Nocturnal stomatal conductance and implications for modelling δ18O of leaf-respired CO2 in temperate tree species
Margaret M. Barbour A G , Lucas A. Cernusak B C , David Whitehead A , Kevin L. Griffin D , Matthew H. Turnbull E , David T. Tissue F and Graham D. Farquhar BA Landcare Research, PO Box 69, Lincoln 8152, New Zealand.
B Research School of Biological Sciences, Australian National University, GPO Box 475, ACT 2601, Australia.
C Current address: Smithsonian Tropical Research Institute, PO Box 2072, Balboa, Ancon, Republic of Panama.
D Lamont-Doherty Earth Observatory, Columbia University, Palisades, NY 10964-8000, USA.
E School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand.
F Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409-3131, USA.
G Corresponding author. Email: barbourm@landcareresearch.co.nz
Functional Plant Biology 32(12) 1107-1121 https://doi.org/10.1071/FP05118
Submitted: 17 May 2005 Accepted: 12 August 2005 Published: 1 December 2005
Abstract
Variation in the oxygen isotope composition of within-canopy CO2 has potential to allow partitioning of the ecosystem respiratory flux into above- and below-ground components. Recent theoretical work has highlighted the sensitivity of the oxygen isotope composition of leaf-respired CO2 (δRl) to nocturnal stomatal conductance. When the one-way flux model was tested on Ricinus communis L. large enrichments in δRl were observed. However, most species for which the isotope flux partitioning technique has been or would be applied (i.e. temperate tree species) are much more conservative users of water than R. communis. So, high stomatal conductance and very high enrichment of δRl observed may not be typical for temperate tree species. Using existing gas-exchange measurements on six temperate tree species, we demonstrate significant water loss through stomata for all species (i.e. statistically significantly greater than cuticular loss alone) at some time for some leaves during the night. δRl values predicted by the one-way flux model revealed that δRl might be very much more enriched than when the net flux alone is considered, particularly close to sunrise and sunset. Incorporation of the one-way flux model into ecosystem respiration partitioning studies will affect model outputs and interpretation of variation in the oxygen isotope composition of atmospheric CO2.
Keywords: leaf respiration, nocturnal stomatal conductance, Quercus rubra, stable oxygen isotope ratio.
Acknowledgments
Funding for this work by the Royal Society of New Zealand Marsden Fund (M.M.B., G.D.F. and D.W.; contract LCR201) is gratefully acknowledged. The original leaf respiration data were collected during work supported by funds from the Andrew W. Mellon Foundation (USA) and the Foundation for Research, Science and Technology (New Zealand).
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Benyon RG
(1999) Nighttime water use in an irrigated Eucalyptus grandis plantation. Tree Physiology 19, 853–859.
| PubMed |
Bottinga Y, Craig H
(1969) Oxygen isotope fractionation between CO2 and water, and the isotopic composition of marine atmospheric CO2. Earth and Planetary Science Letters 5, 285–295.
Bowling DR,
McDowell NG,
Welker JM,
Bond BJ,
Law BE, Ehleringer JR
(2003a) Oxygen isotope content of CO2 in nocturnal ecosystem respiration 1. Observations in forests along a precipitation transect in Oregon, USA. Global Biogeochemical Cycles 17, 1120.
| Crossref | GoogleScholarGoogle Scholar |
Bowling DR,
McDowell NG,
Welker JM,
Bond BJ,
Law BE, Ehleringer JR
(2003b) Oxygen isotope content of CO2 in nocturnal ecosystem respiration. 2. Short-term dynamics of foliar and soil component fluxes in an old-growth ponderosa pine forest. Global Biogeochemical Cycles 17, 1124.
| Crossref | GoogleScholarGoogle Scholar |
Bowling DR,
Sargent SD,
Tanner BD, Ehleringer JR
(2003c) Tunable diode laser absorption spectroscopy for stable isotope studies of ecosystem–atmosphere CO2 exchange. Agricultural and Forest Meteorology 118, 1–19.
| Crossref | GoogleScholarGoogle Scholar |
Boyer JS,
Wong SC, Farquhar GD
(1997) CO2 and water vapor exchange across leaf cuticle (epidermis) at various water potentials. Plant Physiology 114, 185–191.
| PubMed |
Brenninkmeijer C,
Kraft P, Mook W
(1983) Oxygen isotope fractionation between CO2 and H2O. Isotope Geoscience 1, 181–190.
