Ecosystems

, Volume 14, Issue 1, pp 156–167 | Cite as

Plants Mediate the Sensitivity of Soil Respiration to Rainfall Variability

  • Zachary T. Aanderud
  • Donald R. SchoolmasterJr.
  • Jay T. Lennon
Article

Abstract

Soil respiration from grasslands plays a critical role in determining carbon dioxide (CO2) feedbacks between soils and the atmosphere. In these often mesic systems, soil moisture and temperature tend to co-regulate soil respiration. Increasing variance of rainfall patterns may alter aboveground–belowground interactions and have important implications for the sensitivity of soil respiration to fluctuations in moisture and temperature. We conducted a set of field experiments to evaluate the independent and interactive effects of rainfall variability and plant–soil processes on respiration dynamics. Plant removal had strong effects on grassland soils, which included altered CO2 flux owing to absence of root respiration; increased soil moisture and temperature; and reduced availability of dissolved organic carbon (DOC) for heterotrophic respiration by microorganisms. These plant-mediated effects interacted with our rainfall variability treatments to determine the sensitivity of soil respiration to both moisture and temperature. Using time-series multiple regression, we found that plants dampened the sensitivity of respiration to moisture under high variability rainfall treatments, which may reflect the relative stability of root contributions to total soil respiration. In contrast, plants increased the sensitivity of respiration to temperature under low variability rainfall treatment suggesting that the environmental controls on soil CO2 dynamics in mesic habitats may be context dependent. Our results provide insight into the aboveground–belowground mechanisms controlling respiration in grasslands under variable rainfall regimes, which may be important for predicting CO2 dynamics under current and future climate scenarios.

Key words

CO2 heterotrophic respiration pulse root respiration time-series sensors microbial climate change precipitation 

Supplementary material

10021_2010_9401_MOESM1_ESM.pdf (314 kb)
(PDF 315 kb)

