Extreme-duration drought impacts on soil CO2 efflux are regulated by plant species composition

  • Chaoting Zhou
  • Joel A. Biederman
  • Hui Zhang
  • Linfeng Li
  • Xiaoyong Cui
  • Yakov Kuzyakov
  • Yanbin HaoEmail author
  • Yanfen Wang
Regular Article



Long-duration drought can alter ecosystem plant species composition with subsequent effects on carbon cycling. We conducted a rainfall manipulation field experiment to address the question: how does drought-induced vegetation change, specifically shrub encroachment into grasslands, regulate impacts of subsequent drought on soil CO2 efflux (Rs) and its components (autotrophic and heterotrophic, Ra and Rh)?


We conducted a two-year experiment in Inner Mongolia plateau, China, using constructed steppe communities including graminoids, shrubs and their mixture (graminoid + shrub) to test the effects of extreme-duration drought (60-yr return time) on Rs, Rh and Ra.


Our results indicated that extreme-duration drought reduced net primary production, with subsequent effects on Rs, Rh and Ra in all three vegetation communities. There was a larger relative decline in Ra (35–54%) than Rs (30–37%) and Rh (28–35%). Interestingly, we found Rs in graminoids is higher than in shrubs under extreme drought. Meanwhile, Rh declines were largest in the shrub community. Although Ra and Rh both decreased rapidly during drought treatment, Rh recovered quickly after the drought, while Ra did not, limiting the Rs recovery.


This study suggests that plant species composition regulates several aspects of soil CO2 efflux response to climate extremes. This regulation may be limited by above- and below-ground net primary production depending on soil water availability. The results of this experiment address a critical knowledge gap in the relationship between soil respiration and plant species composition. With shrub encroachment into grasslands, total soil respiration is reduced and can partly offset the effect of reduction in productivity under drought stress.


Extreme drought Soil CO2 efflux Autotrophic Heterotrophic Plant species composition Net primary production 



This project was funded by the CAS Strategic Priority Research Programmer (A) (Grant No. XDA20050103 and XDA19030202) and the funds for International Cooperation and Exchange of National Natural Science Foundation of China (Grant No. 31761123001 and 31761143018). We also show great appreciation for two anonymous reviewer’s suggestions.

Supplementary material

11104_2019_4025_MOESM1_ESM.docx (680 kb)
ESM 1 (DOCX 679 kb)


