To what extent do current and projected increases in surface ozone affect photosynthesis and stomatal conductance of trees? A meta-analytic review of the last 3 decades of experiments.

The surface concentration of ozone ([O(3)]) has risen from less than 10 ppb prior to the industrial revolution to a day-time mean concentration of approximately 40 ppb over much of the northern temperate zone. If current global emission trends continue, surface [O(3)] is projected to rise a further 50% over this century, with larger increases in many locations including Northern Hemisphere forests. This review uses statistical meta-analysis to determine mean effects, and their confidence limits, of both the current and projected elevations of [O(3)] on light-saturated photosynthetic CO(2) uptake (A(sat)) and stomatal conductance (g(s)) in trees. In total, 348 measurements of A(sat) from 61 studies and 266 measures of g(s) from 55 studies were reviewed. Results suggested that the elevation of [O(3)] that has occurred since the industrial revolution is depressing A(sat) and g(s) by 11% (CI 9-13%) and 13% (CI 11-15%), respectively, where CI is the 95% confidence interval. In contrast to angiosperms, gymnosperms were not significantly affected. Both drought and elevated [CO(2)] significantly decreased the effect of ambient [O(3)]. Younger trees (<4 years) were affected less than older trees. Elevation of [O(3)] above current levels caused progressively larger losses of A(sat) and g(s), including gymnosperms. Results are consistent with the expectation that damage to photosynthesis depends on the cumulative uptake of ozone (O(3)) into the leaf. Thus, factors that lower g(s) lessen damage. Where both g(s) and [O(3)] were recorded, an overall decline in A(sat) of 0.21% per mmol m(-2) of estimated cumulative O(3) uptake was calculated. These findings suggest that rising [O(3)], an often overlooked aspect of global atmospheric change, is progressively depressing the ability of temperate and boreal forests to assimilate carbon and transfer water vapour to the atmosphere, with significant potential effects on terrestrial carbon sinks and regional hydrologies.

[1]  K. Pregitzer,et al.  Scaling ozone responses of forest trees to the ecosystem level in a changing climate , 2005 .

[2]  A. Chappelka,et al.  Ambient ozone effects on forest trees of the eastern United States: a review , 1998 .

[3]  Robert J. Scholes,et al.  The Carbon Cycle and Atmospheric Carbon Dioxide , 2001 .

[4]  R. Betts,et al.  Changes in Atmospheric Constituents and in Radiative Forcing. Chapter 2 , 2007 .

[5]  Rainer Matyssek,et al.  Impacts of Air Pollution and Climate Change on Forest Ecosystems — Emerging Research Needs , 2007, TheScientificWorldJournal.

[6]  G. Arnqvist,et al.  MetaWin: Statistical Software for Meta-Analysis with Resampling Tests. Version 1.Michael S. Rosenberg , Dean C. Adams , Jessica Gurevitch , 1998 .

[7]  G. Host,et al.  Simulating the growth response of aspen to elevated ozone: a mechanistic approach to scaling a leaf-level model of ozone effects on photosynthesis to a complex canopy architecture. , 2001, Environmental pollution.

[8]  U. Maier-Maercker,et al.  Experiments on the control capacity of stomata of Picea abies (L.) Karst. after fumigation with ozone and in environmentally damaged material , 1991 .

[9]  R. Grote,et al.  Testing the unifying theory of ozone sensitivity with mature trees of Fagus sylvatica and Picea abies. , 2006, Tree physiology.

[10]  J. Skelly,et al.  Perspectives regarding 50 years of research on effects of tropospheric ozone air pollution on US forests. , 2007, Environmental pollution.

[11]  L. Samuelson,et al.  Scaling ozone effects from seedlings to forest trees. , 2001, The New phytologist.

[12]  L. Skärby,et al.  Impacts of ozone on forests: a European perspective , 1998 .

[13]  Ronald G. Prinn,et al.  Effects of ozone on net primary production and carbon sequestration in the conterminous United States using a biogeochemistry model , 2004 .

[14]  S. Long,et al.  The Sequence of Change within the Photosynthetic Apparatus of Wheat following Short-Term Exposure to Ozone. , 1991, Plant physiology.

[15]  Jessica Gurevitch,et al.  MetaWin: Statistical Software for Meta-analysis with Resampling Tests , 1997 .

[16]  J. Kangasjärvi,et al.  Signalling and cell death in ozone‐exposed plants , 2005 .

[17]  R. E. Dickson,et al.  Tropospheric O3 moderates responses of temperate hardwood forests to elevated CO2: a synthesis of molecular to ecosystem results from the Aspen FACE project , 2003 .

[18]  Robert L. Heath,et al.  Possible mechanisms for the inhibition of photosynthesis by ozone , 1994, Photosynthesis Research.

[19]  D. Schimel,et al.  Atmospheric Chemistry and Greenhouse Gases , 1999 .

[20]  M. Leuchner,et al.  Extraordinary drought of 2003 overrules ozone impact on adult beech trees (Fagus sylvatica) , 2006, Trees.

