Skip to main content

Advertisement

Log in

Carbon fluxes to the soil in a mature temperate forest assessed by 13C isotope tracing

  • Ecosystem Ecology
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Photosynthetic carbon uptake and respiratory C release from soil are major components of the global carbon balance. The use of 13C depleted CO213C = −30‰) in a free air CO2 enrichment experiment in a mature deciduous forest permitted us to trace the carbon transfer from tree crowns to the rhizosphere of 100–120 years old trees. During the first season of CO2 enrichment the CO2 released from soil originated substantially from concurrent assimilation. The small contribution of recent carbon in fine roots suggests a much slower fine root turnover than is often assumed.13C abundance in soil air correlated best with temperature data taken from 4 to 10 days before air sampling time and is thus rapidly available for root and rhizosphere respiration. The spatial variability of δ13C in soil air showed relationships to above ground tree types such as conifers versus broad-leaved trees. Considering the complexity and strong overlap of roots from different individuals in a forest, this finding opens an exciting new possibility of associating respiration with different species. What might be seen as signal noise does in fact contain valuable information on the spatial heterogeneity of tree-soil interaction.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Amundson R, Stern L, Baisden T, Wang Y (1998) The isotopic composition of soil and soil-respired CO2. Geoderma 82:83–114

    Article  Google Scholar 

  • Andrews JA, Harrison KG, Matamala R, Schlesinger WH (1999) Separation of root respiration from total soil respiration using carbon 13 labeling during free-air carbon dioxide enrichment (FACE). Soil Sci Soc Am J 63:1429–1435

    CAS  Google Scholar 

  • Bhupinderpal-Singh, Nordgren A, Ottosson-Löfvenius M, Högberg MN, Mellander PE, 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  CAS  Google Scholar 

  • Bowling DR, McDowell NG, Bond BJ, Law BE, Ehleringer JR (2002) 13C content of ecosystem respiration is linked to precipitation and vapor pressure deficit. Oecologia 131:113–124

    Article  Google Scholar 

  • Buchmann N, Brooks JR, Rapp KD, Ehleringer JR (1996) Carbon isotope composition of C4 grasses is influenced by light and water supply. Plant Cell Environ 19:392–402

    CAS  Google Scholar 

  • Burton AJ, Pregitzer KS, Zogg GP, Zak DR (1998) Drought reduces root respiration in sugar maple forests. Ecol Appl 3:771–778

    Google Scholar 

  • Davidson EC, Belk E, Boone RD (1998) Soil water content and temperature as independent or confounded factors controlling soil respiration in a temperate mixed hardwood forest. Global Change Biol 4:217–227

    Article  Google Scholar 

  • Ekblad A, Högberg P (2001) Natural abundance of 13C in CO2 respired from forest soils reveals speed of link between tree photosynthesis and root respiration. Oecologia 127:305–308

    Article  Google Scholar 

  • Fahey TJ, Hughes JW (1994) Fine root dynamics in a northern hardwood forest ecosystem, Hubbard Brook experimental forest, NH. J Ecol 82:533–548

    Google Scholar 

  • Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537

    Article  CAS  Google Scholar 

  • Gärdenäs AI (2000) Soil respiration fluxes measured along a hydrological gradient in a Norway spruce stand in south Sweden (Skogaby). Plant Soil 221:273–280

    Article  Google Scholar 

  • Garten CT, Taylor GEJ (1992) Foliar δ13C within a temperate deciduous forest: spatial, temporal, and species sources of variation. Oecologia 90:1–7

    Google Scholar 

  • Gaudinski JB, Trumbore SE, Davidson EA, Zheng S (2000) Soil carbon cycling in a temperate forest: radiocarbon-based estimates of residence times, sequestration rates and partitioning of fluxes. Biogeochemistry 51:33–69

    Article  Google Scholar 

  • Gaudinski JB, Trumbore SE, Davidson EA, Cook AC, Markewitz D, Richter DD (2001) The age of fine-root carbon in three forests of the eastern United States measured by radiocarbon. Oecologia 129:420–429

    Google Scholar 

  • Hanson PJ, Wullschleger SD, Bohlman A, Todd DE (1993) Seasonal and topographic patterns of forest floor CO2 efflux from an upland oak forest. Tree Physiol 13:1–15

    CAS  PubMed  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 

  • Hättenschwiler S, Körner C (1997) Annual CO2 budget of spruce model ecosystems in the third year of exposure to elevated CO2. Acta Oecol 18:319–325

    Google Scholar 

  • Hendrick RL, Pregitzer KS (1993) The dynamics of fine root length, biomass, and nitrogen content in two northern hardwood ecosystems. Can J For Res 23:2507–2520

    Google Scholar 

  • Hesterberg R, Siegenthaler U (1991) Production and stable isotopic composition of CO2 in a soil near Bern, Switzerland. Tellus 43B:197–205

