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

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].

[1]  P. Eliasson,et al.  Simulated mechanisms of soil N feedback on the forest CO2 response , 2007 .

[2]  O. Franklin.  Optimal nitrogen allocation controls tree responses to elevated CO2. , 2007, New Phytologist.

[3]  Evan H. DeLucia,et al.  Forest carbon use efficiency: is respiration a constant fraction of gross primary production? , 2007 .

[4]  A. Rogers,et al.  The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. , 2007, Plant, cell & environment.

[5]  J. O H N,et al.  Forest carbon use efficiency : is respiration a constant fraction of gross primary production ? , 2007 .

[6]  R. Oren,et al.  Canopy leaf area constrains [CO2]-induced enhancement of productivity and partitioning among aboveground carbon pools , 2006, Proceedings of the National Academy of Sciences.

[7]  Jane A. Catford,et al.  Ecohydrology: Vegetation Function, Water and Resource Management , 2006 .

[8]  P. Reich,et al.  Carbon-Nitrogen Interactions in Terrestrial Ecosystems in Response to Rising Atmospheric Carbon Dioxide , 2006 .

[9]  Johan Six,et al.  Interactions between plant growth and soil nutrient cycling under elevated CO2: a meta‐analysis , 2006 .

[10]  E. Ceschia,et al.  A whole-tree chamber system for examining tree-level physiological responses of field-grown trees to environmental variation and climate change. , 2006, Plant, cell & environment.

[11]  P. Reich,et al.  Nitrogen limitation constrains sustainability of ecosystem response to CO2 , 2006, Nature.

[12]  Mark G. Tjoelker,et al.  Universal scaling of respiratory metabolism, size and nitrogen in plants , 2006, Nature.

[13]  E. Va,et al.  Annual basal area increment and growth duration of Pinus taeda in response to eight years of free-air carbon dioxide enrichment , 2006 .

[14]  M. Stitt,et al.  Managed Ecosystems and CO2 : Case Studies, Processes and Perspectives , 2006 .

[15]  R. Norby,et al.  Nitrogen uptake, distribution, turnover, and efficiency of use in a CO2-enriched sweetgum forest. , 2006, Ecology.

[16]  T. Tschaplinski,et al.  CO2 Enrichment of a Deciduous Forest: The Oak Ridge FACE Experiment , 2006 .

[17]  Yiqi Luo,et al.  Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. , 2006, Ecology.

[18]  R. Ceulemans,et al.  Forest response to elevated CO2 is conserved across a broad range of productivity. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[19]  David Joseph Moore,et al.  Contrasting responses of forest ecosystems to rising atmospheric CO2: Implications for the global C cycle , 2005 .

[20]  R. Leuning,et al.  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 , 2005 .

[21]  William J. Parton,et al.  Simulated carbon sink response of shortgrass steppe, tallgrass prairie and forest ecosystems to rising [CO2], temperature and nitrogen input , 2005 .

[22]  K. Hikosaka,et al.  Leaf canopy as a dynamic system: ecophysiology and optimality in leaf turnover. , 2004, Annals of botany.

[23]  N. Anten.  Optimal photosynthetic characteristics of individual plants in vegetation stands and implications for species coexistence. , 2004, Annals of botany.

[24]  S. Long,et al.  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. , 2004, The New phytologist.

[25]  M. Shaw,et al.  Modern and Future Semi-Arid and Arid Ecosystems , 2005 .

[26]  Robert B. Jackson,et al.  A history of atmospheric CO[2] and its effects on plants, animals, and ecosystems , 2005 .

[27]  P. Reich,et al.  Photosynthesis, carboxylation and leaf nitrogen responses of 16 species to elevated pCO2 across four free‐air CO2 enrichment experiments in forest, grassland and desert , 2004 .

[28]  Herbert Blum,et al.  Ten years of free‐air CO2 enrichment altered the mobilization of N from soil in Lolium perenne L. swards , 2004 .

[29]  W. Parton,et al.  Progressive Nitrogen Limitation of Ecosystem Responses to Rising Atmospheric Carbon Dioxide , 2004 .

[30]  N. E. Miller,et al.  Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[31]  M. R. Shaw,et al.  Water relations in grassland and desert ecosystems exposed to elevated atmospheric CO2 , 2004, Oecologia.

[32]  R. Norby,et al.  Persistent stimulation of photosynthesis by elevated CO2 in a sweetgum (Liquidambar styraciflua) forest stand , 2004 .

