Temperature sensitivity patterns of carbon and nitrogen processes in decomposition of boreal organic soils – Quantification in different compounds and molecule sizes based on a multifactorial experiment

Autoři: Ari Laurén aff001;  Mari Lappalainen aff001;  Antti-Jussi Kieloaho aff002;  Kristiina Karhu aff003;  Marjo Palviainen aff003
Působiště autorů: School of Forest Sciences, Faculty of Science and Forestry, University of Eastern Finland, Joensuu, Finland aff001;  Natural Resources Institute Finland (Luke), Helsinki, Finland aff002;  Department of Forest Sciences, University of Helsinki, Helsinki, Finland aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223446


Climate warming and organic matter decomposition are connected in a recursive manner; this recursion can be described by temperature sensitivity. We conducted a multifactorial laboratory experiment to quantify the temperature sensitivity of organic carbon (C) and nitrogen (N) decomposition processes of common boreal organic soils. We incubated 36 mor and 36 slightly decomposed Carex-Sphagnum peat samples in a constant moisture and ambient temperature for 6 months. The experiment included three temperature and two moisture levels and two food web manipulations (samples with and without fungivore enchytraeid worms). We determined the release of carbon dioxide (CO2) and dissolved organic carbon (DOC) in seven molecular size classes together with ammonium N and dissolved organic N in low molecular weight and high molecular weight fractions. The temperature sensitivity function Q10 was fit to the data. The C and N release rate was almost an order of magnitude higher in mor than in peat. Soil fauna increased the temperature sensitivity of C release. Soil fauna played a key role in N release; when fauna was absent in peat, the N release was ceased. The wide range of the studied C and N compounds and treatments (68 Q10 datasets) allowed us to recognize five different temperature sensitivity patterns. The most common pattern (37 out of 68) was a positive upwards temperature response, which was observed for CO2 and DOC release. A negative downward pattern was observed for extractable organic nitrogen and microbial C. Sixteen temperature sensitivity patterns represented a mixed type, where the Q10function was not applicable, as this does not allow changing the sign storage change rate with increasing or decreasing temperature. The mixed pattern was typically connected to intermediate decomposition products, where input and output fluxes with different temperature sensitivities may simultaneously change the storage. Mixed type was typical for N processes. Our results provide useful parameterization for ecosystem models that describe the feedback loop between climate warming, organic matter decomposition, and productivity of N-limited vegetation.

Klíčová slova:

Carbon dioxide – Climate change – Decomposition – Forests – Specimen storage – Wetlands – Q10 temperature coefficient – Ultrafiltration


1. IPCC. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J et al., editors. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, 2013 1535 p.

2. Deluca T, Boisvenue C. Boreal forest soil carbon: distribution, function and modelling. Forestry 2012; 85: 161–84.

3. Moore T, Basiliko N. Decomposition in boreal peatlands. In: Wieder RK, Vitt DH, editors. Boreal Peatland Ecosystems. Springer-Verlag, Berlin; 2006.

4. Bragazza L, Freeman C, Jones T, Rydin H, Limpens J, Fenner N, et al. Atmospheric nitrogen deposition promotes carbon loss from peat bogs. Proceedings of the National Academy of Sciences of the United States of America 2006; 103: 19386–9. doi: 10.1073/pnas.0606629104 17151199

5. Lappalainen M, Palviainen M, Kukkonen JVK, Setälä H, Piirainen S, Sarjala T, et al. Release of carbon in different molecule size fractions from decomposing boreal mor and peat as affected by Enchytraeid worms. Water Air Soil Poll 2018; 229: 240 https://doi.org/10.1007/s11270-018-3871-5

6. Heimann M., Reichstein M. Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 2008; 451: 289–92. doi: 10.1038/nature06591 18202646

7. Li J, Pei J, Cui J, Chen X, Li B, Nie M. et al. Carbon quality mediates the temperature sensitivity of soil organic carbon decomposition in managed ecosystems. Agr Ecosyst Environ 2017; 250, 44–50.

