Ecological Research

, Volume 33, Issue 5, pp 901–915 | Cite as

A multiple time scale modeling investigation of leaf water isotope enrichment in a temperate grassland ecosystem

  • Pei Wang
  • Tsutomu Yamanaka
  • Xiao-Yan Li
  • Xiuchen Wu
  • Bo Chen
  • Yaping Liu
  • Zhongwang Wei
  • Wenchao Ma
Original Article


Understanding the controls on temporal variation in plant leaf δ2H and δ18O values is important for understanding carbon–water dynamics of the biosphere and interpreting a wide range of proxies for past environments. Explaining the enrichment mechanisms under field conditions is challenging. To clarify the leaf water isotopic enrichment process at the ecosystem scale, four models with a range of complexities that were previously conducted at the leaf scale have been tested to simulate canopy foliage water in a multispecies grassland ecosystem. Although the exact importance of considering non-steady-state or/and isotopic diffusion in bulk leaf isotopic simulations has been reported in previous studies, our findings suggested that the steady-state assumption (SSA) is practically acceptable as a first-order approximation. The SSA two-pool model was the best option for reproducing seasonality of the bulk-leaf-water isotopic ratio for a grassland ecosystem. Relative humidity at canopy layer as the most controlling factor for canopy foliage water stable isotope composition because of its high sensitivity and variation. The results highlighted that canopy foliage water was a well-behaved property that was predictable for a multispecies grassland ecosystem at hourly or daily time-scales.


Foliage isotopic enrichment Relative humidity Numerical modeling Non-steady-state Advection–diffusion 

List of symbols


Canopy cluster parameter, dimensionless


The proportion of water associated with the evaporation site to the total leaf water, dimensionless


Relative humidity of the ambient air reference to TL, %


Relative humidity at the reference level, %


Soil-plant-atmosphere continuum with isotopic tracer


Leaf area index, m2 m−2


Downward long-wave radiation, W m−2


Scaled effective path length where isotopic diffusion occur, m


Air pressure at the reference level, hPa


Specific humidity at reference height, kg kg−1


Aerodynamic resistance above the vegetation canopy, s m−1


Aerodynamic resistance in the canopy air layer, s m−1


Canopy-scale boundary layer resistance, s m−1


Canopy-scale stomata resistance, s m−1


Leaf-scale stomata resistance, s m−1


Minimum stomata resistance, s m−1


Maximum stomata resistance, s m−1


Canopy-scale total resistance to water vapor and heat from canopy surface to reference height, s m−1


Soil-plant-atmosphere continuum


Downward short-wave radiation, W m−2


Sensitivity coefficient, dimensionless


Plant transpiration rate, mm h−1


Air temperature at the reference level, K


Leaf canopy temperature, K


Soil surface temperature at a depth Zsoil (m), °C


Wind speed at the reference level, m s−1


Wind speed inside the canopy, m s−1


Wind speed at vegetation height, m s−1


Vapor pressure deficit, kPa


Vapor pressure deficit reference to TL, kPa


Leaf water content (mass of water per unit ground area at the canopy scale), kg m−2


The height of temperature and humidity measurement, m


The height of wind speed measurement, m


Depth of ground heat flux measurement, m


Vegetation height, m


Equilibrium fractionation factor for water (> 1), dimensionless


Albedo of ground surface, dimensionless


Kinetic fractionation factor for water vapor (> 1), dimensionless


Kinetic fractionation factor for water vapor (> 1) at leaf temperature, dimensionless


Equilibrium fractionation factor for water (> 1) at leaf tempreture, dimensionless


Albedo of vegetation canopy, dimensionless


Isotope composition of sample water relative to a standard, ‰


Stable isotope composition of hydrogen in water, ‰


Stable isotope composition of oxygen in water, ‰


δ at evaporative site in leaf under SSA, ‰


δ at evaporative site in leaf under SSA, ‰


δ of bulk leaf water, ‰


δ at evaporative site in leaf, ‰


δ of water vapor, ‰


δ of xylem water, ‰


Isotopic equilibrium fractionation factor between liquid water and vapor, ‰


Isotopic kinetic fractionation factor between liquid water and vapor, ‰


Volumetric soil water content, m3 m−3


Thermal conductivity of surface soil, W m−1 K−1



The study was financially supported by the National Natural Science Foundation of China (41671019, 41730854, and 91425301), under a project from State Key Laboratory of Earth Surface Processes and Resource Ecology.