References

  1. 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.CrossRefGoogle Scholar
  2. Ambus P, Robertson GP. 2006. The effect of increased N deposition on nitrous oxide, methane, and carbon dioxide fluxes from unmanaged forest and grassland communities in Michigan. Biogeochemistry 79:315–37.CrossRefGoogle Scholar
  3. Anderson JM. 1973. Carbon dioxide evolution from two temperate, deciduous woodland soils. J Appl Ecol 10:361–78.CrossRefGoogle Scholar
  4. Atkin OK, Bruhn D, Hurry VM, Tjoelker MG. 2005. The hot and the cold: unravelling the variable response of plant respiration to temperature. Funct Plant Biol 32:87–105.CrossRefGoogle Scholar
  5. Bartholomew WV, Broadbent FE. 1950. Apparatus for control of moisture, temperature, and air composition in microbiological respiration experiments. Soil Sci Soc Am J 14:156–60.CrossRefGoogle Scholar
  6. Bence JR. 1995. Analysis of short time series: correcting for autocorrelation. Ecology 76:628–39.CrossRefGoogle Scholar
  7. Boone RD, Nadelhoffer KJ, Canary JD, Kaye JP. 1998. Roots exert a strong influence on the temperature sensitivity of soil respiration. Nature 396:570–2.CrossRefGoogle Scholar
  8. Borken W, Matzner E. 2009. Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soils. Glob Chang Biol 15:808–24.CrossRefGoogle Scholar
  9. 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 11:961–79.CrossRefGoogle Scholar
  10. 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:G02022.CrossRefGoogle Scholar
  11. Cardon ZG, Gage DJ. 2006. Resource exchange in the rhizosphere: molecular tools and the microbial perspective. Annu Rev Ecol Evol Syst 37:459–88.CrossRefGoogle Scholar
  12. Carpenter SR. 1990. Large-scale perturbations: opportunities for innovation. Ecology 71:2038–43.CrossRefGoogle Scholar
  13. Cisneros-Dozal LM, Trumbore S, Hanson PJ. 2006. Partitioning sources of soil-respired CO2 and their seasonal variation using a unique radiocarbon tracer. Glob Chang Biol 12:194–204.CrossRefGoogle Scholar
  14. Cleveland CC, Nemergut DR, Schmidt SK, Townsend AR. 2007. Increases in soil respiration following labile carbon additions linked to rapid shifts in soil microbial community composition. Biogeochemistry 82:229–40.CrossRefGoogle Scholar
  15. Conant RT, Dalla-Betta P, Klopatek CC, Klopatek JA. 2004. Controls on soil respiration in semiarid soils. Soil Biol Biochem 36:945–51.CrossRefGoogle Scholar
  16. Cook FJ, Orchard VA. 2008. Relationships between soil respiration and soil moisture. Soil Biol Biochem 40:1013–18.CrossRefGoogle Scholar
  17. Cottingham KL, Lennon JT, Brown BL. 2005. Designing more informative ecological experiments. Front Ecol Environ 3:145–52.CrossRefGoogle Scholar
  18. Crow SE, Wieder RK. 2005. Sources of CO2 emission from a northern peatland: root respiration, exudation, and decomposition. Ecology 86:1825–34.CrossRefGoogle Scholar
  19. Daly E, Oishi CA, Porporato A, Katul GG. 2008. A stochastic model for daily subsurface CO2 concentration and related soil respiration. Adv Water Resour 31:987–94.CrossRefGoogle Scholar
  20. 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 4:217–27.CrossRefGoogle Scholar
  21. Davidson EA, Janssens IA. 2006. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–73.CrossRefPubMedGoogle Scholar
  22. Davidson EA, Janssens IA, Luo YQ. 2006. On the variability of respiration in terrestrial ecosystems: moving beyond Q10. Glob Chang Biol 12:154–64.CrossRefGoogle Scholar
  23. Diggle PJ. 1990. Time series: a biostatistical introduction. Oxford: Oxford University Press.Google Scholar
  24. Fay PA, Carlisle JD, Knapp AK, Blair JM, Collins SL. 2000. Altering rainfall timing and quantity in a mesic grassland ecosystem: design and performance of rainfall manipulation shelters. Ecosystems 3:308–19.CrossRefGoogle Scholar
  25. Fay PA, Kaufman DM, Nippert JB, Carlisle JD, Harper CW. 2008. Changes in grassland ecosystem function due to extreme rainfall events: implications for responses to climate change. Glob Chang Biol 14:1600–8.CrossRefGoogle Scholar
