Skip to main content
Log in

Relationships between carbon allocation and partitioning of soil respiration across world mature forests

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

Partitioning of soil CO2 flux (FS) into autotrophic and heterotrophic components depends on how the plant carbon is allocated above- vs. belowground and how the belowground carbon is allocated for respiration and production of roots and their microbial associations. Data of litterfall (FA), root respiration (FR), and FS of world old-growth or mature forests (≥45 ages) were compiled, and the relationship between carbon allocation above- vs. belowground (indexed as the FA/FS ratio) and FS partitioning (indexed as the FR/FS ratio) was examined. The FA/FS ratio ranged from 0.08 to 0.64 and was positively correlated with mean annual air temperature and mean annual precipitation. The ratio increased from boreal to temperate to tropical forests, and was higher in broadleaved forests than in coniferous forests. Site-specific belowground carbon use efficiency (BCUE, root production per unit carbon used by roots and microbial associations) varied from 0.10 to 0.87, contrasting with the common assumption of a constant BCUE. Site-specific FR/FS ranged from 0.09 to 0.71 and increased with FS due to a decrease in BCUE. Deciduousness had a significant effect on the FR/FS ratios, with FR/FS ratios greater in deciduous forests than in evergreen forests. Methods of separating root respiration from soil heterotrophic respiration had a significant effect on estimated FR/FS. The estimated FR/FS ratio was negatively related to the FA/FS ratio, indicating that factors favouring carbon allocation belowground over aboveground will increase the autotrophic contribution to total soil respiration. The relatively low explaining power (r 2 = 0.270) of this relationship resulted from deviations from assumptions of constant BCUE and a near steady-state belowground pools.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bolstad PV, Davis KJ, Martin J, Cook BD, Wang W (2004) Component and whole-system respiration fluxes in northern deciduous forests. Tree Physiol 24:493–504

    CAS  PubMed  Google Scholar 

  • Bond-Lamberty B, Wang CK, Gower ST (2004a) A global relationship between the hetero-trophic and autotrophic components of soil respiration? Glob Chang Biol 10:1756–1766

    Article  Google Scholar 

  • Bond-Lamberty B, Wang CK, Gower ST (2004b) Contribution of root respiration to soil surface CO2 flux in a boreal black spruce chronosequence. Tree Physiol 24:1387–1395

    PubMed  Google Scholar 

  • Bond-Lamberty B, Wang CK, Gower ST (2004c) Net primary production and net ecosystem production of a boreal black spruce wildfire chronosequence. Glob Chang Biol 10:473–487

    Article  Google Scholar 

  • Borken W, Xu YJ, Brumme R, Lamersdorf N (1999) A climate change scenario for carbon dioxide and dissolved organic carbon fluxes from a temperate forest soil. Drought and rewetting effects. Soil Sci Soc Am J 63:1848–1855

    Article  CAS  Google Scholar 

  • Bowden RD, Nadelhoffer KJ, Boone RD, Melillo JM, Garrison JB (1993) Contributions of aboveground litter, belowground litter, and root respiration to total soil respiration in a temperate mixed hardwood forest. Can J For Res 23:1402–1407

    Article  Google Scholar 

  • Buchmann N (2000) Biotic and abiotic factors controlling soil respiration rates in Picea abies stand. Soil Biol Biochem 32:1625–1635

    Article  CAS  Google Scholar 

  • Chambers JQ, Tribuzy ES, Toledo LC, Crispim BF, Higuchi N, dos Santos J, Araújo AC, Kruijt B, Nobre AD, Trumbore SE (2004) Respiration from a tropical forest ecosystem: partitioning of sources and low carbon use efficiency. Ecol Appl 14:72–88

    Article  Google Scholar 

  • Chen GS, Yang YS, Qian W, Gao R, Niu ZP, Han YG (2005) Total belowground carbon allocation in Castanopsis kawakamii and Chinese fir plantations in subtropical area of China. Acta Ecologica Sinica 25:2824–2829

    CAS  Google Scholar 

  • Chen GS, Yang YS, Gao R, Xie JS, Yang ZJ, Mao YL (2008) Changes in belowground carbon allocation in a Chinese fir chronosequence in Fujian Province, China. J Plant Ecol 32:1285–1293

