Advances in understanding ozone impact on forest trees: messages from novel phytotron and free-air fumigation studies.

Recent evidence from novel phytotron and free-air ozone (O3) fumigation experiments in Europe and America on forest tree species is highlighted in relation to previous chamber studies. Differences in O3 sensitivity between pioneer and climax species are examined and viewed for trees growing at the harsh alpine timberline ecotone. As O3 apparently counteracts positive effects of elevated CO2 and mitigates productivity increases, response is governed by genotype, competitors, and ontogeny rather than species per se. Complexity in O3 responsiveness increased under the influence of pathogens and herbivores. The new evidence does not conflict in principle with previous findings that, however, pointed to a low ecological significance. This new knowledge on trees' O3 responsiveness beyond the juvenile stage in plantations and forests nevertheless implies limited predictability due to complexity in biotic and abiotic interactions. Unravelling underlying mechanisms is mandatory for assessing O3 risks as an important component of climate change scenarios.

[1]  G. Wieser,et al.  Design and testing of twig chambers for ozone fumigation and gas exchange measurements in mature trees , 1994 .

[2]  R. Barbehenn,et al.  Effects of elevated atmospheric CO2 on the nutritional ecology of C3 and C4 grass-feeding caterpillars , 2004, Oecologia.

[3]  O. Canziani,et al.  Climate change 2007: synthesis report. Summary for policymakers , 2007 .

[4]  K. Pregitzer,et al.  Populus tremuloides photosynthesis and crown architecture in response to elevated CO2 and soil N availability , 1997, Oecologia.

[5]  H. Rennenberg,et al.  Antioxidative defence of old growth beech (Fagus sylvatica) under double ambient O3 concentrations in a free-air exposure system. , 2007, Plant biology.

[6]  P. Reich,et al.  Response Mechanisms of Conifers to Air Pollutants , 1995 .

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

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

[9]  P. Dizengremel,et al.  The impact of elevated ozone and carbon dioxide on young Acer saccharum seedlings. , 2003, Physiologia plantarum.

[10]  R. Ceulemans,et al.  FACEing the future: planning the next generation of elevated CO2 experiments on crops and ecosystems. , 2009 .

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

[12]  H. Blaschke,et al.  Above-ground space sequestration determines competitive success in juvenile beech and spruce trees. , 2005, The New phytologist.

[13]  R. E. Dickson,et al.  Root growth and physiology of potted and field-grown trembling aspen exposed to tropospheric ozone. , 1996, Tree physiology.

[14]  C. Andersen,et al.  Nutrient availability alters belowground respiration of ozone-exposed ponderosa pine. , 1997, Tree physiology.

[15]  A. Noormets,et al.  Interacting elevated CO2 and tropospheric O3 predisposes aspen (Populus tremuloides Michx.) to infection by rust (Melampsora medusae f. sp. tremuloidae) , 2002 .

[16]  P. Rundel,et al.  Stand characteristics of ozone-stressed populations of Pinus jeffreyi (Pinaceae): extent, development, and physiological consequences of visible injury. , 1995 .

[17]  H. Rennenberg,et al.  Competition modifies effects of enhanced ozone/carbon dioxide concentrations on carbohydrate and biomass accumulation in juvenile Norway spruce and European beech. , 2004, Tree physiology.

[18]  M R Ashmore,et al.  Critical levels for ozone effects on vegetation in Europe. , 1997, Environmental pollution.

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

[20]  E. Goto,et al.  Responses of plant metabolism to air pollution and global change , 1998 .

[21]  R. Matyssek,et al.  Flux-based response of sucrose and starch in leaves of adult beech trees (Fagus sylvatica L.) under chronic free-air O3 fumigation. , 2007, Plant biology.

[22]  E. Beuker,et al.  Differences in leaf characteristics between ozone-sensitive and ozone-tolerant hybrid aspen (Populus tremula x Populus tremuloides) clones. , 2008, Tree physiology.

