, Volume 24, Issue 6, pp 1029–1043

Microclimatic conditions determined by stem density influence leaf anatomy and leaf physiology of beech (Fagus sylvatica L.) growing within stands that naturally regenerate from clear-cutting

  • Iván Closa
  • Juan José Irigoyen
  • Nieves Goicoechea
Original Paper


Beech forests naturally regenerating from clear-cutting can exhibit different microclimates depending on size of saplings and stem density. When beech trees are young and stem density is low, the level of radiation inside the ecosystem reaching the soil surface is high; consequently, air and soil temperatures rise and the soil water content may decrease. These microclimatic parameters presumably will affect the anatomy, photosynthesis, and carbon metabolism of beech leaves. We studied the morphology and physiology of sun and shade leaves of beech trees differing in age and growing within clear-cut areas with distinct microclimate. Results were compared with those of adult trees in an unmanaged forest. We selected a stand clear-cut in 2001 (14,000 trees ha−1), another clear-cut in 1996 (44,000 trees ha−1) and an unmanaged forest (1,000 trees ha−1). Photosynthetic photon flux density (PPFD) incident on sun leaves, air temperature, soil moisture, and soil temperature within the forests affected water status and carbohydrate storage in all trees. As trees became older, PPFD also influenced pigment composition and Rubisco activity in sun leaves. On the other hand, shade leaves from the oldest trees were the most sensitive to PPFD, air temperature, and soil moisture and temperature inside the forest. Contrariwise, microclimatic parameters slightly affected the physiology of shade leaves of the beech in the stand with the highest light attenuation. Air and soil temperatures were the parameters that most affected the photosynthetic pigments and carbohydrate storage in shade leaves of the youngest trees.


