Plant Biol (Stuttg) 2006; 8(1): 52-63
DOI: 10.1055/s-2005-872988
Research Paper

Georg Thieme Verlag Stuttgart KG · New York

Physiological Performance of Beech (Fagus sylvatica L.) at its Southeastern Distribution Limit in Europe: Seasonal Changes in Nitrogen, Carbon and Water Balance

M. Nahm1 , K. Radoglou2 , G. Halyvopoulos2 , A. Geßler1 , 3 , H. Rennenberg1 , M. N. Fotelli2
  • 1Chair of Tree Physiology, Institute of Forest Botany and Tree Physiology, Albert Ludwig University of Freiburg, Georges Köhler Allee, Geb. 053/054, 79110 Freiburg i. Br., Germany
  • 2Forest Research Institute, National Agricultural Research Foundation, Vassilika 57006, Thessaloniki, Greece
  • 3Present address: School of Forest and Ecosystem Science, University of Melbourne, Water Street, Creswick, VIC 3363, Australia
Further Information

Publication History

Received: April 18, 2005

Accepted: October 18, 2005

Publication Date:
25 January 2006 (online)

Abstract

To assess the physiological performance of drought-sensitive European beech (Fagus sylvatica L.) under the dry Mediterranean climate prevailing at its southeastern distribution limit in Europe, we analyzed seasonal changes in carbon, nitrogen and water balance of naturally grown adult trees. We determined the foliar C and N contents, δ13C and δ18O signatures, total soluble non-protein nitrogen compounds (TSNN) in xylem, leaves, and phloem, as well as leaf water potential and photosynthetic quantum yield in northern Greece during 2003. Tissue sampling was performed in May, July, and September, while field measurements were conducted regularly. Climatic conditions for the 2003 growing season fall within the typical range of the studied area. The N- and C-related parameters displayed distinct seasonal courses. TSNN was highest in May in all tissues, and asparagine (Asn) was then the most abundant compound. Thereafter, TSNN decreased significantly in all tissues and both its concentration and composition remained constant in July and September. In both months, glutamate (Glu) prevailed in leaves, γ-aminobutyric acid (GABA) in phloem exudates from twigs and trunks, and arginine (Arg) in the xylem sap, where loading with amino acids was rather low during that period, amounting to only 0.8 µmol N ml-1 in September. Highest total foliar N and C contents were detected in May, and the elevated abundance of nutrients as well as an increased foliar δ13C signature at the beginning of the growing season is attributed to remobilization processes. The signatures of δ18O, quantum yield and leaf water potentials varied only slightly throughout the growing season. Although summer precipitation at the study site was considerably lower compared to what is usual for typical central European beech forests, no intensive drought responses of the physiological apparatus were detected in the studied beech trees. This suggests efficient internal regulation mechanisms, constantly ensuring a favourable physiological status under the relatively dry Mediterranean climate.

