Plant and Soil

, Volume 428, Issue 1–2, pp 279–290 | Cite as

Important interaction of chemicals, microbial biomass and dissolved substrates in the diel hysteresis loop of soil heterotrophic respiration

  • Qing Wang
  • Nianpeng He
  • Yuan Liu
  • Meiling Li
  • Li Xu
  • Xuhui Zhou
Regular Article


Background and aims

Increasing the emission of carbon dioxide by heterotrophic respiration (Rh) might lead to global warming. However, issues remain on how Rh responds to changing temperatures, especially with respect to the hysteresis loop in the relationship between Rh and temperature at the daily scale, along with elucidating the underlying mechanisms.


We investigated hysteresis loop by measuring Rh in subtropical forest soil at the daily scale (12 h for warm-up (6–30 °C) and cool-down processes (30–6 °C), respectively) using continuous temperature variation and high resolution of measurements over a 56-day incubation period. The ratios of R20 and Q10 between warm-up and cool-down were calculated as the characteristics of diel hysteresis. We measured chemical (pH, conductivity, oxidation-reduction potential), microbial biomass and dissolved substrate (carbon and nitrogen) parameters to explain variation of diel hysteresis.


Rh was strongly dependent on temperature, with a clockwise hysteresis loop of Rh between the warm-up and cool-down daily processes. The average value of R20 [at a reference temperature of 20 °C] during the whole incubation period under the warm-up process was significantly higher (46.05 ± 0.96 μgC g−1 d−1) than that under the cool-down process (14.74 ± 0.03 μgC g−1 d−1). In comparison, the average value of Q10 under the cool-down process (5.27 ± 0.2) was significantly higher than that under the warm-up process (1.66 ± 0.02). Redundancy analysis showed that the interaction effects of soil chemical, microbial biomass, and dissolved substrate parameters explain most variation of diel hysteresis: 98% variation in R20 and 93.5% variation in Q10. Compared with the weak effect of chemistry parameters on the diel hysteresis, the sole and interactive effects of microbial biomass and substrate were more important, especially their interaction.


Interactions of chemical, microbial biomass, and dissolved substrate parameters dominated the variation in diel hysteresis of Rh with temperature, especially the interaction of microbial biomass and dissolved substrate. Of note, Q10 during the warm-up process might be overestimated when using the highly fitted temperature-dependent function of cool-down period. Furthermore, using a constant value of Q10 (Q10 = 2) in carbon cycle models might be an important source of uncertainty.


Warm-up Cool-down Substrate Microbial biomass Heterotrophic respiration 



This work was partially supported by the National Key R&D Program of China (2016YFC0500102) and the National Natural Science Foundation of China (31770655, 41571130043). Nianpeng He contributes the conception and design; Qing Wang conducted the experiment and analyzes the data. All authors contributed to the final version. There are no conflicts of interest to declare. We thank the reviewers to improve the manuscript.

Supplementary material

11104_2018_3644_MOESM1_ESM.docx (914 kb)
ESM 1 (DOCX 914 kb)


