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Plant and Soil

, Volume 291, Issue 1–2, pp 93–107 | Cite as

Hydrogen isotope fractionation during water uptake by woody xerophytes

  • Patrick Z. Ellsworth
  • David G. Williams
Original Paper

Abstract

Stable isotope measurements are employed extensively in plant–water relations research to investigate physiological and hydrological processes from whole plant to ecosystem scales. Stable isotopes of hydrogen and oxygen are routinely measured to identify plant source water. This application relies on the assumption that no fractionation of oxygen and hydrogen isotopes in water occurs during uptake by roots. However, a large fraction of the water taken up through roots in halophytic and xerophytic plants transverses cell membranes in the endodermis before entering the root xylem. Passage of water through this symplastic pathway has been hypothesized to cause fractionation leading to a decrease in 2H of root xylem water relative to that in the surrounding soil medium. We examined 16 woody halophytic and xerophytic plant species in controlled conditions for evidence of hydrogen isotope fractionation during uptake at the root–soil interface. Isotopic separation (Δ2H = δ2Hsoil water − δ2Hxylem water) ranging from 3‰ to 9‰ was observed in 12 species. A significant positive correlation between salinity tolerance and the magnitude of Δ2H was observed. Water in whole stem segments, sapwood, and roots had significantly lower δ2H values relative to soil water in Prosopis velutina Woot., the species expressing the greatest Δ2H values among the 16 species examined. Pressurized water flow through intact root systems of Artemisia tridentata Nutt. and Atriplex canescens (Pursh) Nutt. caused the δ2H values to decrease as flow rate increased. This relationship was not observed in P. velutina. Destroying the plasma membranes of root cells by excessive heat from boiling did not significantly alter the relationship between δ2H of expressed water and flow rate. In light of these results, care should be taken when using the stable isotope method to examine source-water use in halophytic and xerophytic species.

Keywords

Hydrogen isotope fractionation Roots Xerophyte Halophyte Transpiration 

Notes

Acknowledgements

We thank Enrico Yepez, Victor Resco, Rico Gazal, and Ayme Ahrens for their help with the greenhouse experiments. We also thank Ann Hild and Brent Ewers for their help during the manuscript preparation.

