Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Why is plant-growth response to elevated CO2 amplified when water is limiting, but reduced when nitrogen is limiting? A growth-optimisation hypothesis

Ross E. McMurtrie A G , Richard J. Norby B , Belinda E. Medlyn C , Roderick C. Dewar D , David A. Pepper A , Peter B. Reich E and Craig V. M. Barton F
+ Author Affiliations
- Author Affiliations

A School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia.

B Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831-6422, USA.

C School of Biological Sciences, Macquarie University, Sydney, NSW 2019, Australia.

D Laboratory of Functional Ecology and Environmental Physics (EPHYSE), INRA Centre de Bordeaux-Aquitaine, BP81, 33883 Villenave d’Ornon, France.

E Department of Forest Resources, University of Minnesota, St Paul, MN 55108, USA.

F Forest Resources Research, NSW Department of Primary Industry, PO Box 100, Beecroft, NSW 2119, Australia.

G Corresponding author. Email: r.mcmurtrie@unsw.edu.au

H This paper originates from a presentation at EcoFIZZ 2007, Richmond, New South Wales, Australia, September 2007.

Functional Plant Biology 35(6) 521-534 https://doi.org/10.1071/FP08128
Submitted: 15 April 2008  Accepted: 4 June 2008   Published: 4 August 2008

Abstract

Experimental evidence indicates that the stomatal conductance and nitrogen concentration ([N]) of foliage decline under CO2 enrichment, and that the percentage growth response to elevated CO2 is amplified under water limitation, but reduced under nitrogen limitation. We advance simple explanations for these responses based on an optimisation hypothesis applied to a simple model of the annual carbon–nitrogen–water economy of trees growing at a CO2-enrichment experiment at Oak Ridge, Tennessee, USA. The model is shown to have an optimum for leaf [N], stomatal conductance and leaf area index (LAI), where annual plant productivity is maximised. The optimisation is represented in terms of a trade-off between LAI and stomatal conductance, constrained by water supply, and between LAI and leaf [N], constrained by N supply. At elevated CO2 the optimum shifts to reduced stomatal conductance and leaf [N] and enhanced LAI. The model is applied to years with contrasting rainfall and N uptake. The predicted growth response to elevated CO2 is greatest in a dry, high-N year and is reduced in a wet, low-N year. The underlying physiological explanation for this contrast in the effects of water versus nitrogen limitation is that leaf photosynthesis is more sensitive to CO2 concentration ([CO2]) at lower stomatal conductance and is less sensitive to [CO2] at lower leaf [N].

Additional keywords: carbon–nitrogen–water economy, climate change, CO2 enrichment, forest model, leaf area index, stomatal conductance.


Acknowledgements

We acknowledge financial support from the Australian Research Council, the Australian Department of Climate Change, the US Department of Energy Office of Science, Biological and Environmental Research Program, the US National Science Foundation (LTER: 0080382, Biocomplexity: 0322057) and the Department of Energy Program for Ecological Research (Grant DE-FG02–96ER62291). We are grateful for support provided by TERACC (NSF Grant No. 0090238) for a modelling workshop held in Cronulla, Sydney, Australia, in 2006.


References


Ackerly DD (1999) Self-shading, carbon gain and leaf dynamics: a test of alternative optimality models. Oecologia 119, 300–310.
Crossref | GoogleScholarGoogle Scholar | open url image1

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, 351–372.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2], mechanisms and environmental interactions. Plant, Cell & Environment 30, 258–270.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Anten NPR (2002) Evolutionarily stable leaf area production in plant populations. Journal of Theoretical Biology 217, 15–32.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Anten NPR (2005) Optimal photosynthetic characteristics of individual plants in vegetation stands and implications for species coexistence. Annals of Botany 95, 495–506.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Anten NPR, Schieving F, Medina E, Werger MJA, Schuffelen P (1995) Optimal leaf area indices in C3 and C4 mono- and dicotyledonous species at low and high nitrogen availability. Physiologia Plantarum 95, 541–550.
Crossref | GoogleScholarGoogle Scholar | open url image1

Arp WJ, van Mierlo JEM, Berendse F, Snijders W (1998) Interactions between elevated CO2 concentration, nitrogen and water: effects on growth and water use of six perennial species. Plant, Cell & Environment 21, 1–11.
Crossref | GoogleScholarGoogle Scholar | open url image1

Baker JT, Allen LH, Boote KJ, Pickering NB (1997) Rice responses to drought under carbon dioxide enrichment. Photosynthesis and evapotranspiration. Global Change Biology 3, 129–138.
Crossref | GoogleScholarGoogle Scholar | open url image1