  1. Balser TC, Wixon DL (2009) Investigating biological control over soil carbon temperature sensitivity. Glob Chang Biol 15:2935–2949CrossRefGoogle Scholar
  2. Barron-Gafford GA, Scott RL, Jenerette GD, Huxman TE (2011) The relative controls of temperature, soil moisture, and plant functional group on soil CO2 efflux at diel, seasonal, and annual scales. J Geophys Res Biogeo 116:G010223CrossRefGoogle Scholar
  3. Baumann A, Schimmack W, Steindl H, Bunzl K (1996) Association of fallout radiocesium with soil constituents: Effect of sterilization of forest soils by fumigation with chloroform. Radiat Environ Biophys 35:229–233CrossRefPubMedGoogle Scholar
  4. Bosatta E, Ågren GI (1999) Soil organic matter quality interpreted thermodynamically. Soil Biol Biochem 31:1889–1891CrossRefGoogle Scholar
  5. Bradford MA (2013) Thermal adaptation of decomposer communities in warming soils. Front Microbiol 4:333CrossRefPubMedPubMedCentralGoogle Scholar
  6. 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 11:1316–1327CrossRefPubMedGoogle Scholar
  7. Briones MJ, McNamara NP, Poskitt J, Crow SE, Ostle NJ (2014) Interactive biotic and abiotic regulators of soil carbon cycling: evidence from controlled climate experiments on peatland and boreal soils. Glob Chang Biol 20:2971–2982CrossRefPubMedGoogle Scholar
  8. Brookes PC, Kragt JF, Powlson DS, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: the effects of fumigation time and temperature. Soil Biol Biochem 17:831–835CrossRefGoogle Scholar
  9. Cheng L, Zhang NF, Yuan MT, Xiao J, Qin YJ, Deng Y, Tu QC, Xue K, Van Nostrand JD, Wu LY, He ZL, Zhou XH, Leigh MB, Konstantinidis KT, Schuur EAG, Luo YQ, Tiedje JM, Zhou JZ (2017) Warming enhances old organic carbon decomposition through altering functional microbial communities. ISME J 11:1825–1835CrossRefPubMedPubMedCentralGoogle Scholar
  10. Chi X, Tang Z, Xie Z, Guo Q, Zhang M, Ge J, Xiong G, Fang J (2015) Effects of size, neighbors, and site condition on tree growth in a subtropical evergreen and deciduous broad-leaved mixed forest, China. Ecol Evol 5:5149–5161CrossRefPubMedPubMedCentralGoogle Scholar
  11. Craine JM, Fierer N, McLauchlan KK (2010) Widespread coupling between the rate and temperature sensitivity of organic matter decay. Nat Geosci 3:854–857CrossRefGoogle Scholar
  12. Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173CrossRefPubMedGoogle Scholar
  13. De Bruijn AMG, Butterbach-Bahl K (2010) Linking carbon and nitrogen mineralization with microbial responses to substrate availability - the DECONIT model. Plant Soil 328:271–290CrossRefGoogle Scholar
  14. Ding JZ, Chen LY, Zhang BB, Liu L, Yang GB, Fang K, Chen YL, Li F, Kou D, Ji CJ, Luo YQ, Yang YH (2016) Linking temperature sensitivity of soil CO2 release to substrate, environmental, and microbial properties across alpine ecosystems. Global Biogeochem Cycles 30:1310–1323CrossRefGoogle Scholar
  15. Eberwein JR, Oikawa PY, Allsman LA, Jenerette GD (2015) Carbon availability regulates soil respiration response to nitrogen and temperature. Soil Biol Biochem 88:158–164CrossRefGoogle Scholar
  16. Fang C, Moncrieff JB (2001) The dependence of soil CO2 efflux on temperature. Soil Biol Biochem 33:155–165CrossRefGoogle Scholar
  17. Fierer N, Craine JM, McLauchlan K, Schimel JP (2005) Litter quality and the temperature sensitivity of decomposition. Ecology 86:320–326CrossRefGoogle Scholar
  18. Frey SD, Drijber R, Smith H, Melillo J (2008) Microbial biomass, functional capacity, and community structure after 12 years of soil warming. Soil Biol Biochem 40:2904–2907CrossRefGoogle Scholar
  19. Gaumont-Guay D, Black TA, Griffis TJ, Barr AG, Jassal RS, Nesic Z (2006) Interpreting the dependence of soil respiration on soil temperature and water content in a boreal aspen stand. Agric For Meteorol 140:220–235CrossRefGoogle Scholar
  20. Gershenson A, Bader NE, Cheng WX (2009) Effects of substrate availability on the temperature sensitivity of soil organic matter decomposition. Glob Chang Biol 15:176–183CrossRefGoogle Scholar
  21. Hall EK, Neuhauser C, Cotner JB (2008) Toward a mechanistic understanding of how natural bacterial communities respond to changes in temperature in aquatic ecosystems. Isme J 2:471–481CrossRefPubMedGoogle Scholar
  22. He NP, Wang RM, Gao Y, Dai JZ, Wen XF, Yu GR (2013) Changes in the temperature sensitivity of SOM decomposition with grassland succession: Implications for soil C sequestration. Ecol Evol 3:5045–5054CrossRefGoogle Scholar
