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Partitioning of root respiration into growth, maintenance, and ion uptake components in a young larch-dominated forest

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Abstract

Purpose

Fine roots play an essential role in global carbon cycles, but phenological variations in root function and metabolism are poorly understood. To illustrate the dynamics of fine root function and metabolism in the field, we partitioned root respiration (Rr) into growth (Rg), maintenance (Rm), and ion uptake (Rion) components using a modified traditional model.

Methods

A year-round experiment was conducted in a young larch-dominated forest regrowing on bare soil. Soil respiration was measured with a chamber method and partitioned into Rr and heterotrophic respiration by trenching. Fine root biomass and production were measured simultaneously. Using the field data, the model was parameterized, and Rr was further partitioned.

Results

Annually, Rr (210–253 g C m−2 yr−1) accounts for 45–47% of the total soil respiration. The contribution of fine root Rg, fine root Rm, coarse root Rm, and fine root Rion were 26–40, 46–51, 10–16, and 12%, respectively. The Rg contribution showed a clear seasonal variation, with a peak in mid-spring and a minimum in early fall, mainly because of different seasonality between fine root production and soil temperature.

Conclusion

The model parameters were consistent with those from our previous study conducted by the same method in the same site. Thus, we believe that our approach was robust under a relatively simple condition. However, our growth respiration parameter resulting from only field data was much higher than those from laboratory experiments. To further improve our understanding of root respiration, more field data should be accumulated.

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References

  • Abramoff RZ, Finzi AC (2015) Are above- and below-ground phenology in sync? New Phytol 205:1054–1061. https://doi.org/10.1111/nph.13111

    Article  Google Scholar 

  • Addo-Danso SD, Prescott CE, Smith AR (2016) Methods for estimating root biomass and production in forest and woodland ecosystem carbon studies: A review. For Ecol Manage 359:332–351. https://doi.org/10.1016/j.foreco.2015.08.015

    Article  Google Scholar 

  • Amthor J (2000) The McCree–de Wit-Penning de Vries-Thornley respiration paradigms: 30 years later. Ann Bot-London 86:1–20. https://doi.org/10.1006/anbo.2000.1175

    Article  CAS  Google Scholar 

  • Ballantyne A, Smith W, Anderegg W, Kauppi P, Sarmiento J, Tans P, Shevliakova E, Pan Y, Poulter B, Anav A, Friedlingstein P, Houghton R, Running S (2017) Accelerating net terrestrial carbon uptake during the warming hiatus due to reduced respiration. Nat Clim Chang 7:148–152. https://doi.org/10.1038/nclimate3204

    Article  CAS  Google Scholar 

  • Boone RD, Nadelhoffer KJ, Canary JD, Kaye JP (1998) Roots exert a strong influence on the temperature sensitivity of soil respiration. Nature 396:570–572

    Article  CAS  Google Scholar 

  • Brunner I, Bakker MR, Björk RG, Hirano Y, Lukac M, Aranda X, Børja I, Eldhuset TD, Helmisaari HS, Jourdan C, Konôpka B, López BC, Miguel Pérez C, Persson H, Ostonen I (2013) Fine-root turnover rates of European forests revisited: an analysis of data from sequential coring and ingrowth cores. Plant Soil 362:357–372. https://doi.org/10.1007/s11104-012-1313-5

    Article  CAS  Google Scholar 

  • Cannell MGR, Thornley JHM (2000) Modeling the components of plant respiration: some guiding principle. Ann Bot-London 85:45–54

    Article  CAS  Google Scholar 

  • Chapin FSI, Matson PA, Vitousek PM (2011) Plant carbon buddgets. Principle of terrestrial ecosystem eclogoy, 2nd edn. Springer, New York

    Book  Google Scholar 

  • Collalti A, Tjoelker MG, Hoch G, Makela A, Guidolotti G, Heskel M, Petit G, Ryan MG, Battipaglia G, Matteucci G, Prentice IC (2020) Plant respiration: Controlled by photosynthesis or biomass? Glob Chang Biol 26:1739–1753. https://doi.org/10.1111/gcb.14857

    Article  Google Scholar 

  • Cui R, Hirano T, Sun L, Teramoto M, Liang N (2021) Variations in biomass, production and respiration of fine roots in a young larch forest. J Agric Meteorol 77:167–178. https://doi.org/10.2480/agrmet.D-20-00049

    Article  Google Scholar 

  • Dornbush ME, Isenhart TM, Raich JW (2002) Quantifying fine-root deomposition: an alternative to buried litterbags. Ecology 83:2985–2990

