Abstract
Aims
Soil respiration is a major flux of CO2 to the atmosphere. Despite its significance there is a limited understanding of its magnitude, controlling factors and how it varies over time and space in arid ecosystems. We evaluated the temporal pattern of soil CO2 efflux and their response to rain pulses in a patagonian steppe, taking into account the spatial heterogeneity (bare soil and vegetated patches).
Materials and methods
We measured soil CO2 efflux in bare soil and vegetated patches along the year. We also analyzed physical and chemical soil traits, root density and heterotrophic bacterial count.
Results
Soil water content and temperature exhibited seasonal variability and it was larger in bare soil patches than in vegetated patches. Root density, organic matter and phosphorus were higher in vegetated patches than in bare soil. CO2 efflux was 48% higher in vegetated patches than in bare soil patches. Soil CO2 efflux decreased from summer to winter, reaching its maximum value (about 0.6 μmol m2 s−1) in spring. In both patch types, soil CO2 efflux was explained by the interaction between soil temperature and soil water content. Soil CO2 efflux also was positively correlated with soil root density. Bare soil and vegetated patches exhibited distinct response to a rain pulses. Vegetated patches were highly sensitive to rainfall events, generating a large CO2 pulse, returning to previous values after three days. Bare soil CO2 efflux did not exhibit significant changes after a rain pulse.
Conclusions
In patagonian arid ecosystems, the seasonal variation in soil respiration is explained mainly by the interaction between soil temperature and water content. Bare soil patches had higher water content but lower root density resulting in lower soil CO2 respiration than vegetated patches. However, at ecosystem level the contribution of bare soil to total soil CO2 efflux was similar to the contribution of vegetated patches because bare soil cover is 65% in the study area. Changes in the number of small rain events as well as changes in plant cover could have large consequences on soil ecology and biochemistry in dry and heterogeneous ecosystems.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11104-019-04268-7/MediaObjects/11104_2019_4268_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11104-019-04268-7/MediaObjects/11104_2019_4268_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11104-019-04268-7/MediaObjects/11104_2019_4268_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11104-019-04268-7/MediaObjects/11104_2019_4268_Fig4_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11104-019-04268-7/MediaObjects/11104_2019_4268_Fig5_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11104-019-04268-7/MediaObjects/11104_2019_4268_Fig6_HTML.png)
Similar content being viewed by others
References
Aguiar MR, Sala OE (1999) Patch structure, dynamics and implications for the functioning of arid ecosystems. Tree 14:273–277
Ahlström A, Raupach MR, Schurgers G et al (2015) The dominant role of semi-arid ecosystems in the trend and variability of the land CO2 sink. Science 348(6237):895–899. https://doi.org/10.1126/science.aaa1668
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 141:221–235. https://doi.org/10.1007/s00442-004-1519-1-
Bao X, Zhu X, Chang X, Wang S, Xu B, Luo C, Zhang Z, Wang Q, Rui Y, Cui X (2016) Effects of soil temperature and moisture on soil respiration on the Tibetan plateau. PLoS One 11:e0165212
Bertiller MB, Mazzarino MJ, Carrera AL, Diehl P, Satti P, Gobbi M, Sain CL (2006) Leaf strategies and soil N across a regional humidity gradient in Patagonia. Oecologia 148:612–624. https://doi.org/10.1007/s00442-006-0401-8-
Bolstad PV, Davis KJ, Martin J, Cook BD, Wang W (2004) Component and whole-system respiration fluxes in northern deciduous forests. Tree Physiol 24:493–504
Borken W, Savage KE, Davidson EA, Trumbore SE (2006) Effects of experimental drought on soil respiration and radiocarbon efflux from a temperate forest soil. Glob Chang Biol 12(2):177–193. https://doi.org/10.1111/j.1365-2486.2005.01058.x
Breheny P, Burchett W (2017) Visualization of regression models using visreg. The R Journal 9(2):56–71
Bremner JM (1996) Nitrogen Total. In: methods of soil analysis. Part 3. Chemical methods. Madison WI. SSSA-ASA. Pp 1149-1176
Bretz F, Hothorn T, Westfall P (2010) Multiple comparisons using R. CRC Press
Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Arce ME (2009) Soil water availability and rooting depth as determinants of hydraulic architecture of Patagonian woody species. Oecologia 160:631–641. https://doi.org/10.1007/s00442-009-1331-z
Bucci SJ, Scholz FG, Peschiutta ML et al (2013) The stem xylem of Patagonian shrubs operates far from the point of catastrophic dysfunction and is additionally protected from drought-induced embolism by leaves and roots. Plant Cell Environ 36:2163–2174. https://doi.org/10.1111/pce.12126
Burnham KP, Anderson DR (2002) Model Selection and Multimodel Inference: a practical information-theoretic approach. New York Springer-Verlag
Cable JM, Ogle K, Williams DG, Weltzin JF, Huxman TE (2008) Soil texture drives responses of soil respiration to precipitation pulses in the Sonoran desert: implications for climate change. Ecosystems 11(6):961–979. https://doi.org/10.1007/s10021-008-9172-x
Cable JM, Ogle K, Lucas RW et al (2011) The temperature responses of soil respiration in deserts: a seven desert synthesis. Biogeochemistry 103(1–3):71–90. https://doi.org/10.1007/s10533-010-9448-z
Carbone MS, Winston GC, Trumbore SE (2008) Soil respiration in perennial grass and shrub ecosystems: linking environmental controls with plant and microbial sources on seasonal and diel timescales. J Geophys Res Biogeosci 113(G2). https://doi.org/10.1029/2007JG000611
Carlyle JC, Than UB (1988) Abiotic controls of soil respiration beneath an eighteen-year-old Pinus Radiata stand in south-eastern Australia. J Ecol 76:654–662
Collins SL, Sinsabaugh RL, Crenshaw C, Green L, Porras-Alfaro A, Stursova M, Zeglin LH (2008) Pulse dynamics and microbial processes in aridland ecosystems. J Ecol 96:413–420. https://doi.org/10.1111/j.1365-2745.2008.01362.x
Conant RT, Klopatek JM, Klopatek CC (2000) Environmental factors controlling soil respiration in three semiarid ecosystems. Soil Sci Soc Am J 64:383–390
Cox DR, Snell EJ (1989) Analysis of binary data, 2nd edn. Chapman and Hall/CRC, London
Curiel Yuste J, Janssens IA, Carrara A et al (2003) Interactive effects of temperature and precipitation on soil respiration in a temperate maritime pine forest. Tree Physiol 23:1263–1270
Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173
Davidson EA, Belk E, Boone RD (1998) Soil water content and temperature as independent or confounded factors controlling soil respiration in a temperate mixed hardwood forest. Glob Chang Biol 4:217–227. https://doi.org/10.1046/j.1365-2486.1998.00128.x
Deng Q, Hui D, Zhang D, Zhou G, Liu J, Liu S, Chu G, Li J (2012) Effects of precipitation increase on soil respiration: a three-year field experiment in subtropical forests in China. PLoS One 7:e41493
Euskirchen ES, Pregitzer KS, Chen J (2006) Carbon fluxes in a young, naturally regenerating jack pine ecosystem. J Geophys Res 111. https://doi.org/10.1029/2005JD005793
Fang C, Moncrieff J (2001) The dependence of soil CO2 efflux on temperature. Soil Biol Biochem 33:155–165
Giardina CP, Binkley D, Ryan MG, Fownes JH, Senock RS (2004) Belowground carbon cycling in a humid tropical forest decreases with fertilization. Oecologia 139:545–550. https://doi.org/10.1007/s00442-004-1552-0
Golluscio A, Sala E, Lauenroth K (1998) Differential use of large summer rainfall events by shrubs and grasses: a manipulative experiment in the Patagonian steppe. Oecologia 115:17–25
Golluscio RA, Sigal Escalada V, Pérez J (2009) Minimal plant responsiveness to summer water pulses : Ecophysiological constraints of three species of semiarid Patagonia. Rangel Ecol Manag 62:171–178
Gonzalez-Polo M, Austin AT (2009) Spatial heterogeneity provides organic matter refuges for soil microbial activity in the Patagonian steppe, Argentina. Soil Biol Biochem 41:1348–1351. https://doi.org/10.1016/j.soilbio.2009.03.008
Han G, Luo Y, Li D, **a J, **ng Q, Yu J (2014a) Ecosystem photosynthesis regulates soil respiration on a diurnal scale with a short-term time lag in a coastal wetland. Soil Biol Biochem 68:85–94. https://doi.org/10.1016/j.soilbio.2013.09.024
Han G, **ng Q, Luo Y, Rafique R, Yu J, Mikle N (2014b) Vegetation types Alter soil respiration and its temperature sensitivity at the field scale in an estuary wetland. PLoS One 9:e91182
Han T, Huang W, Liu J, Zhou G, **ao Y (2015) Different soil respiration responses to litter manipulation in three subtropical successional forests. Sci Rep 5:18166
