Plant and Soil

, Volume 369, Issue 1–2, pp 657–668 | Cite as

Minor contribution of leaf litter to N nutrition of beech (Fagus sylvatica) seedlings in a mountainous beech forest of Southern Germany

  • Chanjuan Guo
  • Judy Simon
  • Rainer Gasche
  • Pascale Sarah Naumann
  • Carolin Bimüller
  • Rodica Pena
  • Andrea Polle
  • Ingrid Kögel-Knabner
  • Bernd Zeller
  • Heinz Rennenberg
  • Michael DannenmannEmail author
Regular Article



Our aims were to characterize the fate of leaf-litter-derived nitrogen in the plant-soil-microbe system of a temperate beech forest of Southern Germany and to identify its importance for N nutrition of beech seedlings.


15N-labelled leaf litter was traced in situ into abiotic and biotic N pools in mineral soil as well as into beech seedlings and mycorrhizal root tips over three growing seasons.


There was a rapid transfer of 15N into the mineral soil already 21 days after tracer application with soil microbial biomass initially representing the dominant litter-N sink. However, 15N recovery in non-extractable soil N pools strongly increased over time and subsequently became the dominant 15N sink. Recovery in plant biomass accounted for only 0.025 % of 15N excess after 876 days. After three growing seasons, 15N excess recovery was characterized by the following sequence: non-extractable soil N >> extractable soil N including microbial biomass >> plant biomass > ectomycorrhizal root tips.


After quick vertical dislocation and cycling through microbial N pools, there was a rapid stabilization of leaf-litter-derived N in non-extractable N pools of the mineral soil. Very low 15N recovery in beech seedlings suggests a high importance of other N sources such as root litter for N nutrition of beech understorey.


Nitrogen cycling Beech 15N-labelled leaf litter 15N tracing Microbial biomass Ectomycorrhiza 



Funding of this work by the German Research Foundation/Deutsche Forschungsgemeinschaft (DFG) within the framework of the Beech Research Group under contract numbers FOR 788/1, KO 1035/29-1, RE 515/27-1 and PO 362/17-1 as well as the follow-up joint proposal under the contract numbers KO 1035/41-1, RE 515/33-1 and DA 1217/2-1 is gratefully acknowledged. Chanjuan Guo was financially supported by a scholarship from the China Scholarship Council (no. 2007U27036). Judy Simon was financially supported by the European Social Fund and by the Ministry of Science, Research and the Arts Baden-Württemberg. We like to acknowledge Martin Leberecht for help during sampling and Franz Buegger and Rudolf Meier for conducting stable isotope analyses. Furthermore we are grateful to Vitomira Erac and Regina Wiegel for help with laboratory work.


