Separating the effects of temperature and carbon allocation on the diel pattern of soil respiration in the different phenological stages in dry grasslands

Autoři: János Balogh aff001;  Szilvia Fóti aff001;  Marianna Papp aff001;  Krisztina Pintér aff001;  Zoltán Nagy aff001
Působiště autorů: Institute of Botany and Ecophysiology, Szent István University, Gödöllő, Hungary aff001;  MTA-SZIE Agroecology Research Group, Szent István University, Gödöllő, Hungary aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article


Diel variability of soil respiration is influenced by several factors including temperature and carbon allocation as the most significant ones, co-varying on multiple time scales. In an attempt to disentangle their effects we analyzed the dynamics of soil respiration components using data from a three-year soil respiration study. We measured CO2 efflux in intact, root-excluded and root- and mycorrhizal fungi excluded plots and analyzed the diel variability in different phenological stages. We used sine wave models to describe the diel pattern of soil respiration and to disentangle the effects of temperature from belowground carbon allocation based on the differences between component dynamics inferred from the fitted models. Rhizospheric respiration peaked 8–12 hours after GPP peak, while mycorrhizal fungi respiration had a longer time lag of 13–20 hours. Results of δ13CO2 isotopic signals from the respiration components showed similar patterns. It was found that drought affected the component respiration rates differently. Also, the speed and the amount of carbon allocation to the roots as well as to the mycorrhizal fungi was reduced under drought. We conclude that the diel variability of soil respiration is the result of the integrated patterns of temperature- and carbon allocation-driven components in dry grasslands and their share depends on their phenological stages and stress state.

Klíčová slova:

Carbon dioxide – Ecosystems – Fungi – Grasslands – Rhizosphere – Sine waves – Soil respiration – Carbon sink


1. Baldocchi D, Chu H, Reichstein M. Inter-annual variability of net and gross ecosystem carbon fluxes: A review. Agric For Meteorol. Elsevier; 2018;249: 520–533. doi: 10.1016/J.AGRFORMET.2017.05.015

2. Phillips CL, Bond-Lamberty B, Desai AR, Lavoie M, Risk D, Tang J, et al. The value of soil respiration measurements for interpreting and modeling terrestrial carbon cycling. Plant Soil.; 2017;413: 1–25. doi: 10.1007/s11104-016-3084-x

3. Vargas R, Baldocchi DD, Bahn M, Hanson PJ, Hosman KP, Kulmala L, et al. On the multi-temporal correlation between photosynthesis and soil CO2 efflux: reconciling lags and observations. New Phytol. 2011;191: 1006–17. doi: 10.1111/j.1469-8137.2011.03771.x 21609333

4. Moyano FE, Manzoni S, Chenu C. Responses of soil heterotrophic respiration to moisture availability: An exploration of processes and models. Soil Biol Biochem. Elsevier Ltd; 2013; 1–14. doi: 10.1016/j.soilbio.2013.01.002

5. Balogh J, Pintér K, Fóti S, Cserhalmi D, Papp M, Nagy Z. Dependence of soil respiration on soil moisture, clay content, soil organic matter, and CO2 uptake in dry grasslands. Soil Biol Biochem. Elsevier Ltd; 2011;43: 1006–1013. doi: 10.1016/j.soilbio.2011.01.017

6. Hopkins F, Gonzalez-Meler M a, Flower CE, Lynch DJ, Czimczik C, Tang J, et al. Ecosystem-level controls on root-rhizosphere respiration. New Phytol. 2013;199: 339–51. doi: 10.1111/nph.12271 23943914

7. Barba J, Cueva A, Bahn M, Barron-Gafford GA, Bond-Lamberty B, Hanson PJ, et al. Comparing ecosystem and soil respiration: Review and key challenges of tower-based and soil measurements. Agric For Meteorol. 2018;249: 434–443. doi: 10.1016/j.agrformet.2017.10.028

8. Ahlström A, Raupach MR, Schurgers G, Smith B, Arneth A, Jung M, et al. The dominant role of semi-arid ecosystems in the trend and variability of the land CO2 sink. Science (80-). 2015;348: 895–899. doi: 10.1126/science.aaa1668 25999504

9. Nagy Z, Pintér K, Czóbel S, Balogh J, Horváth L, Fóti S, et al. The carbon budget of semi-arid grassland in a wet and a dry year in Hungary. Agric Ecosyst Environ. Elsevier; 2007;121: 21–29. doi: 10.1016/j.agee.2006.12.003