8. Bagherzadeh A, Brumme R, Beese F. Temperature dependence of nitrogen mineralization and microbial status in OH horizon of a temperate forest ecosystem. J Forestry Res 2008; 19(1): 37–43.

9. Fraser FC, Hallett PD, Wookey PA, Hartley IP, Hopkins DW. How do enzymes catalysing soil nitrogen transformations respond to changing temperatures? Biol Fert Soils 2013; 49: 99–103.

10. Liu Y, Wang C, He N, Wen X, Gao Y, Li S, et al. Global synthesis of the rate and temperature sensitivity of soil nitrogen mineralization: Latitudinal patterns and mechanism. Glob Change Biol 2017; 23: 455–464.

11. Davidson EA, Janssens IA, Luo Y. On the variability of respiration in terrestrial ecosystems: moving beyond Q10. Glob Change Biol 2006; 12: 154–64. https://doi.org/10.1111/j.1365-2486.2005.01065.x

12. Karhu K, Fritze H, Tuomi M, Vanhala P, Spetz P, Kitunen V, et al. Temperature sensitivity of organic matter decomposition in two boreal forest soil profiles. Soil Biol Biochem 2010; 42: 72–82.

13. Beier C, Emmet PA, Peñuelas J, Schmidt IK, Tietema A, Estiarte M, et al. Carbon and nitrogen cycles in European: ecosystems respond differently to global warming. Sci Total Environ 2008; 407: 692–97. doi: 10.1016/j.scitotenv.2008.10.001 18930514

14. Weedon JT, Kowalchuk GA, Aerts R, van Hal JR, van Logtestijn RKSP, Tas N, et al. Summer warming accelerates sub-arctic peatland nitrogen cycling without changing enzyme pools or microbial community structure. Glob Change Biol 2012; 18: 138–50.

15. Mastný J, Kaštovská E, Bárta J, Chronáková A, Borovec J, Šantrucková H., et al. Quality of DOC produced during litter decomposition of peatland plant dominants. Soil Biol Biochem 2018; 121: 221–30.

16. Mellilo JM, Butler S, Johnsson J, Mohan J, Steudler P, Lux H, et al. Soil warming, carbon–nitrogen interactions, and forest carbon budgets. PNAS 2011; 108 (23): 9508–12. doi: 10.1073/pnas.1018189108 21606374

17. Guntiñas ME, Leirós MC, Trasar-Cepeda C, Gil-Sotres F. Effects of moisture and temperature on net soil nitrogen mineralization: A laboratory study. Eur J Soil Biol 2012; 48: 73–80.

18. Novem Auyeung DS, Suseela VA, Dukes JS. Warming and drought reduce temperature sensitivity of nitrogen transformations. Glob Change Biol 2013; 19: 662–76.

19. Huhta V, Persson T, Setälä H. Functional implications of soil fauna diversity in boreal forests. Appl Soil Ecol 1998; 10: 277–88.

20. Berg M, de Ruiter P, Didden W, Janssen M, Schouten T, Verhoef H. Community food web, decomposition and nitrogen mineralisation in a stratified Scots pine forest soil. Oikos 2001; 93: 130–42.

21. Popatov AM, Tiunov AV. Stabile isotope composition of mycophagous collembolas versus mycotrophic plants: Do soil invertebrates feed on mycorrhizal fungi? Soil Biol Biochem 2016; 93: 115–8.

22. Nurminen M. Ecology of enchytraeids (Oligochaeta) in Finnish coniferous forest soil. Ann Zool Fenn 1967; 4: 147–57.

23. Abrahamsen G. Ecological study of Enchytraeidae (Oligochaeta) in Norwegian coniferous forest soils. Pedobiologia 1972; 12: 26–82.

24. Laakso J, Setälä H. Sensitivity of primary production to changes in the architecture of belowground foodwebs. Oikos 1999; 87: 57–64.

25. Silvan N, Laiho R, Vasander H. Changes in mesofauna abundance in peat soils drained for forestry. Forest Ecol Manag 2000; 133: 127–33.

