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Provenance plasticity of European beech leaf traits under differing environmental conditions at two Serbian common garden sites

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Abstract

Climate change will affect European beech (Fagus sylvatica L.) ecosystems negatively due to well-known vulnerability of this species to drought. Phenotypic plasticity has been recognized as the primary means in rapid acclimation to adverse environmental conditions. Provenance trials of forest tree species represent a valuable tool for assessing provenance adaptive potential to changing environments. In the present study, we examined the adaptive response capability (plasticity) of certain leaf anatomical traits in different European beech provenances to contrasting environmental conditions prevailing in two provenance trials. While one location of the trials is an isolated, marginal site, the other is a site within the original geographic range of beech forests in Serbia. The study involved 12 provenances originating from Austria, Bosnia and Herzegovina, Croatia, Germany, Hungary, Romania and Serbia. The results of the study evidenced that genetic differences of the provenances are mainly responsible for the differences in leaf traits. Cluster analysis showed absence of association between provenances from the same geographic regions (e.g., Germany and Balkan Peninsula, respectively), revealing phenotypic heterogeneity between them. Steep reaction norms, observed for anatomical traits studied, indicate the possibility of plastic provenance response to changes in environmental conditions. The highest values of plasticity index, observed for stomatal density and thicknesses of palisade and spongy parenchyma, seem to be the result of a regulative function of stomata and mesophyll structure on physiological adaptation to the unfavorable growth conditions at the marginal site. Such sclerophyllous leaf structures, indicating drought resistance, were observed in certain provenances from Central/Eastern Europe and mesic sites, indicating that beech provenances from warmer sites in Southern Europe may not necessarily be the only source of drought-resistant ecotypes.

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References

  • Aasamaa K, Sober A, Rahi M (2001) Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. Aust J Plant Physiol 28:765–774

    Google Scholar 

  • Ashton PMS, Berlyn GP (1994) A Comparison of leaf physiology and anatomy of quercus (section Erythrobalanus-Fagaceae) species in different light environments. Am J Bot 81:589–597

    Article  Google Scholar 

  • Avramov S, Pemac D, Tucic B (2007) Phenotypic plasticity in response to an irradiance gradient in Iris pumila: adaptive value and evolutionary constraints. Plant Ecol 190:275–290

    Article  Google Scholar 

  • Baquedano FJ, Valladares F, Castillo FJ (2008) Phenotypic plasticity blurs ecotypic divergence in the response of Quercus coccifera and Pinus halepensis to water stress. Eur J For Res 127:495–506

    Article  Google Scholar 

  • Bayramzadeh V, Funada R, Kubo T (2008) Relationships between vessel element anatomy and physiological as well as morphological traits of leaves in Fagus crenata seedlings originating from different provenances. Trees Struct Funct 22:217–224

    Article  Google Scholar 

  • Bayramzadeh V, Attarod P, Ahmadi MT, Ghadiri M, Akbari R, Safarkar T, Shirvany A (2011) Variation of leaf morphological traits in natural populations of Fagus orientalis Lipsky in the Caspian forests of Northern Iran. Ann For Res 55:33–42

    Google Scholar 

  • Bolte A, Czajkowski T, Kompa T (2007) The north-eastern distribution range of European beech—a review. Forestry 80:413–429

    Article  Google Scholar 

  • Buck AL (1981) New equations for computing vapor pressure and enhancement factor. J Appl Meteorol 20:1527–1532

    Article  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, Pancrazi M, Matteucci G, Gerosa G (2005) Leaf morphology and chemistry in Fagus sylvatica (beech) trees as affected by site factors and ozone: results from CONECOFOR permanent monitoring plots in Italy. Tree Physiol 25:211–219

    Article  CAS  PubMed  Google Scholar 

  • Campbell GS, Norman JM (1998) An introduction to environmental biophysics, 2nd edn. Springer, New York

    Book  Google Scholar 

  • Carins Murphy MR, Jordan GJ, Brodribb TJ (2014) Acclimation to humidity modifies the link between leaf size and the density of veins and stomata. Plant Cell Environ 37:124–131

    Article  CAS  PubMed  Google Scholar 

  • Casson S, Gray JE (2008) Influence of environmental factors on stomatal development. New Phytol 178:9–23