Bucci SJ,
Scholz FB,
Goldstein G,
Meinzer FC,
Hinojsa JA,
Hoffmann WA, Franco AC
(2004) Processes preventing nocturnal equilibration between leaf and soil water potential in tropical savanna woody species. Tree Physiology 24, 1119–1127.
| PubMed |
Cappa CD,
Hendricks MB,
DePaulo DJ, Cohen RC
(2003) Isotopic fractionation of water during evaporation. Journal of Geophysical Research 108, 4525.
| Crossref | GoogleScholarGoogle Scholar |
Cernusak LA,
Pate JS, Farquhar GD
(2002) Diurnal variation in the stable isotope composition of water and dry matter in fruiting Lupinus angustifolius under field conditions. Plant, Cell & Environment 25, 893–907.
| Crossref | GoogleScholarGoogle Scholar |
Cernusak LA,
Wong S-C, Farquhar GD
(2003) Oxygen isotope composition of phloem sap in relation to leaf water in Ricinus communis.
Functional Plant Biology 30, 1059–1070.
| Crossref | GoogleScholarGoogle Scholar |
Cernusak LA,
Farquhar GD,
Wong SC, Stuart-Williams H
(2004) Measurement and interpretation of the oxygen isotope composition of carbon dioxide respired by leaves in the dark. Plant Physiology 136, 3350–3363.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cernusak LA,
Farquhar GD, Pate JS
(2005) Environmental and physiological controls over carbon and oxygen isotope composition of Tasmanian blue gum, Eucalyptus globulus.
Tree Physiology 25, 129–146.
| PubMed |
Ciais P,
Denning AS,
Tans PP,
Berry JA, Randall DA ,
et al
.
(1997) A three-dimensional synthesis study of δ18O in atmospheric CO2. 1. Surface fluxes. Journal of Geophysical Research 102, 5857–5872.
| Crossref | GoogleScholarGoogle Scholar |
Cowan, IR ,
and
Farquhar, GD (1977). Stomatal function in relation to leaf metabolism and environment. In ‘Integration of activity in the higher plant’. pp. 471–505. (Cambridge University Press: New York)
Craig, H ,
and
Gordon, LI (1965). Deuterium and oxygen-18 variations in the ocean and the marine atmosphere. In ‘Proceedings of a conference on stable isotopes in oceanographic studies and palaeotemperatures’ pp. 9–130. (Lischi and Figli: Pisa)
Dongmann G,
Nurnberg HW,
Förstel H, Wagener K
(1974) On the enrichment of H2
18O in the leaves of transpiring plants. Radiation and Environmental Biophysics 11, 41–52.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Donovan LA,
Linton MJ, Richards JH
(2001) Predawn plant water potential does not necessarily equilibrate with soil water potential under well-watered conditions. Oecologia 129, 328–335.
Ekblad A,
Boström B,
Holm A, Comstedt A
(2005) Forest soil respiration rate and δ13C is regulated by recent above ground weather conditions. Oecologia 143, 136–142.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ethier GJ, Livingston NJ
(2004) On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar–von Caemmerer–Berry leaf photosynthesis model. Plant, Cell & Environment 27, 137–153.
| Crossref | GoogleScholarGoogle Scholar |
Farquhar, GD ,
and
Lloyd, J (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’. pp. 47–70. (Academic Press: San Diego)
Farquhar GD, Cernusak LA
(2005) On the isotopic composition of leaf water in the non-steady state. Functional Plant Biology 32, 293–303.
| Crossref |
Farquhar, GD ,
Hubick, KT ,
Condon, AG ,
and
Richards, RA (1989). Carbon isotope discrimination and water-use efficiency. In ‘Stable isotopes in ecological research’. pp. 21–46. (Springer-Verlag: New York)
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.
| Crossref | GoogleScholarGoogle Scholar |
Fisk MC,
Fahey TJ,
Groffman PM, Bohlen PJ
(2004) Earthworm invasion, fine root distributions, and soil respiration in north temperate forests. Ecosystems 7, 55–62.
| Crossref |
Flanagan LB, Ehleringer JR
(1991) Effects of mild water stress and diurnal changes in temperature and humidity on the stable oxygen and hydrogen isotopic composition of leaf water in Cornus stolonifera L. Plant Physiology 97, 298–305.
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 Biogeochemical Cycles 11, 83–98.
| Crossref | GoogleScholarGoogle Scholar |
Flanagan LB,
Kubien DS, Ehleringer JR
(1999) Spatial and temporal variation in the carbon and oxygen stable isotope ratio of respired CO2 in a boreal forest ecosystem. Tellus 51B, 367–384.
