Does the growth response of woody plants to elevated CO2 increase with temperature? A model‐oriented meta‐analysis

The temperature dependence of the reaction kinetics of the Rubisco enzyme implies that, at the level of a chloroplast, the response of photosynthesis to rising atmospheric CO2 concentration (Ca) will increase with increasing air temperature. Vegetation models incorporating this interaction predict that the response of net primary productivity (NPP) to elevated CO2 (eCa) will increase with rising temperature and will be substantially larger in warm tropical forests than in cold boreal forests. We tested these model predictions against evidence from eCa experiments by carrying out two meta‐analyses. Firstly, we tested for an interaction effect on growth responses in factorial eCa × temperature experiments. This analysis showed a positive, but nonsignificant interaction effect (95% CI for above‐ground biomass response = −0.8, 18.0%) between eCa and temperature. Secondly, we tested field‐based eCa experiments on woody plants across the globe for a relationship between the eCa effect on plant biomass and mean annual temperature (MAT). This second analysis showed a positive but nonsignificant correlation between the eCa response and MAT. The magnitude of the interactions between CO2 and temperature found in both meta‐analyses were consistent with model predictions, even though both analyses gave nonsignificant results. Thus, we conclude that it is not possible to distinguish between the competing hypotheses of no interaction vs. an interaction based on Rubisco kinetics from the available experimental database. Experiments in a wider range of temperature zones are required. Until such experimental data are available, model predictions should aim to incorporate uncertainty about this interaction.

[1]  Atul K. Jain,et al.  Global Carbon Budget 2015 , 2015 .

[2]  P. Jones,et al.  Updated high‐resolution grids of monthly climatic observations – the CRU TS3.10 Dataset , 2014 .

[3]  P. Lasch-Born,et al.  Projections of regional changes in forest net primary productivity for different tree species in Europe driven by climate change and carbon dioxide , 2014, Annals of Forest Science.

[4]  S. Kellomäki,et al.  Combination treatment of elevated UVB radiation, CO2 and temperature has little effect on silver birch (Betula pendula) growth and phytochemistry. , 2013, Physiologia plantarum.

[5]  Benjamin Smith,et al.  Implications of incorporating N cycling and N limitations on primary production in an individual-based dynamic vegetation model , 2013 .

[6]  F. Hagedorn,et al.  Central European hardwood trees in a high‐CO2 future: synthesis of an 8‐year forest canopy CO2 enrichment project , 2013 .

[7]  S. Linder,et al.  Growth of mature boreal Norway spruce was not affected by elevated [CO(2)] and/or air temperature unless nutrient availability was improved. , 2013, Tree physiology.

[8]  B. Hungate,et al.  The effects of 11 yr of CO₂ enrichment on roots in a Florida scrub-oak ecosystem. , 2013, The New phytologist.

[9]  T. Koike,et al.  Elevated CO2 enhances the growth of hybrid larch F1 (Larix gmelinii var. japonica × L. kaempferi) seedlings and changes its biomass allocation , 2013, Trees.

[10]  T. Koike,et al.  Elevated CO2 enhances the growth of hybrid larch F1 (Larix gmelinii var. japonica × L. kaempferi) seedlings and changes its biomass allocation , 2013, Trees.

[11]  B. Choat,et al.  Carbon dynamics of eucalypt seedlings exposed to progressive drought in elevated [CO2] and elevated temperature. , 2013, Tree physiology.

[12]  S. Fatichi,et al.  Reconciling observations with modeling: The fate of water and carbon allocation in a mature deciduous forest exposed to elevated CO2 , 2013 .

[13]  B. Logan,et al.  Industrial-age changes in atmospheric [CO2] and temperature differentially alter responses of faster- and slower-growing Eucalyptus seedlings to short-term drought. , 2013, Tree physiology.

[14]  Andrew R. Smith,et al.  Elevated CO2 enrichment induces a differential biomass response in a mixed species temperate forest plantation. , 2013, The New phytologist.

[15]  K. Steppe,et al.  The effect of heat waves, elevated [CO2] and low soil water availability on northern red oak (Quercus rubra L.) seedlings , 2013, Global change biology.

[16]  C. Körner Growth controls photosynthesis - mostly , 2013 .

[17]  F. Dijkstra,et al.  Simple additive effects are rare: a quantitative review of plant biomass and soil process responses to combined manipulations of CO2 and temperature , 2012, Global change biology.

[18]  David T. Tissue,et al.  Effects of elevated atmospheric [CO2] on instantaneous transpiration efficiency at leaf and canopy scales in Eucalyptus saligna , 2012 .

[19]  S. Heckathorn,et al.  A meta-analysis of plant physiological and growth responses to temperature and elevated CO2 , 2012, Oecologia.

