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Drought differentially affects autotrophic and heterotrophic soil respiration rates and their temperature sensitivity

  • Shouqin Sun
  • Haiqing Lei
  • Scott X. ChangEmail author
Original Paper
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Abstract

Climate change predictions indicate that extreme drought is likely to become more frequent in the future. In this study, the impact of drought on soil respiration (Rs) and its autotrophic (Ra) and heterotrophic components (Rh) were studied in a cultivated Black Chernozemic soil in central Alberta, Canada. The mean Rs was 24.4% lower in the drought relative to the plots with ambient precipitation (P < 0.001), with a larger decrease in Ra (26.8%) relative to Rh (21.0%), and a higher (P < 0.05) contribution of Rh to Rs under drought (52.8%) than under the ambient condition (47.7%). Both Rs and its Ra and Rh components had an exponential relationship with soil temperature and a quadratic relationship with soil water content. Drought caused a greater decrease in the tipping point of soil water content for Rh (a 39.6% reduction) than for Ra (a 15.1% reduction) relative to the ambient precipitation treatment. In addition, drought resulted in a greater increase in the temperature sensitivity (Q10 values) of Ra (a 45.0% increase) than that of Rh (a 14.1% increase) relative to the ambient precipitation treatment. The results suggest that drought amplified the water limitation effect on CO2 emission, especially that from microbial respiration, and resulted in a tighter relationship between temperature and root or autotrophic respiration, based on this 1-year study. We conclude that it is important to assess the impact of drought on soil respiration components rather than the total soil respiration, and such differential effects of drought on soil respiration components should be incorporated into global carbon circulation models.

Keywords

Autotrophic respiration Drought Heterotrophic respiration Soil respiration Soil water content tipping point Temperature sensitivity of soil respiration (Q10) 
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Notes

Acknowledgments

We would like to thank Zheng Shi for technical assistance and invaluable contributions in the laboratory and field.

