, 21:79 | Cite as

Seasonal courses of key parameters of nitrogen, carbon and water balance in European beech (Fagus sylvatica L.) grown on four different study sites along a European North–South climate gradient during the 2003 drought

  • Michael Nahm
  • Andreas Matzarakis
  • Heinz Rennenberg
  • Arthur GeßlerEmail author
Original Article


During the growing season of the exceptionally dry and warm year 2003, we assessed seasonal changes in nitrogen, carbon and water balance related parameters of mature naturally grown European beech (Fagus sylvatica L.) along a North–South transect in Europe that included a beech forest stand in central Germany, two in southern Germany and one in southern France. Indicators for N balance assessed at all four sites were foliar N contents and total soluble non-protein nitrogen compounds (TSNN) in xylem sap, leaves and phloem exudates; C and water balance related parameters determined were foliar C contents, δ13C and δ18O signatures. Tissue sampling was performed in May, July and September. The N related parameters displayed seasonal courses with highest concentrations during N remobilization in May. Decreased total foliar N contents as well as higher C/N ratios in the stands in central Germany and southern France compared to the other study sites point to an impaired N nutrition status due to lower soil N contents and precipitation perception. TSNN concentrations in leaves and phloem exudates of all study sites were in ranges previously reported, but xylem sap content of amino compounds in July was lower at all study sites when compared to literature data (c. 1 μmol N mL−1). In September, TSNN concentrations increased again at the two study sites in southern Germany after a rain event, whereas they remained constant at sites in central Germany and southern France which hardly perceived precipitation during that time. Thus, TSNN concentrations in the xylem sap might be indicative for water balance related N supply in the beech trees. TSNN profiles at all study sites, however, did not indicate drought stress. Foliar δ13C, but not foliar C and δ18O followed a seasonal trend at all study sites with highest values in May. Differences in foliar δ13C and δ18O did not reflect climatic differences between the sites, and are attributed to differences in altitude, photosynthesis and δ18O signatures of the water sources. Except of low TSNN concentrations in the xylem sap, no physiological indications of drought stress were detected in the trees analysed. We suppose that the other parameters assessed might not have been sensitive to the drought events because of efficient regulation mechanisms that provide a suitable physiological setting even under conditions of prolonged water limitation. The uniform performance of the trees from southern France and central Germany under comparably dry climate conditions denotes that the metabolic plasticity of mature beech from the different sites studied might be similar.


Mature European beech North–South transect Drought Total foliar N Amino compounds TSNN Xylem loading Climate 



We thank Dr. Thomas Holst and Prof. Dr. Helmut Mayer (Meteorological Institute, University of Freiburg) for providing the climatical data from the study sites in Tuttlingen. The climatical data from Chateaux-Arnoux-Saint-Auban near Sisteron were provided by Météo-France, Division des Etudes, Strasbourg, France; the data from Mühlhausen by Deutscher Wetterdienst, Referat Datenservice, Offenbach, Germany. We thank Landwirtschaftliches Labor Dr. Janssen in Gillersheim, Germany for the nitrate and ammonium measurements in soil extracts. Financial support by Deutsche Forschungsgemeinschaft (DFG) under contract number (Re515/13-1) is acknowledged.