    Article  CAS  PubMed  Google Scholar 

  • Catoni R, Granata MU, Sartori F, Varone L, Gratani L (2015) Corylus avellana responsiveness to light variations: morphological, anatomical, and physiological leaf trait plasticity. Photosynthetica 53:35–46

    Article  Google Scholar 

  • Comps B, Thiebaut B, Sugar I, Trinajstic I, Plazibat M (1991) Genetic variation of the Croatian beech stands—spatial differentiation in connection with the environment. Ann Sci For 48:15–28

    Article  Google Scholar 

  • Cools N, De Vos B (2010) Sampling and analysis of soil. Manual part X. In: Manual on methods and criteria for harmonized sampling, assessment, monitoring and analysis of the effects of air pollution on forests. UNECE, ICP Forests, Hamburg, Germany

  • Cvjetićanin R (2003) Fitocenoze bukve u Srbiji. Šumarstvo 55:107–112 (in Serbian with English summary)

    Google Scholar 

  • Czajkowski T, Bolte A (2005) Unterschiedliche Reaktion deutscher und polnischer Herkünfte der Buche (Fagus sylvatica L.) auf Trockenheit. Allg Forst Jagdztg 177:30–40

    Google Scholar 

  • Davis ME, Shaw RG, Etterson JR (2005) Evolutionary responses to climate change. Ecology 86:1704–1714

    Article  Google Scholar 

  • Dunlap JM, Stettler RF (2001) Variation in leaf epidermal and stomatal traits of Populus trichocarpa from two transects across the Washington Cascades. Can J Bot 79:528–536

    Google Scholar 

  • Eilmann B, Sterck F, Wegner L, de Vries SMG, von Arx G, Mohren GMJ, den Ouden J, Sass-Klaassen U (2014) Wood structural differences between northern and southern beech provenances growing at a moderate site. Tree Physiol 34:882–893

    Article  CAS  PubMed  Google Scholar 

  • Ennajeh M, Vadel AM, Cochard H, Khemira H (2010) Comparative impacts of water stress on the leaf anatomy of a drought-resistant and a drought-sensitive olive cultivar. J Hortic Sci Biotech 85:289–294

    Google Scholar 

  • Evans JR, Von Caemmerer S, Setchell BA, Hudson GS (1994) The relationship between CO2 transfer and leaf anatomy in transgenic tobacco with a reduced content of Rubisco. Aust J Plant Physiol 21:475–495

    Article  CAS  Google Scholar 

  • Fraser HL, Greenall A, Carlyle C, Turkington R, Ross Friedman C (2009) Adaptive phenotypic plasticity of Pseudoroegneria spicata: response of stomatal density, leaf area and biomass to changes in water supply and increased temperature. Ann Bot Lond 103:769–775

    Article  Google Scholar 

  • Funk JL, Jones CG, Lerdau MT (2007) Leaf- and shoot-level plasticity in response to different nutrient and water availabilities. Tree Physiol 27:1731–1739

    Article  PubMed  Google Scholar 

  • García-Plazaola JI, Becerril JM (2000) Effects of drought on photoprotective mechanisms in European beech (Fagus sylvatica L.) seedlings from different provenances. Trees Struct Funct 14:485–490

    Article  Google Scholar 

  • Geßler A, Keitel C, Kreuzwieser J, Matyssek R, Seiler W, Rennenberg H (2007) Potential risks for European beech (Fagus sylvatica L.) in a changing climate. Trees Struct Funct 21:1–11

    Article  Google Scholar 

  • Ghalambor CK, Mckay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407

    Article  Google Scholar 

  • Giorio P, Sorrentino G, d’Andria R (1999) Stomatal behaviour leaf water status and photosynthetic response in field-grown olive trees under water deficit. Environ Exp Bot 42:95–104

    Article  Google Scholar 

  • Gitz DC, Baker JT (2009) Methods for creating stomatal impressions directly onto archivable slides. Agron J 101:232–236

    Article  Google Scholar 

  • Gömöry D, Paule L, Brus R, Zhelev P, Tomović Z, Gračan J (1999) Genetic differentiation and phylogeny of beech on the Balkan peninsula. J Evol Biol 12:746–754

    Article  Google Scholar 

  • Gratani L (2014) Plant phenotypic plasticity in response to environmental factors. Adv Bot. doi:10.1155/2014/20874

