The long way down - Are carbon and oxygen isotope signals in the tree ring uncoupled from canopy physiological processes?

Tree Physiology

Volumn 31, Issue 10, 2011, Pages 1088-1102

  Offermann, Christine ^a   Ferrio, Juan Pedro ^b   Holst, Jutta ^a   Grote, Rüdiger ^c   Siegwolf, Rolf ^d   Kayler, Zachary ^e   Gessler, Arthur ^e  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF LLEIDA   (Spain)

^c KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^d PAUL SCHERRER INSTITUTE   (Switzerland)

^e LEIBNIZ CENTRE FOR AGRICULTURAL LANDSCAPE RESEARCH ZALF   (Germany)

Author keywords

evaporative enrichment; oxygen atom exchange; phloem transport; post photosynthetic isotope fractionation

Indexed keywords

CARBON; OXYGEN; WATER;

ANNUAL VARIATION; CANOPY; CARBOHYDRATE; CARBON ISOTOPE; DENDROCHRONOLOGY; DEVELOPMENTAL BIOLOGY; ENVIRONMENTAL MONITORING; GENETIC ANALYSIS; GROWING SEASON; ISOTOPIC COMPOSITION; ISOTOPIC FRACTIONATION; OXYGEN ISOTOPE; PHLOEM; PHOTOSYNTHESIS; RECONSTRUCTION; SIGNAL; SOIL WATER; STABLE ISOTOPE; TIMESCALE; TREE RING; WATER VAPOR;

ARTICLE; BEECH; GERMANY; METABOLISM; PHLOEM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT LEAF; PLANT STOMA; SOIL; SUNLIGHT; TEMPERATURE; WOOD;

CARBON; CARBON ISOTOPES; FAGUS; GERMANY; OXYGEN; OXYGEN ISOTOPES; PHLOEM; PHOTOSYNTHESIS; PLANT LEAVES; PLANT STOMATA; SOIL; SUNLIGHT; TEMPERATURE; WATER; WOOD;

FAGUS SYLVATICA;

EID: 80054688552     PISSN: 0829318X     EISSN: 17584469     Source Type: Journal    
DOI: 10.1093/treephys/tpr093     Document Type: Article

References (77)