Supplementary material

11284_2018_1591_MOESM1_ESM.pdf (77 kb)
Supplementary material 1 (PDF 76 kb)


  1. Baldocchi DD, Hincks BB, Meyers TP (1988) Measuring biosphere-atmosphere exchanges of biologically related gases with micrometeorological methods. Ecology 69:1331–1340. CrossRefGoogle Scholar
  2. Barbour MM, Schurr U, Henry BK, Wong SC, Farquhar GD (2000) Variation in the oxygen isotope ratio of phloem sap sucrose from castor bean. Evidence in support of the Péclet effect. Plant Physiol 123(2):671–680. CrossRefPubMedPubMedCentralGoogle Scholar
  3. Barbour MM, Roden JS, Farquhar GD, Ehleringer JR (2004) Expressing leaf water and cellulose oxygen isotope ratios as enrichment above source water reveals evidence of a Péclet effect. Oecologia 138:426–435. CrossRefPubMedGoogle Scholar
  4. Barnard RL, Salmon Y, Kodama N, Sorgel K, Holst J, Rennenbegr H, Gessler A, Buchmann N (2007) Evaporative enrichment and time lags between δ18O of leaf water and organic pools in a pine stand. Plant Cell Environ 30:539–550. CrossRefPubMedGoogle Scholar
  5. Brutsaert W (1982) Evaporation into the atmosphere: theory, history, and applications. Reidel, Dordrecht. CrossRefGoogle Scholar
  6. Campbell JP (1977) On the nature of organizational effectiveness. In: Goodman PS, Pennings JM (eds) New perspectives on organizational effectiveness. Jossey-Bass, San Francisco, pp 13–55Google Scholar
  7. Cernusak LA, Arthur DJ, Pate JS, Farquhar GD (2003) Water relations link carbon and oxygen isotope discrimination to phloem sap sugar concentration in Eucalyptus globulus. Plant Physiol 131:1544–1554. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cernusak LA, Barbour MM, Arndt SK, Cheesman AW, English NB, Feild TS, Helliker BR, Holloway-Phillips MM, Holtum JA, Kahmen A, McInerney FA, Munksgaard NC, Simonin KA, Song X, Stuart-Williams H, West JB, Farquhar GD (2016) Stable isotopes in leaf water of terrestrial plants. Plant Cell Environ. CrossRefPubMedGoogle Scholar
  9. Craig H, Gordon LI (1965) Deuterium and oxygen18 variations in the ocean and the marine atmosphere. In: Tongiogi E (ed) Proceedings of a conference on stable isotopes in oceanographic studies and palaeotemperatures. Spoleto, Italy, pp 9–130Google Scholar
  10. Cuntz M, Ogee J, Farquhar GD, Peylin P, Cernusak LA (2007) Modelling advection and diffusion of water isotopologues in leaves. Plant Cell Environ 30:892–909. CrossRefPubMedGoogle Scholar
  11. Dawson TE, Ehleringer JR (1993) Isotopic enrichment of water in the woody tissues of plants: implications for plant water source, water uptake, and other studies which use the stable isotopic composition of cellulose. Geochim Cosmochim Acta 57:3487–3492. CrossRefGoogle Scholar
  12. Dongmann G, Nürnberg HW, Förstel H, Wagener K (1974) On the enrichment of H218O in the leaves of transpiring plants. Radiat Environ Bioph 11:41–52CrossRefGoogle Scholar
  13. Dubbert M, Cuntz M, Piayda A, Werner C (2014) Oxygen isotope signatures of transpired water vapor: the role of isotopic non-steady-state transpiration under natural conditions. New Phytol 203:1242–1252. CrossRefPubMedGoogle Scholar
  14. Farquhar GD, Cernusak LA (2005) On the isotopic composition of leaf water in the non-steady state. Funct Plant Biol 32:293–303. CrossRefGoogle Scholar