Barnard R, Barthes L, Le Roux X, Harmens H, Raschi A, Soussana J, Winkler B, Leadley PW (2004) Atmospheric CO2 elevation has little effect on nitrifying and denitrifying enzyme activity in four European grasslands. Global Change Biology 10, 488–497.
Crossref | GoogleScholarGoogle Scholar | open url image1

Byrne C, Jones MB (2002) Effects of elevated CO2 and nitrogen fertiliser on biomass productivity, community structure and species diversity of a semi-natural grassland in Ireland. Biology and Environment Proceedings of the Royal Irish Academy. Section B: Biological, Geological, and Chemical Science 102B, 141–150. open url image1

Centritto M, Lee HSJ, Jarvis PG (1999) Interactive effects of elevated [CO2] and drought on cherry (Prunus avium) seedlings – I. Growth, whole-plant water use efficiency and water loss. The New Phytologist 141, 129–140.
Crossref | GoogleScholarGoogle Scholar | open url image1

Comins HN, McMurtrie RE (1993) Long-term response of nutrient-limited forests to CO2-enrichment: equilibrium behavior of plant–soil models. Ecological Applications 3, 666–681.
Crossref | GoogleScholarGoogle Scholar | open url image1

Curtis PS, Wang XZ (1998) A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology. Oecologia 113, 299–313.
Crossref | GoogleScholarGoogle Scholar | open url image1

de Graaff M-A, van Groenigen K-J, Six J, Hungate B, van Kessel C (2006) Interactions between plant growth and soil nutrient cycling under elevated CO2: a meta-analysis. Global Change Biology 12, 2077–2091.
Crossref | GoogleScholarGoogle Scholar | open url image1

DeLucia EH, Moore DJ, Norby RJ (2005) Contrasting responses of forest ecosystems to rising atmospheric CO2: implications for the global C cycle. Global Biogeochemical Cycles 19, GB3006.
Crossref | GoogleScholarGoogle Scholar | open url image1

DeLucia EH, Drake JE, Thomas RB, Gonzalez-Meler M (2007) Forest carbon use efficiency: is respiration a constant fraction of gross primary production? Global Change Biology 13, 1157–1167.
Crossref | GoogleScholarGoogle Scholar | open url image1

Derner JD, Johnson HB, Kimball BA, Pinter PJ, Polley HW , et al. (2003) Above- and below-ground responses of C3–C4 species mixtures to elevated CO2 and soil water availability. Global Change Biology 9, 452–460.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dewar RC, McMurtrie RE (1996) Sustainable stemwood yield in relation to the nitrogen balance of forest plantations: a model analysis. Tree Physiology 16, 173–182.
PubMed |
open url image1

Dewar RC, Medlyn BE, McMurtrie RE (1998) A mechanistic analysis of light and carbon use efficiencies. Plant, Cell & Environment 21, 573–588.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dewar RC, Medlyn BE, McMurtrie RE (1999) Acclimation of the respiration/photosynthesis ratio to temperature: insights from a model. Global Change Biology 5, 615–622.
Crossref | GoogleScholarGoogle Scholar | open url image1

Diaz S, Grime J, Harris J, McPherson E (1993) Evidence of a feedback mechanism limiting plant response to elevated carbon dioxide. Nature 364, 616–617.
Crossref | GoogleScholarGoogle Scholar | open url image1

Eamus D , Hatton T , Cook P , Colvin C (2006) ‘Ecohydrology: vegetation function, water and resource management.’ (CSIRO Publishing: Collingwood)

Ellsworth DS, Reich PB, Naumburg ES, Koch GW, Kubiske ME, Smith SD (2004) Photosynthesis, carboxylation and leaf nitrogen responses of 16 species to elevated pCO2 across four free-air CO2 enrichment experiments in forest, grassland and desert. Global Change Biology 10, 2121–2138.
Crossref | GoogleScholarGoogle Scholar | open url image1

Farquhar GD , von Caemmerer S (1982) Modelling of photosynthetic response to environmental conditions. In ‘Physiological plant ecology II: water relations and carbon assimilation. Encyclopaedia of plant physiology. Vol. 12B’. (Eds O Lange, P Nobel, CB Osmond, H Zieger) pp. 549–587. (Springer-Verlag: Berlin)

Farquhar GD, Buckley TN, Miller JM (2002) Optimal stomatal control in relation to leaf area and nitrogen content. Silva Fennica 36, 625–637. open url image1

Field CB, Jackson RB, Mooney HA (1995) Stomatal responses to CO2: implications from the plant to the global scale. Plant, Cell & Environment 18, 1214–1225.
Crossref | GoogleScholarGoogle Scholar | open url image1

