Abstract
The rate of CO2 diffusion from soils to the atmosphere (soil CO2 efflux, soil respiration; Rsoil) reflects the integrated activity of roots and microbes and is among the largest fluxes of the terrestrial global C cycle. Most experiments have demonstrated that Rsoil increases by 20–35% following the exposure of an ecosystem to an atmosphere enriched in CO2 (i.e., eCO2), but such experiments have largely been performed in young and N-limited ecosystems. Here, we exposed a mature and phosphorus-limited eucalypt woodland to eCO2 and measured Rsoil across three full years with a combination of manual surveys and automated measurements. We also implemented an empirical model describing the dependence of Rsoil on volumetric soil water content (θ) and soil temperature (Tsoil) to produce annual Rsoil flux estimates. Rsoil varied strongly with Tsoil, θ, and precipitation in complex and interacting ways. The realized long-term (weeks to years) temperature dependence (Q10) of Rsoil increased from ~ 1.6 at low θ up to ~ 3 at high θ. Additionally, Rsoil responded strongly and rapidly to precipitation events in a manner that depended on the conditions of θ and Tsoil at the beginning of the rain event; Rsoil increased by up to 300% within 30 min when rain fell on dry soil that had not experience rain in the preceding week, but Rsoil was rapidly reduced by up to 70% when rain fell on wet soil, leading to flooding. Repeated measures analysis of Rsoil observations over 3 years indicated no significant change in response to CO2 enrichment (P = 0.7), and elevated CO2 did not alter the dependence of Rsoil on Tsoil or θ. However, eCO2 increased Rsoil observations by ~ 10% under some constrained and moderate environmental conditions. Annual Rsoil flux sums estimated with an empirical model were ~ 7% higher in eCO2 plots than in aCO2 plots, but this difference was not statistically significant. The lack of a large eCO2 effect on Rsoil is consistent with recent evidence that aboveground net primary production was not stimulated by eCO2 in this ecosystem. The C budget of this mature woodland may be less affected by eCO2 than the young N-limited ecosystems that have been studied previously.
Similar content being viewed by others
References
Adair CE, Reich PB, Trost JJ, Hobbie SE (2011) Elevated CO2 stimulates grassland soil respiration by increasing carbon inputs rather than by enhancing soil moisture. Glob Change Biol 17:3546–3563. https://doi.org/10.1111/j.1365-2486.2011.02484.x
Allison SD (2012) A trait-based approach for modelling microbial litter decomposition. Ecol Lett 15:1058–1070. https://doi.org/10.1111/j.1461-0248.2012.01807.x
Almagro M, Lopez J, Querejeta JI, Martinez-Mena M (2009) Temperature dependence of soil CO2 efflux is strongly modulated by seasonal patterns of moisture availability in a Mediterranean ecosystem. Soil Biol Biochem 41:594–605. https://doi.org/10.1016/j.soilbio.2008.12.021
Bader MK-F, Leuzinger S, Keel SG et al (2013) Central European hardwood trees in a high-CO2 future: synthesis of an 8-year forest canopy CO2 enrichment project. J Ecol 101:1509–1519. https://doi.org/10.1111/1365-2745.12149
Birch HF (1958) The effect of soil drying on humus decomposition and nitrogen availability. Plant Soil 10:9–31. https://doi.org/10.1007/BF01343734
Bond-Lamberty B, Thomson A (2010) A global database of soil respiration data. Biogeosciences 7:1915–1926. https://doi.org/10.5194/bg-7-1915-2010
Borken W, Matzner E (2009) Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soils. Glob Change Biol 15:808–824. https://doi.org/10.1111/j.1365-2486.2008.01681.x
Bottner P (1985) Response of microbial biomass to alternate moist and dry conditions in a soil incubated with 14C- and 15 N-labelled plant material. Soil Biol Biochem 17:329–337. https://doi.org/10.1016/0038-0717(85)90070-7
Bradford MA, Davies CA, Frey SD et al (2008) Thermal adaptation of soil microbial respiration to elevated temperature. Ecol Lett 11:1316–1327. https://doi.org/10.1111/j.1461-0248.2008.01251.x
Cable JM, Ogle K, Barron-Gafford GA et al (2013) Antecedent conditions influence soil respiration differences in shrub and grass patches. Ecosystems 16:1230–1247. https://doi.org/10.1007/s10021-013-9679-7
Chen X, Eamus D, Hutley LB (2002) Seasonal patterns of soil carbon dioxide efflux from a wet-dry tropical savanna of northern Australia. Aust J Bot 50:43–52. https://doi.org/10.1071/bt01049