Francey RJ, Tans PP
(1987) Latitudinal variation in oxygen-18 of atmospheric CO2. Nature 327, 495–497.
| Crossref | GoogleScholarGoogle Scholar |
Gansert D
(2003) Xylem sap flow as a major pathway for oxygen supply to the sapwood of birch (Betula pubescens Ehr.). Plant, Cell & Environment 26, 1803–1814.
| Crossref | GoogleScholarGoogle Scholar |
Gillon JS, Yakir D
(2001) Influence of carbonic anhydrase activity in terrestrial vegetation on the 18O content of atmospheric CO2. Science 291, 2584–2587.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Griffin KL,
Anderson OR,
Tissue DT,
Turnbull MH, Whitehead D
(2004) Variations in dark respiration and mitochondrial numbers within needles of Pinus radiata grown in ambient or elevated CO2 partial pressure. Tree Physiology 24, 347–353.
| PubMed |
Grulke NE,
Alonso R,
Nguyen T,
Cascio C, Dobrowolski W
(2004) Stomata open at night in pole-sized and mature ponderosa pine: implications for O3 exposure metrics. Tree Physiology 24, 1001–1010.
| PubMed |
Harwood KG,
Gillon JS,
Griffiths H, Broadmeadow MSJ
(1998) Diurnal variation of Δ13CO2, ΔC18O16O, and evaporative site enrichment of δH2
18O in Piper aduncum under field condition in Trinidad. Plant, Cell & Environment 21, 269–283.
| Crossref | GoogleScholarGoogle Scholar |
Kato T,
Nakazawa T,
Aoki S,
Sugawara S, Ishizawa M
(2004) Seasonal variation of the oxygen isotopic ratio of atmospheric carbon dioxide in a temperate forest, Japan. Global Biogeochemical Cycles 18, GB2020.
| Crossref | GoogleScholarGoogle Scholar |
Kays, WM (1966).
Kelliher FM,
Ross DJ,
Law BE,
Baldocchi DD, Rodda NJ
(2004) Limitations to carbon mineralization in litter and mineral soil of young and old ponderosa pine forests. Forest Ecology and Management 191, 201–213.
| Crossref | GoogleScholarGoogle Scholar |
Klumpp K,
Schäufele R,
Lötscher M,
Lattanzi FA,
Feneis W, Schnyder H
(2005) C-isotope composition of CO2 respired by shoots and roots: fractionation during dark respiration? Plant, Cell & Environment 28, 241–250.
| Crossref | GoogleScholarGoogle Scholar |
Li-Cor Biosciences (2002).
Litton CM,
Ryan MG,
Knight DH, Stahl PD
(2003) Soil-surface carbon dioxide efflux and microbial biomass in relation to tree density 13 years after a stand replacing fire in a lodgepole pine ecosystem. Global Change Biology 9, 680–696.
| Crossref | GoogleScholarGoogle Scholar |
Masle J,
Farquhar GD, Wong SC
(1992) Transpiration ratio and plant mineral content are related among genotypes of a range of species. Australian Journal of Plant Physiology 19, 709–721.
McDonald EP,
Erickson JE, Kruger EL
(2002) Can decreased transpiration limit plant nutrient acquisition in elevated CO2? Functional Plant Biology 29, 1115–1120.
| Crossref | GoogleScholarGoogle Scholar |
Miller JB,
Yakir D,
White JWC, Tans PP
(1999) Measurement of 18O / 16O in the soil–atmosphere CO2 flux. Global Biogeochemical Cycles 13, 761–774.
| Crossref | GoogleScholarGoogle Scholar |
Moroney JV,
Bartlett SG, Samuelsson G
(2001) Carbonic anhydrases in plants and algae. Plant, Cell & Environment 24, 141–153.
Muchow RC,
Ludlow MM,
Fisher MJ, Myers RJK
(1980) Stomatal behaviour of kenaf and sorghum in a semiarid tropical environment. I. During the night. Australian Journal of Plant Physiology 7, 609–619.
Musselman RC, Minnick TJ
(2000) Nocturnal stomatal conductance and ambient air quality standards for ozone. Atmospheric Environment 34, 719–733.
| Crossref | GoogleScholarGoogle Scholar |
Nobel, PS (1983).
Ogée J,
Peylin P,
Cuntz M,
Bariac T,
Brunet Y,
Berbigier P,
Richard P, Ciais P
(2004) Partitioning net ecosystem carbon exchange into net assimilation and respiration with canopy-scale isotopic measurements: an error propagation analysis with 13CO2 and CO18O data. Global Biogeochemical Cycles 18, 2019.
| Crossref |
Ometto JPH,
Flanagan LB,
Martinelli LA, Ehleringer JR
(2005) Oxygen isotope ratios of waters and respired CO2 in Amazonian forest and pasture ecosystems. Ecological Applications 15, 58–70.