Field CB , Chapin FS III , Chiariello NR , Holland EA , Mooney HA (1996) The Jasper Ridge CO2 experiment: design and motivation. In ‘Carbon dioxide and terrestrial ecosystems’. (Eds GW Koch, HA Mooney) pp. 112–145. (Academic Press: San Diego)

Field CB, Lund CP, Chiariello NR, Mortimer BE (1997) CO2 effects on the water budget of grassland microcosm communities. Global Change Biology 3, 197–206.
Crossref | GoogleScholarGoogle Scholar | open url image1

Franklin O (2007) Optimal nitrogen allocation controls tree responses to elevated CO2. The New Phytologist 174, 811–822.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Franklin O, Ågren GI (2002) Leaf senescence and resorption as mechanisms of maximizing photosynthetic production during canopy development at N limitation. Functional Ecology 16, 727–733.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gill RA, Polley HW, Johnson HB, Anderson LJ, Maherali H, Jackson RB (2002) Nonlinear grassland responses to past and future atmospheric CO2. Nature 417, 279–282.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Guehl JM, Picon C, Aussenac G, Gross P (1994) Interactive effects of elevated CO2 and soil drought on growth and transpiration efficiency and its determinants in two European forest tree species. Tree Physiology 14, 707–724.
PubMed |
open url image1

Gunderson CA, Sholtis JD, Wullschleger SD, Tissue DT, Hanson PJ, Norby RJ (2002) Environmental and stomatal control of photosynthetic enhancement in the canopy of a sweetgum (Liquidambar styraciflua L.) plantation during three years of CO2 enrichment. Plant, Cell & Environment 25, 379–393.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hikosaka K (2005) Leaf canopy as a dynamic system: ecophysiology and optimality in leaf turnover. Annals of Botany 95, 521–533.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jarvis PG, McNaughton SJ (1986) Stomatal control of transpiration: scaling up from leaf to region. Advances in Ecological Research 15, 1–49.
Crossref |
open url image1

Kimball BA, Mauney JR (1993) Response of cotton to varying CO2, irrigation, and nitrogen – yield and growth. Agronomy Journal 85, 706–712. open url image1

King DA (1993) A model analysis of the influence of root and foliage allocation on forest production and competition between trees. Tree Physiology 12, 119–135.
PubMed |
open url image1

Lee TD, Tjoelker MG, Ellsworth DS, Reich PB (2001) Leaf gas exchange responses of 13 prairie grassland species to elevated CO2 and increased nitrogen supply. The New Phytologist 150, 405–418.
Crossref | GoogleScholarGoogle Scholar | open url image1

Leuning R, Cleugh HA, Zegelin SJ, Hughes D (2005) Carbon and water fluxes over a temperate Eucalyptus forest and a tropical wet/dry savanna in Australia: measurements and comparison with MODIS remote sensing estimates. Agricultural and Forest Meteorology 129, 151–173.
Crossref | GoogleScholarGoogle Scholar | open url image1

Luo Y, Su B, Currie WS, Dukes JS, Finzi A , et al. (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric CO2. Bioscience 54, 731–739.
Crossref | GoogleScholarGoogle Scholar | open url image1

Luo Y, Hui D, Zhang D (2006) Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology 87, 53–63.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mäkelä A, Valentine HT (2001) The ratio of NPP to GPP: evidence of change over the course of stand development. Tree Physiology 21, 1015–1030.
PubMed |
open url image1

McCarthy HR, Oren R, Finzi AC, Johnsen KH (2006) Canopy leaf area constrains [CO2]-induced enhancement of productivity and partitioning among aboveground carbon pools Proceedings of the National Academy of Sciences of the United States of America 103, 19356–19361.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

McMurtrie RE (1991) Relationship of forest productivity to nutrient and carbon supply – a modelling analysis. Tree Physiology 9, 87–99.
PubMed |
open url image1

McMurtrie RE, Comins HN (1996) The temporal response of forest ecosystems to doubled atmospheric CO2 concentration. Global Change Biology 2, 49–57.
Crossref | GoogleScholarGoogle Scholar | open url image1

McMurtrie RE, Wang Y-P (1993) Mathematical models of the photosynthetic response of tree stands to rising CO2 concentrations and temperatures. Plant, Cell & Environment 16, 1–13.
Crossref | GoogleScholarGoogle Scholar | open url image1