  23. He NP, Liu CC, Tian M, Li ML, Yang H, Yu GR, Guo DL, Smith MD, Yu Q, Hou JH (2018) Variation in leaf anatomical traits from tropical to cold-temperate forests and linkage to ecosystem functions. Funct Ecol 32:10–19CrossRefGoogle Scholar
  24. Iqbal J, Hu RG, Feng ML, Lin S, Malghani S, Ali IM (2010) Microbial biomass, and dissolved organic carbon and nitrogen strongly affect soil respiration in different land uses: A case study at Three Gorges Reservoir Area, South China. Agric Ecosyst Environ 137:294–307CrossRefGoogle Scholar
  25. Ise T, Moorcroft PR (2006) The global-scale temperature and moisture dependencies of soil organic carbon decomposition: an analysis using a mechanistic decomposition model. Biogeochemistry 80:217–231CrossRefGoogle Scholar
  26. Jiang H, Deng Q, Zhou G, Hui D, Zhang D, Liu S, Chu G, Li J (2013) Responses of soil respiration and its temperature/moisture sensitivity to precipitation in three subtropical forests in southern China. Biogeosciences 10:3963–3982CrossRefGoogle Scholar
  27. Lefevre R, Barre P, Moyano FE, Christensen BT, Bardoux G, Eglin T, Girardin C, Houot S, Katterer T, van Oort F, Chenu C (2014) Higher temperature sensitivity for stable than for labile soil organic carbon-Evidence from incubations of long- term bare fallow soils. Glob Chang Biol 20:633–640CrossRefPubMedGoogle Scholar
  28. Lehmann J, Kleber M (2015) The contentious nature of soil organic matter. Nature 528:60–68CrossRefPubMedGoogle Scholar
  29. Li J, He NP, Xu L, Chai H, Liu Y, Wang DL, Wang L, Wei XH, Xue JY, Wen XF, Sun XM (2017) Asymmetric responses of soil heterotrophic respiration to rising and decreasing temperatures. Soil Biol Biochem 106:18–27CrossRefGoogle Scholar
  30. Liski J, Ilvesniemi H, Mäkelä A, Westman CJ (1999) CO2 emissions from soil in response to climatic warming are overestimated-The decomposition of old soil organic matter istolerant of temperature. Ambio 28:171–174Google Scholar
  31. Liu Q, Edwards NT, Post WM, Gu L, Ledford J, Lenhart S (2006) Temperature-independent diel variation in soil respiration observed from a temperate deciduous forest. Glob Chang Biol 12:2136–2145CrossRefGoogle Scholar
  32. Liu Y, He NP, Zhu JX, Xu L, Yu GR, Niu SL, Sun XM, Wen XF (2017) Regional variation in the temperature sensitivity of soil organic matter decomposition in China's forests and grasslands. Glob Chang Biol 23:3393–3402CrossRefPubMedGoogle Scholar
  33. Liu Y, He NP, Wen XF, Xu L, Sun XM, Yu GR, Liang LY, Schipper LA (2018) The optimum temperature of soil microbial respiration: Patterns and controls. Soil Biol Biochem 121:35–42CrossRefGoogle Scholar
  34. Lloyd J, Taylor JA (1994) On the temperature dependence of soil respiration. Funct Ecol 8:315–323CrossRefGoogle Scholar
  35. Malcolm GM, Lopez-Gutierrez JC, Koide RT, Eissenstat DM (2008) Acclimation to temperature and temperature sensitivity of metabolism by ectomycorrhizal fungi. Glob Chang Biol 14:1169–1180CrossRefGoogle Scholar
  36. Min K, Lehmeier CA, Ballantyne F, Tatarko A, Billings SA (2014) Differential effects of pH on temperature sensitivity of organic carbon and nitrogen decay. Soil Biol Biochem 76:193–200CrossRefGoogle Scholar
  37. Moren AS, Lindroth A (2000) CO2 exchange at the floor of a boreal forest. Agric For Meteorol 101:1–14CrossRefGoogle Scholar
  38. Nakai Y, Kitamura K, Suzuki S, Abe S (2003) Year-long carbon dioxide exchange above a broadleaf deciduous forest in Sapporo, Northern Japan. Tellus Ser B Chem Phys Meteorol 55:305–312CrossRefGoogle Scholar
  39. Niu SL, Luo YQ, Fei SF, Montagnani L, Bohrer G, Janssens IA, Gielen B, Rambal S, Moors E, Matteucci G (2011) Seasonal hysteresis of net ecosystem exchange in response to temperature change: patterns and causes. Glob Chang Biol 17:3102–3114CrossRefGoogle Scholar
  40. Phillips CL, Nickerson N, Risk D, Bond BJ (2011) Interpreting diel hysteresis between soil respiration and temperature. Glob Chang Biol 17:515–527CrossRefGoogle Scholar
  41. Riveros-Iregui DA, Emanuel RE, Muth DJ, McGlynn BL, Epstein HE, Welsch DL, Pacific VJ, Wraith JM (2007) Diurnal hysteresis between soil CO2 and soil temperature is controlled by soil water content. Geophys Res Lett:34Google Scholar
  42. Rousk J, Baath E (2011) Growth of saprotrophic fungi and bacteria in soil. Fems Microbiol Ecol 78:17–30Google Scholar
  43. Rousk J, Frey SD, Bååth E (2012) Temperature adaptation of bacterial communities in experimentally warmed forest soils. Glob Chang Biol 18:3252–3258CrossRefPubMedGoogle Scholar