[20]  Marc J. Lajeunesse,et al.  On the meta-analysis of response ratios for studies with correlated and multi-group designs. , 2011 .

[21]  Philippe Ciais,et al.  Carbon benefits of anthropogenic reactive nitrogen offset by nitrous oxide emissions , 2011 .

[22]  P. Cox,et al.  The Joint UK Land Environment Simulator (JULES), model description – Part 2: Carbon fluxes and vegetation dynamics , 2011 .

[23]  P. Cox,et al.  The Joint UK Land Environment Simulator (JULES), model description – Part 1: Energy and water fluxes , 2011 .

[24]  B. Medlyn,et al.  Forest productivity under climate change: a checklist for evaluating model studies , 2011 .

[25]  Marc J Lajeunessei On the meta-analysis of response ratios for studies with correlated and multi-group designs. , 2011, Ecology.

[26]  Christian Körner,et al.  Species‐specific tree growth responses to 9 years of CO2 enrichment at the alpine treeline , 2010 .

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

[28]  Wolfgang Viechtbauer,et al.  Conducting Meta-Analyses in R with the metafor Package , 2010 .

[29]  M. Ball,et al.  Disturbance is required for CO2-dependent promotion of woody plant growth in grasslands , 2010 .

[30]  A. Friend,et al.  Terrestrial plant production and climate change. , 2010, Journal of experimental botany.

[31]  Andrew D. Friend,et al.  Carbon and nitrogen cycle dynamics in the O‐CN land surface model: 1. Model description, site‐scale evaluation, and sensitivity to parameter estimates , 2010 .

[32]  Pierre Friedlingstein,et al.  Carbon and nitrogen cycle dynamics in the O‐CN land surface model: 2. Role of the nitrogen cycle in the historical terrestrial carbon balance , 2010 .

[33]  B. Logan,et al.  Exposure to preindustrial, current and future atmospheric CO2 and temperature differentially affects growth and photosynthesis in Eucalyptus , 2010 .

[34]  R. McMurtrie,et al.  CO2 enhancement of forest productivity constrained by limited nitrogen availability , 2009, Proceedings of the National Academy of Sciences.

[35]  K. Wang,et al.  EFFECTS OF ELEVATED CO2 AND TEMPERATURE ON GROWTH AND MORPHOLOGY OF FIR (ABIES FAXONIANA REHD. ET WILS.) AND NATIVE HERBS IN A TREELINE ECOTONE: AN EXPERIMENTAL APPROACH , 2010 .

[36]  A. S. Raghavendra,et al.  The impact of global elevated CO2 concentration on photosynthesis and plant productivity , 2010 .

[37]  Charles W. Cook,et al.  Re-assessment of plant carbon dynamics at the Duke free-air CO(2) enrichment site: interactions of atmospheric [CO(2)] with nitrogen and water availability over stand development. , 2010, The New phytologist.

[38]  Martijn Gough Climate change , 2009, Canadian Medical Association Journal.

[39]  S. Linder,et al.  Stem wood properties of mature Norway spruce after 3 years of continuous exposure to elevated [CO2] and temperature , 2009 .

[40]  I. C. Prentice,et al.  Evaluation of the terrestrial carbon cycle, future plant geography and climate‐carbon cycle feedbacks using five Dynamic Global Vegetation Models (DGVMs) , 2008 .

[41]  Benjamin Smith,et al.  CO2 fertilization in temperate FACE experiments not representative of boreal and tropical forests , 2008 .

[42]  J. Canadell,et al.  Managing Forests for Climate Change Mitigation , 2008, Science.

[43]  F. Miglietta,et al.  Future atmospheric CO2 leads to delayed autumnal senescence , 2007 .

[44]  S. Idso,et al.  Seventeen years of carbon dioxide enrichment of sour orange trees: final results , 2007 .

[45]  D. Overdieck,et al.  Temperature responses of growth and wood anatomy in European beech saplings grown in different carbon dioxide concentrations. , 2007, Tree physiology.

[46]  M. G. Ryan,et al.  The likely impact of elevated [CO2], nitrogen deposition, increased temperature and management on carbon sequestration in temperate and boreal forest ecosystems: a literature review. , 2007, The New phytologist.

[47]  T. Wilbanks,et al.  Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change , 2007 .

[48]  Hans W. Linderholm,et al.  Growing season changes in the last century , 2006 .

[49]  M. Ball,et al.  CO2 enrichment predisposes foliage of a eucalypt to freezing injury and reduces spring growth , 2005 .

[50]  E. P. McDonald,et al.  Tropospheric O3 compromises net primary production in young stands of trembling aspen, paper birch and sugar maple in response to elevated atmospheric CO2 , 2005 .

[51]  T. Barnett,et al.  Potential impacts of a warming climate on water availability in snow-dominated regions , 2005, Nature.