    Article  Google Scholar 

  • Högberg P et al (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792

    Article  PubMed  Google Scholar 

  • Högberg P, Nordgren A, Agren GI (2002) Carbon allocation between tree root growth and root respiration in boreal pine forest. Oecologia 132:579–581

    Article  Google Scholar 

  • Janssens IA et al (2001) Productivity overshadows temperature in determining soil and ecosystem respiration across European forests. Global Change Biol 7:269–278

    Article  Google Scholar 

  • Keeling CD (1958) The concentration and isotopic abundances of atmospheric carbon dioxide in rural areas. Geochim Cosmochim Acta 13:322–334

    Article  CAS  Google Scholar 

  • Kelting DL, Burger JA, Edwards GS (1997) Estimating root respiration, microbial respiration in the rhizosphere, and root-free soil respiration in forest soils. Soil Biol Biochem 30:961–968

    Google Scholar 

  • Körner C, Arnone A (1992) Responses to elevated carbon dioxide in artificial tropical ecosystems. Science 1992:1672–1675

    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 

  • Matamala R, Gonzàlez-Meler MA, Jastrow JD, Norby RJ, Schlesinger WH (2003) Impacts of fine root turnover on forest NPP and soil C sequestration potential. Science 302:1385–1387

    Article  CAS  PubMed  Google Scholar 

  • McClaugherty CA, Aber JD, Melillo JM (1982) The role of fine roots in the organic matter and nitrogen budgets of two forested ecosystems. Ecology 63:1481–1490

    Google Scholar 

  • Norby RJ, Gunderson CA, Wullschleger SD, O’ Neill E, McCracken M (1992) Productivity and compensatory responses of yellow-poplar trees in elevated CO2. Nature 357:322–324

    Article  Google Scholar 

  • Panek JA (1996) Correlations between stable carbon-isotope abundance and hydraulic conductivity in Douglas-fir across a climate gradient in Oregon, USA. Tree Physiol 16:747–755

    CAS  PubMed  Google Scholar 

  • Pepin S, Körner C (2002) Web-FACE: a new canopy free-air CO2 enrichment system for tall trees in mature forests. Oecologia 133:1–9

    Article  Google Scholar 

  • Polomski J, Kuhn N (1998) Wurzelsysteme Eidg Forschungsanstalt für Wald, Schnee und Landschaft (WSL/FNP):153–175

  • Pregitzer KS, King JS, Burton AJ, Brown SE (2000) Responses of tree fine roots to temperature. New Phytol 147:105–115

    Article  CAS  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

    Article  Google Scholar 

  • Robinson D, Scrimgeour CM (1995) The contribution of plant C to soil CO2 measured using δ13C. Soil Biol Biochem 27:1653–1656

    Article  CAS  Google Scholar 

  • Rygiewicz PT, Andersen CP (1994) Mycorrhizae alter quality and quantity of carbon allocated below ground. Nature 369:58–60

    Google Scholar 

  • Trumbore S (2000) Age of soil organic matter and soil respiration: radiocarbon constraints on belowground C dynamics. Belowground Process Global Change 10:39–11

    Google Scholar 

  • Widen B, Majdi H (2001) Soil CO2 efflux and root respiration at three sites in a mixed pine and spruce forest: seasonal and diurnal variation. Can J For Res 31:786–796

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to Steeve Pepin, Olivier Bignucolo and Sibylle Sigrist for leaf sampling. We thank Karin Bleidissel for her support in the laboratory and Dieter Spinnler for statistics advice. Frank Hagedorn collected the fine root samples, and Inga Bucher provided the map of tree species for Fig. 3. The ongoing forest CO2 enrichment experiment is funded by the Swiss National Science Foundation project No. 3100-059769. The Swiss Canopy Crane is funded by the Swiss Agency for the Environment, Forests and Landscape (SAEFL).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rolf T. W. Siegwolf.

Appendix

Appendix

The regression line of a Keeling plot can be derived from a simple mass balance equation, where the isotopic 13C signature of atmospheric CO2 mixes with the 13C signature of soil respiratory CO2 (see Eqs. 1, 2):

$$ \delta ^{{13}} {\text{C}}_{{{\text{mixed}}}} [{\text{CO}}_{2} ]_{{{\text{mixed}}}} = \delta ^{{13}} {\text{C}}_{{{\text{atmosphere}}}} [{\text{CO}}_{2} ]_{{{\text{atmosphere}}}} + \delta ^{{13}} {\text{C}}_{{{\text{respired}}}} \;[{\text{CO}}_{2} ]_{{{\text{respired}}}} $$
(1)
$$[{\text{CO}}_{2} ]_{{{\text{mixed}}}} = [{\text{CO}}_{2} ]_{{{\text{atmosphere}}}} + [{\text{CO}}_{2} ]_{{{\text{respired}}}} $$
(2)

where δ13Cmixed is the δ13C of the analyzed soil gas sample, [CO2]mixed is the CO2-concentration of the analyzed soil gas sample, δ13Catmosphere is the atmospheric δ13C, [CO2]atmosphere is above the canopy the atmospheric CO2-concentration, δ13Crespired is the δ13C of respiratory CO2, and [CO2]respired is the CO2-concentration of respiratory CO2 in the soil.