10. Van der Molen MK, Dolman AJ, Ciais P, Eglin T, Gobron N, Law BE, et al. Drought and ecosystem carbon cycling. Agric For Meteorol. Elsevier B.V.; 2011;151: 765–773. doi: 10.1016/j.agrformet.2011.01.018

11. Moyes AB, Bowling DR. Plant community composition and phenological stage drive soil carbon cycling along a tree-meadow ecotone. Plant Soil. 2016;401: 231–242. doi: 10.1007/s11104-015-2750-8

12. Burri S, Niklaus PA, Grassow K, Buchmann N, Kahmen A. Effects of plant productivity and species richness on the drought response of soil respiration in temperate grasslands. PLoS One. 2018;13: e0209031. doi: 10.1371/journal.pone.0209031 30576332

13. Savage K, Davidson E a., Tang J. Diel patterns of autotrophic and heterotrophic respiration among phenological stages. Glob Chang Biol. 2013;19: 1151–1159. doi: 10.1111/gcb.12108 23504892

14. Kuzyakov Y, Gavrichkova O. Review: Time lag between photosynthesis and carbon dioxide efflux from soil: a review of mechanisms and controls. Glob Chang Biol. 2010;16: 3386–3406. doi: 10.1111/j.1365-2486.2010.02179.x

15. Abramoff RZ, Finzi AC. Are above- and below-ground phenology in sync? New Phytol. 2015;205: 1054–1061. doi: 10.1111/nph.13111 25729805

16. Högberg MN, Briones MJI, Keel SG, Metcalfe DB, Campbell C, Midwood AJ, et al. Quantification of effects of season and nitrogen supply on tree below-ground carbon transfer to ectomycorrhizal fungi and other soil organisms in a boreal pine forest. New Phytol. 2010;187: 485–493. doi: 10.1111/j.1469-8137.2010.03274.x 20456043

17. Hasibeder R, Fuchslueger L, Richter A, Bahn M. Summer drought alters carbon allocation to roots and root respiration in mountain grassland. New Phytol. 2014; doi: 10.1111/nph.13146 25385284

18. Vargas R, Detto M, Baldocchi DD, Allen MF. Multiscale analysis of temporal variability of soil CO2 production as influenced by weather and vegetation. Glob Chang Biol. Wiley Online Library; 2010;16: 1589–1605. doi: 10.1111/j.1365-2486.2009.02111.x

19. Gomez-Casanovas N, Matamala R, Cook DR, Gonzalez-Meler M a. Net ecosystem exchange modifies the relationship between the autotrophic and heterotrophic components of soil respiration with abiotic factors in prairie grasslands. Glob Chang Biol. 2012;18: 2532–2545. doi: 10.1111/j.1365-2486.2012.02721.x

20. Lloyd J, Taylor J. On the temperature dependence of soil respiration. Funct Ecol. JSTOR; 1994;8: 315–323. Available:

21. Reichstein M, Subke JA, Angeli AC, Tenhunen JD. Does the temperature sensitivity of decomposition of soil organic matter depend upon water content, soil horizon, or incubation time? Glob Chang Biol. 2005;11: 1754–1767. doi: 10.1111/j.1365-2486.2005.001010.x

22. Subke J-A, Bahn M. On the ‘temperature sensitivity’ of soil respiration: Can we use the immeasurable to predict the unknown? Soil Biol Biochem. Pergamon Press; 2010;42: 1653–1656. doi: 10.1016/j.soilbio.2010.05.026 21633517

23. Pavelka M, Acosta M, Marek M V., Kutsch W, Janous D. Dependence of the Q10 values on the depth of the soil temperature measuring point. Plant Soil. 2007;292: 171–179. doi: 10.1007/s11104-007-9213-9

24. Darenova E, Pavelka M, Acosta M. Diurnal deviations in the relationship between CO2 efflux and temperature: A case study. Catena. Elsevier B.V.; 2014;123: 263–269. doi: 10.1016/j.catena.2014.08.008

25. Pingintha N, Leclerc MY, Beasley JP Jr., Zhang G, Senthong C. Assessment of the soil CO2 gradient method for soil CO2 efflux measurements: comparison of six models in the calculation of the relative gas diffusion coefficient. Tellus B. 2010;62: 47–58. doi: 10.1111/j.1600-0889.2009.00445.x

26. Zhang Q, Katul G, Oren R, Daly E, Manzoni S, Yang D. The hysteresis response of soil CO2 concentration and soil respiration to soil temperature. J Geophys Res Biogeosciences. 2015;120: 1–14.

