Oecologia

, Volume 143, Issue 4, pp 652–660

Stomatal conductance and not stomatal density determines the long-term reduction in leaf transpiration of poplar in elevated CO2

  • Penny J. Tricker
  • Harriet Trewin
  • Olevi Kull
  • Graham J. J. Clarkson
  • Eve Eensalu
  • Matthew J. Tallis
  • Alessio Colella
  • C. Patrick Doncaster
  • Maurizio Sabatti
  • Gail Taylor
Global Change Ecology

Abstract

Using a free-air CO2 enrichment (FACE) experiment, poplar trees (Populus × euramericana clone I214) were exposed to either ambient or elevated [CO2] from planting, for a 5-year period during canopy development, closure, coppice and re-growth. In each year, measurements were taken of stomatal density (SD, number mm−2) and stomatal index (SI, the proportion of epidermal cells forming stomata). In year 5, measurements were also taken of leaf stomatal conductance (gs, μmol m−2 s−1), photosynthetic CO2 fixation (A, mmol m−2 s−1), instantaneous water-use efficiency (A/E) and the ratio of intercellular to atmospheric CO2 (Ci:Ca). Elevated [CO2] caused reductions in SI in the first year, and in SD in the first 2 years, when the canopy was largely open. In following years, when the canopy had closed, elevated [CO2] had no detectable effects on stomatal numbers or index. In contrast, even after 5 years of exposure to elevated [CO2], gs was reduced, A/E was stimulated, and Ci:Ca was reduced relative to ambient [CO2]. These outcomes from the long-term realistic field conditions of this forest FACE experiment suggest that stomatal numbers (SD and SI) had no role in determining the improved instantaneous leaf-level efficiency of water use under elevated [CO2]. We propose that altered cuticular development during canopy closure may partially explain the changing response of stomata to elevated [CO2], although the mechanism for this remains obscure.