    Article  Google Scholar 

  • Finér L, Ohashi M, Noguchi K, Hirano Y (2011a) Factors causing variation in fine root biomass in forest ecosystems. For Ecol Manage 261:265–277. https://doi.org/10.1016/j.foreco.2010.10.016

    Article  Google Scholar 

  • Finér L, Ohashi M, Noguchi K, Hirano Y (2011b) Fine root production and turnover in forest ecosystems in relation to stand and environmental characteristics. For Ecol Manage 262:2008–2023. https://doi.org/10.1016/j.foreco.2011.08.042

    Article  Google Scholar 

  • Friedlingstein P, O’Sullivan M, Jones MW, Andrew RM, Hauck J, Olsen A, Peters GP, Peters W, Pongratz J, Sitch S, Le Quéré C, Canadell JG, Ciais P, Jackson RB, Alin S, Aragão LEOC, Arneth A, Arora V, Bates NR, Becker M, Benoit-Cattin A, Bittig HC, Bopp L, Bultan S, Chandra N, Chevallier F, Chini LP, Evans W, Florentie L, Forster PM, Gasser T, Gehlen M, Gilfillan D, Gkritzalis T, Gregor L, Gruber N, Harris I, Hartung K, Haverd V, Houghton RA, Ilyina T, Jain AK, Joetzjer E, Kadono K, Kato E, Kitidis V, Korsbakken JI, Landschützer P, Lefèvre N, Lenton A, Lienert S, Liu Z, Lombardozzi D, Marland G, Metzl N, Munro DR, Nabel JEMS, Nakaoka S-I, Niwa Y, O’Brien K, Ono T, Palmer PI, Pierrot D, Poulter B, Resplandy L, Robertson E, Rödenbeck C, Schwinger J, Séférian R, Skjelvan I, Smith AJP, Sutton AJ, Tanhua T, Tans PP, Tian H, Tilbrook B, van der Werf G, Vuichard N, Walker AP, Wanninkhof R, Watson AJ, Willis D, Wiltshire AJ, Yuan W, Yue X, Zaehle S (2020) Global Carbon Budget 2020. Earth Syst Sci Data 12:3269–3340. https://doi.org/10.5194/essd-12-3269-2020

    Article  Google Scholar 

  • George K, Norby RJ, Hamilton JG, DeLucia EH (2003) Fine-root respiration in a loblolly pine and sweetgum forest growing in elevated CO2. New Phytol 160:511–522. https://doi.org/10.1046/j.1469-8137.2003.00911.x

    Article  CAS  Google Scholar 

  • Granier A (1987) Evaluation of transpiration in a Douglas-fir stand by means of sap flow measurements. Tree Physiol 3:309–320

    Article  CAS  Google Scholar 

  • Hanson PJ, Edwards NT, Gartedn CT, Andrews JA (2000) Separating root and soil microbial contributions to soil respiration: A review of methods and observations. Biogeochemistry 48:114–146

    Article  Google Scholar 

  • Hendricks JJ, Hendrick RL, Wilson CA, Mitchell RJ, Pecot SD, Guo D (2006) Assessing the patterns and controls of fine root dynamics: an empirical test and methodological review. J Ecol 94:40–57. https://doi.org/10.1111/j.1365-2745.2005.01067.x

    Article  Google Scholar 

  • Henriksson N, Lim H, Marshall J, Franklin O, McMurtrie RE, Lutter R, Magh R, Lundmark T, Nasholm T (2021) Tree water uptake enhances nitrogen acquisition in a fertilized boreal forest - but not under nitrogen-poor conditions. New Phytol 232:113–122. https://doi.org/10.1111/nph.17578

    Article  CAS  Google Scholar 

  • Hertel D, Leuschner C (2002) A comparison of four different fine root production estimates with ecosystem carbon balance data in a Fagus-Quercus mixed forest. Plant Soil 239:237–251

    Article  CAS  Google Scholar 

  • Hirano T, Suzuki K, Hirata R (2017) Energy balance and evapotranspiration changes in a larch forest caused by severe disturbance during an early secondary succession. Agric for Meteorol 232:457–468. https://doi.org/10.1016/j.agrformet.2016.10.003

    Article  Google Scholar 

  • Hopkins F, Gonzalez-Meler MA, Flower CE, Lynch DJ, Czimczik C, Tang J, Subke JA (2013) Ecosystem-level controls on root-rhizosphere respiration. New Phytol 199:339–351. https://doi.org/10.1111/nph.12271

    Article  CAS  Google Scholar 

  • Johnson IR (1990) Plant respiration in relation to growth, maintenance, ion uptake and nitrogen assimilation. Plant Cell Environ 13:319–328