References

  1. Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci 8:343–351CrossRefGoogle Scholar
  2. Austin AT, Yahdjian L, Stark JM, Belnap J, Porporato A, Norton U, Ravetta DA, Schaeffer SM (2004) Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141:221–235CrossRefGoogle Scholar
  3. Balogh J, Papp M, Pintér K, Fóti S, Posta K, Eugster W, Nagy Z (2016) Autotrophic component of soil respiration is repressed by drought more than the heterotrophic one in dry grasslands. Biogeosciences 13:5171–5182CrossRefGoogle Scholar
  4. Boone RD, Nadelhoffer KJ, Canary JD, Kaye JP (1998) Roots exert a strong influence on the temperature sensitivity of soil respiration. Nature 36:570–572CrossRefGoogle Scholar
  5. Borken W, Savage K, Davidson EA, Trumbore SE (2006) Effects of experimental drought on soil respiration and radiocarbon efflux from a temperate forest soil. Glob Chang Biol 12:177–193CrossRefGoogle Scholar
  6. Carbone MS, Still CJ, Ambrose AR, Dawson TE, Williams AP, Boot CM, Schaeffer SM, Schimel JP (2011) Seasonal and episodic moisture controls on plant and microbial contributions to soil respiration. Oecologia 167:265–278CrossRefGoogle Scholar
  7. Casals P, Lopez-Sangil L, Carrara A, Gimeno C, Nogués S (2011) Autotrophic and heterotrophic contributions to short-term soil CO2 efflux following simulated summer precipitation pulses in a Mediterranean dehesa. Glob Biogeochem Cycles 25:GB3012CrossRefGoogle Scholar
  8. Cattanio JH, Davidson EA, Nepstad DC, Verchot LV, Ackerman IL (2002) Unexpected results of a pilot throughfall exclusion experiment on soil emissions of CO2, CH4, N2O, and NO in eastern Amazonia. Biol Fertil Soils 36:102–108CrossRefGoogle Scholar
  9. Chen S, Zhang X, Liu Y, Hu Z, Shen X, Ren J (2015) Simulated acid rain changed the proportion of heterotrophic respiration in soil respiration in a subtropical secondary forest. Appl Soil Ecol 86:148–157CrossRefGoogle Scholar
  10. Craine JM, Gelderman TM (2011) Soil moisture controls on temperature sensitivity of soil organic carbon decomposition for a mesic grassland. Soil Biol Biochem 43:455–457CrossRefGoogle Scholar
  11. Curiel yuste J, Janssens IA, Carrara A, Ceulemans R (2004) Annual Q 10 of soil respiration reflects plant phenological patterns as well as temperature sensitivity. Glob Chang Biol 10:161–169CrossRefGoogle Scholar
  12. Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173CrossRefGoogle Scholar
  13. Davidson EA, Ishida FY, Nepstad DC (2004) Effects of an experimental drought on soil emissions of carbon dioxide, methane, nitrous oxide, and nitric oxide in a moist tropical forest. Glob Chang Biol 10:718–730CrossRefGoogle Scholar
  14. Deslippe JR, Hartmann M, Grayston SJ, Simard SW, Mohn WW (2016) Stable isotope probing implicates a species of Cortinarius in carbon transfer through ectomycorrhizal fungal mycelial networks in Arctic tundra. New Phytol 210:383–390CrossRefGoogle Scholar
  15. Epron D (2009) Separating autotrophic and heterotrophic components of soil respiration: lessons learned from trenching and related root exclusion experiments. In: Bahn M, Heinemeyer A, Kutsch W (eds) Soil carbon dynamics: an integrated methodology. Cambridge University Press, Cambridge, pp 289–310Google Scholar
  16. Freeman C, Liska G, Ostle NJ, Lock MA, Reynolds B, Hudson J (1996) Microbial activity and enzymatic decomposition processes following peatland water table drawdown. Plant Soil 180:121–127CrossRefGoogle Scholar
  17. Garten CT, Classen AT, Norby RJ (2009) Soil moisture surpasses elevated CO2 and temperature as a control on soil carbon dynamics in a multi-factor climate change experiment. Plant Soil 319:85–94CrossRefGoogle Scholar
  18. Gomez-Casanovas N, Matamala R, Cook DR, Gonzalez-Meler MA (2012) Net ecosystem exchange modifies the relationship between the autotrophic and heterotrophic components of soil respiration with abiotic factors in prairie grasslands. Glob Chang Biol 18:2532–2545CrossRefGoogle Scholar
  19. Hanson PJ, Edwards NT, Garten CT, Andrews JA (2000) Separating root and soil microbial contributions to soil respiration: a review of methods and observations. Biogeochemistry 48:115–146CrossRefGoogle Scholar