  1. Bai Y, Wu J, Xing Q, Pan Q, Huang J, Yang D, Han X (2008) Primary production and rain use efficiency across a precipitation gradient on the Mongolia plateau. Ecology 89(8):2140–2153CrossRefGoogle Scholar
  2. 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
  3. Batima P, Dagvadorj D (2000) Climate change and its impacts in Mongolia. Natl agency Meteorol Hydrol environ Monit JEMR Publ Ulaanbaatar, Mong 227pGoogle Scholar
  4. Bond-Lamberty B, Wang C, Gower ST (2004) A global relationship between the heterotrophic and autotrophic components of soil respiration? Glob Chang Biol 10:1756–1766CrossRefGoogle Scholar
  5. Breshears DD, Cobb NS, Rich PM, Price KP, Allen CD, Balice RG, Romme WH, Kastens JH, Floyd ML, Belnap J, Anderson JJ, Myers OB, Meyer CW (2005) Regional vegetation die-off in response to global-change-type drought. Proc Natl Acad Sci 102:15144–15148. CrossRefGoogle Scholar
  6. Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil-nitrogen - a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842. CrossRefGoogle Scholar
  7. Ciais Ph, Reichstein M, Viovy N, Granier A, Ogée J, Allard V, Aubinet M, Buchmann N, Bernhofer Chr, Carrara A, Chevallier F, De Noblet N, Friend AD, Friedlingstein P, Grünwald 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(7058):529–533CrossRefGoogle Scholar
  8. Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Pérez-Harguindeguy N, Quested HM, Santiago LS, Wardle DA, Wright IJ, Aerts R, Allison SD, van Bodegom P, Brovkin V, Chatain A, Callaghan TV, Díaz S, Garnier E, Gurvich DE, Kazakou E, Klein JA, Read J, Reich PB, Soudzilovskaia NA, Vaieretti MV, Westoby M (2008) Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol Lett 11:1065–1071CrossRefGoogle Scholar
  9. Correia AC, Minunno F, Caldeira MC, Banza J, Mateus J, Carneiro M, Wingate L, Shvaleva A, Ramos A, Jongen M, Bugalho MN, Nogueira C, Lecomte X, Pereira JS (2012) Soil water availability strongly modulates soil CO2 efflux in different Mediterranean ecosystems: model calibration using the Bayesian approach. Agric Ecosyst Environ 161:88–100. CrossRefGoogle Scholar
  10. Dai A (2012) Increasing drought under global warming in observations and models. Nat Clim Chang 3:52–58. CrossRefGoogle Scholar
  11. Davis MA, Grime JP, Thompson KEN (2000) Fluctuating resources in plant communities : a general theory of invasibility. 528–534Google Scholar
  12. Dias ATC, van Ruijven J, Berendse F (2010) Plant species richness regulates soil respiration through changes in productivity. Oecologia 163:805–813. CrossRefPubMedCentralGoogle Scholar
  13. Domínguez MT, Holthof E, Smith AR, Koller E, Emmett BA (2017) Contrasting response of summer soil respiration and enzyme activities to long-term warming and drought in a wet shrubland (NE Wales, UK). Appl Soil Ecol 110:151–155CrossRefGoogle Scholar
  14. Freeman C, Liska G, Ostle NJ, Lock MA, Reynolds B, Hudson J (1996) Microbial activity and enzymic decomposition processes following peatland water table drawdown. Plant Soil 180:121–127CrossRefGoogle Scholar
  15. Frey SD, Lee J, Melillo JM, Six J (2013) The temperature response of soil microbial efficiency and its feedback to climate. Nat Clim Chang 3:395–398CrossRefGoogle Scholar
  16. Gill RA, Jackson RB (2000) Global patterns of root turnover for terrestrial ecosystems. New Phytol 147(1):13–31CrossRefGoogle Scholar
  17. Golluscio RA, Sala OE, Lauenroth WK (1998) Differential use of large summer rainfall events by shrubs and grasses: a manipulative experiment in the Patagonian steppe. Oecologia 115:17–25CrossRefGoogle Scholar
  18. Hayes DC, Seastedt TR (1987) Root dynamics of tallgrass prairie in wet and dry years. Can J Bot 65:787–791CrossRefGoogle Scholar
  19. Hessl AE, Anchukaitis KJ, Jelsema C, Cook B, Byambasuren O, Leland C, Nachin B, Pederson N, Tian H, Hayles LA (2018) Past and future drought in Mongolia. Sci Adv 4:1–8. CrossRefGoogle Scholar
  20. Hester AJ, Miles J, Gimingham CH (1991) Succession from heather moorland to birch woodland. II. Growth and competition between Vaccinium myrtillus, Deschampsia flexuosa and Agrostis capillaris. J Ecol:317–327Google Scholar
  21. Högberg P, Read DJ (2006) Towards a more plant physiological perspective on soil ecology. Trends Ecol Evol 21:548–554CrossRefGoogle Scholar