1. Barbour, M. 2007. Stable oxygen isotope composition of plant tissue: a review. Funct. Plant Biol. 34:83-94.
2. Barbour, M., R. Fischer, K. Sayre and G. Farquhar. 2000. Oxygen isotope ratio of leaf and grain material correlates with stomatal conductance and grain yield in irrigated wheat. Aust. J. Plant Physiol. 27:625-637. (Pubitemid 30610365)
3. 13C and δ13O of cellulose from growth rings of Pinus radiata. Plant, Cell Environ. 25:1483-1499. (Pubitemid 35241047)
4. Barnard, R., Y. Salmon, N. Kodama, K. Sörgel, J. Holst, H. Rennenberg, A. Gessler and N. Buchmann. 2007. Evaporative enrichment and time lags between δ13O of leaf water and organic pools in a pine stand. Plant, Cell Environ. 30:539-550. (Pubitemid 46537713)
5. 2 fluxes. New Phytol. 178:28-40.
6. Brandes, E., N. Kodama, K. Whittaker, C. Weston, H. Rennenberg, C. Keitel, M. Adams and A. Gessler. 2006. Short-term variations in the isotope signatures of organic matter allocated from the leaves to the axis of Pinus sylvestris - effects of photosynthetic and post-photosynthetic carbon isotope fractionation. Global Change Biol. 12: 1922-1939. (Pubitemid 44383515)
7. Brandes, E., J. Wenninger, P. Koeniger, D. Schindler, H. Rennenberg, C. Leibundgut, H. Mayer and A. Gessler. 2007. Assessing environmental and physiological controls over water relations in a Scots pine (Pinus sylvestris L.) stand through analyses of stable isotope composition of water and organic matter. Plant, Cell Environ. 30:113-127. (Pubitemid 44924285)
8. Brugnoli, E., K. Hubick, S. von Caemmerer, S. Wong and G. Farquhar. 1988. Correlation between the carbon isotope discrimination in leaf starch and sugars of C-3 plants and the ratio of intercellular and atmospheric partial pressures of carbon-dioxide. Plant Physiol. 88:1418-1424.
9. Burk, R. and M. Stuiver. 1981. Oxygen isotope ratios in trees reflect mean annual temperature and humidity. Science 211:1417-1419.
10. Cernusak, L., D. Arthur, J. Pate and G. Farquhar. 2003. Water relations link carbon and oxygen isotope discrimination to phloem sap sugar concentration in Eucalyptus globulus. Plant Physiol. 131: 1544-1554. (Pubitemid 36463584)
11. Cernusak, L., G. Farquhar and J. Pate. 2005. Environmental and physiological controls over oxygen and carbon isotope composition of Tasmanian blue gum, Eucalyptus globulus. Tree 25:129-146. (Pubitemid 40290096)
12. Cernusak, L., G. Tcherkez, C. Keitel, et al. 2009. Viewpoint: Why are non-photosynthetic tissues generally C-13 enriched compared with leaves in C-3 plants?. Review and synthesis of current hypotheses. Funct. Plant Biol. 36:199-213.
13. Craig, H. and L. Gordon. 1965. Deuterium and oxygen-18 variations in the ocean and the marine atmosphere. In Proceedings of the Conference on Stable Isotopes in Oceanographic Studies and Palaeotemperatures in Spoletto, 1965. Ed. E. Tongiorgi. Consiglio Nazionale delle Ricerche Laboratorio di Geologia Nucleare, Pisa, Italy, pp. 9-130.
14. Dawson, T., J. Ward and J. Ehleringer. 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. 18:212-222. (Pubitemid 38504285)
15. Devaux, M., J. Ghashghaie, D. Bert, C. Lambrot, A. Gessler, C. Bathellier, J.Ogée and D. Lousteau. 2009. Carbon stable isotope ratio of phloem sugars in mature pine trees throughout the growing season: comparison of two extraction methods. Rapid Commun. Mass Spectrom. 23:2511-2518.
16. 18O in the leaves of transpiring plants. Rad. Environ. Biophys. 11:41-52.
17. Ehleringer, J., J. Roden and T. Dawson. 2000. Assessing ecosystemlevel water relations through stable isotope ratio analyses. Springer Verlag, New York, pp 181-198.
18. Farquhar, G. and L. Cernusak. 2005. On the isotopic composition of leaf water in the non-steady state. Funct. Plant Biol. 32:293-303. (Pubitemid 40728154)