27. Jia X, Zha T, Wang S, Bourque CPA, Wang B, Qin S, et al. Canopy photosynthesis modulates soil respiration in a temperate semi-arid shrubland at multiple timescales. Plant Soil.; 2018;432: 437–450. doi: 10.1007/s11104-018-3818-z

28. Guan C, Li X, Zhang P, Chen Y. Diel hysteresis between soil respiration and soil temperature in a biological soil crust covered desert ecosystem. PLoS One. 2018;13. doi: 10.1371/journal.pone.0195606 29624606

29. Moyano F, Atkin O, Bahn M, Bruhn D, Burton A, Heinemeyer A, et al. Respiration from roots and the mycorrhizosphere. In: Bahn M, Heinemeyer A, Kutsch WL, editors. Soil Carbon Dynamics: An Integrated Methodology. Cambridge University Press; 2009. pp. 234–288.

30. Högberg P. Is tree root respiration more sensitive than heterotrophic respiration to changes in soil temperature? New Phytol. 2010;188: 9–10. doi: 10.1111/j.1469-8137.2010.03366.x 20673284

31. Balogh J, Papp M, Pintér K, Fóti S, Posta K, Eugster W, et al. Autotrophic component of soil respiration is repressed by drought more than the heterotrophic one in a dry grassland. Biogeosciences. 2016;13: 5171–5182. doi: 10.5194/bg-13-5171-2016

32. Casals P, Lopez-Sangil L, Carrara A, Gimeno C, Nogués S. Autotrophic and heterotrophic contributions to short-term soil CO2 efflux following simulated summer precipitation pulses in a Mediterranean dehesa. Global Biogeochem Cycles. 2011;25: GB3012. doi: 10.1029/2010GB003973

33. Shahzad T, Chenu C, Genet P, Barot S, Perveen N, Mougin C, et al. Contribution of exudates, arbuscular mycorrhizal fungi and litter depositions to the rhizosphere priming effect induced by grassland species. Soil Biol Biochem. 2015;80: 146–155. doi: 10.1016/j.soilbio.2014.09.023

34. Finzi AC, Abramoff RZ, Spiller KS, Brzostek ER, Darby BA, Kramer MA, et al. Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles. Glob Chang Biol. 2015;21: 2082–2094. doi: 10.1111/gcb.12816 25421798

35. Koncz P, Besnyői V, Csathó AI, Nagy J, Szerdahelyi T, Tóth Z, et al. Effect of grazing and mowing on the microcoenological composition of semi-arid grassland in Hungary. Appl Ecol Environ Res. 2014;12: 563–575. doi: 10.15666/aeer/1202_563575

36. Driessen P, Deckers J, Spaargaren O, Nachtergaele F, editors. Lecture notes on the major soils of the world. Food and Agriculture Organization (FAO); 2001.

37. Balogh J, Fóti S, Pintér K, Burri S, Eugster W, Papp M, et al. Soil CO2 efflux and production rates as influenced by evapotranspiration in a dry grassland. Plant Soil. Springer International Publishing; 2015;388: 157–173. doi: 10.1007/s11104-014-2314-3

38. Moyano F, Kutsch W, Schulze E. Response of mycorrhizal, rhizosphere and soil basal respiration to temperature and photosynthesis in a barley field. Soil Biol Biochem. 2007;39: 843–853. doi: 10.1016/j.soilbio.2006.10.001

39. Papp M, Fóti S, Nagy Z, Pintér K, Posta K, Fekete S, et al. Rhizospheric, mycorrhizal and heterotrophic respiration in dry grasslands. Eur J Soil Biol. Elsevier; 2018;85: 43–52. doi: 10.1016/j.ejsobi.2018.01.005

40. Pintér K, Balogh J, Nagy Z. Ecosystem scale carbon dioxide balance of two grasslands in Hungary under different weather conditions. Acta Biol Hung. 2010;61: 130–5. doi: 10.1556/ABiol.61.2010.Suppl.13 21565771

41. Koncz P, Pintér K, Balogh J, Papp M, Hidy D, Csintalan Z, et al. Extensive grazing in contrast to mowing is climate-friendly based on the farm-scale greenhouse gas balance. Agric Ecosyst Environ. 2017;240: 121–134. doi: 10.1016/j.agee.2017.02.022

42. Fratini G, Mauder M. Towards a consistent eddy-covariance processing: An intercomparison of EddyPro and TK3. Atmos Meas Tech. 2014;7: 2273–2281. doi: 10.5194/amt-7-2273-2014

43. Webb EK, Pearman GI, Leuning R. Correction of Flux Measurements for Density Effects Due to Heat and Water-vapor Transfer. Q J R Meteorol Soc. 1980;106: 85–100.