26. Carrera N, Barreal ME, Gallego PP, Briones MJI. Soil invertebrates control peatland C fluxes in response to warming. Funct Ecol 2009; 23: 637–48.

27. Laurén A, Lappalainen M, Saari P., Kukkonen J.V.K, Koivusalo H., Piirainen S. et al. Nitrogen and carbon dynamics and the role of Enchytraeid worms in decomposition of boreal mor. Water Air Soil Poll 2012; 223: 3701–19. doi: 10.1007/s11270-012-1142-4

28. Lappalainen M, Kukkonen JVK, Piirainen S, Sarjala T, Setälä H, Koivusalo H., et al. Nitrogen release in decomposition of boreal mor and peat as affected by enchytraeid worms. Bor Environ Res 2013; 18: 181–94.

29. Grandy AS, Wieder WR, Wickings K, Kyker-Snowman E. Beyond microbes: Are fauna the next frontier in soil biogeochemical models? Soil Biol Biochem 2016; 102: 40–4.

30. Kellomäki S. Managing boreal forests in the context of climate change. Impacts, adaptation and climate change mitigation. CRC Press; 2017.

31. Tamminen P. (Expression of soil nutrient status and regional variation in soil fertility of forested sites in southern Finland). Kangasmaan ravinnetunnusten ilmaiseminen ja viljavuuden alueellinen vaihtelu Etelä-Suomessa. Folia Forestalia 1991; 777. In Finnish with English summary.

32. Tomppo E. (Forest site types and tree stands) Kasvupaikat ja puusto. In: Reinikainen A, Mäkipää R, Vanha-Majamaa I, Hotanen JP, editors. Kasvit muuttuvassa metsäluonnossa (pp. 60–83). Tammi, Helsinki. 2000. In Finnish.

33. Virtanen K, Hänninen P, Kallinen RL, Vartiainen S, Herranen T, Jokisaari R. (The Peat Reserves of Finland in 2000). Suomen turvevarat 2000. Geological Survey of Finland, Report of Investigation 156. 2003. In Finnish with English summary.

34. Pirinen P, Simola H, Aalto J, Kaukoranta JP, Karlsson P, Ruuhela R. Climatological statistics of Finland 1981–2010. Finnish Meteorological Institute. Reports 2012; 1. Helsinki.

35. Finér L, Ahtiainen M, Mannerkoski H, Möttönen V, Piirainen S, Seuna P, et al. Effects of harvesting and scarification on water and nutrient fluxes. A description of catchment and methods, and results from the pretreatment calibration period. Finnish Forest Research Institute, Research Papers 1997; 648.

36. von Post L. Sveriges geologiska undersöknings torvinventering och några av dess hittills vunna resultat. Svenska Mosskulturföreningens Tidskrift 1922; 37: 1–27. Swedish.

37. Ahtiainen M, Huttunen P. Long-term effects of forestry managements on water quality and loading in brooks. Boreal Environ Res 1999; 4: 101–14.

38. Haahti K, Nieminen M, Finér L, Marttila H, Kokkonen T, Leinonen A, et al. Model-based evaluation of sediment control in a drained peatland forest after ditch network maintenance. Can J For Res 2018; 48: 130–40.

39. Päivänen J. Hydraulic conductivity and water retention in peat soils. Acta Forestalia Fennica 1973; 129, 70 p.

40. Laurén A, Mannerkoski H. Hydraulic properties of mor layer in Finland. Scand J Forest Res 2000; 16(5): 429–41.

41. O’Connor FB. 1962. The extraction of Enchytraeidae from soil. In: Murphy PW, editor. Progress in Soil Zoology. Butterworth, London; 1962. p. 279–85.

