O₃ Flux-Related Responsiveness of Photosynthesis, Respiration, and Stomatal Conductance of Adult Fagus sylvatica to Experimentally Enhanced Free-Air O₃ Exposure

Abstract

Knowledge of responses of photosynthesis, respiration, and stomatal conductance to cumulative ozone uptake (COU) is still scarce, and this is particularly the case for adult trees. The effect of ozone (O₃) exposure on trees was examined with 60-year-old beech trees (Fagus sylvatica) at a forest site of southern Germany. Trees were exposed to the ambient O₃ regime (1 × O₃) or an experimentally elevated twice-ambient O₃ regime (2 × O₃). The elevated 2 × O₃ regime was provided by means of a free-air O₃ canopy exposure system. The hypotheses were tested that (1) gas exchange is negatively affected by O₃ and (2) the effects of O₃ are dose-dependent and thus the sizes of differences between treatments are positively related to COU. Gas exchange (light-saturated CO₂ uptake rate A_max, stomatal conductance g_s, maximum rate of carboxylation Vc_max, ribulose-1,5-bisphosphate turnover limited rate of photosynthesis J_max, CO₂ compensation point CP, apparent quantum yield of net CO₂ uptake AQ, carboxylation efficiency CE, day- and nighttime respiration) and chlorophyll fluorescence (electron transfer rate, ETR) were measured in situ on attached sun and shade leaves. Measurements were made periodically throughout the growing seasons of 2003 (an exceptionally dry year) and 2004 (a year with average rainfall). In 2004 Vc_max, J_max, and CE were lower in trees receiving 2 × O₃ compared with the ambient O₃ regime (1 × O₃). Treatment differences in Vc_max, J_max, CE were rather small in 2004 (i.e., parameter levels were lower by 10 - 30 % in 2 × O₃ than 1 × O₃) and not significant in 2003. In 2004 COU was positively correlated with the difference between treatments in A_max, g_s, and ETR (i.e., consistent with the dose-dependence of O₃’s deleterious effects). However, in 2003, differences in A_max, g_s, and ETR between the two O₃ regimes were smaller at the end of the dry summer 2003 (i.e., when COU was greatest). The relationship of COU with effects on gas exchange can apparently be complex and, in fact, varied between years and within the growing season. In addition, high doses of O₃ did not always have significant effects on leaf gas exchange. In view of the key findings, both hypotheses were to be rejected.

Key words

Ozone flux - photosynthesis - stomatal conductance - Fagus sylvatica - drought - free-air ozone exposure - dose response