  26. Fierer N, Schimel JP. 2003. A proposed mechanism for the pulse in carbon dioxide production commonly observed following the rapid rewetting of a dry soil. Soil Sci Soc Am J 67:798–805.CrossRefGoogle Scholar
  27. Frey SD. 2007. Spatial distribution of soil organisms. In: Ecology Biochemistry, Paul EA, Eds. Soil microbiology. London: Academic Press. Google Scholar
  28. Gu LH, Hanson PJ, Mac Post W, Liu Q. 2008. A novel approach for identifying the true temperature sensitivity from soil respiration measurements. Glob Biogeochem Cycles 22:GB4009.CrossRefGoogle Scholar
  29. Halverson LJ, Jones TM, Firestone MK. 2000. Release of intracellular solutes by four soil bacteria exposed to dilution stress. Soil Sci Soc Am J 64:1630–7.CrossRefGoogle Scholar
  30. Hanson PJ, Edwards NT, Garten CT, Andrews JA. 2000. Separating root and soil microbial contributions to soil respiration: a review of methods and observations. Biogeochemistry 48:115–46.CrossRefGoogle Scholar
  31. Harper CW, Blair JM, Fay PA, Knapp AK, Carlisle JD. 2005. Increased rainfall variability and reduced rainfall amount decreases soil CO2 flux in a grassland ecosystem. Glob Chang Biol 11:322–34.CrossRefGoogle Scholar
  32. IPCC. 2007. Climate change 2007: the scientific basis. Cambridge, UK: Cambridge Press.Google Scholar
  33. Jenkinson DS, Adams DE, Wild A. 1991. Model estimates of CO2 emissions from soil in response to global warming. Nature 351:304–6.CrossRefGoogle Scholar
  34. Jobbagy EG, Jackson RB. 2000. The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423–36.CrossRefGoogle Scholar
  35. Knapp AK, Fay PA, Blair JM, Collins SL, Smith MD, Carlisle JD, Harper CW, Danner BT, Lett MS, McCarron JK. 2002. Rainfall variability, carbon cycling, and plant species diversity in a mesic grassland. Science 298:2202–5.CrossRefPubMedGoogle Scholar
  36. Knapp AK, Beier C, Briske DD, Classen AT, Luo Y, Reichstein M, Smith MD, Smith SD, Bell JE, Fay PA, Heisler JL, Leavitt SW, Sherry R, Smith B, Weng E. 2008. Consequences of more extreme precipitation regimes for terrestrial ecosystems. Bioscience 58:811–21.CrossRefGoogle Scholar
  37. Lauenroth WK, Bradford JB. 2006. Ecohydrology and the partitioning AET between transpiration and evaporation in a semiarid steppe. Ecosystems 9:756–67.CrossRefGoogle Scholar
  38. Lee X, Wu HJ, Sigler J, Oishi C, Siccama T. 2004. Rapid and transient response of soil respiration to rain. Glob Chang Biol 10:1017–26.CrossRefGoogle Scholar
  39. Liu XZ, Wan SQ, Su B, Hui DF, Luo YQ. 2002. Response of soil CO2 efflux to water manipulation in a tallgrass prairie ecosystem. Plant Soil 240:213–23.CrossRefGoogle Scholar
  40. Liu WX, Zhang Z, Wan SQ. 2009. Predominant role of water in regulating soil and microbial respiration and their responses to climate change in a semiarid grassland. Glob Chang Biol 15:184–95.CrossRefGoogle Scholar
  41. Ljung GM, Box EP. 1978. On a measure of lack of fit in time series models. Biometrika 65:297–303.CrossRefGoogle Scholar
  42. Livingston GP, Hutchinson GL. 1995. Enclosure-based measurement of trace gas exchange: applications and sources of error. In: Matson PA, Harriss RC, Eds. Biogenic trace gases: measuring emissions from soil, water. Osney Mead, Oxford, UK: Blackwell Science. p 14–51.Google Scholar
  43. Lloyd J, Taylor JA. 1994. On the temperature-dependence of soil respiration. Funct Ecol 8:315–23.CrossRefGoogle Scholar
  44. Miao S, Carstenn S. 2006. A new direction for large-scale experimental design and analysis. Front Ecol Environ 4:227.CrossRefGoogle Scholar
  45. Noormets A, Desai AR, Cook BD, Euskirchen ES, Ricciuto DM, Davis KJ, Bolstad PV, Schmid HP, Vogel CV, Carey EV, Su HB, Chen J. 2008. Moisture sensitivity of ecosystem respiration: comparison of 14 forest ecosystems in the Upper Great Lakes Region, USA. Agric For Meteorol 148:216–30.CrossRefGoogle Scholar
  46. Pole A, West M, Harrison J. 1994. Applied Bayesian forecasting and time series analysis. New York: Chapman-Hall.Google Scholar
  47. Raich JW, Potter CS. 1995. Global patterns of carbon-dioxide emissions from soils. Glob Biogeochem Cycles 9:23–36.CrossRefGoogle Scholar
  48. 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 34:L17404.CrossRefGoogle Scholar
