectorg R package version 0·99875-8

  • Bayer D, Seifert S, Pretzsch H (2013) Structural crown properties of Norway spruce (Picea abies [L] Karst) and European beech (Fagus sylvatica [L]) in mixed versus pure stands revealed by terrestrial laser scanning. Trees 27:1035–1047

    Article  Google Scholar 

  • Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193

    Article  CAS  PubMed  Google Scholar 

  • Boizot N, Charpentier J-P (2006) Méthode rapide d’évaluation du contenu en composés phénoliques des organes d’un arbre forestier. Le Cahier des Techniques de l’Inra, pp 79–82

  • Bottrill DE, Possingham JV, Kriedemann PE (1970) Effect of nutrient deficiencies on photosynthesis and respiration in spinach. Plant Soil 32:424–438

    Article  CAS  Google Scholar 

  • Bresson CC, Vitasse Y, Kremer A, Delzon S (2011) To what extent is altitudinal variation of functional traits driven by genetic adaptation in European oak and beech? Tree Physiol 31:1164–1174

    Article  CAS  PubMed  Google Scholar 

  • Brethes A (1984) Catalogue des stations forestières du nord de la Haute-Normandie Paris: Office National des Forêts

  • Brunet J, Fritz O, Richnau G (2010) Biodiversity in European beech forests—a review with recommendations for sustainable forest management. Ecol Bull 53:77–94

    Google Scholar 

  • Bussotti F, Bottacci A, Bartolesi A, Grossoni P, Tani C (1995) Morpho-anatomical alterations in leaves collected from beech trees (Fagus sylvatica L) in conditions of natural water stress. Environ Exp Bot 35:201–213

    Article  Google Scholar 

  • Bussotti F, Gravano E, Grossoni P, Tani C (1998) Occurrence of tannins in leaves of beech trees (Fagus sylvatica) along an ecological gradient detected by histochemical and ultrastructural analyses. New Phytol 138:469–479

    Article  CAS  Google Scholar 

  • Bussotti F, Pollastrini M, Holland V, Brueggemann W (2015) Functional traits and adaptive capacity of European forests to climate change. Environ Exp Bot 111:91–113

    Article  Google Scholar 

  • Callaway RM, Walker LR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78:1958–1965

    Article  Google Scholar 

  • Castagneyrol B, Regolini M, Jactel H (2014) Tree species composition rather than diversity triggers associational resistance to the pine processionary moth. Basic Appl Ecol 15:516–523

    Article  Google Scholar 

  • Cescatti A, Piutti E (1998) Silvicultural alternatives competition regime and sensitivity to climate in a European beech forest. Forest Ecol Manag 102:213–223

    Article  Google Scholar 

  • Cornelissen JHC, Lavorel S, Garnier E, Diaz 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. Aust J Bot 51:335–380

    Article  Google Scholar 

  • Cornelissen JHC, Quested HM, Logtestijn RSP, Perez-Harguindeguy N, Gwynn-Jones D, Diaz S, Callaghan TV, Press MC, Aerts R (2006) Foliar pH as a new plant trait: can it explain variation in foliar chemistry and carbon cycling processes among subarctic plant species and types? Oecologia 147:315–326

    Article  CAS  PubMed  Google Scholar 

  • de Bello F, Lavorel S, Albert CH, Thuiller W, Grigulis K, Dolezal J, Janecek S, Leps J (2011) Quantifying the relevance of intraspecific trait variability for functional diversity. Method Ecol Evol 2:163–174

    Article  Google Scholar 

  • del Rio M, Schuetze G, Pretzsch H (2014) Temporal variation of competition and facilitation in mixed species forests in Central Europe. Plant Biol 16:166–176

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • FAO 2006 World reference base for soil resources. Rome FAO

  • Freschet GT, Aerts R, Cornelissen JHC (2012) A plant economics spectrum of litter decomposability. Funct Ecol 26:56–65

    Article  Google Scholar 

  • Grigulis K, Lavorel S, Krainer U, Legay N, Baxendale C, Dumont M, Kastl E, Arnoldi C, Bardgett RD, Poly F, Pommier T, Schloter M, Tappeiner U, Bahn M, Clement J-C (2013) Relative contributions of plant traits and soil microbial properties to mountain grassland ecosystem services. J Ecol 101:47–57

    Article  Google Scholar 

  • Haettenschwiler S, Coq S, Barantal S, Handa IT (2011) Leaf traits and decomposition in tropical rainforests: revisiting some commonly held views and towards a new hypothesis. New Phytol 189:950–965

