, Volume 20, Issue 4, pp 796–812 | Cite as

Inter-annual Variability of Soil Respiration in Wet Shrublands: Do Plants Modulate Its Sensitivity to Climate?

  • María T. Domínguez
  • Andrew R. Smith
  • Sabine Reinsch
  • Bridget A. Emmett


Understanding the response of soil respiration to climate variability is critical to formulate realistic predictions of future carbon (C) fluxes under different climate change scenarios. There is growing evidence that the influence of long-term climate variability in C fluxes from terrestrial ecosystems is modulated by adjustments in the aboveground–belowground links. Here, we studied the inter-annual variability in soil respiration from a wet shrubland going through successional change in North Wales (UK) during 13 years. We hypothesised that the decline in plant productivity observed over a decade would result in a decrease in the apparent sensitivity of soil respiration to soil temperature, and that rainfall variability would explain a significant fraction of the inter-annual variability in plant productivity, and consequently, in soil respiration, due to excess-water constraining nutrient availability for plants. As hypothesised, there were parallel decreases between plant productivity and annual and summer CO2 emissions over the 13-year period. Soil temperatures did not follow a similar trend, which resulted in a decline in the apparent sensitivity of soil respiration to soil temperature (apparent Q10 values decreased from 9.4 to 2.8). Contrary to our second hypothesis, summer maximum air temperature rather than rainfall was the climate variable with the greatest influence on aboveground biomass and annual cumulative respiration. Since summer air temperature and rainfall were positively associated, the greatest annual respiration values were recorded during years of high rainfall. The results suggest that adjustments in plant productivity might have a critical role in determining the long-term-sensitivity of soil respiration to changing climate conditions.


plant productivity Q10 soil C climate change drought heathland Calluna vulgaris 

Supplementary material

10021_2016_62_MOESM1_ESM.docx (23 kb)
Supplementary material 1 (DOCX 23 kb)


  1. Aanderud ZT, Schoolmaster DR Jr, Lennon JT. 2011. Plants mediate the sensitivity of soil respiration to rainfall variability. Ecosystems 14:156–67.CrossRefGoogle Scholar
  2. Bader NE, Cheng W. 2007. Rhizosphere priming effect of Populus fremontii obscures the temperature sensitivity of soil organic carbon respiration. Soil Biol Biochem 39:600–6.CrossRefGoogle Scholar
  3. Beier C, Emmett B, Gundersen P, Tietema A, Peñuelas J, Estiarte M, Gordon C, Gorissen A, Llorens L, Roda F, Williams D. 2004. Novel approaches to study climate change effects on terrestrial ecosystems in the field: drought and passive nighttime warming. Ecosystems 7:583–97.CrossRefGoogle Scholar
  4. Beier C, Emmett BA, Tietema A, Schmidt IK, Peñuelas J, Láng EK, Duce P, De Angelis P, Gorissen A, Estiarte M, de Dato GD, Sowerby A, Kröel-Dulay G, Lellei-Kovács E, Kull O, Mand P, Petersen H, Gjelstrup P, Spano D. 2009. Carbon and nitrogen balances for six shrublands across Europe. Global Biogeochemical Cycles 23.Google Scholar
  5. Bond-Lamberty B, Thomson A. 2010. Temperature-associated increases in the global soil respiration record. Nature 464:579–82.CrossRefPubMedGoogle Scholar
  6. Ciais P, Reichstein M, Viovy N, Granier A, Ogee J, Allard V, Aubinet M, Buchmann N, Bernhofer C, Carrara A, Chevallier F, De Noblet N, Friend AD, Friedlingstein P, Grunwald T, Heinesch B, Keronen P, Knohl A, Krinner G, Loustau D, Manca G, Matteucci G, Miglietta F, Ourcival JM, Papale D, Pilegaard K, Rambal S, Seufert G, Soussana JF, Sanz MJ, Schulze ED, Vesala T, Valentini R. 2005. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437:529–33.CrossRefPubMedGoogle Scholar