[23]  M. Tausz,et al.  Internal conductance to CO2 transfer of adult Fagus sylvatica: Variation between sun and shade leaves and due to free-air ozone fumigation , 2007 .

[24]  D. Ernst,et al.  Ozone Responses of Trees: Results from Controlled Chamber Exposures at the GSF Phytotron , 1997 .

[25]  P. Ciais,et al.  Europe-wide reduction in primary productivity caused by the heat and drought in 2003 , 2005, Nature.

[26]  T. Dawson,et al.  Combining δ13C and δ18O analyses to unravel competition, CO2 and O3 effects on the physiological performance of different‐aged trees , 2007 .

[27]  B. Sundberg,et al.  Trends in European Forest Tree Physiology Research , 2001, Tree Physiology.

[28]  D. Vanderklein,et al.  Effects of elevated ozone and low light on diurnal and seasonal carbon gain in sugar maple , 2001 .

[29]  A. Wellburn,et al.  Forest Decline and Ozone , 1997, Ecological Studies.

[30]  H. Werner,et al.  Seasonal ozone response of mature beech trees (Fagus sylvatica) at high altitude in the Bavarian forest (Germany) in comparison with young beech grown in the field and in phytotrons. , 2000, Environmental pollution.

[31]  D Hauglustaine,et al.  The global atmospheric environment for the next generation. , 2006, Environmental science & technology.

[32]  R. Lindroth,et al.  Divergent pheromone‐mediated insect behaviour under global atmospheric change , 2004 .

[33]  S. Long,et al.  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. , 2007, Plant, cell & environment.

[34]  G. Wieser,et al.  Effects of ozone and mild drought stress on gas exchange, antioxidants and chloroplast pigments in current-year needles of young Norway spruce [Picea abies (L.) Karst.] , 1998, Trees.

[35]  The Effects of Ozone , 1882, The Dental register.

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

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

[38]  T. Grams,et al.  Competition for Resources in Trees: Physiological Versus Morphological Plasticity , 2007 .

[39]  J. Nagy,et al.  Free-air exposure systems to scale up ozone research to mature trees. , 2007, Plant biology.

[40]  K. Percy,et al.  Impacts of greenhouse gases on epicuticular waxes of Populus tremuloides Michx.: results from an open-air exposure and a natural O3 gradient. , 2005, Environmental pollution.

[41]  T. Mansfield,et al.  Effects of exposure to ozone and water stress on the following season's growth of beech (Fagus sylvatica L.). , 1994, The New phytologist.

[42]  R. Matyssek,et al.  Acclimation to Ozone Affects Host/Pathogen Interaction and Competitiveness for Nitrogen in Juvenile Fagus sylvatica and Picea abies Trees Infected with Phytophthora citricola , 2005, Plant biology.

[43]  R. E. Dickson,et al.  Changes in growth, leaf abscission, and biomass associated with seasonal tropospheric ozone exposures of Populus tremuloides clones and seedlings , 1996 .

[44]  R. Matyssek,et al.  Ozone‐induced accumulation of carbohydrates changes enzyme activities of carbohydrate metabolism in birch leaves , 1997 .

[45]  R. Lindroth,et al.  Effects of elevated carbon dioxide and ozone on the phytochemistry of aspen and performance of an herbivore , 2002, Oecologia.

[46]  Herbert Werner,et al.  Free-air fumigation of mature trees , 2002, Environmental science and pollution research international.

[47]  R. Lindroth,et al.  Responses of Diciduous Trees to Elevated Atmospheric CO2: Productivity, Phytochemistry, and Insect Performance , 1993 .

[48]  Karl Steiner,et al.  Interactive effects of elevated CO2 and O3 on photosynthesis and biomass production of clonal 5-year-old Norway spruce [Picea abies (L.) Karst.] under different nitrogen nutrition and irrigation treatments , 1996, Trees.