Collins L, Boer MM, de Dios VR et al (2018) Effects of competition and herbivory over woody seedling growth in a temperate woodland trump the effects of elevated CO2. Oecologia. https://doi.org/10.1007/s00442-018-4143-1
Crous KY, Ósvaldsson A, Ellsworth DS (2015) Is phosphorus limiting in a mature Eucalyptus woodland? Phosphorus fertilisation stimulates stem growth. Plant Soil 391:293–305. https://doi.org/10.1007/s11104-015-2426-4
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 Change Biol 4:217–227. https://doi.org/10.1046/j.1365-2486.1998.00128.x
Davidson EA, Janssens IA, Luo Y (2006) On the variability of respiration in terrestrial ecosystems: moving beyond Q10. Glob Change Biol 12:154–164. https://doi.org/10.1111/j.1365-2486.2005.01065.x
Davidson EA, Samanta S, Caramori SS, Savage K (2012) The Dual Arrhenius and Michaelis–Menten kinetics model for decomposition of soil organic matter at hourly to seasonal time scales. Glob Change Biol 18:371–384. https://doi.org/10.1111/j.1365-2486.2011.02546.x
Dawes MA, Hagedorn F, Handa IT et al (2013) An alpine treeline in a carbon dioxide-rich world: synthesis of a nine-year free-air carbon dioxide enrichment study. Oecologia 171:623–637. https://doi.org/10.1007/s00442-012-2576-5
Dieleman WIJ, Janssens IA (2011) Can publication bias affect ecological research? A case study on soil respiration under elevated CO2. New Phytol 190:517–521. https://doi.org/10.1111/j.1469-8137.2010.03499.x
Drake JE, Stoy PC, Jackson RB, DeLUCIA EH (2008) Fine-root respiration in a loblolly pine (Pinus taeda L.) forest exposed to elevated CO2 and N fertilization. Plant Cell Environ 31:1663–1672. https://doi.org/10.1111/j.1365-3040.2008.01869.x
Drake JE, Gallet-Budynek A, Hofmockel KS et al (2011) Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2. Ecol Lett 14:349–357. https://doi.org/10.1111/j.1461-0248.2011.01593.x
Drake JE, Macdonald CA, Tjoelker MG et al (2016) Short-term carbon cycling responses of a mature eucalypt woodland to gradual stepwise enrichment of atmospheric CO2 concentration. Glob Change Biol 22:380–390. https://doi.org/10.1111/gcb.13109
Duursma RA, Gimeno TE, Boer MM et al (2016) Canopy leaf area of a mature evergreen Eucalyptus woodland does not respond to elevated atmospheric [CO2] but tracks water availability. Glob Change Biol 22:1666–1676. https://doi.org/10.1111/gcb.13151
Ellis RC (1969) The respiration of the soil beneath some Eucalyptus forest stands as related to the productivity of the stands. Soil Res 7:349–357. https://doi.org/10.1071/sr9690349
Ellsworth DS, Anderson IC, Crous KY et al (2017) Elevated CO2 does not increase eucalypt forest productivity on a low-phosphorus soil. Nat Clim Change 7:279–282. https://doi.org/10.1038/nclimate3235
Finzi AC, Raymer PCL, Giasson M-A, Orwig DA (2014) Net primary production and soil respiration in New England hemlock forests affected by the hemlock woolly adelgid. Ecosphere 5:1–16. https://doi.org/10.1890/ES14-00102.1
Giardina CP, Litton CM, Crow SE, Asner GP (2014) Warming-related increases in soil CO2 effux are explained by increased below-ground carbon flux. Nat Clim Change 4:822–827. https://doi.org/10.1038/NCLIMATE2322
Giasson M-A, Ellison AM, Bowden RD et al (2013) Soil respiration in a northeastern US temperate forest: a 22-year synthesis. Ecosphere 4:1–28. https://doi.org/10.1890/ES13.00183.1
Gimeno TE, Crous KY, Cooke J et al (2016) Conserved stomatal behaviour under elevated CO2 and varying water availability in a mature woodland. Funct Ecol 30:700–709. https://doi.org/10.1111/1365-2435.12532
Gimeno TE, McVicar TR, O’Grady AP et al (2018) Elevated CO2 did not affect the hydrological balance of a mature native Eucalyptus woodland. Glob Change Biol. https://doi.org/10.1111/gcb.14139
Göransson H, Godbold DL, Jones DL, Rousk J (2013) Bacterial growth and respiration responses upon rewetting dry forest soils: Impact of drought-legacy. Soil Biol Biochem 57:477–486. https://doi.org/10.1016/j.soilbio.2012.08.031
Hasegawa S, Macdonald CA, Power SA (2016) Elevated carbon dioxide increases soil nitrogen and phosphorus availability in a phosphorus-limited Eucalyptus woodland. Glob Change Biol 22:1628–1643. https://doi.org/10.1111/gcb.13147