  44. Rovira P, Jorba M, Romanya J (2010) Active and passive organic matter fractions in Mediterranean forest soils. Biol Fert Soils 46:355-369.Rousk J, Bååth E (2011) Growth of saprotrophic fungi and bacteria in soil. FEMS Microbiol Ecol 78:17–30Google Scholar
  45. Ruehr NK, Knohl A, Buchmann N (2010) Environmental variables controlling soil respiration on diurnal, seasonal and annual time-scales in a mixed mountain forest in Switzerland. Biogeochemistry 98:153–170CrossRefGoogle Scholar
  46. Shen C, Xiong J, Zhang H, Feng Y, Lin X, Li X, Liang W, Chu H (2013) Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol Biochem 57:204–211CrossRefGoogle Scholar
  47. Shibata H, Hiura T, Tanaka Y, Takagi K, Koike T (2005) Carbon cycling and budget in a forested basin of southwestern Hokkaido, northern Japan. Ecol Res 20:325–331CrossRefGoogle Scholar
  48. Sierra CA, Trumbore SE, Davidson EA, Frey SD, Savage KE, Hopkins FM (2012) Predicting decadal trends and transient responses of radiocarbon storage and fluxes in a temperate forest soil. Biogeosciences 9:3013–3028CrossRefGoogle Scholar
  49. Song XL, Zhu JX, He NP, Huang JH, Tian J, Zhao X, Liu Y, Wang CH (2017) Asynchronous pulse responses of soil carbon and nitrogen mineralization to rewetting events at a short-term: Regulation by microbes. Sci Rep 7:7492CrossRefPubMedPubMedCentralGoogle Scholar
  50. Subke JA, Bahn M (2010) On the 'temperature sensitivity' of soil respiration: Can we use the immeasurable to predict the unknown? Soil Biol Biochem 42:1653–1656CrossRefPubMedPubMedCentralGoogle Scholar
  51. ter Braak CJF, Smilauer P (2012) Canoco reference manual and user's guide: software for ordination, version 5.0. Ithaca USA: Microcomputer Power, 2012Google Scholar
  52. von Lutzow M, Kogel-Knabner I, Ekschmitt K, Matzner E, Guggenberger G, Marschner B, Flessa H (2006) Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions - a review. Eur J Soil Sci 57:426–445CrossRefGoogle Scholar
  53. Wagai R, Kishimoto-Mo AW, Yonemura S, Shirato Y, Hiradate S, Yagasaki Y (2013) Linking temperature sensitivity of soil organic matter decomposition to its molecular structure, accessibility, and microbial physiology. Glob Chang Biol 19:1114–1125CrossRefPubMedGoogle Scholar
  54. Wang Q, Wang D, Wen XF, Yu GR, He NP, Wang RF (2015) Differences in SOM decomposition and temperature sensitivity among soil aggregate size classes in a temperate grasslands. PLoS One 10:e0117033CrossRefPubMedPubMedCentralGoogle Scholar
  55. Wang Q, He NP, Liu Y, Li ML, Xu L (2016a) Strong pulse effects of precipitation events on soil microbial respiration in temperate forests. Geoderma 275:67–73CrossRefGoogle Scholar
  56. Wang Q, He NP, Yu GR, Gao Y, Wen XF, Wang RF, Koerner SE, Yu Q (2016b) Soil microbial respiration rate and temperature sensitivity along a North-South forest transect in eastern China: Patterns and influencing factors. J Geophys Res Biogeo 121:399–410CrossRefGoogle Scholar
  57. Wei H, Guenet B, Vicca S, Nunan N, AbdElgawad H, Pouteau V, Shen WJ, Janssens IA (2014) Thermal acclimation of organic matter decomposition in an artificial forest soil is related to shifts in microbial community structure. Soil Biol Biochem 71:1–12CrossRefGoogle Scholar
  58. Wetterstedt JAM, Persson T, Ågren GI (2010) Temperature sensitivity and substrate quality in soil organic matter decomposition: results of an incubation study with three substrates. Glob Chang Biol 16:1806–1819CrossRefGoogle Scholar
  59. Xu X, Luo YQ, Zhou JZ (2012) Carbon quality and the temperature sensitivity of soil organic carbon decomposition in a tallgrass prairie. Soil Biol Biochem 50:142–148CrossRefGoogle Scholar
  60. Xu ZW, Yu GR, Zhang XY, He NP, Wang QF, Wang SZ, Wang RL, Zhao N, Jia YL, Wang CY (2017) Soil enzyme activity and stoichiometry in forest ecosystems along the North-South Transect in eastern China (NSTEC). Soil Biol Biochem 104:152–163CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Ecological and Environmental ScienceEast China Normal UniversityShanghaiChina
  2. 2.Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources ResearchChinese Academy of SciencesBeijingChina
  3. 3.College of Resources and EnvironmentUniversity of Chinese Academy of SciencesBeijingChina
  4. 4.Institute of Grassland Science, Northeast Normal University, and Key Laboratory of Vegetation Ecology, Ministry of EducationChangchunChina

Personalised recommendations