  1. Allen AS, Andrews JA, Finzi AC, Matamala R, Richter DD, Schlesinger WH (2000) Effects of free-air CO2 enrichment (FACE) on belowground processes in a Pinus taeda forest. Ecol Appl 10:437–448Google Scholar
  2. Bimüller C, Naumann PS, Buegger F, Dannenmann M, Zeller B, Kögel-Knabner I (2013) Rapid transfer of 15N from labelled beech leaf litter to functional soil organic matter fractions in a Rendzic Leptosol. Soil Biol Biochem, in pressGoogle Scholar
  3. Buchmann N, Gebauer G, Schulze ED (1996) Partitioning of 15N-labeled ammonium and nitrate among soil, litter, below- and above-ground biomass of trees and understory in a 15-year-old Picea abies plantation. Biogeochem 33:1–23Google Scholar
  4. Butterbach-Bahl K, Gundersen P, Ambus P, Augustin J, Beier C, Boeckx P, Dannenmann M, Gimeno BS, Kiese R, Kitzler B, Ibrom A, Rees RM, Smith K, Stevens C, Vesala T, Zechmeister-Boltenstern S (2011). Nitrogen turnover processes and effects in terrestrial ecosystems. In: Sutton MA, Howard CM, Erisman JW et al (eds) The European Nitrogen Assessment. Cambridge University Press, pp 99–125Google Scholar
  5. Christenson LM, Mitchell MJ, Groffman PM, Lovett GM (2010) Winter climate change implications for decomposition in northeastern forests: comparisons of sugar maple litter with herbivore fecal inputs. Global Change Biol 16:2589–2601Google Scholar
  6. Cotrufo MF, Miller M, Zeller B (2000) Litter decomposition. In: Schulze ED (ed) Carbon and nitrogen cycling in European Forest Ecosystems. SpringerGoogle Scholar
  7. Dannenmann M, Gasche R, Ledebuhr A, Papen H (2006) Effects of forest management on soil N cycling in beech forests stocking on calcareous soils. Plant Soil 287:279–300CrossRefGoogle Scholar
  8. Dannenmann M, Gasche R, Papen H (2007) Nitrogen turnover and N2O production in the forest floor of beech stands as influenced by forest management. J Plant Nutr Soil Sc 170:134–144CrossRefGoogle Scholar
  9. Dannenmann M, Butterbach-Bahl K, Gasche R, Willibald G, Papen H (2008) Dinitrogen emissions and the N2:N2O emission ratio as influenced by pH and forest thinning. Soil Biol Biochem 40:2317–2323CrossRefGoogle Scholar
  10. Dannenmann M, Simon J, Gasche R, Holst J, Naumann PS, Kögel-Knabner I, Knicker H, Mayer H, Schloter M, Pena R, Polle A, Rennenberg H, Papen H (2009) Tree girdling provides insight on the role of labile carbon in nitrogen partitioning between soil microorganisms and adult European beech. Soil Biol Biochem 41:1622–1631CrossRefGoogle Scholar
  11. D’Annunzio R, Zeller B, Nicolas M, Dhôte J-F, Saint-André L (2008) Decomposition of European beech (Fagus sylvatica) litter: combining quality theory and 15N labelling experiments. Soil Biol Biochem 40:322–333CrossRefGoogle Scholar
  12. Fotelli MN, Rienks M, Rennenberg H, Gessler A (2004) Climate and forest management affect 15N-uptake, N balance and biomass of European beech seedlings. Trees 18:157–166CrossRefGoogle Scholar
  13. Gabet EJ, Reichmann OJ, Seabloom EW (2003) The effects of bioturbation on soil processes and sediment transport. Annu Rev Earth Plant Sci 31:249–273CrossRefGoogle Scholar
  14. Geßler A, Jung K, Gasche R, Papen H, Heidenfelder A, Börner E, Metzler B, Augustin S, Hildebrand E, Rennenberg H (2005) Climate and forest management influence nitrogen balance of European beech forests: microbial N transformations and inorganic N net uptake capacity of ectomycorrhizal roots. Eur J For Res 124:95–111CrossRefGoogle Scholar
  15. Guo C, Dannenmann M, Gasche R, Zeller B, Papen H, Polle A, Rennenberg H, Simon J (2012) Drought affects the partitioning of 15N recoverd from root and/or leaf litter between beech seedlings (Fagus sylvatica) and soil microbial biomass. Plant Soil, in pressGoogle Scholar