Parisi G,
Perales M,
Fornasaru MS,
Colaneri A, Gonzalez-Schain N ,
et al
.
(2004) Gamma carbonic anhydrases in plant mitochondria. Plant Molecular Biology 55, 193–207.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Raschke, K (1979). Movements of stomata. In ‘Encyclopedia of plant physiology. Vol. 7’. pp. 383–441. (Springer: Berlin)
Šantrůček J,
Šimáňová E,
Karbulková J,
Šimková M, Scheiber L
(2004) A new technique for measurement of water permeability of stomatous cuticular membranes isolated from Hedera helix leaves. Journal of Experimental Botany 55, 1411–1422.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schnyder H,
Schäufele R,
Lötscher M, Gebbing T
(2003) Disentangling CO2 fluxes: direct measurements of mesocosm-scale natural abundance 13CO2 / 12CO2 gas exchange, 13C discrimination, and labelling of CO2 exchange flux components in controlled environments. Plant, Cell & Environment 26, 1863–1874.
| Crossref | GoogleScholarGoogle Scholar |
Seibt U,
Wingate L,
Berry JA, Lloyd J
(2005) Diurnal discrimination against 13C and 18O during carbon uptake by Picea sitchensis branches: 3. Evidence for non-steady state effects in photosynthetic 18O discrimination in the field. Plant, Cell & Environment (In press) ,
Stern LA,
Amundson R, Baisden WT
(2001) Influence of soils on oxygen isotope ratio of atmospheric CO2. Global Biogeochemical Cycles 15, 753–760.
| Crossref | GoogleScholarGoogle Scholar |
Snyder KA,
Richards JH, Donovan LA
(2003) Night-time conductance in C3 and C4 species: do plants lose water at night? Journal of Experimental Botany 54, 861–865.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tans PP
(1998) Oxygen isotopic equilibrium between carbon dioxide and water in soils. Tellus 50B, 163–178.
Tissue DT,
Griffin KL,
Turnbull MH, Whitehead D
(2005) Stomatal and non-stomatal limitations to photosynthesis in four tree species in a temperate rainforest dominated by Dacrydium cupressinum in New Zealand. Tree Physiology 25, 447–456.
| PubMed |
Turnbull MH,
Whitehead D,
Tissue DT,
Schuster WSF,
Brown KJ, Griffin KL
(2001) Responses of leaf respiration to temperature and leaf characteristics in three deciduous tree species vary with site water availability. Tree Physiology 21, 571–578.
| PubMed |
Tyree MT, Wilmot TR
(1990) Errors in the calculation of evaporation and leaf conductance in steady-state porometry: the importance of accurate measurement of leaf temperature. Canadian Journal of Forestry Research 20, 1031–1035.
von Caemmerer S, Farquhar GD
(1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387.
| Crossref | GoogleScholarGoogle Scholar |
Wang X-F,
Yakir D, Avishai M
(1998) Non-climatic variations in the oxygen isotopic compositions of plants. Global Change Biology 4, 835–849.
| Crossref | GoogleScholarGoogle Scholar |
Whitehead D,
Hall GMJ,
Walcroft AS,
Brown KJ, Landsberg JJ ,
et al
.
(2002) Analysis of the growth of rimu (Dacrydium cupressinum) in South Westland, New Zealand, using process-based simulation models. International Journal of Biometeorology 46, 66–75.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Whitehead D,
Griffin KL,
Turnbull MH,
Tissue DT,
Engel VC,
Brown KJ,
Schuster WSF, Walcroft AS
(2004a) Response of total night-time respiration to differences in total daily photosynthesis for leaves in a Quercus rubra L. canopy: implications for modelling canopy CO2 exchange. Global Change Biology 10, 925–938.
| Crossref | GoogleScholarGoogle Scholar |
Whitehead, D ,
Walcroft, AS ,
Griffin, KL ,
Tissue, DT ,
Turnbull, MH ,
Engel, V ,
Brown, KJ ,
and
Schuster, WSF (2004b). Scaling carbon uptake from leaves to canopies: insights from two forests with contrasting properties. In ‘Forest at the land–atmosphere interface’. b. pp. 231–254. (CAB International: Wallingford)
Yakir D, Wang X-F
(1996) Fluxes of CO2 and water between terrestrial vegetation and the atmosphere estimated from isotope measurements. Nature 380, 515–517.
| Crossref | GoogleScholarGoogle Scholar |
Zeiger, E ,
Field, C ,
and
Mooney, HA (1981). Stomatal opening at dawn : possible roles of the blue light response in nature. In ‘Plants and the daylight spectrum’. pp. 391–407. (Academic Press: London)