42. Brookes PC, Landman A, Pruden G, Jenkinson DS. Chloroform fumigation and the release of soil nitrogen: A rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 1985;17: 837–42. https://doi.org/10.1016/0038-0717(85)90144-0

43. Sparling GP, Feltham CW, Reynolds J, West AW, Singleton P. Estimation of soil microbial C by a fumigation-extraction method: Use on soils of high organic matter content, and a reassessment of the kEC-factor. Soil Biol Biochem 1990; 22(3): 301–7.

44. Vance ED, Brookes PC, Jenkinson DS. An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 1987; 19(6): 703–7.

45. Conant RT, Ryan MG, Ågren GI, Birge HE, Davidson EA, Eliasson PE, et al. Temperature and soil organic matter decomposition rates–synthesis of current knowledge and a way forward. Glob Change Biol 2011; 17: 3392–404.

46. Hamdi S, Moyano F, Sall S, Bernoux M, Chevallier T. Synthesis analysis of the temperature sensitivity of soil respiration studies in relation to incubation methods and soil conditions. Soil Biol Biochem 2013; 58: 115–26.

47. SciPy Reference Guide 2018. Release 1.2.0. 2018; (https://docs.scipy.org/doc/scipy/scipy-ref-1.2.0.pdf), 2411 p.

48. Williams JS, Dungait JAJ, Bol R, Abbot GD. Contrasting temperature responses of dissolved organic carbon and phenols leached from soils. Plant Soil 2016; 399: 13–27. doi: 10.1007/s11104-015-2678-z 26900180

49. Moinet GYK, Hunt JE, Kirchbaum MUF, Morcom CP, Midwood AJ, Millard P. The temperature sensitivity of soil organic matter decomposition is constrained by microbial access to substrates. Soil Biol Biochem 2017; 116: 333–9.

50. Bracho R, Natali S, Pegoraro E, Grummer KG, Schädel C, Ceils G, et al. Temperature sensitivity of organic matter decomposition of permafrost-region soils during laboratory incubations. Soil Biol Biochem 2016; 97: 1–14.

51. Tian Q, Wang X, Wang D, Wang M, Liao C, Yang X, et al. Decoupled linkage between soil carbon and nitrogen mineralization among soil depths in a subtropical mixed forest. Soil Biol Biochem 2017; 109: 135–44.

52. Conant RT, Drijber RA, Haddix ML, Parton WM, Paul EA, Plante AF, et al. Sensitivity of organic matter decomposition to warming varies with its quality. Glob Change Biol 2008; 14: 1–10. doi: 10.1111/j.1365-2486.2008.01541.x

53. Davidson EA, Janssens IA. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 2006; 440: 165–173. doi: 10.1038/nature04514 16525463

54. Feier N, Ladau J, Clemente JC, Leff JW, Owens SM, Pollard KS, et al. Reconstructing the microbial diversity and function of pre-agricultural tallgrass prairie soils in the United States. Science 2013; 342: 621–4. doi: 10.1126/science.1243768 24179225

55. Min K, Lehmeier CA, Ballantyne F, Tatarko A, Billings SA. Differential effects of pH on temperature sensitivity of organic carbon and nitrogen decay. Soil Biol Biochem 2014; 76: 193–200.

56. van Vliet PCJ, Beare MH, Coleman DC, Hendrix PF. Effects of enchytraeids (Annelida: Oligochaeta) on soil carbon and nitrogen dynamics in laboratory incubations. Appl Soil Ecol 2004; 25: 147–60. https://doi.org/10.1016/j.apsoil.2003.08.004

57. Cole L, Bradgett RD, Ineson P. Enchytraeid worms (Oligochaeta) enhance mineralization of carbon in organic upland soil. Eur J Soil Sci 2000; 51: 185–92. https://doi.org/10.1046/j.1365-2389.2000.00297.x

58. Didden WAM. Ecology of terrestrial Enchytraeidae. Pedobiologia 1993; 37: 2–29.

59. Siira-Pietikäinen A, Pietikäinen J, Fritze H, Haimi J. Short-term responses of soil decomposer communities to forest management: clear felling versus alternative forest harvesting methods. Can J For Res 2001; 31: 88–99.

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