Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology

Canopy development and hydraulic function in Eucalyptus tereticornis grown in drought in CO2-enriched atmospheres

Brian J. Atwell A E , Martin L. Henery A B , Gordon S. Rogers C , Saman P. Seneweera D , Marie Treadwell A and Jann P. Conroy D

A Department of Biological Sciences, Macquarie University, NSW 2109, Australia.

B School of Botany and Zoology, The Australian National University, Canberra, ACT 0200, Australia.

C AHR Consulting, PO Box 552, Sutherland, NSW 2232, Australia.

D Centre for Plant and Food Sciences, University of Western Sydney, Hawkesbury, Locked Bag No. 1, Richmond, NSW 2753, Australia.

E Corresponding author. Email:

Functional Plant Biology 34(12) 1137-1149
Submitted: 20 December 2006  Accepted: 3 October 2007   Published: 27 November 2007


We report on the relationship between growth, partitioning of shoot biomass and hydraulic development of Eucalyptus tereticornis Sm. grown in glasshouses for six months. Close coordination of stem vascular capacity and shoot architecture is vital for survival of eucalypts, especially as developing trees are increasingly subjected to spasmodic droughts and rising atmospheric CO2 levels. Trees were exposed to constant soil moisture deficits in 45 L pots (30–50% below field capacity), while atmospheric CO2 was raised to 700 μL CO2 L–1 in matched glasshouses using a hierarchical, multi-factorial design. Enrichment with CO2 stimulated shoot growth rates for 12–15 weeks in well-watered trees but after six months of CO2 enrichment, shoot biomasses were not significantly heavier (30% stimulation) in ambient conditions. By contrast, constant drought arrested shoot growth after 20 weeks under ambient conditions, whereas elevated CO2 sustained growth in drought and ultimately doubled the shoot biomass relative to ambient conditions. These growth responses were achieved through an enhancement of lateral branching up to 8-fold due to CO2 enrichment. In spite of larger transpiring canopies, CO2 enrichment also improved the daytime water status of leaves of droughted trees. Stem xylem development was highly regulated, with vessels per unit area and cross sectional area of xylem vessels in stems correlated inversely across all treatments. Furthermore, vessel numbers related to the numbers of leaves on lateral branches, broadly supporting predictions arising from Pipe Model Theory that the area of conducting tissue should correlate with leaf area. Diminished water use of trees in drought coincided with a population of narrower xylem vessels, constraining hydraulic capacity of stems. Commensurate with the positive effects of elevated CO2 on growth, development and leaf water relations of droughted trees, the capacity for long-distance water transport also increased.

Additional keywords: biomass allocation, carbon dioxide, drought, xylem.


Ainsworth EA Long SP 2005 What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. The New Phytologist 165 351 371 doi:10.1111/j.1469-8137.2004.01224.x

Amthor JS 1995 Terrestrial higher-plant response to increasing atmospheric [CO2] in relation to the global carbon cycle. Global Change Biology 1 243 274 doi:10.1111/j.1365-2486.1995.tb00025.x

Atkinson CJ Taylor JM 1996 Effects of elevated CO2 on stem growth, vessel area and hydraulic conductivity of oak and cherry seedlings. The New Phytologist 133 617 626 doi:10.1111/j.1469-8137.1996.tb01930.x

Atwell BJ Henery ML Whitehead D 2003 Sapwood development in Pinus radiata trees grown for three years at ambient and elevated carbon dioxide partial pressures. Tree Physiology 23 13 21

Australian Greenhouse Office (2003) ‘Climate change: an Australian guide to the science and potential impacts’. (Ed. B Pittock). Commonwealth of Australia. (Paragon Printers: Canberra)

Bazzaz FA Miao SL Wayne PM 1993 CO2-induced growth enhancements of co-occurring tree species decline at different rates. Oecologia 96 478 482

