, Volume 177, Issue 3, pp 811–821 | Cite as

Increase in soil stable carbon isotope ratio relates to loss of organic carbon: results from five long-term bare fallow experiments

  • Lorenzo MenichettiEmail author
  • Sabine Houot
  • Folkert van Oort
  • Thomas Kätterer
  • Bent T. Christensen
  • Claire Chenu
  • Pierre Barré
  • Nadezda A. Vasilyeva
  • Alf Ekblad
Ecosystem ecology - Original research


Changes in the 12C/13C ratio (expressed as δ13C) of soil organic C (SOC) has been observed over long time scales and with depth in soil profiles. The changes are ascribed to the different reaction kinetics of 12C and 13C isotopes and the different isotopic composition of various SOC pool components. However, experimental verification of the subtle isotopic shifts associated with SOC turnover under field conditions is scarce. We determined δ13C and SOC in soil sampled during 1929–2009 in the Ap-horizon of five European long-term bare fallow experiments kept without C inputs for 27–80 years and covering a latitudinal range of 11°. The bare fallow soils lost 33–65 % of their initial SOC content and showed a mean annual δ13C increase of 0.008–0.024 ‰. The 13C enrichment could be related empirically to SOC losses by a Rayleigh distillation equation. A more complex mechanistic relationship was also examined. The overall estimate of the fractionation coefficient (ε) was −1.2 ± 0.3  ‰. This coefficient represents an important input to studies of long-term SOC dynamics in agricultural soils that are based on variations in 13C natural abundance. The variance of ε may be ascribed to site characteristics not disclosed in our study, but the very similar kinetics measured across our five experimental sites suggest that overall site-specific factors (including climate) had a marginal influence and that it may be possible to isolate a general mechanism causing the enrichment, although pre-fallow land use may have some impact on isotope abundance and fractionation.


Stable carbon isotope ratio Isotope fractionation Rayleigh distillation Natural abundance Soil organic carbon 



We want to thank D. Biliou for analyses of soils from the Versailles, Grignon and Kursk experiments. The Danish contribution was financially supported by the EU SmartSoil project. Analyses of the Versailles, Grignon and Kursk soils were supported by an INSU-CNRS project and by the GIS Climat Environnement Société Carbosoil project, under which the European long-term bare fallow network was created. N. Vasilyeva was supported by the Region Ile de France (R2DS). We are grateful to former colleagues for starting these experiments and keeping them running.


  1. Bahn M, Schmitt M, Siegwolf R, Richter A, Brüggemann N (2009) Does photosynthesis affect grassland soil-respired CO2 and its carbon isotope composition on a diurnal timescale? New Phytol 182:451–460CrossRefPubMedCentralPubMedGoogle Scholar
  2. Balesdent J, Mariotti A (1996) Measurement of soil organic matter turnover using 13C natural abundance. In: Yamasaki S, Boutton T (eds) Mass spectrometry of soil. Dekker, New York, pp 47–82Google Scholar
  3. Barré P, Eglin T, Christensen BT, Ciais P, Houot S, Kätterer T, van Oort F, Peylin P, Poulton PR, Romanenkov V, Chenu C (2010) Quantifying and isolating stable soil organic carbon using long-term bare fallow experiments. Biogeosciences 7:3839–3850CrossRefGoogle Scholar