References

• 1 Amthor J. S.. Growth and maintenance respiration in leaves of bean (Phaseolus vulgaris L.) exposed to ozone on open-top chambers in the field.  New Phytologist. (1988);  110 319-325
• 2 Ashmore M. R.. Assessing the future global impacts of ozone on vegetation.  Plant, Cell and Environment. (2005);  28 949-964
• 3 Bazzaz F. A.. Allocation of resources in plants: state of the science and critical questions. Bazzaz, F. A., ed. Plant Resource Allocation. London; Academic Press (1997): 303
• 4 Bernacchi C. J., Singsaas E. L., Pimentel C., Portis A. R., Long S. P.. Improved temperature response functions for models of Rubisco-limited photosynthesis.  Plant, Cell and Environment. (2001);  24 253-259
• 5 Blumenröther M. C., Löw M., Matyssek R., Oßwald W.. Flux-based response of sucrose and starch in leaves of adult beech trees (Fagus sylvatica L.) under chronic free-air O₃ fumigation.  Plant Biology. (2007);  9 207-214
• 6 Bortier K., De Temmerman L., Ceulemans R.. Effects of ozone exposure in open-top chambers on poplar (Populus nigra) and beech (Fagus sylvatica): a comparison.  Environmental Pollution. (2000);  109 509-516
• 7 CLRTAP (ed.) .Mapping Manual. Convention on Long-Range Transboundary Air Pollution. (2004)
• 8 De Temmerman L. D., Vandermeiren K., D'Haese D., Bortier K., Asard H., Ceulemans R.. Ozone effects on trees, where uptake and detoxification meet.  Dendrobiology. (2002);  47 9-19
• 9 Deckmyn G., Op de Beeck M., Löw M., Then C., Verbeeck H., Wipfler P., Ceulemans R.. Modelling ozone effects on adult beech trees through simulation of defence, damage, and repair costs: implementation of the CASIROZ ozone model in the ANAFORE forest model.  Plant Biology. (2007);  9 320-330
• 10 Dizengremel P.. Effects of ozone on the carbon metabolism of forest trees.  Plant Physiology and Biochemistry. (2001);  39 729-742
• 11 Edwards G. S., Wullschleger S. D., Kelly J. M.. Growth and physiology of northern red oak - preliminary comparisons of mature tree and seedling responses to ozone.  Environmental Pollution. (1994);  83 215-221
• 12 Emberson L., Ashmore M., Cambridge H., Simpson D., Tuovinen J.. Modelling stomatal ozone flux across Europe.  Environmental Pollution. (2000);  109 403-413
• 13 Farquhar G. D., Caemmerer S. V., Berry J. A.. A biochemical-model of photosynthetic CO₂ assimilation in leaves of C₃ species.  Planta. (1980);  149 78-90
• 14 Farquhar G. D., Sharkey T. D.. Stomatal conductance and photosynthesis.  Annual Review of Plant Physiology and Plant Molecular Biology. (1982);  33 317-345
• 15 Fuhrer J., Skärby L., Ashmore M. R.. Critical levels for ozone effects on vegetation in Europe.  Environmental Pollution. (1997);  97 91-106
• 16 Giles J.. Hikes in surface ozone could suffocate crops.  Nature. (2005);  435 7
• 17 Grassi G., Magnani F.. Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees.  Plant, Cell and Environment. (2005);  28 834-849
• 18 Haberer K., Herbinger K., Alexou M., Tausz M., Rennenberg H.. Antioxidative defence of old growth beech (Fagus sylvatica) under double ambient O₃ concentrations in a free-air exposure system.  Plant Biology. (2007);  9 215-226
• 19 Harley P. C., Thomas R. B., Reynolds J. F., Strain B. R.. Modeling photosynthesis of cotton grown in elevated CO₂.  Plant, Cell and Environment. (1992);  15 271-282
• 20 Herbinger K., Then C., Löw M., Haberer K., Alexous M., Koch N., Remele K., Heerdt C., Grill D., Rennenberg H.. Tree age dependence and within-canopy variation of leaf gas exchange and antioxidative defence in Fagus sylvatica under experimental free-air ozone exposure.  Environmental Pollution. (2005);  137 476-482
• 21 Karlsson P. E., Uddling J., Braun S., Broadmeadow M., Elvira S., Gimeno B. S., Le Thiec D., Oksanen E., Vandermeiren K., Wilkinson M., Emberson L.. New critical levels for ozone effects on young trees based on AOT40 and simulated cumulative leaf uptake of ozone.  Atmospheric Environment. (2004);  38 2283-2294
• 22 Karnosky D. F., Pregitzer K. S., Zak D. R., Kubiske M. E., Hendrey G. R., Weinstein D., Nosal M., Percy K. E.. Scaling ozone responses of forest trees to the ecosystem level in a changing climate.  Plant, Cell and Environment. (2005);  28 965-981