Berryman CA Eamus D Duff GA 1993 The influence of CO2 enrichment on growth, nutrient content and biomass allocation of Maranthes corymbosa. Australian Journal of Botany 41 195 209 doi:10.1071/BT9930195

Bucher JB , Tarjan DP , Siegwolf RTW , Saurer M , Blum H , Hendrey GR (1997) Growth of deciduous tree seedling communities in response to elevated CO2 and nutrient supply. In ‘Proceedings from the IUFRO 17th international meeting for specialists in air pollution effects on forest ecosystems – stress factors and air pollution, Florence, Italy. Vol. 36’. pp. 777–782. (Elsevier: Oxford)

Bunce JA Ziska LH 1998 Decreased hydraulic conductance in plants at elevated carbon dioxide. Plant, Cell & Environment 21 121 123 doi:10.1046/j.1365-3040.1998.00256.x

Ceulemans R Mousseau M 1994 Effects of elevated atmospheric CO2 on woody plants. The New Phytologist 127 425 446 doi:10.1111/j.1469-8137.1994.tb03961.x

Conroy JP Milham PJ Barlow EWR 1992 Effect of nitrogen and phosphorus availability on the growth response of Eucalyptus grandis to high carbon dioxide. Plant, Cell & Environment 15 843 847 doi:10.1111/j.1365-3040.1992.tb02152.x

Cowan IR (1977) Stomatal behaviour and environment. In ‘Advances in botanical research. Vol. 4’. (Eds RD Preston, HW Woolhouse) pp. 117–228. (Academic Press: NY, USA)

Curtis PS Wang X 1998 A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology. Oecologia 113 299 313 doi:10.1007/s004420050381

Dufrêne E Pontailler JY Saugier B 1993 A branch bag technique for simultaneous CO2 enrichment and assimilation measurements on beech (Fagus sylvatics L.). Plant, Cell & Environment 16 1131 1138 doi:10.1111/j.1365-3040.1996.tb02071.x

Eamus D Berryman CA Duff GA 1995 The impact of CO2 enrichment on water relations in Maranthes corymbosa and Eucalyptus tetrodonta. Australian Journal of Botany 43 273 282 doi:10.1071/BT9950273

Eamus D Jarvis PG 1989 The direct effects of increase in the global atmospheric CO2 concentration on natural and commercial temperate trees and forests. Advances in Ecological Research 19 1 55

Field CB Jackson RB Mooney HA 1995 Stomatal responses to increased CO2: implications from the plant to the global scale. Plant, Cell & Environment 18 1214 1225

Gardner WR (1968) Availability and measurement of soil water. In ‘Water deficits and plant growth. Vol 1’. (Ed. TT Kozlowski) pp. 107–135. (Academic Press: New York)

Gielen B Calfapietra C Claus C Sabatti M Ceulemans R 2002 Crown architecture of Populus spp. is differentially modified by free-air CO2 enrichment (POPFACE). The New Phytologist 153 91 99 doi:10.1046/j.0028-646X.2001.00301.x

Gunderson CA Wullschleger SD 1994 Photosynthetic acclimation in trees to rising atmospheric CO2: a broader perspective. Photosynthesis Research 39 369 388 doi:10.1007/BF00014592

Hacke UG Sperry JS Ewers BE Ellsworth DE Schafer DVR Oren R 2000 Influence of soil porosity on water use in Pinus taeda. Oecologia 124 495 505 doi:10.1007/PL00008875

Hättenschwiler S Körner C 1997 Biomass allocation and canopy development in spruce model ecosystems under elevated CO2 and increased N deposition. Oecologia 113 104 114 doi:10.1007/s004420050358

Heath J Kerstiens G 1997 Effects of elevated CO2 on leaf gas exchange in beech and oak at two levels of nutrient supply: consequences for sensitivity to drought in beech. Plant, Cell & Environment 20 57 67 doi:10.1046/j.1365-3040.1997.d01-13.x

