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Biogeochemistry

, Volume 141, Issue 1, pp 63–73 | Cite as

Temperature sensitivity of soil respiration in a low-latitude forest ecosystem varies by season and habitat but is unaffected by experimental warming

  • Megan B. Machmuller
  • Ford Ballantyne
  • Daniel Markewitz
  • Aaron Thompson
  • Nina Wurzburger
  • Paul T. Frankson
  • Jacqueline E. Mohan
Article
  • 69 Downloads

Abstract

Experimental warming of forest ecosystems typically stimulates soil respiration (CO2 efflux), but most warming experiments have been conducted in northern latitudes (> 40°N) with relatively young soils. We quantified the influence of experimental warming on soil respiration (RT) in two adjacent forest habitats—a mature, closed canopy forest and a gap where trees were manually removed— on highly-weathered Ultisols of the southeastern U.S. (33°N). Using temperature variation, both natural and induced by experimental warming, we also quantified the temperature sensitivity of RT, defined as the activation energy, EA in the Arrhenius equation. Experimental warming (either + 3 °C or + 5 °C above ambient) did not significantly increase soil respiration rate or cumulative CO2 loss over the 3 years of the experiment, and did not influence the temperature sensitivity of soil respiration, once the influence of natural temperature variation was taken into consideration. Despite the absence of an experimental warming effect, we observed that EA varied on monthly time scales, and varied differently in each habitat. Soil moisture and habitat also influenced RT, but the effects were not consistent, and varied by month. Our results suggest that although RT does depend on temperature, the sensitivity of RT to temperature variation is influenced primarily by factors like microclimate and plant phenology that can change on relatively short (< monthly) time scales. Thus, using the temperature sensitivity of RT to predict future CO2 losses due to warming is only reasonable if monthly variation in EA is incorporated into models for lower-latitude subtropical ecosystems with highly weathered soils, such as those in this study. Finally, our results suggest that higher temperatures may not enhance RT in highly-weathered, C-poor soils to the extent that has been reported in prior studies of high-latitude soils, which may constrain ecosystem-atmosphere carbon exchanges and feedbacks to the climate system.

Keywords

Soil respiration Temperature sensitivity Soil carbon Soil organic matter Decomposition Warming Terrestrial carbon-climate feedback 

Notes

Acknowledgements

This work was supported in part by funding from NSF DEB-1242013, and support from the University of Georgia’s Office of the Vice-President for Research (OVPR). Analytical work was done in the UGA Odum School of Ecology Analytical Laboratory and Georgia Institute of Technology, Biochemistry Department. We thank the Warnell School of Forestry and Natural Resources for assistance with establishing and maintaining the project in Whitehall Forest.

Supplementary material

10533_2018_501_MOESM1_ESM.docx (8.5 mb)
Supplementary material 1 (DOCX 8697 kb)

