Free-Air Exposure Systems to Scale up Ozone Research to Mature Trees

Abstract

Because seedlings and mature trees do not necessarily respond similarly to O₃ stress, it is critically important that exposure systems be developed that allow exposure of seedlings through to mature trees. Here we describe three different O₃ Free-Air Exposure Systems that have been used successfully for exposure at all growth stages. These systems of spatially uniform O₃ release have been shown to provide reliable O₃ exposure with minimal, if any, impact on the microclimate. This methodology offers a welcome alternative to chamber studies which had severe space constraints precluding stand or community-level studies and substantial chamber effects on the microclimate and, hence physiological tree performance.

Key words

Free-air - greenhouse gases - ozone - mature trees - sugar maple (Acer saccharum) - paper birch (Betula papyrifera) - trembling aspen (Populus tremuloides) - European beech (Fagus sylvatica) - Norway spruce (Picea abies) - European white birch (Betula pendula).

References

• 1 Ashmore M. R.. Assessing the future global impacts of ozone on vegetation.  Plant, Cell and Environment. (2005);  28 1-16
• 2 Bahnweg G., Heller W., Stich S., Knappe C., Betz G., Heerdt C., Kehr R. D., Ernst D., Langebartels C., Nunn A. J., Rothenburger J., Schubert R., Wallis P., Muller-Starck G., Werner H., Matyssek R., Sandermann H.. Beech leaf colonization by the endophyte Apiognomonia errabunda dramatically depends on light exposure and climatic conditions.  Plant Biology. (2005);  7 659-669
• 3 Baumgarten M., Werner H., Häberle K.-H., Emberson L. D., Fabian P., Matyssek R.. Seasonal ozone response of mature beech trees (Fagus sylvatica) at high elevation of the Bavarian Forest (Germany) in comparison with young beech in field and phytotron.  Environmental Pollution. (2000);  109 431-442
• 4 Büker P., Emberson L. D., Ashmore M. R., Gambridge H. M., Jacobs C., Massman W. J., Müller J., Nikolov N., Novak K., Kristopher N., Oksanen E., Schaub M., De la Torre D.. Comparison of different stomatal conductance algorithms for ozone flux modelling.  Environmental Pollution. (2006); 
• 5 Cox R. M., Malcolm J. W.. Passive ozone monitoring for forest health assessment.  Water, Air, and Soil Pollution. (1999);  116 339-344
• 6 Dickson R. E., Lewin K. F., Isebrands J. G., Coleman M. D., Heilman W. E., Riemenschneider D. E., Sober J., Host G. E., Zak D. R., Hendrey G. R., Pregitzer K. S., Karnosky D. F.. Forest atmosphere carbon transfer storage-II (FACTS II) - the aspen free-air CO₂ and O₃ enrichment (FACE) project in an overview. USDA Forest Service North Central Research Station, General Tech. Rep. NC‐214. (2000): 68pp
• 7 Felzer B., Reilly J., Melillo J., Kicklighter D., Sarofim M., Wang C., Prinn R., Zhuang Q.. Future effects of ozone on carbon sequestration and climate change policy using a global biogeochemical model.  Climatic Change. (2005);  73 345-373
• 8 Fowler D., Cape J. N., Coyle M., Flechard C., Kuylenstierna J., Hicks K., Derwent D., Johnson C., Stevenson D.. The global exposure of forests to air pollutants.  Water, Air, and Soil Pollution. (1999);  116 5-32
• 9 Fredericksen T. S., Joyce B. J., Skelly J. M., Steiner K. C., Kolb T. E., Kouterick K. B., Savage J. E., Snyder K. R.. Physiology, morphology, and ozone uptake of leaves of black cherry seedlings, saplings and canopy trees.  Environmental Pollution. (1995);  89 273-283