  16. Hatton PJ, Kleber M, Zeller B, Moni C, Plante AF, Townsend K, Gelhaye L, Lajtha K, Derrien D (2012) Transfer of litter-derived N to soil mineral-organic associations: Evidence from decadal N-15 experiments. Org Geochem 42:1489–1501CrossRefGoogle Scholar
  17. Hendricks JJ, Mitchell RJ, Kuehn KA, Pecot SD, Sims SE (2006) Measuring external mycelia production of ectomycorrhizal fungi in the field: the soil matrix matters. New Phyt 171:179–186CrossRefGoogle Scholar
  18. Kaiser C, Fuchslueger L, Koranda M, Gorfer M, Stange CF, Kitzler B, Rasche F, Strauss J, Sessitsch A, Zechmeister-Boltenstern S, Richter A (2011) Plants control the seasonal dynamics of microbial N cycling in a beech forest soil by belowground C allocation. Ecology 92:1036–1051PubMedCrossRefGoogle Scholar
  19. Lamontagne S, Schiff SL, Elgood RJ (2000) Recovery of 15N-labelled nitrate applied to a small upland boreal forest catchment. Can J For Res 30:1165–1177Google Scholar
  20. Pena R (2011) Functional diversity of beech (Fagus sylvatica) ectomycorrhizas with respect to nitrogen nutrition in response to plant carbon supply. Ph.D Thesis. University of Göttingen. Cuvillier Verlag, 196 pGoogle Scholar
  21. Pena R, Offermann C, Simon J, Naumann PS, Geßler A, Holst J, Dannenmann M, Mayer H, Kögel-Knabner I, Rennenberg H, Polle A (2010) Girdling affects ectomycorrhizal fungal diversity and reveals functional differences of EMF community composition in a beech forest. Appl Env Microbiol 76:1831–1841CrossRefGoogle Scholar
  22. Perakis SS, Hedin LO (2001) Fluxes and Fates of Nitrogen in soil of an unpolluted old-growth temperate forest, Southern Chile. Ecology 82:2245–2260CrossRefGoogle Scholar
  23. Providoli I, Bugmann H, Siegwolf R, Buchmann N, Schleppi P (2006) Pathways and dynamics of 15NO3− and 15NH4+ applied in a mountain Picea abies forest and in a nearby meadow in central Switzerland. Soil Biol Biochem 38:1645–1657Google Scholar
  24. Rennenberg H, Dannenmann M, Gessler A, Kreuzwieser J, Simon J, Papen H (2009) Nitrogen balance in forest soils: nutritional limitation of plants under climate change stresses. Plant Biol 11:4–23PubMedCrossRefGoogle Scholar
  25. Rosenkranz P, Dannenmann M, Brüggemann N, Papen H, Berger U, Zumbusch E, Butterbach-Bahl K (2010) Gross rates of ammonification and nitrification at a nitrogen-saturated spruce (Picea abies (L.) Karst.) stand in Southern Germany. Eur J Soil Sc 61:745–758CrossRefGoogle Scholar
  26. Scheu S, Falca M (2000) The soil food web of two beech forests (Fagus sylvatica) of contrasting humus type: stable isotope analysis of a macro- and a mesofauna-dominated community. Oecologia 123:285–296CrossRefGoogle Scholar
  27. Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602CrossRefGoogle Scholar
  28. Simon J, Waldhecker P, Brüggemann N, Rennenberg H (2010) Competition for nitrogen resources between beech and sycamore maple seedlings. Plant Biol 12:453–458PubMedCrossRefGoogle Scholar
  29. Simon J, Dannenmann M, Gasche R, Holst J, Mayer H, Papen H, Rennenberg H (2011) Competition for nitrogen between adult European beech and its offspring is reduced by avoidance strategy. Forest Ecol Manage 262:105–114CrossRefGoogle Scholar
  30. Sollins P, Swanston C, Kleber M, Filley T, Kramer M, Crow S, Caldwell BA, Lajtha K, Bowden R (2006) Organic C and N stabilization in a forest soil: evidence from sequential density fractionation. Soil Biol Biochem 38:3313–3324CrossRefGoogle Scholar