  4. Bergkvist P, Jarvis N, Berggren D, Carlgren K (2003) Long-term effects of sewage sludge applications on soil properties, cadmium availability and distribution in arable soil. Agric Ecosyst Environ 97:167–179CrossRefGoogle Scholar
  5. Blagodatskaya E, Yuyukina T, Blagodatsky S, Kuzyakov Y (2011) Turnover of soil organic matter and of microbial biomass under C3-C4 vegetation change: consideration of 13C fractionation and preferential substrate utilization. Soil Biol Biochem 43:159–166CrossRefGoogle Scholar
  6. Blair N, Leu A, Munoz E, Olsen J, Kwong E, Des Marais D (1985) Carbon isotopic fractionation in heterotrophic microbial metabolism. Appl Environ Microb 50:996–1001Google Scholar
  7. Boström B (2008) Achieving carbon isotope mass balance in northern forest soils, soil respiration and fungi. Örebro University, Örebro, SwedenGoogle Scholar
  8. Boström B, Comstedt D, Ekblad A (2007) Isotope fractionation and 13C enrichment in soil profiles during the decomposition of soil organic matter. Oecologia 153:89–98CrossRefPubMedGoogle Scholar
  9. Bowling DR, Sargent SD, Tanner BD, Ehleringer JR (2003) Tunable diode laser absorption spectroscopy for stable isotope studies of ecosystem-atmosphere CO2 exchange. Agric For Meteorol 118:1–19CrossRefGoogle Scholar
  10. Bowling DR, Pataki DE, Randerson JT (2008) Carbon isotopes in terrestrial ecosystem pools and CO2 fluxes. New Phytol 178:24–40CrossRefPubMedGoogle Scholar
  11. Cheng W (1996) Measurement of rhizosphere respiration and organic matter decomposition using natural 13C. Plant Soil 183:263–268CrossRefGoogle Scholar
  12. Christensen BT, Johnston AE (1997) Soil organic matter and soil quality—lessons learned from long-term experiments at Askov and Rothamsted. Dev Soil Sci 25:399–430CrossRefGoogle Scholar
  13. Christensen BT, Olesen JE, Hansen EM, Thomsen IK (2011) Annual variation in δ13C values of maize and wheat: effect on estimates of decadal scale soil carbon turnover. Soil Biol Biochem 43:1961–1967CrossRefGoogle Scholar
  14. Clay DE, Clapp CE, Reese C, Liu Z, Carlson C, Woodard H, Bly A (2007) Carbon-13 fractionation of relic soil organic carbon during mineralization affects calculated half-lives. Soil Sci Soc Am J 71:1003–1009CrossRefGoogle Scholar
  15. Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay RD, Wardle DA, Lindahl BD (2013) Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339:1615–1618CrossRefPubMedGoogle Scholar
  16. Colbach N, Roger-Estrade J, Chauvel B, Caneill J (2000) Modeling vertical and lateral seed bank movements during mouldboard ploughing. Eur J Agron 13:111–124CrossRefGoogle Scholar
  17. Ehleringer JR, Buchmann N, Flanagan LB (2000) Carbon isotope ratios in belowground carbon cycle processes. Ecol Appl 10:412–422CrossRefGoogle Scholar
  18. Ekblad A, Högberg P (2000) Analysis of δ13C of CO2 distinguishes between microbial respiration of added C4-sucrose and other soil respiration in a C3-ecosystem. Plant Soil 219:197–209CrossRefGoogle Scholar
  19. Ekblad A, Nyberg G, Högberg P (2002) 13C-discrimination during microbial respiration of added C3-, C4- and 13C-labelled sugars to a C3-forest soil. Oecologia 131:245–249CrossRefGoogle Scholar