44. Reichstein M, Falge E, Baldocchi D, Papale D, Aubinet M, Berbigier P, et al. On the separation of net ecosystem exchange into assimilation and ecosystem respiration: Review and improved algorithm. Glob Chang Biol. 2005;11: 1424–1439. doi: 10.1111/j.1365-2486.2005.001002.x

45. Nagy Z, Pintér K, Pavelka M, Darenová E, Balogh J. Carbon balance of surfaces vs. ecosystems: advantages of measuring eddy covariance and soil respiration simultaneously in dry grassland ecosystems. Biogeosciences. 2011;8: 2523–2534. doi: 10.5194/bg-8-2523-2011

46. R Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria; 2018. Available:

47. Heinemeyer A, Tortorella D, Petrovičová B, Gelsomino A. Partitioning of soil CO2 flux components in a temperate grassland ecosystem. Eur J Soil Sci. 2012;63: 249–260. doi: 10.1111/j.1365-2389.2012.01433.x

48. Burri S, Sturm P, Prechsl UE, Knohl a., Buchmann N. The impact of extreme summer drought on the short-term carbon coupling of photosynthesis to soil CO2 efflux in a temperate grassland. Biogeosciences. 2014;11: 961–975. doi: 10.5194/bg-11-961-2014

49. De Deyn GB, Quirk H, Oakley S, Ostle N, Bardgett RD. Rapid transfer of photosynthetic carbon through the plant-soil system in differently managed species-rich grasslands. Biogeosciences. 2011;8: 1131–1139. doi: 10.5194/bg-8-1131-2011

50. Aubrey DP, Teskey RO. Stored root carbohydrates can maintain root respiration for extended periods. New Phytol. 2018;218: 142–152. doi: 10.1111/nph.14972 29281746

51. Aubrey DP, Teskey RO. Root-derived CO2 efflux via xylem stream rivals soil CO2 efflux. New Phytol. 2009;184: 35–40. doi: 10.1111/j.1469-8137.2009.02971.x 19674328

52. Bloemen J, McGuire MA, Aubrey DP, Teskey RO, Steppe K. Transport of root-respired CO2 via the transpiration stream affects aboveground carbon assimilation and CO2 efflux in trees. New Phytol. 2013;197: 555–65.

53. Lynch DJ, Matamala R, Iversen CM, Norby RJ, Gonzalez-Meler MA. Stored carbon partly fuels fine-root respiration but is not used for production of new fine roots. New Phytol. 2013;199: 420–430. doi: 10.1111/nph.12290 23646982

54. Nickerson N, Risk D. Physical controls on the isotopic composition of soil-respired CO2. J Geophys Res Biogeosciences. 2009;114: 1–14. doi: 10.1029/2008JG000766

55. Kayler ZE, Ganio L, Hauck M, Pypker TG, Sulzman EW, Mix AC, et al. Bias and uncertainty of δ13CO2 isotopic mixing models. Oecologia. 2010;163: 227–34. doi: 10.1007/s00442-009-1531-6 20043179

56. Moyes AB, Gaines SJ, Siegwolf RTW, Bowling DR. Diffusive fractionation complicates isotopic partitioning of autotrophic and heterotrophic sources of soil respiration. Plant Cell Environ. 2010;33: 1804–19. doi: 10.1111/j.1365-3040.2010.02185.x 20545887

57. Brüggemann N, Gessler A, Kayler Z, Keel SG, Badeck F, Barthel M, et al. Carbon allocation and carbon isotope fluxes in the plant soil-atmosphere continuum: a review. Biogeosciences. 2011;8: 3457–3489. doi: 10.5194/bgd-8-3619-2011

58. Gessler A, Tcherkez G, Peuke AD, Ghashghaie J, Farquhar GD. Experimental evidence for diel variations of the carbon isotope composition in leaf, stem and phloem sap organic matter in Ricinus communis. Plant, Cell Environ. 2008; 31: 941–953. doi: 10.1111/j.1365-3040.2008.01806.x 18331588

59. Kayler Z, Gessler A, Buchmann N. What is the speed of link between aboveground and belowground processes? New Phytol. 2010;187: 885–888. doi: 10.1111/j.1469-8137.2010.03332.x 20707852

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2019 Číslo 10
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