Photosynthesis of temperate Eucalyptus globulus trees outside their native range has limited adjustment to elevated CO2 and climate warming

Eucalyptus species are grown widely outside of their native ranges in plantations on all vegetated continents of the world. We predicted that such a plantation species would show high potential for acclimation of photosynthetic traits across a wide range of growth conditions, including elevated [CO2] and climate warming. To test this prediction, we planted temperate Eucalyptus globulus Labill. seedlings in climate‐controlled chambers in the field located >700 km closer to the equator than the nearest natural occurrence of this species. Trees were grown in a complete factorial combination of elevated CO2 concentration (eC; ambient [CO2] +240 ppm) and air warming treatments (eT; ambient +3 °C) for 15 months until they reached ca. 10 m height. There was little acclimation of photosynthetic capacity to eC and hence the CO2‐induced photosynthetic enhancement was large (ca. 50%) in this treatment during summer. The warming treatment significantly increased rates of both carboxylation capacity (Vcmax) and electron transport (Jmax) (measured at a common temperature of 25 °C) during winter, but decreased them significantly by 20–30% in summer. The photosynthetic CO2 compensation point in the absence of dark respiration (Γ*) was relatively less sensitive to temperature in this temperate eucalypt species than for warm‐season tobacco. The temperature optima for photosynthesis and Jmax significantly changed by about 6 °C between winter and summer, but without further adjustment from early to late summer. These results suggest that there is an upper limit for the photosynthetic capacity of E. globulus ssp. globulus outside its native range to acclimate to growth temperatures above 25 °C. Limitations to temperature acclimation of photosynthesis in summer may be one factor that defines climate zones where E. globulus plantation productivity can be sustained under anticipated global environmental change.

[1]  J. R. Evans,et al.  Temperature response of carbon isotope discrimination and mesophyll conductance in tobacco. , 2013, Plant, cell & environment.

[2]  T. Sharkey.  Advances in photosynthesis and respiration , 2012, Photosynthesis Research.

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

[4]  D. Ellsworth,et al.  Temperature responses of leaf net photosynthesis: the role of component processes. , 2012, Tree physiology.

[5]  P. Reich,et al.  Local ecotypic and species range-related adaptation influence photosynthetic temperature optima in deciduous broadleaved trees , 2011, Plant Ecology.

[6]  D. Way,et al.  On the role of ecological adaptation and geographic distribution in the response of trees to climate change. , 2011, Tree physiology.

[7]  T. Mikkelsen,et al.  Effects of Single and Multifactor Treatments with Elevated Temperature, CO2 and Ozone on Oilseed Rape and Barley , 2011 .

[8]  R. Teskey,et al.  Higher growth temperatures decreased net carbon assimilation and biomass accumulation of northern red oak seedlings near the southern limit of the species range. , 2011, Tree physiology.

[9]  S. Heckathorn,et al.  A meta-analysis of plant physiological and growth responses to temperature and elevated CO2 , 2011, Oecologia.

[10]  A. Michelsen,et al.  Interactive effects of drought, elevated CO2 and warming on photosynthetic capacity and photosystem performance in temperate heath plants. , 2011, Journal of plant physiology.

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

[12]  J. R. Evans,et al.  Using tunable diode laser spectroscopy to measure carbon isotope discrimination and mesophyll conductance to CO₂ diffusion dynamically at different CO₂ concentrations. , 2011, Plant, cell & environment.

[13]  D. Ellsworth,et al.  Seasonal acclimation of leaf respiration in Eucalyptus saligna trees: impacts of elevated atmospheric CO2 and summer drought , 2011 .

[14]  B. Logan,et al.  Photosynthetic responses of two eucalypts to industrial-age changes in atmospheric [CO2] and temperature. , 2010, Plant, cell & environment.

[15]  R. McMurtrie,et al.  Whole-tree chambers for elevated atmospheric CO2 experimentation and tree scale flux measurements in south-eastern Australia: the Hawkesbury Forest Experiment. , 2010 .

[16]  E. Kruger,et al.  Thermal acclimation of photosynthesis: a comparison of boreal and temperate tree species along a latitudinal transect. , 2010, Plant, cell & environment.

[17]  Ram Oren,et al.  Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data. , 2010, Tree physiology.

