Skip to main content
SpringerLink
Log in

Responses of Soil, Heterotrophic, and Autotrophic Respiration to Experimental Open-Field Soil Warming in a Cool-Temperate Deciduous Forest

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

How global warming will affect soil respiration (R S) and its source components is poorly understood despite its importance for accurate prediction of global carbon (C) cycles. We examined the responses of R S, heterotrophic respiration (R H), autotrophic respiration (R A), nitrogen (N) availability, and fine-root biomass to increased temperature in an open-field soil warming experiment. The experiment was conducted in a cool-temperate deciduous forest ecosystem in northern Japan. As this forest is subjected to strong temporal variation in temperature, on scales ranging from daily to seasonal, we also investigated the temporal variation in the effects of soil warming on R S, R H, and R A. Soil temperature was continuously elevated by about 4.0°C from 2007 to 2014 using heating wires buried in the soil, and we measured soil respiratory processes in all four seasons from 2012 to 2014. Soil warming increased annual R S by 32–45%, but the magnitude of the increase was different between the components: R H and R A were also stimulated, and increased by 39–41 and 17–18%, respectively. Soil N availability during the growing season and fine-root biomass were not remarkably affected by the warming treatment. We found that the warming effects varied seasonally. R H increased significantly throughout the year, but the warming effect showed remarkable seasonal differences, with the maximum stimulation in the spring. This suggests that warmer spring temperature will produce a greater increase in CO2 release than warmer summer temperatures. In addition, we found that soil warming reduced the temperature sensitivity (Q 10) of R S. Although the Q 10 of both R H and R A tended to be reduced, the decrease in the Q 10 of R S was caused mainly by a decrease in the response of R A to warming. These long-term results indicate that a balance between the rapid and large response of soil microbes and the acclimation of plant roots both play important roles in determining the response of R S to soil warming, and must be carefully considered to predict the responses of soil C dynamics under future temperature conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  • Atkin OK, Tjoelker MG. 2003. Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci 8:343–51.

    Article  CAS  PubMed  Google Scholar 

  • Allison SD, Treseder KK. 2008. Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Glob Change Biol 14:2898–909.

    Article  Google Scholar 

  • Bekku Y, Koizumi H, Nakadai T, Iwaki H. 1995. Measurement of soil respiration using closed chamber method: an IRGA technique. Ecol Res 10:369–73.

    Article  Google Scholar 

  • Binkley D, Matson P. 1983. Ion exchange resin bag method for assessing forest soil nitrogen availability. Soil Sci Soc Am J 47:1050–2.

    Article  CAS  Google Scholar 

  • Bonan GB, Van Cleve K. 1992. Soil temperature, nitrogen mineralization, and carbon source-sink relationships in boreal forests. Can J For Res 22:629–39.

    Article  CAS  Google Scholar 

  • Bond-Lamberty B, Bronson D, Bladyka E, Gower ST. 2011. A comparison of trenched plot techniques for partitioning soil respiration. Soil Biol Biochem 43:2108–14.

    Article  CAS  Google Scholar 

  • Bond-Lamberty B, Thomson A. 2010. Temperature-associated increases in the global soil respiration record. Nature 464:579–82.

    Article  CAS  PubMed  Google Scholar 

  • 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 11:1316–27.

    Article  PubMed  Google Scholar 

  • Bronson DR, Gower ST, Tanner N, Linder S, Van Herk I. 2008. Response of soil surface CO2 flux in a boreal forest to ecosystem warming. Glob Change Biol 14:856–67.

    Article  Google Scholar 

  • Chen X, Post WM, Norby RJ, Classen AT. 2011. Modeling soil respiration and variations in source components using a multi-factor global climate change experiment. Clim Change 107:459–80.

    Article  CAS  Google Scholar 

  • Chung H, Muraoka H, Nakamura N, Han S, Muller O, Son Y. 2013. Experimental warming studies on tree species and forest ecosystems: a literature review. J Plant Res 126:447–60.

    Article  PubMed  Google Scholar 

  • Contosta AR, Frey SD, Cooper AB. 2011. Seasonal dynamics of soil respiration and N mineralization in chronically warmed and fertilized soils. Ecosphere 2:art36.

    Article  Google Scholar 

  • Curiel Yuste J, Janssens JA, Carrara A, Ceulemans R. 2004. Annual Q10 of soil respiration reflect plant phenological patterns as well as temperature sensitivity. Glob Change Biol 10:161–9.

    Article  Google Scholar 

  • Curiel Yuste J, Ma S, Baldocchi DD. 2010. Plant-soil interactions and acclimation to temperature of microbial-mediated soil respiration may affect prediction of soil CO2 efflux. Biogeochemistry 98:127–38.