  31. Sollins P, Kramer MG, Swanston C, Lajtha K, Filley T, Aufdenkampe AK, Wagai R, Bowden RD (2009) Sequential density fractionation across soils of contrasting mineralogy: evidence for both microbial- and mineral-controlled soil organic matter stabilization. Biogeochemistry 96:209–231CrossRefGoogle Scholar
  32. Stoelken G, Pritsch K, Simon J, Mueller CW, Grams TEE, Esperschuetz S, Gayler S, Buegger F, Brueggemann N, Meier R, Zeller B, Winkler JB, Rennenberg H (2010) Enhanced ozone exposure of European beech (Fagus sylvatica) stimulates nitrogen mobilization from leaf litter and nitrogen accumulation in the soil. Plant Biosyst 144:537–546Google Scholar
  33. Von Lützow M, Kögel-Knabner I, Ekschmitt K, Matzner E, Guggenberger G, Marschner B, Flessa H (2007) Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions – a review. Eur J Soil Sc 57:426–445CrossRefGoogle Scholar
  34. Wallander H, Nilsson LO, Hagerberg D, Baath E (2001) Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. New Phyt 151:753–760CrossRefGoogle Scholar
  35. Wallander H, Göransson H, Rosengren U (2004) Production, standing biomass and natural abundance of 15N and 13C in ectomycorrhizal mycelia collected at different soil depths in two forest types. Oecologia 139:89–97PubMedCrossRefGoogle Scholar
  36. Wilkinson MT, Richards PJ, Humphreys GS (2009) Breaking ground: Pedological, geological and ecological implications of soil bioturbation. Earth Sci Rev 97:257–272CrossRefGoogle Scholar
  37. Wu H, Dannenmann M, Fanselow N, Wolf B, Yao ZS, Wu X, Brüggemann N, Zheng X, Han X, Dittert K, Butterbach-Bahl K (2011) Feedback of grazing on gross rates of N mineralization and inorganic N partitioning in steppe soils of Inner Mongolia. Plant Soil 340:127–139CrossRefGoogle Scholar
  38. Zeller B, Colin-Belgrand M, Dambrine É, Martin F (1998) 15N partitioning and production of 15N labeled litter in beech trees following (15N) urea spray. Ann For Sc 55:375–383CrossRefGoogle Scholar
  39. Zeller B, Colin-Belgrand M, Dambrine É, Martin F, Bottner P (2000) Decomposition of 15N-labelled leaf litter and fate of nitrogen derived from litter in a beech forest. Oecologia 123:550–559CrossRefGoogle Scholar
  40. Zeller B, Colin-Belgrand M, Dambrine É, Martin F (2001) Fate of nitrogen released from 15N-labelled litter in European beech forests. Tree Phys 21:153–162CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Chanjuan Guo
    • 1
  • Judy Simon
    • 1
  • Rainer Gasche
    • 2
  • Pascale Sarah Naumann
    • 3
  • Carolin Bimüller
    • 3
  • Rodica Pena
    • 4
  • Andrea Polle
    • 4
  • Ingrid Kögel-Knabner
    • 3
    • 5
  • Bernd Zeller
    • 6
  • Heinz Rennenberg
    • 1
    • 7
  • Michael Dannenmann
    • 2
    • 1
    Email author
  1. 1.Institute of Forest Botany and Tree Physiology, Chair of Tree PhysiologyUniversity of FreiburgFreiburgGermany
  2. 2.Institute for Meteorology and Climate Research, Atmospheric Environmental Research (IMK-IFU), Karlsruhe Institute of Technology (KIT)Garmisch-PartenkirchenGermany
  3. 3.Lehrstuhl für Bodenkunde, Department für Ökologie und Ökosystemmanagement, Wissenschaftszentrum Weihenstephan. Technische Universität MünchenFreising-WeihenstephanGermany
  4. 4.Abteilung Forstbotanik und Baumphysiologie, Büsgen-Institut, Büsgenweg 2, Georg-August Universität GöttingenGöttingenGermany
  5. 5.IAS-Institute for Advanced Study, Technische Universität MünchenGarchingGermany
  6. 6.INRA Centre de Nancy, UR 1138, Biogéochimie des Ecosystèmes Forestiers16 ChampenouxFrance
  7. 7.King Saud UniversityRiyadhSaudi Arabia

Personalised recommendations