[49]  R. I C H,et al.  Aphid individual performance may not predict population responses to elevated CO 2 or O 3 , 2003 .

[50]  P. Reich,et al.  Interaction of ozone pollution and light effects on photosynthesis in a forest canopy experiment , 1995 .

[51]  H. Kraigher,et al.  Changes in the community of ectomycorrhizal fungi and increased fine root number under adult beech trees chronically fumigated with double ambient ozone concentration. , 2007, Plant biology.

[52]  K. Pihlaja,et al.  Effects of Long-Term Open-Field Ozone Exposure on Leaf Phenolics of European Silver Birch (Betula pendula Roth) , 2001, Journal of Chemical Ecology.

[53]  D. Le Thiec,et al.  Ozone-induced changes in photosynthesis and photorespiration of hybrid poplar in relation to the developmental stage of the leaves. , 2008, Physiologia plantarum.

[54]  B. Hale,et al.  Methods for Controlled and Field Ozone Exposures of Forest Tree Species in North America , 1997 .

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

[56]  T. Mansfield,et al.  Interacting effects of ozone and water stress on the stomatal resistance of beech (Fagus sylvatica L.). , 1993 .

[57]  A. Noormets,et al.  Ozone affects the fitness of trembling aspen , 2003 .

[58]  P. Curtis,et al.  Interacting effects of soil fertility and atmospheric CO2 on leaf area growth and carbon gain physiology in Populus×euramericana (Dode) Guinier. , 1995, The New phytologist.

[59]  V. Fontaine,et al.  Carbon fixation in Pinus halepensis submitted to ozone. Opposite response of ribulose‐1,5‐bisphosphate carboxylase/oxygenase and phosphoenolpyruvate carboxylase , 1999 .

[60]  J. Bennett,et al.  Natural selection for ozone tolerance in Populus tremuloides: field verification , 1989 .

[61]  R. Matyssek,et al.  Contrasting ozone × pathogen interaction as mediated through competition between juvenile European beech (Fagus sylvatica) and Norway spruce (Picea abies) , 2009, Plant and Soil.

[62]  A. Price,et al.  Effects of long-term, free-air ozone fumigation on the cytokinin content of mature beech trees. , 2007, Plant biology.

[63]  M. Kubiske,et al.  Effects of elevated atmospheric CO2 and/or O3 on intra- and interspecific competitive ability of aspen. , 2007, Plant biology.

[64]  A. Chappelka,et al.  Diversity of an early successional plant community as influenced by ozone , 1998 .

[65]  H. Ellenberg,et al.  Vegetation Mitteleuropas mit den Alpen , 1984 .

[66]  R. Matyssek,et al.  Whole-plant growth and leaf formation in ozonated hybrid poplar (Populus x euramericana). , 1993, Environmental pollution.

[67]  S. Gayler,et al.  Analysis of competition effects in mono- and mixed cultures of juvenile beech and spruce by means of the plant growth simulation model PLATHO. , 2006, Plant biology.

[68]  E. Pääkkönen,et al.  Influence of nitrogen supply on the response of clones of birch (Betula pendula Roth.) to ozone , 1995 .

[69]  E. P. McDonald,et al.  Competitive status influences tree‐growth responses to elevated CO2 and O3 in aggrading aspen stands , 2002 .

[70]  Michael H. Depledge,et al.  Ground-level ozone in the 21st century: future trends, impacts and policy implications , 2008 .

[71]  H. Blaschke,et al.  Competition increasingly dominates the responsiveness of juvenile beech and spruce to elevated CO2 and/or O3 concentrations throughout two subsequent growing seasons , 2005 .

[72]  A. Legge,et al.  New exposure-based metric approach for evaluating O(3) risk to North American aspen forests. , 2007, Environmental pollution.

[73]  R. E. Dickson,et al.  Genetic control of responses to interacting tropospheric ozone and CO2 in Populus tremuloides , 1998 .

[74]  M. Saurer,et al.  Response Mechanisms of Birch and Poplar to Air Pollutants , 1997 .

