A trait-based ecosystem model suggests that long-term responsiveness to rising atmospheric CO2 concentration is greater in slow-growing than fast-growing plants

Summary 1. Atmospheric carbon dioxide concentration (Ca) has a direct and measurable effect on plant growth. However, it does not affect all plant species equally, which could lead to shifts in competitive dominance of species in ecosystems. 2. We used a dynamic plant carbon–nitrogen model to systematically examine how species traits affect the long-term Ca responsiveness of C3 plants when growing as established monocultures in the field. The model was tested against responses of 7 C3 herbaceous species growing in a free-air Ca enrichment (FACE) experiment (BioCON) in Minnesota, USA. 3. Model simulations showed that several species traits affected the Ca response strongly, giving rise to a number of testable hypotheses about interspecific differences in responsiveness to Ca. The largest responses to rising Ca were obtained for species with low carbon-use efficiency (net primary production: gross primary production ratio), low foliar carbon allocation, low stomatal conductance, low instantaneous photosynthetic nitrogen use efficiency and low specific leaf area. 4. In general, our model predicted that, for established plants growing in resource-limited field conditions, species with slow growth rates would be most responsive to elevated Ca. This prediction was supported by data from the BioCON experiment. 5. Our model also predicts that, for young plants growing in non-resource-limited conditions, species with high growth rates will be most responsive to elevated Ca. This difference in species ranking under different resource availabilities is largely explained by the indirect effects of Ca on leaf area. Leaf-area feedbacks favour fast-growing species the most during leaf-area expansion, but following stand maturation they favour slow-growing species the most. 6. These results imply that species that respond strongly to elevated Ca in short-term (nonresource-limited) glasshouse experiments are unlikely to also be the most responsive in resource-limited field conditions, and therefore that we cannot directly extrapolate from glasshouse experiments to predict which species will be most responsive to elevated Ca in the long term.

[1]  H. Jones.  Plants and Microclimate: Other environmental factors: wind, altitude, climate change and atmospheric pollutants , 2013 .

[2]  P. E T E,et al.  Photosynthetic responses of 13 grassland species across 11 years of free-air CO 2 enrichment is modest , consistent and independent of N supply , 2012 .

[3]  P. Reich,et al.  Photosynthetic responses of 13 grassland species across 11 years of free‐air CO2 enrichment is modest, consistent and independent of N supply , 2011 .

[4]  Paolo De Angelis,et al.  Reconciling the optimal and empirical approaches to modelling stomatal conductance , 2011 .

[5]  J. Peñuelas,et al.  Evergreens favored by higher responsiveness to increased CO₂. , 2011, Trends in ecology & evolution.

[6]  C. F. Stange,et al.  Species‐specific differences in nitrogen uptake and utilization by six European tree species , 2011 .

[7]  M. Kirschbaum,et al.  Does Enhanced Photosynthesis Enhance Growth? Lessons Learned from CO2 Enrichment Studies[W] , 2010, Plant Physiology.

[8]  P. Reich,et al.  Maintenance of leaf N controls the photosynthetic CO2 response of grassland species exposed to 9 years of free‐air CO2 enrichment , 2010 .

[9]  A. Rogers,et al.  Will Elevated Carbon Dioxide Concentration Amplify the Benefits of Nitrogen Fixation in Legumes?1 , 2009, Plant Physiology.

[10]  D. DeAngelis,et al.  The R* rule and energy flux in a plant-nutrient ecosystem. , 2009, Journal of theoretical biology.

[11]  Peter B Reich,et al.  Why is plant-growth response to elevated CO2 amplified when water is limiting, but reduced when nitrogen is limiting? A growth-optimisation hypothesis. , 2008, Functional plant biology : FPB.

[12]  Peter B Reich,et al.  Scaling of respiration to nitrogen in leaves, stems and roots of higher land plants. , 2008, Ecology letters.

[13]  K. Crous.  Nitrogen Availability Alters Species Photosynthetic Responses to Elevated Atmospheric CO2. , 2008 .

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

[15]  M. I C H A E,et al.  Carbon allocation in forest ecosystems , 2007 .

[16]  S. Hart,et al.  Nutrient covariance between forest foliage and fine roots , 2006 .

[17]  C. Körner.  Plant CO2 responses: an issue of definition, time and resource supply. , 2006, The New phytologist.

[18]  W. Post,et al.  Plant Respiration in a Warmer World , 2006, Science.

[19]  P. Reich,et al.  Linking leaf and root trait syndromes among 39 grassland and savannah species. , 2005, The New phytologist.

[20]  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.

[21]  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 .

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

[23]  A. Rogers,et al.  Rising atmospheric carbon dioxide: plants FACE the future. , 2004, Annual review of plant biology.

[24]  Sean C. Thomas,et al.  The worldwide leaf economics spectrum , 2004, Nature.