  1. Adams MA, Grierson PF (2001) Stable isotopes at natural abundance in terrestrial plant ecology and ecophysiology: an update. Plant Biol 3:299–310CrossRefGoogle Scholar
  2. Barbour MM, Fischer RA, Sayre KD, Farquhar GD (2000) Oxygen isotope ratio of leaf and grain material correlates with stomatal conductance and grain yield in irrigated wheat. Aust J Plant Physiol 27:625–637Google Scholar
  3. Bauer G, Schulze ED, Mund M (1997) Nutrient contents and concentrations in relation to growth of Picea abies and Fagus sylvatica along a European transect. Tree Physiol 17:777–786PubMedGoogle Scholar
  4. Caputo C, Barneix AJ (1997) Export of amino acids to the phloem in relation to N supply in wheat. Physiologia Plantarum 101:853–860CrossRefGoogle Scholar
  5. Cermak J, Matyssek R, Kucera J (1993) Rapid response of large, drought-stressed beech trees to irrigation. Tree Physiol 12:281–290PubMedGoogle Scholar
  6. Collier MD, Fotelli MN, Nahm M, Kopriva S, Rennenberg H, Hanke DE, Geßler A (2003) Regulation of nitrogen uptake by Fagus sylvatica on a whole plant level— interactions between cytokinins and soluble N compounds. Plant Cell Environ 26:1549–1560CrossRefGoogle Scholar
  7. Cooper HD, Clarkson DT (1989) Cycling of amino-nitrogen and other nutrients between shoots and roots in cereals—a possible mechanism integrating shoot and root in the regulation of nutrient-uptake. J Exp Bot 40:753–762Google Scholar
  8. Cortufo MF, Miller M, Zeller B (2000) Litter decomposition. In: Schulze ED (ed) Carbon and nitrogen cycling in European forest ecosystems. Springer Verlag, Berlin, Germany, pp 276–296Google Scholar
  9. Damesin C, Lelarge C (2003) Carbon isotope composition of current-year shoots from Fagus sylvatica in relation to growth, respiration and use of reserves. Plant Cell Environ 26:207–219CrossRefGoogle Scholar
  10. Farquhar GD, Barbour MM, Henry BK (1998) Interpretation of oxygen isotope composition of leaf material. In: Griffiths H (ed) Stable isotopes: integration of biological, ecological and geochemical processes. BIOS Scientific Publishers, Oxford, pp 27–62Google Scholar
  11. Farquhar GD, O'Leary MH, Berry JA (1982) On the relationship between carbon isotope concentration and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9:121–137CrossRefGoogle Scholar
  12. Fink U, Brücher T, Krüger A, Leckebusch G, Pinto J, Ulbrich U, Adams MA (2004) The 2003 European summer heatwaves and drought—synoptic diagnosis and impacts. Weather 59:209–216CrossRefGoogle Scholar
  13. Fotelli MN, Geßler A, Peuke AD, Rennenberg H (2001) Drought affects the competitive interactions between Fagus sylvatica seedlings and an early successional species, Rubus fruticosus: responses of growth, water status and delta C-13 composition. New Phytol 151:427–435CrossRefGoogle Scholar
  14. Fotelli MN, Nahm M, Heidenfelder A, Papen H, Rennenberg H, Geßler A (2002a) Soluble nonprotein nitrogen compounds indicate changes in the nitrogen status of beech seedlings due to climate and thinning. New Phytol 154:85–97CrossRefGoogle Scholar
  15. Fotelli MN, Rennenberg H, Geßler A (2002b) Effects of drought on the competitive interference of an early successional species (Rubus fruticosus) on Fagus sylvatica L. seedlings: N-15 uptake and partitioning, responses of amino acids and other N compounds. Plant Biol 4:311–320CrossRefGoogle Scholar
  16. Fotelli MN, Rennenberg H, Holst T, Mayer H, Geßler A (2003) Carbon isotope composition of various tissues of beech (Fagus sylvatica) regeneration is indicative of recent environmental conditions within the forest understorey. New Phytol 159:229–244CrossRefGoogle Scholar
  17. Frak E, Millard P, Le Roux X, Guillaumie S, Wendler R (2002) Coupling sap flow velocity and amino acid concentrations as an alternative method to N-15 labeling for quantifying nitrogen remobilization by walnut trees. Plant Physiol 130:1043–1053PubMedCrossRefGoogle Scholar
  18. Fritsch J (1998) Energiebilanz und Verdunstung eines bewaldeten Hanges im Hochschwarzwald. Bericht des Meteorologischen Institutes der Universität Freiburg 1Google Scholar