    Google Scholar 

  • Gratani L, Meneghini M, Pesoli P, Crescente MF (2003) Structural and functional plasticity of Quercus ilex seedlings of different provenances in Italy. Trees Struct Funct 17:515–521

    Article  Google Scholar 

  • Gratani L, Covone F, Larcher W (2006) Leaf plasticity in response to light of three evergreen species of the Mediterranean maquis. Trees Struct Funct 20:549–558

    Article  Google Scholar 

  • Gravano E, Bussotti F, Grossoni P, Tani C (1999) Morpho-anatomical and functional modifications in beech leaves on the top ridge of the Apennines (central Italy). Phyton Aust 39:41–46

    Google Scholar 

  • Günthardt-Goerg MS, Thomas K, Arend M, Vollenweider P (2013) Foliage response of young central European oaks to air warming, drought and soil type. Plant Biol 15:185–197

    Article  PubMed  Google Scholar 

  • Gutschick VP (1999) Biotic and abiotic consequences of differences in leaf structure. New Phytol 144:3–18

    Article  Google Scholar 

  • Hamanishi ET, Thomas BR, Campbell MM (2012) Drought induces alterations in the stomatal development program in Populus. J Exp Bot 63:695–709

    Article  Google Scholar 

  • Hazler K, Comps B, Šugar I, Melovski L, Tashev A, Gračan J (1997) Genetic structure of Fagus sylvatica L. Populations in southeastern Europe. Silvae Genet 46:229–236

    Google Scholar 

  • Hladká D, Čaňová I (2005) Morphological and physiological parameters of beech leaves (Fagus sylvatica L.) in research demonstration object Poľana. J For Sci 51:168–176

    Google Scholar 

  • Hlwatika CNM, Bhat RB (2002) An ecological interpretation of the difference in leaf anatomy and its plasticity in contrasting tree species in Orange Kloof, Table Mountain, South Africa. Ann Bot Lond 89:109–114

    Article  CAS  Google Scholar 

  • Horák R, Borišev M, Pilipović A, Orlović S, Pajević S, Nikolić N (2014) Drought impact on forest trees in four nature protected areas in Serbia. Šumar List 5–6:301–308

    Google Scholar 

  • Hovenden MJ, Vander Schoor JK, Osanai Y (2012) Relative humidity has dramatic impacts on leaf morphology but little effect on stomatal index or density in Nothofagus cunninghamii (Nothofagaceae). Aust J Bot 60:700–706

    Article  Google Scholar 

  • Ivanković M, Bogdan S, Božić G (2008) Varijabilnost visinskog rasta obične bukve (Fagus sylvatica L.) u testovima provenijencija u Hrvatskoj i Sloveniji. Šumar List 11–12:529–541

    Google Scholar 

  • Ivanković M, Popović M, Katičić I, Von Wuehlisch G, Bogdan S (2011) Kvantitativna genetska varijabilnost provenijencija obične bukve (Fagus sylvatica L.) iz jugoistočne Europe. Šumar List 135:25–37

    Google Scholar 

  • Jazbec A, Segotic K, Ivankovic M, Marjanovic H, Peric S (2007) Ranking of European beech provenances in Croatia using statistical analysis and analytical hierarchy process. Forestry 80:151–162

    Article  Google Scholar 

  • Jump AS, Hunt JM, Penuelas J (2006) Rapid climate change-related growth decline at the southern range edge of Fagus sylvatica. Glob Change Biol 12:2163–2174

    Article  Google Scholar 

  • Jump AS, Hunt JM, Penuelas J (2007) Climate relationships of growth and establishment across the altitudinal range of Fagus sylvatica in the Montseny mountains, northeast Spain. Ecoscience 14:507–518

    Article  Google Scholar 

  • Koike T, Maruyama Y (1998) Comparative ecophysiology of the leaf photosynthetic traits in Japanese beech grown in provenances facing the Pacific Ocean side and the sea side of Japan. J Phytogeogr Taxon 46:23–28

    Google Scholar 

  • Körner C (2011) The grand challenges in functional plant ecology. Front Plant Sci 2:1. doi:10.3389/fpls.2011.00001