[18]  M. Hozain,et al.  The differential response of photosynthesis to high temperature for a boreal and temperate Populus species relates to differences in Rubisco activation and Rubisco activase properties. , 2010, Tree physiology.

[19]  R. Norby,et al.  A comment on ''Appropriate experimental ecosystem warming methods by ecosystem, objective, and practicality'' by Aronson and McNulty § , 2010 .

[20]  Michael Battaglia,et al.  Managing productivity and drought risk in Eucalyptus globulus plantations in south-western Australia. , 2009 .

[21]  C. Gunderson,et al.  Thermal plasticity of photosynthesis: the role of acclimation in forest responses to a warming climate , 2009 .

[22]  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 .

[23]  R. Sage,et al.  Thermal acclimation of photosynthesis in black spruce [Picea mariana (Mill.) B.S.P.]. , 2008, Plant, cell & environment.

[24]  D. Whitehead,et al.  Thermal acclimation of respiration but not photosynthesis in Pinus radiata. , 2008, Functional plant biology : FPB.

[25]  R. Sage,et al.  Rubisco, Rubisco activase, and global climate change. , 2008, Journal of experimental botany.

[26]  R. Morcuende,et al.  Future CO2 concentrations, though not warmer temperatures, enhance wheat photosynthesis temperature responses. , 2007, Physiologia plantarum.

[27]  Fernando Valladares,et al.  Ecological limits to plant phenotypic plasticity. , 2007, The New phytologist.

[28]  Jens Kattge,et al.  Temperature acclimation in a biochemical model of photosynthesis: a reanalysis of data from 36 species. , 2007, Plant, cell & environment.

[29]  Joseph D. Bowden,et al.  The influence of temperature on within-canopy acclimation and variation in leaf photosynthesis: spatial acclimation to microclimate gradients among climatically divergent Acer rubrum L. genotypes. , 2007, Journal of experimental botany.

[30]  K. Hikosaka,et al.  Seasonal changes in the temperature response of photosynthesis in canopy leaves of Quercus crispula in a cool-temperate forest. , 2007, Tree physiology.

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

[32]  Y. Kosugi,et al.  Seasonal fluctuations and temperature dependence of leaf gas exchange parameters of co-occurring evergreen and deciduous trees in a temperate broad-leaved forest. , 2006, Tree physiology.

[33]  K. Hikosaka,et al.  Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate. , 2006, Journal of experimental botany.

[34]  Y. Cen,et al.  The Regulation of Rubisco Activity in Response to Variation in Temperature and Atmospheric CO2 Partial Pressure in Sweet Potato1[w] , 2005, Plant Physiology.

[35]  J. Peñuelas,et al.  Running to stand still: adaptation and the response of plants to rapid climate change. , 2005, Ecology letters.

[36]  P. Reich,et al.  Acclimation of leaf respiration to temperature is rapid and related to specific leaf area, soluble sugars and leaf nitrogen across three temperate deciduous tree species , 2005 .

[37]  S. Lavorel,et al.  Niche properties and geographical extent as predictors of species sensitivity to climate change , 2005 .

[38]  R. Petit,et al.  Conserving biodiversity under climate change: the rear edge matters. , 2005, Ecology letters.

[39]  K. Noguchi,et al.  Temperature acclimation of photosynthesis in spinach leaves: analyses of photosynthetic components and temperature dependencies of photosynthetic partial reactions , 2005 .

[40]  K. Hikosaka,et al.  Seasonal change in the balance between capacities of RuBP carboxylation and RuBP regeneration affects CO2 response of photosynthesis in Polygonum cuspidatum. , 2005, Journal of experimental botany.

[41]  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.

[42]  M. Tjoelker,et al.  Response of plant respiration to changes in temperature: mechanisms and consequences of variations in Q(10) values and acclimation , 2005 .

[43]  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 .

[44]  Ranga B. Myneni,et al.  Thresholds for warming‐induced growth decline at elevational tree line in the Yukon Territory, Canada , 2004 .

[45]  Ü. Niinemets,et al.  Photosynthetic acclimation to simultaneous and interacting environmental stresses along natural light gradients: optimality and constraints. , 2004, Plant biology.

[46]  M. Salvucci,et al.  Relationship between the Heat Tolerance of Photosynthesis and the Thermal Stability of Rubisco Activase in Plants from Contrasting Thermal Environments1 , 2004, Plant Physiology.