• 23 Karnosky D. F., Werner H., Holopainen T., Percy K., Oksanen T., Oksanen E., Heerdt C., Fabian P., Nagy J., Heilman W., Cox R., Nelson N., Matyssek R.. Free-air exposure systems to scale up ozone research to mature trees.  Plant Biology. (2007);  9 181-190
• 24 Koike T.. Autumn coloring, photosynthetic performance and leaf development of deciduous broad-leaved trees in relation to forest succession.  Tree Physiology. (1990);  7 21-32
• 25 Kolb T. E., Matyssek R.. Limitations and perspectives about scaling ozone impacts in trees.  Environmental Pollution. (2001);  115 373-393
• 26 Körner C.. Carbon limitation in trees.  Journal of Ecology. (2003);  91 4-17
• 27 Kronfuss G., Polle A., Tausz M., Havranek W.-M., Wieser G.. 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.).  Trees. (1998);  12 482-489
• 28 Leuschner C., Backes K., Hertel D., Schipka F., Schmitt U., Terborg O., Runge M.. Drought responses at leaf, stem and fine root levels of competitive Fagus sylvatica L. and Quercus petraea (Matt.) Liebl. trees in dry and wet years.  Forest Ecology and Management. (2001);  149 33-46
• 29 Löw M., Herbinger K., Nunn A. J., Häberle K.-H., Leuchner M., Heerdt C., Werner H., Wipfler P., Pretzsch H., Tausz M., Matyssek R.. Extraordinary drought of 2003 overrules ozone impact on adult beech trees (Fagus sylvatica).  Trees. (2006);  DOI: 10.1007/s00468-006-0069-z
• 30 Matyssek R., Agerer R., Ernst D., Munch J. C., Osswald W., Pretzsch H., Priesack E., Schnyder H., Treutter D.. The plant's capacity in regulating resource demand.  Plant Biology. (2005);  7 560-580
• 31 Matyssek R., Bahnweg G., Ceulemans R., Fabian P., Grill D., Hanke D. E., Kraigher H., Oßwald W., Rennenberg H., Sandermann H., Tausz M., Wieser G.. 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.  Plant Biology. (2007);  9 163-180
• 32 Matyssek R., Bytnerowicz A., Karlsson P.-E., Paoletti E., Sanz M., Schaub M., Wieser G.. Promoting the O₃ flux concept for European forest trees.  Environmental Pollution. (2006 a); 
• 59 Matyssek R., Günthardt-Goerg M. S., Keller T., Scheidegger C.. Impairment of gas-exchange and structure in birch leaves (Betula pendula) caused by low ozone concentrations.  Trees. (1991);  5 5-13
• 33 Matyssek R., Le Thiec D., Löw M., Dizengremel P., Nunn A. J., Häberle K.-H.. Drought stress in the presence of O₃ impact on forest trees.  Plant Biology. (2006 b);  8 11-17
• 34 Matyssek R., Sandermann H.. Impact of ozone on trees: an ecophysiological perspective.  Progress in Botany. (2003);  64 349-404
• 35 Matyssek R., Wieser G., Nunn A. J., Kozovits A. R., Reiter I. M., Heerdt C., Winkler J. B., Baumgarten M., Häberle K.-H., Grams T. E. E.. Comparison between AOT40 and ozone uptake in forest trees of different species, age and site conditions.  Atmospheric Environment. (2004);  38 2271-2281
• 60 Maurer S., Matyssek R., Günthardt-Goerg M. S., Landolt W., Einig W.. Nutrition and the ozone sensitivity of birch (Betula pendula). I. Responses at the leaf level.  Trees. (1997);  12 1-10
• 36 Medical Dictionary. Weinheim; Wileys Publishers (2003)
• 37 Musselman R. C., Lefohn A. S., Massman W. J., Heath R. L.. A critical review and analysis of the use of exposure- and flux-based ozone indices for predicting vegetation effects.  Atmospheric Environment. (2006);  40 1869-1888
• 38 Novak K., Schaub M., Fuhrer J., Skelly J. M., Hug C., Landolt W., Bleuler P., Krauchi N.. Seasonal trends in reduced leaf gas exchange and ozone-induced foliar injury in three ozone sensitive woody plant species.  Environmental Pollution. (2005);  136 33-45
• 39 Nunn A. J., Kozovits A. R., Reiter I. M., Heerdt C., Leuchner M., Lütz C., Liu X., Löw M., Winkler J. B., Grams T. E. E., Matyssek R.. Comparison of ozone uptake and sensitivity between a phytotron study with young beech and a field experiment with adult beech (Fagus sylvatica).  Environmental Pollution. (2005 a);  137 494-506
• 40 Nunn A. J., Reiter I. M., Häberle K.-H., Langebartels C., Bahnweg G., Pretzsch H., Sandermann H., Matyssek R.. Response patterns in adult forest trees to chronic ozone stress: identification of variations and consistencies.  Environmental Pollution. (2005 b);  136 365-369