Hibbs DE Chan SS Castellano M Niu C-H 1995 Response of red alder seedlings to CO2 enrichment and water stress. The New Phytologist 129 569 577 doi:10.1111/j.1469-8137.1995.tb03024.x

Hopmans P Stewart HTL Flinn DW 1993 Impacts of harvesting on nutrients in a eucalypt ecosystem in southeastern Australia. Forest Ecology and Management 59 29 51 doi:10.1016/0378-1127(93)90069-Y

Idso SB Kimball BA Allen SG 1991 CO2 enrichment of sour orange trees: 2.5 years into a long-term experiment. Plant, Cell & Environment 14 351 353 doi:10.1111/j.1365-3040.1991.tb01512.x

Jach ME Ceulemans R 1999 Effects of elevated atmospheric CO2 on phenology, growth and crown structure of Scots pine (Pinus sylvestris) seedlings after two years of exposure in the field. Tree Physiology 19 289 300

Janssens IA Medlyn B Gielen B Laureysens I Jach ME van Hove D Ceulemans R 2005 Carbon budget of Pinus sylvestris saplings after four years of exposure to elevated atmospheric carbon dioxide concentration. Tree Physiology 25 325 337

Johnsen KH 1993 Growth and ecophysiological responses of black spruce seedlings to elevated CO2 under varied water and nutrient additions. Canadian Journal of Forest Research 23 1033 1042

Kirschbaum M Kueppers M Schneider H Giersch C Noe S 1997 Modelling photosynthesis in fluctuating light with inclusion of stomatal conductance, biochemical activation and pools of key photosynthetic intermediates. Planta 204 16 26 doi:10.1007/s004250050225

Li C Wang K 2003 Differences in drought responses of three contrasting Eucalyptus microtheca F. Muell. populations. Forest Ecology and Management 179 377 385 doi:10.1016/S0378-1127(02)00552-2

Liberloo M Calfapietra C Lukac M Godbold D Luo Z-B et al 2006 Woody biomass production during the second rotation of a bio-energy Populus plantation increases in a future high CO2 world. Global Change Biology 12 1094 1106 doi:10.1111/j.1365-2486.2006.01118.x

Lovisolo C Schubert A 1998 Effects of water stress on vessel size and xylem hydraulic conductivity in Vitis vinifera L. Journal of Experimental Botany 49 693 700 doi:10.1093/jexbot/49.321.693

Medlyn BE Barton CVM Broadmeadow MSJ Ceulemans R De Angelis P et al 2001 Stomatal conductance of forest species after long-term exposure to elevated CO2 concentration: a synthesis. The New Phytologist 149 247 264 doi:10.1046/j.1469-8137.2001.00028.x

Meinzer FC 2002 Co-ordination of vapour and liquid phase water transport properties in plants. Plant, Cell & Environment 25 265 274 doi:10.1046/j.1365-3040.2002.00781.x

Melillo JM McGuire AD Kicklighter DW Moore BIII Vorosmarty CJ Schloss AL 1993 Global climate change and terrestrial net primary production. Nature 363 234 240 doi:10.1038/363234a0

Milburn JA (1979) ‘Water flow in plants.’ (Longman: London, UK)

Mokany K McMurtrie RE Atwell BJ Keith H 2003 The interaction between the sapwood and foliage of Alpine ash (Eucalyptus delegatensis) trees as they grow taller. Tree Physiology 23 949 958

Murray MB , Ceulemans R (1996) Will tree foliage be larger and live longer? In ‘The likely impact of rising CO2 and temperature on European forests. ECOCRAFT Final Report’. (Ed. P Jarvis) pp. 95–125.