    Article  CAS  Google Scholar 

  • Davidson EA, Janssens IA. 2006. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–73.

    Article  CAS  PubMed  Google Scholar 

  • Díaz-Pinés E, Schindlbacher A, Pfeffer M, Jandl R, Zechmeister-Boltenstern S, Rubio A. 2010. Root trenching: a useful tool to estimate autotrophic soil respiration? A case study in an Austrian mountain forest. Eur J Forest Res 129:101–9.

    Article  Google Scholar 

  • Dieleman WIJ, Vicca S, Dijkstra FA, Hagedorn F, Hovenden MJ, Larsen KS, Morgan JA, Volder A, Beier C, Dukes JS, King J, Leuzinger S, Linder S, Luo Y, Oren R, de Angelis P, Tingey D, Hoosbeek MR, Janssens IA. 2012. Simple additive effects are rare: a quantitative review of plant biomass and soil process responses to combined manipulations of CO2 and temperature. Glob Change Biol 18:2681–93.

    Article  Google Scholar 

  • Du E, Fang J. 2014. Linking belowground and aboveground phenology in two boreal forests in Northeast China. Oecologia 176:883–92.

    Article  PubMed  Google Scholar 

  • Eliasson PE, Mcmurtrie RE, Pepper DA, Strömgren M, Linder S, Ågren GI. 2005. The response of heterotrophic CO2 flux to soil warming. Glob Change Biol 11:167–81.

    Article  Google Scholar 

  • Gomez-Casanovas N, Matamala R, Cook DR, Gonzalez-Meler MA. 2012. Net ecosystem exchange modifies the relationship between the autotrophic and heterotrophic components of soil respiration with abiotic factors in prairie grasslands. Glob Change Biol 18:2532–45.

    Article  Google Scholar 

  • Hagedorn F, Martin M, Rixen C, Rusch S, Bebi P, Zürcher A, Siegwolf RTW, Wipf S, Escape C, Roy J, Hättenschwiler S. 2010. Short-term responses of ecosystem carbon fluxes to experimental soil warming at the Swiss alpine treeline. Biogeochemistry 97:7–19.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Houghton RA. 2003. Revised estimates of the annual net flux of carbon to the atmosphere from changes in land use and land management 1850-2000. Tellus B 55:378–90.

    Article  Google Scholar 

  • IPCC. 2013. Climate change 2013: the physical science basis. Contribution of Working Group I to the fifth assessment report of the intergovernmental panel on climate change. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM, Eds. Cambridge: Cambridge University Press. pp. 1029–1136.

  • Ishioka R, Muller O, Hiura T, Kudo G. 2013. Responses of leafing phenology and photosynthesis to soil warming in forest-floor plants. Acta Oecol 51:34–41.

    Article  Google Scholar 

  • Janssens IA, Pilegaard K. 2003. Large seasonal changes in Q10 of soil respiration in a beech forest. Glob Change Biol 9:911–18.

    Article  Google Scholar 

  • Jarvi MP, Burton AJ. 2013. Acclimation and soil moisture constrain sugar maple root respiration in experimentally warmed soil. Tree Physiol 33:949–59.

    Article  CAS  PubMed  Google Scholar 

  • Kirschbaum MUF. 2004. Soil respiration under prolonged soil warming: are rate reductions caused by acclimation or substrate loss? Glob Change Biol 10:1870–7.

    Article  Google Scholar 

  • Kirschbaum MUF. 2013. Seasonal variations in the availability of labile substrate confound the temperature dependence of organic matter decomposition. Soil Biol Biochem 57:568–76.

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Gavrichkova O. 2010. Time lag between photosynthesis and carbon dioxide efflux from soil: a review of mechanisms and controls. Glob Change Biol 16:3386–406.

    Article  Google Scholar 

  • Lee MS, Nakane K, Nakatsubo T, Koizumi H. 2003. Seasonal changes in the contribution of root respiration to total soil respiration in a cool-temperate deciduous forest. Plant Soil 255:311–18.

    Article  CAS  Google Scholar 

  • Li DJ, Zhou XH, Wu LY, Zhou JH, Luo Y. 2013. Contrasting responses of heterotrophic and autotrophic respiration to experimental warming in a winter annual-dominated prairie. Glob Change Biol 19:3553–64.

    Google Scholar 

  • 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 94:726–38.

    Article  PubMed  Google Scholar 

  • Luo YQ, Wan SQ, Hui DF, Wallace LL. 2001. Acclimatization of soil respiration to warming in a tall grass prairie. Nature 413:622–5.