  19. Garcia-Plazaola JI, Becerril JM (2000) Effects of drought on photoprotective mechanisms in European beech (Fagus sylvatica L.) seedlings from different provenances. Trees-Struct Funct 14:485–490Google Scholar
  20. Gauger T, Köble R, Spranger T, Bleeker A, Draaijers G (2001) Deposition loads of sulphur and nitrogen in Germany. Water Air Soil Pollut: Focus 1:353–373CrossRefGoogle Scholar
  21. Geßler A (1999) Untersuchungen zum Stickstoffhaushalt von Buchen (Fagus sylvatica) in einem stickstoffübersättigten Waldökosystem. PhD thesis, University of Freiburg, GermanyGoogle Scholar
  22. Geßler A, Duarte HM, Franco AC, Lüttge U, de Mattos EA, Nahm M, Rodrigues PJFP, Scarano FR, Rennenberg H (2005a) Ecophysiology of selected tree species in different plant communities at the periphery of the Atlantic forest of SE-Brazil. III: Three legume trees in a semi-deciduous dry forest. Trees 19:523–530CrossRefGoogle Scholar
  23. Geßler A, Weber P, Schneider S, Rennenberg H (2003) Bidirectional exchange of amino compounds between phloem and xylem during long-distance transport in Norway spruce trees (Picea abies [L.] Karst). J Exp Bot 54:1389–1397PubMedCrossRefGoogle Scholar
  24. Geßler A, Jung K, Gasche R, Papen H, Heidenfelder A, Borner E, Metzler B, Augustin S, Hildebrand E, Rennenberg H (2005b) Climate and forest management influence nitrogen balance of European beech forests: microbial N transformations and inorganic N net uptake capacity of mycorrhizal roots. Eur J For Res 124:95–111Google Scholar
  25. Geßler A, Keitel C, Nahm M, Rennenberg H (2004) Water shortage affects the water and nitrogen balance in central European beech forests. Plant Biol 6:289–298PubMedCrossRefGoogle Scholar
  26. Geßler A, Kreuzwieser J, Dopatka T, Rennenberg H (2002) Diurnal courses of ammonium net uptake by the roots of adult beech (Fagus sylvatica) and spruce (Picea abies) trees. Plant Soil 240:23–32CrossRefGoogle Scholar
  27. Geßler A, Rennenberg H (2000) The effect of liming on the soluble nitrogen pool in Norway spruce (Picea abies) exposed to high loads of nitrogen. Phyton-Annales Rei Botanicae 40:51–64Google Scholar
  28. Geßler A, Schneider S, Weber P, Hanemann U, Rennenberg H (1998) Soluble N compounds in trees exposed to high loads of N: a comparison between the roots of Norway spruce (Picea abies) and beech (Fagus sylvatica) trees grown under field conditions. New Phytol 138:385–399CrossRefGoogle Scholar
  29. Geßler A, Schrempp S, Matzarakis A, Mayer H, Rennenberg H, Adams MA (2001) Radiation modifies the effect of water availability on the carbon isotope composition of beach (Fagus sylvatica). New Phytol 150:653–664CrossRefGoogle Scholar
  30. Glavac V, Jochheim H (1993) A contribution to understanding the internal nitrogen budget of beech (Fagus sylvatica L). Trees-Struct Funct 7:237–241Google Scholar
  31. Gruber F (2001) Wachstum von Altbuchen (Fagus sylvatica L.) auf einem Kalkstandort (Göttingen/Södderich) in Abhängigkeit von der Witterung. Allgemeine Forst- und Jagd-Zeitung 173:117–122Google Scholar
  32. Hayashi H, Chino M (1985) Nitrate and other anions in rice phloem sap. Plant Cell Physiol 26:325–330Google Scholar
  33. Helle G, Schleser GH (2004) Beyond CO2-fixation by Rubisco—an interpretation of C-13/C-12 variations in tree rings from novel intra-seasonal studies on broad-leaf trees. Plant Cell Environ 27:367–380CrossRefGoogle Scholar
  34. Holst T, Mayer H, Schindler D (2004) Microclimate within beech stands—Part II: Thermal conditions. Eur J For Res 123:13–28Google Scholar
  35. Hultine KR, Marshall JD (2000) Altitude trends in conifer leaf morphology and stable carbon isotope composition. Oecologia 123:32–40CrossRefGoogle Scholar
  36. IPCC (2001) Climate change 2001 impacts, adaptation and vulnerability. Scholar
  37. Jäggi M, Saurer M, Fuhrer J, Siegwolf R (2003) Seasonality of delta O-18 in needles and wood of Picea abies. New Phytol 158:51–59CrossRefGoogle Scholar
  38. Kamphake LJ, Hannah SA, Cohen JM (1967) Automated analysis for nitrate by hydrazine reduction. Water Res 1:205–216CrossRefGoogle Scholar