References

  1. Allison SD, Treseder KK (2008) Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Glob Chang Biol 14(12):2898–2909CrossRefGoogle Scholar
  2. Arora VK, Boer GJ, Friedlingstein P, Eby M, Jones CD, Christian JR, Bonan G, Bopp L, Brovkin V, Cadule P (2013) Carbon–concentration and carbon–climate feedbacks in CMIP5 earth system models. J Clim 26(15):5289–5314CrossRefGoogle Scholar
  3. Arrhenius SZ (1889) Über die Reaktionsgeschwindigkeit bei der Inversion von Rohrzucker durch Säuren. Z Phys Chem 4:226–248Google Scholar
  4. Balser TC, Wixon DL (2009) Investigating biological control over soil carbon temperature sensitivity. Glob Chang Biol 15(12):2935–2949CrossRefGoogle Scholar
  5. Billings SA, Ballantyne F (2013) How interactions between microbial resource demands, soil organic matter stoichiometry, and substrate reactivity determine the direction and magnitude of soil respiratory responses to warming. Glob Chang Biol 19(1):90–102CrossRefGoogle Scholar
  6. Bradford MA, Davies CA, Frey SD, Maddox TR, Melillo JM, Mohan JE, Reynolds JF, Treseder KK, Wallenstein MD (2008) Thermal adaptation of soil microbial respiration to elevated temperature. Ecol Lett 11(12):1316–1327CrossRefGoogle Scholar
  7. Brzostek ER, Finzi AC (2012) Seasonal variation in the temperature sensitivity of proteolytic enzyme activity in temperate forest soils. J Geophys Res Biogeosci 117(G1):G01018CrossRefGoogle Scholar
  8. Carey JC, Tang J, Templer PH, Kroeger KD, Crowther TW, Burton AJ, Dukes JS, Emmett B, Frey SD, Heskel MA (2016) Temperature response of soil respiration largely unaltered with experimental warming. Proc Natl Acad Sci 113(48):13797–13802CrossRefGoogle Scholar
  9. Clark JS, Salk C, Melillo J, Mohan J (2014) Tree phenology responses to winter chilling, spring warming, at north and south range limits. Funct Ecol 28(6):1344–1355CrossRefGoogle Scholar
  10. Commane R, Lindaas J, Benmergui J, Luus KA, Chang RY-W, Daube BC, Euskirchen ES, Henderson JM, Karion A, Miller JB, Miller SM, Parazoo NC, Randerson JT, Sweeney C, Tans P, Thoning K, Veraverbeke S, Miller CE, Wofsy SC (2017) Carbon dioxide sources from Alaska driven by increasing early winter respiration from Arctic tundra. Proc Natl Acad Sci 114(21):5361–5366CrossRefGoogle Scholar
  11. Craine JM, Fierer N, McLauchlan KK (2010) Widespread coupling between the rate and temperature sensitivity of organic matter decay. Nat Geosci 3(12):854–857CrossRefGoogle Scholar
  12. Crews TE, Kitayama K, Fownes JH, Riley RH, Herbert DA, Mueller-Dombois D, Vitousek PM (1995) Changes in soil phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii. Ecology 76(5):1407–1424CrossRefGoogle Scholar
  13. Crowther TW, Bradford MA (2013) Thermal acclimation in widespread heterotrophic soil microbes. Ecol Lett 16(4):469–477CrossRefGoogle Scholar
  14. Crowther T, Todd-Brown K, Rowe C, Wieder W, Carey J, Machmuller M, Snoek B, Fang S, Zhou G, Allison S (2016) Quantifying global soil carbon losses in response to warming. Nature 540(7631):104–108CrossRefGoogle Scholar
  15. Davidson E, Janssens I (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440(7081):165–173CrossRefGoogle Scholar
  16. 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 Chang Biol 18(1):371–384CrossRefGoogle Scholar
  17. Easterling DR, Arnold J, Knutson T, Kunkel K, LeGrande A, Leung LR, Vose R, Waliser D, Wehner M (2017) Precipitation change in the United States. In: Wuebbles DJ, Fahey DW, Hibbard KA, Dokken DJ, Stewart BC, Maycock TK (eds) Climate science special report: fourth national climate assessment, vol 1. U.S. Global Change Research Program, Washington, DC, pp 301–335Google Scholar
  18. Friedlingstein P, Meinshausen M, Arora VK, Jones CD, Anav A, Liddicoat SK, Knutti R (2014) Uncertainties in CMIP5 climate projections due to carbon cycle feedbacks. J Clim 27(2):511–526CrossRefGoogle Scholar
  19. Hartley IP, Heinemeyer A, Ineson P (2007) Effects of three years of soil warming and shading on the rate of soil respiration: substrate availability and not thermal acclimation mediates observed response. Glob Chang Biol 13(8):1761–1770CrossRefGoogle Scholar