[33]  D. Ellsworth,et al.  Functional responses of plants to elevated atmospheric CO2– do photosynthetic and productivity data from FACE experiments support early predictions? , 2004 .

[34]  J. Soussana,et al.  Atmospheric CO2 elevation has little effect on nitrifying and denitrifying enzyme activity in four European grasslands , 2004 .

[35]  S. Long,et al.  Review Tansley Review , 2022 .

[36]  R. Norby,et al.  Soil nitrogen cycling under elevated CO2: A synthesis of forest face experiments , 2003 .

[37]  R. Norby,et al.  Leaf dynamics of a deciduous forest canopy: no response to elevated CO2 , 2003, Oecologia.

[38]  P. Pinter,et al.  Above‐ and below‐ground responses of C3–C4 species mixtures to elevated CO2 and soil water availability , 2003 .

[39]  Damian Barrett,et al.  Conversion of canopy intercepted radiation to photosynthate: review of modelling approaches for regional scales. , 2003, Functional plant biology : FPB.

[40]  P. Reich,et al.  Least‐Cost Input Mixtures of Water and Nitrogen for Photosynthesis , 2002, The American Naturalist.

[41]  G. Ågren,et al.  Leaf senescence and resorption as mechanisms of maximizing photosynthetic production during canopy development at N limitation , 2002 .

[42]  S. Wullschleger,et al.  Leaf respiration at different canopy positions in sweetgum (Liquidambar styraciflua) grown in ambient and elevated concentrations of carbon dioxide in the field. , 2002, Tree physiology.

[43]  S. Running,et al.  Global products of vegetation leaf area and fraction absorbed PAR from year one of MODIS data , 2002 .

[44]  Stan D. Wullschleger,et al.  Net primary productivity of a CO2-enriched deciduous forest and the implications for carbon storage , 2002 .

[45]  N. Anten.  Evolutionarily stable leaf area production in plant populations. , 2002, Journal of theoretical biology.

[46]  R. B. Jackson,et al.  Nonlinear grassland responses to past and future atmospheric CO2 , 2002, Nature.

[47]  R. Norby,et al.  Environmental and stomatal control of photosynthetic enhancement in the canopy of a sweetgum (Liquidambar styraciflua L.) plantation during 3 years of CO2 enrichment , 2002 .

[48]  T. Tschaplinski,et al.  Plant water relations at elevated CO2 -- implications for water-limited environments. , 2002, Plant, cell & environment.

[49]  MICHAEL B. Jones,et al.  Effects of Elevated Co₂ and Nitrogen Fertiliser on Biomass Productivity, Community Structure and Species Diversity of a Semi-Natural Grassland in Ireland , 2022, Biology and Environment: Proceedings of the Royal Irish Academy.

[50]  G. Farquhar,et al.  Optimal stomatal control in relation to leaf area and nitrogen content , 2002 .

[51]  A. Mäkelä,et al.  The ratio of NPP to GPP: evidence of change over the course of stand development. , 2001, Tree physiology.

[52]  G. Katul,et al.  Soil fertility limits carbon sequestration by forest ecosystems in a CO2-enriched atmosphere , 2001, Nature.

[53]  R. Norby,et al.  Sap velocity and canopy transpiration in a sweetgum stand exposed to free‐air CO2 enrichment (FACE) , 2001 .

[54]  P. Reich,et al.  Leaf gas exchange responses of 13 prairie grassland species to elevated CO2 and increased nitrogen supply , 2001 .

[55]  R. Ceulemans,et al.  Stomatal conductance of forest species after long-term exposure to elevated CO2 concentration: a synthesis. , 2001, The New phytologist.

[56]  K. Pregitzer,et al.  Elevated atmospheric CO2, fine roots and the response of soil microorganisms: a review and hypothesis , 2000 .

[57]  R. Dewar,et al.  Soil processes dominate the long-term response of forest net primary productivity to increased temperature and atmospheric CO2 concentration. , 2000 .

[58]  P. De Angelis,et al.  Effects of elevated (CO2) on photosynthesis in European forest species: a meta-analysis of model parameters , 1999 .

[59]  P. Reich,et al.  Generality of leaf trait relationships: a test across six biomes: Ecology , 1999 .

[60]  S. Wand,et al.  Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a meta‐analytic test of current theories and perceptions , 1999 .

[61]  F. Schieving,et al.  Carbon gain in a multispecies canopy: the role of specific leaf area and photosynthetic nitrogen‐use efficiency in the tragedy of the commons , 1999 .