    Article  Google Scholar 

  • Ishii H, Asano S (2010) The role of crown architecture leaf phenology and photosynthetic activity in promoting complementary use of light among coexisting species in temperate forests. Ecol Res 25:715–722

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Jactel H, Brockerhoff EG (2007) Tree diversity reduces herbivory by forest insects. Ecol Lett 10:835–848

    Article  PubMed  Google Scholar 

  • Jamagne M, Bétrémieux R, Bégon JC, Mori A (1977) Quelques données sur la variabilité dans le milieu naturel de la réserve en eau des sols. Bull Tech Inf 324–325:627–641

    Google Scholar 

  • Kelty MJ, Larson BC (1992) The ecology of silviculture of mixed species forest. Kluwer Academic Publishers, New York

  • Knoke T, Seifert T (2008) Integrating selected ecological effects of mixed European beech-Norway spruce stands in bioeconomic modelling. Ecol Model 210:487–498

    Article  Google Scholar 

  • Lavorel S (2013) Plant functional effects on ecosystem services. J Ecol 101:4–8

    Article  Google Scholar 

  • Lecerf A, Chauvet E (2008) Intraspecific variability in leaf traits strongly affects alder leaf decomposition in a stream. Basic Appl Ecol 9:598–605

    Article  Google Scholar 

  • Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76

    Article  CAS  PubMed  Google Scholar 

  • McGill BJ, Enquist B, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185

    Article  PubMed  Google Scholar 

  • Mellert KH, Göttlein A (2012) Comparison of new foliar nutrient thresholds derived from van den Burg’s literature compilation with established central European references. Eur J For Res 131:1461–1472

    Article  Google Scholar 

  • Merlin M, Perot T, Perret S, Korboulewsky N, Vallet P (2015) Effects of stand composition and tree size on resistance and resilience to drought in sessile oak and Scots pine. Forest Ecol Manag 339:22–33

    Article  Google Scholar 

  • Miller R O (1998) High-temperature oxidation: Dry ashing. In: Handbook of reference methods for plant analysis. Boca Raton CRC Press, New York, pp 53–56

  • Nardini A, Peda G, La Rocca N (2012) Trade-offs between leaf hydraulic capacity and drought vulnerability: morpho-anatomical bases carbon costs and ecological consequences. New Phytol 196:788–798

    Article  PubMed  Google Scholar 

  • Nickmans H, Verheyen K, Guiz J, Jonard M, Ponette Q (2015) Effects of neighbourhood identity and diversity on the foliar nutrition of sessile oak and beech. Forest Ecol Manag 335:108–117

    Article  Google Scholar 

  • Paquette A, Messier C (2011) The effect of biodiversity on tree productivity: from temperate to boreal forests. Global Ecol Biogeogr 20:170–180

    Article  Google Scholar 

  • Pluess AR, Weber P (2012) Drought-adaptation potential in Fagus sylvatica: linking moisture availability with genetic diversity and dendrochronology. Plos One 7:e33636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poorter H, Niinemets U, 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 

  • Prescott CE, Vesterdal L, Pratt J, Venner KH, de Montigny LM, Trofymow JA (2000) Nutrient concentrations and nitrogen mineralization in forest floors of single species conifer plantations in coastal British Columbia. Can J Forest Res 30:1341–1352

    Article  CAS  Google Scholar 

  • Pretzsch H (2005) Diversity and productivity in forests: evidence from long-term experimental plots. In: Körner C, Schulze E-D, Scherer-Lorenzen M (eds) Forest diversity and function. Springer, Berlin, pp 41–64

    Chapter  Google Scholar 

  • Pretzsch H, Schütze G (2009) Transgressive overyielding in mixed compared with pure stands of Norway spruce and European beech in Central Europe: evidence on stand level and explanation on individual tree level. Eur J For Res 128:183–204

    Article  Google Scholar 

  • Pretzsch H, Block J, Dieler J, Dong PH, Kohnle U, Nagel J, Spellmann H, Zingg A (2010) Comparison between the productivity of pure and mixed stands of Norway spruce and European beech along an ecological gradient. Ann Forest Sci 67:712p1–712p12

  • Pretzsch H, Bielak K, Block J, Bruchwald A, Dieler J, Ehrhart H-P, Kohnle U, Nagel J, Spellmann H, Zasada M, Zingg A (2013) Productivity of mixed versus pure stands of oak (Quercus petraea (Matt) Liebl and Quercus robur L) and European beech (Fagus sylvatica L) along an ecological gradient. Eur J For Res 132:263–280

    Article  Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing Vienna R Foundation for statistical computing