Keywords

Populus × euramericana Stomatal numbers Stomatal conductance POPFACE 

References

  1. Ainsworth EA, Rogers A, Blum H, Nösberger J, Long SP (2003) Variation in acclimation of photosynthesis in Trifolium repens after eight years of exposure to free air CO2 enrichment (FACE). J Exp Bot 54:2769–2774PubMedCrossRefGoogle Scholar
  2. Baker JT, Allen LH (1994) Assessment of the impact of rising Carbon-dioxide and other potential climate changes on vegetation. Environ Pollut 83:223–235PubMedCrossRefGoogle Scholar
  3. Bernacchi CJ, Calfapietra C, Davey PA, Wittig VE, Scarascia-Mugnozza GE, Raines CA, Long SP (2003) Photosynthesis and stomatal conductance responses of poplars to free-air CO2 enrichment (PopFACE) during the first growth cycle and immediately following coppice. New Phytol 159:609–621CrossRefGoogle Scholar
  4. Bird SM, Gray JE (2003) Signals from the cuticle affect epidermal cell differentiation. New Phytol 157:9–23CrossRefGoogle Scholar
  5. Calfapietra C, Gielen B, Galema ANJ, Lukac M, Moscatelli MC, Ceulemans R, Scarascia-Mugnozza G (2003) Free-air CO2 enrichment (FACE) enhances biomass production in a short-rotation poplar plantation (POPFACE). Tree Physiol 23:805–814PubMedGoogle Scholar
  6. Cech PG, Pepin S, Körner C (2003) Elevated CO2 reduces sap flux in mature deciduous forest trees. Oecologia 137:258–268PubMedCrossRefGoogle Scholar
  7. Ceulemans R, Van Praet L, Jiang XN (1995) Effects of CO2 enrichment, leaf position and clone on stomatal index and epidermal cell density in poplar (Populus). New Phytol 131:99–107CrossRefGoogle Scholar
  8. Crawley MJ (2002) Statistical computing: an introduction to data analysis using S-plus. Wiley, ChichesterGoogle Scholar
  9. Croxdale JL (2000) Stomatal patterning in angiosperms. Am J Bot 87:1069–1080PubMedCrossRefGoogle Scholar
  10. Eamus D (1999) The interaction of rising CO2 and temperature with water-use efficiency. Plant Cell Environ 14:843–852CrossRefGoogle Scholar
  11. Ferris G, Taylor G (1994) Stomatal characteristics of four native herbs following exposure to elevated CO2. Ann Bot 73:477–453CrossRefGoogle Scholar
  12. Ferris R, Sabatti M, Miglietta F, Mills RF, Taylor G (2001) Leaf area is stimulated in Populus by free air CO2 enrichment (POPFACE) through increased cell expansion and production. Plant Cell Environ 24:305–315CrossRefGoogle Scholar
  13. Fiscus EL, Reid CD, Miller JE, Heagle AS (1997) Elevated CO2 reduces O3 flux and O3-induced yield losses in soybeans: possible implications for elevated CO2 studies. J Exp Bot 48:307–313CrossRefGoogle Scholar
  14. Frechilla S, Talbott LD, Zeiger E (2002) The CO2 response of Vicia cells acclimates to growth environment. J Exp Bot 53:1–6CrossRefGoogle Scholar
  15. Gielen B, Calfapietra C, Sabatti M, Ceulemans R (2001) Leaf area dynamics in a closed poplar plantation under free-air carbon dioxide enrichment. Tree Physiol 21:1245–1255PubMedGoogle Scholar
  16. Gielen B, Liberloo M, Bogaert J, Calfapietra C, de Angelis P, Miglietta F, Scarascia-Mugnozza G, Ceulemans R (2003) Three years of free-air CO2 enrichment (POPFACE) only slightly affect profiles of light and leaf characteristics in closed canopies of Populus. Global Change Biol 9:1022–1037CrossRefGoogle Scholar
  17. Gray JE, Holroyd GH, van der Lee FM, Bahrami AR, Sijmons PC, Woodward FI, Schuch W, Hetherington AM (2000) The HIC signalling pathway links CO2 perception to stomatal development. Nature 408:713–716PubMedCrossRefGoogle Scholar
  18. Gunderson CA, Sholtis JD, Wullschleger SD, Tisuue DT, Hanson PJ (2002) Environmental and stomatal control of photosynthetic enhancement in the canopy of a sweetgum (Liquidambar styraciflua L.) plantation during 3 years of CO2 enrichment. Plant Cell Environ 25:379–393CrossRefGoogle Scholar
  19. Heath OVS, Russell J (1954) An investigation of the light response of wheat stomata with attempted elimination of control by the mesophyll. II Interactions with carbon dioxide. J Exp Bot 5:269–292CrossRefGoogle Scholar
  20. Herrick JD, Maherali H, Thomas RB (2004) Reduced stomatal conductance in sweetgum (Liquidambar styaciflua) sustained over long-term CO2 enrichment. New Phytol 162:387–396CrossRefGoogle Scholar
  21. Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908PubMedCrossRefGoogle Scholar
  22. Holroyd GH, Hetherington AM, Gray JE (2002) A role for the cuticular waxes in the environmental control of stomatal development. New Phytol 153:433–439Google Scholar
  23. Jackson RB, Sala OE, Field CB, Mooney HA (1994) CO2 alters water-use, carbon gain and yield for the dominant species in a natural grassland. Oecologia 98:257–262CrossRefGoogle Scholar
  24. Jarvis AJ, Mansfield TA, Davies WJ (1999) Stomatal behaviour, photosynthesis and transpiration under rising CO2. Plant Cell Environ 22:639–648CrossRefGoogle Scholar