• 41 Nunn A. J., Reiter I. M., Häberle K.-H., Werner H., Langebartels C., Sandermann H., Heerdt C., Fabian P., Matyssek R.. “Free air” ozone canopy fumigation in an old-growth mixed forest: concept and observations in beech.  Phyton. (2002);  42 105-119
• 42 Panek J. A., Kurpius M. R., Goldstein A. H.. An evaluation of ozone exposure metrics for a seasonally drought-stressed ponderosa pine ecosystem.  Environmental Pollution. (2002);  117 93-100
• 43 Peñuelas J., Ribas-Carbó M., González-Meler M., Azcón-Bieto J.. Water status, photosynthetic pigments, C/N ratios and respiration rates of sitka spruce seedling exposed to 70 ppbv ozone for a summer.  Environmental and Experimental Botany. (1994);  34 443-449
• 44 Pleijel H., Danielsson H., Ojanpera K., De Temmerman L., Hogy P., Badiani M., Karlsson P. E.. Relationships between ozone exposure and yield loss in European wheat and potato - a comparison of concentration- and flux-based exposure indices.  Atmospheric Environment. (2004);  38 2259-2269
• 45 Polle A., Schwanz P., Rudolf C.. Developmental and seasonal changes of stress responsiveness in beech leaves (Fagus sylvatica L.).  Plant, Cell and Environment. (2001);  24 821-829
• 46 Pretzsch H., Kahn M., Grote R.. Die Fichten-Buchen-Mischbestände des Sonderforschungsbereiches „Wachstum oder Parasitenabwehr?“ im Kranzberger Forst.  Forstwissenschaftliches Centralblatt. (1998);  117 241-257
• 61 Reich P. B.. Effects of low concentrations of O₃ on net photosynthesis, dark respiration, and chlorophyll contents in aging hybrid poplar leaves.  Plant Physiology. (1983);  73 291-296
• 47 Reiter I., Häberle K.-H., Nunn A., Heerdt C., Reitmayer H., Grote R., Matyssek R.. Competitive strategies in adult beech and spruce: space-related foliar carbon investment versus carbon gain.  Oecologia. (2005);  146 337-349
• 48 Riikonen J., Holopainen T., Oksanen E., Vapaavuori E.. Leaf photosynthetic characteristics of silver birch during three years of exposure to elevated concentrations of CO₂ and O₃ in the field.  Tree Physiology. (2005);  25 621-632
• 49 Sandermann H., Matyssek R.. Scaling up from molecular to ecological processes. Sandermann, H., ed. Molecular Ecotoxicology of Plants. Berlin, Heidelberg, New York; Springer-Verlag (2004): 207-226
• 50 Schär C., Jendritzky G.. Climate change: hot news from summer 2003.  Nature. (2004);  432 559-560
• 51 Uddling J., Günthardt-Goerg M. S., Matyssek R., Oksanen E., Pleijel H., Sellden G., Karlsson P. E.. Biomass reduction of juvenile birch is more strongly related to stomatal uptake of ozone than to indices based on external exposure.  Atmospheric Environment. (2004);  38 4709-4719
• 52 Uemura A., Ishida A., Tobias D. J., Koike N., Matsumoto Y.. Linkage between seasonal gas exchange and hydraulic acclimation in the top canopy leaves of Fagus trees in a mesic forest in Japan.  Trees. (2004);  18 452-459
• 53 Velikova V., Tsonev T., Pinelli P., Alessio G. A., Loreto F.. Localized ozone fumigation system for studying ozone effects on photosynthesis, respiration, electron transport rate and isoprene emission in field-grown Mediterranean oak species.  Tree Physiology. (2005);  25 1523-1532
• 54 Warren C. R., Löw M., Matyssek R., Tausz M.. Internal conductance to CO₂ transfer of adult Fagus sylvatica: variation between sun and shade leaves and due to free-air ozone fumigation.  Environmental and Experimental Botany. (2006);  DOI: 10.1016/j.envexpbot.2005.1011.1004
• 55 Werner H., Fabian P.. Free-air fumigation of mature trees: a novel system for controlled ozone enrichment in grown-up beech and spruce canopies.  Environmental Science and Pollution Research International. (2002);  9 117-121
• 56 Wieser G., Tausz M.. Critical levels for ozone: further applying and developing the flux concept. UNECE Workshop report. Wieser, G. and Tausz, M., eds. UNECE Workshop Obergurgl. Wien, Austria; BFW (2005)
• 57 Wilson K.-B., Baldocchi D.-D., Hanson P.-J.. Quantifying stomatal and non-stomatal limitations to carbon assimilation resulting from leaf aging and drought in mature deciduous tree species.  Tree Physiology. (2000);  20 787-797
• 58 Wipfler P., Seifert T., Heerdt C., Werner H., Pretzsch H.. Growth of adult Norway spruce (Picea abies [L.] Karst.) and European beech (Fagus sylvatica L.) under free-air ozone fumigation.  Plant Biology. (2005);  7 611-618

Editor: H. Rennenberg