[75]  S. Long,et al.  Quantifying the impact of current and future tropospheric ozone on tree biomass, growth, physiology and biochemistry: a quantitative meta‐analysis , 2009 .

[76]  G. Wieser,et al.  Environmental control of ozone uptake in Larix decidua Mill.: a comparison between different altitudes. , 1995, Tree physiology.

[77]  G. Wieser,et al.  Upscaling Ozone Flux in Forests from Leaf to Landscape , 2008 .

[78]  Robert L. Heath,et al.  Forest decline and ozone. A comparison of controlled chamber and field experiments. , 1997 .

[79]  Rainer Matyssek,et al.  FACE systems for studying the impacts of greenhouse gases on forest ecosystems , 2001 .

[80]  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.

[81]  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.

[82]  C. Reid,et al.  Effects of elevated [CO2] and/or ozone on limitations to CO2 assimilation in soybean (Glycine max) , 1998 .

[83]  G. Wieser,et al.  Evaluation of Ozone Impact on Mature Spruce and Larch in the Field , 1996 .

[84]  W. Manning.  Establishing a cause and effect relationship for ambient ozone exposure and tree growth in the forest: progress and an experimental approach. , 2005, Environmental pollution.

[85]  A. Farrell,et al.  Prospects for International Management of Intercontinental Air Pollution Transport , 2004 .

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

[87]  R. Häsler,et al.  Role of climate, crown position, tree age and altitude in calculated ozone flux into needles of Picea abies and Pinus cembra: a synthesis. , 2000, Environmental pollution.

[88]  H. Payer,et al.  Assessing the impact of elevated O3 and CO2 on gas exchange characteristics of differently K supplied clonal Norway spruce trees during exposure and the following season , 1997, Trees.

[89]  R. Matyssek,et al.  Leaf and stem structure of poplar (Populus ×euramericana) as Influenced by O3, NO2, their combination, and different soil N supplies , 1996 .

[90]  G. Wieser,et al.  Responses of Photosynthesis, Carbohydrates and Antioxidants in Needles of Norway Spruce to Slow and Rapid Changes in Ozone , 1998 .

[91]  E. Priesack,et al.  The plant's capacity in regulating resource demand. , 2005, Plant biology.

[92]  C. Andersen.  Source-sink balance and carbon allocation below ground in plants exposed to ozone. , 2003, The New phytologist.

[93]  H. Sandermann,et al.  Response patterns in adult forest trees to chronic ozone stress: identification of variations and consistencies. , 2005, Environmental pollution.

[94]  R. Vingarzan.  A review of surface ozone background levels and trends , 2004 .

[95]  C. Andersen,et al.  Ozone and natural systems: understanding exposure, response, and risk. , 2003, Environment international.

[96]  J. Barnes,et al.  Effects of elevated CO2 and/or O3 on growth, development and physiology of wheat (Triticum aestivum L.) , 1995 .

[97]  D Grill,et al.  Synopsis of the CASIROZ case study: carbon sink strength of Fagus sylvatica L. in a changing environment--experimental risk assessment of mitigation by chronic ozone impact. , 2007, Plant biology.

[98]  R. Matyssek,et al.  Interactions between drought and O3 stress in forest trees. , 2006, Plant biology.

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

[100]  A. Fangmeier,et al.  Air Pollutant Combinations - Significance for Future Impact Assessments on Vegetation , 2002 .

[101]  R. E. Dickson,et al.  Carbon allocation and partitioning in aspen clones varying in sensitivity to tropospheric ozone. , 1995, Tree physiology.

[102]  Wade K. Smith,et al.  The Ecophysiology of Coniferous Forests , 1995 .

[103]  H. Sandermann,et al.  The challenge of making ozone risk assessment for forest trees more mechanistic. , 2008, Environmental pollution.

