Nine years of in situ soil warming and topography impact the temperature sensitivity and basal respiration rate of the forest floor in a Canadian boreal forest


Autoři: Charles Marty aff001;  Joanie Piquette aff001;  Hubert Morin aff001;  Denis Bussières aff002;  Nelson Thiffault aff003;  Daniel Houle aff004;  Robert L. Bradley aff005;  Myrna J. Simpson aff006;  Rock Ouimet aff004;  Maxime C. Paré aff001
Působiště autorů: Laboratoire d’écologie végétale et animale, Département des sciences fondamentales, Université du Québec à Chicoutimi, Chicoutimi, Québec, Canada aff001;  Département des sciences fondamentales, Université du Québec à Chicoutimi, Chicoutimi, Québec, Canada aff002;  Centre Canadien sur la fibre de bois, Service canadien des forêts, Québec, Québec, Canada aff003;  Direction de la recherche forestière, Ministère des Forêts, de la Faune et des Parcs, Québec, Québec, Canada aff004;  Département de Biologie, Université de Sherbrooke, Sherbrooke, Québec, Canada aff005;  Environmental NMR Centre and Department of Physical and Environmental Sciences, University of Toronto Scarborough, Toronto, Ontario, Canada aff006
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226909

Souhrn

The forest floor of boreal forest stores large amounts of organic C that may react to a warming climate and increased N deposition. It is therefore crucial to assess the impact of these factors on the temperature sensitivity of this C pool to help predict future soil CO2 emissions from boreal forest soils to the atmosphere. In this study, soil warming (+2–4°C) and canopy N addition (CNA; +0.30–0.35 kg·N·ha-1·yr-1) were replicated along a topographic gradient (upper, back and lower slope) in a boreal forest in Quebec, Canada. After nine years of treatment, the forest floor was collected in each plot, and its organic C composition was characterized through solid-state 13C nuclear magnetic resonance (NMR) spectroscopy. Forest floor samples were incubated at four temperatures (16, 24, 32 and 40°C) and respiration rates (RR) measured to assess the temperature sensitivity of forest floor RR (Q10 = e10k) and basal RR (B). Both soil warming and CNA had no significant effect on forest floor chemistry (e.g., C, N, Ca and Mg content, amount of soil organic matter, pH, chemical functional groups). The NMR analyses did not show evidence of significant changes in the forest floor organic C quality. Nonetheless, a significant effect of soil warming on both the Q10 of RR and B was observed. On average, B was 72% lower and Q10 45% higher in the warmed, versus the control plots. This result implies that forest floor respiration will more strongly react to changes in soil temperature in a future warmer climate. CNA had no significant effect on the measured soil and respiration parameters, and no interaction effects with warming. In contrast, slope position had a significant effect on forest floor organic C quality. Upper slope plots had higher soil alkyl C:O-alkyl C ratios and lower B values than those in the lower slope, across all different treatments. This result likely resulted from a relative decrease in the labile C fraction in the upper slope, characterized by lower moisture levels. Our results point towards higher temperature sensitivity of RR under warmer conditions, accompanied by an overall down-regulation of RR at low temperatures (lower B). Since soil C quantity and quality were unaffected by the nine years of warming, the observed patterns could result from microbial adaptations to warming.

Klíčová slova:

Carbon dioxide – Fertilizers – Forest ecology – Forests – Chemical deposition – Landforms – Q10 temperature coefficient – Soil chemistry


Zdroje

1. Davidson EA, Janssens IA. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature [Internet]. 2006 Mar 9 [cited 2011 Jun 11];440(7081):165–73. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16525463 doi: 10.1038/nature04514

2. 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 Chang Biol [Internet]. 2011 Nov 2 [cited 2013 Oct 22];17(11):3392–404. Available from: http://doi.wiley.com/10.1111/j.1365-2486.2011.02496.x

3. Kirschbaum MUFF. The temperature dependence of soil organic matter decomposition, and the effect of global warming on soil organic C storage. Soil Biol Biochem [Internet]. 1995;27(6):753–60. Available from: http://linkinghub.elsevier.com/retrieve/pii/003807179400242S

4. Melillo JM, Frey SD, Deangelis KM, Werner WJ, Bernard MJ, Bowles FP, et al. Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world. Science (80-). 2017;358:101–5.