  20. Epron D, Ngao J, Dannoura M, Bakker MR, Zeller B, Bazot S, Bosc A, Plain C, Lata JC, Priault P, Barthes L, Loustau D (2011) Seasonal variations of belowground carbon transfer assessed by in situ 13CO2 pulse labelling of trees. Biogeosciences 8:885–919CrossRefGoogle Scholar
  21. Francey RJ, Allison CE, Etheridge DM, Trudinger CM, Enting IG, Leuenberg M, Lagenfelds RL, Michel E, Steele LP (1999) A 1000-year high precision record of δ13C in atmospheric CO2. Tellus B 51:170–193CrossRefGoogle Scholar
  22. Gerzabek M, Pichlmayer F, Kirchmann H, Habernauer G (1997) The response of soil organic matter to manure amendments in a long-term experiment at Ultuna, Sweden. Eur J Soil Sci 48:273–282CrossRefGoogle Scholar
  23. Gerzabek M, Habernauer G, Kirchmann H (2001) Soil organic matter pools and carbon 13C natural abundances in particle size fractions of a long term agricultural field experiment receiving organic amendments. Soil Sci Soc Am J 65:352–358CrossRefGoogle Scholar
  24. Ghosh P, Brand WA (2003) Stable isotope ratio mass spectrometry in global climate change research. Int J Mass Spectrom 228:1–33CrossRefGoogle Scholar
  25. Gleixner G, Danier HJ, Werner RA, Schmidt HL (1993) Correlations between the 13C content of primary and secondary plant products in different cell compartments and that in decomposing basidiomycetes. Plant Physiol 102:1287–1290PubMedCentralPubMedGoogle Scholar
  26. Gleixner G, Scrimgeour C, Schmidt H, Viola R (1998) Stable isotope distribution in the major metabolites of source and sink organs of Solanum tuberosum L.: a powerful tool in the study of metabolic partitioning in intact plants. Planta 207:241–245CrossRefGoogle Scholar
  27. IUSS Working Group (2007) World reference base for soil resources 2006, first update 2007. World soil resources reports no. 103. FAO, RomeGoogle Scholar
  28. Guenet B, Juares S, Bardoux G, Pouteau V, Cheviron N, Marrauld C, Abbadie L, Chenu C (2011) Metabolic capacities of microorganisms from a long-term bare fallow. Appl Soil Ecol 51:87–93CrossRefGoogle Scholar
  29. Hobbie E, Colpaert J (2004) Nitrogen availability and mycorrhizal colonization influence water use efficiency and carbon isotope patterns in Pinus sylvestris. New Phytol 164:515–525CrossRefGoogle Scholar
  30. Houot S, Molina JAE, Chaussod R, Clapp CE (1989) Simulation by NC-Soil of net mineralization in soils from the Deherain and 36 parcelles fields at Grignon. Soil Sci Soc Am J 53:451–455CrossRefGoogle Scholar
  31. Jagadamma S, Lal R (2010) Integrating physical and chemical methods for isolating stable soil organic carbon. Geoderma 158:322–330CrossRefGoogle Scholar
  32. Kätterer T, Bolinder M, Andrén O, Kirchmann H, Menichetti L (2011) Roots contribute more to refractory soil organic matter than aboveground crop residues, as revealed by a long-term field experiment. Agric Ecosyst Environ 141:184–192CrossRefGoogle Scholar
  33. Keeling CD (1979) The Suess effect: 13C-14C interrelations. Environ Int 2:229–300CrossRefGoogle Scholar
  34. Kindler R, Siemens J, Kaiser K, Walmsley DC, Bernhofer C, Buchmann N, Cellier P, Eugster W, Gleixner G, Grünwald T, Heim A, Ibrom A, Jones SK, Jones M, Klumpp K, Kutsch W, Steenberg Larsen K, Lehuger S, Loubet B, Mckenzie R, Moors E, Osborne B, Pilegaard K, Rebmann C, Saunders M, Schmidt MWI, Schrumpp M, Seyfferth J, Skiba U, Soussana JF, Sutton MA, Tefs C, Vowinckel B, Zeeman MJ, Kaupenjohann M (2011) Dissolved carbon leaching from soil is a crucial component of the net ecosystem carbon balance. Glob Change Biol 17:1167–1185CrossRefGoogle Scholar