Hendrey GR, Ellsworth DS, Lewin KF, Nagy J (1999) A free-air enrichment system for exposing tall forest vegetation to elevated atmospheric CO2. Glob Change Biol 5:293–309. https://doi.org/10.1046/j.1365-2486.1999.00228.x
Huxman TE, Cable JM, Ignace DD et al (2004) Response of net ecosystem gas exchange to a simulated precipitation pulse in a semi-arid grassland: the role of native versus non-native grasses and soil texture. Oecologia 141:295–305. https://doi.org/10.1007/s00442-003-1389-y
Keidel L, Kammann C, Gruenhage L et al (2015) Positive feedback of elevated CO2 on soil respiration in late autumn and winter. Biogeosciences 12:1257–1269. https://doi.org/10.5194/bg-12-1257-2015
Keith H, Jacobsen KL, Raison RJ (1997) Effects of soil phosphorus availability, temperature and moisture on soil respiration in Eucalyptus pauciflora forest. Plant Soil 190:127–141. https://doi.org/10.1023/A:1004279300622
Keith H, Leuning R, Jacobsen KL et al (2009) Multiple measurements constrain estimates of net carbon exchange by a Eucalyptus forest. Agric For Meteorol 149:535–558. https://doi.org/10.1016/j.agrformet.2008.10.002
King JS, Hanson PJ, Bernhardt E et al (2004) A multiyear synthesis of soil respiration responses to elevated atmospheric CO2 from four forest FACE experiments. Glob Change Biol 10:1027–1042. https://doi.org/10.1111/j.1529-8817.2003.00789.x
Lewin KF, Nagy J, Robert Nettles W et al (2009) Comparison of gas use efficiency and treatment uniformity in a forest ecosystem exposed to elevated [CO2] using pure and prediluted free-air CO2 enrichment technology. Glob Change Biol 15:388–395. https://doi.org/10.1111/j.1365-2486.2008.01748.x
Liu X, Wan S, Su B et al (2002) Response of soil CO2 efflux to water manipulation in a tallgrass prairie ecosystem. Plant Soil 240:213–223. https://doi.org/10.1023/A:1015744126533
Lloyd J, Taylor JA (1994) On the temperature dependence of soil respiration. Funct Ecol 8:315–323. https://doi.org/10.2307/2389824
Maier M, Schack-Kirchner H, Hildebrand EE, Holst J (2010) Pore-space CO2 dynamics in a deep, well-aerated soil. Eur J Soil Sci 61:877–887. https://doi.org/10.1111/j.1365-2389.2010.01287.x
Mildner M, Bader MK-F, Baumann C, Körner C (2015) Respiratory fluxes and fine root responses in mature Picea abies trees exposed to elevated atmospheric CO2 concentrations. Biogeochemistry 124:95–111. https://doi.org/10.1007/s10533-015-0084-5
Morton FI (1983) Operational estimates of areal evapotranspiration and their significance to the science and practice of hydrology. J Hydrol 66:1–76. https://doi.org/10.1016/0022-1694(83)90177-4
Nielsen UN, Prior S, Delroy B et al (2015) Response of belowground communities to short-term phosphorus addition in a phosphorus-limited woodland. Plant Soil 391:321–331. https://doi.org/10.1007/s11104-015-2432-6
Norby RJ, DeLucia EH, Gielen B et al (2005) Forest response to elevated CO2 is conserved across a broad range of productivity. Proc Natl Acad Sci USA 102:18052–18056. https://doi.org/10.1073/pnas.0509478102
Ochoa-Hueso R, Hughes J, Delgado-Baquerizo M et al (2017) Rhizosphere-driven increase in nitrogen and phosphorus availability under elevated atmospheric CO2 in a mature Eucalyptus woodland. Plant Soil 416:283–295. https://doi.org/10.1007/s11104-017-3212-2
Oishi AC, Palmroth S, Johnsen KH et al (2014) Sustained effects of atmospheric [CO2] and nitrogen availability on forest soil CO2 efflux. Glob Change Biol 20:1146–1160. https://doi.org/10.1111/gcb.12414
Palmroth S, Oren R, McCarthy HR et al (2006) Aboveground sink strength in forests controls the allocation of carbon below ground and its [CO2]-induced enhancement. Proc Natl Acad Sci 103:19362–19367. https://doi.org/10.1073/pnas.0609492103
Pathare VS, Crous KY, Cooke J et al (2017) Water availability affects seasonal CO2-induced photosynthetic enhancement in herbaceous species in a periodically dry woodland. Glob Change Biol. https://doi.org/10.1111/gcb.13778
Pendall E, Del Grosso S, King JY et al (2003) Elevated atmospheric CO2 effects and soil water feedbacks on soil respiration components in a Colorado grassland. Glob Biogeochem Cycles 17:1046. https://doi.org/10.1029/2001GB001821
Phillips RP, Finzi AC, Bernhardt ES (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–194. https://doi.org/10.1111/j.1461-0248.2010.01570.x
Pinheiro J, Bates D, Debroy S, Sarkar D (2011) nlme: Linear and Nonlinear Mixed Effects Models. R Package Version 31-109.