5. Hamdi S, Moyano F, Sall S, Bernoux M, Chevallier T. Synthesis analysis of the temperature sensitivity of soil respiration from laboratory studies in relation to incubation methods and soil conditions. Soil Biol Biochem [Internet]. 2013;58:115–26. Available from: http://dx.doi.org/10.1016/j.soilbio.2012.11.012

6. Aguilos M, Takagi K, Liang N, Watanabe Y, Teramoto M, Goto S, et al. Sustained large stimulation of soil heterotrophic respiration rate and its temperature sensitivity by soil warming in a cool-temperate forested peatland. Tellus, Ser B Chem Phys Meteorol. 2013;65(1):0–13.

7. Tremblay SL, D’Orangeville L, Lambert MC, Houle D. Transplanting boreal soils to a warmer region increases soil heterotrophic respiration as well as its temperature sensitivity. Soil Biol Biochem [Internet]. 2018;116(October 2017):203–12. Available from: http://dx.doi.org/10.1016/j.soilbio.2017.10.018

8. D’Orangeville L, Côté B, Houle D, Whalen J. Reduced mineralizable carbon in a boreal forest soil after three years of artificial warming. Can J Soil Sci [Internet]. 2013;93(5):567–72. Available from: http://pubs.aic.ca/doi/abs/10.4141/cjss2013-046

9. Bronson DR, Gower ST, Tanner M, Linder S, Van Herk I. Response of soil surface CO2 flux in a boreal forest to ecosystem warming. Glob Chang Biol [Internet]. 2007;14(4):856–67. Available from: http://doi.wiley.com/10.1111/j.1365-2486.2007.01508.x

10. Schinlbacher A, Schnecker G, Takriti M, Borken W, Wanek W. Microbial physiology and soil CO2 efflux after 9 years of soil warming in a temperate forest–no indications for thermal adaptations. Glob Chang Biol. 2015;21:4265–77. doi: 10.1111/gcb.12996 26046333

11. Melillo JM, Steudler PA, Aber JD, Newkirk K, Lux H, Bowles FP, et al. Soil warming and carbon-cycle feedbacks to the climate system. Science (80-). 2002;298(5601):2173–6.

12. Luo Y, Wan S, Hui D, Wallace LL. Acclimatization of soil respiration to warming in a tall grass prairie. Nature. 2001;413(6856):622–5. doi: 10.1038/35098065 11675783

13. Bradford MA, Davies CA, Frey SD, Maddox TR, Melillo JM, Mohan JE, et al. Thermal adaptation of soil microbial respiration to elevated temperature. Ecol Lett. 2008;11(12):1316–27. doi: 10.1111/j.1461-0248.2008.01251.x 19046360

14. Dalias P, Anderson JM, Bottner P, Coûteaux MM. Temperature responses of carbon mineralization in conifer forest soils from different regional climates incubated under standard laboratory conditions. Glob Chang Biol. 2001;7(2):181–92.

15. Walker TWN, Kaiser C, Strasser F, Herbold CW, Leblans NIW, Woebken D, et al. Microbial temperature sensitivity and biomass change explain soil carbon loss with warming. Nat Clim Chang [Internet]. 2018;8(10):885–9. Available from: https://doi.org/10.1038/s41558-018-0259-x 30288176

16. Houle D, Bouffard A, Duchesne L, Logan T, Harvey R. Projections of Future Soil Temperature and Water Content for Three Southern Quebec Forested Sites. J Clim [Internet]. 2012 Nov [cited 2012 Nov 13];25(21):7690–701. Available from: http://journals.ametsoc.org/doi/abs/10.1175/JCLI-D-11-00440.1

17. Fierer N, Craine JM, Mclauchlan KK, Schimel JP. Litter quality and the temperature sensitivity of decomposition. Ecology. 2005;86(2):320–6.

18. Conant RT, Drijber RA, Haddix ML, Parton WJ, Paul EA, Plante AF, et al. Sensitivity of organic matter decomposition to warming varies with its quality. Glob Chang Biol. 2008;14(4):868–77.

19. Conant RT, Steinweg MJ, Haddix ML, Paul EA, Plante AF, Six J. Experimental warming shows that decomposition temperature sensitivity increases with soil organic matter recalcitrance. Ecology [Internet]. 2008;89(9):2384–91. Available from: http://www.esajournals.org/doi/pdf/10.1890/08-0137.1 18831158

20. Noh NJ, Kuribayashi M, Saitoh TM, Nakaji T, Nakamura M, Hiura T, et al. Responses of soil, heterotrophic, and autotrophic respiration to experimental open-field soil warming in a cool-temperate deciduous forest. Ecosystems. 2016;19(3):504–20.