[25]  R. T. Belote,et al.  Response of an understory plant community to elevated [CO2 ] depends on differential responses of dominant invasive species and is mediated by soil water availability. , 2004, The New phytologist.

[26]  Hendrik Poorter.  Interspecific variation in the growth response of plants to an elevated ambient CO2 concentration , 2004, Vegetatio.

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

[28]  S. Ta.  Photosynthesis , carboxylation and leaf nitrogen responses of 16 species to elevated pCO 2 across four free-air CO 2 enrichment experiments in forest , grassland and desert , 2004 .

[29]  M. Navas,et al.  Plant growth and competition at elevated CO2 : on winners, losers and functional groups. , 2003, The New phytologist.

[30]  Denis Loustau,et al.  Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data , 2002 .

[31]  B. Medlyn,et al.  Temperature response of parameters of a biochemically based model of photosynthesis. I. Seasonal changes in mature maritime pine (Pinus pinaster Ait.) , 2002 .

[32]  Michael L. Roderick,et al.  Estimating mixtures of leaf functional types using continental-scale satellite and climatic data , 2002 .

[33]  P. Reich,et al.  FIRE AND VEGETATION EFFECTS ON PRODUCTIVITY AND NITROGEN CYCLING ACROSS A FOREST-GRASSLAND CONTINUUM , 2001 .

[34]  P. Reich,et al.  Do species and functional groups differ in acquisition and use of C, N and water under varying atmospheric CO2 and N availability regimes? : a field test with 16 grassland species , 2001 .

[35]  P. Reich,et al.  [Letters to nature] , 1975, Nature.

[36]  F. Chapin,et al.  Species‐specific responses of plant communities to altered carbon and nutrient availability , 2001 .

[37]  H. Bassirirad,et al.  Interspecies variation in nitrogen uptake kinetic responses of temperate forest species to elevated CO2: potential causes and consequences , 2001 .

[38]  John R. Evans,et al.  The response of fast- and slow-growing Acacia species to elevated atmospheric CO2: an analysis of the underlying components of relative growth rate , 1999, Oecologia.

[39]  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 .

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

[41]  P. Reich,et al.  Temperature and ontogeny mediate growth response to elevated CO2 in seedlings of five boreal tree species. , 1998, The New phytologist.

[42]  H. Poorter.  Do slow‐growing species and nutrient‐stressed plants respond relatively strongly to elevated CO2? , 1998 .

[43]  D. Ellsworth,et al.  Tree and forest functioning in an enriched CO2 atmosphere , 1998 .

[44]  P. Reich,et al.  Photosynthesis and respiration rates depend on leaf and root morphology and nitrogen concentration in nine boreal tree species differing in relative growth rate , 1998 .

[45]  M. Williams,et al.  Net primary production of forests: a constant fraction of gross primary production? , 1998, Tree physiology.

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

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

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

[49]  Gretchen Stockmayer.  Carbon dioxide, populations, and communities , 1997 .

[50]  J. Roy,et al.  Growth response of grasses to elevated CO2: a physiological plurispecific analysis , 1996 .

[51]  Christian Körner,et al.  Carbon Dioxide, Populations, and Communities , 1996 .

[52]  G. Farquhar,et al.  The CO 2 Dependence of Photosynthesis, Plant Growth Responses to Elevated Atmospheric CO 2 Concentrations and Their Interaction with Soil Nutrient Status. I. General Principles and Forest Ecosystems , 1996 .

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

[54]  Roderick Hunt,et al.  Further responses to CO2 enrichment in British herbaceous species. , 1993 .

[55]  M. Badger,et al.  Effects of Ambient CO2 Concentration on Growth and Nitrogen Use in Tobacco (Nicotiana tabacum) Plants Transformed with an Antisense Gene to the Small Subunit of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase , 1993, Plant physiology.

[56]  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.

[57]  Xiusheng Yang.  Plants and Microclimate: A Quantitative Approach to Environmental Plant Physiology: Hamlyn G. Jones, 2nd edn., 1992, Cambridge University Press, Cambridge, 428 pp., hardcover, £55.00, ISBN 0-521-41502-0; paperback, £19.95, ISBN 0-521-42524-7 , 1993 .

[58]  Stan D. Wullschleger,et al.  Biochemical Limitations to Carbon Assimilation in C3 Plants—A Retrospective Analysis of the A/Ci Curves from 109 Species , 1993 .

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

[60]  W. Thompson,et al.  Photosynthetic Response to Light and Nutrients in Sun-Tolerant and Shade-Tolerant Rainforest Trees. II. Leaf Gas Exchange and Component Processes of Photosynthesis , 1992 .

[61]  M. Stitt.  Rising Co2 Levels and Their Potential Significance for Carbon Flow in Photosynthetic Cells , 1991 .

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

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

[64]  F. Bazzaz.  The Physiological Ecology of Plant Succession , 1979 .

[65]  K. Abromeit.  Music Received , 2023, Notes.