[62]  Roderick C. Dewar,et al.  Acclimation of the respiration/photosynthesis ratio to temperature: insights from a model , 1999 .

[63]  D. Ackerly,et al.  Self-shading, Carbon Gain and Leaf Dynamics: a Test of Alternative Optimality Models , 1998 .

[64]  P. Jarvis,et al.  Interactive effects of elevated [CO2] and drought on cherry (Prunus avium) seedlings I. Growth, whole‐plant water use efficiency and water loss , 1999 .

[65]  B. Hungate.  Ecosystem Responses to Rising Atmospheric CO2 , 1999 .

[66]  Roderick C. Dewar,et al.  A mechanistic analysis of light and carbon use efficiencies , 1998 .

[67]  F. Berendse,et al.  Interactions between elevated CO2 concentration, nitrogen and water: effects on growth and water use of six perennial plant species , 1998 .

[68]  Peter S. Curtis,et al.  A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology , 1998, Oecologia.

[69]  C. Field,et al.  CO2 effects on the water budget of grassland microcosm communities , 1997 .

[70]  K. Boote,et al.  Rice responses to drought under carbon dioxide enrichment. 2. Photosynthesis and evapotranspiration , 1997 .

[71]  Ross E. McMurtrie,et al.  The temporal response of forest ecosystems to doubled atmospheric CO2 concentration , 1996 .

[72]  F. Chapin,et al.  8 – The Jasper Ridge CO2 Experiment: Design and Motivation , 1996 .

[73]  P. Sands.  Modelling Canopy Production. III. Canopy Light-Utilisation Efficiency and Its Sensitivity to Physiological and Environmental Variables , 1996 .

[74]  Roderick C. Dewar,et al.  Sustainable stemwood yield in relation to the nitrogen balance of forest plantations: a model analysis. , 1996, Tree physiology.

[75]  M. Werger,et al.  Optimal leaf area indices in C3 and C4 mono‐ and dicotyledonous species at low and high nitrogen availability , 1995 .

[76]  Christopher B. Field,et al.  Stomatal responses to increased CO2: implications from the plant to the global scale , 1995 .

[77]  P. Sands.  Modelling Canopy Production. II. From Single-Leaf Photosynthesis Parameters to Daily Canopy Photosynthesis , 1995 .

[78]  P. Gross,et al.  Interactive effects of elevated CO(2) and soil drought on growth and transpiration efficiency and its determinants in two European forest tree species. , 1994, Tree physiology.

[79]  Gérard Dedieu,et al.  Methodology for the estimation of terrestrial net primary production from remotely sensed data , 1994 .

[80]  J. Randerson,et al.  Terrestrial ecosystem production: A process model based on global satellite and surface data , 1993 .

[81]  R. McMurtrie,et al.  Long-Term Response of Nutrient-Limited Forests to CO"2 Enrichment; Equilibrium Behavior of Plant-Soil Models. , 1993, Ecological applications : a publication of the Ecological Society of America.

[82]  J. P. Grime,et al.  Evidence of a feedback mechanism limiting plant response to elevated carbon dioxide , 1993, Nature.

[83]  B. Kimball,et al.  Response of Cotton to Varying COz, Irrigation, and Nitrogen: Yield and Growth , 1993 .

[84]  D. A. King.  A model analysis of the influence of root and foliage allocation on forest production and competition between trees. , 1993, Tree physiology.

[85]  Ross E. McMurtrie,et al.  Mathematical models of the photosynthetic response of tree stands to rising CO2 concentrations and temperatures , 1993 .

[86]  R. McMurtrie.  Relationship of forest productivity to nutrient and carbon supply-a modeling analysis. , 1991, Tree physiology.

[87]  M. G. Ryan,et al.  Effects of Climate Change on Plant Respiration. , 1991, Ecological applications : a publication of the Ecological Society of America.

[88]  Steven W. Running,et al.  Water/Nutrient Interactions Affecting the Productivity of Stands of Pinus radiata , 1990 .

[89]  K. G. McNaughton,et al.  Stomatal Control of Transpiration: Scaling Up from Leaf to Region , 1986 .

[90]  Graham D. Farquhar,et al.  Modelling of Photosynthetic Response to Environmental Conditions , 1982 .

[91]  Donald,et al.  NITROGEN CYCLING UNDER ELEVATED CO 2 : A SYNTHESIS OF FOREST FACE EXPERIMENTS , 2022 .

[92]  P. Xavier,et al.  Interactions between plant growth and soil nutrient cycling under elevated CO 2 : a meta-analysis , 2022 .