McMurtrie RE, Benson ML, Linder S, Running SW, Talsma T, Crane WJB, Myers BJ (1990) Water/nutrient interactions affecting the productivity of stands of Pinus radiata. Forest Ecology and Management 30, 415–423.
Crossref | GoogleScholarGoogle Scholar | open url image1

Medhurst J, Parsby J, Linder S, Wallin G, Ceschia E, Slaney M (2006) A whole-tree chamber system for examining tree-level physiological responses of field-grown trees to environmental variation and climate change. Plant, Cell & Environment 29, 1853–1869.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Medlyn BE, Badeck FW, De Pury DGG, Barton CVM, Broadmeadow M , et al. (1999) Effects of elevated [CO2] on photosynthesis in European forest species: a meta-analysis of model parameters. Plant, Cell & Environment 22, 1475–1495.
Crossref | GoogleScholarGoogle Scholar | open url image1

Medlyn BE, McMurtrie RE, Dewar RC, Jeffreys MP (2000) Soil processes dominate the long-term response of forest net primary productivity to increased temperature and atmospheric CO2 concentration. Canadian Journal of Forest Research 30, 873–888.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Medlyn BE, Barrett D, Landsberg J, Sands P, Clement R (2003) Conversion of canopy intercepted radiation to photosynthate: review of modelling approaches for regional scales. Functional Plant Biology 30, 153–169.
Crossref | GoogleScholarGoogle Scholar | open url image1

Moore DJP, Aref S, Ho RM, Pippen JS, Hamilton JG, De Lucia EH (2006) Annual basal area increment and growth duration of Pinus taeda in response to eight years of free-air carbon dioxide enrichment. Global Change Biology 12, 1367–1377.
Crossref | GoogleScholarGoogle Scholar | open url image1

Morgan JA, Pataki DE, Körner C, Clark H, Del Grosso SJ , et al. (2004) Water relations in grassland and desert ecosystems exposed to elevated atmospheric CO2. Oecologia 140, 11–25.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Myneni RB, Hoffman S, Knyazikhin Y, Privette JL, Glassy J , et al. (2002) Global products of vegetation leaf area and fraction absorbed PAR from year one of MODIS data. Remote Sensing of Environment 83, 214–231.
Crossref | GoogleScholarGoogle Scholar | open url image1

Norby RJ, Iversen CM (2006) Nitrogen uptake, distribution, turnover, and efficiency of use in a CO2-enriched sweetgum forest. Ecology 87, 5–14.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Norby RJ, Hanson PJ, O’Neill EG, Tschaplinski TJ, Weltzin JF , et al. (2002) Net primary productivity of a CO2-enriched deciduous forest and the implications for carbon storage. Ecological Applications 12, 1261–1266. open url image1

Norby RJ, Sholtis JD, Gunderson CA, Jawdy SS (2003) Leaf dynamics of a deciduous forest canopy: no response to elevated CO2. Oecologia 136, 574–584.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Norby RJ, Ledford J, Reilly CD, Miller NE, O’Neill EG (2004) Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment. Proceedings of the National Academy of Sciences of the United States of America 101, 9689–9693.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Norby RJ, DeLucia EH, Gielen B, Calfapietra C, Giardina CP , et al. (2005) Forest response to elevated CO2 is conserved across a broad range of productivity. Proceedings of the National Academy of Sciences of the United States of America 102, 18052–18056.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Norby RJ , Wullschleger SD , Hanson PJ , Gunderson CA , Tschaplinski TJ , Jastrow JD (2006) CO2 enrichment of a deciduous forest: the Oak Ridge FACE experiment. In ‘Managed ecosystems and CO2: case studies, processes and perspectives’. (Eds J Nösberger, SP Long, RJ Norby, M Stitt, GR Hendrey, H Blum) Ecological Studies Vol. 187. pp. 231–251. (Springer-Verlag, Berlin, Heidelberg)

Nowak RS, Ellsworth DS, Smith SD (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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Oren R, Ellsworth DS, Johnson KH, Phillips N, Ewers BE , et al. (2001) Soil fertility limits carbon sequestration by a forest ecosystem in a CO2-enriched atmosphere. Nature 411, 469–472.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pepper DA, Del Grosso SJ, McMurtrie RE, Parton WJ (2005) Simulated carbon sink response of shortgrass steppe, tallgrass prairie and forest ecosystems to rising [CO2], temperature and nitrogen input. Global Biogeochemical Cycles 19, GB1004.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pepper DA, Eliasson PE, McMurtrie RE, Corbeels M, Ågren GI, Strömgren M, Linder S (2007) Simulated mechanisms of soil N feedback on the forest CO2 response. Global Change Biology 13, 1265–1281.
Crossref | GoogleScholarGoogle Scholar | open url image1