19. Farquhar, G. and J. Lloyd. 1993. carbon and oxygen isotope effects in the exchange of carbon dioxide between terrestrial plants and the atmosphere. In Stable Isotopes and Plant Carbon Water Relations. eds. J.R. Ehleringer, A.E. Hall and G.D. Farquhar. Academic Press, San Diego, CA, USA, pp 47-70.
20. Farquhar, G., M. O'Leary and J. Berry. 1982. On the relationship between carbon isotope discrimination and the intercellular carbon-dioxide concentration in leaves. Aust. J. Plant Physiol. 9:121-137. (Pubitemid 13280643)
21. Farquhar, G., M. Barbour and B. Henry. 1998. Interpretation of oxygen isotope composition of leaf material. In Stable Isotopes-Integration of Biological, Ecological and Geochemical Processes. ed. H. Griffiths. Bios Scientific Publishers, Oxford, pp 24-27.
22. Ferrio, J., and J. Voltas. 2005. Carbon and oxygen isotope ratios in wood constituents of Pinus halepensis as indicators of precipitation, temperature and vapour pressure deficit. Tellus Series B-Chem. Phys. Meteorol. 57:164-173. (Pubitemid 40473113)
23. Ferrio, J., M. Cuntz, C. Offermann, R. Siegwolf, M. Saurer and A. Gessler. 2009. Effect of water availability on leaf water isotopic enrichment in beech seedlings shows limitations of current fractionation models. Plant, Cell Environ. 32:1285-1296.
24. Gessler, A., S. Schrempp, A. Matzarakis, H. Mayer, H. Rennenberg and M. Adams. 2001. Radiation modifies the effect of water availability on the carbon isotope composition of beech (Fagus sylvatica). New Phytol. 150:653-664. (Pubitemid 32602213)
25. Gessler, A., H. Rennenberg and C. Keitel. 2004. Stable isotope composition of organic compounds transported in the phloem of European beech-evaluation of different methods of phloem sap collection and assessment of gradients in carbon isotope composition during leaf-to-stem transport. Plant Biol. 6:721-729. (Pubitemid 39623055)
26. Gessler, A., A.D. Peuke, C. Keitel and G.D. Farquhar. 2007. Oxygen isotope enrichment of organic matter in Ricinus communis during the diel course and as affected by assimilate transport. New Phytol. 174:600-613. (Pubitemid 46640461)
27. Gessler, A., E. Brandes, N. Buchmann, G. Helle, H. Rennenberg and R. Barnard. 2009a. Tracing carbon and oxygen isotope signals from newly assimilated sugars in the leaves to the tree-ring archive. Plant, Cell Environ. 32:780-795.
28. 18O in adult beech (Fagus sylvatica) trees: relation to meteorological and gas exchange parameters. Tree Physiol. 29:1349-1365.
29. Gleixner, G., C. Scrimgeour, H.-L. Schmidt and R. Viola. 1998. Stable isotope distribution in the major metabolites of source and sink organs of Solanum tuberosum L.: a powerful tool in the study of metabolic partitioning in intact plants. Planta 207:241-245. (Pubitemid 29051685)
30. Grissino-Mayer, H. 2001. Evaluating crossdating accuracy: a manual and tutorial for the computer program COFECHA. Tree-ring Res. 57:205-221.
31. 2 fixation by Rubisco - an interpretation of 13C/12C variations in tree rings from novel intra-seasonal studies on broad-leaf trees. Plant, Cell Environ. 27:367-380. (Pubitemid 38300543)
32. Hill, S.A., J.S. Waterhouse, E.M. Field, V.R. Switsur and T. Ap Rees. 1995. Rapid recycling of triose phosphates in oak stem tissue. Plant, Cell Environ. 18:931-936.
33. Hobbie, E.A. and R.A. Werner. 2004. Intramolecular, compound-specific, and bulk carbon isotope patterns in C-3 and C-4 plants: a review and synthesis. New Phytol. 161:371-385. (Pubitemid 38126950)
34. Holm, S. 1979. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6:65-70.
35. Holmes, R. 1983. Computer-assisted quality control in tree-ring dating and measurement. Tree-Ring Bull. 43:69-78.