Norby RJ Wullschleger SD Gunderson CA Nietch CT 1995 Increased growth efficiency of Quercus alba trees in a CO2-enriched atmosphere. The New Phytologist 131 91 97

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 & Environment 22 683 714 doi:10.1046/j.1365-3040.1999.00391.x

Nowak RS Smith SD Ellsworth DS 2004 Functional responses of plants to elevated atmospheric CO2 – do photosynthetic and productivity data from FACE experiments support early predictions? The New Phytologist 162 253 280 doi:10.1111/j.1469-8137.2004.01033.x

Osório J Osório ML Chaves MM Pereira JS 1998 Water deficits are more important in delaying growth then in changing patterns of carbon allocation in Eucalyptus globulus. Tree Physiology 18 363 373

Reekie EG Bazzaz F 1989 Competition and patterns of resource use among seedlings of five tropical trees grown at ambient and elevated CO2. Oecologia 79 212 222

Rey A Jarvis PG 1997 Growth response of young birch trees (Betula pendula Roth.) after four and a half years of CO2 exposure. Annals of Botany 80 809 816 doi:10.1006/anbo.1997.0526

Roden JS Ball MC 1996 The effect of elevated [CO2] on growth and photosynthesis of two eucalyptus species exposed to high temperatures and water deficits. Plant Physiology 111 909 919

Rogers GS Payne L Milham P Conroy J 1993 Nitrogen and phosphorus requirements of cotton and wheat under changing CO2 concentrations. Plant and Soil 155–156 231 234

Rogers HH Sionit N Cure JD Smith JM Bingham GE 1984 Influence of elevated carbon dioxide on water relations of soybeans Glycine max cultivar Bragg. Plant Physiology 74 233 238

Santiago LS Goldstein G Meinzer FC Fisher JB Machado K Woodruff D Jones T 2004 Leaf photosynthetic traits scale with hydraulic conductivity and wood density in Panamanian forest canopy trees. Oecologia 140 543 550

Saxe H Ellsworth DS Heath J 1998 Tree and forest functioning in an enriched CO2 atmosphere. The New Phytologist 139 395 436 doi:10.1046/j.1469-8137.1998.00221.x

Sperry JS Hacke UG Wheeler JK 2005 Comparative analysis of end wall resistivity in xylem conduits. Plant, Cell & Environment 28 456 465 doi:10.1111/j.1365-3040.2005.01287.x

Tissue DT Thomas RB Strain BR 1997 Atmospheric CO2 enrichment increases growth and photosynthesis of Pinus taeda: a four year experiment in the field. Plant, Cell & Environment 20 1123 1134 doi:10.1046/j.1365-3040.1997.d01-140.x

Tyree MT Ewers FW 1991 The hydraulic architecture of trees and other woody plants. The New Phytologist 119 345 360 doi:10.1111/j.1469-8137.1991.tb00035.x

Tyree MT , Zimmermann MH (1983) ‘Xylem structure and the ascent of sap.’ (Springer Verlag: Berlin)

Waring RH , Schlesinger WH (1985) ‘Forest ecosystems: concepts and management.’ (Academic Press Inc.: Orlando, FL, USA)

Whitehead D Hogan KP Rogers GND Byers JN Hunt JE McSeveny TM Hollinger DY Dungan RJ Earl WB Bourke MP 1995 Performance of large open-top changers for long-term field investigations of tree response to elevated carbon dioxide concentration. Journal of Biogeography 22 307 313 doi:10.2307/2845925

Wong SC Kriedemann PE Farquhar GD 1992 CO2 × nitrogen interaction on seedling growth of four species of eucalypt. Australian Journal of Botany 40 457 472 doi:10.1071/BT9920457

Wullschleger SD , Norby RJ , Gunderson CA (1997) Forest trees and their response to atmospheric carbon dioxide enrichment: a compilation of results. In ‘Advances in carbon dioxide effects research’. Special Publication No. 61. (Eds LH Allen Jr, MB Kirkham, DM Olszyk, CE Whitman) pp. 79–100. (American Society of Agronomy: Madison, WI)

Wullschleger SD Tschaplinski TJ Norby RJ 2002 Plant water relations at elevated CO2 – implications for water-limited environments. Plant, Cell & Environment 25 319 331 doi:10.1046/j.1365-3040.2002.00796.x

Export Citation