  20. Harper CW, Blair JM, Fay PA, Knapp AK, Carlisle JD (2005) Increased rainfall variability and reduced rainfall amount decreases soil CO2 flux in a grassland ecosystem. Glob Chang Biol 11:322–334CrossRefGoogle Scholar
  21. Hinko-Najera N, Fest B, Livesley SJ, Arndt SK (2015) Reduced throughfall decreases autotrophic respiration, but not heterotrophic respiration in a dry temperate broadleaved evergreen forest. Agric For Meteorol 200:66–77CrossRefGoogle Scholar
  22. Huang S, Ye G, Lin J, Chen K, Xu X, Ruan H, Tan F, Chen HYH (2018) Autotrophic and heterotrophic soil respiration responds asymmetrically to drought in a subtropical forest in the Southeast China. Soil Biol Biochem 123:242–249CrossRefGoogle Scholar
  23. Inglima I, Alberti G, Bertolini T, Vaccari FP, Gioli B, Miglietta F, Cotrufo MF, Peressotti A (2010) Precipitation pulses enhance respiration of Mediterranean ecosystems: the balance between organic and inorganic components of increased soil CO2 efflux. Glob Chang Biol 15:1289–1301CrossRefGoogle Scholar
  24. IPCC (2013) The physical science basis. Contribution of working group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, CambridgeGoogle Scholar
  25. Jassal RS, Black TA (2006) Estimating heterotrophic and autotrophic soil respiration using small-area trenched plot technique: theory and practice. Agric For Meteorol 140:193–202CrossRefGoogle Scholar
  26. Jassal RS, Black TA, Novak MD, Gaumont-Guay D, Nesic Z (2008) Effect of soil water stress on soil respiration and its temperature sensitivity in an 18-year-old temperate Douglas-fir stand. Glob Chang Biol 14:1305–1318CrossRefGoogle Scholar
  27. Jensen KD, Beier C, Michelsen A, Emmett BA (2003) Effects of experimental drought on microbial processes in two temperate heathlands at contrasting water conditions. Appl Soil Ecol 24:165–176CrossRefGoogle Scholar
  28. Johnson D, Leake JR, Read DJ (2002) Transfer of recent photosynthate into mycorrhizal mycelium of an upland grassland: short-term respiratory losses and accumulation of C-14. Soil Biol Biochem 34:1521–1524CrossRefGoogle Scholar
  29. Knapp AK, Smith MD (2001) Variation among biomes in temporal dynamics of aboveground primary production. Science 291:481–484CrossRefGoogle Scholar
  30. Kuzyakov Y (2002) Review: factors affecting rhizosphere priming effects. J Plant Nutr Soil Sci 165:421–431CrossRefGoogle Scholar
  31. Kuzyakov Y (2006) Sources of CO2 efflux from soil and review of partitioning methods. Soil Biol Biochem 38:425–448CrossRefGoogle Scholar
  32. Lal R (2004) Soil carbon sequestration to mitigate climate change. Geoderma 123:1–22CrossRefGoogle Scholar
  33. Lang R, Blagodatsky S, Xu J, Cadisch G (2017) Seasonal differences in soil respiration and methane uptake in rubber plantation and rainforest. Agric Ecosyst Environ 240:314–328CrossRefGoogle Scholar
  34. Lei L, Xiao W, Zeng L, Zhu J, Huang Z, Cheng R, Gao S, Li MH (2017) Thinning but not understory removal increased heterotrophic respiration and total soil respiration in Pinus massoniana stands. Sci Total Environ 621:1360–1369CrossRefGoogle Scholar
  35. Linn DM, Doran JW (1984) Effect of water-filled pore-space on carbon-dioxide and nitrous-oxide production in tilled and nontilled soils. Soil Sci Soc Am J 48:1267–1272CrossRefGoogle Scholar
  36. Manzoni S, Schimel JP, Porporato A (2012) Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology 93:930–938CrossRefGoogle Scholar
  37. Marella VSSR, Roberts P, Hill PW, Jones DL (2017) Different ways in which CO2 can be released during the turnover of roots in soil. Biol Fertil Soils 53:369–374CrossRefGoogle Scholar
  38. Mbogga MS, Hamann A, Wang T (2009) Historical and projected climate data for natural resource management in western Canada. Agric For Meteorol 149:881–890CrossRefGoogle Scholar
  39. Moyano FE, Kutsch WL, Schulze E (2007) Response of mycorrhizal, rhizosphere and soil basal respiration to temperature and photosynthesis in a barley field. Soil Biol Biochem 39:843–853CrossRefGoogle Scholar
  40. Muhr J, Borken W (2009) Delayed recovery of soil respiration after wetting of dry soil further reduces C losses from a Norway spruce forest soil. J Geophys Res 114:G04023CrossRefGoogle Scholar