References

  1. Armitage P (1980) Statistical methods in medical research. Blackwell Scientific Publications, Oxford UK, pp 279–301Google Scholar
  2. Atkinson MR, Findlay GP, Hope AB, Pitman MG, Saddler HDW, West KR (1966) Salt regulation in the mangroves Rhizophora mucronata Lam. and Aegialitis annulata R.Br. Aust J Biol Sci 20:589–599Google Scholar
  3. Chacko T, Cole DR, Horita J (2001) Equilibrium oxygen, hydrogen, and carbon isotope fractionation factors applicable to geologic systems. In: Valley JW, Cole DR (eds) Reviews in mineralogy and geochemistry, vol 43. Stable isotope geochemistry. Mineralogical Society of America. Washington, DC pp 1–82Google Scholar
  4. Coleman ML, Shepard TJ, Durham JJ, Rouse JE, Moore GR (1982) Reduction of water with zinc for hydrogen isotope analysis. Anal Chem 54:993–995Google Scholar
  5. Coplens TB, Hanshaw BB (1973) Ultratitration by a compacted clay membrane-I. Oxygen and hydrogen isotopic fractionation. Geochim Cosmochim Acta 37:2295–2310CrossRefGoogle Scholar
  6. Craig GF, Bell DT, Atkins CA (1990) Response to salt and waterlogging stress of ten taxa of Acacia selected from naturally saline areas of Western Australia. Aust J Bot 38:619–630CrossRefGoogle Scholar
  7. Craig H (1961) Isotopic variations in meteoric water. Science 133:1702–1703CrossRefPubMedGoogle Scholar
  8. Dansgaard W (1964) Stable isotopes in precipitation. Tellus 16:436–468CrossRefGoogle Scholar
  9. Dawson TE (1996) Determining water use by trees and forests from isotopic, energy balance and transpiration analyses—the roles of tree size and hydraulic lift. Tree Physiol 16:263–272PubMedGoogle Scholar
  10. Dawson TE, Ehleringer JR (1991) Streamside trees that do not use stream water. Nature 350:335–337CrossRefGoogle Scholar
  11. Dawson TE, Ehleringer JR (1993) Isotopic enrichment of water in the ‘woody’ tissues: Implications for plant water source, water uptake, and other studies which use the stable isotopic composition of cellulose. Geochim Cosmochim Acta 57:3487–3492CrossRefGoogle Scholar
  12. Ehleringer JR, Osmond CB (1989) Stable isotopes. In: Pearcy RW, Ehleringer JR, Mooney HA, Rundel PW (eds) Plant physiological ecology: field techniques and instrumentation. Chapman & Hall, London, UK, pp 281–300Google Scholar
  13. El-Ghonemy AA, Wallace A, Romney EM (1980) Socioecological and soil-plant studies of the natural vegetation in the northern Mojave desert-Great Basin desert interface. Gt Basin Nat Mem 4:73–88Google Scholar
  14. Epstein S, Mayeda T (1953) Variation of 18O content of water from natural sources. Geochim Cosmochim Acta 4:213–224CrossRefGoogle Scholar
  15. Feder M, Taube H (1952) Ionic hydration: an isotopic fractionation technique. J Chem Phys 20:1335–1336CrossRefGoogle Scholar
  16. Feucht JR (2001) Trees and shrubs for high alkaline and high salt conditions. Cooperative Extension Service, Tri River Area, Colorado State UniversityGoogle Scholar
  17. Flanagan LB, Ehleringer JR (1991) Stable isotope composition of stem and leaf water: applications to the study of plant water use. Funct Ecol 5:270–277CrossRefGoogle Scholar
  18. Forti M (1986) Salt tolerant and halophytic plants in Israel. Reclam Reveg Res 5:83–96Google Scholar
  19. Houerou Le (1986) Salt tolerant plants of economic value in the Mediterranean Basin. Reclam Reveg Res 5:319–341Google Scholar
  20. Jackson J, Ball JT, Rose MR (1990) Assessment of the salinity tolerance of eight Sonoran desert riparian trees and shrubs. USBR Contract No. 9-CP-30-017170. University of Nevada SystemGoogle Scholar
  21. Karan DM, Macey RI (1980) The permeability of the human red cell to deuterium oxide (heavy water). J Cell Physiol 104:209–214PubMedCrossRefGoogle Scholar
  22. Kendall C, Caldwell EA (1998) Fundamentals of isotope geochemistry. In: Kendall C, McDonnell JJ (eds) Isotope tracers in catchment hydrology. Elsevier Science Publishers, New York, pp 51–86Google Scholar
  23. Lin G, da Sternberg LSL (1993) Hydrogen isotopic fractionation by plant roots during water uptake in coastal wetland plants. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable isotopes and plant carbon-water relations. Academic Press Inc., New York, pp 497–510Google Scholar
  24. Lin G, da Sternberg LSL (1992) Comparative study of water uptake and photosynthetic gas exchange between scrub and fringe red mangroves, Rhizophora mangle L. Oecologia 90:399–403CrossRefGoogle Scholar
  25. Luo Y-H, da Sternberg LSL, Suda S, Kumazawa S, Mitsui A (1991) Extremely low D/H ratios of photoproduced hydrogen by cyanobacteria. Plant Cell Physiol 32:897–900Google Scholar
  26. Maas EV (1985) Crop tolerance to saline sprinkling water. Plant Soil 89:273–284CrossRefGoogle Scholar
  27. McMillan P (1985) Vibrational spectroscopy in the mineral sciences. In: Kieffer SW, Navrotsky A (eds) Reviews in mineralogy and geochemistry, vol 14. Macroscopic to microscopic: Atomic environments to mineral thermodynamics. Mineralogical Society of America, Washington, DC, pp 9–64Google Scholar