21. Vanhala P, Karhu K, Tuomi M, Björklöf K, Fritze H, Hyvärinen H, et al. Transplantation of organic surface horizons of boreal soils into warmer regions alters microbiology but not the temperature sensitivity of decomposition. Glob Chang Biol. 2011;17(1):538–50.

22. Hobbie SE, Nadelhoffer KJ, Högberg P. A synthesis: The role of nutrients as constraints on carbon balances in boreal and arctic regions. Plant Soil. 2002;242(1):163–70.

23. Schimel JP, Bennett JB. Nitrogen mineralization: challenges of a changing paradigm. Ecology. 2004;85(3):591–602.

24. Eberwein JR, Oikawa PY, Allsman LA, Jenerette GD. Carbon availability regulates soil respiration response to nitrogen and temperature. Soil Biol Biochem [Internet]. 2015;88:158–64. Available from: http://dx.doi.org/10.1016/j.soilbio.2015.05.014

25. Knorr AM, Frey SD, Curtis PS. Nitrogen additions and litter decomposition : A meta-analysis. Ecology. 2005;86(12):3252–7.

26. Zak DR, Freedman ZB, Upchurch RA, Steffens M, Kögel-Knabner I. Anthropogenic N deposition increases soil organic matter accumulation without altering its biochemical composition. Glob Chang Biol [Internet]. 2017 Feb;23(2):933–44. Available from: http://doi.wiley.com/10.1111/gcb.13480 27562874

27. Maaroufi NI, Nordin A, Hasselquist NJ, Bach LH, Palmqvist K, Gundale MJ. Anthropogenic nitrogen deposition enhances carbon sequestration in boreal soils. Glob Chang Biol. 2015;21(8):3169–80. doi: 10.1111/gcb.12904 25711504

28. Janssens IA, Dieleman W, Luyssaert S, Subke JA, Reichstein M, Ceulemans R, et al. Reduction of forest soil respiration in response to nitrogen deposition. Nat Geosci [Internet]. 2010;3:315–22. Available from: http://dx.doi.org/10.1038/ngeo844

29. Pisani O, Frey SD, Simpson AJ, Simpson MJ. Soil warming and nitrogen deposition alter soil organic matter composition at the molecular-level. Biogeochemistry. 2015;123(3):391–409.

30. Frey SD, Knorr M, Parrent JL, Simpson RT. Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manage. 2004;196(1):159–71.

31. Frey SD, Ollinger S, Nadelhoffer K, Bowden R, Brzostek E, Burton A, et al. Chronic nitrogen additions suppress decomposition and sequester soil carbon in temperate forests. Biogeochemistry. 2014;121(2):305–16.

32. Pan Y, Birdsey RA, Fang J, Houghton R, Kauppi PE, Kurz WA, et al. A large and persistent carbon sink in the world’s forests. Science (80-). 2011;333(July):988–93.

33. Lal R. Forest soils and carbon sequestration. For Ecol Manage [Internet]. 2005 Dec 10 [cited 2011 Aug 1];220(1–3):242–58. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0378112705004834

34. Laganière J, Paré D, Bergeron Y, Chen HYH, Brassard BW, Cavard X. Stability of soil carbon stocks varies with forest composition in the Canadian boreal biome. Ecosystems [Internet]. 2013 Mar 21 [cited 2013 Jul 19];16(5):852–65. Available from: http://link.springer.com/10.1007/s10021-013-9658-z

35. Frey SD, Drijber R, Smith H, Melillo J. Microbial biomass, functional capacity, and community structure after 12 years of soil warming. Soil Biol Biochem [Internet]. 2008;40(11):2904–7. Available from: http://dx.doi.org/10.1016/j.soilbio.2008.07.020

36. Tang J, Cheng H, Fang C. The temperature sensitivity of soil organic carbon decomposition is not related to labile and recalcitrant carbon. PLoS One. 2017;12(11):1–15.

37. Houle D, Bouffard A, Duchesne L, Logan T, Harvey R. Projections of Future Soil Temperature and Water Content for Three Southern Quebec Forested Sites. J Clim [Internet]. 2012 Nov [cited 2013 Oct 7];25(21):7690–701. Available from: http://journals.ametsoc.org/doi/abs/10.1175/JCLI-D-11-00440.1

38. De Barba D, Rossi S, Deslauriers A, Morin H. Effects of soil warming and nitrogen foliar applications on bud burst of black spruce. Trees. 2016;30:87–97.