Beech Leaf anatomy Leaf physiology Microclimate Natural regeneration Rubisco 


  1. Amores G, Bermejo R, Elustondo D, Lasheras E, Santamaría JM (2006) Nutritional status of northern Spain beech forests. Water Air Soil Pollut 177:227–238CrossRefGoogle Scholar
  2. Barthod S, Epron D (2005) Variations of construction cost associated to leaf area renewal in saplings of two co-occurring temperate tree species Acer platanoides L. and Fraxinus excelsior L. along a light gradient. Ann Sci 62:545–551CrossRefGoogle Scholar
  3. Bethlenfalvay GJ, Brown MS, Franson RL (1990) The Glycine-Glomus-Bradyrhizobium symbiosis. X. Relationships between leaf gas exchange and plant and soil water status in nodulated, mycorrhizal soybean under drought stress. Plant Physiol 94:723–728CrossRefPubMedGoogle Scholar
  4. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  5. Čaňová I, Ďurkovič J, Hladká D (2008) Stomatal and chlorophyll fluorescence characteristics in European beech cultivars during leaf development. Biol Plantarum 52:577–581CrossRefGoogle Scholar
  6. Closa I, Goicoechea N (2010) Seasonal dynamics of the physicochemical and biological properties of soils in naturally regenerating, unmanaged and clear-cut beech stands in northern Spain. Eur J Soil Biol 46:190–199CrossRefGoogle Scholar
  7. Comstock JP, Ehleringer JR (1988) Contrasting photosynthetic behaviour in leaves and twigs of Hymenoclea salsola, a green-twigged warm desert shrub. Am J Bot 75:1360–1370CrossRefGoogle Scholar
  8. Cutter EG (1969) Plant anatomy: experiment and interpretation. Part I. Cells and tissues. Addison, Wesley, LondonGoogle Scholar
  9. Dale JE (1988) The control of leaf expansion. Annu Rev Plant Phys 39:267–295CrossRefGoogle Scholar
  10. Darwish DS, Fahmy GM (1997) Transpiration decline curves and stomatal characteristics of faba bean genotypes. Biol Plantarum 39:243–249CrossRefGoogle Scholar
  11. Ellenberg H (1988) Vegetation ecology of central Europe. Cambridge University Press, CambridgeGoogle Scholar
  12. Evans J (1988) Natural regeneration of broadleaves. Forestry Commission Bulletin No 78. HMSO, LondonGoogle Scholar
  13. García-Plazaola JI, Becerril JM (2000) Photoprotection mechanisms in European beech (Fagus sylvatica L.) seedlings from diverse climatic origins. Trees 14:339–343Google Scholar
  14. García-Plazaola JI, Becerril JM (2001) Seasonal changes in photosynthetic pigments and antioxidants in beech (Fagus sylvatica) in a Mediterranean climate: implications for tree decline diagnosis. Aust J Plant Physiol 28:225–232Google Scholar
  15. Geisler M, Nadeau J, Sack FD (2000) Oriented asymmetric divisions that generate the stomatal spacing pattern in Arabidopsis are disrupted by the too many mouths mutation. Plant Cell 12:2075–2086CrossRefPubMedGoogle Scholar
  16. Goicoechea N, Closa I, de Miguel A (2009) Ectomycorrhizal communities within beech (Fagus sylvatica L.) forests that naturally regenerate from clear-cutting in northern Spain. New Forests 38:157–175CrossRefGoogle Scholar
  17. Halldin S, Saugier B, Pontailler JY (1984) Evapotranspiration of a deciduous forest: simulation using routine meteorological data. J Hydrol 75:323–341CrossRefGoogle Scholar
  18. Hansen U, Fiedler B, Rank B (2002) Variation of pigment composition and antioxidative systems along the canopy light gradient in a mixed beech/oak forest: a comparative study on deciduous tree species differing in shade tolerance. Trees 16:354–364CrossRefGoogle Scholar
  19. Harmer R, Gill R (2000) Natural Regeneration in broadleaved woodlands: deer browsing and the establishment of advance regeneration. Information Note. Forestry Commission, 6 pp. Accessed online September, 2006:
  20. Harmer R, Morgan G (2007) Development of Quercus robur advance regeneration following canopy reduction in an oak woodland. Forestry 80:137–149CrossRefGoogle Scholar
  21. Harmer R, Kerr G, Boswell R (1997) Characteristics of lowland broadleaved woodland being restocked by natural regeneration. Forestry 70:199–209CrossRefGoogle Scholar
  22. Harmer R, Boswell R, Robertson M (2005) Survival and growth of tree seedlings in relation to changes in the ground flora during natural regeneration of an oak shelterwood. Forestry 78:21–32CrossRefGoogle Scholar
  23. Herbinger K, Ch Then, Löw M, Haberer K, Alexous M, Koch N, Remele K, Heerdt C, Grill D, Rennenberg H, Häberle K-H, Matyssek R, Tausz M, Wieser G (2005) Tree age dependence and within-canopy variation of leaf gas exchange and antioxidative defence in Fagus sylvatica under experimental free-air ozone exposure. Environ Pollut 137:476–482CrossRefPubMedGoogle Scholar
  24. Hovenden MJ, Vander Schoor JK (2003) Nature vs nurture in the leaf morphology of Southern beech, Nothofagus cunninghamii (Nothofagaceae). New Phytol 161:585–594CrossRefGoogle Scholar
  25. Jarvis CE, Walker JRL (1993) Simultaneous, rapid, spectrophotometric determination of total starch, amylose and amylopectin. J Sci Food Agric 63:53–57CrossRefGoogle Scholar
  26. Kerr G (2000) Natural regeneration of Corsican pine (Pinus nigra subsp. laricio) in Great Britain. Forestry 73:479–488CrossRefGoogle Scholar
  27. King DA (2003) Allocation of above-ground growth is related to light in temperate deciduous saplings. Funct Ecol 17:482–488CrossRefGoogle Scholar