  15. Farquhar GD, Gan KS (2003) On the progressive enrichment of the oxygen isotopic composition of water along a leaves. Plant Cell Environ 26:801–819. PubMedCrossRefGoogle Scholar
  16. Farquhar GD, Lloyd J (1993) Carbon and oxygen isotope effects in the exchange of carbon dioxide between plants and the atmosphere. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable isotopes and plant carbon-water relations. Academic Press, San Diego, pp 47–70. CrossRefGoogle Scholar
  17. Farquhar GD, Lloyd J, Taylor JA, Flanagan LB, Syvertsen JP, Hubick KT, Wong SC, Ehleringer JR (1993) Vegetation effects on the isotope composition of oxygen in atmospheric CO2. Nature 363:439–443. CrossRefGoogle Scholar
  18. Farquhar GD, Cernusak LA, Barnes B (2007) Heavy water fractionation during transpiration. Plant Physiol 143:11–18. CrossRefPubMedPubMedCentralGoogle Scholar
  19. Gan KS, Wong SC, Yong JWH, Farquhar GD (2002) 18O spatial patterns of vein xylem water, leaf water, and dry matter in cotton leaves. Plant Physiol 130:1008–1021. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Gupta P, Noone D, Galewsky J, Sweeney C, Vaughn BH (2009) Demonstration of high-precision continuous measurements of water vapor isotopologues in laboratory and remote field deployments using wavelength-scanned cavity ring-down spectroscopy (WS-CRDS) technology. Rapid Commun Mass Spectrom 23(16):2534–2542. CrossRefPubMedGoogle Scholar
  21. Helliker BR, Ehleringer JR (2000) Establishing a grassland signature in veins: 18o in the leaf water of c3 and c4 grasses. Proc Natl Acad Sci USA 97(14):7894–7898. CrossRefPubMedGoogle Scholar
  22. Hiyama T, Sugita M, Mikami M (1993) Comparisons of the latent heat fluxes evaluated by a weighing lysimeter and an energy balance method. Bull Environ Res Center Univ Tsukuba 18:41–53Google Scholar
  23. Hoffmann G, Cuntz M, Weber C, Ciais P, Friedlingstein P, Heimann M, Jouzel J, Kaduk J, Maier-Reimer E, Seibt U, Six K (2004) A model of the Earth’s Dole effect. Global Biogeochem Cycles 18:1008. CrossRefGoogle Scholar
  24. Hou JZ, D’Andrea WJ, Huang YS (2008) Can sedimentary leaf waxes record D/H ratios of continental precipitation? Field, model, and experimental assessments. Geochim Cosmochim Acta 72:3503–3517. CrossRefGoogle Scholar
  25. Jarvis P (1976) The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field. Philos Trans R Soc Lond B Biol Sci 273:593–610. CrossRefGoogle Scholar
  26. Kahmen A, Simonin K, Tu KP, Merchant A, Callister A, Siegwolf R, Dawson TE, Arndt SK (2008) Effects of environmental parameters, leaf physiological properties and leaf water relations on leaf water δ 18O enrichment in different Eucalyptus species. Plant Cell Environ 31:738–751. CrossRefPubMedGoogle Scholar
  27. Lai CT, Ehleringer JR, Bond BJ, Paw UKT (2005) Contributions of evaporation, isotopic non-steady state transpiration and atmospheric mixing on the δ18O of water vapor in Pacific Northwest coniferous forests. Plant Cell Environ 29:77–94. CrossRefGoogle Scholar
  28. Leaney FW, Osmond CB, Allison GB, Ziegler H (1985) Hydrogen-isotope composition of leaf water in C3 and C4 plants: its relationship to the hydrogen-isotope composition of dry matter. Planta 164:215–220. CrossRefPubMedGoogle Scholar