39. Dao MCE, Rossi S, Walsh D, Morin H, Houle D. A 6-year-long manipulation with soil warming and canopy nitrogen additions does not affect xylem phenology and cell production of mature black spruce. Front Plant Sci. 2015;6:877. doi: 10.3389/fpls.2015.00877 26617610

40. Rossi S, Bordeleau A, Morin H, Houle D. The effects of N-enriched rain and warmer soil on the ectomycorrhizae of black spruce remain inconclusive in the short term. Ann For Sci. 2013;70:825–834.

41. Rossi S, Morin H, Deslauriers A. Multi-scale influence of snowmelt on xylogenesis of black spruce. Arctic, Antarct Alp Res. 2011;43:457–464.

42. Lupi C, Morin H, Deslauriers A, Rossi S, Houle D. Increasing nitrogen availability and soil temperature: effects on xylem phenology and anatomy of mature black spruce. Can J For Res. 2012;42(1277–1288).

43. Ouimet R, Duchesne L. Dépôts atmosphériques dans les forêts au Québec: retombées actuelles et tendances au cours des 20 à 30 dernières années. Le Nat Can. 2009;133(1):56–64.

44. Laganière J, Paré D, Bergeron Y, Chen HYH. The effect of boreal forest composition on soil respiration is mediated through variations in soil temperature and C quality. Soil Biol Biochem. 2012;53:18–27.

45. Laganière J, Podrebarac F, Billings SA, Edwards KA, Ziegler SE. A warmer climate reduces the bioreactivity of isolated boreal forest soil horizons without increasing the temperature sensitivity of respiratory CO2 loss. Soil Biol Biochem. 2015;84:177–88.

46. Fierer N, Allen AS, Schimel JP, Holden PA. Controls on microbial CO2 production: A comparison of surface and subsurface soil horizons. Glob Chang Biol. 2003;9(9):1322–32.

47. Moyano FE, Manzoni S, Chenu C. Responses of soil heterotrophic respiration to moisture availability: An exploration of processes and models. Soil Biol Biochem [Internet]. 2013 Apr [cited 2013 Mar 6];59:72–85. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0038071713000138

48. Zhou W, Hui D, Shen W. Effects of soil moisture on the temperature sensitivity of soil heterotrophic respiration: a laboratory incubation study. PLoS One. 2014;9(3):e92531. doi: 10.1371/journal.pone.0092531 24647610

49. Fierer N, Colman BP, Schimel JP, Jackson RB. Predicting the temperature dependence of microbial respiration in soil : A continental-scale analysis. Global Biogeochem Cycles. 2006;20:GB3026.

50. R Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org.; 2015.

51. Conte P, Spaccini R, Piccolo A. State of the art of CPMAS 13C-NMR spectroscopy applied to natural organic matter. Prog Nucl Magn Reson Spectrosc. 2004;44:215–23.

52. Preston CM, Trofymow JA, Sayer BG, Niu J. 13C nuclear magnetic resonance spectroscopy with cross-polarization and magic-angle spinning investigation of the proximate-analysis fractions used to assess litter quality in decomposition studies. Can J Bot. 1997;75(9):1601–13.

53. Baldock JA, Oades JM, Waters AG, Peng X, Vassallo AM, Wilson MA. Aspects of the chemical structure of soil organic materials as revealed by solid-state 13C NMR spectroscopy. Biogeochemistry. 1992;16:1–42.

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

55. Peng S, Piao S, Wang T, Sun J, Shen Z. Temperature sensitivity of soil respiration in different ecosystems in China. Soil Biol Biochem [Internet]. 2009;41(5):1008–14. Available from: http://dx.doi.org/10.1016/j.soilbio.2008.10.023

56. Craine JM, Fierer N, McLauchlan KK, Elmore AJ. Reduction of the temperature sensitivity of soil organic matter decomposition with sustained temperature increase. Biogeochemistry. 2013;113(1–3):359–68.

57. Tuomi M, Vanhala P, Karhu K, Fritze H, Liski J. Heterotrophic soil respiration-Comparison of different models describing its temperature dependence. Ecol Modell. 2008;211(1–2):182–90.