    CAS  Google Scholar 

  • Chu JX (2005) Effects of land use and land cover changes on soil respiration in subalpine region in western Sicuan. Master Thesis for Shandong Agriculture University

  • Curtis PS, Hanson PJ, Bolstad P, Barford C, Randolph JC, Schmid HP, Wilson KB (2002) Biometric and eddy-covariance based estimates of annual carbon storage in five eastern North American deciduous forests. Agric For Meteorol 113:3–19

    Article  Google Scholar 

  • Czimczik CI, Trumbore SE, Carbone MS, Winston GC (2006) Changing sources of soil respiration with time since fire in a boreal forest. Glob Chang Biol 12:957–971

    Article  Google Scholar 

  • Davidson RL (1969) Effect of root/leaf temperature differentials on root/shoot ratios in some pasture grasses and clover. Ann Bot 33:561–569

    Google Scholar 

  • Davidson EA, Savage K, Bolstad P, Clark PA, Curtis PS, Ellsworth DS, Hanson PJ, Law BE, Luo Y, Pregitzer KS, Randolph JC, Zak D (2002) Belowground carbon allocation in forests estimated from litterfall and IRGA-based soil respiration measurements. Agric For Meteorol 113:39–51

    Article  Google Scholar 

  • Davidson EA, Ishida FY, Nepstad DC (2004) Effects of an experimental drought on soil emissions of carbon dioxide, methane, nitrous oxide, and nitric oxide in a moist tropical forest. Glob Chang Biol 10:718–730

    Article  Google Scholar 

  • Desai AR, Bolstad PV, Cook BD, Davis KJ, Carey EV (2005) Comparing net ecosystem exchange of carbon dioxide between an old-growth and mature forest in the upper Midwest, USA. Agric For Meteorol 128:33–55

    Article  Google Scholar 

  • Dewar RC, Medlyn BE, McMurtrie RE (1999) Acclimation of the respiration/photosynthesis ratio to temperature: insight from a model. Glob Chang Biol 5:615–622

    Article  Google Scholar 

  • Ewel KC, Jr Cropper WP, Gholz HL (1987) Soil CO2 evolution in Florida slash pine plantations. 2. Importance of root respiration. Can J For Res 17:330–333

    Article  Google Scholar 

  • Fahey TJ, Siccama TG, Driscoll CT, Likens GE, Campbell J, Johnson CE, Battles JJ, Aber JD, Cole JJ, Fisk MC, Groffman PM, Hamburg SP, Holmes RT, Schwarz PA, Yanai RD (2005) The biogeochemistry of carbon at Hubbard Brook. Biogeochemistry 75:109–176

    Article  CAS  Google Scholar 

  • Fan GK (2008) The effects of different regeneration patterns to the deforested lands of Chinese fir plantation on the soil carbon storage and the soil carbon quality. Master Thesis for Fujian Agriculture and Forestry University

  • Fang JY, Liu GH, Zhu B, Wang XK, Liu SH (2007) Carbon budgets of three temperate forest ecosystems in Dongling Mt., Beijing, China. Sci China Ser D Earth Sci 50:92–101

    Article  Google Scholar 

  • Fischer DG, Hart SC, LeRoy CJ, Whitham TG (2007) Variation in below-ground carbon fluxes along a Populus hybridization gradient. New Phytol 176:415–425

    Article  PubMed  Google Scholar 

  • Giardina CP, Ryan MG (2002) Total belowground carbon allocation in a fast growing Eucalyptus plantation. Ecosystems 5:487–499

    Article  CAS  Google Scholar 

  • Giardina CP, Ryan MG, Binkley D, Fownes J (2003) Primary production and carbon allocation in relation to nutrient supply in a tropical experimental forest. Glob Chang Biol 9:1–13

    Article  Google Scholar 

  • Giardina CP, Coleman MD, Hancock JE, Binkley D, King JS, Lilleskov E, Loya WM, Pregitzer KS, Ryan MG, Trettin CC (2005) The response of belowground carbon allocation in forests to global change. In: Binkley D, Menyailo O (eds) Tree species effects on soils: implications for global change. NATO Science Series, Kluwer Academic Publishers, Dordrecht, pp 119–154