  22. Hoover DL, Rogers BM (2016) Not all droughts are created equal: the impacts of interannual drought pattern and magnitude on grassland carbon cycling. Glob Chang Biol 22:1809–1820. CrossRefGoogle Scholar
  23. Huenneke LF, Clason D, Muldavin E (2001) Spatial heterogeneity in Chihuahuan Desert vegetation: implications for sampling methods in semi-arid ecosystems. J Arid Environ 47:257–270. CrossRefGoogle Scholar
  24. Huxman TE, Snyder KA, Tissue D, Leffler AJ, Ogle K, Pockman WT, Sandquist DR, Potts DL, Schwinning S (2004) Precipitation pulses and carbon fluxes in semiarid and arid ecosystems. Oecologia 141:254–268CrossRefGoogle Scholar
  25. 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
  26. Jentsch A, Kreyling J, Elmer M, Gellesch E, Glaser B, Grant K, Hein R, Lara M, Mirzae H, Nadler SE, Nagy L, Otieno D, Pritsch K, Rascher U, Schädler M, Schloter M, Singh BK, Stadler J, Walter J, Wellstein C, Wöllecke J, Beierkuhnlein C (2011) Climate extremes initiate ecosystem-regulating functions while maintaining productivity. J Ecol 99:689–702. CrossRefGoogle Scholar
  27. Johnson D, Phoenix GK, Grime JP (2008) Plant community composition, not diversity, regulates soil respiration in grasslands. Biol Lett 4:345–348CrossRefPubMedCentralGoogle Scholar
  28. Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant Soil 321:5–33CrossRefGoogle Scholar
  29. Kieft TL, Carleton S, White S, et al (1998) Temporal Dynamics in Soil Carbon and Nitrogen Resources at a Grassland-Shrubland EcotoneGoogle Scholar
  30. Knapp A, Briggs J, … SC-GC, 2008a Undefined shrub encroachment in north American grasslands: shifts in growth form dominance rapidly alters control of ecosystem carbon inputs. Wiley Online LibrGoogle Scholar
  31. Knapp AK, Briggs JM, Collins SL et al (2008b) Shrub encroachment in north American grasslands: shifts in growth form dominance rapidly alters control of ecosystem carbon inputs. Glob Chang Biol 14:615–623. CrossRefGoogle Scholar
  32. Kuzyakov Y (2006) Sources of CO 2 efflux from soil and review of partitioning methods. Soil Biol Biochem 38:425–448CrossRefGoogle Scholar
  33. Lange M, Eisenhauer N, Sierra CA, Bessler H, Engels C, Griffiths RI, Mellado-Vázquez PG, Malik AA, Roy J, Scheu S, Steinbeiss S, Thomson BC, Trumbore SE, Gleixner G (2015) Plant diversity increases soil microbial activity and soil carbon storage. Nat Commun 6:6707CrossRefGoogle Scholar
  34. Le Houérou HN (2000) Utilization of fodder trees and shrubs in the arid and semiarid zones of West Asia and North Africa. Arid Soil Res Rehabil 14:101–135CrossRefGoogle Scholar
  35. Li S, Verburg PH, Lv S, Wu J, Li X (2012) Spatial analysis of the driving factors of grassland degradation under conditions of climate change and intensive use in Inner Mongolia, China. Reg Environ Chang 12:461–474CrossRefGoogle Scholar
  36. Liu W, Zhang Z, Wan S (2009) Predominant role of water in regulating soil and microbial respiration and their responses to climate change in a semiarid grassland. Glob Chang Biol 15:184–195. CrossRefGoogle Scholar
  37. Martin JG, Bolstad PV (2009) Variation of soil respiration at three spatial scales: components within measurements, intra-site variation and patterns on the landscape. Soil Biol Biochem 41:530–543CrossRefGoogle Scholar
  38. Meisner A, Bååth E, Rousk J (2013) Microbial growth responses upon rewetting soil dried for four days or one year. Soil Biol Biochem 66:188–192CrossRefGoogle Scholar
  39. Metcalfe DB, Fisher RA, Wardle DA (2011) Plant communities as drivers of soil respiration: pathways, mechanisms, and significance for global change. Biogeosciences 8:2047–2061. CrossRefGoogle Scholar
  40. Moyano FE, Kutsch WL, Schulze ED (2007) Response of mycorrhizal, rhizosphere and soil basal respiration to temperature and photosynthesis in a barley field. Soil Biol Biochem 39:843–853. CrossRefGoogle Scholar
  41. Moyano FE, Manzoni S, Chenu C (2013) Responses of soil heterotrophic respiration to moisture availability: an exploration of processes and models. Soil Biol Biochem 59:72–85CrossRefGoogle Scholar