    Article  PubMed Central  PubMed  Google Scholar 

  • Kramer K, Degen B, Buschbom J, Hickler T, Thuiller W, Sykes MT, de Winter W (2010) Modelling exploration of the future of European beech (Fagus sylvatica L.) under climate change—range, abundance, genetic diversity and adaptive response. For Ecol Manag 259:2213–2222

    Article  Google Scholar 

  • Krstić M, Medarević M, Lj Stojanović, Banković S (2002) Stanje i uzgojni problemi bukovih šuma severoistočne Srbije. Glasnik Šumarskog fakuleta 86:161–171 (in Serbian with English summary)

    Article  Google Scholar 

  • Laajimi NO, Boussadia O, Skhiri FH, Teixeira da Silva JA, Rezgui S, Hellali R (2011) Anatomical adaptations in vegetative structures of Apricot tree (Prunus armeniaca L.) cv. ‘Amor El Euch’ grown under water stress. Fruit. Veg Cereal Sci Biotechnol 5:46–51

    Google Scholar 

  • Lakatos F, Molnar M (2009) Mass mortality of beech on Southwest Hungary. Acta Silv Lign Hung 5:75–82

    Google Scholar 

  • Lake JA, Woodward FI (2008) Response of stomatal numbers to CO2 and humidity: control by transpiration rate and abscisic acid. New Phytol 179:397–404

    Article  CAS  PubMed  Google Scholar 

  • Lamy JB, Delzon S, Bouche PS, Alia R, Vendramin GG, Cochard H, Plomion C (2013) Limited genetic variability and phenotypic plasticity detected for cavitation resistance in a Mediterranean pine. New Phytol 201:874–886

    Article  PubMed  Google Scholar 

  • Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189

    Article  Google Scholar 

  • Lewis MC (1972) The physiological significance of variation in leaf structure. Sci Prog 60:25–51

    Google Scholar 

  • Lindner M, Maroschek M, Netherer S, Kremer A, Barbati A, Garcia-Gonzalo J, Seidl R, Delzon S, Corona P, Kolstrom M, Lexer M, Marchetti M (2010) Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems. For Ecol Manag 259:698–709

    Article  Google Scholar 

  • Ljungström M, Stjernquist I (1993) Factors toxic to beech (Fagus sylvatica L.) seedlings in acid soils. Plant Soil 157:19–29

    Article  Google Scholar 

  • Löf M, Bolte A, Welander NT (2005) Interacting effects of irradiance and water stress on dry weight and biomass partitioning in Fagus sylvatica seedlings. Scand J For Res 20:322–328

    Article  Google Scholar 

  • Luković J, Lj Merkulov, Pajević S, Zorić L, Nikolić N, Borišev M, Karanović D (2012) Quantitative assessment of effects of cadmium on the histological structure of poplar and willow leaves. Water Air Soil Pollut 223:2979–2993

    Article  Google Scholar 

  • Magri D, Vendramin GG, Comps B, Dupanloup I, Geburek T, Gömöry D, Latalowa M, Litt T, Paule L, Roure JM, Tantau I, van der Knaap WO, Petit RJ, de Beaulieu JL (2006) A new scenario for the Quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytol 171:199–221

    Article  CAS  PubMed  Google Scholar 

  • Makbul S, Saruhan Güler N, Durmuş N, Güven S (2011) Changes in anatomical and physiological parameters of soybean under drought stress. Turk J Bot 35:369–377

    Google Scholar 

  • Matesanz S, Gianoli E, Valladares F (2010) Global change and the evolution of phenotypic plasticity in plants. Ann NY Acad Sci 1206:35–55

    Article  PubMed  Google Scholar 

  • Matyas S (1994) Modeling climate change effects with provenance test data. Tree Physiol 14:797–804

    Article  PubMed  Google Scholar 

  • McLean EH, Prober SM, Stock WD, Steane DA, Potts BM, Vaillancourt RE, Byrne M (2014) Plasticity of functional traits varies clinally along a rainfall gradient in Eucalyptus tricarpa. Plant Cell Environ 37:1440–1451

    Article  CAS  PubMed  Google Scholar 

  • Meier IC, Leuschner C (2008a) Genotypic variation and phenotypic plasticity in the drought response of fine roots of European beech. Tree Physiol 28:297–309

