, Volume 112, Issue 1–3, pp 441–455 | Cite as

Short-term temperature impact on soil heterotrophic respiration in limed agricultural soil samples

  • Pauline BuysseEmail author
  • Stéphanie Goffin
  • Monique Carnol
  • Sandrine Malchair
  • Alain Debacq
  • Bernard Longdoz
  • Marc Aubinet


This study sought to investigate the hourly and daily timescale responses of soil CO2 fluxes to temperature in a limed agricultural soil. Observations from different incubation experiments were compared with the results of a model combining biotic (heterotrophic respiration) and abiotic (carbonate weathering) components. Several samples were pre-incubated for 8–9 days at three temperatures (5, 15 and 25 °C) and then submitted to short-term temperature (STT) cycles (where the temperature was increased from 5 to 35 °C in 10 °C stages, with each stage being 3 h long). During the temperature cycles (hourly timescale), the soil CO2 fluxes increased significantly with temperature under all pre-incubation temperature (PIT) treatments. A hysteresis effect and negative fluxes during cooling phases were also systematically observed. At a given hourly timescale temperature, there was a negative relationship of the CO2 fluxes with the PIT. Using the combined model allowed the experimental results to be clearly described, including the negative fluxes and the hysteresis effect, showing the potentially large contribution of abiotic fluxes to total fluxes in limed soils, after STT changes. The fairly good agreement between the measured and simulated flux results also suggested that the biotic flux temperature sensitivity was probably unaffected by timescale (hourly or daily) or PIT. The negative relationship of the CO2 fluxes with the PIT probably derived from very labile soil carbon depletion, as shown in the simulations. This was not, however, confirmed by soil carbon measurements, which leaves open the possibility of adaptation within the microbial community.


Soil CO2 flux Temperature Limed agricultural soil Incubation experiment Organic carbon model Short-term 



Pauline Buysse holds a Research Fellow Grant from the FRS-FNRS, Belgium. The authors thank Dr Gilles Colinet for the soil pH measurements, Marie-Christine Requier for her technical support during the soil C analyses, Eléonore Horge for helping with the soil CO2 flux measurements, and Martin Maier and Marilyn Roland for helping to improve our understanding of the abiotic processes. The authors also thank the two anonymous reviewers for providing the thoughtful comments that helped improve the manuscript.

Supplementary material

10533_2012_9739_MOESM1_ESM.pdf (19 kb)
Supplementary material 1 (PDF 20 kb)