  42. Poulter B, Frank D, Ciais P, Myneni RB, Andela N, Bi J, Broquet G, Canadell JG, Chevallier F, Liu YY, Running SW, Sitch S, van der Werf GR (2014) Contribution of semi-arid ecosystems to interannual variability of the global carbon cycle. Nature 509:600–603CrossRefGoogle Scholar
  43. Preece C, Peñuelas J (2016) Rhizodeposition under drought and consequences for soil communities and ecosystem resilience. Plant Soil 409:1–17CrossRefGoogle Scholar
  44. Putten WH, Bardgett RD, Bever JD et al (2013) Plant–soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276CrossRefGoogle Scholar
  45. Raich JW, Tufekciogul A (2000) Vegetation and soil respiration: correlations and controls. Biogeochemistry 48:71–90CrossRefGoogle Scholar
  46. 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
  47. Sanaullah M, Blagodatskaya E, Chabbi A, Rumpel C, Kuzyakov Y (2011) Drought effects on microbial biomass and enzyme activities in the rhizosphere of grasses depend on plant community composition. Appl Soil Ecol 48:38–44. CrossRefGoogle Scholar
  48. Sanaullah M, Chabbi A, Girardin C, Durand JL, Poirier M, Rumpel C (2014) Effects of drought and elevated temperature on biochemical composition of forage plants and their impact on carbon storage in grassland soil. Plant Soil 374:767–778. CrossRefGoogle Scholar
  49. Savage KE, Davidson EA (2001) Interannual variation of soil respiration in two New England forests. Glob Biogeochem Cycles 15:337–350CrossRefGoogle Scholar
  50. Schlesinger WH, Andrews JA (2000) Soil respiration and the global carbon cycle. Biogeochemistry 48:7–20CrossRefGoogle Scholar
  51. 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
  52. Silver WL, Miya RK (2001) Global patterns in root decomposition: comparisons of climate and litter quality effects. Oecologia 129:407–419. CrossRefGoogle Scholar
  53. 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
  54. Tielbörger K, Bilton MC, Metz J, Kigel J, Holzapfel C, Lebrija-Trejos E, Konsens I, Parag HA, Sternberg M (2014) Middle-eastern plant communities tolerate 9 years of drought in a multi-site climate manipulation experiment. Nat Commun 5:5102. CrossRefPubMedCentralGoogle Scholar
  55. Tietjen B, Schlaepfer D, Bradford J, et al (2016) Climate change-induced vegetation shifts lead to more ecological droughts despite projected rainfall increases in many global temperate drylandsGoogle Scholar
  56. Trenberth KE, Dai A, van der Schrier G, Jones PD, Barichivich J, Briffa KR, Sheffield J (2013) Global warming and changes in drought. Nat Clim Chang 4:17–22. CrossRefGoogle Scholar
  57. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass-C. Soil Biol Biochem 19:703–707. CrossRefGoogle Scholar
  58. Wang X, Liu L, Piao S, Janssens IA, Tang J, Liu W, Chi Y, Wang J, Xu S (2014) Soil respiration under climate warming: differential response of heterotrophic and autotrophic respiration. Glob Chang Biol 20:3229–3237. CrossRefGoogle Scholar
  59. 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
  60. Zhang Q, Lei H-M, Yang D-W (2013) Seasonal variations in soil respiration, heterotrophic respiration and autotrophic respiration of a wheat and maize rotation cropland in the North China plain. Agric For Meteorol 180:34–43CrossRefGoogle Scholar
  61. Zhao C, Miao Y, Yu C, Zhu L, Wang F, Jiang L, Hui D, Wan S (2016) Soil microbial community composition and respiration along an experimental precipitation gradient in a semiarid steppe. Sci Rep 6:24317CrossRefPubMedCentralGoogle Scholar
  62. Zhou X, Wan S, Luo Y (2007) Source components and interannual variability of soil CO2 efflux under experimental warming and clipping in a grassland ecosystem. Glob Chang Biol 13:761–775Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.College of Life SciencesUniversity of Chinese Academy of SciencesBeijingChina
  2. 2.Southwest Watershed Research Center, Agricultural Research ServiceTucsonUSA
  3. 3.College of Bioscience and BiotechnologyYangzhou UniversityYangzhouChina
  4. 4.CAS Center for Excellence in Tibetan Plateau Earth SciencesChinese Academy of Sciences (CAS)BeijingChina
  5. 5.Department of Soil Science of Temperate Ecosystems, Department of Agricultural Soil ScienceUniversity of GöttingenGöttingenGermany
  6. 6.Institute of Environmental SciencesKazan Federal UniversityKazanRussia

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