References

  • 1 Aranda I., Gil L., Pardos J. A.. Water relations and gas exchange in Fagus sylvatica L. and Quercus petraea (Mattuschka) Liebl. in a mixed stand at their southern limit of distribution in Europe.  Trees - Structure and Function. (2000);  14 344-352
  • 2 Barbour M. M., Fischer R. A., Sayre K. D., Farquhar G. D.. Oxygen isotope ratio of leaf and grain material correlates with stomatal conductance and grain yield in irrigated wheat.  Australian Journal of Plant Physiology. (2000);  27 625-637
  • 3 Bergmeier E., Dimopoulos P.. Fagus sylvatica forest vegetation in Greece: syntaxonomy and gradient analysis.  Journal of Vegetation Science. (2001);  12 109-126
  • 4 Caputo C., Barneix A. J.. Export of amino acids to the phloem in relation to N supply in wheat.  Physiologia Plantarum. (1997);  101 853-860
  • 5 Cermak J., Matyssek R., Kucera J.. Rapid response of large, drought-stressed beech trees to irrigation.  Tree Physiology. (1993);  12 281-290
  • 6 Cescatti A., Piutti E.. Silvicultural alternatives, competition regime and sensitivity to climate in a European beech forest.  Forest Ecology and Management. (1998);  102 213-223
  • 7 Collier M. D., Fotelli M. N., Nahm M., Kopriva S., Rennenberg H., Hanke D. E., Geßler A.. Regulation of nitrogen uptake by Fagus sylvatica on a whole plant level - interactions between cytokinins and soluble N compounds.  Plant, Cell and Environment. (2003);  26 1549-1560
  • 8 Cooper H. D., Clarkson D. T.. 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.  Journal of Experimental Botany. (1989);  40 753-762
  • 9 Damesin C., Lelarge C.. Carbon isotope composition of current-year shoots from Fagus sylvatica in relation to growth, respiration and use of reserves.  Plant, Cell and Environment. (2003);  26 207-219
  • 10 Dasilva M. C., Shelp B. J.. Xylem-to-phloem transfer of organic nitrogen in young soybean plants.  Plant Physiology. (1990);  92 797-801
  • 11 Ellenberg H.. Vegetation Mitteleuropas mit den Alpen. Stuttgart, Germany; Eugen Ulmer (1992)
  • 12 Farquhar G. D., Barbour M. M., Henry B. K.. Interpretation of oxygen isotope composition of leaf material. Griffiths, H., ed. Stable Isotopes: Integration of Biological, Ecological and Geochemical Processes. Oxford; BIOS Scientific Publishers (1998): 27-62
  • 13 Fotelli M. N., Geßler A., Peuke A. D., Rennenberg H.. 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 Phytologist. (2001);  151 427-435
  • 14 Fotelli M. N., Nahm M., Heidenfelder A., Papen H., Rennenberg H., Geßler A.. Soluble nonprotein nitrogen compounds indicate changes in the nitrogen status of beech seedlings due to climate and thinning.  New Phytologist. (2002 a);  154 85-97
  • 15 Fotelli M. N., Rennenberg H., Geßler A.. 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 Biology. (2002 b);  4 311-320
  • 16 Fotelli M. N., Rennenberg H., Holst T., Mayer H., Geßler A.. Carbon isotope composition of various tissues of beech (Fagus sylvatica) regeneration is indicative of recent environmental conditions within the forest understorey.  New Phytologist. (2003);  159 229-244
  • 17 Fotelli M. N., Rienks M., Rennenberg H., Geßler A.. Climate and forest management affect N‐15-uptake, N balance and biomass of European beech seedlings.  Trees - Structure and Function. (2004);  18 157-166
  • 18 Fotelli M., Rudolph P., Rennenberg H., Geßler A.. Irradiance and temperature affect the interference of the early successional Rubus fruticosus L. on the physiological performance of European beech seedlings.  New Phytologist. (2005);  165 453-462
  • 19 Frak E., Millard P., Le Roux X., Guillaumie S., Wendler R.. Coupling sap flow velocity and amino acid concentrations as an alternative method to N‐15 labeling for quantifying nitrogen remobilization by walnut trees.  Plant Physiology. (2002);  130 1043-1053
  • 20 Geßler A.. Untersuchungen zum Stickstoffhaushalt von Buchen (Fagus sylvatica) in einem stickstoffübersättigten Waldökosystem. PhD Thesis, University of Freiburg, Germany. (1999)
  • 21 Geßler A., Weber P., Schneider S., Rennenberg H.. Bidirectional exchange of amino compounds between phloem and xylem during long-distance transport in Norway spruce trees (Picea abies [L.] Karst).  Journal of Experimental Botany. (2003);  54 1389-1397
  • 22 Geßler A., Keitel C., Nahm M., Rennenberg H.. Water shortage affects the water and nitrogen balance in central European beech forests.  Plant Biology. (2004);  6 289-298
  • 23 Geßler A., Schneider S., Weber P., Hanemann U., Rennenberg H.. 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 Phytologist. (1998);  138 385-399