    Article  PubMed  Google Scholar 

  • Meier IC, Leuschner C (2008b) Leaf size and leaf area index in Fagus sylvatica forests: competing effects of precipitation, temperature, and nitrogen availability. Ecosystems 11:655–669

    Article  CAS  Google Scholar 

  • Minotta G, Pinzauti S (1996) Effects of light and soil fertility on growth, leaf chlorophyll content and nutrient use efficiency of beech (Fagus sylvatica L.) seedlings. For Ecol Manag 86:61–71

    Article  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 15:684–692

    Article  CAS  PubMed  Google Scholar 

  • Nielsen CN, Jørgensen FV (2003) Phenology and diameter increment in seedlings of European beech (Fagus sylvatica L.) as affected by different soil water contents: variation between and within provenances. For Ecol Manag 174:233–249

    Article  Google Scholar 

  • Paule L (1995) Gene conservation in European beech (Fagus sylvatica L.). For Genet 2:161–170

    Google Scholar 

  • Pearce DW, Millard S, Bray DF, Rood SB (2005) Stomatal characteristics of riparian poplar species in a semi-arid environment. Tree Physiol 26:211–218

    Article  Google Scholar 

  • Petruccelli R, Ganino T, Ciaccheri L, Maselli F, Mariotti P (2013) Phenotypic diversity of traditional cherry accessions present in the Tuscan region. Sci Hortic 150:334–347

    Article  Google Scholar 

  • Piero Bruschi P, Grossoni P, Bussotti F (2003) Within- and among-tree variation in leaf morphology of Quercus petraea (Matt.) Liebl. natural populations. Trees Struct Funct 17:164–172

    Google Scholar 

  • Pluta S, Madryb W, Sieczkob L (2012) Phenotypic diversity for agronomic traits in a collection of blackcurrant (Ribes nigrum L.) cultivars evaluated in Poland. Sci Hortic 145:136–144

    Article  Google Scholar 

  • RHMZ (2012) Meteorološki godišnjak 1. Klimatološki podaci 2011. Republika Srbija. http://www.hidmet.gov.rs/

  • RHMZ (2013) Meteorološki godišnjak 1. Klimatološki podaci 2012. Republika Srbija. http://www.hidmet.gov.rs/

  • Richardson AD, Ashton PMS, Berlyn GP, McGroddy ME, Cameron IR (2001) Within-crown foliar plasticity of western hemlock, Tsuga heterophylla, in relation to stand age. Ann Bot Lond 88:1007–1015

    Article  Google Scholar 

  • Robson TM, Sánchez-Gómez D, Cano FJ, 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 

  • Rose L, Leuchner C, Köckemann B, Buschmann H (2009) Are marginal beech (Fagus sylvatica L.) provenances a source for drought tolerant ecotypes? Eur J For Res 128:335–343

    Article  Google Scholar 

  • SAS Institute, Inc (2011) SAS/STAT users guide, version 9.1.3. SAS Institute, Inc, Cary, NC

  • Shaw RG, Etterson JR (2012) Rapid climate change and the rate of adaptation: insight from experimental quantitative genetics. New Phytol 195:752–765

    Article  PubMed  Google Scholar 

  • Šijačić Nikolić M, Milovanović J, Nonić M, Knežević R, Stanković D (2013) Leaf morphometric characteristics variability of different beech provenances in juvenile development stage. Genetika 45:369–380

    Article  Google Scholar 

  • Štajner D, Orlović S, Popović B, Kebert M, Stojnić S, Klašnja B (2013) Chemical parameters of oxidative stress adaptability in beech. J Chem. doi:10.1155/2013/592695

    Google Scholar 

  • StatSoft, Inc (2012) STATISTICA (data analysis software system), version 12. www.statsoft.com

  • Stojanovic DB, Krzic A, Matovic B, Orlovic S, Duputie A, Djurdjevic V, Galic Z, Stojnic S (2013) Prediction of the European beech (Fagus sylvatica L.) xeric limit using a regional climate model: an example from southeast Europe. Agric For Meteorol 176:94–103

    Article  Google Scholar 

  • Stojnic S, Sass-Klaassen U, Orlovic S, Matovic B, Eilmann B (2013) Plastic growth response of European beech provenances to dry site conditions. IAWA J 34:475–484