  29. Lee X (2000) Air motion within and above forest vegetation in non-ideal conditions. For Ecol Manage 135:3–18. CrossRefGoogle Scholar
  30. Lee X, Kim K, Smith R (2007) Temporal variations of the O18/O16 signal of the whole-canopy transpiration in a temperate forest. Glob Biogeochem Cycles 21:12. CrossRefGoogle Scholar
  31. Lee X, Griffis TJ, Baker JM, Billmark KA, Kim K, Welp LR (2009) Canopy-scale kinetic fractionation of atmospheric carbon dioxide and water vapor isotopes. Glob Biogeochem Cycles 23:GB1002. CrossRefGoogle Scholar
  32. Li SG, Lai CT, Lee G, Shimoda S, Yokoyama T, Higuchi A, Oikawa T (2005) Evapotranspiration from a wet temperate grassland and its sensitivity to microenvironmental variables. Hydrol Process 19:517–532. CrossRefGoogle Scholar
  33. Loader NJ, Hemming DL (2004) The stable isotope analysis of pollen as an indicator of terrestrial palaeoenvironmental change: a review of progress and recent developments. Quat Sci Rev 23:893–900. CrossRefGoogle Scholar
  34. Loucos KE, Simonin KA, Song X, Barbour MM (2015) Observed relationships between leaf H218O Péclet effective length and leaf hydraulic conductance reflect assumptions in Craig–Gordon model calculations. Tree Physiol 35:16–26. CrossRefPubMedGoogle Scholar
  35. Majoube M (1971) Oxygen-18 and deuterium fractionation between water and steam. J chim Phys Phys Chim Biol 68:1423–1436CrossRefGoogle Scholar
  36. Merlivat L (1978) Molecular diffusivities of H216O, HD16O, and H218O in gases. J Chem Phys 69:2864–2871. CrossRefGoogle Scholar
  37. Miller DL, Mora CI, Grissino-Mayer HD, Mock CJ, Uhle ME, Sharp Z (2006) Tree-ring isotope records of tropical cyclone activity. Proc Natl Acad Sci USA 103:14294–14297. CrossRefPubMedGoogle Scholar
  38. Ogée J, Cuntz M, Peylin P, Bariac T (2007) Non-steady-state, non-uniform transpiration rate and leaf anatomy effects on the progressive stable isotope enrichment of leaf water along monocot leaves. Plant Cell Environ 30:367–387. CrossRefPubMedGoogle Scholar
  39. Roden JS, Ehleringer JR (1999) Observations of hydrogen and oxygen isotopes in leaf water confirm the Craig-Gordon model under wide-ranging environmental conditions. Plant Physiol 120:1165–1174. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Schuepp P, Leclerc M, MacPherson J, Desjardins R (1990) Footprint prediction of scalar fluxes from analytical solutions of the diffusion equation. Bound Layer Meteorol 50(1):355–373. CrossRefGoogle Scholar
  41. Shugart HH (2000) Ecosystem modeling. In: Sala OE, Jackson RB, Mooney HA, Howarth RW (eds) Methods in ecosystem science. Springer, New York, pp 373–388CrossRefGoogle Scholar
  42. Snyder KA, Monnar R, Poulson SR, Hartsough P, Biondi F (2010) Diurnal variations of needle water isotopic ratios in two pine species. Trees Struct Funct 24:585–595. CrossRefGoogle Scholar
  43. Song X, Barbour MM, Farquhar GD, Vann DR, Helliker BR (2013) Transpiration rate relates to within- and across- species variations in effective pathlength in a leaf water model of oxygen isotope enrichment. Plant Cell Environ 36:1338–1351. CrossRefPubMedGoogle Scholar
  44. Song X, Loucos KE, Simonin KA, Farquhar GD, Barbour MM (2015) Measurements of transpiration isotopologues and leaf water to assess enrichment models in cotton. New Phytol 206:637–646. CrossRefPubMedGoogle Scholar