58. Feng X, Simpson AJ, Wilson KP, Dudley Williams D, Simpson MJ. Increased cuticular carbon sequestration and lignin oxidation in response to soil warming. Nat Geosci. 2008;1(12):836–9.

59. Zhang W, Parker KM, Luo Y, Wan S, Wallace LL, Hu S. Soil microbial responses to experimental warming and clipping in a tallgrass prairie. Glob Chang Biol. 2005;11:266–77.

60. Zogg GP, Zak DR, Ringelberg DB, Macdonald NW, Pregitzer KS, White DC. Compositional and functional shifts in microbial communities due to soil warming. Soil sci Soc Am J. 1993;61:475–81.

61. Hartley IP, Heinemeyer A, Ineson P. 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 Chang Biol. 2007;13:1761–70.

62. Liu D, Keiblinger KM, Schindlbacher A, Wegner U, Sun H, Fuchs S, et al. Microbial functionality as affected by experimental warming of a temperate mountain forest soil—A metaproteomics survey. Appl Soil Ecol [Internet]. 2017;117–118(May):196–202. Available from: http://dx.doi.org/10.1016/j.apsoil.2017.04.021

63. Saleska SR, Harte J, Torn MS. The effect of experimental ecosystem warming on CO2 fluxes in a montane meadow. Glob Chang Biol. 1999;5(2):125–41.

64. Moinet GYK, Hunt JE, Kirschbaum 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 [Internet]. 2018;116(October 2017):333–9. Available from: https://doi.org/10.1016/j.soilbio.2017.10.031

65. Fontaine S, Barot S, Barré P, Bdioui N, Mary B, Rumpel C. Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature [Internet]. 2007 Nov 8 [cited 2013 Sep 24];450(7167):277–80. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17994095 17994095

66. Six J, Frey SD, Thiet RK, Batten KM. Bacterial and Fungal Contributions to Carbon Sequestration in Agroecosystems. Soil Sci Soc Am J [Internet]. 2006;70(2):555. Available from: https://www.soils.org/publications/sssaj/abstracts/70/2/555

67. Benbi DK, Boparai AK, Brar K. Decomposition of particulate organic matter is more sensitive to temperature than the mineral associated organic matter. Soil Biol Biochem [Internet]. 2014;70:183–92. Available from: http://dx.doi.org/10.1016/j.soilbio.2013.12.032

68. Ramirez KS, Craine JM, Fierer N. Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Glob Chang Biol. 2012;18:1918–27.

69. Liu J, Wu N, Wang H, Sun J, Peng B, Jiang P, et al. Nitrogen addition affects chemical compositions of plant tissues, litter and soil organic matter. Ecology. 2016;97:1796–806. doi: 10.1890/15-1683.1 27859176

70. Houle D, Marty C, Duschesne L. Response of nitrogen canopy uptake to a rapid decrease in bulk nitrate deposition in two eastern Canadian boreal forests. Oecologia. 2015;(177):29–37.

71. Gundale MJ, Deluca TH, Nordin A. Bryophytes attenuate anthropogenic nitrogen inputs in boreal forests. Glob Chang Biol [Internet]. 2011 Aug 1 [cited 2011 Aug 18];17(8):2743–53. Available from: http://doi.wiley.com/10.1111/j.1365-2486.2011.02407.x

72. Hobbie SE, Schimel JP, Trumbore SE, Randerson JR. Controls over carbon storage and turnover in high-latitude soils. Glob Chang Biol. 2000;6:196–210.

73. Yano Y, Shaver GR, Giblin AE, Rastetter EB, Nadelhoffer KJ. Nitrogen dynamics in a small arctic watershed: Retention and downhill movement of15N. Ecol Monogr. 2010;80(2):331–51.

74. Paré MC, Bedard-Haughn A. Landscape-scale N mineralization and greenhouse gas emissions in Canadian Cryosols. Geoderma. 2012;189–190:469–79.

75. Simpson MJ, Simpson AJ. The Chemical Ecology of Soil Organic Matter Molecular Constituents. J Chem Ecol. 2012;38(6):768–84. doi: 10.1007/s10886-012-0122-x 22549555

76. Kögel-Knabner I. The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem. 2002;34:139–62.

77. Paré MC, Bedard-Haughn A. Soil organic matter quality influences mineralization and GHG emissions in cryosols: A field-based study of sub- to high Arctic. Glob Chang Biol. 2013;19(4):1126–40. doi: 10.1111/gcb.12125 23504890


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