  28. Nelson ST, Dettman D (2001) Improving hydrogen isotope ratio measurements for on-line chromium reduction systems. Rapid Commun Mass Spectrom 15:2301–2306CrossRefGoogle Scholar
  29. Nobel PS, Sanderson J (1984) Rectifier-like activities of roots of two desert succulents. J Exp Bot 35:727–737CrossRefGoogle Scholar
  30. Passioura JB (1981) Water collection by roots. In: Paleg LG, Aspinell D (eds) The physiology and biochemistry of drought resistance in plants. Academic Press, New York, pp 39–53Google Scholar
  31. Phillips FM, Bentley HW (1987) Isotopic fractionation during ion filtration: I. Theory. Geochim Cosmochim Acta 51:683–695CrossRefGoogle Scholar
  32. Poljakoff-Mayber A (1975) Morphological and anatomical changes in plants as a response to salinity stress. In: Poljakoff-Mayber A, Gale J (eds) Plants in saline environments. Springer-Verlag, New YorkGoogle Scholar
  33. Reinoso H, Soas L, Ramírez L, Luna V (2004) Salt-induced changes in the vegetative anatomy of Prosopis strombulifera (Leguminosae). Can J Bot 82:618–628CrossRefGoogle Scholar
  34. Scholander PF, Bradstreet ED, Hammel HT, Hemmingsen EA (1966) Sap concentrations in halophytes and some other plants. Plant Physiol 41:529–532PubMedGoogle Scholar
  35. Serrato Valenti G, Ferro M, Ferraro D, Riveros F (1991) Anatomical changes in Prosopis tamarugo Phil. Seedlings growing at different levels of NaCl salinity. Ann Bot London 68:47–53Google Scholar
  36. Serrato Valenti G, Melone L, Orsi O, Riveros F (1992) Anatomical changes in Prosopis cineraria (L.) Ducehil. Seedlings growing at different levels of NaCl salinity. Ann Bot London 70:399–404Google Scholar
  37. Shannon MC (1997) Adaptation of plants to salinity. Adv Agron 60:75–120CrossRefGoogle Scholar
  38. Sharma ML (1982) Aspects of salinity and water relations of Australian chenopods. In: Sen DN, Rajpurohit KS (eds) Task for vegetation science. 2. Contribution to the biology of halophyte. Junk, The Hague, pp 155–172Google Scholar
  39. Sternberg LSL, Swart PK (1987) Utilization of freshwater and ocean water by coastal plants of southern Florida. Ecology 68:1898–1905CrossRefGoogle Scholar
  40. Stewart MK, Friedman I (1975) Deuterium fractionation between aqueous salt solutions and water vapor. J Geophys Res 80:3812–3818CrossRefGoogle Scholar
  41. Thorburn PJ, Mensforth LS (1993) Sampling water from alfalfa (Medicago sativa) for analysis of stable isotopes of water. Commun Soil Sci Plan 24:549–557Google Scholar
  42. Thorburn PJ, Walker GR, Brunel J-P (1993) Extraction of water from Eucalyptus trees for analysis of deuterium and oxygen-18: laboratory and field techniques. Plant Cell Environ 16:269–277CrossRefGoogle Scholar
  43. Tyree MT, Sperry JS (1989) The vulnerability of xylem to cavitation and embolism. Annu Rev Plant Phys 40:19–38CrossRefGoogle Scholar
  44. Vartanian N (1981) Some aspects of structural and functional modifications induced by drought in root systems. Plant Soil 63:83–92CrossRefGoogle Scholar
  45. Waisel Y (1972) Biology of halophytes. Academic Press, New YorkGoogle Scholar
  46. Waisel Y, Eshel A, Agami M (1986) Salt balance of leaves of the mangrove Avicennia marina. Physiol Plantarum 67:67–72CrossRefGoogle Scholar
  47. Walker CD, Richardson SB (1991) The use of stable isotopes of water in characterizing the source of water in vegetation. Chem Geol (Iso Geosci) 94:145–158CrossRefGoogle Scholar
  48. Washburn EW, Smith ER (1934) The isotopic fractionation of water by physiological processes. Science 79:188–189CrossRefPubMedGoogle Scholar
  49. Wershaw RL, Friedman I, Heller SJ, Frank PA (1966) Hydrogen isotopic fractionation of water passing through trees. In: Hobson GD, Speers GC, Inderson DE (eds) Advances in organic geochemistry. International series of monographs on earth sciences, vol 32. Pergamon Press, New York, pp 55–67Google Scholar
  50. White JWC, Cook ER, Lawrence JR, Broecker WS (1985) The D/H ratios of sap in tree: Implications for water sources and tree ring D/H ratios. Geochim Cosmochim Acta 49:237–246CrossRefGoogle Scholar
  51. Williams DG, Ehleringer JR (2000) Intra- and interspecific variation for summer precipitation use in pinyon-juniper woodlands. Ecol Monogr 70:517–537CrossRefGoogle Scholar
  52. Yakir D, da Sternberg LSL (2000) The use of stable isotopes to study ecosystem gas exchange. Oecologia 123:297–311CrossRefGoogle Scholar
  53. Ziegler H, Osmond CB, Stichler W, Trimborn P (1976) Hydrogen isotope discrimination in higher plants: Correlations with photosynthetic pathway and environment. Planta 128:85–92CrossRefGoogle Scholar
  54. Zimmermann U, Ehhalt E, Munnich KO (1967) Soil-water movement and evapotranspiration: changes in the isotopic composition of the water. In: Proceedings of the symposium on isotopes in hydrology, 14–18 November 1966. IAEA, Vienna, pp 567–585Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.Department of BiologyUniversity of MiamiCoral GablesUSA
  2. 2.Department of Renewable ResourcesUniversity of WyomingLaramieUSA
  3. 3.Department of BotanyUniversity of WyomingLaramieUSA

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