, Volume 140, Issue 2, pp 340–351 | Cite as

Comparisons of δ13C of photosynthetic products and ecosystem respiratory CO2 and their responses to seasonal climate variability

  • Andrea Scartazza
  • Catarina Mata
  • Giorgio Matteucci
  • Dan Yakir
  • Stefano Moscatello
  • Enrico Brugnoli
Ecosystem Ecology


This study investigated the relationship between δ13C of ecosystem components, soluble plant carbohydrates and the isotopic signature of ecosystem respired CO213CR) during seasonal changes in soil and atmospheric moisture in a beech (Fagus sylvatica L.) forest in the central Apennine mountains, Italy. Decrease in soil moisture and increase in air vapour pressure deficit during summer correlated with substantial increase in δ13C of leaf and phloem sap soluble sugars. Increases in δ13C of ecosystem respired CO2 were linearly related to increases in phloem sugar δ13C (r2=0.99, P≤0.001) and leaf sugar δ13C (r2=0.981, P≤0.01), indicating that a major proportion of ecosystem respired CO2 was derived from recent assimilates. The slopes of the best-fit lines differed significantly (P≤0.05), however, and were about 0.86 (SE=0.04) for phloem sugars and about 1.63 (SE=0.16) for leaf sugars. Hence, changes in isotopic signature in phloem sugars were transferred to ecosystem respiration in the beech forest, while leaf sugars, with relatively small seasonal changes in δ13C, must have a slower turnover rate or a significant storage component. No significant variation in δ13C was observed in bulk dry matter of various plant and ecosystem components (including leaves, bark, wood, litter and soil organics). The apparent coupling between the δ13C of soluble sugars and ecosystem respiration was associated with large apparent isotopic disequilibria. Values of δ13CR were consistently more depleted by about 4‰ relative to phloem sugars, and by about 2‰ compared to leaf sugars. Since no combination of the measured pools could produce the observed δ13CR signal over the entire season, a significant isotopic discrimination against 13C might be associated with short-term ecosystem respiration. However, these differences might also be explained by substantial contributions of other not measured carbon pools (e.g., lipids) to ecosystem respiration or contributions linked to differences in footprint area between Keeling plots and carbohydrate sampling. Linking the seasonal and inter-annual variations in carbon isotope composition of carbohydrates and respiratory CO2 should be applicable in carbon cycle models and help the understanding of inter-annual variation in biospheric sink strength.


Biospheric carbon sink Beech forest Phloem sugar δ13Ecosystem respiration Net ecosystem exchange 



This work was supported in part by the European Community’s Human Potential Programme under contract HPRN-CT-1999-00059, NETCARB. C.M. also acknowledges the support provided by The European Community under the same contract. Collelongo experimental site is part of CARBOEUROFLUX network (Contract EVK2-CT-1999-00032) and of the Centre of Excellence “Forest and Climate” co-funded by The Italian Ministry of University and Scientific Research and by The University of Tuscia, Viterbo. The authors thank Prof. Giuseppe Scarascia Mugnozza for providing access to the Collelongo site and for useful discussion during the work and Dr. Alberto Battistelli for useful discussion on carbohydrates sampling methods. We are grateful to two anonymous reviewers for useful suggestions on the manuscript.