[104]  T. Schmülling,et al.  Arabidopsis Cytokinin Receptor Mutants Reveal Functions in Shoot Growth, Leaf Senescence, Seed Size, Germination, Root Development, and Cytokinin Metabolism[W] , 2005, The Plant Cell Online.

[105]  A. Lefohn.  Surface-Level Ozone Exposures and Their Effects on Vegetation , 1991 .

[106]  R. Ceulemans,et al.  Chronic ozone exposure affects leaf senescence of adult beech trees: a chlorophyll fluorescence approach. , 2006, Journal of experimental botany.

[107]  Reinhart Ceulemans,et al.  Tansley Review No. 71 Effects of elevated atmospheric CO2on woody plants , 1994 .

[108]  H. Blaschke,et al.  Effects of the extreme drought in 2003 on soil respiration in a mixed forest , 2009, European Journal of Forest Research.

[109]  Rainer Matyssek,et al.  Impairment of gas exchange and structure in birch leaves (Betula pendula) caused by low ozone concentrations , 1991, Trees.

[110]  E. Oksanen,et al.  Ozone exposure results in various carry-over effects and prolonged reduction in biomass in birch (Betula pendula Roth) , 1999 .

[111]  J. Innes,et al.  Ozone and the Forests in Austria and Switzerland , 1997 .

[112]  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 .

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

[114]  G. Wieser,et al.  Effects of Ozone on Conifers in the Timberline Ecotone , 2001 .

[115]  R. Matyssek,et al.  O3 flux-related responsiveness of photosynthesis, respiration, and stomatal conductance of adult Fagus sylvatica to experimentally enhanced free-air O3 exposure. , 2007, Plant biology.

[116]  T. Mikkelsen,et al.  Acceleration of leaf senescence in , 1996 .

[117]  C. Huntingford,et al.  Indirect radiative forcing of climate change through ozone effects on the land-carbon sink , 2007, Nature.

[118]  G. Wieser,et al.  Effects of atmospheric and climate change at the timberline of the Central European Alps , 2009, Annals of Forest Science.

[119]  R. Lindroth,et al.  Altered genotypic and phenotypic frequencies of aphid populations under enriched CO2 and O3 atmospheres , 2005 .

[120]  R. Matyssek,et al.  Stable isotope signatures reflect competitiveness between trees under changed CO2/O3 regimes. , 2010, Environmental pollution.

[121]  T. Holopainen,et al.  Nitrogen availability modifies the ozone responses of Scots pine seedlings exposed in an open-field system. , 2001, Tree physiology.

[122]  M. Tausz,et al.  Free Radical Scavengers and Photosynthetic Pigments in Pinus Cembra L. Needles as Affected by Ozone Exposure , 2001, Biologia Plantarum.

[123]  E. P. McDonald,et al.  Interannual climatic variation mediates elevated CO2 and O3 effects on forest growth , 2006 .

[124]  R. Matyssek,et al.  Nutrition and the ozone sensitivity of birch (Betula pendula) , 1997, Trees.

[125]  R. E. Dickson,et al.  Interacting effects of multiple stresses on growth and physiological processes in northern forests , 2000 .

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

[127]  E. Va,et al.  Interannual climatic variation mediates elevated CO 2 and O 3 effects on forest growth , 2006 .

[128]  A. McLeod.  An open-air system for exposure of young forest trees to sulphur dioxide and ozone , 1995 .

[129]  K. Pregitzer,et al.  Growth and C allocation of Populus tremuloides genotypes in response to atmospheric CO2 and soil N availability. , 1998, The New phytologist.

[130]  C. Scheidegger,et al.  Ozone-induced cytochemical and ultrastructural changes in leaf mesophyll cell walls , 1997 .

[131]  A C Turner,et al.  Environmental pollution. , 1970, Canadian Medical Association journal.

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

[133]  T. Holopainen,et al.  Responses of two birch (Betula pendula Roth) clones to different ozone profiles with similar AOT40 exposure , 2001 .