  • 24 Geßler A., Schrempp S., Matzarakis A., Mayer H., Rennenberg H., Adams M. A.. Radiation modifies the effect of water availability on the carbon isotope composition of beach (Fagus sylvatica). .  New Phytologist. (2001);  150 653-664
  • 25 Glavac V., Jochheim H.. A contribution to understanding the internal nitrogen budget of beech (Fagus sylvatica L.).  Trees. (1993);  7 237-241
  • 26 Grassi G., Millard P., Gioacchini P., Tagliavini M.. Recycling of nitrogen in the xylem of Prunus avium trees starts when spring remobilization of internal reserves declines.  Tree Physiology. (2003);  23 1061-1068
  • 27 Grassi G., Millard P., Wendler R., Minotta G., Tagliavini M.. Measurement of xylem sap amino acid concentrations in conjunction with whole tree transpiration estimates spring N remobilization by cherry (Prunus avium L.) trees.  Plant, Cell and Environment. (2002);  25 1689-1699
  • 28 Guak S., Neilsen D., Millard P., Wendler R., Neilsen G. H.. Determining the role of N remobilization for growth of apple (Malus domestica Borkh.) trees by measuring xylem-sap N flux.  Journal of Experimental Botany. (2003);  54 2121-2131
  • 29 Hayashi H., Chino M.. Nitrate and other anions in rice phloem sap.  Plant and Cell Physiology. (1985);  26 325-330
  • 30 Helle G., Schleser G. H.. 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 and Environment. (2004);  27 367-380
  • 31 IPCC .Climate Change 2001: Impacts, Adaptation and Vulnerability. http://www.IPCC.ch/wg2SPM.pdf (2001)
  • 32 Jäggi M., Saurer M., Fuhrer J., Siegwolf R.. Seasonality of delta O‐18 in needles and wood of Picea abies. .  New Phytologist. (2003);  158 51-59
  • 33 Kamphake L. J., Hannah S. A., Cohen J. M.. Automated analysis for nitrate by hydrazine reduction.  Water Research. (1967);  1 205-216
  • 34 Keitel C., Adams M. A., Holst T., Matzarakis A., Mayer H., Rennenberg H., Geßler A.. 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 and Environment. (2003);  26 1157-1168
  • 35 Kreuzwieser J., Herschbach C., Stulen I., Wiersema P., Vaalburg W., Rennenberg H.. Interactions of NH4 + and L-glutamate with NO3 - transport processes of non-mycorrhizal Fagus sylvatica roots.  Journal of Experimental Botany. (1997);  48 1431-1438
  • 36 Krom M. D.. Spectrophotometric determination of ammonia - a study of a modified Berthelot reaction using salicylate and dichloroisocyanurate.  Analyst. (1980);  105 305-316
  • 37 Lemoine D., Jacquemin S., Granier A.. Beech (Fagus sylvatica L.) branches show acclimation of xylem anatomy and hydraulic properties to increased light after thinning.  Annals of Forest Science. (2002);  59 761-766
  • 38 Leuzinger S., Zotz G., Asshoff R., Körner C.. Responses of deciduous forest trees to severe drought in Central Europe.  Tree Physiology. (2005);  25 641-650
  • 39 Marschner H.. Mineral Nutrition of Higher Plants. London; Academic Press (1995)
  • 40 Milios E.. Dynamics and development patterns of Pinus sylvestris L. - Fagus sylvatica L. stands in Central Rhodope.  Silva Gandavensis. (2000);  65 154-172
  • 41 Milios E.. The influence of stand development process on the height and volume growth of dominant Fagus sylvatica L. s. l. trees in the central Rhodope Mountains of north-eastern Greece.  Forestry. (2004);  77 17-26
  • 42 Milios E., Smiris P.. Structure and development patterns analysis of Fagus sylvatica s. l. - Quercus dalechampii Ten. stands in two araes in the Rhodope mountains of Xanthi region.  Silva Gandavensis. (2001);  66 1-15
  • 43 Millard P.. Ecophysiology of the internal cycling of nitrogen for tree growth.  Zeitschrift für Pflanzenernährung und Bodenkunde. (1996);  159 1-10
  • 44 Millard P., Wendler R., Hepburn A., Smith A.. Variations in the amino acid composition of xylem sap of Betula pendula Roth. trees due to remobilization of stored N in the spring.  Plant, Cell and Environment. (1998);  21 715-722
  • 45 Muller B., Touraine B., Rennenberg H.. Interaction between atmospheric and pedospheric nitrogen nutrition in spruce (Picea abies [L.] Karst.) seedlings.  Plant, Cell and Environment. (1996);  19 345-355
  • 46 Nahm M., Holst T., Matzarakis A., Mayer H., Rennenberg H., Geßler A.. Soluble N compound profiles and concentrations in European beech (Fagus sylvatica L.) are influenced by local climate and thinning.  European Journal of Forest Research. (2005);  in press
  • 48 Nordin A., Uggla C., Näsholm T.. Nitrogen forms in bark, wood and foliage of nitrogen-fertilized Pinus sylvestris. .  Tree Physiology. (2001);  21 59-64
  • 49 Penuelas J., Boada M.. A global change-induced biome shift in the Montseny mountains (NE Spain).  Global Change Biology. (2003);  9 131-140