  7. Cranfield University. 2014. The Soils Guide. Available: Cranfield University, UK. ( Accessed on 18 November 2014.
  8. Curiel-Yuste J, Janssens IA, Carrara A, Ceulemans R. 2004. Annual Q10 of soil respiration reflects plant phenological patterns as well as temperature sensitivity. Glob Change Biol 10:161–9.CrossRefGoogle Scholar
  9. Curiel-Yuste J, Ma S, Baldocci DD. 2010. Plant-soil interactions and acclimation to temperature of microbial-mediated soil respiration may affect predictions of soil CO2 efflux. Biogeochemistry 98:38–127.CrossRefGoogle Scholar
  10. Davidson EA, Holbrook NM. 2009. Is temporal variation of soil respiration linked to the phenology of photosynthesis? In: Noormets A, Ed. Phenology of ecosystem processes-applications in global change research. New York: Springer. p 187–99.CrossRefGoogle Scholar
  11. Davidson EA, Janssens IA. 2006. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–73.CrossRefPubMedGoogle Scholar
  12. Delpierre N, Soudani K, François C, Le Maire G, Bernhofer C, Kutsch W, Misson L, Rambal S, Vesala T, Dufrêne E. 2012. Quantifying the influence of climate and biological drivers on the interannual variability of carbon exchanges in European forests through process-based modelling. Agric For Meteorol 154–155:99–112.CrossRefGoogle Scholar
  13. Domínguez MT, Sowerby A, Smith A, Robinson D, Van Baarsel S, Mills RE, Marshall M, Koller E, Lebron I, Hall J, Emmett B. 2015. Sustained impact of drought on wet shrublands mediated by soil physical changes. Biogeochemistry 122:151–63.CrossRefGoogle Scholar
  14. Dijkstra FA, Cheng W. 2007. Interactions between soil and tree roots accelerate long-term soil carbon decomposition. Ecol Lett 10:1046–53.CrossRefPubMedGoogle Scholar
  15. Emmett BA, Beier C, Estiarte M, Tietema A, Kristensen HL, Williams D, Peñuelas J, Schmidt I, Sowerby A. 2004. The response of soil processes to climate change: results from manipulation studies of shrublands across an environmental gradient. Ecosystems 7:625–37.CrossRefGoogle Scholar
  16. Epron D, Nouvellon Y, Roupsard O, Mouvondy W, Mabiala A, Saint-André L, Joffre R, Jourdan C, Bonnefond J-M, Berbigier P, Hamel O. 2004. Spatial and temporal variations of soil respiration in a Eucalyptus plantation in Congo. For Ecol Manag 202:149–60.CrossRefGoogle Scholar
  17. Freeman C, Ostle N, Kang H. 2001. An enzymic ‘latch’ on a global carbon store. Nature 409:149.CrossRefPubMedGoogle Scholar
  18. Fenner N, Freeman C. 2011. Drought-induced carbon loss in peatlands. Nature Geosci 4:895–900.CrossRefGoogle Scholar
  19. Fierer N, Colman BP, Schimel JP, Jackson RB. 2006. Predicting the temperature dependence of microbial respiration in soil: A continental-scale analysis. Glob Biogeochem Cycles 20:GB3026.CrossRefGoogle Scholar
  20. Fontaine S, Barot S, Barre P, Bdioui N, Mary B, Rumpel C. 2007. Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450:277–80.CrossRefPubMedGoogle Scholar
  21. Gimingham CH. 1972. Ecology of heathlands. London: Chapman Hall.Google Scholar
  22. Hall J, Curti C, Dore T, Smith R. 2014. Methods for the calculation of critical loads and their exceedances in the UK, draft report to UK Department of Environment and Rural Affairs-DEFRA. Accessed 7 September 2015.
  23. Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Lofvenius M, Read DJ. 2001. Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–92.CrossRefPubMedGoogle Scholar
  24. Irvine J, Law BE, Martin JG, Vickers D. 2008. Interannual variation in soil CO2 efflux and the response of root respiration to climate and canopy gas exchange in mature ponderosa pine. Glob Change Biol 14:2848–59.CrossRefGoogle Scholar
  25. Ise T, Dunn AL, Wofsy SC, Moorcroft PR. 2008. High sensitivity of peat decomposition to climate change through water-table feedback. Nat Geosci 1:763–6.CrossRefGoogle Scholar
