European Journal of Forest Research

, Volume 124, Issue 2, pp 95–111 | Cite as

Climate and forest management influence nitrogen balance of European beech forests: microbial N transformations and inorganic N net uptake capacity of mycorrhizal roots

  • Arthur Geßler
  • Klaus Jung
  • Rainer Gasche
  • Hans Papen
  • Anita Heidenfelder
  • Eric Börner
  • Berthold Metzler
  • Sabine Augustin
  • Ernst Hildebrand
  • Heinz Rennenberg
Original Paper


The effects of local climate and silvicultural treatment on the inorganic N availability, net N uptake capacity of mycorrhizal beech roots and microbial N conversion were assessed in order to characterise changes in the partitioning of inorganic N between adult beech and soil microorganisms. Fine root dynamics, inorganic N in the soil solution and in soil extracts, nitrate and ammonium uptake kinetics of beech as well as gross ammonification, nitrification and denitrification rates were determined in a beech stand consisting of paired sites that mainly differed in aspect (SW vs. NE) and stand density (controls and thinning treatments). Nitrate was the only inorganic N form detectable in the soil water. Its concentration was high in control plots of the NE aspect, but only in canopy gaps and not influenced by thinning. Neither thinning nor aspect affected the abundance of root tips in the soil. Maximum nitrate net uptake by mycorrhizal fine roots of beech, however, differed with aspect, showing significantly lower values at the SW aspect with warm–dry local climate. There were no clear-cut significant effects of local climate or thinning on microbial N conversion, but a tendency towards higher ammonification and nitrification and lower denitrification rates on the untreated controls of the SW as compared to the NE aspect. Apparently, the observed sensitivity of beech towards reduced soil water availability is at least partially due to impaired N acquisition. This seems to be mainly a consequence of reduced N uptake capacity rather than of limited microbial re-supply of inorganic N or of changed patterns of inorganic N partitioning between soil bacteria and roots.


Nitrification Denitrification Ammonification Nitrate net uptake Fine root abundance Desorption solution 



This study was financially supported by the Deutsche Forschungsgemeinschaft (DFG; SFB 433). We wish to thank Marc Dressen, Kristine Haberer, Ilka Hetzger, Carola Holweg, Martin Kock, Michael Nahm and Michael Pfeiffer for their assistance in the field.


  1. Adam ML, Kelly JM, Graves WR, Dixon PM (2003) Net nitrate uptake by red maple is a function of root-zone temperature. J Plant Nutr 26:203–222Google Scholar
  2. Baeumler R, Zech W (1998) Soil solution chemistry and impact of forest thinning in mountain forests in the Bavarian Alps. For Ecol Manag 108:231–238Google Scholar
  3. Barraclough D, Puri G (1995) The use of 15N pool dilution and enrichment to separate the heterotrophic and autotrophic pathways of nitrification. Soil Biol Biochem 27:17–22Google Scholar
  4. Barrett DJ, Hatton TJ, Ash JE, Ball MC (1996) Transpiration of trees from contrasting forest types. Aust J Bot 44:249–263Google Scholar
  5. BassiriRad H (2000) Kinetics of nutrient uptake by roots: responses to global change. New Phytol 147:155–169Google Scholar
  6. BassiriRad H, Caldwell MM, Bilbrough C (1993) Effects of soil temperature and nitrogen status on kinetics of NO3—uptake by roots of field-grown Agropyron desertorum (Fisch. Ex link) Schult. New Phytol 123:485–489Google Scholar
  7. BassiriRad H, Griffin KL, Strain BR, Reynolds JF (1996) Effects of CO2 enrichment on growth and 15NH4+ uptake rates of loblolly pine and ponderosa pine seedlings. Tree Physiol 16:957–962Google Scholar