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

[22]  J. Middleton,et al.  Problems of Air Pollution in Plant Pathology , 1966 .

[23]  P. Farage The effect of ozone fumigation over one season on photosynthetic processes of Quercus robur seedlings , 1996 .

[24]  E. Oksanen Physiological responses of birch (Betula pendula) to ozone: a comparison between open-soil-grown trees exposed for six growing seasons and potted seedlings exposed for one season. , 2003, Tree physiology.

[25]  P. Dizengremel Effects of ozone on the carbon metabolism of forest trees , 2001 .

[26]  P. Curtis,et al.  A meta‐analysis of elevated [CO2] effects on soybean (Glycine max) physiology, growth and yield , 2002 .

[27]  H. Preisler,et al.  A statistical approach to estimate O3 uptake of ponderosa pine in a mediterranean climate. , 2002, Environmental pollution.

[28]  D Fowler,et al.  Modelling photochemical oxidant formation, transport, deposition and exposure of terrestrial ecosystems. , 1999, Environmental pollution.

[29]  Richard N. Arteca,et al.  Ozone‐induced oxidative stress: Mechanisms of action and reaction , 1997 .

[30]  M. Sanz,et al.  Promoting the O3 flux concept for European forest trees. , 2007, Environmental pollution.

[31]  J. Fuhrer,et al.  Seasonal trends in reduced leaf gas exchange and ozone-induced foliar injury in three ozone sensitive woody plant species. , 2005, Environmental pollution.

[32]  G. Wieser,et al.  Linking ozone uptake and defense towards a mechanistic risk assessment for forest trees. , 2007, The New phytologist.

[33]  Andreas Volz,et al.  Evaluation of the Montsouris series of ozone measurements made in the nineteenth century , 1988, Nature.

[34]  P. Reich,et al.  Effects of low level O3 exposure on leaf diffusive conductance and water‐use efficiency in hybrid poplar , 1984 .

[35]  J. Skelly,et al.  Light environment alters ozone uptake per net photosynthetic rate in black cherry trees. , 1996, Tree physiology.

[36]  J. Innes,et al.  Ozone - a Risk Factor for Trees and Forests in Europe? , 1999 .

[37]  W. Collins,et al.  Global climate projections , 2007 .

[38]  S. Long,et al.  How does elevated ozone impact soybean? A meta‐analysis of photosynthesis, growth and yield , 2003 .

[39]  G. J. Collatz,et al.  Comparison of Radiative and Physiological Effects of Doubled Atmospheric CO2 on Climate , 1996, Science.

[40]  Trevor Platt,et al.  Primary productivity of planet earth: biological determinants and physical constraints in terrestrial and aquatic habitats , 2001 .

[41]  P. Reich,et al.  Quantifying plant response to ozone: a unifying theory. , 1987, Tree physiology.

[42]  B. Kimball,et al.  Decreases in Stomatal Conductance of Soybean under Open-Air Elevation of [CO2] Are Closely Coupled with Decreases in Ecosystem Evapotranspiration12[W][OA] , 2006, Plant Physiology.

[43]  B. Gimeno,et al.  Risk assessments for forest trees: the performance of the ozone flux versus the AOT concepts. , 2007, Environmental pollution.

[44]  Jessica Gurevitch,et al.  STATISTICAL ISSUES IN ECOLOGICAL META‐ANALYSES , 1999 .

[45]  J. Grace Understanding and managing the global carbon cycle , 2004 .

[46]  Scott V. Ollinger,et al.  SIMULATING OZONE EFFECTS ON FOREST PRODUCTIVITY: INTERACTIONS AMONG LEAF‐, CANOPY‐, AND STAND‐LEVEL PROCESSES , 1997 .

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

[48]  H. Akimoto Global Air Quality and Pollution , 2003, Science.

[49]  O. Kull,et al.  Ozone concentration in leaf intercellular air spaces is close to zero. , 1989, Plant physiology.

[50]  D. Derwent,et al.  The Global Exposure of Forests to Air Pollutants , 1999 .

[51]  M. S. J. Broadmeadow Ozone and forest trees , 1998 .

[52]  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.

[53]  S. Long,et al.  An in vivo analysis of photosynthesis during short-term O3 exposure in three contrasting species , 2004, Photosynthesis Research.

[54]  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 .

[55]  N. Grulke,et al.  Stomata open at night in pole-sized and mature ponderosa pine: implications for O3 exposure metrics. , 2004, Tree physiology.

[56]  Kenneth L. Denman Canada Couplings between changes in the climate system and biogeochemistry , 2008 .

[57]  S. McLaughlin,et al.  Interactive effects of ozone and climate on tree growth and water use in a southern Appalachian forest in the USA. , 2007, The New phytologist.

[58]  E. P. McDonald,et al.  Growth responses of Populus tremuloides clones to interacting elevated carbon dioxide and tropospheric ozone. , 2001, Environmental pollution.

[59]  M. Ashmore Assessing the future global impacts of ozone on vegetation , 2005 .

[60]  J. Middleton Response of Plants to Air Pollution , 1956 .

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