  49. Robertson GP, Paul EA, Harwood RR. 2000. Greenhouse gases in intensive agriculture: contributions of individual gases to the radiative forcing of the atmosphere. Science 289:1922–5.CrossRefPubMedGoogle Scholar
  50. Schimel J, Balser TC, Wallenstein M. 2007. Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–94.CrossRefPubMedGoogle Scholar
  51. Schlesinger WH. 1997. Biogeochemistry, an analysis of global change. San Diego: Academic Press.Google Scholar
  52. Scott-Denton LE, Rosenstiel TN, Monson RK. 2006. Differential controls by climate and substrate over the heterotrophic and rhizospheric components of soil respiration. Glob Chang Biol 12:205–16.CrossRefGoogle Scholar
  53. Shim JH, Pendall E, Morgan JA, Ojima DS. 2009. Wetting and drying cycles drive variations in the stable carbon isotope ratio of respired carbon dioxide in semi-arid grassland. Oecologia 160:321–33.CrossRefPubMedGoogle Scholar
  54. Sponseller RA. 2007. Precipitation pulses and soil CO2 flux in a Sonoran Desert ecosystem. Glob Chang Biol 13:426–36.CrossRefGoogle Scholar
  55. Tang JW, Baldocchi DD, Qi Y, Xu LK. 2003. Assessing soil CO2 efflux using continuous measurements of CO2 profiles in soils with small solid-state sensors. Agric For Meteorol 118:207–20.CrossRefGoogle Scholar
  56. Tang JW, Misson L, Gershenson A, Cheng WX, Goldstein AH. 2005. Continuous measurements of soil respiration with and without roots in a ponderosa pine plantation in the Sierra Nevada Mountains. Agric For Meteorol 132:212–27.CrossRefGoogle Scholar
  57. Trumbore S. 2006. Carbon respired by terrestrial ecosystems—recent progress and challenges. Glob Chang Biol 12:141–53.CrossRefGoogle Scholar
  58. van der Putten WH, Bardgett RD, de Ruiter PC, Hol WHG, Meyer KM, Bezemer TM, Bradford MA, Christensen S, Eppinga MB, Fukami T, Hemerik L, Molofsky J, Schadler M, Scherber C, Strauss SY, Vos M, Wardle DA. 2009. Empirical and theoretical challenges in aboveground-belowground ecology. Oecologia 161:1–14.CrossRefPubMedGoogle Scholar
  59. Wang W, Fang JY. 2009. Soil respiration and human effects on global grasslands. Glob Planet Change 67:20–8.CrossRefGoogle Scholar
  60. Weltzin JF, Loik ME, Schwinning S, Williams DG, Fay PA, Haddad BM, Harte J, Huxman TE, Knapp AK, Lin GH, Pockman WT, Shaw MR, Small EE, Smith MD, Smith SD, Tissue DT, Zak JC. 2003. Assessing the response of terrestrial ecosystems to potential changes in precipitation. Bioscience 53:941–52.CrossRefGoogle Scholar
  61. Wolfinger R, Chang M. 1999. Comparing the SAS GLM and MIXED Procedures for repeated measures. Cary, NC: SAS Institute, Inc.Google Scholar
  62. Xu LK, Baldocchi DD. 2004. Seasonal variation in carbon dioxide exchange over a Mediterranean annual grassland in California. Agric For Meteorol 123:79–96.CrossRefGoogle Scholar
  63. Yepez EA, Scott RL, Cable WL, Williams DG. 2007. Intraseasonal variation in water and carbon dioxide flux components in a semiarid riparian woodland. Ecosystems 10:1100–15.CrossRefGoogle Scholar
  64. Yuste JC, Baldocchi DD, Gershenson A, Goldstein A, Misson L, Wong S. 2007. Microbial soil respiration and its dependency on carbon inputs, soil temperature and moisture. Glob Chang Biol 13:2018–35.CrossRefGoogle Scholar
  65. Zhang XB, Zwiers FW, Hegerl GC, Lambert FH, Gillett NP, Solomon S, Stott PA, Nozawa T. 2007. Detection of human influence on twentieth-century precipitation trends. Nature 448:461–464.CrossRefPubMedGoogle Scholar
  66. Zobitz JM, Moore DJP, Sacks WJ, Monson RK, Bowling DR, Schimel DS. 2008. Integration of process-based soil respiration models with whole-ecosystem CO2 measurements. Ecosystems 11:250–69.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Zachary T. Aanderud
    • 1
    • 2
  • Donald R. SchoolmasterJr.
    • 1
  • Jay T. Lennon
    • 1
    • 3
  1. 1.W. K. Kellogg Biological StationMichigan State UniversityHickory CornersUSA
  2. 2.Department of Plant and Wildlife SciencesBrigham Young UniversityUtahUSA
  3. 3.Department of Microbiology and Molecular GeneticsMichigan State UniversityHickory CornersUSA

Personalised recommendations