  8. BassiriRad H, Prior SA, Norby RJ, Rogers HH (1999) A field method of determining NH4+ and NO3 uptake kinetics in intact roots: effects of CO2 enrichment on trees and crop species. Plant Soil 217:195–204Google Scholar
  9. Blattner MS, Augustin S, Schack-Kirchner H, Hildebrand EE (2000) The desorption solution: an alternative approach to measure water soluble ions in soils. J Plant Nutr Soil Sci 163:583–587Google Scholar
  10. Breda N, Granier A, Aussenac G (1995) Effects of thinning on soil and tree water relations. Transpiration and growth in an oak forest (Quercus petraea (Matt) Liebl.). Tree Physiol 15:295–306Google Scholar
  11. Breuer L, Kiese R, Butterbach-Bahl K (2002) Temperature and moisture effects on nitrification rates in tropical rain-forest soils. Soil Sci Soc Am J 66:834–844Google Scholar
  12. Brooks PD, Stark JM, McInteer BB, Preston T (1989) Diffusion method to prepare soil extracts for automated nitrogen-15 analysis. Soil Sci Soc Am J 53:1707–1711Google Scholar
  13. Butterbach-Bahl K, Willibald G, Papen H (2002) Soil core method for direct simultaneous determination of N2 and N2O emissions from forest soils. Plant Soil 240:105–116Google Scholar
  14. Cerezo M, Tillard P, Gojon A, Primo-Millo E, Garcia-Agustin P (2001) Characterization and regulation of ammonium transport systems in Citrus plants. Planta 214:97–105Google Scholar
  15. Chapin FS III, Van Cleve K, Tryon PR (1986) Relationship of ion absorption to growth rate in taiga trees. Oecologia 69:238–242Google Scholar
  16. Davidson EA, Hart SC, Firestone MK (1992) Internal cycling of nitrate in soils of a mature coniferous forest. Ecology 73:1148–1156Google Scholar
  17. Drennan PM, Nobel PS (1997) Frequencies of major C3, C4 and CAM perennials on different slopes in the northwestern Sonoran Desert. Flora 192:297–304Google Scholar
  18. Ellenberg H (1992) Vegetation mitteleuropas mit den alpen. Eugen Ulmer, StuttgartGoogle Scholar
  19. Eno CF (1960) Nitrate production in the field by incubating the soil in polyethylene bags. Soil Sci Soc Am Proc 24:277–279Google Scholar
  20. Etherington JR (1982) Environment and plant ecology. Wiley, ChichesterGoogle Scholar
  21. Finlay RD, Ek R, Odham G, Söderström B (1988) Mycelial uptake, translocation and assimilation of nitrogen from 15N labelled ammonium by Pinus sylvestris plants infect. New Phytol 110:59–66Google Scholar
  22. Fotelli NM, 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 154:85–97Google Scholar
  23. Fotelli NM, Rennenberg H, Geßler A (2002b) Effects of drought on the competitive interference of an early successional species (Rubus fruticosus) on Fagus sylvatica L. seedlings: 15N uptake and partitioning, responses of amino acids and other N compounds. Plant Biol 4:311–320Google Scholar
  24. Fotelli MN, Rennenberg H, Holst T, Mayer H, Geßler A (2003) Effects of climate and silviculture on the carbon isotope composition of understorey species in a beech (Fagus sylvatica L.) forest. New Phytol 159:229–244Google Scholar
  25. Fotelli NM, Rienks M, Rennenberg H, Geßler A (2004) Climate and forest management affect 15N-uptake, N balance and biomass of European beech (Fagus sylvatica L.) seedlings. Trees 18:157–160Google Scholar
  26. Garnett TP, Smethurst PJ (1999) Ammonium and nitrate uptake by Eucalyptus nitens: effects of pH and temperature. Plant Soil 214:133–140Google Scholar
  27. Gasche R, Papen H (1999) A 3-year continuous record of nitrogen trace gas fluxes from untreated and limed soil of a N-saturated spruce and beech forest ecosystem in Germany 2. NO and NO2 fluxes. J Geophys Res 104:18505–18520Google Scholar