    Article  CAS  PubMed  Google Scholar 

  • Melillo JM, Butler S, Johnson J, Mohan J, Steudler P, Lux H, Burrows E, Bowles R, Smith R, Scott L, Vario C, Hill T, Burton A, Zhou YM, Tang J. 2011. Soil warming, carbon-nitrogen interactions, and forest carbon budgets. Proc Natl Acad Sci 108:9508–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Melillo JM, Steudler PA, Aber JD, Newkirk Lux H, Bowles FP, Catricala C, Magill A, Ahrens T, Morrisseau S. 2002. Soil warming and carbon-cycle feedbacks to the climate system. Science 298:2173–6.

    Article  CAS  PubMed  Google Scholar 

  • Mo W, Lee MS, Uchida M, Inatomi M, Saigusa N, Mariko S, Koizumi H. 2005. Seasonal and annual variations in soil respiration in a cool-temperate deciduous broad-leaved forest in Japan. Agric For Meteorol 134:81–94.

    Article  Google Scholar 

  • Muraoka H, Noda HM, Nagai S, Motohka T, Saitoh TM, Nasahara KN, Saigusa N. 2013. Spectral vegetation indices as the indicator of canopy photosynthetic productivity in a deciduous broadleaf forest. J Plant Ecol 6:393–407.

    Article  Google Scholar 

  • Nakamura M, Nakaji T, Muller O, Hiura T. 2014. Different initial responses of the canopy herbivory rate in mature oak trees to experimental soil and branch warming in a soil-freezing area. Oikos 124:1071–7.

    Article  Google Scholar 

  • Noh NJ, Chung H, Ryu SR, Son Y, Lee SK, Yoon TK, Yang AR, Kim J. 2012. Changes in soil properties of Abies holophylla and Quercus-dominated stands 4 years after trenching. Scand J For Res 27:597–604.

    Article  Google Scholar 

  • Norby RJ, Luo Y. 2004. Evaluating ecosystem responses to rising atmospheric CO2 and global warming in a multi-factor world. New Phytol 162:281–93.

    Article  Google Scholar 

  • Orlowsky B, Seneviratne SI. 2012. Global changes in extreme events: regional and season l dimension. Clim Change 110:669–96.

    Article  Google Scholar 

  • Pan Y, Birdsey RA, Fang J, Houghton R, Kauppi PE, Kurz WA, Phillips OL, Shvidenko A, Lewis SL, Canadell JG, Ciais P, Jackson RB, Pacala SW, McGuire AD, Piao S, Rautiainen A, Sitch S, Hayes D. 2011. A large and persistent carbon sink in the world’s forests. Science 333:988–93.

    Article  CAS  PubMed  Google Scholar 

  • Peterjohn WT, Melillo JM, Steudler PA, Newkirk KM, Bowles FP, Aber JD. 1994. Responses of trace gas fluxes and N availability to experimentally elevated soil temperatures. Ecol Appl 4:617–25.

    Article  Google Scholar 

  • Reichstein M, Kätterer T, Andrén O, Ciais P, Schulze ED, Cramer W, Papale D, Valentini R. 2005. Temperature sensitivity of decomposition in relation to soil organic matter pools: critique and outlook. Biogeosciences 2:317–21.

    Article  CAS  Google Scholar 

  • Rustad LE, Campbell JL, Marion GM, Norby RJ, Mitchell MJ, Hartley AE, Cornelissen JHC, Gurevitch J, GCTE-NEWS. 2001. A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–62.

    Article  Google Scholar 

  • Rustad LE, Fernandez IJ. 1998. Experimental soil warming effects on CO2 and CH4 flux from a low elevation spruce-fir forest soil in Maine, USA. Glob Change Biol 4:597–605.

    Article  Google Scholar 

  • Ryan MG, Hubbard RM, Pongracic S, Raison RJ, McMurtrie RE. 1996. Foliage, fine-root, woody tissue and stand respiration in Pinus radiate in relation to nitrogen status. Tree Physiol 16:333–43.

    Article  PubMed  Google Scholar 

  • SAS Institute. 2013. SAS/STAT 9.4 user’s guide. Cary: SAS Institute.

    Google Scholar 

  • Savage K, Davidson EA, Tang J. 2013. Diel patterns of autotrophic and heterotrophic respiration among phenological stages. Glob Change Biol 19:1151–9.

    Article  CAS  Google Scholar 

  • Schindlbacher A, Wunderlich S, Borken W, Kitzler B, Zechmeister-Boltenstern S, Jandl R. 2012. Soil respiration under climate change: prolonged summer drought offsets soil warming effects. Glob Change Biol 18:2270–9.

    Article  Google Scholar 

  • Schindlbacher A, Zechmeister-Boltenstern S, Jandl R. 2009. Carbon losses due to soil warming: do autotrophic and heterotrophic soil respiration respond equally? Glob Change Biol 15:901–13.