  25. Lake JA, Quick WP, Beerling DJ, Woodward FI (2001) Signals from mature to new leaves. Nature 411:154PubMedCrossRefGoogle Scholar
  26. Lake JA, Woodward FI, Quick WP (2002) Long-distance CO2 signalling in plants. J Exp Bot 53:183–193PubMedCrossRefGoogle Scholar
  27. Maherali H, Reid CD, Polley HW, Johnson HB, Jackson RB (2002) Stomatal acclimation over a subambient to elevated CO2 gradient in a C3/C4 grassland. Plant Cell Environ 25:557–566CrossRefGoogle Scholar
  28. Medlyn BE, Barton CVM, Broadmeadow MSJ, Ceulemans R, De Angelis P, Forstreuter M, Freeman M, Jackson SB, Kelomäski S, Laitat E, Rey A, Roberntz P, Sigurdsson SB, Strassmeyer J, Wang K, Curtis PS, Jarvis PG (2001) Stomatal conductance of forest species after long-term exposure to elevated CO2 concentration: a synthesis. New Phytol 149:247–264CrossRefGoogle Scholar
  29. Miglietta F, Peresotti A, Vaccari FP, Zaldei A, deAngelis P, Scarascia-Mugnozza G (2001) Free-air CO2 enrichment (FACE) of a poplar plantation: The POPFACE fumigation system. New Phytol 150:465–476CrossRefGoogle Scholar
  30. Noormets A, Sôber A, Pell EJ, Dickson RE, Podila GK, Sôber J, Isebrands JG, Karnosky DF (2001) Stomatal and non-stomatal limitation to photosynthesis in two trembling aspen (Populus tremuloides Michx.) clones exposed to elevated CO2 and/ or O3. Plant Cell Environ 24:327–336CrossRefGoogle Scholar
  31. Norby RJ, Wullschleger SD, Gunderson CA, Johnson DW, Ceulemans R (1999) Tree responses to rising CO2 in field experiments: Implications for the future forest. Plant Cell Environ 22:683–714CrossRefGoogle Scholar
  32. Reid CD, Maherali H, Johnson HB, Smith SD, Wullschleger SD, Jackson RB (2003) On the relationship between stomatal characters and atmospheric CO2. Geophys Res Lett 30:1–4CrossRefGoogle Scholar
  33. Rey A, Jarvis PG (1997) An overview of long-term effects of elevated atmospheric CO2 concentration on growth and physiology of birch (Betula pendula Roth.). Bot J Scotland 49:325–340CrossRefGoogle Scholar
  34. Royer DL (2001) Stomatal density and stomatal index as indicators of paleoatmospheric CO2 concentration. Rev Paleobot Palynol 114:1–28CrossRefGoogle Scholar
  35. Saxe H, Ellsworth DS, Heath J (1998) Tree and forest functioning in an enriched CO2 atmosphere. New Phytol 139:395–436CrossRefGoogle Scholar
  36. Talbott LD, Srivastava A, Zeiger E (1996) Stomata from growth-chamber grown Vicia faba have an enhanced sensitivity to CO2. Plant Cell Environ 19:1188–1194PubMedCrossRefGoogle Scholar
  37. Talbott LD, Rahveh E, Zeiger E (2003) Relative humidity is a key factor in the acclimation of the stomatal response to CO2. J Exp Bot 54:2141–2147PubMedCrossRefGoogle Scholar
  38. Taylor G (2002) Populus. Arabidopsis for forestry. Do we need a model tree? Ann Bot 90:681–689PubMedCrossRefGoogle Scholar
  39. Taylor G, Tricker PJ, Zhang FZ, Alston VJ, Miglietta F, Kuzminsky E (2003) Spatial and temporal effects of free-air CO2 enrichment (POPFACE) on leaf growth, cell expansion and production in a closed canopy of Populus. Plant Physiol 131:177–185PubMedCrossRefGoogle Scholar
  40. Underwood AJ (1997) Experiments in Ecology: Their Logical Design and Interpretation Using Analysis of Variance. Cambridge Univ Press, CambridgeGoogle Scholar
  41. Woodward FI (1987) Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels. Nature 327:617–618CrossRefGoogle Scholar
  42. Woodward FI, Kelly CK (1995) The influence of CO2 concentration on stomatal density. New Phytol 131:311–327CrossRefGoogle Scholar
  43. Woodward FI, Lake JA, Quick WP (2002) Stomatal development and CO2: ecological consequences. New Phytol 153:477–484CrossRefGoogle Scholar
  44. Wullschleger SD, Gunderson CA, Hanson PJ, Wilson KB, Norby RJ (2002) Sensitivity of stomatal and canopy conductance to elevated CO2 concentration—interacting variables and perspectives of scale. New Phytol 153:485–496CrossRefGoogle Scholar
  45. Wullschleger SD, Tschaplinski TJ, Norby RJ (2002) Plant water relations at elevated CO2—implications for water-limited environments. Plant Cell Environ 25:319–331PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Penny J. Tricker
    • 1
  • Harriet Trewin
    • 1
  • Olevi Kull
    • 2
  • Graham J. J. Clarkson
    • 1
  • Eve Eensalu
    • 2
  • Matthew J. Tallis
    • 1
  • Alessio Colella
    • 3
  • C. Patrick Doncaster
    • 1
  • Maurizio Sabatti
    • 4
  • Gail Taylor
    • 1
  1. 1.School of Biological SciencesUniversity of SouthamptonSouthamptonUK
  2. 2.Institute of Botany and EcologyTartuEstonia
  3. 3.Department of Environmental SciencesII University of NaplesCasertaItaly
  4. 4.Department of Forest Environment and ResourcesUniversita degli Studi della TusciaViterboItaly

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