  20. Ito A, Wagai R (2017) Global distribution of clay-size minerals on land surface for biogeochemical and climatological studies. Sci Data 4:170103CrossRefGoogle Scholar
  21. Jobbagy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10(2):423–436CrossRefGoogle Scholar
  22. Karhu K, Auffret MD, Dungait JA, Hopkins DW, Prosser JI, Singh BK, Subke J-A, Wookey PA, Ågren GI, Sebastia M-T (2014) Temperature sensitivity of soil respiration rates enhanced by microbial community response. Nature 513(7516):81–84CrossRefGoogle Scholar
  23. Kirschbaum MUF (2004) Soil respiration under prolonged soil warming: are rate reductions caused by acclimation or substrate loss? Glob Chang Biol 10(11):1870–1877CrossRefGoogle Scholar
  24. Knorr W, Prentice I, House J, Holland E (2005) Long-term sensitivity of soil carbon turnover to warming. Nature 433(7023):298–301CrossRefGoogle Scholar
  25. Lloyd J, Taylor J (1994) On the temperature dependence of soil respiration. Funct Ecol 8:315–323CrossRefGoogle Scholar
  26. Lu M, Zhou X, Yang Q, Li H, Luo Y, Fang C, Chen J, Yang X, Li B (2013) Responses of ecosystem carbon cycle to experimental warming: a meta-analysis. Ecology 94(3):726–738CrossRefGoogle Scholar
  27. Luo Y, Wan S, Hui D, Wallace LL (2001) Acclimatization of soil respiration to warming in a tall grass prairie. Nature 413(6856):622–625CrossRefGoogle Scholar
  28. Machmuller MB, Mohan JE, Minucci JM, Phillips CA, Wurzburger N (2016) Season, but not experimental warming, affects the activity and temperature sensitivity of extracellular enzymes. Biogeochemistry 131(3):255–265CrossRefGoogle Scholar
  29. Mahecha MD, Reichstein M, Carvalhais N, Lasslop G, Lange H, Seneviratne SI, Vargas R, Ammann C, Arain MA, Cescatti A (2010) Global convergence in the temperature sensitivity of respiration at ecosystem level. Science 329(5993):838–840CrossRefGoogle Scholar
  30. Mearns L, Giorgi F, McDaniel L, Shields C (2003) Climate scenarios for the southeastern US based on GCM and regional model simulations. Clim Change 60(1):7–35CrossRefGoogle Scholar
  31. Meehl GA, Washington WM, Arblaster JM, Hu A, Teng H, Kay JE, Gettelman A, Lawrence DM, Sanderson BM, Strand WG (2013) Climate change projections in CESM1 (CAM5) compared to CCSM4. J Clim 26(17):6287–6308CrossRefGoogle Scholar
  32. Melillo J, Steudler P, Aber J, Newkirk K, Lux H, Bowles F, Catricala C, Magill A, Ahrens T, Morrisseau S (2002) Soil warming and carbon-cycle feedbacks to the climate system. Science 298(5601):2173CrossRefGoogle Scholar
  33. Melillo JM, Frey SD, DeAngelis KM, Werner WJ, Bernard MJ, Bowles FP, Pold G, Knorr MA, Grandy AS (2017) Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world. Science 358(6359):101–105CrossRefGoogle Scholar
  34. 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
  35. NOAA (2013) National oceanic and atmospheric administration. National climate data center, Athens, Georgia, Ben Epps Airport Climate StationGoogle Scholar
  36. NRCS Soil Survey Staff (2014) Natural Resources Conservation Service, United States Department of Agriculture. http://websoilsurvey.nrcs.usda.gov/. Accessed May 2014
  37. Peterjohn W, Melillo J, Bowles F, Steudler P (1993) Soil warming and trace gas fluxes: experimental design and preliminary flux results. Oecologia 93(1):18–24CrossRefGoogle Scholar
  38. Rustad L, Campbell J, Marion G, Norby R, Mitchell M, Hartley A, Cornelissen J, Gurevitch J (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126(4):543–562CrossRefGoogle Scholar
  39. Schlesinger WH, Bernhardt ES (2013) Biogeochemistry: an analysis of global change, 3rd edn. Elsevier Science, Maryland Height, MOGoogle Scholar
  40. Serreze MC, Barry RG (2011) Processes and impacts of Arctic amplification: a research synthesis. Glob Planet Change 77(1):85–96CrossRefGoogle Scholar