  35. Kirchmann H, Persson J, Carlgren K (1994) The Ultuna long-term soil organic matter experiment, 1956–1991. Depart Soil Science. Reports and dissertation. Swed Univ Agric Sci Upps 17:1–55Google Scholar
  36. Kortekaas M, Murray AS, Sandgren P, Björck S (2007) OSL chronology for a sediment core from the southern Baltic sea: a continuous sedimentation record since deglaciation. Quat Geochronol 2:95–101CrossRefGoogle Scholar
  37. Kristiansen SM, Brandt M, Hansen EM, Magid J, Christensen BT (2004) 13C signature of CO2 evolved from incubated maize residues and maize-derived sheep faeces. Soil Biol Biochem 36:99–105CrossRefGoogle Scholar
  38. Krull ES, Skjemstad JO (2003) δ13C and δ14N profiles in 14C-dated Oxisol and Vertisols as a function of soil chemistry and mineralogy. Geoderma 112:1–29CrossRefGoogle Scholar
  39. Lal R (2004) Soil carbon sequestration to mitigate climate change. Geoderma 123:1–22CrossRefGoogle Scholar
  40. Lerch T, Nunan N, Dignac MF, Chenu C, Mariotti A (2011) Variations in microbial isotopic fractionation during soil organic matter decomposition. Biogeochemistry 106:5–21CrossRefGoogle Scholar
  41. Lichtfouse É, Budzinski H, Garrigues P, Eglinton TI (1997) Ancient polycyclic aromatic hydrocarbons in modern soils: 13C, 14C and biomarker evidence. Org Geochem 26:353–359CrossRefGoogle Scholar
  42. Mariotti A, Germon J, Hubert P, Kaiser P, Letolle R, Tardieux A, Tardieux P (1981) Experimental determination of nitrogen kinetic isotope fractionation: some principles; illustration for the denitrification and nitrification processes. Plant Soil 61:413–430CrossRefGoogle Scholar
  43. Menichetti L, Ekblad A, Kätterer T (2013) Organic amendments affect δ13C signature of soil respiration and soil organic C accumulation in a long-term field experiment in Sweden. Eur J Soil Sci 64:621–628CrossRefGoogle Scholar
  44. Mikhailova EA, Post CJ (2006) Organic carbon stocks in the Russian Chernozem. Eur J Soil Sci 57:330–336CrossRefGoogle Scholar
  45. Miltner A, Emeis K, Struck U, Leipe T, Voss M (2005) Terrigenous organic matter in Holocene sediments from the central Baltic sea, NW Europe. Chem Geol 216:313–328CrossRefGoogle Scholar
  46. Morel R, Lasnier T, Burgeois P (1984) Les essais de fertilisation de longue duree de la station agronomique de Grignon; dispositif deherain et des 36 parcelles: resultats experimentaux (periode 1938–1982). Institut National de la Recherche Agronomique, ParisGoogle Scholar
  47. Peel MC, Finlayson BL, Mcmahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Sys Sci 11:1633–1644CrossRefGoogle Scholar
  48. Plummer M (2003) A program for analysis of Bayesian graphical models using Gibbs sampling. In: Hornik K, Leisch F, Zeileis A (eds) JAGS: just another Gibbs sampler. Proceedings of the 3rd International Workshop on Distributed Statistical Computing, Vienna.
  49. Powlson DS, Goulding KWT, Willison TW, Webster CP (1997) The effect of agriculture on methane oxidation in soil. Nutr Cycl Agroecosys 49:59–70CrossRefGoogle Scholar
  50. R Development Core Team (2012) A language and environment for statistical computing, reference index version 3.0.2. R Foundation for Statistical Computing, Vienna.