    Article  Google Scholar 

  • Schlesinger WH, Andrews JA. 2000. Soil respiration and the global carbon cycle. Biogeochemistry 48:7–20.

    Article  CAS  Google Scholar 

  • Subke JA, Inglima I, Cortufo MF. 2006. Trends and methodological impacts in soil CO2 efflux partitioning: a metaanalytical review. Glob Change Biol 12:921–43.

    Article  Google Scholar 

  • Ueda MU, Muller O, Nakamura M, Nakaji T, Hiura T. 2013. Soil warming decreases inorganic and dissolved organic nitrogen pools by preventing the soil from freezing in a cool temperate forest. Soil Biol Biochem 61:105–8.

    Article  CAS  Google Scholar 

  • Vogel J, Bronson D, Gower ST, Schuur EAG. 2014. The response of root and microbial respiration to the experimental warming of boreal black spruce forest. Can J For Res 44:986–93.

    Article  CAS  Google Scholar 

  • Wang C, Wan S, Xing X, Zhang L, Han X. 2006. Temperate and soil moisture interactively affected soil net N mineralization in temperate grassland in Northern China. Soil Biol Biochem 38:1101–10.

    Article  CAS  Google Scholar 

  • Wang X, Liu LL, Piao SL, 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 Change Biol 20:3229–37.

    Article  Google Scholar 

  • Withington JM, Reich PB, Oleksyn J, Eissenstat DM. 2006. Comparisons of structure and life span in roots and leaves among temperate trees. Ecol Monogr 76:381–97.

    Article  Google Scholar 

  • Xu X, Sherry RA, Niu S, Zhou J, Luo Y. 2012. Long-term experimental warming decreased labile soil organic carbon in a tallgrass prairie. Plant Soil 361:307–15.

    Article  CAS  Google Scholar 

  • Yin H, Xia J, Li Y, Chen Z, Cheng X, Zhao C, Liu Q. 2013. Warming effects on root morphological and physiological traits: the potential consequences on soil C dynamics as altered root exudation. Agric For Meteorol 180:287–96.

    Article  Google Scholar 

  • 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 Change Biol 13:761–75.

    Google Scholar 

  • Zhou Y, Tang J, Melillo JM, Butler S, Mohan JE. 2011. Root standing crop and chemistry after six years of soil warming in a temperate forest. Tree Physiol 31:707–17.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Japan Society for the Promotion of Science (JSPS) Funding Program for Next Generation World-Leading Researchers (NEXT Program GR048 to H. Muraoka), the JSPS KAKENHI program (Grant Number 26241005 to H. Muraoka, and Grant Number PU13007 for foreign researchers to N.J. Noh), and the Japanese Alps Inter-University Cooperative Project Fund of the Ministry of Education, Culture, Sports, Science and Technology. We would like to thank Dr. Y. Son for experimental assistance. We also thank the journal’s subject-matter editor and the two anonymous reviewers for their constructive comments.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Author notes

  1. Masatoshi Kuribayashi

    Present address: Nagano Environmental Conservation Research Institute, 2054-120 Kitago, Nagano, 381-0075, Japan

Authors and Affiliations

  1. River Basin Research Center, Gifu University, 1-1 Yanagido, Gifu, 501-1193, Japan

    Nam-Jin Noh, Masatoshi Kuribayashi, Taku M. Saitoh & Hiroyuki Muraoka

  2. Tomakomai Research Station, Field Science Center for Northern Biosphere, Hokkaido University, Tomakomai, 053-0035, Japan

    Tatsuro Nakaji & Tsutom Hiura

  3. Nakagawa Research Station, Field Science Center for Northern Biosphere, Hokkaido University, Otoineppu, Nakagawa, 098-2501, Japan

    Masahiro Nakamura

Authors
  1. Nam-Jin Noh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masatoshi Kuribayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Taku M. Saitoh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tatsuro Nakaji
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Masahiro Nakamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tsutom Hiura
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hiroyuki Muraoka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nam-Jin Noh.

Additional information

Author Contributions

NJN, HM, TN, and TH designed the study. NJN, MK, TMS, and TN collected field data. NJN performed laboratory analyses and analyzed the data. NJN led writing of the manuscript, and all other authors contributed to finalizing the manuscript.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 281 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Noh, NJ., Kuribayashi, M., Saitoh, T.M. et al. Responses of Soil, Heterotrophic, and Autotrophic Respiration to Experimental Open-Field Soil Warming in a Cool-Temperate Deciduous Forest. Ecosystems 19, 504–520 (2016). https://doi.org/10.1007/s10021-015-9948-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-015-9948-8

Keywords

Search

Navigation