Potter CS, Randerson JT, Field CB, Matson PA, Vitousek PM, Mooney HA, Klooster SA (1993) Terrestrial ecosystem production: a process model based on global satellite and surface data. Global Biogeochemical Cycles 7, 811–841.
Crossref | GoogleScholarGoogle Scholar | open url image1

Reich PB, Ellsworth DS, Walters MB, Vose JM, Gresham C, Volin JC, Bowman WD (1999) Generality of leaf trait relationships: a test across six biomes. Ecology 80, 1955–1969. open url image1

Reich PB, Hobbie SE, Lee T, Ellsworth DS, West JB, Tilman D, Knops JMH, Naeem S, Trost J (2006a) Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440, 922–925.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Reich PB, Hungate BA, Luo Y (2006b) Carbon–nitrogen interactions in terrestrial ecosystems in response to rising atmospheric carbon dioxide. Annual Review of Ecology Evolution and Systematics 37, 611–636.
Crossref | GoogleScholarGoogle Scholar | open url image1

Reich PB, Tjoelker J-L, Machado J-L, Oleksyn J (2006c) Universal scaling of respiratory metabolism, size and nitrogen in plants. Nature 439, 457–461.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ruimy A, Saugier B, Dedieu G (1994) Methodology for the estimation of terrestrial net primary production from remotely sensed data. Journal of Geophysical Research D3 99, 5263–5283.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ryan MG (1991) Effect of climate change on plant respiration. Ecological Applications 1, 157–167.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sands PJ (1995) Modelling canopy production. II. From single-leaf photosynthetic parameters to daily canopy photosynthesis. Australian Journal of Plant Physiology 22, 603–614. open url image1

Sands PJ (1996) Modelling canopy production. III. Canopy light-utilisation efficiency and its sensitivity to physiological environmental variables. Australian Journal of Plant Physiology 23, 103–114. open url image1

Schieving F, Poorter H (1999) Carbon gain in a multispecies canopy: the role of specific leaf area and photosynthetic nitrogen-use efficiency in the tragedy of the commons. The New Phytologist 143, 201–211.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schneider MK, Lüscher A, Richter M, Aeschlimann U, Hartwig UA, Blum H, Frossard E, Nösberger J (2004) Ten years of free-air CO2 enrichment altered the mobilization of N from soil in Lolium perenne L. swards. Global Change Biology 10, 1377–1388.
Crossref | GoogleScholarGoogle Scholar | open url image1

Shaw MR , Huxman TE , Lund CP (2005) Modern and future semi-arid and arid ecosystems. In ‘History of atmospheric CO2 and its effects on plants, animals, and ecosystems’. (Eds JR Ehleringer, TE Cerling, MD Dearing) Ecological Studies Vol. 177. pp. 415–440. (Springer-Verlag: New York)

Sholtis DJ, Gunderson CA, Norby RJ, Tissue DT (2004) Persistent stimulation of photosynthesis by elevated CO2 in a sweetgum (Liquidambar styraciflua) forest stand. The New Phytologist 162, 343–354.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tissue DT, Lewis JD, Wullschleger SD, Amthor JS, Griffin KL, Anderson OR (2002) Leaf respiration at different canopy positions in sweetgum (Liquidambar styraciflua) grown in ambient and elevated concentrations of carbon dioxide in the field. Tree Physiology 22, 1157–1166.
PubMed |
open url image1

Wand S, Midgeley G, Jones M, Curtis PS (1999) Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a meta-analytic test of current theories and perceptions. Global Change Biology 5, 723–741.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wright IJ, Reich PB, Westoby M (2003) Least-cost input mixtures of water and nitrogen for photosynthesis. American Naturalist 161, 98–111.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wullschleger SD, Norby RJ (2001) Sap velocity and canopy transpiration in a sweetgum stand exposed to free-air CO2 enrichment (FACE). The New Phytologist 150, 489–498.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wullschleger SD, Tschaplinski TJ, Norby RJ (2002) Plant water relations at elevated CO2 – implications for water-limited environments. Plant, Cell & Environment 25, 319–331.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zak D, Pregitzer K, King J, Holmes W (2000) Elevated atmospheric CO2, fine roots and the response of soil microorganisms: a review and hypothesis. The New Phytologist 147, 201–222.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zak DR, Holmes WE, Finzi AC, Norby RJ, Schlesinger WH (2003) Soil nitrogen cycling under elevated CO2: a synthesis of forest FACE experiments. Ecological Applications 13, 1508–1514.
Crossref | GoogleScholarGoogle Scholar | open url image1