[47]  Michael E. Salvucci,et al.  Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. , 2004, Physiologia plantarum.

[48]  F. I. Woodward,et al.  Climate and plant distribution at global and local scales , 1987, Vegetatio.

[49]  G. Farquhar,et al.  Effect of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light , 1985, Planta.

[50]  J. Berry,et al.  A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species , 1980, Planta.

[51]  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 .

[52]  M. Peisker,et al.  Inhibition by light of CO2 evolution from dark respiration: Comparison of two gas exchange methods , 2004, Photosynthesis Research.

[53]  Carl J. Bernacchi,et al.  In vivo temperature response functions of parameters required to model RuBP-limited photosynthesis , 2003 .

[54]  R. McKane,et al.  Elevated CO2 and temperature alter nitrogen allocation in Douglas‐fir , 2003 .

[55]  Mark G Tjoelker,et al.  Thermal acclimation and the dynamic response of plant respiration to temperature. , 2003, Trends in plant science.

[56]  Susanne von Caemmerer,et al.  Temperature Response of Mesophyll Conductance. Implications for the Determination of Rubisco Enzyme Kinetics and for Limitations to Photosynthesis in Vivo , 2002, Plant Physiology.

[57]  Olevi Kull,et al.  Acclimation of photosynthesis in canopies: models and limitations , 2002, Oecologia.

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

[59]  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 .

[60]  T. Mikkelsen,et al.  Does the direct effect of atmospheric CO2 concentration on leaf respiration vary with temperature? Responses in two species of Plantago that differ in relative growth rate. , 2002, Physiologia plantarum.

[61]  D. Tingey,et al.  ELEVATED CO2 AND TEMPERATURE ALTER THE RESPONSE OF PINUS PONDEROSA TO OZONE: A SIMULATION ANALYSIS , 2001 .

[62]  D. Olszyk,et al.  Seasonal patterns of photosynthesis in Douglas fir seedlings during the third and fourth year of exposure to elevated CO2 and temperature , 2001 .

[63]  R. Shaw,et al.  Range shifts and adaptive responses to Quaternary climate change. , 2001, Science.

[64]  Michael R. Raupach,et al.  Combination theory and equilibrium evaporation , 2001 .

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

[66]  Ü. Niinemets,et al.  Shape of leaf photosynthetic electron transport versus temperature response curve is not constant along canopy light gradients in temperate deciduous trees , 1999 .

[67]  K. Hikosaka,et al.  Balancing carboxylation and regeneration of ribulose‐1,5‐ bisphosphate in leaf photosynthesis: temperature acclimation of an evergreen tree, Quercus myrsinaefolia , 1999 .

[68]  J. H. M. Thornley,et al.  Temperature and CO2Responses of Leaf and Canopy Photosynthesis: a Clarification using the Non-rectangular Hyperbola Model of Photosynthesis , 1998 .

[69]  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.

[70]  K. R. Reddy,et al.  Interactions of CO2 enrichment and temperature on cotton growth and leaf characteristics , 1998 .

[71]  D. Whitehead,et al.  The response of photosynthetic model parameters to temperature and nitrogen concentration in Pinus radiata D. Don , 1997 .

[72]  M. Battaglia,et al.  Photosynthetic temperature responses of Eucalyptus globulus and Eucalyptus nitens. , 1996, Tree physiology.

[73]  D. Eamus.  Tree responses to CO(2) enrichment: CO(2) and temperature interactions, biomass allocation and stand-scale modeling. , 1996, Tree physiology.

[74]  M. Kirschbaum.  The sensitivity of C3 photosynthesis to increasing CO2 concentration: a theoretical analysis of its dependence on temperature and background CO2 concentration , 1994 .

[75]  James F. Reynolds,et al.  Modelling photosynthesis of cotton grown in elevated CO2 , 1992 .

[76]  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 .

[77]  R. Slatyer,et al.  Photosynthetic Temperature Acclimation in Eucalyptus Species From Diverse Habitats, and a Comparison With Nerium oleander , 1989 .

[78]  D. Jordan,et al.  The CO2/O 2 specificity of ribulose 1,5-bisphosphate carboxylase/oxygenase : Dependence on ribulosebisphosphate concentration, pH and temperature. , 1984, Planta.

[79]  V. Barnett,et al.  Applied Linear Statistical Models , 1975 .