  41. Nikolova PS, Raspe S, Andersen CP, Mainiero R, Blaschke H, Matyssek R, Häberle K (2009) Effects of the extreme drought in 2003 on soil respiration in a mixed forest. Eur J For Res 128:87–98CrossRefGoogle Scholar
  42. Peng F, You QG, Xu MH, Zhou XH, Wang T, Guo J, Xue X (2015) Effects of experimental warming on soil respiration and its components in an alpine meadow in the permafrost region of the Qinghai-Tibet Plateau. Eur J Soil Sci 66:145–154CrossRefGoogle Scholar
  43. Prudhomme C, Giuntoli I, Robinson EL, Clark DB, Arnell NW, Dankers R, Fekete BM, Franssen W, Gerten D, Gosling SN, Hagemann S, Hannah DM, Kim H, Masaki Y, Satoh Y, Stacke T, Wada Y, Wisser D (2014) Hydrological droughts in the 21st century, hotspots and uncertainties from a global multimodel ensemble experiment. PNAS 111:3262–3267CrossRefGoogle Scholar
  44. Raich JW, Schlesinger WH (1992) The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus 44B:81–99CrossRefGoogle Scholar
  45. Raich JW, Tufekciogul A (2000) Vegetation and soil respiration: correlations and controls. Biogeochem 48:71–90CrossRefGoogle Scholar
  46. Raich JW, Potter CS, Bhagawati D (2002) Interannual variability in global soil respiration, 1980–1994. Glob Chang Biol 8:800–812CrossRefGoogle Scholar
  47. Reichstein M, Bahn M, Ciais P, Frank D, Mahecha MD, Seneviratne SI, Zscheischler J, Beer C, Buchmann N, Frank DC, Papale D, Rammig A, Smith P, Thonicke K, van der Velde M, Vicca S, Walz A, Wattenbach M (2013) Climate extremes and the carbon cycle. Nature 500:287–295CrossRefGoogle Scholar
  48. Saiz G, Byrne KA, Butterbach-Bahl K, Kiese R, Blujdeas V, Farrell EP (2006) Stand age-related effects on soil respiration in a first rotation Sitka spruce chronosequence in central Ireland. Glob Chang Biol 12:1007–1020CrossRefGoogle Scholar
  49. Sakamoto K, Oba Y (1994) Effect of fungal to bacterial biomass ratio on the relationship between CO2 evolution and total soil microbial biomass. Biol Fertil Soils 17:39–44CrossRefGoogle Scholar
  50. Savage KE, Davidson EA (2001) Interannual variation of soil respiration in two New England forests. Glob Biogeochem Cycles 15:337–350CrossRefGoogle Scholar
  51. Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394CrossRefGoogle Scholar
  52. Schindlbacher A, Zechmeister-Boltenstern S, Jandl R (2009) Carbon losses due to soil warming: do autotrophic and heterotrophic soil respiration respond equally? Glob Chang Biol 15:901–913CrossRefGoogle Scholar
  53. Schindler DW, Donahue WF (2006) An impending water crisis in Canada’s western prairie provinces. PNAS 103:7210–7216CrossRefGoogle Scholar
  54. Scott-Denton LE, Rosenstiel TN, Monson RK (2006) Differential controls by climate and substrate over the heterotrophic and rhizospheric components of soil respiration. Glob Chang Biol 12:205–216CrossRefGoogle Scholar
  55. Selsted MB, Linden L, Ibrom A, Michelsen A, Larsen KS, Pedersen JK, Mikkelsen TN, Pilegaard K, Beier C, Ambus P (2012) Soil respiration is stimulated by elevated CO2 and reduced by summer drought: three years of measurements in a multifactor ecosystem manipulation experiment in a temperate heathland (CLIMAITE). Glob Chang Biol 18:1216–1230CrossRefGoogle Scholar
  56. Shahbaz M, Kuzyakov Y, Sanaullah M, Heitkamp F, Zelenev V, Kumar A, Blagodatskaya E (2017) Microbial decomposition of soil organic matter is mediated by quality and quantity of crop residues: mechanisms and thresholds. Biol Fertil Soils 53:287–301CrossRefGoogle Scholar
  57. Shi WY, Tateno R, Zhang JG, Wang YL, Yamanaka N, Du S (2011) Response of soil respiration to precipitation during the dry season in two typical forest stands in the forest-grassland transition zone of the Loess Plateau. Agric For Meteorol 151:854–863CrossRefGoogle Scholar
  58. Soil Classification Working Group (1998) The Canadian system of soil classification, 3rd edn. NRC Research Press, Ottawa, p 187Google Scholar
  59. Sotta ED, Veldkamp E, Schwendenmann L, Guimaraes BR, Paixao RK, Ruivo M, Da Costa ACL, Meir P (2007) Effects of an induced drought on soil carbon dioxide (CO2) efflux and soil CO2 production in an Eastern Amazonian rainforest, Brazil. Glob Chang Biol 13:2218–2229CrossRefGoogle Scholar