R Development Core Team (2012) R: a languange and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Raich JW, Potter CS (1995) Global patterns of carbon dioxide emissions from soils. Glob Biogeochem Cycles 9:23–36. https://doi.org/10.1029/94GB02723
Raich JW, Potter CS, Bhagawati D (2002) Interannual variability in global soil respiration, 1980–94. Glob Change Biol 8:800–812. https://doi.org/10.1046/j.1365-2486.2002.00511.x
Ryan EM, Ogle K, Zelikova TJ et al (2015) Antecedent moisture and temperature conditions modulate the response of ecosystem respiration to elevated CO2 and warming. Glob Change Biol 21:2588–2602. https://doi.org/10.1111/gcb.12910
Savage KE, Davidson EA (2003) A comparison of manual and automated systems for soil CO2 flux measurements: trade-offs between spatial and temporal resolution. J Exp Bot 54:891–899. https://doi.org/10.1093/jxb/erg121
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, Andrews JA (2000) Soil respiration and the global carbon cycle. Biogeochemistry 48:7–20. https://doi.org/10.1023/A:1006247623877
Selsted MB, van der Linden L, Ibrom A et al (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 Change Biol 18:1216–1230. https://doi.org/10.1111/j.1365-2486.2011.02634.x
van Groenigen KJ, Qi X, Osenberg CW et al (2014) Faster decomposition under increased atmospheric CO2 limits soil carbon storage. Science. https://doi.org/10.1126/science.1249534
Wan S, Norby RJ, Ledford J, Weltzin JF (2007) Responses of soil respiration to elevated CO2, air warming, and changing soil water availability in a model old-field grassland. Glob Change Biol 13:2411–2424. https://doi.org/10.1111/j.1365-2486.2007.01433.x
Warren CR (2014) Response of organic N monomers in a sub-alpine soil to a dry–wet cycle. Soil Biol Biochem 77:233–242. https://doi.org/10.1016/j.soilbio.2014.06.028
Yan L, Chen S, Xia J, Luo Y (2014) Precipitation regime shift enhanced the rain pulse effect on soil respiration in a semi-arid steppe. PLoS ONE 9:e104217. https://doi.org/10.1371/journal.pone.0104217
Zaragoza-Castells J, Sánchez-Gómez D, Hartley IP et al (2008) Climate-dependent variations in leaf respiration in a dry-land, low productivity Mediterranean forest: the importance of acclimation in both high-light and shaded habitats. Funct Ecol 22:172–184. https://doi.org/10.1111/j.1365-2435.2007.01355.x
Acknowledgements
We thank Steven Wohl, Vinod Kumar, Craig McNamara, and Craig Barton (Western Sydney University) for running all technical aspects of the EucFACE facility. We thank Angelica Vårhammer, Loïc Nazaries, and Jasmine Grinyer (Western Sydney University) for their contribution to the Rsoil measurements. EucFACE is an initiative supported by the Australian Government through the Education Investment Fund, the Department of Industry and Science, and the Australian Research Council in partnership with Western Sydney University. Facilities at EucFACE were built as an initiative of the Australian Government as part of the Nation-building Economic Stimulus Package.
Author information
Authors and Affiliations
Contributions
JED co-designed the Rsoil study, led the data collection and analysis, and led the writing. CM made a large contribution to the design of the Rsoil study and data collection, and assisted with writing. MGT assisted in the design of the EucFACE experiment and the Rsoil study, and contributed to data analysis and writing. PBR and BKS assisted with writing and the design of the EucFACE experiment and the Rsoil study. DSE led the design and implementation of the EucFACE experiment, contributed to the design of the Rsoil study, and assisted with writing.
Corresponding author
Additional information
Responsible Editor: Egbert Matzner.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Drake, J.E., Macdonald, C.A., Tjoelker, M.G. et al. Three years of soil respiration in a mature eucalypt woodland exposed to atmospheric CO2 enrichment. Biogeochemistry 139, 85–101 (2018). https://doi.org/10.1007/s10533-018-0457-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10533-018-0457-7