  28. Gasche R, Butterbach-Bahl K, Papen H (2002) Development and application of a method for determination of net nitrification rates. Plant Soil 240:57–65Google Scholar
  29. Geßler A, Schneider S, v. Sengbusch D, Weber P, Hanemann U, Huber C, Rothe A, Kreutzer K, Rennenberg H (1998a) Field and laboratory experiments on net uptake of nitrate and ammonium by the roots of spruce (Picea abies) and beech (Fagus sylvatica) trees. New Phytol 138:275–285Google Scholar
  30. 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 beech (Fagus sylvatica L.). New Phytol 50:653–664Google Scholar
  31. 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 24:23–32Google Scholar
  32. Geßler A, Keitel C, Nahm N, Rennenberg H (2004) Effects of water shortage on water and nitrogen balance in Central European beech forests. Plant Biol 6:289–298Google Scholar
  33. Gobert A, Plassard C (2002) Differential NO3-dependent patterns of NO3-uptake in Pinus pinaster, Rhizopogon roseolus and their ectomycorrhizal association. New Phytol 154:509–516Google Scholar
  34. Harley JL (1978) Ectomycorrhizas as nutrient absorbing organs. Proc R Soc Lond 203B:388–397Google Scholar
  35. Hart SC, Binkley D, Perry DA (1997) Influence of red alder on soil nitrogen transformations in two conifer forests of contrasting productivity. Soil Biol Biochem 29:1111–1123Google Scholar
  36. Hutchison LJ (1990) Studies on the systematics of ectomycorrhizal fungi in axenic culture. II. The enzymatic degradation of selected carbon and nitrogen compounds. Can J Bot 68:1522–1530Google Scholar
  37. Ingwersen J, Butterbach-Bahl K, Gasche R, Richter O, Papen H (1999) Barometric process separation: new method for quantifying nitrification, denitrification, and nitrous oxide sources in soils. Soil Sci Soc Am J 63:117–128Google Scholar
  38. IPCC (2001) Climate change 2001: impacts, adaptation and vulnerability. In: McCarthy JJ, Canziani OF, Leary NA, Dokken DJ, White KS (eds) Contribution of working group II to the third assessment report of the intergovernmental panel on climate change (IPCC). Cambridge University Press, CambridgeGoogle Scholar
  39. ISSS Working Group RB (1998) World reference base for soil resources: introduction. In: Deckers JA, Nachtergaele FO, Spaargaren OC (eds) International Society of Soil Science (ISSS), International Soil Reference and Information Centre (ISRIC) and Food and Agriculture Organization of the United Nations (FAO). ACCO, LeuvenGoogle Scholar
  40. Jaeger CH III, Monson RK, Fisk MC, Schmidt SK (1999) Seasonal partitioning of nitrogen by plants and soil microorganisms in an alpine ecosystem. Ecology 80:1883–1891Google Scholar
  41. Kamminga-Van Wijk C, Prins HBA (1993) The kinetics of NH4+ and NO3 uptake by Douglas fir from single N solutions containing both NH4+ and NO3. Plant Soil 151:91–106Google Scholar
  42. 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-time indicator for stomatal conductance of European beech (Fagus sylvatica L.). Plant Cell Environ 26:1157–1168Google Scholar
  43. Kiese R, Papen H, Zumbusch E, Butterbach-Bahl K (2002) Nitrification activity in tropical rain forest soils of the Coastal Lowlands and Atherton Tablelands, Queensland, Australia. J Plant Nutr Soil Sci 165:682–685Google Scholar
  44. Kirkham D, Bartholomew WV (1954) Equations for following nutrient transformations in soil, utilizing tracer data. Soil Sci Soc Am Proc 18:33–34Google Scholar
  45. 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
  46. Kreuzwieser J, Stulen I, Wiersema P, Vaalburg W, Rennenberg H. (2000) Nitrate transport processes in Fagus-Laccaria-Mycorrhizae. Plant Soil 220:107–117Google Scholar