  26. Janssens IA, Lankreijer H, Matteucci G, Kowalski AS, Buchmann N, Epron D, Pilegaard K, Kutsch W, Longdoz B, Grünwald T, Montagnani L, Dore S, Rebmann C, Moors EJ, Grelle A, Rannik Ü, Morgenstern K, Oltchev S, Clement R, Guðmundsson J, Minerbi S, Berbigier P, Ibrom A, Moncrieff J, Aubinet M, Bernhofer C, Jensen NO, Vesala T, Granier A, Schulze E-D, Lindroth A, Dolman AJ, Jarvis PG, Ceulemans R, Valentini R. 2001. Productivity overshadows temperature in determining soil and ecosystem respiration across European forests. Glob Change Biol 7:269–78.CrossRefGoogle Scholar
  27. Jia X, Zhou X, Luo Y, Xue K, Xue X, Xu X, Yang Y, Wu L, Zhou J. 2014. Effects of substrate addition on soil respiratory carbon release under long-term warming and clipping in a tallgrass prairie. PLoS ONE 9:e114203.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Jing Y, Guan D, Wu J, Wang A, Jin C, Yuan F. 2015. An experimental comparison of two methods on photosynthesis driving soil respiration: girdling and defoliation. PLoS ONE 10:e0132649.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Jones PD, Jonsson T, Wheeler D. 1997. Extension to the North Atlantic oscillation using early instrumental pressure observations from Gibraltar and south-west Iceland. Int J Climatol 17:1433–50.CrossRefGoogle Scholar
  30. Kirschbaum MUF. 2004. Soil respiration under prolonged soil warming: are rate reductions caused by acclimation or substrate loss? Glob Change Biol 10:1870–7.CrossRefGoogle Scholar
  31. Knohl A, Werner R, Brand W, Buchmann N. 2005. Short-term variations in δ13C of ecosystem respiration reveals link between assimilation and respiration in a deciduous forest. Oecologia 142:70–82.CrossRefPubMedGoogle Scholar
  32. Knapp A, Carroll CW, Denton E, La Pierre K, Collins S, Smith M. 2015. Differential sensitivity to regional-scale drought in six central US grasslands. Oecologia 177:949–57.CrossRefPubMedGoogle Scholar
  33. Kopittke GR, van Loon EE, Tietema A, Asscheman D. 2013. Soil respiration on an aging managed heathland: identifying an appropriate empirical model for predictive purposes. Biogeosciences 10:3007–38.CrossRefGoogle Scholar
  34. Knorr W, Prentice IC, House JI, Holland EA. 2005. Long-term sensitivity of soil carbon turnover to warming. Nature 433:298–301.CrossRefPubMedGoogle Scholar
  35. Kuzyakov Y, Gavrichkova O. 2010. Time lag between photosynthesis and carbon dioxide efflux from soil: a review of mechanisms and controls. Glob Change Biol 16:3386–406.CrossRefGoogle Scholar
  36. Larsen KS, Ibrom A, Beier C, Jonasson S, Michelsen A. 2007. Ecosystem respiration depends strongly on photosynthesis in a temperate heath. Biogeochemistry 85:201–13.CrossRefGoogle Scholar
  37. Liu L, King JS, Booker FL, Giardina CP, Lee Allen H, Hu S. 2009. Enhanced litter input rather than changes in litter chemistry drive soil carbon and nitrogen cycles under elevated CO2: a microcosm study. Glob Change Biol 15:441–53.CrossRefGoogle Scholar
  38. Luo Y, Zhou X. 2006. Soil respiration and the environment. Burlington: Academic Press.Google Scholar
  39. Mahecha M, Reichstein M, Carvalhais N, Lasslop G, Lange H, Seneviratne SI, Vargas R, Ammann C, Arain MA, Cescatti A, Janssens IA, Migliavacca M, Montagnani L, Richardson AD. 2010. Global convergence in the temperature sensitivity of respiration at ecosystem level. Science 329:838–40.CrossRefPubMedGoogle Scholar
  40. Maier CA, Kress LW. 2000. Soil CO2 evolution and root respiration in 11 year-old loblolly pine (Pinus taeda) plantations as affected by moisture and nutrient availability. Can J For Res 30:347–59.CrossRefGoogle Scholar
  41. Marcolla B, Cescatti A, Manca G, Zorer R, Cavagna M, Fiora A, Gianelle D, Rodeghiero M, Sottocornola M, Zampedri R. 2011. Climatic controls and ecosystem responses drive the inter-annual variability of the net ecosystem exchange of an alpine meadow. Agric For Meteorol 151:1233–43.CrossRefGoogle Scholar
  42. Met Office. 2012. Met Office Integrated Data Archive System (MIDAS) Land and Marine Surface Stations Data (1853-current). NCAS British Atmospheric Data Center.Google Scholar