    Chapter  Google Scholar 

  • Gifford RM (1995) Whole plant respiration and photosynthesis of wheat under increased CO2 concentration and temperature: long-term vs. short-term distinctions for modeling. Glob Chang Biol 1:385–396

    Article  Google Scholar 

  • Gough CM, Vogel CS, Harrold K, George K, Curtis PS (2007) The legacy of harvest and fire on ecosystem carbon storage in a north temperate forest. Glob Chang Biol 13:1935–1949

    Article  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 48:115–146

    Article  CAS  Google Scholar 

  • Harris WF, Sollins P, Edwards NT, Kinger BE, Shugart HH (1975) Productivity of world ecosystems. National Academy of Sciences, Washington, DC, pp 116–122

    Google Scholar 

  • Haynes BE, Gower ST (1995) Belowground carbon allocation in unfertilized and fertilized red pine plantations in northern Wisconsin. Tree Physiol 15:317–325

    PubMed  Google Scholar 

  • Herbert DA, Fownes JH (1999) Forest productivity and efficiency of resource use across a chronosequence of tropical montane soils. Ecosystems 2:242–254

    Article  CAS  Google Scholar 

  • Huang SD (2007) Effects of vegetation reconstruction on soil respiration in degraded red soil. Dissertation for Master’s Degree of Fujian Agriculture & Forestry University

  • Hunt R, Burnett JA (1973) The effects of light intensity and external potassium level on root/shoot ratio and rates of potassium uptake in perennial ryegrass (Lolium perenne L.). Ann Bot 37:519–537

    CAS  Google Scholar 

  • Keith H, Raison RJ, Jacobsen KL (1997) Allocation of carbon in a mature Eucalypt forest and some effects of soil phosphorus availability. Plant Soil 196:81–99

    Article  CAS  Google Scholar 

  • Kelting DL, Burger JA, Edwards GS (1995) The effects of ozone on the root dynamics of seedlings and mature red oak (Quercus rubra L.). For Ecol Manage 79:197–206

    Article  Google Scholar 

  • Klopatek JM (2002) Belowground carbon pools and processes in different age stands of Douglas-fir. Tree Physiol 22:197–204

    CAS  PubMed  Google Scholar 

  • Kutsch W, Eschenbach C, Dilly O (2001) The carbon cycle of contrasting landscape elements of the Bornhöved District. In: Tenhunen J (ed) Ecosystem approaches to landscape management in central Europe, Ecological Studies 147. Springer-Verlag, Berlin, Heidelberg, pp 75–95

    Google Scholar 

  • Law BE, Ryan MG, Anthoni PM (1999) Seasonal and annual respiration of a ponderosa pine ecosystem. Glob Chang Biol 5:169–182

    Article  Google Scholar 

  • Law BE, Thornton PE, Irvine J, Anthoni PM, Van Tuyl S (2001) Carbon storage and fluxes in ponderosa pine forests at different developmental stages. Glob Chang Biol 7:755–777

    Article  Google Scholar 

  • Li YD, Wu ZM, Zeng QB, Zhou GY, Chen BF, Fang JY (1998) Carbon pool and carbon dioxide dynamics of tropical mountain rain forest ecosystem at Jianfengling, Hainan Island. Acta Ecologica Sinica 18:371–378

    Google Scholar 

  • Lin B (2002) Litter of the artificial and natural subalpine Picea forest in western Sichuan. Master Thesis for Chengdu Institute of Biology, CAS

  • Litton CM, Giardina CP (2008) Below-ground carbon flux and partitioning: global patterns and response to temperature. Funct Ecol 22:941–954

    Article  Google Scholar 

  • Litton CM, Ryan MG, Raich JW (2007) Carbon allocation patterns in forest ecosystems. Glob Chang Biol 13:2089–2109

    Article  Google Scholar 

  • Liu Y (2005) Soil carbon efflux in the typical forest ecosystems of Changbai Mountains. Doctor Thesis for SAE Institute of CAS