    Article  Google Scholar 

  • Kuzyakov Y (2006) Sources of CO2 efflux from soil and review of partitioning methods. Soil Biol Biochem 38:425–448. https://doi.org/10.1016/j.soilbio.2005.08.020

    Article  CAS  Google Scholar 

  • Kuzyakov Y (2010) Priming effects: Interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371. https://doi.org/10.1016/j.soilbio.2010.04.003

    Article  CAS  Google Scholar 

  • Lambers H, Chapin FSI, Pons TL (2008) The role of respiration in plant carbon balance. Plant Physiological Ecology, 2nd edn. Springer, New York

    Book  Google Scholar 

  • Lavigne MB, Foster RJ, Goodine G (2004) Seasonal and annual changes in soil respiration in relation to soil temperature, water potential and trenching. Tree Physiol 24:415–424

    Article  CAS  Google Scholar 

  • Li X, Zhu J, Lange H, Han S (2013) A modified ingrowth core method for measuring fine root production, mortality and decomposition in forests. Tree Physiol 33:18–25. https://doi.org/10.1093/treephys/tps124

    Article  CAS  Google Scholar 

  • Makita N, Fujimoto R, Tamura A (2021) The contribution of roots, mycorrhizal hyphae, and soil free-living microbes to soil respiration and its temperature sensitivity in a Larch Forest. Forests 12. https://doi.org/10.3390/f12101410

  • McCormack ML, Adams TS, Smithwick EAH, Eissenstat DM (2014) Variability in root production, phenology, and turnove rate among 12 temperate tree species. Ecology 98:2224–2235

    Article  Google Scholar 

  • McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB, Leppalammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M (2015a) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–518. https://doi.org/10.1111/nph.13363

    Article  Google Scholar 

  • McCormack ML, Gaines KP, Pastore M, Eissenstat DM (2015b) Early season root production in relation to leaf production among six diverse temperate tree species. Plant Soil 389:121–129. https://doi.org/10.1007/s11104-014-2347-7

    Article  CAS  Google Scholar 

  • McCree KJ (1974) Equation for the rae of dark respiration of white clove and grain sorghum, as functions of dry weight, photosynthetic rate, and tempearture. Crop Sci 14:509–514

    Article  Google Scholar 

  • McMurtrie RE, Nasholm T (2018) Quantifying the contribution of mass flow to nitrogen acquisition by an individual plant root. New Phytol 218:119–130. https://doi.org/10.1111/nph.14927

    Article  Google Scholar 

  • Moyano FE, Atkin OK, Bahn M, Bruhn D, Burton AJ, Heinemeyer A, Kutsch WL, Wieser G (2009) Respiration from roots and the mycorrhizosphere. In: Kutsch WL, Bahn M, Heinemeyer A (eds) Soil carbon dynamics. Cambridge University Press, New York

    Google Scholar 

  • Oyewole OA, Inselsbacher E, Nasholm T (2014) Direct estimation of mass flow and diffusion of nitrogen compounds in solution and soil. New Phytol 201:1056–1064. https://doi.org/10.1111/nph.12553

    Article  CAS  Google Scholar 

  • Penning de Vries FWT (1974) Substrate utilization and respiration in relation to growth and maintenance in higher plants. Neth J Agric Sci 22:40–44

    Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, authors E, Heisterkamp S, Willigen BV, Ranke J, R-core (2022) Linear and Nonlinear Mixed Effects Models, Package 'nlme', V 3.1–155

  • Poorter H (1994) Construction costs and payback time of biomass: A whole-plant perspective. In: Roy J, Garnier E (eds) A whole-plant perspective on carbon-nitrogen interactions. SPB Academic Publishing, The Hague

    Google Scholar 

  • Radville L, McCormack ML, Post E, Eissenstat DM (2016) Root phenology in a changing climate. J Exp Bot 67:3617–3628. https://doi.org/10.1093/jxb/erw062

    Article  CAS  Google Scholar 

  • Richter DD, Markewitz D, Trumbore SE, Wells CG (1999) Rapid accumulation and turnover of soil carbon in a re-establishing forest. Nature 400:56–58

    Article  CAS  Google Scholar 

  • Sano T, Hirano T, Liang N, Hirata R, Fujinuma Y (2010) Carbon dioxide exchange of a larch forest after a typhoon disturbance. For Ecol Manage 260:2214–2223. https://doi.org/10.1016/j.foreco.2010.09.026

    Article  Google Scholar 

  • Scott-Denton LE, Rosenstiel TN, Monson RK (2006) Differential controls by climate and substrate over the heterotrophic and rhizospheric components of soil respiration. Glob Change Biol 12:205–216. https://doi.org/10.1111/j.1365-2486.2005.01064.x