  1. Allison SD, Wallenstein MD, Bradford MA (2010) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3:336–340CrossRefGoogle Scholar
  2. Bertrand I, Delfosse O, Mary B (2007) Carbon and nitrogen mineralization in acidic, limed and calcareous agricultural soils: apparent and actual effects. Soil Biol Biochem 39:276–288CrossRefGoogle Scholar
  3. Biasi C, Lind SE, Pekkarinen NM, Huttunen JT, Shurpali NJ, Hyvönen NP, Repo ME, Martikainen PJ (2008) Direct experimental evidence for the contribution of lime to CO2 release from managed peat soil. Soil Biol Biochem 40:2660–2669CrossRefGoogle Scholar
  4. Bradford MA, Davies CA, Frey SD, Maddox TR, Melillo JM, Mohan JE, Reynolds JF, Treseder KK, Wallenstein MD (2008) Thermal adaptation of soil microbial respiration to elevated temperature. Ecol Lett 11:1316–1327CrossRefGoogle Scholar
  5. Bradford MA, Watts BW, Davies CA (2010) Thermal adaptation of heterotrophic soil respiration in laboratory microcosms. Glob Change Biol 16:1576–1588CrossRefGoogle Scholar
  6. Ciais P, Wattenbach M, Vuichard N, Smith P, Piao SL, Don A, Luyssaerts S, Janssens IA, Bondeau A, Dechow R, Leip A, Smith PC, Beer C, Van Der Werf GR, Gervois S, Van Oost K, Tomelleri E, Freibauer A, Schulze ED, CarboEurope Synthesis Team (2010) The European carbon balance. Part 2: croplands. Glob Change Biol 16:1409–1428CrossRefGoogle Scholar
  7. Curiel-Yuste J, Baldocchi DD, Gershenson A, Goldstein A, Misson L, Wong S (2007) Microbial soil respiration and its dependency on carbon inputs, soil temperature and moisture. Glob Change Biol 13:2018–2035CrossRefGoogle Scholar
  8. Curiel-Yuste J, Ma S, Baldocchi DD (2010) Plant-soil interactions and acclimation to temperature of microbial-mediated soil respiration may affect predictions of soil CO2 efflux. Biogeochemistry 98:127–138CrossRefGoogle Scholar
  9. Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173CrossRefGoogle Scholar
  10. Davidson EA, Savage K, Verchot LV, Navarro R (2002) Minimizing artifacts and biases in chamber-based measurements of soil respiration. Agric For Meteorol 113:21–37CrossRefGoogle Scholar
  11. Davidson EA, Janssens IA, Luo Y (2006) On the variability of respiration in terrestrial ecosystems: moving beyond Q10. Glob Change Biol 12:154–164CrossRefGoogle Scholar
  12. Emmerich WE (2003) Carbon dioxide fluxes in a semiarid environment with high carbonate soils. Agric For Meteorol 116:91–102CrossRefGoogle Scholar
  13. FAOSTAT (2009) ResourceSTAT-Land Accessed 22 Jan 2010
  14. Franzluebbers AJ (1999) Potential C and N mineralization and microbial biomass from intact and increasingly disturbed soils of varying texture. Soil Biol Biochem 31:1083–1090CrossRefGoogle Scholar
  15. Gershenson A, Bader NE, Cheng W (2009) Effects of substrate availability on the temperature sensitivity of soil organic matter decomposition. Glob Change Biol 15:176–183CrossRefGoogle Scholar
  16. Ghani A, Dexter M, Perrott KW (2003) Hot-water extractable carbon in soils: a sensitive measurement for determining impacts of fertilisation, grazing and cultivation. Soil Biol Biochem 35:1231–1243CrossRefGoogle Scholar
  17. Gocke M, Pustovoytov K, Kuzyakov Y (2011) Carbonate recrystallization in root-free soil and rhizosphere of Triticum aestivum and Lolium perenne estimated by 14C labeling. Biogeochemistry. doi: 10.1007/s10533-010-9456-z Google Scholar
  18. Hamdi S, Chevallier T, Ben Aïssa N, Ben Hammouda M, Gallali A, Chotte J-L, Bernoux M (2011) Short-term temperature dependence of heterotrophic soil respiration after one-month pre-incubation at different temperatures. Soil Biol Biochem 43:1752–1758CrossRefGoogle Scholar
  19. Hamilton SK, Kurzman AL, Arango C, Jin L, Robertson GP (2007) Evidence for carbon sequestration by agricultural liming. Glob Biogeochem Cycles. doi: 10.1029/2006GB002738 Google Scholar
  20. Haney RL, Senseman SA, Hons FM (2002) Effect of Roundup Ultra on microbial activity and biomass from selected soils. J Environ Qual 31:730–735CrossRefGoogle Scholar
  21. Hartley IP, Heinemeyer A, Ineson P (2007) Effects of three years of soil warming and shading on the rate of soil respiration: substrate availability and not thermal acclimation mediates observed response. Glob Change Biol 13:1761–1770CrossRefGoogle Scholar
  22. Hartley IP, Hopkins DW, Garnett MH, Sommerkorn M, Wookey PA (2008) Soil microbial respiration in arctic soil does not acclimate to temperature. Ecol Lett 11:1092–1100CrossRefGoogle Scholar
  23. IUSS Working Group WRB (2006) World reference base for soil resources 2006, 2nd edn. World Soil Resources reports no. 103. FAO, RomeGoogle Scholar
  24. Jenkinson DS, Powlson DS (1976) The effects of biocidal treatments on metabolism in soil—V: a method for measuring soil biomass. Soil Biol Biochem 8:209–213CrossRefGoogle Scholar
  25. Joergensen RG (1996) The fumigation-extraction method to estimate soil microbial biomass: calibration of the kEC value. Soil Biol Biochem 28:25–31CrossRefGoogle Scholar