[134]  Stephen P. Long,et al.  Will elevated CO2 concentrations protect the yield of wheat from O3 damage , 1997 .

[135]  T. Seifert,et al.  Growth of adult Norway spruce (Picea abies [L.] Karst.) and European beech (Fagus sylvatica L.) under free-air ozone fumigation. , 2005, Plant biology.

[136]  J. Fuhrer,et al.  Ozone effects on visible foliar injury and growth of Fagus sylvatica and Viburnum lantana seedlings grown in monoculture or in mixture , 2008 .

[137]  R. Matyssek,et al.  Nutrition and the ozone sensitivity of birch (Betula pendula) , 1997, Trees.

[138]  H. Sandermann,et al.  Impact of Ozone on Trees: an Ecophysiological Perspective , 2003 .

[139]  T. Holopainen,et al.  Interactive effects of elevated ozone and springtime frost on growth and physiology of birch (Betula pendula) in field conditions , 2008, Trees.

[140]  V. Ossipov,et al.  Shift in birch leaf metabolome and carbon allocation during long‐term open‐field ozone exposure , 2007 .

[141]  M. Saurer,et al.  Seasonal growth, δ13C in leaves and stem, and phloem structure of birch (Betula pendula) under low ozone concentrations , 1992, Trees.

[142]  E. Nordheim,et al.  CO2 and O3 Effects on Paper Birch (Betulaceae: Betula papyrifera) Phytochemistry and Whitemarked Tussock Moth (Lymantriidae: Orgyia leucostigma) Performance , 2001 .

[143]  J. Vahala,et al.  Physiological, stomatal and ultrastructural ozone responses in birch (Betula pendula Roth.) are modified by water stress , 1998 .

[144]  S. Yun,et al.  Do elevated ozone and variable light alter carbon transport to roots in sugar maple , 2004 .

[145]  R. Martin,et al.  Stratospheric versus pollution influences on ozone at Bermuda: Reconciling past analyses , 2002 .

[146]  H. Payer,et al.  Assessing the impact of elevated O , 1997 .

[147]  E. Pääkkönen,et al.  Variation in ozone sensitivity among clones of Betula pendula and Betula pubescens. , 1997, Environmental pollution.

[148]  M. Fenn,et al.  Photochemical smog effects in mixed conifer forests along a natural gradient of ozone and nitrogen deposition in the San Bernardino Mountains. , 2003, Environment international.

[149]  R. Matyssek,et al.  ELEVATED CO2 COUNTERACTS THE LIMITATION BY CHRONIC OZONE EXPOSURE ON PHOTOSYNTHESIS IN FAGUS SYLVATICA L. : COMPARISON BETWEEN CHLOROPHYLL FLUORESCENC E AND LEAF GAS EXCHANGE , 1999 .

[150]  Rainer Matyssek,et al.  Quantifying Competitiveness in Woody Plants , 2002 .

[151]  K. Pregitzer,et al.  Soil respiration in northern forests exposed to elevated atmospheric carbon dioxide and ozone , 2006, Oecologia.

[152]  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.

[153]  H. Werner,et al.  Beech Leaf Colonization by the Endophyte Apiognomonia errabunda Dramatically Depends on Light Exposure and Climatic Conditions , 2005, Plant biology.

[154]  A. Noormets,et al.  Photosynthetic parameters and stomatal conductance of aspen under elevated CO2 and O3 as affected by leaf hydraulic properties. Proc. Air Pollution, Global Change and Forests in the New Millennium , 2000 .

[155]  E. Oksanen.  Responses of selected birch (Betula pendula Roth) clones to ozone change over time. , 2003, Plant, cell & environment.

[156]  R. Matyssek,et al.  Effects of chronic elevated ozone exposure on gas exchange responses of adult beech trees (Fagus sylvatica) as related to the within-canopy light gradient. , 2009, Environmental pollution.