  43. Migliavacca M, Reichstein M, Richardson AD, Colombo R, Sutton MA, Lasslop G, Tomelleri E, Wohlfahrt G, Carvalhais N, Cescatti A, Mahecha MD, Montagnani L, Papale D, Zaehle S, Arain A, Arneth A, Black TA, Carrara A, Dore S, Gianelle D, Helfter C, Hollinger D, Kutsch WL, Lafleur PM, Nouvellon Y, Rebmann C, Da Rocha HR, Rodeghiero M, Roupsard O, Sebastiá MT, Seufert G, Soussana JF, Van Der Molen MK. 2011. Semiempirical modeling of abiotic and biotic factors controlling ecosystem respiration across eddy covariance sites. Glob Change Biol 17:390–409.CrossRefGoogle Scholar
  44. Ottersen G, Planque B, Belgrano A, Post E, Reid PC, Stenseth NC. 2001. Ecological effects of the North Atlantic Oscillation. Oecologia 128:1–14.CrossRefGoogle Scholar
  45. Peñuelas J, Prieto P, Beier C, Cesaraccio C, De Angelis P, De Dato G, Emmett BA, Estiarte M, Garadnai J, Gorissen A, Láng EK, Kröel-Dulay G, Llorens L, Pellizzaro G, Riis-Nielsen T, Schmidt IK, Sirca C, Sowerby A, Spano D, Tietema A. 2007. Response of plant species richness and primary productivity in shrublands along a north–south gradient in Europe to seven years of experimental warming and drought: reductions in primary productivity in the heat and drought year of 2003. Glob Change Biol 13:2563–81.CrossRefGoogle Scholar
  46. Pietikäinen J, Pettersson M, Bååth E. 2005. Comparison of temperature effects on soil respiration and bacterial and fungal growth rates. FEMS Microbiol Ecol 52:49–58.CrossRefPubMedGoogle Scholar
  47. Quin SLO, Artz RRE, Coupar AM, Woodin SJ. 2015. Calluna vulgaris-dominated upland heathland sequesters more CO2 annually than grass-dominated upland heathland. Sci Total Environ 505:740–7.CrossRefPubMedGoogle Scholar
  48. Raich JW, Potter CS, Bhagawati D. 2002. Interannual variability in global soil respiration, 1980–94. Glob Change Biol 8:800–12.CrossRefGoogle Scholar
  49. Ratkowsky DA, Olley J, McMeekin TA, Ball A. 1982. Relationship between temperature and growth rate of bacterial cultures. J Bacteriol 149:1–5.PubMedPubMedCentralGoogle Scholar
  50. Reichstein M. 2003. Modeling temporal and large-scale spatial variability of soil respiration from soil water availability, temperature and vegetation productivity indices. Glob Biogeochem Cycles 17:1104.CrossRefGoogle Scholar
  51. Reynolds B, Chamberlain PM, Poskitt J, Woods C, Scott WA, Rowe EC, Robinson DA, Frogbrook ZL, Keith AM, Henrys PA, Black HIJ, Emmett BA. 2013. Countryside Survey: National “Soil Change” 1978–2007 for Topsoils in Great Britain—acidity, carbon, and total nitrogen status. Vadose Zone J 12.Google Scholar
  52. Richardson AD, Hollinger DY, Aber JD, Ollinger SV, Braswell BH. 2007. Environmental variation is directly responsible for short- but not long-term variation in forest-atmosphere carbon exchange. Glob Change Biol 13:788–803.CrossRefGoogle Scholar
  53. Rinnan R, Rousk J, Yergeau E, Kowalchuk GA, Bååth E. 2009. Temperature adaptation of soil bacterial communities along an Antarctic climate gradient: predicting responses to climate warming. Glob Change Biol 15:2615–25.CrossRefGoogle Scholar
  54. Rinnan R, Michelsen A, Bååth E. 2011. Long-term warming of a subarctic heath decreases soil bacterial community growth but has no effects on its temperature adaptation. Appl Soil Ecol 47:217–20.CrossRefGoogle Scholar
  55. Robinson DA, Jones SB, Lebron I, Reinsch S, Domínguez MT, Smith AR, Jones DL, Marshall MR, Emmett BA. 2016. Experimental evidence for drought induced alternative stable states of soil moisture. Sci Rep 6:20018.CrossRefPubMedPubMedCentralGoogle Scholar
  56. Sampson DA, Janssens IA, Curiel-Yuste J, Ceulemans R. 2007. Basal rates of soil respiration are correlated with photosynthesis in a mixed temperate forest. Glob Change Biol 13:2008–17.CrossRefGoogle Scholar
  57. Scott-Denton LE, Sparks KL, Monson RK. 2003. Spatial and temporal controls of soil respiration rate in a high-elevation, subalpine forest. Soil Biol Biochem 35:525–34.CrossRefGoogle Scholar
  58. Shao J, Zhou X, He H, Yu G, Wang H, Yi Luo, Chen J, Gu L, Li B. 2014. Partitioning climatic and biotic effects on interannual variability of ecosystem carbon exchange in three ecosystems. Ecosystems 17:1186–201.CrossRefGoogle Scholar