36. Holst, T., S. Hauser, A. Kirchgäßner, A. Matzarakis, H. Mayer and D. Schindler. 2004. Measuring and modelling plant area index in beech stands. Int. J. Biometeorol. 48:192-201. (Pubitemid 38819124)
37. Holst, J., R. Grote, C. Offermann, J. Ferrio, A. Gessler, H. Mayer and H. Rennenberg. 2010. Water fluxes within beech stands in complex terrain. Int. J. Biometeorol. 54:23-36.
38. Jones, H. 1992. Plants and microclimate. Cambridge University Press, Cambridge, UK.
39. 2 pulse-labelling of photoassimilates reveals carbon allocation within and between tree rings. Plant, Cell Environ. 29:1571-1584. (Pubitemid 44362269)
40. 13C pulse-labeled photoassimilate in naturally growing Larix gmelinii saplings. New Phytol. 171:793-804. (Pubitemid 44175199)
41. Keitel, C., M.A. Adams, T. Holst, A. Matzarakis, H. Mayer, H. Rennenberg and A. Gessler. 2003. Carbon and oxygen isotope composition of organic compounds in the phloem sap provides a short-term measure for stomatal conductance of European beech Fagus sylvatica L. Plant, Cell Environ. 26:1157-1168. (Pubitemid 36900898)
42. Keitel, C., A. Matzarakis, H. Rennenberg and A. Gessler. 2006. Carbon isotopic composition and oxygen isotopic enrichment in phloem and total leaf organic matter of European beech (Fagus sylvatica L.) along a climate gradient. Plant, Cell Environ. 29:1492-1507. (Pubitemid 44356587)
43. 13C and leaf gas exchange in Pinus halapensis under semi-arid conditions. Oecologia 144:45-54. (Pubitemid 41175370)
44. Korol, R., M. Kirschbaum, G. Farquhar and M. Jeffreys. 1999. Effects of water status and soil fertility on the C-isotope signature in Pinus radiata. Tree Physiol. 19:551-562. (Pubitemid 29326289)
45. 13C of tree rings. J. Geophys. Res. Atmos. 112:D06107.
46. Leavitt, S.W. and A. Long. 1986. Stable carbon isotope variability in tree foliage and wool. Ecology 67:1002-1010.
47. Leavitt, S.W. and A. Long. 1991. Seasonal stable-carbon isotope variability in tree rings: possible paleoenvironmental signals. Chem. Geol. (Isot. Geosci. Sect.) 87:59-70.
48. Li, C., S. Frolking and T.A. Frolking. 1992. A model of nitrous oxide evolution from soil driven by rainfall events: 1. Model structure and sensitivity. J. Geophys. Res. 97:9759-9776. (Pubitemid 23372966)
49. Libby, L., L. Pandolfi, P. Payton, J. Marshall, B. Becker and V. Giertz- Siebenlist. 1976. Isotopic tree thermometers. Nature 261:284-288.
50. Loader, N.J. and V.R. Switsur. 1996. Reconstructing past environmental change using stable isotopes in tree-rings. Bot. J. Scotland 48:65-78.
51. Loader, N.J., V.R. Switsur and E.M. Field. 1995. High-resolution stable isotope analysis of tree rings: implications of 'microdendroclimatology' for palaeoenvironmental research. Holocene 5:457-460. (Pubitemid 3005130)
52. McCarroll, D. and N. Loader. 2004. Stable isotopes in tree rings. Quaternary Sci. Rev. 23:771-801. (Pubitemid 38355769)
53. McCarroll, D. and F. Pawellek. 2001. Stable carbon isotope ratios of Pinus sylvestris from northern Finland and the potential for extracting a climate signal from long Fennoscandian chronologies. Holocene 11:517-526. (Pubitemid 32770149)
54. Nahm, M., T. Holst, A. Matzarakis, H. Mayer, H. Rennenberg and A. Gessler. 2006. Soluble N compound profiles and concentrations in European beech (Fagus sylvatica L) a re i nfluenced by l ocal c limate and thinning. Eur. J. For. Res. 125:1-14.
55. Ogee, J., M. Barbour, L. Wingate, et al. 2009. A single-substrate model to interpret intra-annual stable isotope signals in tree-ring cellulose. Plant, Cell Environ. 32:1071-1090.
56. Pendall, E., G. William and S. Leavitt. 2005. Comparison of measured and modelled variations in pinon pine leaf water isotopic enrichment across a summer moisture gradient. Oecologia 145:605-618. (Pubitemid 41437696)