  39. Keitel C (2004) Isotope signatures (d13C,18O, d15N) as a measure of environmental effects on the physiology of trees in the northern and southern hemispheres. PhD thesis, University of Freiburg, GermanyGoogle Scholar
  40. Keitel C, Adams MA, Holst T, Matzarakis A, Mayer H, Rennenberg H, Geßler A (2003) Carbon and oxygen isotope composition of organic compounds in the phloem sap provides a short-term measure for stomatal conductance of European beech (Fagus sylvatica L.). Plant Cell Environ 26:1157–1168CrossRefGoogle Scholar
  41. Keitel C, Matzarakis A, Rennenberg H, Gessler A (2006) Carbon isotope composition and oxygen isotope enrichment in phloem and total leaf organic matter of European beech (Fagus sylvatica L.) along a climate gradient. Plant Cell Environ 23:1432–1507Google Scholar
  42. Körner C, Farquhar GD, Roksandic Z (1988) A global survey of carbon isotope discrimination in plants from high-altitude. Oecologia 74:623–632CrossRefGoogle Scholar
  43. Korol RL, Kirschbaum MUF, Farquhar GD, Jeffreys M (1999) Effects of water status and soil fertility on the C-isotope signature in Pinus radiata. Tree Physiol 19:551–562PubMedGoogle Scholar
  44. Kreuzwieser J, Herschbach C, Stulen I, Wiersema P, Vaalburg W, Rennenberg H (1997) Interactions of NH4 + and L-glutamate with NO3 transport processes of non-mycorrhizal Fagus sylvatica roots. J Exp Bot 48:1431–1438Google Scholar
  45. Krom MD (1980) Spectrophotometric determination of ammonia—a study of a modified Berthelot reaction using salicylate and dichloroisocyanurate. Analyst 105:305–316CrossRefGoogle Scholar
  46. Leuzinger S, Zotz G, Asshoff R, Körner C (2005) Responses of deciduous forest trees to severe drought in Central Europe. Tree Physiol 25:641–650PubMedGoogle Scholar
  47. Livingston NJ, Spittlehouse DL (1996) Carbon isotope fractionation in tree ring early and late wood in relation to intra-growing season water balance. Plant Cell Environ 19:768–774CrossRefGoogle Scholar
  48. Matzarakis A, Mayer H, Schindler D, Fritsch J (2000) Simulation des Wasserhaushaltes eines Buchenwaldes mit dem forstlichen Wasserhaushaltsmodell WBS3. Ber Meteorol Inst Univ Freiburg 5:137–146Google Scholar
  49. Mayer H, Holst T, Schindler D (2002) Mikroklima in Buchenbeständen—Teil 1: Photosynthetisch aktive Strahlung. Forstwissenschaftliches Centralblatt 121:301–321CrossRefGoogle Scholar
  50. Millard P (1996) Ecophysiology of the internal cycling of nitrogen for tree growth. Zeitschrift fur Pflanzenernahrung und Bodenkunde 159:1–10Google Scholar
  51. Muller B, Touraine B, Rennenberg H (1996) Interaction between atmospheric and pedospheric nitrogen nutrition in spruce (Picea abies L. Karst) seedlings. Plant Cell Environ 19:345–355CrossRefGoogle Scholar
  52. Nahm M, Holst T, Matzarakis A, Mayer H, Rennenberg H, Geßler A (2005a) Soluble N compound profiles and concentrations in European beech (Fagus sylvatica L.) are influenced by local climate and thinning. Eur J For Res 125:1–14Google Scholar
  53. Nahm M, Radoglou K, Halyvopoulos G, Geßler A, Rennenberg H, Fotelli MN (2005b) Seasonal changes in nitrogen, carbon and water balance of adult Fagus sylvatica L. grown at its south-eastern distribution limit in Europe. Plant Biol 8:52–63CrossRefGoogle Scholar
  54. Nambiar EKS, Sands R (1993) Competition for water and nutrients in forests. Can J For Res 23:1955–1968Google Scholar
  55. Nielsen CN, Jorgensen 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 Manage 174:233–249CrossRefGoogle Scholar
  56. Nordin A, Uggla C, Näsholm T (2001) Nitrogen forms in bark, wood and foliage of nitrogen-fertilized Pinus sylvestris. Tree Physiol 21:59–64PubMedGoogle Scholar
  57. Pahlsson AMB (1992) Influence of nitrogen-fertilization on minerals, carbohydrates, amino-acids and phenolic-compounds in beech (Fagus sylvatica L.) leaves. Tree Physiol 10:93–100PubMedGoogle Scholar
  58. Penuelas J, Boada M (2003) A global change-induced biome shift in the Montseny mountains (NE Spain). Global Change Biol 9:131–140CrossRefGoogle Scholar