  • 50 Peuke A. D., Schraml C., Hartung W., Rennenberg H.. Identification of drought-sensitive beech ecotypes by physiological parameters.  New Phytologist. (2002);  154 373-387
  • 51 Radoglou K., Raftoyannis Y.. Comparative physiological study of Fagus sylvatica and Quercus petraea in a natural mixed stand. Radoglou, K., ed. Proceedings of the International Conference on Forest Research: A Challenge for an Integrated European Approach, Vol. 1. Thessaloniki, Greece; NAGREF - Forest Research Institute (2001): 317-320
  • 52 Raftoyannis Y., Radoglou K.. Physiological responses of beech and sessile oak in a natural mixed stand during a dry summer.  Annals of Botany. (2002);  89 723-730
  • 53 Rebetez et al. M.. Heat and drought 2003: a climate analysis. In Impacts of the Drought and Heat in 2003 on Forests (Fakultät für Forst- und Umweltwissenschaften, Albert-Ludwigs-Universität Freiburg und Forstliche Versuchs- und Forschungsanstalt Baden-Württemberg [FVA], eds.), Proceedings of the Scientific Conference 17 - 19 Nov. 2004, Freiburg, Germany. (2004): 1
  • 54 Rennenberg H., Seiler W., Matyssek R., Geßler A., Kreuzwieser J.. Die Buche (Fagus sylvatica L.) - ein Waldbaum ohne Zukunft im südlichen Mitteleuropa?.  Allgemeine Forst und Jagdzeitung. (2004);  175 210-223
  • 55 Rennenberg H., Geßler A.. Consequences of N deposition to forest ecosystems - recent results and future research needs.  Water, Air and Soil Pollution. (1999);  116 47-64
  • 56 Rennenberg H., Kreutzer K., Papen H., Weber P.. Consequences of high loads of nitrogen for spruce (Picea abies) and beech (Fagus sylvatica) forests.  New Phytologist. (1998);  139 71-86
  • 57 Rennenberg H., Schneider S., Weber P.. Analysis of uptake and allocation of nitrogen and sulphur compounds by trees in the field.  Journal of Experimental Botany. (1996);  47 1491-1498
  • 58 Sabate S., Gracia C. A., Sanchez A.. Likely effects of climate change on growth of Quercus ilex, Pinus halepensis, Pinus pinaster, Pinus sylvestris and Fagus sylvatica forests in the Mediterranean region.  Forest Ecology and Management. (2002);  162 23-37
  • 59 Saurer M., Siegenthaler U., Schweingruber F.. The climate-carbon isotope relationship in tree-rings and the significance of site conditions.  Tellus Series B - Chemical and Physical Meteorology. (1995);  47 320-330
  • 60 Schär C., Vidale P. L., Lüthi D., Frei C., Häberli C., Liniger M. A., Appenzeller C.. The role of increasing temperature variability in European summer heatwaves.  Nature. (2004);  427 332-336
  • 61 Scheidegger Y., Saurer M., Bahn M., Siegwolf R.. Linking stable oxygen and carbon isotopes with stomatal conductance and photosynthetic capacity: a conceptual model.  Oecologia. (2000);  125 350-357
  • 62 Schipka K.. Blattwasserzustand und Wasserumsatz von vier Buchenwäldern entlang eines Niederschlagsgradienten in Mitteldeutschland. PhD Thesis, Georg-August-Universität Göttingen, Germany, http://webdoc.sub.gwdg.de/diss/2003/schipka. (2003)
  • 63 Schneider S., Geßler A., Weber P., von Sengbusch D., Hanemann U., Rennenberg H.. 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 Phytologist. (1996);  134 103-114
  • 64 Shi L. B., Guttenberger M., Kottke I., Hampp R.. The effect of drought on mycorrhizas of beech (Fagus sylvatica L.): changes in community structure, and the content of carbohydrates and nitrogen storage bodies of the fungi.  Mycorrhiza. (2002);  12 303-311
  • 65 Spiecker H., Kahle H.-P., Hauser S.. 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. University of Freiburg, Germany: Abschlussbericht des SFB 433. (2001): 307-334
  • 66 Tognetti R., Johnson J. D., Michelozzi M.. The response of European beech (Fagus sylvatica L.) seedlings from 2 Italian populations to drought and recovery.  Trees - Structure and Function. (1995);  9 348-354
  • 67 Turner N. C.. Measurement of plant water status by the pressure chamber technique.  Irrigation Science. (1988);  9 289-308
  • 68 Winter H., Lohaus G., Heldt W.. Phloem transport of amino acids in relation to their cytosolic levels in barley leaves.  Plant Physiology. (1992);  99 996-1004
  • 69 Zianis D., Mencuccini M.. Aboveground net primary productivity of a beech (Fagus moesiaca) forest: a case study of Naousa forest, northern Greece.  Tree Physiology. (2005);  25 713-722

M. N. Fotelli

Laboratory of Plant Physiology and Morphology
Department of Agricultural Biotechnology
Agricultural University of Athens

Iera Odos 75

118 55 Athens

Greece

Email: fotelli@in.gr

Email: fotelli@aua.gr

Editor: M. C. Ball

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