57. Poussart, P.F., M.N. Evans and D.P. Schrag. 2004. Resolving seasonality in tropical trees: multi-decade, high resolution oxygen and carbon isotope records from Indonesia and Thailand. Earth Planet. Sci. Lett. 218:301-316. (Pubitemid 38204456)
58. R Development Team. 2008. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
59. 13C time series. Chem. Geol. 252:72-79.
60. Roden, J. and J.R. Ehleringer. 1999. Hydrogen and oxygen isotope ratios of tree-ring cellulose for riparian trees grown long-term under hydroponically controlled environments. Oecologia 121:467-477. (Pubitemid 30031117)
61. Roden, J.S., J. Johnstone and T.E. Dawson. 2009. Intra-annual variation in the stable oxygen and carbon isotope ratios of cellulose in tree rings of coast redwood (Sequoia sempervirens). Holocene 19:189-197.
62. Rozanski, K., L. Araguás-Araguás and R. Gonfiantini. 1992. Relation between long-term trends of oxygen-18 isotope composition of precipitation and climate. Science 258:981-985. (Pubitemid 23375565)
63. 18O of the growing season precipitation. Tellus 49:80-92.
64. Scheidegger, Y., M. Saurer, M. Bahn and R. Siegwolf. 2000. Linking stable oxygen and carbon isotopes with stomatal conductance and photosynthetic capacity: a conceptual model. Oecologia 125: 350-357.
65. Schmidt, H.-L. 2003. Fundamentals and systematics of the non-statistical distributions of isotopes in natural compounds. Naturwissenschaften 90:537-552. (Pubitemid 38037289)
66. 18O pattern and biosynthesis of natural plant products. Phytochemistry 58:9-32. (Pubitemid 32750845)
67. Schneider, S., A. Gessler, P. Weber, D. v. Sengbusch, U. Hanemann and H. Rennenberg. 1996. Soluble N compounds in trees exposed to high loads of N: a comparison of spruce (Picea abies) and beech (Fagus sylvatica) grown under field conditions. New Phytol. 134:103-114. (Pubitemid 126556727)
68. Sternberg, L. 2009. Oxygen stable isotope ratios of tree-ring cellulose: the next phase of understanding. New Phytol. 181:553-562.
69. Sternberg, L. and M.J. DeNiro. 1983. Bio-geochemical implications of the isotopic equilibrium fractionation factor between oxygen atoms of acetone and water. Geochim. Cosmochim. Acta 47:2271-2274.
70. Sternberg, L.D.S., M.J. Deniro and A. Savidge. 1986. Oxygen isotope exchange between metabolites and water during biochemical reactions leading to cellulose synthesis. Plant Physiol. 82:423-427.
71. Tcherkez, G. and G. Farquhar. 2005. Carbon isotope effect predictions for enzymes involved in the primary carbon metabolism of plant leaves. Funct. Plant Biol. 32:277-291. (Pubitemid 40728153)
72. Treydte, K., D. Frank, J. Esper, et al. 2007. Signal strength and climate calibration of a European tree-ring isotope network. Geophys. Res. Lett. 34:6.
73. van Bel, A. 2003. The phloem, a miracle of ingenuity. Plant, Cell Environ. 26:125-149. (Pubitemid 36117284)
74. White, J.W., J.R. Lawrence and W.S. Broecker. 1994. Modeling and interpreting D/H ratios in tree rings: A test case of white pine in northeastern United States. Geochim. Cosmochim. Acta 58: 851-862. (Pubitemid 24423749)
75. Wilson, A.T. and M.J. Grinsted. 1975. Palaeotemperatures from tree rings and the D/H ratio of cellulose as a biochemical thermometer. Nature 257:387-388.
76. Wittmann, C., G. Aschan and H. Pfanz. 2001. Leaf and twig photosynthesis of young beech (Fagus sylvatica) and aspen (Populus tremula) trees grown under different light regimes. Basic Appl. Ecol. 2: 145-154. (Pubitemid 32442410)
77. Yakir, D. and M. Deniro. 1990. Oxygen and hydrogen isotope fractionation during cellulose metabolism in Lemna gibba. Plant Physiol. 93:325-332. (Pubitemid 120029875)