  26. Karhu K, Fritze H, Tuomi M, Vanhala P, Spetz P, Kitunen V, Liski J (2010) Temperature sensitivity of organic matter decomposition in two boreal forest soil profiles. Soil Biol Biochem 42:72–82CrossRefGoogle Scholar
  27. Kätterer T, Reichstein M, Andrèn O, Lomander A (1998) Temperature dependence of organic matter decomposition: a critical review using literature data analyzed with different models. Biol Fertil Soils 27:258–262CrossRefGoogle Scholar
  28. Kirschbaum MUF (2004) Soil respiration under prolonged soil warming: are rate reductions caused by acclimation or substrate loss? Glob Change Biol 10:1870–1877CrossRefGoogle Scholar
  29. Kirschbaum MUF (2006) The temperature dependence of soil organic matter decomposition—still a topic of debate. Soil Biol Biochem 38:2510–2518CrossRefGoogle Scholar
  30. Langmuir D (1997) Aqueous environmental geochemistry. Prentice Hall, New JerseyGoogle Scholar
  31. Larionova AA, Yevdokimov IV, Bykhovets SS (2007) Temperature response of soil respiration is dependent on concentration of readily decomposable C. Biogeosciences 4:1073–1081CrossRefGoogle Scholar
  32. Lloyd J, Taylor JA (1994) On the temperature dependence of soil respiration. Funct Ecol 8:315–323CrossRefGoogle Scholar
  33. Lömander A, Kätterer T, Andrén O (1998) Modelling the effects of temperature and moisture on CO2 evolution from top- and subsoil using a multi-compartment approach. Soil Biol Biochem 30:2023–2030CrossRefGoogle Scholar
  34. Longdoz B, Yernaux M, Aubinet M (2000) Soil CO2 efflux measurements in a mixed forest: impact of chamber disturbances, spatial variability and seasonal evolution. Glob Change Biol 6:907–917CrossRefGoogle Scholar
  35. Luo Y, Wan S, Hui D, Wallace LL (2001) Acclimatization of soil respiration to warming in a tall grass prairie. Nature 413:622–625CrossRefGoogle Scholar
  36. Maier M, Schack-Kirchner H, Hildebrand EE, Holst J (2010) Pore-space CO2 dynamics in a deep, well-aerated soil. Eur J Soil Sci 61:877–887CrossRefGoogle Scholar
  37. Malcolm GM, Lopez-Gutierrez JC, Koide RT (2009) Little evidence for respiratory acclimation by microbial communities to short-term shifts in temperature in red pine (Pinus resinosa) litter. Glob Change Biol 15:2485–2492CrossRefGoogle Scholar
  38. Moureaux C, Debacq A, Bodson B, Heinesch B, Aubinet M (2006) Annual net ecosystem carbon exchange by a sugar beet crop. Agric For Meteorol 139:25–39CrossRefGoogle Scholar
  39. Perrin D (2005) Flux de respiration de sols forestiers: analyse et modélisation à différentes échelles spatiales et temporelles. PhD Thesis. Université de Liège, Gembloux Agro-Bio TechGoogle Scholar
  40. Raich JW, Potter CS, Bhagawati D (2002) Interannual variability in global soil respiration, 1980–94. Glob Change Biol 8:800–812CrossRefGoogle Scholar
  41. Reichstein M, Beer C (2008) Soil respiration across scales: the importance of a model-data integration framework for data interpretation. J Plant Nutr Soil Sc 171:344–354CrossRefGoogle Scholar
  42. Smith P, Martino D, Cai Z, Gwary D, Janzen H, Kumar P, McCarl B, Ogle S, O’Mara F, Rice C, Scholes B, Sirotenko O (2007) Agriculture. In: Metz B, Davidson OR, Bosch PR, Dave R, Meyer LA (eds) Climate change 2007: mitigation. Contribution of Working Group III to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 497–540Google Scholar
  43. Stumm W, Morgan JJ (1996) Aquatic chemistry: chemical equilibria and rates in natural waters, 3rd edn. Wiley, New YorkGoogle Scholar
  44. Suleau M, Moureaux C, Dufranne D, Buysse P, Bodson B, Destain J-P, Heinesch B, Debacq A, Aubinet M (2011) Respiration of three Belgian crops: partitioning of total ecosystem respiration in its heterotrophic, above- and below-ground autotrophic components. Agric For Meteorol 151:633–643CrossRefGoogle Scholar
  45. Tamir G, Shenker M, Heller H, Bloom PR, Fine P, Bar-Tal A (2011) Can soil carbonate dissolution lead to overestimation of soil respiration? Soil Sci Soc Am J 75:1414–1422CrossRefGoogle Scholar
  46. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707CrossRefGoogle Scholar
  47. Wetterstedt JÅM, Persson T, Ågren GI (2010) Temperature sensitivity and substrate quality in soil organic matter decomposition: results of an incubation study with three substrates. Glob Change Biol 16:1806–1819CrossRefGoogle Scholar
  48. Willey JM, Sherwood LM, Woolverton CJ (2007) Prescott, Harley and Klein’s microbiology, 7th edn. McGraw-Hill, New YorkGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Pauline Buysse
    • 1
    Email author
  • Stéphanie Goffin
    • 1
  • Monique Carnol
    • 2
  • Sandrine Malchair
    • 2
  • Alain Debacq
    • 1
  • Bernard Longdoz
    • 3
  • Marc Aubinet
    • 1
  1. 1.Gembloux Agro-Bio Tech, Unit of Biosystem PhysicsUniversity of LiègeGemblouxBelgium
  2. 2.Laboratory of Plant and Microbial Ecology, Institute of Botany B22University of LiègeLiègeBelgium
  3. 3.INRA, Centre INRA de Nancy, UMR1137 Ecologie et Ecophysiologie ForestièresChampenouxFrance

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