  • Richards AE, Forrester DI, Bauhus J, Scherer-Lorenzen M (2010) The influence of mixed tree plantations on the nutrition of individual species: a review. Tree Physiol 30:1192–1208

    Article  PubMed  Google Scholar 

  • Robson TM, Sanchez-Gomez D, Javier Cano F, Aranda I (2012) Variation in functional leaf traits among beech provenances during a Spanish summer reflects the differences in their origin. Tree Genet Genomes 8:1111–1121

    Article  Google Scholar 

  • Rozendaal DMA, Hurtado VH, Poorter L (2006) Plasticity in leaf traits of 38 tropical tree species in response to light; relationships with light demand and adult stature. Funct Ecol 20:207–216

    Article  Google Scholar 

  • Sanchez-Gomez D, Robson TM, Gasco A, Gil-Pelegrin E, Aranda I (2013) Differences in the leaf functional traits of six beech (Fagus sylvatica L) populations are reflected in their response to water limitation. Environ Exp Bot 87:110–119

    Article  Google Scholar 

  • Sardin T, Bock J, Becquey J (2008) Les peuplements mélangés: enjeux et interrogations des gestionnaires. Revue Forestière Française 60:121–128

    Google Scholar 

  • Toigo M, Vallet P, Perot T, Bontemps J-D, Piedallu C, Courbaud B (2015) Overyielding in mixed forests decreases with site productivity. J Ecol 103:502–512

    Article  Google Scholar 

  • Trap J, Haettenschwiler S, Gattin I, Aubert M (2013a) Forest ageing: an unexpected driver of beech leaf litter quality variability in European forests with strong consequences on soil processes. Forest Ecol Manag 302:338–345

    Article  Google Scholar 

  • Trap J, Bureau F, Perez G, Aubert M (2013b) PLS-regressions highlight litter quality as the major predictor of humus form shift along forest maturation. Soil Biol Biochem 57:969–971

    Article  CAS  Google Scholar 

  • Vallet P, Perot T (2011) Silver fir stand productivity is enhanced when mixed with Norway spruce: evidence based on large-scale inventory data and a generic modelling approach. J Veg Sci 22:932–942

    Article  Google Scholar 

  • Van Soest P J (1994) Nutritional ecology of the ruminant, 2nd edn. New York Cornell University Press, New York

  • Vila M, Vayreda J, Comas L, Ibáñez JJ, Mata T, Obón B (2007) Species richness and wood production: a positive association in Mediterranean forests. Ecol Lett 10:241–250

    Article  PubMed  Google Scholar 

  • 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 worldwide leaf economics spectrum. Nature 428:821–827

    Article  CAS  PubMed  Google Scholar 

  • Youngentob KN, Zdenek C, van Gorsel E (2016) A simple and effective method to collect leaves and seeds from tall trees. Methods Ecol Evol. doi:10.1111/2041-210X.12554

    Google Scholar 

Download references

Acknowledgments

The authors would like to thank the ECODIV laboratory and especially Philippe Delporte and Marthe Apka-Vinceslas for technical help in soil and leaf analyses. This study was financially supported by GRR TERA and SFR SCALE (Haute-Normandie, France). TMR is funded by the Academy of Finland decision 266523.

Author information

Authors and Affiliations

  1. Ecodiv URA/EA-1293, Normandie Université, Université de Rouen, IRSTEA, SFR Scale 4116, UFR Sciences et Techniques, 76821, Mont Saint Aignan Cedex, France

    Estelle Forey, Estelle Langlois, Gauthier Lapa & Michaël Aubert

  2. UMR SPE CNRS 6134, Université de Corse Pasquale Paoli, 20250, Corte, France

    Gauthier Lapa

  3. Irstea – UR EFNO, 45290, Nogent-Sur-Vernisson, France

    Nathalie Korboulewsky

  4. Viikki Plant Science Centre (ViPS), Plant Biology Division, Dept Biosciences, University of Helsinki, PO Box 65, 00014, Helsinki, Finland

    T. Matthew Robson

Authors
  1. Estelle Forey
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Estelle Langlois
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gauthier Lapa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nathalie Korboulewsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. T. Matthew Robson
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Michaël Aubert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Estelle Forey.

Additional information

Handling Editor : Dr. Rainer Matyssek.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 857 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Forey, E., Langlois, E., Lapa, G. et al. Tree species richness induces strong intraspecific variability of beech (Fagus sylvatica) leaf traits and alleviates edaphic stress. Eur J Forest Res 135, 707–717 (2016). https://doi.org/10.1007/s10342-016-0966-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10342-016-0966-7

Keywords

Search

Navigation