  1. Aubinet M, Grelle A, Ibrom A, Rannik Ü, Moncrieff J, Foken T, Kowalski AS, Martin PH, Berbigier P, Bernhofer C, Clement R, Elbers J, Granier A, Grünwald T, Morgenstern K, Pilegaard K, Rebmann C, Snijders W, Valentini R, Vesala T (2000) Estimates of the annual net carbon and water exchange of forests: the EUROFLUX methodology. Adv Ecol Res 30:113–175Google Scholar
  2. Bowling DR, Tans PP, Monson RK (2001) Partitioning net ecosystem carbon exchange with isotopic fluxes of CO2. Global Change Biol 7:127–145CrossRefGoogle Scholar
  3. Bowling DR, Mc Dowell NG, Bond BJ, Law BE, Ehleringer JR (2002) 13C content of ecosystem respiration is linked to precipitation and vapor pressure deficit. Oecologia 131:113–124CrossRefGoogle Scholar
  4. Brugnoli E, Farquhar GD (2000) Photosynthetic fractionation of carbon isotopes. In: Leegood RC, Sharkey TD, von Caemmerer S (eds) Advances in photosynthesis—photosynthesis: physiology and metabolism, vol 9. Kluwer, The Netherlands, pp 399–434Google Scholar
  5. Brugnoli E, Hubick KT, von Caemmerer S, Wong SC, Farquhar GD (1988) Correlation between carbon isotope discrimination in leaf starch and sugars of C3 plants and the ratio of intercellular and atmospheric partial pressures of carbon dioxide. Plant Physiol 88:1418–1424Google Scholar
  6. Buchmann N, Guehl J-M, Barigah TS, Ehleringer JR (1997a) Interseasonal comparison of CO2 concentrations, isotopic composition, and carbon dynamics in an Amazonian rainforest (French Guiana). Oecologia 110:120–131CrossRefGoogle Scholar
  7. Buchmann N, Kao WY, Ehleringer JR (1997b) Influence of stand structure on carbon-13 of vegetation, soils, and canopy air within deciduous and evergreen forests in Utah, United States. Oecologia 110:109–119CrossRefGoogle Scholar
  8. Buchmann N, Brooks JR, Flanagan LB, Ehleringer JR (1998) Carbon isotope discrimination of terrestrial ecosystems. In: Griffiths H (ed) Stable isotopes, integration of biological, ecological and geochemical processes. BIOS Scientific, Oxford, pp 203–221Google Scholar
  9. Buchmann N, Brooks JR, Ehleringer JR (2002) Predicting daytime carbon isotope ratios of atmospheric CO2 within forest canopies. Funct Ecol 16:49–57CrossRefGoogle Scholar
  10. Cutini A, Matteucci G, Scarascia Mugnozza G (1998) Estimation of leaf area index with the Li-Cor LAI 2000 in deciduous forests. For Ecol Manage 105:55–65CrossRefGoogle Scholar
  11. Damesin C, Lelarge C (2003) Carbon isotope composition of current-year shoots from Fagus sylvatica in relation to growth, respiration and use of reserves. Plant Cell Environ 26:207–219CrossRefGoogle Scholar
  12. Ehleringer JR, Bowling DR, Flanagan LB, Fessenden J, Helliker B, Martinelli LA, Ometto JP (2002) Stable isotopes and carbon cycle processes in forests and grasslands. Plant Biol 4:189–191CrossRefGoogle Scholar
  13. Ekblad A, Högberg P (2001) Natural abundance of 13C in CO2 respired from forest soils reveals speed of link between photosynthesis and root respiration. Oecologia 127:305–308CrossRefGoogle Scholar
  14. Farquhar GD, Ehleringer JR, Hubick KJ (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537Google Scholar
  15. Fessenden JE, Ehleringer JR (2003) Temporal variation in δ13C of ecosystem respiration in the Pacific Northwest: links to moisture stress. Oecologia 136:129–136CrossRefPubMedGoogle Scholar
  16. Flanagan LB, Ehleringer JR (1998) Ecosystem-atmosphere CO2 exchange: interpreting signals of change using stable isotope ratios. Trends Ecol Evol 13:10–14Google Scholar
  17. Flanagan LB, Brooks JR, Varney GT, Berry SC, Ehleringer JR (1996) Carbon isotope discrimination during photosynthesis and the isotope ratio of respired CO2 in boreal forest ecosystems. Global Biogeochem Cycles 10:629–640Google Scholar
  18. Flanagan LB, Brooks JR, Varney GT, Ehleringer JR (1997) Discrimination against C18O16O during photosynthesis and the oxygen isotope ratio of respired CO2 in boreal forest ecosystems. Global Biogeochem Cycles 11:83–98CrossRefGoogle Scholar
  19. Francey RJ, Gifford RM, Sharkey TD, Weir B (1985) Physiological influences on carbon isotope discrimination in huon pine (Lagarostrobos franklinii). Oecologia 66:211–218Google Scholar
  20. Fung IY, Field CB, Berry JA, Thompson MV, Randerson TJ, Malmström CM, Vitousek PM, Collatz GJ, Sellers PJ, Randall DA, Denning AS, Badeck F, John J (1997) Carbon-13 exchanges between the atmosphere and biosphere. Global Biogeochem Cycles 11:507–533Google Scholar
  21. Geßler A, Schrempp S, Matzarakis A, Mayer H, Rennenberg H, Adams MA (2001) Radiation modifies the effect of water availability on the carbon isotope composition of beech (Fagus sylvatica L.). New Phytol 50:653–664Google Scholar
  22. Gleixner G, Schmidt H-L (1997) Carbon isotope effects on the fructose-1,6-bisphosphate aldolase reaction, origin for non-statistical 13C distributions in carbohydrates. J Biol Chem 272:5382–5387CrossRefPubMedGoogle Scholar
  23. Harris D, Horwath WR, van Kessel C (2001) Acid fumigation of soils to remove carbonates prior to total organic carbon or carbon-13 isotopic analysis. Soil Sci Soc Am J 65:1853–1856Google Scholar
