, Volume 144, Issue 1, pp 45–54 | Cite as

Association between tree-ring and needle δ13C and leaf gas exchange in Pinus halepensis under semi-arid conditions

  • Tamir Klein
  • Deborah Hemming
  • Tongbao Lin
  • José M. Grünzweig
  • Kadmiel Maseyk
  • Eyal Rotenberg
  • Dan YakirEmail author


Associations between δ13C values and leaf gas exchanges and tree-ring or needle growth, used in ecophysiological compositions, can be complex depending on the relative timing of CO2 uptake and subsequent redistribution and allocation of carbon to needle and stem components. For palaeoenvironmental and dendroecological studies it is often interpreted in terms of a simple model of δ13C fractionation in C3 plants. However, in spite of potential complicating factors, few studies have actually examined these relationships in mature trees over inter- and intra-annual time-scales. Here, we present results from a 4 years study that investigated the links between variations in leaf gas-exchange properties, growth, and dated δ13C values along the needles and across tree rings of Aleppo pine trees growing in a semi-arid region under natural conditions or with supplemental summer irrigation. Sub-sections of tissue across annual rings and along needles, for which time of formation was resolved from growth rate analyses, showed rapid growth and δ13C responses to changing environmental conditions. Seasonal cycles of growth and δ13C (up to ~4‰) significantly correlated (P<0.01) with photosynthetically active radiation, vapour pressure deficit, air temperature, and soil water content. The irrigation significantly increased leaf net assimilation, stomatal conductance and needle and tree-ring growth rate, and markedly decreased needle and tree-ring δ13C values and its sensitivity to environmental parameters. The δ13C estimates derived from gas-exchange parameters, and weighted by assimilation, compared closely with seasonal and inter-annual δ13C values of needle- and tree-ring tissue. Higher stomatal conductances of the irrigated trees (0.22 vs. 0.08 mol m−2 s−1 on average) corresponded with ~2.0‰ lower average δ13C values, both measured and derived. Derived and measured δ13C values also indicated that needle growth, which occurs throughout the stressful summer was supported by carbon from concurrent, low rate assimilation. For Aleppo pine under semi-arid and irrigated conditions, the δ13C of tree-ring and needle material proved, in general, to be a reasonable indicator of integrated leaf gas-exchange properties.


13C discrimination Soil moisture Dendroecology Stomatal conductance Carbon allocation 



We thank Emanuela Negreanu for technical expertise and help with the δ13C analyses. Funding of this project was provided by the Israel Science Foundation (ISF), the European Union (Carboeuroflux), the US-Israel Binational Science Foundation (BSF) and the International Arid Land Consortium (IALC). DH and DY acknowledge the financial support provided through the European Community’s Human Potential Programme under contract HPRN-CT-1999-00059, NETCARB. (Declaration: all experiments in this research comply with the current law of Israel.)