[52]  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 .

[53]  R. Ceulemans,et al.  Carbon budget of Pinus sylvestris saplings after four years of exposure to elevated atmospheric carbon dioxide concentration. , 2005, Tree physiology.

[54]  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.

[55]  E. P. McDonald,et al.  Tropospheric O(3) compromises net primary production in young stands of trembling aspen, paper birch and sugar maple in response to elevated atmospheric CO(2). , 2005, The New phytologist.

[56]  J. Riikonen,et al.  Silver birch and climate change: variable growth and carbon allocation responses to elevated concentrations of carbon dioxide and ozone. , 2004, Tree physiology.

[57]  R. Norby,et al.  CO2 enrichment and warming of the atmosphere enhance both productivity and mortality of maple tree fine roots , 2004 .

[58]  R. Norby,et al.  Evaluating ecosystem responses to rising atmospheric CO2 and global warming in a multi‐factor world , 2004 .

[59]  R. Norby,et al.  Nitrogen resorption in senescing tree leaves in a warmer, CO2-enriched atmosephere , 2000, Plant and Soil.

[60]  R. Qualls,et al.  Effects of increased atmospheric CO2, temperature, and soil N availability on root exudation of dissolved organic carbon by a N-fixing tree (Robinia pseudoacacia L.) , 2000, Plant and Soil.

[61]  P. Curtis,et al.  Growth and nitrogen accretion of dinitrogen-fixing Alnus glutinosa (L.) Gaertn. under elevated carbon dioxide , 1997, Plant Ecology.

[62]  D. Johnson,et al.  Effects of CO2 and nitrogen fertilization on vegetation and soil nutrient content in juvenile ponderosa pine , 1997, Plant and Soil.

[63]  W. Schlesinger,et al.  Compensatory responses of CO2 exchange and biomass allocation and their effects on the relative growth rate of ponderosa pine in different CO2 and temperature regimes , 1994, Oecologia.

[64]  P. Curtis,et al.  Elevated atmospheric CO2 and feedback between carbon and nitrogen cycles , 1993, Plant and Soil.

[65]  Richard J. Norby,et al.  Phenological responses in maple to experimental atmospheric warming and CO2 enrichment , 2003 .

[66]  P. Jarvis,et al.  Effects of elevated carbon dioxide concentration on growth and nitrogen fixation in Alnus glutinosa in a long-term field experiment. , 2003, Tree physiology.

[67]  R. Ceulemans,et al.  Free-air CO2 enrichment (FACE) enhances biomass production in a short-rotation poplar plantation. , 2003, Tree physiology.

[68]  D. Olszyk,et al.  Whole-seedling biomass allocation, leaf area, and tissue chemistry for Douglas-fir exposed to elevated CO2 and temperature for 4 years. , 2003 .

[69]  J. Holopainen,et al.  Contrasting effects of elevated carbon dioxide concentration and temperature on Rubisco activity, chlorophyll fluorescence, needle ultrastructure and secondary metabolites in conifer seedlings. , 2003, Tree physiology.

[70]  J. Blair,et al.  Rainfall Variability, Carbon Cycling, and Plant Species Diversity in a Mesic Grassland , 2002, Science.

[71]  R. Julkunen‐Tiitto,et al.  Effects of elevated CO2 and temperature on plant growth and herbivore defensive chemistry , 2002 .

[72]  H. Peltola,et al.  Diameter growth of Scots pine (Pinus sylvestris) trees grown at elevated temperature and carbon dioxide concentration under boreal conditions. , 2002, Tree physiology.

[73]  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 .

[74]  C. Körner,et al.  Four-year growth dynamics of beech-spruce model ecosystems under CO2 enrichment on two different forest soils , 2002, Trees.

[75]  T. Usami,et al.  Interactive effects of increased temperature and CO2 on the growth of Quercus myrsinaefolia saplings , 2001 .

[76]  R. Julkunen‐Tiitto,et al.  The effect of elevated CO2 and temperature on the secondary chemistry of Betula pendula seedlings , 2001, Trees.

[77]  H. Thorgeirsson,et al.  Growth and dry-matter partitioning of young Populus trichocarpa in response to carbon dioxide concentration and mineral nutrient availability. , 2001, Tree physiology.

[78]  S. Kellomäki,et al.  Growth and Resource Use of Birch Seedlings Under Elevated Carbon Dioxide and Temperature , 2001 .

[79]  Carl J. Bernacchi,et al.  Improved temperature response functions for models of Rubisco‐limited photosynthesis , 2001 .

[80]  K. Pregitzer,et al.  Combined effects of atmospheric CO2 and N availability on the belowground carbon and nitrogen dynamics of aspen mesocosms , 2000, Oecologia.