    Article  Google Scholar 

  • Subke J-A, Inglima I, Francesca Cotrufo M (2006) Trends and methodological impacts in soil CO2 efflux partitioning: A metaanalytical review. Glob Change Biol 12:921–943. https://doi.org/10.1111/j.1365-2486.2006.01117.x

    Article  Google Scholar 

  • Sun LF, Teramoto M, Liang N, Yazaki T, Hirano T (2017) Comparison of litter-bag and chamber methods for measuring CO2 emissions from leaf litter decomposition in a temperate forest. J Agric Meteorol 73:59–67. https://doi.org/10.2480/agrmet.D-16-00012

    Article  Google Scholar 

  • Sun L, Hirano T, Yazaki T, Teramoto M, Liang N (2020) Fine root dynamics and partitioning of root respiration into growth and maintenance components in cool temperate deciduous and evergreen forests. Plant Soil 446:471–486. https://doi.org/10.1007/s11104-019-04343-z

    Article  CAS  Google Scholar 

  • Sweetlove LJ, Williams TC, Cheung CY, Ratcliffe RG (2013) Modelling metabolic CO(2) evolution–a fresh perspective on respiration. Plant Cell Environ 36:1631–1640. https://doi.org/10.1111/pce.12105

    Article  CAS  Google Scholar 

  • Tang X, Fan S, Zhang W, Gao S, Chen G, Shi L (2019) Global variability in belowground autotrophic respiration in terrestrial ecosystems. Earth Syst Sci Data 11:1839–1852. https://doi.org/10.5194/essd-11-1839-2019

    Article  Google Scholar 

  • ThongoM’Bou A, Saint-André L, de Grandcourt A, Nouvellon Y, Jourdan C, Mialoundama F, Epron D (2010) Growth and maintenance respiration of roots of clonal Eucalyptus cuttings: scaling to stand-level. Plant Soil 332:41–53. https://doi.org/10.1007/s11104-009-0272-y

    Article  CAS  Google Scholar 

  • Thornley JHM (1970) Respiration, growth and maintenance in plants. Nature 227:304–305

    Article  CAS  Google Scholar 

  • Thornley JH (2011) Plant growth and respiration re-visited: maintenance respiration defined - it is an emergent property of, not a separate process within, the system - and why the respiration: photosynthesis ratio is conservative. Ann Bot 108:1365–1380. https://doi.org/10.1093/aob/mcr238

    Article  CAS  Google Scholar 

  • Warren JM, Hanson PJ, Iversen CM, Kumar J, Walker AP, Wullschleger SD (2015) Root structural and functional dynamics in terrestrial biosphere models–evaluation and recommendations. New Phytol 205:59–78. https://doi.org/10.1111/nph.13034

    Article  Google Scholar 

  • Wieser G, Bahn M (2004) Seasonal and spatial variation of woody tissue respiration in a Pinus cembra tree at the alpine timberline in the central Austrian Alps. Trees 18. https://doi.org/10.1007/s00468-004-0341-z

  • Yazaki T, Hirano T, Sano T (2016) Biomass accumulation and net primary production during the early stage of secondary succession after a severe forest disturbance in Northern Japan. Forests 7. https://doi.org/10.3390/f7110287

  • Yuan ZY, Chen HYH (2010) Fine root biomass, production, turnover rates, and nutrient contents in boreal forest ecosystems in relation to species, climate, fertility, and stand age: literature review and meta-analyses. Crit Rev Plant Sci 29:204–221. https://doi.org/10.1080/07352689.2010.483579

    Article  CAS  Google Scholar 

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Acknowledgements

We thank the Hokkaido Regional Office of the Forestry Agency for allowing us to use the study site, N. Saigusa, Y. Takahashi, R. Hirata and the staff of CGER for managing the site, and K. Ishikura for sharing an R script for the nonlinear mixed effect model.

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Correspondence to Takashi Hirano.

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This study was supported by JPSP KAKENHI (17K20037) and the Environment Research and Technology Development Fund (JPMEERF20172005 and JPMEERF20202006) of Environmental Restoration and Conservation Agency of Japan. The authors have no relevant financial or non-financial interests to disclose. All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Takashi Hirano, Rui Cui and Lifei Sun. The first draft of the manuscript was written by Takashi Hirano and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript. The datasets generated during the current study are available from the corresponding author on reasonable request.

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Hirano, T., Cui, R., Sun, L. et al. Partitioning of root respiration into growth, maintenance, and ion uptake components in a young larch-dominated forest. Plant Soil 482, 57–72 (2023). https://doi.org/10.1007/s11104-022-05674-0

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