  24. Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Löfvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792PubMedGoogle Scholar
  25. Janssens IA, Lankreijer H, Matteucci G, Kowalski AS, Buchmann N, Epron D, Pilegaard K, Kutsch W, Longdoz B, Grünwald T, Montagnani L, Dore S, Rebmann C, Moors EJ, Grelle A, Rannik Ü, Morgenstern K, Oltchev S, Clement R, Guômundsson J, Minerbi S, Berbigier P, Ibrom A, Moncrieff J, Aubinet M, Bernhofer C, Jensen NO, Vesala T, Granier A, Schulze E-D, Lindroth A, Dolman AJ, Jarvis PG, Ceulemans R, Valentini R (2001) Productivity overshadows temperature in determining soil and ecosystem respiration across European forests. Global Change Biol 7:269–278CrossRefGoogle Scholar
  26. Keeling CD (1958) The concentration and isotopic abundances of atmospheric carbon dioxide in rural areas. Geochim Cosmochim Acta 13:322–334Google Scholar
  27. Keeling CD (1961) The concentration and isotopic abundances of atmospheric carbon dioxide in rural and marine areas. Geochim Cosmochim Acta 24:277–298CrossRefGoogle Scholar
  28. Lin G, Ehleringer JR (1997) Carbon isotope fractionation does not occur during dark respiration in C3 and C4 plants. Plant Physiol 114:391–394Google Scholar
  29. Lloyd J, Farquhar GD (1994) 13C discrimination during CO2 assimilation by the terrestrial biosphere. Oecologia 99:201–215Google Scholar
  30. Lloyd J, Kruijt B, Hollinger DY, Grace J, Francey RJ, Wong S-C, Kelliher FM, Miranda AC, Farquhar GD, Gash JHC, Vygodskaya NN, Wright IR, Miranda HS, Schulze E-D (1996) Vegetation effects on the isotopic composition of atmospheric CO2 at local and regional scales: theoretical aspects and a comparison between a rain forest in Amazonia and a boreal forest in Siberia. Aust J Plant Physiol 23:371–399Google Scholar
  31. Matteucci G (1998) Bilancio del Carbonio in una Faggeta dell’Italia Centro-Meridionale: Determinanti Ecofisiologici, Integrazione a Livello di Copertura e Simulazione dell’Impatto dei Cambiamenti Ambientali. PhD thesis, Università degli Studi di PadovaGoogle Scholar
  32. Matteucci G, Dore S, Stivanello S, Rebmann C, Buchmann N (2000) Soil respiration in beech and spruce forests in Europe: trends, controlling factors, annual budgets and implications for the ecosystem carbon balance. In: Schulze E-D (ed) Carbon and nitrogen cycling in European forest ecosystems. Ecological Studies, vol 142. Springer, Berlin Heidelberg New York, pp 217–236Google Scholar
  33. Ometto JPHB, Flanagan LB, Martinelli LA, Moreira MZ, Higuchi N, Ehleringer J (2002) Carbon isotope discrimination in forest and pasture ecosystems of the Amazon basin, Brazil. Global Biogeochem Cycles 16:1–10CrossRefGoogle Scholar
  34. Pataki DE, Ehleringer JR, Flanagan LB, Yakir D, Bowling DR, Still CJ, Buchmann N, Kaplan JO, Berry JA (2003) The application and interpretation of Keeling plots in terrestrial carbon cycle research. Global Biogeochem Cycles 17:1022. DOI 10.1029/2001 GB001850CrossRefGoogle Scholar
  35. Pate JS, Arthur D (1998) δ13C analysis of phloem sap carbon: novel means of evaluating seasonal water stress and interpreting carbon isotope signatures of foliage and trunk wood of Eucalyptus globulus. Oecologia 117:301–311CrossRefGoogle Scholar
  36. Sokal RR, Rohlf FJ (1995) Biometry. Freeman, New YorkGoogle Scholar
  37. Tcherkez G, Nogués S, Bleton J, Cornic G, Badeck F, Ghashghaie J (2003) Metabolic origin of carbon isotope composition of leaf dark-respired CO2 in French bean. Plant Physiol 131:237–244CrossRefPubMedGoogle Scholar
  38. Valentini R, De Angelis P, Matteucci G, Monaco R, Dore S, Scarascia Mugnozza G (1996) Seasonal net carbon dioxide exchange of a Beech forest with the atmosphere. Global Change Biol 2:199-207Google Scholar
  39. Valentini R, Matteucci G, Dolman AJ, Schulze E-D, Rebmann C, Moors EJ, Granier A, Gross P, Jensen NO, Pilegaard K, Lindroth A, Grelle A, Bernhofer C, Grünwald T, Aubinet M, Ceulemans R, Kowalski AS, Vesala T, Rannik Ü, Berbigier P, Loustau D, Guômundsson J, Thorgeirsson H, Ibrom A, Morgenstern K, Clement R, Moncrieff J, Montagnani L, Minerbi S, Jarvis PG (2000) Respiration as the main determinant of carbon balance in European forest. Nature 404:861–865CrossRefPubMedGoogle Scholar
  40. Yakir D, Sternberg L da SL (2000) The use of stable isotopes to study ecosystem gas exchange. Oecologia 123:297–311CrossRefGoogle Scholar
  41. Yakir D, Wang X-F (1996) Fluxes of CO2 and water between terrestrial vegetation and the atmosphere estimated from isotope measurements. Nature 380:515–517Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Andrea Scartazza
    • 1
  • Catarina Mata
    • 1
  • Giorgio Matteucci
    • 2
    • 4
  • Dan Yakir
    • 3
  • Stefano Moscatello
    • 1
  • Enrico Brugnoli
    • 1
  1. 1.CNRIstituto di Biologia Agroambientale e ForestalePorano (TR)Italy
  2. 2.DISAFRIUniversità della TusciaViterboItaly
  3. 3.Environmental Sciences and Energy ResearchWeizmann Institute of ScienceRehovotIsrael
  4. 4.Joint Research CentreInstitute for Environment and SustainabilityIspra (VA)Italy

Personalised recommendations