  1. Coplen TB (1994) Reporting of stable hydrogen, carbon, and oxygen isotopic abundances. Pure Appl Chem 66:273–276CrossRefGoogle Scholar
  2. Dawson TE, Ward JK, Ehleringer JR (2004) Temporal scaling of physiological responses from gas exchange to tree rings: a gender-specific study of Acer negundo (Boxelder) growing under different conditions. Funct Ecol 18:212–222CrossRefGoogle Scholar
  3. Ehleringer JR, Hall AE, Farquhar GD (1993) Stable isotopes and plant carbon-water relations. Academic, San DiegoGoogle Scholar
  4. Evans JR, Sharkey TD, Berry JA, Farquhar GD (1986) Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants. Aust J Plant Phys 13:281–292Google Scholar
  5. Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and intercellular carbon dioxide concentration in leaves. Aust J Plant Phys 9:121–137CrossRefGoogle Scholar
  6. Feng X, Epstein S (1995) Carbon isotopes of trees from arid environments and implications for reconstructing atmospheric CO2 concentration. Geochim Cosmochim Acta 59:2599–2608CrossRefGoogle Scholar
  7. Ferrio JP, Florit A, Vega A, Serrano L, Voltas J (2003) Δ 13 C and tree-ring width reflect different drought responses in Quercus ilex and Pinus halepensis. Oecologia 442:512–518CrossRefGoogle Scholar
  8. Fritts HC (1976) Tree rings and climate. Academic, LondonGoogle Scholar
  9. Gleixner G, Danier HJ, Werner RA, Schmidt HL (1993) Correlations between the 13C content of primary and secondary plant products in different cell compartments and that in decomposing basidiomycetes. Plant Physiol 102:1287–1290PubMedGoogle Scholar
  10. Grunwald C, Schiller G (1988). Needle xylem water potential and water saturation deficit in provenances of Pinus halepensis Mill. and P. brutia Ten. Forêt méditerranéene 10:407–414Google Scholar
  11. Grünzweig JM, Lin T, Rotenberg E, Schwartz A, Yakir D (2003) Carbon sequestration in arid-land forest. Global Change Biol 9:791–799CrossRefGoogle Scholar
  12. Hemming D, Fritts HC, Leavitt SW, Wright W, Long A, Shashkin A (2001) Modelling tree-ring δ13C. Dendrochronologia 19(1):23–38Google Scholar
  13. IPCC (2001) Climate change: the scientific basis. Cambridge University Press, CambridgeGoogle Scholar
  14. Leavitt SW, Long A (1989) The atmospheric δ13C record as derived from 56 pinyon trees at 14 sites in the southwestern United States. Radiocarbon 31:469–474Google Scholar
  15. Lev-Yadun S (2000) Cellular patterns in dicotyledonous woods: their regulation. In: Savidge R, Barnett J and Napier R (eds) Cell and molecular biology of wood formation, vol 25. BIOS Scientific Publishers, Oxford, pp 315–324Google Scholar
  16. Lev-Yadun S, Liphschitz N, Waisel Y (1981) Dendrochronological investigations in Israel: Pinus halepensis—the oldest living pines in Israel. La-Yaaran 31:1–8, 49–52 (in Hebrew)Google Scholar
  17. Liphschitz N, Lev-Yadun S (1986) Cambial activity of evergreen and seasonal dimorphics around the Mediterranean. IAWA Bull 7(2):145–153Google Scholar
  18. Loader NJ, Switsur VR, Field EM (1995) High-resolution stable isotope analysis of tree rings: implications of ‘microdendroclimatology’ for palaeoenvironmental research. Holocene 5(4):457–460CrossRefGoogle Scholar
  19. Marshall JD, Monserud RA (1996) Homeostatic gas-exchange parameters inferred from 13C/12C in tree rings of conifers. Oecologia 105:13–21CrossRefGoogle Scholar
  20. Melzack RN, Bravdo B, Riov J (1985) The effect of water stress on photosynthesis and related parameters in Pinus halepensis. Physiol Plant 64:295–300CrossRefGoogle Scholar
  21. Noormets A, McDonald EP, Dickson RE, Kruger EL, Sober A, Isebrands JG, Karnosky DF (2001) The effect of elevated carbon dioxide and ozone on leaf- and branch-level photosynthesis and potential plant-level carbon gain in aspen. Trees 15:262–270CrossRefGoogle Scholar
  22. Ogle N, McCormac FG (1994) High-resolution δ13C measurements of oak show a previously unobserved spring depletion. Geophys Res Lett 21(22):2373–2375CrossRefGoogle Scholar
  23. Robertson I, Switsur VR, Carter AHC, Barker AC, Waterhouse JS, Briffa KF, Jones PD (1997) Signal strength and climate relationships in 13C/12C ratios of tree ring cellulose from oak in east England. J Geophys Res 102(D16):19507–19516CrossRefGoogle Scholar
  24. Saurer M, Siegenthaler U (1989) 13C/12C isotope ratios in trees are sensitive to relative humidity. Dendrochronologia 7:9–13Google Scholar
  25. Scartazza A, Mata C, Matteucci G, Yakir D, Moscatello S, Brugnoli E (2004) Comparisons of δ13C of photosynthetic products and ecosystem respiratory CO2 and their responses to seasonal climate variability. Oecologia 140:340–351CrossRefPubMedGoogle Scholar
  26. Schiller G, Cohen Y (1998) Water balance of a Pinus halepensis Mill. afforestations in an arid region. For Ecol Manag 105:121–128CrossRefGoogle Scholar
  27. Schleser GH (1985) Parameters determining carbon isotope ratios in plants. In: Frenzel B (ed) Problems of stable isotopes in tree-rings, lake-sediments and peat-bogs as climatic evidence for the Holocene. Palaeoclim Res 15:71–96Google Scholar
  28. Schleser GH, Frielingsdorf J, Blair A (1999) Carbon isotope behaviour in wood and cellulose during artificial aging. Chem Geol 158:121–130CrossRefGoogle Scholar
  29. Schweingruber FH (1996) Tree rings and environment dendroecology. Paul Haupt, BernGoogle Scholar
  30. Switsur VR, Waterhouse J (1989) Stable isotopes in tree ring cellulose. In: Griffiths H (ed) Stable Istopes: Integration of biological, ecological and geochemical processes, vol 18. BIOS Scientific Publishers, Oxford, pp 303–321Google Scholar
  31. Tcherkez G, Nogues 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(1):237–244CrossRefPubMedGoogle Scholar
  32. Terwilliger VJ, Huang J (1996) Heterotrophic whole plant tissues show more C-13 enrichment than their carbon sources. Phytochemistry 43(6):1183–1188CrossRefGoogle Scholar
  33. Van der Water PK, Leavitt SW, Betancourt JL (1994) Trends in stomatal density and 13C/12C ratios of Pinus flexilis needles during last glacial-interglacial cycle. Science 264:239–243PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Tamir Klein
    • 1
  • Deborah Hemming
    • 1
    • 2
  • Tongbao Lin
    • 1
  • José M. Grünzweig
    • 1
  • Kadmiel Maseyk
    • 1
  • Eyal Rotenberg
    • 1
  • Dan Yakir
    • 1
    Email author
  1. 1.Department of Environmental Science and Energy ResearchWeizmann Institute of ScienceRehovotIsrael
  2. 2.Hadley Centre for Climate Prediction and Research, Met OfficeExeterUK

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