    Article  Google Scholar 

  • Sulkowska M (2010) Genetic and ecotypic characterization of European beech (Fagus sylvatica L.) in Poland. Acta Silv Lign Hung 6:115–122

    Google Scholar 

  • Thiel D, Kreyling J, Backhaus S, Beierkuhnlein C, Buhk C, Egen K, Huber G, Konnert M, Nagy L, Jentsch A (2014) Different reactions of central and marginal provenances of Fagus sylvatica to experimental drought. Eur J For Res 133:247–260

    Article  Google Scholar 

  • Trentacoste ER, Puertas CM (2011) Preliminary characterization and morpho-agronomic evaluation of the olive germplasm collection of the Mendoza province (Argentina). Euphytica 177:99–109

    Article  Google Scholar 

  • Valladares F, Wright SJ, Lasso E, Kitajima K, Pearcy RW (2000) Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81:1925–1936

    Article  Google Scholar 

  • Valladares F, Chico J, Aranda I, Balaguer L, Dizengremel P, Manrique E, Dreyer E (2002) The greater seedling high-light tolerance of Quercus robur over Fagus sylvatica is linked to a greater physiological plasticity. Trees Struct Funct 16:395–403

    CAS  Google Scholar 

  • Vitasse Y, Bresson CC, Kremer A, Michalet R, Delzon S (2010) Quantifying phenological plasticity to temperature in two temperate tree species. Funct Ecol 24:1211–1218

    Article  Google Scholar 

  • von Wuehlisch G (2008) EUFORGEN technical guidelines for genetic conservation and use for European beech (Fagus sylvatica). Bioversity International, Rome

    Google Scholar 

  • von Wuehlisch G (2010) Introductory note. In: Frýdl J, Novotný P, Fennessy J, von Wühlisch G (eds) Genetic resources of beech in Europe—current state. Forestry and Game Management Research Institute, Prague, pp 8–9

    Google Scholar 

  • von Wuehlisch G, Liesebach M, Muhs HJ, Stephan R (1997) A network of international beech provenance trials. In: Turok J, Kremer A, de Vries S (eds) First EUFORGEN meeting on social broadleaves. International Plant Genetic Resources Institute, Rome, pp 164–172

    Google Scholar 

  • Wolf L (1950) Mikroskopicka tehnica. Statni zdravotnicke nakladatelstva, Praha

    Google Scholar 

  • Wyka T, Robakowski P, Żytkowiak R (2007) Acclimation of leaves to contrasting irradiance in juvenile trees differing in shade tolerance. Tree Physiol 27:1293–1306

    Article  CAS  PubMed  Google Scholar 

  • Wyka TP, Oleksyn J, Żytkowiak R, Karolewski P, Jagodziński AM, Reich PB (2012) Responses of leaf structure and photosynthetic properties to intra-canopy light gradients: a common garden test with four broadleaf deciduous angiosperm and seven evergreen conifer tree species. Oecologia 170:11–24

    Article  PubMed Central  PubMed  Google Scholar 

  • Xu Z, Zhou G (2008) Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. J Exp Bot 59:3317–3325

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zacchini M, Morini S, Vitagliano C (1997) Effect of photoperiod on some stomatal characteristics of in vitro cultured fruit tree shoots. Plant Cell Tissue Org 49:195–200

    Article  Google Scholar 

  • Zenni RD, Lamy J, Lamarque LJ, Porte AJ (2014) Adaptive evolution and phenotypic plasticity during naturalization and spread of invasive species: implications for tree invasion biology. Biol Invasions 16:635–644

    Article  Google Scholar 

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Acknowledgments

This paper was realized as a part of the project “Biosensing Technologies and Global System for Long-Term Research and Integrated Management of Ecosystems” (43002) financed by the Ministry of Education and Science of the Republic of Serbia within the framework of integrated and interdisciplinary research for the period 2011–2015.

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Correspondence to Srđan Stojnić.

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Communicated by Rainer Matyssek.

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Stojnić, S., Orlović, S., Miljković, D. et al. Provenance plasticity of European beech leaf traits under differing environmental conditions at two Serbian common garden sites. Eur J Forest Res 134, 1109–1125 (2015). https://doi.org/10.1007/s10342-015-0914-y

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