  • Liu GQ, Tu XN, Zhao SD, Sun SH, Gravenhorst G (2001) Distributional characteristics on biomass and nutrient elements of pine-oak forest belt in Mt. Qinling. Scientia Silvae Sinicae 37:28–36

    CAS  Google Scholar 

  • Liu JJ, Wang DX, Lei RD, Wu QX (2003) Soil respiration and release of carbon dioxide from natural forest of Pinus tabulaeformis and Quercus aliena var. acuteserrata in Qinling mountains. Scientia Silvae Sinicae 39:8–13

    Google Scholar 

  • Malhi Y, Baldocchi DD, Jarvis PG (1999) The carbon balance of tropical, temperate and boreal forests. Plant Cell Environ 22:715–740

    Article  CAS  Google Scholar 

  • Malhi Y, Aragão LE, Metcalfe DB, Patiño S, Quesada CA, Almeida S, Anderson L, Brando P, Chambers JQ, Costa ACL, Martins L, Hutyra LR, Oliveira P, Pyle EH, Robertson AL (2009) Comprehensive assessment of carbon productivity, allocation and storage in three Amazonian forests. Glob Chang Biol 15:1255–1274

    Article  Google Scholar 

  • McDowell NG, Balster NJ, Marshall JD (2001) Belowground carbon allocation of Rocky Mountain Douglas-fir. Can J For Res 31:1425–1436

    Article  CAS  Google Scholar 

  • Miller HG (1981) Forest fertilization: some guiding concepts. Forestry 54(2):157–167

    Article  Google Scholar 

  • Nordgren A, Ottosson Löfvenius M, Högberg MN, Mellander P-E, Högberg P (2003) Tree root and soil heterotrophic respiration as revealed by girdling of boreal Scots pine forest: extending observations beyond the first year. Plant Cell Environ 26:1287–1296

    Article  Google Scholar 

  • Olsson P, Linder S, Giesler R, Högberg P (2005) Fertilization of boreal forest reduces both autotrophic and heterotrophic soil respiration. Glob Chang Biol 11:1745–1753

    Article  Google Scholar 

  • Palmroth S, Oren R, McCarthy HR, Johnsen KH, Finzi AC, Butnor JR, Ryan MG, Schlesinger WH (2006) Aboveground sink strength in forests controls the allocation of carbon below ground and its [CO2]-induced enhancement. PNAS 103:19362–19367

    Article  CAS  PubMed  Google Scholar 

  • Pongracic S (2001) Influence of irrigation and fertilization on the belowground carbon allocation in a pine plantation. Doctor Thesis of University of New South Wales

  • Raich JW, Nadelhoffer KJ (1989) Belowground carbon allocation in forest ecosystems: global trends. Ecology 70:1346–1354

    Article  Google Scholar 

  • Raich JW, Schlesinger WH (1992) The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus 44B:81–99

    CAS  Google Scholar 

  • Raich JW, Russell AE, Kitayama K, Parton WJ, Vitousek PM (2006) Temperature influences carbon accumulation in moist tropical forests. Ecology 87:76–87

    Article  PubMed  Google Scholar 

  • Rodeghiero M, Cescatti A (2006) Indirect partitioning of soil respiration in a series of evergreen forest ecosystem. Plant Soil 284:7–22

    Article  CAS  Google Scholar 

  • Ryan MG (1991) A simple method for estimating gross carbon budgets for vegetation in forest ecosystems. Tree Physiol 9:255–266

    PubMed  Google Scholar 

  • Ryan MG, Hubbard RM, Pongracic S, Raison RJ, McMurtrie RE (1996) Foliage, fine-root, woody-tissue and stand respiration in Pinus radiata in relation to nutrient status. Tree Physiol 16:333–343

    PubMed  Google Scholar 

  • Ryan MG, Lavigne MB, Gower ST (1997) Annual carbon cost of autotrophic respiration in boreal forest ecosystems in relation to species and climate. J Geophys Res 102:28871–28883

    Article  CAS  Google Scholar 

  • Saiz G, Byrne KA, Butterbach-Bahl K, Kiese R, Blujdea V, Farrell EP (2006) Stand age related effects on soil respiration in a first rotation Sitka spruce chronosequence in central Ireland. Glob Chang Biol 12:1007–1020