[157]  H. Rennenberg,et al.  Tree internal signalling and defence reactions under ozone exposure in sun and shade leaves of European beech (Fagus sylvatica L.) trees. , 2007, Plant biology.

[158]  R. E. Dickson,et al.  Photosynthetic productivity of aspen clones varying in sensitivity to tropospheric ozone. , 1995, Tree physiology.

[159]  H. Pretzsch,et al.  Tree and stand growth of mature Norway spruce and European beech under long-term ozone fumigation. , 2010, Environmental pollution.

[160]  G. D. Hogan,et al.  Growth of five hybrid poplar genotypes exposed to interacting elevated CO 2 and O 3 , 1998 .

[161]  E. Pääkkönen,et al.  Differences in growth, leaf senescence and injury, and stomatal density in birch (Betula pendula Roth.) in relation to ambient levels of ozone in Finland. , 1997, Environmental pollution.

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

[163]  R. Harrington,et al.  Aphid individual performance may not predict population responses to elevated CO2 or O3 , 2004 .

[164]  J. Vahala,et al.  Growth responses and related biochemical and ultrastructural changes of the photosynthetic apparatus in birch (Betula pendula) saplings exposed to low concentrations of ozone. , 1996, Tree physiology.

[165]  R. Ceulemans,et al.  The impact of carbon dioxide and other greenhouse gases on forest ecosystems. Report No. 3 of the IUFRO Task Force on Environmental Change. , 2001 .

[166]  L. Mortensen.  Effects of carbon dioxide concentrations on three grass species grown in mixture in two soil types at different ozone concentrations or temperatures , 1997 .

[167]  S. Wullschleger,et al.  Seasonal patterns of light-saturated photosynthesis and leaf conductance for mature and seedling Quercus rubra L. foliage: differential sensitivity to ozone exposure. , 1994, Tree physiology.

[168]  M. Evans,et al.  Seasonal changes in pollutant transport to the North Pacific: The relative importance of Asian and European sources , 2000 .

[169]  D. Davis,et al.  Physiological and foliar symptom response in the crowns of Prunus serotina, Fraxinus americana and Acer rubrum canopy trees to ambient ozone under forest conditions. , 2005, Environmental pollution.

[170]  R. Matyssek,et al.  Effect of fertilization on ozone-induced changes in the metabolism of birch (Betula pendula) leaves. , 1997, The New phytologist.

[171]  B. Frey,et al.  The effects of ozone and nutrient supply on stomatal response in birch (Betula pendula) leaves as determined by digital image-analysis and X-ray microanalysis. , 1996, The New phytologist.

[172]  G. Wieser,et al.  Effects of ozone and mild drought stress on gas exchange, antioxidants and chloroplast pigments in current-year needles of young Norway spruce [ , 1998 .

[173]  R. Lindroth,et al.  Transgenerational phenotypic plasticity under future atmospheric conditions , 2004 .

[174]  G. Wieser,et al.  Ozone fumigation of Norway spruce at timberline , 1989 .

[175]  D. Grill,et al.  Pigmentgehalte und Gaswechsel von Tief- und Hochlagenfichten nach chronischer Ozonbelastung , 1990, European Journal of Forest Research.

[176]  E. Oksanen.  Increasing Tropospheric Ozone Level Reduced Birch (Betula Pendula) Dry Mass within a Five Years Period , 2001 .

[177]  C. Richardson,et al.  Ozone-Induced Changes in Primary Carbon Metabolism Enzymes of Loblolly Pine Needles* , 1994 .

[178]  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 .

[179]  Impacts of elevated ozone and nitrogen on growth and photosynthesis of European aspen (Populus tremula) and hybrid aspen (P. tremula × Populus tremuloides) clones , 2007 .

[180]  G. Somers,et al.  Ozone impacts on loblolly pine (Pinus taeda L.) grown in a competitive environment. , 2002, Environmental pollution.

[181]  R. Matyssek,et al.  Limitations and perspectives about scaling ozone impacts in trees. , 2001, Environmental pollution.