  60. Sowerby A, Emmett B, Beier C, Tietema A, Peñuelas J, Estiarte M, Van Meeteren MJM, Hughes S, Freeman C (2005) Microbial community changes in heathland soil communities along a geographical gradient: interaction with climate change manipulations. Soil Biol Biochem 37:1805–1813CrossRefGoogle Scholar
  61. Sowerby A, Emmett BA, Tietema A, Claus B (2008) Contrasting effects of repeated summer drought on soil carbon efflux in hydric and mesic heathland soils. Glob Chang Biol 14:2388–2404CrossRefGoogle Scholar
  62. Subke J, Inglima I, Francesca Cotrufo M (2006) Trends and methodological impacts in soil CO2 efflux partitioning: a meta-analytical review. Glob Chang Biol 12:921–943CrossRefGoogle Scholar
  63. Sulzman EW, Brant JB, Bowden RD, Laijtha K (2005) Contribution of aboveground litter, belowground litter, and rhizosphere respiration to total soil CO2 efflux in an old growth coniferous forest. Biogeochem 73:231–256CrossRefGoogle Scholar
  64. Sun SQ, Bhatti JS, Jassal RS, Chang SX, Arevalo C, Black TA, Sidders D (2015) Stand age and soil productivity control soil CO2 efflux and soil organic carbon dynamics in hybrid poplar plantations. Soil Sci Soc Am J 79:1638–1649CrossRefGoogle Scholar
  65. Suseela V, Conant RT, Wallenstein MD, Dukes JS (2012) Effects of soil moisture on the temperature sensitivity of heterotrophic respiration vary seasonally in an old-field climate change experiment. Glob Chang Biol 18:336–348CrossRefGoogle Scholar
  66. Trumbore S (2006) Carbon respired by terrestrial ecosystems: recent progress and challenges. Glob Chang Biol 12:141–153CrossRefGoogle Scholar
  67. UKIUSS Working Group WRB (1998) World reference base for soil resources. World Soil Resources Reports 84. ISSS, FAO, ISRIC, RomeGoogle Scholar
  68. van der Molen MK, Dolman AJ, Ciais P, Eglin T, Gobron N, Law BE, Meir P, Peters W, Phillips OL, Reichstein M, Chen T, Dekker SC, Doubková M, Friedl MA, Jung M, van den Hurk BJJM, de Jeu RAM, Kruijt B, Ohta T, Rebel KT, Plummer S, Seneviratne SI, Sitch S, Teuling AJ, van der Werf GR, Wang G (2011) Drought and ecosystem carbon cycling. Agric For Meteorol 151:765–773CrossRefGoogle Scholar
  69. Wang Y, Hao Y, Cui X, Zhao H, Xu C, Zhou Z, Xu Z (2014) Responses of soil respiration and its components to drought stress. J Soils Sediments 14:99–109CrossRefGoogle Scholar
  70. Wood TE, Detto M, Silver WL (2013) Sensitivity of soil respiration to variability in soil moisture and temperature in a humid tropical forest. PLoS One 8:7Google Scholar
  71. Xu X, Shi Z, Li D, Zhou X, Sherry RA, Luo Y (2015) Plant community structure regulates responses of prairie soil respiration to decadal experimental warming. Glob Chang Biol 21:3846–3853CrossRefGoogle Scholar
  72. Yahdjian L, Sala OE (2002) A rainout shelter design for intercepting different amounts of rainfall. Oecologia 133:95–101CrossRefGoogle Scholar
  73. Zhang Q, Zak JC (1998) Effects of water and nitrogen amendment on soil microbial biomass and fine root production in a semi-arid environment in West Texas. Soil Biol Biochem 30:39–45CrossRefGoogle Scholar
  74. Zhang C, Niu D, Hall SJ, Wen H, Lia X, Fu H, Wan C, Elser JJ (2014) Effects of simulated nitrogen deposition on soil respiration components and their temperature sensitivities in a semiarid grassland. Soil Biol Biochem 75:113–123CrossRefGoogle Scholar
  75. Zhang X, Zhang Y, Sha L, Wu C, Tan Z, Song Q, Liu Y, Dong L (2015) Effects of continuous drought stress on soil respiration in a tropical rainforest in southwest China. Plant Soil 394:343–353CrossRefGoogle Scholar
  76. Zhang L, Xiao J, Zhou Y, Zheng Y, Li J, Xiao H (2016) Drought events and their effects on vegetation productivity in China. Ecosphere 7:e01591CrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Mountain Surface Processes and Ecological Regulation, Institute of Mountain Hazards and EnvironmentChinese Academy of SciencesChengduChina
  2. 2.Department of Renewable ResourcesUniversity of AlbertaEdmontonCanada
  3. 3.Zhejiang Subtropical Crop Research InstituteWenzhouChina
  4. 4.State Key Laboratory of Subtropical SilvicultureZhejiang A & F UniversityHangzhouChina

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