  28. Kutsch WL, Herbst M, Vanselow R, Hummelshoj P, Jensen NO, Kappen L (2001) Stomatal acclimation influences water and carbon fluxes of a beech canopy in northern Germany. Basic Appl Ecol 2:265–281CrossRefGoogle Scholar
  29. Last FT, Pelham J, Mason PA, Ingleby K (1979) Influence of leaves on sporophore production by fungi forming sheathing mycorrhizas with Betula spp. Nature 280:168–169CrossRefGoogle Scholar
  30. Le Dantec V, Dufrene E, Saugier B (2000) Interannual and spatial variation in maximum leaf area index of temperate deciduous stands. Forest Ecol Manage 134:71–81CrossRefGoogle Scholar
  31. Leuchner C, Voβ S, Foetzki A, Clases Y (2006) Variation in leaf area index and stand mass of European beech across gradients of soil acidity and precipitation. Plant Ecol 182:247–258CrossRefGoogle Scholar
  32. Lichtenthaler HK (1981) Adaptation of leaves and chloroplasts to high quanta fluence rates. In: Akoyunoglou G (ed) Photosynthesis VI. Balaban International Science Service, Philadelphia, pp 273–285Google Scholar
  33. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In: Colowick SP, Kaplan NO (eds) Methods in enzymology, vol 148. Academic Press, San Diego, pp 350–382Google Scholar
  34. Lichtenthaler HK, Babani F (2004) Light adaptation and senescence of the photosynthetic apparatus. Changes in pigment composition, chlorophyll fluorescence parameters and photosynthetic activity. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis. Springer, Dordrecht, pp 713–736Google Scholar
  35. Lichtenthaler HK, Buschmann C, Döll M, Fietz HJ, Bach T, Kozel U, Meier D, Rahmsdorf U (1981) Photosynthetic activity, chloroplast ultrastructure, and leaf characteristics of high-light and low-light plants and of sun and shade leaves. Photosynth Res 2:115–141CrossRefGoogle Scholar
  36. Lichtenthaler HK, Ac A, Marek MV, Kalina J, Urban O (2007) Differences in pigment composition, photosynthetic rates and chlorophyll fluorescence images of sun and shade leaves of four tree species. Plant Physiol Biochem 45:577–588CrossRefPubMedGoogle Scholar
  37. Loidi J, Báscones JC (2006) Memoria del Mapa de Series de Vegetación de Navarra. E 1:200, 000. Departamento de Medio Ambiente. Ordenación del Territorio y Vivienda, Gobierno de Navarra, SpainGoogle Scholar
  38. Matschonat G, Falkengren-Grerup U (2000) Recovery of soil Ph. cation-exchange capacity and the saturation sites from stemflow-induced soil acidification in three Swedish beech (Fagus sylvatica L.) forests. Scand J For Res 15:39–48CrossRefGoogle Scholar
  39. Petritan AM, von Lüpke B, Petritan IC (2009) Influence of light availability on growth. Leaf morphology and plant architecture of beech (Fagus sylvatica L.), maple (Acer pseudoplatanus L.) and ash (Fraxinus excelsior L.) saplings. Eur J For Res 128:61–74Google Scholar
  40. Piper FI, Reyes-Díaz M, Corcuera LJ, Lusk CH (2009) Carbohydrate storage, survival, and growth of two evergreen Nothofagus species in two contrasting light environments. Ecol Res 24:1233–1241CrossRefGoogle Scholar
  41. Quisenberry JE, Roark B, McMichael BL (1982) Use of transpiration decline curves to identify drought-tolerant cotton germplasm. Crop Sci 22:918–922CrossRefGoogle Scholar
  42. Sarijeva G, Knapp M, Lichtenthaler HK (2007) Differences in photosynthetic activity, chlorophyll and carotenoid levels, and in chlorophyll fluorescence parameters in green sun and shade leaves of Ginkgo and Fagus. J Plant Physiol 164:950–955CrossRefPubMedGoogle Scholar
  43. Séstak Z, Càtsky J, Jarvis P (1971) Plant photosynthetic production. Manual of Methods. Dr Junk Publishers, The Hague, The NetherlandsGoogle Scholar
  44. Sharkey TD, Savitch LV, Butz ND (1991) Photometric method for routine determination of Kcat and carbamylation of rubisco. Photosynth Res 28:41–48CrossRefGoogle Scholar
  45. Smith SE, Gianinazzi-Pearson V (1988) Physiological interactions between symbionts in vesicular-arbuscular mycorrhizal plants. Annu Rev Plant Physiol 39:221–244CrossRefGoogle Scholar
  46. USDA (1999) Soil Taxonomy, 2nd edn. Agriculture Handbook number 436, United States Department of Agriculture, WashingtonGoogle Scholar
  47. Van der Hout P (2000) Testing the applicability of reduced impact logging in greenheart forest in Guyana. Int For Rev 2:24–32Google Scholar
  48. Von Stamm S (1994) Linked stomata and photosynthesis model for Corylus avellana (hazel). Ecol Model 75(76):345–357Google Scholar
  49. Weatherley PE (1950) Studies in the water relations of the cotton plant. I. The field measurements of water deficits in leaves. New Phytol 49:81–87CrossRefGoogle Scholar
  50. Wittmann C, Aschan G, Pfanz H (2001) Leaf and twig photosynthesis of young beech (Fagus sylvatica) and aspen (Populus tremula) trees grown under different light regime. Basic Appl Ecol 2:145–154CrossRefGoogle Scholar
  51. Wu L, Shinzato T, Kudo T, Ishigaki C, Aramoto M (2008) Characteristics of a 20-year-old evergreen broad-leaved forest restocked by natural regeneration after clearcut-burning. Ann For Sci 65:505CrossRefGoogle Scholar
  52. Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Iván Closa
    • 1
  • Juan José Irigoyen
    • 1
  • Nieves Goicoechea
    • 1
  1. 1.Departamento de Biología Vegetal, sección Biología Vegetal (Unidad Asociada al CSIC, EEAD, Zaragoza e ICVV, Logroño), Facultades de Ciencias y FarmaciaUniversidad de NavarraPamplonaSpain

Personalised recommendations