  59. Peuke AD, Schraml C, Hartung W, Rennenberg H (2002) Identification of drought-sensitive beech ecotypes by physiological parameters. New Phytol 154:373–387CrossRefGoogle Scholar
  60. Peuke AD, Rennenberg H (2004) Carbon, nitrogen, phosphorus, and sulphur concentration and partitioning in beech ecotypes (Fagus sylvatica L.): phosphorus most affected by drought. Trees 18:639–648CrossRefGoogle Scholar
  61. Raftoyannis Y, Radoglou K (2002) Physiological responses of beech and sessile oak in a natural mixed stand during a dry summer. Ann Bot 89:723–730PubMedCrossRefGoogle Scholar
  62. Rebetez M, et al. (2004) Heat and drought 2003: a climate analysis. In: Impacts of the drought and heat in 2003 on forests (eds A-L-UF Fakultät für Forst- und Umweltwissenschaften & F Forstliche Versuchs- und Forschungsanstalt Baden-Württemberg (FVA)), Proceedings of the scientific conference, Freiburg, Germany p 1Google Scholar
  63. Rennenberg H, Seiler W, Matyssek R, Geßler A, Kreuzwieser J (2004) Die Buche (Fagus sylvatica L.)—ein Waldbaum ohne Zukunft im südlichen Mitteleuropa? Allgemeine Forst und Jagdzeitung 175. Jg.:210–223Google Scholar
  64. Rennenberg H, Schneider S, Weber P (1996) Analysis of uptake and allocation of nitrogen and sulphur compounds by trees in the field. J Exp Bot 47:1491–1498Google Scholar
  65. Scarano FR, Duarte HM, Franco AC, Geßler A, de Mattos EA, Nahm M, Rennenberg H, Zaluar HLT, Lüttge U (2005) Ecophysiology of selected tree species in different plant communities at the periphery of the Atlantic forest of SE-Brazil. I: Performance of three different species of Clusia in an array of plant communities. Trees 19:497–509CrossRefGoogle Scholar
  66. Schär C, Vidale PL, Lüthi D, Frei C, Häberli C, Liniger MA, Appenzeller C (2004) The role of increasing temperature variability in European summer heatwaves. Nature 427:332–336PubMedCrossRefGoogle Scholar
  67. Scheidegger Y, Saurer M, Bahn M, Siegwolf R (2000) Linking stable oxygen and carbon isotopes with stomatal conductance and photosynthetic capacity: a conceptual model. Oecologia 125:350–357CrossRefGoogle Scholar
  68. Schneider S, Geßler A, Weber P, vonSengbusch D, Hanemann U, Rennenberg H (1996) Soluble N compounds in trees exposed to high loads of N: a comparison of spruce (Picea abies) and beech (Fagus sylvatica) grown under field conditions. New Phytol 134:103–114CrossRefGoogle Scholar
  69. Sparks JP, Ehleringer JR (1997) Leaf carbon isotope discrimination and nitrogen content for riparian trees along elevational transects. Oecologia 109:362–367CrossRefGoogle Scholar
  70. Spiecker H, Kahle H-P, Hauser S (2001) Klima und Witterung als Einflußfaktoren auf das Baumwachstum in Laubwäldern: Retrospektive Analysen und Monitoring. In: Buchendominierte Laubwälder unter dem Einfluss von Klima und Bewirtschaftung: Ökologische, waldbauliche und sozialwissenschaftliche Analysen. Abschlussbericht des SFB 433. University of Freiburg, Germany, pp 307–334Google Scholar
  71. Tognetti R, Johnson JD, Michelozzi M (1995) The response of European beech (Fagus sylvatica L.) seedlings from 2 Italian populations to drought and recovery. Trees-Struct Funct 9:348–354Google Scholar
  72. Winter H, Lohaus G, Heldt W (1992) Phloem transport of amino acids in relation to their cytosolic levels in barley leaves. Plant Physiol 99:996–1004PubMedCrossRefGoogle Scholar
  73. Yakir D (1992) Variations in the natural abundance of O-18 and Deuterium in plant carbohydrates. Plant Cell Environ 15:1005–1020CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Michael Nahm
    • 1
  • Andreas Matzarakis
    • 2
  • Heinz Rennenberg
    • 1
  • Arthur Geßler
    • 3
    • 4
    Email author
  1. 1.Institute of Forest Botany and Tree PhysiologyAlbert Ludwigs University of FreiburgFreiburgGermany
  2. 2.Meteorological InstituteAlbert Ludwigs University of FreiburgFreiburgGermany
  3. 3.Institut National de la Recherche Agronomique (INRA)Centre de Recherche de NancyChampenouxFrance
  4. 4.Zentrum für Biosystem analyse, Core Facility MetabolomicsAlbert Ludwigs University of FreiburgFreiburgGermany

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