Han C, Liu T, Duan L, Zhang S, Singh VP (2017) Spatio-temporal distribution of soil respiration in dune-meadow cascade ecosystems in the Horqin Sandy land, China. CATENA 157:397–406. https://doi.org/10.1016/j.Catena.2017.05.012
Hanson PJ, Edwards NT, Garrten CT, Andrews JA (2000) Separating root and soil microbial contributions to soil respiration: a review of methods and observations. Biogeochemistry 48:115–146. https://doi.org/10.1023/A:1006244819642
Helmuth B, Kingsolver JG, Carrington E (2005) Biophysics, physiological ecology and climate change: does mechanism matter? Annu Rev Physiol 67:177–201. https://doi.org/10.1146/annurev.physiol.67.040403.105027
Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Löfvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792. https://doi.org/10.1038/35081058
Hursh A, Ballantyne A, Cooper L, Maneta M, Kimball J, Watts J (2016) The sensitivity of soil respiration to soil temperature, moisture, and carbon supply at the global scale. Glob Chang Biol 23:2090–2103. https://doi.org/10.1111/gcb.13489
Jarvis P, Rey A, Petsikos C, Wingate L, Rayment M, Pereira J, Banza J, David J, Miglietta F, Borghetti M, Manca G, Valentini R (2007) Drying and wetting of Mediterranean soils stimulates decomposition and carbon dioxide emission: the “birch effect”. Tree Physiol 27:929–940. https://doi.org/10.1093/treephys/27.7.929
Kelliher FM, Ross DJ, Law BE, Baldocchi DD, Rodda NJ (2004) Limitations to carbon mineralization in litter and mineral soil of young and old ponderosa pine forests. For Ecol Manag 191:201–213. https://doi.org/10.1016/j.foreco.2003.12.005
Lai L, Zhao X, Jiang L, Wang Y, Luo L, Zheng Y, Chen X, Rimmington GM (2012) Soil respiration in different agricultural and natural ecosystems in an arid region. PLoS One 7:e48011
Lai L, Wang J, Tian Y, Zhao X, Jiang L, Chen X, Gao Y, Wang S, Zheng Y (2013) Organic matter and water addition enhance soil respiration in an arid region. PLoS One 8:e77659
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. https://doi.org/10.1111/j.1365-2486.2008.01728.x
Maestre FT, Cortina J (2003) Small-scale spatial variation in soil CO2 efflux in a Mediterranean semiarid steppe. Appl Soil Ecol 23:199–209. https://doi.org/10.1016/S0929-1393(03)00050-7
Mangiafico SS (2015) An R companion for the handbook of biological statistics, version 1.09c. New Brunswick, NJ: Rutgers cooperative extension, 274 p. Available from: http://rcompanion.org/documents/RCompanionBioStatistics.pdf
Manzoni S, Schimel JP, Porporato A (2012) Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology 93:930–938. https://doi.org/10.1890/11-0026.1
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 41:530–543. https://doi.org/10.1016/j.soilbio.2008.12.012
Mazzarino MJ, Bertiller M, Schlichter T, Gobbi M (1998) Nutrient cycling in Patagonian ecosystems. Doctoral dissertation, Asociación Argentina de Ecología
Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. Circular no. 939. USDA
Paruelo JM, Aguiar MR, Golluscio RA (1988) Soil water availability in the Patagonian arid steppe: gravel content effect. Arid Soil Res Rehabil 2:67–74
Pepper IL, Gerba CP (2015) Cultural methods. In: Pepper IL, Gerba CP, gentry TJ (eds) environmental microbiology, 3rd edn. Pp 195-212 https://doi.org/10.1016/B978-0-12-394626-3.00010-7
Pereyra DA, Bucci SJ, Arias NS, Ciano N, Cristiano PM, Goldstein G, Scholz FG (2017) Grazing increases evapotranspiration without the cost of lowering soil water storages in arid ecosystems. Ecohydrology 10:1–12. https://doi.org/10.1002/eco.1850
Peri PL (2011) Carbon storage in cold temperate ecosystems in southern Patagonia, Argentina. In:Atazadeh I (ed) biomass and remote sensing of biomass, pp 213-226. InTech Publisher, Croatia, 262 pp. ISBN: 978-953-307-490-0
Peri PL, Bahamonde H, Christiansen R (2015) Soil respiration in Patagonian semiarid grasslands under contrasting environmental and use conditions. J Arid Environ 119:1–8. https://doi.org/10.1016/j.jaridenv.2015.03.008
Pinheiro JC, Bates DM (2000) Mixed effects models in S and S-PLUS. Springer, New York
Prieto LH, Bertiller MB, Carrera AL, Olivera NL (2011) Soil enzyme and microbial activities in a grazing ecosystem of Patagonian Monte, Argentina. Geoderma 162:281–287. https://doi.org/10.1016/j.geoderma.2011.02.011
R Development Core Team (2018) R: a language and environment for statistical computing. R Foundation for statistical computing. Vienna, Austria