[81]  J. Leverenz,et al.  Effects of tree size and temperature on relative growth rate and its components of Fagus sylvatica seedlings exposed to two partial pressures of atmospheric [CO2] , 2000 .

[82]  M. Broadmeadow,et al.  Growth responses of Quercus petraea, Fraxinus excelsior and Pinus sylvestris to elevated carbon dioxide, ozone and water supply , 2000 .

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

[84]  Alan R. Ek,et al.  Process-based models for forest ecosystem management: current state of the art and challenges for practical implementation. , 2000, Tree physiology.

[85]  P. Curtis,et al.  Atmospheric Co2, Soil‐N Availability, And Allocation Of Biomass And Nitrogen By Populus Tremuloides , 2000 .

[86]  E. DeLucia,et al.  Interactive effects of elevated CO2 and temperature on water transport inponderosa pine. , 2000, American journal of botany.

[87]  N. Ramankutty,et al.  Estimating historical changes in global land cover: Croplands from 1700 to 1992 , 1999 .

[88]  Jessica Gurevitch,et al.  THE META‐ANALYSIS OF RESPONSE RATIOS IN EXPERIMENTAL ECOLOGY , 1999 .

[89]  B. Sheu,et al.  Photosynthetic response of seedlings of the sub-tropical tree Schima superba with exposure to elevated carbon dioxide and temperature , 1999 .

[90]  J. Roden,et al.  Effect of elevated [CO2] on photosynthesis and growth of snow gum (Eucalyptus pauciflora) seedlings during winter and spring , 1999 .

[91]  P. Reich,et al.  Seedlings of five boreal tree species differ in acclimation of net photosynthesis to elevated CO(2) and temperature. , 1998, Tree physiology.

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

[93]  F. Bazzaz,et al.  Elevated CO2 ameliorates birch response to high temperature and frost stress: implications for modeling climate-induced geographic range shifts , 1998, Oecologia.

[94]  C. Lovelock,et al.  Responses of communities of tropical tree species to elevated CO2 in a forest clearing , 1998, Oecologia.

[95]  P. Jarvis,et al.  Growth Response of Young Birch Trees (Betula pendulaRoth.) After Four and a Half Years of CO2Exposure , 1997 .

[96]  D. Tissue,et al.  Atmospheric CO2 enrichment increases growth and photosynthesis of Pinus taeda: a 4 year experiment in the field , 1997 .

[97]  D. Eamus,et al.  Diurnal and seasonal changes in the impact of CO(2) enrichment on assimilation, stomatal conductance and growth in a long-term study of Mangifera indica in the wet-dry tropics of Australia. , 1997, Tree physiology.

[98]  R. Teskey Combined effects of elevated CO2 and air temperature on carbon assimilation of Pinus taeda trees , 1997 .

[99]  W. Schlesinger,et al.  Mechanisms of Phosphorus Acquisition for Ponderosa Pine Seedlings under High CO 2 and Temperature , 1997 .

[100]  V. Dantec,et al.  Sweet Chestnut and Beech Saplings under Elevated CO2 , 1997 .

[101]  I. Prentice,et al.  A general model for the light-use efficiency of primary production , 1996 .

[102]  J. King,et al.  Growth and carbon accumulation in root systems of Pinus taeda and Pinus ponderosa seedlings as affected by varying CO(2), temperature and nitrogen. , 1996, Tree physiology.

[103]  R. Ceulemans,et al.  First- and second-year aboveground growth and productivity of two Populus hybrids grown at ambient and elevated CO2 , 1996 .

[104]  C. Nietch,et al.  Increased growth efficiency of Quercus alba trees in a CO2 -enriched atmosphere. , 1995, The New phytologist.

[105]  P. Curtis,et al.  Atmospheric CO2, soil nitrogen and turnover of fine roots , 1995 .

[106]  L. Mortensen Effect of carbon dioxide concentration on biomass production and partitioning in Betula pubescens Ehrh. seedlings at different ozone and temperature regimes. , 1995, Environmental pollution.

[107]  S. Idso,et al.  Effects of atmospheric CO2 enrichment on biomass accumulation and distribution in Eldarica pine trees , 1994 .

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

[109]  Stan D. Wullschleger,et al.  Productivity and compensatory responses of yellow-poplar trees in elevated C02 , 1992, Nature.

[110]  Stephen P. Long,et al.  Modification of the response of photosynthetic productivity to rising temperature by atmospheric CO2 concentrations: Has its importance been underestimated? , 1991 .

[111]  G. Collatz,et al.  Physiological and environmental regulation of stomatal conductance, photosynthesis and transpiration: a model that includes a laminar boundary layer , 1991 .

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

[113]  S S I T C H,et al.  Evaluation of Ecosystem Dynamics, Plant Geography and Terrestrial Carbon Cycling in the Lpj Dynamic Global Vegetation Model , 2022 .