  51. Rayleigh J (1896) Theoretical considerations respecting the separation of gases by diffusion and similar processes. Philos Mag 42:493–593CrossRefGoogle Scholar
  52. Rubino M, Etheridge DM, Trudinger CM, Allison CE, Battle MO, Langenfelds RL, Steele LP, Curran M, Bender M, White JWC, Jenk TM, Blunier T, Francey RJ (2013) A revised 1000 year atmospheric δ13C-CO2 record from Law Dome and South Pole, Antarctica. J Geophys Res-Atmos 118:8482–8499CrossRefGoogle Scholar
  53. Šantručková H, Bird MI, Lloyd J (2000) Microbial processes and carbon-isotope fractionation in tropical and temperate grassland soils. Funct Ecol 14:108–114CrossRefGoogle Scholar
  54. Schmidt MWI, Gleixner G (2005) Carbon and nitrogen isotope composition of bulk soils, particle-size fractions and organic material after treatment with hydrofluoric acid. Eur J Soil Sci 56:407–416CrossRefGoogle Scholar
  55. Skidmore M, Sharp M, Tranter M (2004) Kinetic isotopic fractionation during carbonate dissolution in laboratory experiments: implications for detection of microbial CO2 signatures using δ13C-DIC. Geochim Cosmochim Ac 68:4309–4317CrossRefGoogle Scholar
  56. Subke JA, Vallack HW, Magnusson T, Keel SG, Metcalfe DB, Högberg P, Ineson P (2009) Short-term dynamics of abiotic and biotic soil 13CO2 effluxes after in situ 13CO2 pulse labelling of a boreal pine forest. New Phytol 183:349–357CrossRefPubMedGoogle Scholar
  57. Tu K, Dawson T (2005) Partitioning ecosystem respiration using stable isotope analyses of CO2. In: Flanagan LB, Ehleringer JR, Pataki DE (eds) Stable isotopes and biosphere-atmosphere interactions: processes and biological controls. Elsevier, Amsterdam, pp 297–311Google Scholar
  58. Vasilyeva NA (2009) Aggregate structure of typical Chernozem soil under grassland and fallow. Moscow State University, MoscowGoogle Scholar
  59. Webster R (2007) Analysis of variance, inference, multiple comparisons and sampling effects in soil research. Eur J Soil Sci 58:74–82CrossRefGoogle Scholar
  60. Werth M, Kuzyakov Y (2009) Three-source partitioning of CO2 efflux from maize field soil by 13C natural abundance. J Plant Nutr Soil Sci 172:487–499CrossRefGoogle Scholar
  61. Werth M, Kuzyakov Y (2010) 13C fractionation at the root-microorganisms-soil interface: a review and outlook for partitioning studies. Soil Biol Biochem 42:1–13CrossRefGoogle Scholar
  62. Worrall F, Davies H, Bhogal A, Lilly A, Evans M, Turner K, Burt T, Barraclough D, Smith P, Merrington G (2012) The flux of DOC from the UK—predicting the role of soils, land use and net watershed losses. J Hydrol 448–449:149–160CrossRefGoogle Scholar
  63. Wynn JG, Bird MI, Wong VNL (2005) Rayleigh distillation and the depth profile of 13C/12C ratios of soil organic carbon from soils of disparate texture in Iron Range National Park, Far North Queensland, Australia. Geochim Cosmochim Acta 69:1961–1973CrossRefGoogle Scholar
  64. Yang W, Magid J, Christensen S, Rønn R, Ambus P, Ekelund F (2014) Biological 12C-13C fractionation increases with increasing community-complexity in soil microcosms. Soil Biol Biochem 69:197–201CrossRefGoogle Scholar
  65. Zhao FJ, Spiro B, McGrath S (2001) Trends in 13C/12C ratios and C isotope discrimination of wheat since 1845. Oecologia 128:336–342CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Lorenzo Menichetti
    • 1
    Email author
  • Sabine Houot
    • 2
  • Folkert van Oort
    • 3
  • Thomas Kätterer
    • 4
  • Bent T. Christensen
    • 5
  • Claire Chenu
    • 6
  • Pierre Barré
    • 7
  • Nadezda A. Vasilyeva
    • 6
    • 8
  • Alf Ekblad
    • 9
  1. 1.Department of Soil and EnvironmentSwedish University of Agricultural SciencesUppsalaSweden
  2. 2.INRA, UMR Environnement et Grandes CulturesThiverval-GrignonFrance
  3. 3.INRA, Unité PessacVersaillesFrance
  4. 4.Department of EcologySwedish University of Agricultural SciencesUppsalaSweden
  5. 5.Department of AgroecologyAarhus University, AU-FoulumTjeleDenmark
  6. 6.AgroParisTech, UMR 7618 BIOEMCO, Bâtiment EGERThiverval-GrignonFrance
  7. 7.Laboratoire de Geologie, UMR8538, Ecole Normale SupérieureParisFrance
  8. 8.North-Eastern Federal UniversityYakutskRussia
  9. 9.School of Science and TechnologyÖrebro UniversityÖrebroSweden

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