Rey A, Pegoraro E, Oyonarte C, Were A, Escribano P, Raimundo J (2011) Impact of land degradation on soil respiration in a steppe (Stipa tenacissima L.) semi-arid ecosystem in the SE of Spain. Soil Biol Biochem 43(2):393–403. https://doi.org/10.1016/j.soilbio.2010.11.007
Reyes MF, Aguiar MR (2017) Is the zone of influence colonized by roots of neighboring species? Field tests in a Patagonian steppe. J Arid Environ 137:30–34. https://doi.org/10.1016/j.jaridenv.2016.10.012
Reynolds JF, Kemp PR, Ogle K, Fernández RJ (2004) Modifying the “pulse-reserve” paradigm for deserts of North America: precipitation pulses, soil water, and plant responses. Oecologia 141:194–210. https://doi.org/10.1007/s00442-004-1524-4
Richards LA (1954) Diagnosis and improvement of saline and alkali soils. Handbook no. 60. US Department of Agriculture, Washington, DC. https://doi.org/10.2136/sssaj1954.03615995001800030032x
Rousk J, Bengtson P (2014) Microbial regulation of global biogeochemical cycles. Front Microbiol 5:103–307. https://doi.org/10.1038/495305a
Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394. https://doi.org/10.1890/06-0219
Schlesinger WH, Raikes JA, Hartley AE, Cross AF (1996) On the spatial pattern of soil nutrients in desert ecosystems: ecological archives E077-002. Ecology 77(2):364–374
Scholz FG, Bucci SJ, Arias N, Meinzer FC, Goldstein G (2012) Osmotic and elastic adjustments in cold desert shrubs differing in rooting depth: co** with drought and subzero temperatures. Oecologia 170:885–897. https://doi.org/10.1007/s00442-012-2368-y
Song W, Chen S, Wu B, Zhu Y, Zhou Y, Li Y, Cao Y, Lu Q, Lin G (2012) Vegetation cover and rain timing co-regulate the responses of soil CO2 efflux to rain increase in an arid desert ecosystem. Soil Biol Biochem 49:114–123. https://doi.org/10.1016/j.soilbio.2012.01.028
Soriano A, Golluscio RA, Satorre EH (1987) Spatial heterogeneity of the root system of grasses in the Patagonian arid steppe. Bull Torrey Bot Club 114:103–108
Soriano A, Sala OE, Perelman SB (1994) Patch structure and dynamics in a Patagonian arid steppe. Vegetatio 111(2):127–135. https://doi.org/10.1007/BF00040332
Sponseller RA (2007) Precipitation pulses and soil CO2 flux in a Sonoran Desert ecosystem. Glob Chang Biol 13(2):426–436. https://doi.org/10.1111/j.1365-2486.2006.01307.x
Trumbore S (2000) Age of soil organic matter and soil respiration : radiocarbon constraints on belowground C dynamics. Ecol Appl 10(2):399–411
Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, as a proposed modification of the chromic acid titration method. Soil Sci 37:29–38
Wang Y, Hao Y, Cui XY, Zhao H, Xu C, Zhou X, Xu Z (2014) Responses of soil respiration and its components to drought stress. J Soils Sediments 14(1):99–109. https://doi.org/10.1007/s11368-013-0799-7
Xu M, Shang H (2016) Contribution of soil respiration to the global carbon equation. J Plant Physiol 203:16–28. https://doi.org/10.1016/j.jplph.2016.08.007
Yan L, Chen S, **a J, Luo Y (2014) Precipitation regime shift enhanced the rain pulse effect on soil respiration in a semi-arid steppe. PLoS One 9:e104217
Zhang LH, Chen YN, Zhao RF, Li WH (2010) Significance of temperature and soil water content on soil respiration in three desert ecosystems in Northwest China. J Arid Environ 74(10):1200–1211. https://doi.org/10.1016/j.jaridenv.2010.05.031
Zhang YJ, Bucci SJ, Arias NS, Scholz FG, Hao GY, Cao KF, Goldstein G (2016) Freezing resistance in Patagonian woody shrubs: the role of cell wall elasticity and stem vessel size. Tree Physiol 36:1007–1018. https://doi.org/10.1093/treephys/tpw036
Acknowledgements
The authors acknowledge the funding support from Fondo para la Promoción Científica y Tecnológica (FONCyT; grant PICT 2010-960, PICT 2013-2426, PICT 2016-3019). We thank to staff of Instituto Nacional de Tecnologia Agropecuaria (INTA) for allowing the access and assistance in the Rio Mayo Experimental Field. This work complies with Argentinian law. We also thank to Conicet by the grant PUE # 22920180100033CO.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest.
Additional information
Responsible Editor: Lucas Silva.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Silletta, L.C., Cavallaro, A., Kowal, R. et al. Temporal and spatial variability in soil CO2 efflux in the patagonian steppe. Plant Soil 444, 165–176 (2019). https://doi.org/10.1007/s11104-019-04268-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-019-04268-7