  45. Stewart J (1988) Modelling surface conductance of pine forest. Agric For Meteorol 43:19–35. CrossRefGoogle Scholar
  46. Twine TE, Kustas W, Norman J, Cook D, HouserP Meyers T, Wesely M (2000) Correcting eddy-covariance flux underestimates over a grassland. Agric For Meteorol 103:279–300. CrossRefGoogle Scholar
  47. Wang P, Yamanaka T (2014) Application of a two-source model for partitioning evapotranspiration and assessing its controls in temperate grasslands in central Japan. Ecohydrol 7:345–353. CrossRefGoogle Scholar
  48. Wang P, Yamanaka T, Li Xiao-Yan, Wei Zhongwang (2015) Partitioning evapotranspiration in a temperate grassland ecosystem: numerical modeling with isotopic tracers. Agric For Meteorol 208:16–31. CrossRefGoogle Scholar
  49. Werner C, Schnyder H, Cuntz M, Keitel C, Zeeman MJ, Dawson TE, Badeck FW, Brugnoli E, Ghashghaie J, Grams TEE, Kayler ZE, Lakatos M, Lee X, Máguas C, Ogée J, Rascher KG, Siegwolf RTW, Unger S, Welker J, Wingate L, Gessler A (2012) Progress and challenges in using stable isotopes to trace plant carbon and water relations across scales. Biogeosciences 9:3083–3111. CrossRefGoogle Scholar
  50. West AG, Patrickson SJ, Ehleringer JR (2006) Water extraction times for plant and soil materials used in stale isotope analysis. Rapid Commun Mass Spectrom 20:1317–1321. CrossRefPubMedGoogle Scholar
  51. Willmott CJ, Ackleson SG, Davis RE, Feddema JJ, Klink KM, Legates DR, O’Donnell J, Rowe CM (1985) Statistics for the evaluation and comparison of models. J Geophys Res 90:8995–9005. CrossRefGoogle Scholar
  52. Wilson K, Goldstein A, Falge E, Aubinet M, Baldocchi D, Berbigier P, Bernhofer C, Ceulemans R, Dolman H, Field C, Grelle A, Ibrom A, Law B, Kowalski A, Meyers T, Moncrieff J, Monson R, Oechel W, Tenhunen J, Valentini R, Verma S (2002) Energy balance closure at FLUXNET sites. Agric For Meteorol 113:223–243. CrossRefGoogle Scholar
  53. Xiao W, Lee X, Wen X, Sun X, Zhang S (2012) Modeling biophysical controls on canopy foliage water 18O enrichment in wheat and corn. Glob Chang Biol 18:1769–1780. CrossRefGoogle Scholar
  54. Yamanaka T, Onda Y (2011) On measurement accuracy of liquid water isotope analyzer based on wavelength-scanned cavity ring-down spectroscopy (WS-CRDS). Bull Terr Environ Res Cent Univ Tsukuba 12:31–40 (in Japanese) Google Scholar
  55. Yamanaka T, Tsunakawa A (2007) Isotopic signature of evapotranspiration flux and its use for partitioning evaporation/transpiration components. Tsukuba Geoenviron Sci Univ Tsukuba 3:11–21Google Scholar

Copyright information

© The Ecological Society of Japan 2018

Authors and Affiliations

  1. 1.State Key Laboratory of Earth Surface Processes and Resource EcologyBeijing Normal UniversityBeijingChina
  2. 2.School of Natural Resources, Faculty of Geographical ScienceBeijing Normal UniversityBeijingChina
  3. 3.Joint Center for Global Change Studies (JCGCS)BeijingChina
  4. 4.Faculty of Life and Environmental SciencesUniversity of TsukubaTsukubaJapan
  5. 5.College of Resource Environment and TourismCapital Normal UniversityBeijingChina
  6. 6.School of Forestry and Environmental StudiesYale UniversityNew HavenUSA
  7. 7.Center for Research in Isotopes and Environmental Dynamics (CRiED)University of TsukubaTsukubaJapan

Personalised recommendations