[182]  P. Rundel.  Stable Isotopes in Ecological Research , 1989, Ecological Studies.

[183]  R. E. Dickson,et al.  Photosynthetic responses of aspen clones to simultaneous exposures of ozone and CO2 , 1996 .

[184]  G. Wieser,et al.  Effects of Ozone and Mild Drought Stress on Total and Apoplastic Guaiacol Peroxidase and Lipid Peroxidation in Current-Year Needles of Young Norway Spruce (Picea abies L., Karst.) , 1996 .

[185]  Graham D. Farquhar,et al.  Carbon Isotope Fractionation and Plant Water-Use Efficiency , 1989 .

[186]  Branch growth and leaf gas exchange of Populus tremula exposed to low ozone concentrations throughout two growing seasons. , 1993, Environmental pollution.

[187]  J. Riikonen,et al.  Northern environment predisposes birches to ozone damage. , 2007, Plant biology.

[188]  Rainer Matyssek,et al.  Age effects on Norway spruce (Picea abies) susceptibility to ozone uptake: a novel approach relating stress avoidance to defense. , 2002, Tree physiology.

[189]  P. Reich,et al.  Relative growth rate in relation to physiological and morphological traits for northern hardwood tree seedlings: species, light environment and ontogenetic considerations , 1993, Oecologia.

[190]  I. Dry,et al.  The Tricarboxylic Acid Cycle in Plant Mitochondria: Its Operation and Regulation , 1985 .

[191]  T. Holopainen,et al.  Influence of nitrogen and phosphorous availability and ozone stress on Norway spruce seedlings. , 2001, Tree physiology.

[192]  R. Matyssek,et al.  Interactions of chronic exposure to elevated CO2 and O3 levels in the photosynthetic light and dark reactions of European beech (Fagus sylvatica) , 1999 .

[193]  V. Fontaine,et al.  Effects of ozone and elevated atmospheric carbon dioxide on carbohydrate metabolism of spruce needles. Catabolic and detoxification pathways , 1998 .

[194]  W. Massman,et al.  Ozone flux to vegetation and its relationship to plant response and ambient air quality standards , 1998 .

[195]  M. Saurer,et al.  The influence of ozone and nutrition on δ13C in Betula pendula , 1995, Oecologia.

[196]  E. Pääkkönen,et al.  The ozone sensitivity of birch (Betula pendula) in relation to the developmental stage of leaves. , 1996, The New phytologist.

[197]  H. Sandermann,et al.  Scaling Up from Molecular to Ecological Processes , 2004 .

[198]  J. Sõber,et al.  Ozone-induced H2 O2 accumulation in field-grown aspen and birch is linked to foliar ultrastructure and peroxisomal activity. , 2004, The New phytologist.

[199]  S. Schneider,et al.  Climate Change 2007 Synthesis report , 2008 .

[200]  M. P. Costella,et al.  A branch exposure chamber for fumigating ponderosa pine to atmospheric pollution , 1991 .

[201]  C. Scheidegger,et al.  Differentiation and structural decline in the leaves and bark of birch (Betula pendula) under low ozone concentrations , 2004, Trees.

[202]  H. Blaschke,et al.  Belowground effects of enhanced tropospheric ozone and drought in a beech/spruce forest (Fagus sylvatica L./Picea abies [L.] Karst). , 2010, Environmental pollution.

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

[204]  R. Grote,et al.  Competitive strategies in adult beech and spruce: space-related foliar carbon investment versus carbon gain , 2005, Oecologia.

[205]  S. Long,et al.  The interactive effects of elevated CO2 and O3 concentration on photosynthesis in spring wheat , 1995, Photosynthesis Research.

[206]  R. Lindroth,et al.  Responses of trembling aspen (Populus tremuloides) phytochemistry and aspen blotch leafminer (Phyllonorycter tremuloidiella) performance to elevated levels of atmospheric CO2 and O3 , 2003 .