  41. Sulman BN, Phillips RP, Oishi AC, Shevliakova E, Pacala SW (2014) Microbe-driven turnover offsets mineral-mediated storage of soil carbon under elevated CO2. Nat Clim Change 4(12):1099CrossRefGoogle Scholar
  42. Suseela V, Dukes JS (2013) The responses of soil and rhizosphere respiration to simulated climatic changes vary by season. Ecology 94(2):403–413CrossRefGoogle Scholar
  43. 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.  https://doi.org/10.1111/j.1365-2486.2011.02516.x CrossRefGoogle Scholar
  44. Tjoelker MG, Oleksyn J, Reich PB (2001) Modelling respiration of vegetation: evidence for a general temperature-dependent Q10. Glob Chang Biol 7(2):223–230CrossRefGoogle Scholar
  45. Van Dooremalen C, Berg MP, Ellers J (2013) Acclimation responses to temperature vary with vertical stratification: implications for vulnerability of soil-dwelling species to extreme temperature events. Glob Chang Biol 19(3):975–984CrossRefGoogle Scholar
  46. Vanderwel MC, Slot M, Lichstein JW, Reich PB, Kattge J, Atkin OK, Bloomfield KJ, Tjoelker MG, Kitajima K (2015) Global convergence in leaf respiration from estimates of thermal acclimation across time and space. New Phytol 207(4):1026–1037CrossRefGoogle Scholar
  47. Vasconcelos SS, Zarin DJ, Capanu M, Littell R, Davidson EA, Ishida FY, Santos EB, Araújo MM, Aragão DV, Rangel-Vasconcelos LG (2004) Moisture and substrate availability constrain soil trace gas fluxes in an eastern Amazonian regrowth forest. Glob Biogeochem Cycles 18(2):GB2009CrossRefGoogle Scholar
  48. Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20(1):5–15CrossRefGoogle Scholar
  49. Vose RS, Easterling DR, Kunkel KE, LeGrande AN, Wehner MF (2017) Temperature changes in the United States. In: Wuebbles DJ, Fahey DW, Hibbard KA, Dokken DJ, Stewart BC, Maycock TK (eds) Climate science special report: fourth national climate assessment, vol 1. U.S. Global Change Research Program, Washington, DC, pp 185–206Google Scholar
  50. Wallenstein MD, Mcmahon SK, Schimel JP (2009) Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils. Glob Chang Biol 15(7):1631–1639CrossRefGoogle Scholar
  51. Wan S, Hui D, Wallace L, Luo Y (2005) Direct and indirect effects of experimental warming on ecosystem carbon processes in a tallgrass prairie. Glob Biogeochem Cycles 19(2):GB2014CrossRefGoogle Scholar
  52. Wan S, Norby RJ, Ledford J, Weltzin J (2007) Responses of soil respiration to elevated CO2, air warming, and changing soil water availability in a model old-field grassland. Glob Chang Biol 13(11):2411–2424CrossRefGoogle Scholar
  53. Wu Z, Dijkstra P, Koch GW, Penuelas J, Hungate BA (2011) Responses of terrestrial ecosystems to temperature and precipitation change: a meta-analysis of experimental manipulation. Glob Chang Biol 17(2):927–942CrossRefGoogle Scholar
  54. Yang X, Post WM (2011) Phosphorus transformations as a function of pedogenesis: a synthesis of soil phosphorus data using Hedley fractionation method. Biogeosciences 8(10):2907–2916CrossRefGoogle Scholar
  55. Yvon-Durocher G, Caffrey JM, Cescatti A, Dossena M, Giorgio Pd, Gasol JM, Montoya JM, Pumpanen J, Staehr PA, Trimmer M, Woodward G, Allen AP (2012) Reconciling the temperature dependence of respiration across timescales and ecosystem types. Nature 487:472CrossRefGoogle Scholar
  56. Zhou X, Sherry RA, An Y, Wallace LL, Luo Y (2006) Main and interactive effects of warming, clipping, and doubled precipitation on soil CO2 efflux in a grassland ecosystem. Glob Biogeochem Cycles 20(1):GB1003CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Megan B. Machmuller
    • 1
  • Ford Ballantyne
    • 2
  • Daniel Markewitz
    • 3
  • Aaron Thompson
    • 2
    • 4
  • Nina Wurzburger
    • 2
  • Paul T. Frankson
    • 2
  • Jacqueline E. Mohan
    • 2
  1. 1.Natural Resource Ecology LaboratoryColorado State UniversityFort CollinsUSA
  2. 2.Odum School of EcologyUniversity of GeorgiaAthensUSA
  3. 3.Warnell School of Forestry and Natural ResourcesUniversity of GeorgiaAthensUSA
  4. 4.Crop and Soil SciencesUniversity of GeorgiaAthensUSA

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