Except for δ13Crespired and [CO2] respired all parameters can be measured. Thus the equations can be solved for δ13Crespired. The equation solved for δ13 Crespired corresponds to an individual Keeling plot based on two points (one point defined by atmospheric CO2 concentration and its δ13C, the other by the CO2 concentration of the soil air sample and its measured δ13C). The difference to the classic Keeling approach is that δ13Catmosphere and [CO2]atmosphere are assumed to be known.

Air samples collected 5–10 m above the canopy, showed highly variable values in both atmospheric CO2 concentrations and δ13C. It is likely that this variation was influenced by the vegetation and the CO2 enrichment experiment. Therefore we extrapolated the CO2 concentrations and δ13C values from different monitoring stations (Ireland, Mace Head, Count Galway 53°20′N 9°54′E 25 m a.s.l.; Azores, Terceira Island 38°46′N 27°23′E, 30 m a.s.l; Malta, Gozo 36°03′N 14°11′E 475 m a.s.l; Tenerife, Izana Observatory 28°18′N 2°00′E 7 m a.s.l) to the year 2001. Since both atmospheric CO2 and its appropriate δ13C vary seasonally due to a seasonal change in respiratory and photosynthetic activity of the vegetation, we used monthly data of the respective parameters. We assumed that the average of these data taken from different northern latitudes would give an approximate description of the free atmospheric CO2 around our experimental site and thus could be used for both, calculation of soil respiratory δ13C in the treated and control area.

Sensitivity analysis of the Keeling approach

Since our new approach of using the Keeling plot is not yet established, we tested its robustness by calculating the C isotopic signature for pure respiratory soil CO2 for every combination of atmospheric conditions in CO2 concentration (between 350 and 400 ppm in 1 ppm steps) and δ13C (between −9 and −7‰ in 0.1‰ steps). In general the sensitivity of the calculated soil respiratory δ13C towards changing atmospheric conditions decreases with increasing soil air CO2 concentrations. To be on the safe side, we performed a sensitivity analysis for a soil air sample with a CO2 concentration of 2,300 ppm (δ13 C=−20.8‰), as was found in October and November, the 2  months with lowest soil air CO2 concentrations. As shown in Fig. 8 the calculated isotopic value for pure respiratory CO2 changes less than 0.015 ‰ when atmospheric CO2 concentration shifts from 360 to 370 ppm (a shift which is related to ca. 0.5‰ in atmospheric δ13C). Even when the atmospheric δ13C is not adjusted to a change in atmospheric CO2 concentration, a shift of 10 ppm in atmospheric CO2 is followed by a potential error of less than 0.08‰ in the calculated respiratory δ13C. Therefore in the range of 360 ppm a change in atmospheric CO2 concentration of 10 ppm does not significantly affect the calculated δ13C value of respired CO2. The same modeling applied to a soil air sample with a CO2 concentration of 1,000 ppm (δ13C=−18.4‰) revealed a shift of less than 0.1 ‰ when the atmospheric CO2 concentration changed from 360 to 370 ppm. The maximal potential error was 0.2 ‰ when the related shift of 0.5‰ in atmospheric δ13C was not considered. Less than 3% of all soil air samples had a CO2 concentration lower than 1,000 ppm. In general the soil samples showed a high enough CO2 concentration so that the potential error of the calculated respiratory δ13C was below the measuring precision. Thus we conclude that our method of calculating the δ13C values of pure respiratory CO2 of every single soil air sample is sufficiently accurate and can be used to visualize the spatial variability of the biological δ13C input into the ground.

Fig. 8
figure 8

δ13C of pure respiratory CO2 for varying atmospheric CO2 concentration and atmospheric δ13C. For the simulation typical soil air CO2 concentration (2,300 ppm) and δ13C (−20.8‰) were used. A 10 ppm increase in atmospheric CO2, (roughly related to a decrease in atmospheric δ13C of 0.5‰, indicated by the arrow), results in a potential error of less than 0.1‰ (open triangle) in calculated soil respiratory CO2. See Appendix for details

Rights and permissions

Reprints and permissions

About this article

Cite this article

Steinmann, K., Siegwolf, R.T.W., Saurer, M. et al. Carbon fluxes to the soil in a mature temperate forest assessed by 13C isotope tracing. Oecologia 141, 489–501 (2004). https://doi.org/10.1007/s00442-004-1674-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-004-1674-4

Keywords

Navigation