    Article  Google Scholar 

  • Schulze E-D (2000) The carbon and nitrogen cycle in forest ecosystems. In: Schulz E-D (eds) Carbon and nitrogen cycling in European forest ecosystems. Ecological Studies, vol 142. Spinger, Berlin, p 500

  • Silver WL, Thompson AW, Mcgroddy ME, Varner RK, Dias JD, Silva H, Crill PM, Keller M (2005) Fine root dynamics and trace gas fluxes in two lowland tropical forest soils. Glob Chang Biol 11:290–306

    Article  Google Scholar 

  • Subke JA, Inglimaw I, Cotrufow MF (2006) Trends and methodological impacts in soil CO2 efflux partitioning: a metaanalytical review. Glob Chang Biol 12:921–943

    Article  Google Scholar 

  • Sulzman EW, Brant JB, Bowden RD, Lajtha K (2005) Contribution of aboveground litter, belowground litter, and rhizosphere respiration to total soil CO2 efflux in an old growth coniferous forest. Biogeochemistry 73:231–256

    Article  Google Scholar 

  • Takahashi M, Limtong P, Suksawang S, Hirai K (2002) A comparison of the carbon balance in the soil between a natural forest and a teak plantation. 17th WCSS, Thailand

  • Trumbore SE (2000) Age of soil organic matter and soil respiration: radiocarbon constraints on belowground C dynamics. Ecol Appl 10:399–411

    Article  Google Scholar 

  • Trumbore SE, Camargo PB, Camargo PB (1995) Below ground cycling of carbon in forests and pastures of eastern Amazonia. Global Biogeochem Cycles 9:515–528

    Article  CAS  Google Scholar 

  • Vogel JG, Bond-lamberty BP, Schuur EAG, Gower ST, Mack MC, O’Connell KEB, Valentine DW, Ruess RW (2008) Carbon allocation in boreal black spruce forests across regions varying in soil temperature and precipitation. Glob Chang Biol 14:1–14

    Article  Google Scholar 

  • Warembourg FR, Estelrich HD (2001) Plant phenology and soil fertility effects on below-ground carbon allocation for an annual (Bromus madritensis) and a perennial (Bromus erectus) grass species. Soil Biol Biochem 33:1291–1303

    Article  CAS  Google Scholar 

  • Waring RH, Landseberg JJ, Williams M (1998) Net primary production of forests: a constant fraction of gross primary production? Tree Physiol 18:113–129

    Google Scholar 

  • Whittaker RH, Woodwell GM (1969) Structure, production and diversity of the oak-pine forest at Brookhaven, New York. J Ecol 57:155–174

    Article  Google Scholar 

  • Yan JH, Wang YP, Zhou GY, Zhang DQ (2006) Estimates of soil respiration and net primary production of three forests at different succession stages in South China. Glob Chang Biol 12:1–12

    Article  Google Scholar 

  • Yang YS, Lin P, Guo JF, Lin RY, Chen GS, He ZM (2003) Litter production, nutrient return and leaf-litter decomposition in natural and monoculture plantation forests of Castanopsis kawakamii in subtropical China. Acta Ecologica Sinica 23:1278–1289

    Google Scholar 

  • Yang YS, Chen GS, Wang XG, Xie JS, Gao R, Li Z (2005) Response of soil CO2 efflux to forest conversion in subtropical China. Acta Ecologica Sinica 25:1684–1690

    CAS  Google Scholar 

  • Zhou G, Liu S, Li Z, Zhang D, Tang X, Zhou C, Yan J, Mo J (2006) Old-growth forests can accumulate carbon in soils. Science 314:1417

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was funded by the National Natural Science Foundation of China (No. 30972347) and the Natural Science Foundation of Fujian Province (No. 2008J0124).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yu-sheng Yang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chen, Gs., Yang, Ys., Guo, Jf. et al. Relationships between carbon allocation and partitioning of soil respiration across world mature forests. Plant Ecol 212, 195–206 (2011). https://doi.org/10.1007/s11258-010-9814-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-010-9814-x

Keywords

Navigation