  47. Kronzucker HJ, Siddiqi MY, Glass ADM (1995) Kinetics of NO3 influx in spruce. Plant Physiol 109:319–326Google Scholar
  48. Kronzucker HJ, Siddiqi MY, Glass ADM (1996) Kinetics of NH4+ influx in spruce. Plant Physiol 110:773–779Google Scholar
  49. Lainé P, Ourry A, MacDuff J, Boucaud J, Salette J (1993) Kinetic parameters of nitrate uptake by different cash crop species: effects of low temperatures or previous nitrate starvation. Physiol Plant 88:85–92Google Scholar
  50. Macduff JH, Jackson SB (1991) Growth and preferences for ammonium or nitrate uptake by barley in relation to root temperature. J Exp Bot 42:521–530Google Scholar
  51. Manderscheid B, Matzner E (1995) Spatial heterogeneity of soil solution chemistry in a mature Norway spruce (Picea abies (L.) Karst.) stand. Water Air Soil Pollut 85:1185–1190Google Scholar
  52. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, LondonGoogle Scholar
  53. Marschner H, Häussling M, George E (1991) Ammonium and nitrate uptake rates and rhizosphere pH in non-mycorrhizal roots of Norway spruce [Picea abies (L.) Karst.]. Trees 5:14–21Google Scholar
  54. Mary B, Recous S, Robin D (1998) A model for calculating nitrogen fluxes in soil using 15N tracing. Soil Biol Biochem 30:1963–1979Google Scholar
  55. Min X, Siddiqi MY, Guy RD, Glass ADM, Kronzucker HJ (2000) A comparative kinetic analysis of nitrate and ammonium influx in two early-successional tree species of temporal and boreal forest ecosystems. Plant Cell Environ 23:321–328Google Scholar
  56. Misson L, Vincke C, Devillez F (2003) Frequency responses of radial growth series after different thinning intensities in Norway spruce (Picea abies (L.) Karst.) stands. For Ecol Manag 177:51–63Google Scholar
  57. Moosmayer H-U (2002) Langfristige regionale Waldbauplanung in Baden-Württemberg—Grundlagen und Ergebnisse. Landesforstverwaltung Baden-Württemberg, StuttgartGoogle Scholar
  58. Nilsson L-O, Wiklund K (1994) Nitrogen uptake in a Norway spruce stand following ammonium sulphate application, fertigation, irrigation, drought and nitrogen-free-fertilisation. Plant Soil 164:221–229Google Scholar
  59. Nohrstedt HO, Sikstrom U, Ring E, Nasholm T, Hogberg P, Persson T, (1996) Nitrate in soil water in three Norway spruce stands in southwest Sweden as related to N-deposition and soil, stand, and foliage properties. Can J For Res 26:836–848Google Scholar
  60. Nye PH, Tinker P (1977) Solute movement in the soil-root system. University of California Press, BerkleyGoogle Scholar
  61. Papen H, Butterbach-Bahl K (1999) A 3-year continuous record of nitrogen trace gas fluxes from untreated and limed soil of a N-saturated spruce and beech forest ecosystem in Germany 1. N2O emissions. J Geophys Res 104:18487–18503Google Scholar
  62. Pedersen H, Dunkin KA, Firestone MK (1999) The relative importance of autotrophic and heterotrophic nitrification in a conifer forest soil as measured by 15N tracer and pool dilution techniques. Biogeochemistry 44:135–150Google Scholar
  63. Persson T, Wiren A (1993) Effects of experimental acidification on C and N mineralization in forest soils. Agri Ecosyst Environ 47:159–174Google Scholar
  64. Peuke AD, Schraml C, Hartung W, Rennenberg H (2002) Identification of drought-sensitive beech ecotypes by physiological parameters. New Phytol 154:373–387Google Scholar
  65. Plassard C, Chalot M, Botton B, Martin F (1997) Le rôle des ectomycorhizes dans la nutrition azotée des arbes forestiers. Rev For Fr 49:82–98Google Scholar
  66. Price NC, Stevens L (1989) Fundamentals of enzymology. Oxford University Press, OxfordGoogle Scholar