  59. Stoy PC, Richardson AD, Baldocchi DD, Katul GG, Stanovick J, Mahecha MD, Reichstein M, Detto M, Law BE, Wohlfahrt G, Arriga N, Campos J, McCaughey JH, Montagnani L, Paw UKT, Sevanto S, Williams M. 2009. Biosphere-atmosphere exchange of CO2 in relation to climate: a cross-biome analysis across multiple time scales. Biogeosciences 6:2297–312.CrossRefGoogle Scholar
  60. Sowerby A, Emmett BA, Williams D, Beier C, Evans CD. 2010. The response of dissolved organic carbon (DOC) and the ecosystem carbon balance to experimental drought in a temperate shrubland. Eur J Soil Sci 61:697–709.CrossRefGoogle Scholar
  61. Sulzman EW, Brant JB, Bowden RD, Lajtha K. 2005. Contribution of aboveground litter, belowground litter, and rhizosphere respiration to total soil CO2 efflux in an old growth coniferous forest. Biogeochemistry 73:231–56.CrossRefGoogle Scholar
  62. 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 Change Biol 18:336–48.CrossRefGoogle Scholar
  63. Tang X-L, Zhou G-Y, Liu S-G, Zhang D-Q, Liu S-Z, Li J, Zhou C-Y. 2006. Dependence of soil Respiration on soil Temperature and soil moisture in successional forests in Southern China. J Integr Plant Biol 48:654–63.CrossRefGoogle Scholar
  64. Thiessen S, Gleixner G, Wutzler T, Reichstein M. 2013. Both priming and temperature sensitivity of soil organic matter decomposition depend on microbial biomass—an incubation study. Soil Biol Biochem 57:739–48.CrossRefGoogle Scholar
  65. Thomas CK, Law BE, Irvine J, Martin JG, Pettijohn JC, Davis KJ. 2009. Seasonal hydrology explains interannual and seasonal variation in carbon and water exchange in a semiarid mature ponderosa pine forest in central Oregon. J Geophys Res 114.Google Scholar
  66. Trumbore S. 2000. Age of soil organic matter and soil respiration: radiocarbon constraints on belowground C dynamics. Ecol Appl 10:399–411.CrossRefGoogle Scholar
  67. Wan S, Luo Y. 2003. Substrate regulation of soil respiration in a tallgrass prairie: results of a clipping and shading experiment. Glob Biogeochem Cycles 17.Google Scholar
  68. Wang X, Piao S, Ciais P, Janssens IA, Reichstein M, Peng S, Wang T. 2010. Are ecological gradients in seasonal Q10 of soil respiration explained by climate or by vegetation seasonality? Soil Biol Biochem 42:1728–34.CrossRefGoogle Scholar
  69. Wang Y, Li Q, Wang H, Wen X, Yang F, Ma Z, Liu Y, Sun X, Yu G. 2011. Precipitation frequency controls interannual variation of soil respiration by affecting soil moisture in a subtropical forest plantation. Can J For Res 41:1897–906.CrossRefGoogle Scholar
  70. Wei W, Weile C, Shaopeng W. 2010. Forest soil respiration and its heterotrophic and autotrophic components: global patterns and responses to temperature and precipitation. Soil Biol Biochem 42:1236–44.CrossRefGoogle Scholar
  71. Yan J, Zhang D, Zhou G, Liu J. 2009. Soil respiration associated with forest succession in subtropical forests in Dinghushan Biosphere Reserve. Soil Biol Biochem 41:991–9.CrossRefGoogle Scholar
  72. Zhou T, Shi P, Hui D, Luo Y. 2009. Global pattern of temperature sensitivity of soil heterotrophic respiration (Q10) and its implications for carbon-climate feedback. J Geophys Res 114.Google Scholar
  73. Zhu B, Cheng W. 2011. Rhizosphere priming effect increases the temperature sensitivity of soil organic matter decomposition. Glob Change Biol 17:2172–83.CrossRefGoogle Scholar
  74. Zuur A, Ieno EN, Walker N, Saveliev A, Smith GM. 2009. Mixed effects models and extensions in ecology with R. New York: Springer.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • María T. Domínguez
    • 1
    • 2
  • Andrew R. Smith
    • 3
  • Sabine Reinsch
    • 1
  • Bridget A. Emmett
    • 1
  1. 1.Centre for Ecology and Hydrology BangorNatural Environment Research CouncilBangorUK
  2. 2.Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS-CSIC)SevilleSpain
  3. 3.School of Environment, Natural Resources and GeographyBangor UniversityBangorUK

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