  67. Rennenberg H, Kreutzer K, Papen H, Weber P (1998) Consequences of high loads of nitrogen for spruce (Picea abies L.) and beech (Fagus sylvatica L.) forests. New Phytol 139:71–86Google Scholar
  68. Rennenberg H, Stoermer H, Weber P, Daum M, Papen H (2001) Competition of spruce trees for substrates of microbial N2O-production and -emission in a forest ecosystem. J Appl Bot 75:101–106Google Scholar
  69. Rothe A, Kreutzer K, Kuchenhoff H (2002) Influence of tree species composition on soil and soil solution properties in two mixed spruce-beech stands with contrasting history in Southern Germany. Plant Soil 240:47–56Google Scholar
  70. Schulze E-D (2000) The carbon and nitrogen cycle in forest ecosystems. In: Schulze E-D (ed) Ecological studies vol 142 carbon and nitrogen cycling in European forest ecosystems. Springer, Berlin Heidelberg New York, pp 3–13Google Scholar
  71. Segel IH (1975) Enzyme kinetics: behavior and analysis of rapid equilibrium and steady-state enzyme systems. Wiley, New York, pp 18–89Google Scholar
  72. Shi LB, Guttenberger M, Kottke I, Hampp R (2002) 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 12:303–311Google Scholar
  73. Silla F, Escudero A (2003) Uptake, demand and internal cycling of nitrogen in saplings of Mediterranean Quercus species. Oecologia 136:28–36Google Scholar
  74. Smart DR, Bloom AJ (1991) Influence of root NH4+ and NO3 content on the temperature response of net NH4+ and NO3 uptake in chilling sensitive and chilling resistant Lycopersicon taxa. J Exp Bot 42:331–338Google Scholar
  75. Tarp P, Helles F, Holten-Andersen P, Larsen JB, Strange N (2000) Modelling near-natural silvicultural regimes for beech—an economic sensitivity analysis. For Ecol Manag 130:187–198Google Scholar
  76. Thibodeau L, Raymond P, Camire C, Munson AD (2000) Impact of precommercial thinning in balsam fir stands on soil N dynamics, microbial biomass, decomposition, and foliar nutrition. Can J For Res 30:229–238Google Scholar
  77. Tietema A (1998) Microbial carbon and nitrogen dynamics in coniferous forest floor material collected along a European nitrogen deposition gradient. For Ecol Manag 101:29–36Google Scholar
  78. Verchot LV, Holmes Z, Mulon L, Groffman PM, Lovett GM (2001) Gross vs. net rates of N mineralization as indicators of functional differences between forest types. Soil Biol Biochem 33:1889–1901Google Scholar
  79. Woods PV, Nambiar EKS, Smethurst PJ (1990) Effect of annual weeds on water and nitrogen availability of Pinus radiata trees in a young plantation. For Ecol Manag 48:145–163Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Arthur Geßler
    • 1
  • Klaus Jung
    • 2
  • Rainer Gasche
    • 3
  • Hans Papen
    • 3
  • Anita Heidenfelder
    • 3
  • Eric Börner
    • 4
  • Berthold Metzler
    • 4
  • Sabine Augustin
    • 5
    • 6
  • Ernst Hildebrand
    • 5
  • Heinz Rennenberg
    • 1
  1. 1.Chair of Tree Physiology, Institute of Forest Botany and Tree PhysiologyAlbert Ludwigs University of FreiburgFreiburgGermany
  2. 2.UFZ Umweltforschungszentrum Leipzig-Halle GmbHCentre for Environmental ResearchLeipzigGermany
  3. 3.Institute for Meteorology and Climate Research, Atmospheric Environmental Research (IMK-IFU)Forschungszentrum Karlsruhe GmbHGarmisch-PartenkirchenGermany
  4. 4.Department of Forest ProtectionForestry Research Institute Baden-Wuerttemberg (FVA)FreiburgGermany
  5. 5.Institute of Soil Science and Forest NutritionUniversity of FreiburgFreiburgGermany
  6. 6.Federal Research Centre for Forestry and Forest ProductsInstitute for Forest Ecology and Forest InventoryEberswaldeGermany

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