• 10 Fredericksen T. S., Skelly J. M., Steiner K. C., Kolb T. E., Kouterick K. B.. Size mediated foliar response to ozone in black cherry trees.  Environmental Pollution. (1996);  91 53-63
• 11 Grulke N. E., Miller P. R.. Changes in gas exchange characteristics during the life span of giant sequoia: implications for response to current and future concentrations of atmospheric ozone.  Tree Physiology. (1994);  14 659-668
• 12 Häberle K.-H., Reiter I. M., Nunn A. J., Gruppe A., Simon U., Gossner M., Werner H., Leuchner M., Heerdt C., Fabian P., Matyssek R.. KROCO, Freising, Germany: canopy research in a temperate mixed forest of Southern Germany. Basset, Y., Horlyck, V., and Wright, S. J., eds. Studying Forest Canopies from Above: The International Canopy Crane Network. Smithsonian Tropical Research Institute and UNEP (2003): 71-78
• 13 Hanson P. J., Samuelson L. J., Wullschleger S. D., Tabberer T. A., Edwards G. S.. Seasonal patterns of light-saturated photosynthesis and leaf conductance for mature and seedling Quercus rubra L. foliage: differential sensitivity to ozone exposure.  Tree Physiology. (1994);  14 1351-1366
• 14 Heerdt C.. Methoden zum Ozonmonitoring in einem Buchen-, Fichten-Mischbestand unter Free-Air-Ozonbegasung. PhD Thesis, Technische Universität München, in prep. (2006)
• 15 Hendrey G. R., Ellsworth D. S., Lewin K. F., Nagy J.. A free-air enrichment system for exposing tall forest vegetation to elevated atmospheric CO₂.  Global Change Biology. (1999);  5 293-309
• 16 IPCC .A report of working group I of the Intergovernmental Panel on Climate Change. http://www.ipcc.ch/. (2001)
• 17 Kainulainen P., Utriainen J., Holopainen J. K., Oksanen J., Holopainen T.. Influence of elevated ozone and limited nitrogen availability on conifer seedlings in an open-air fumigation system: effects on growth, nutrient content, mycorrhiza, needle ultrastructure, starch and secondary compounds.  Global Change Biology. (2000);  6 345-355
• 18 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
• 19 Karnosky D. F., Gielen B., Ceulemans R., Schlesinger W. H., Norby R. J., Oksanen E., Matyssek R., Hendrey G. R.. FACE systems for studying the impacts of greenhouse gases on forest ecosystems. Karnosky, D. F., Ceulemans, R., Scarascia-Mugnozza, G. E., and Innes, J. L., eds. Impacts of Carbon Dioxide and Other Greenhouse Gases on Forest Ecosystems. CAB International (2001): 297-324
• 20 Karnosky D. F., Zak D. R., Pregitzer K. S., Awmack C. S., Bockheim J. G., Dickson R. E., Hendrey G. R., Host G. E., King J. S., Kopper B. J., Kruger E. L., Kubiske M. E., Lindroth R. L., Mattson W. J., McDonald E. P., Noormets A., Oksanen E., Parsons W. F. J., Percy K. E., Podila G. K., Riemenschneider D. E., Sharma P., Thakur R. C., Sober A., Sober J., Jones W. S., Anttonen S., Vapaavuori E., Mankovska B., Heilman W. E., Isebrands J. G.. Tropospheric O₃ moderates responses of temperate hardwood forests to elevated CO₂: a synthesis of molecular to ecosystem results from the Aspen FACE project.  Functional Ecology. (2003);  17 289-304
• 21 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
• 22 Karnosky D. F., Skelly J. M., Percy K. E., Chappelka A. H.. Perspectives regarding 50 years of research on effects of tropospheric ozone air pollution on U.S. forests.  Environmental Pollution. (2006); 
• 23 Kolb T. E., Matyssek R.. Limitations and perspectives about scaling ozone impacts in trees.  Environmental Pollution. (2001);  115 373-393
• 24 Leuchner M., Fabian P., Werner H.. Spectral multichannel monitoring of radiation within a mature mixed forest.  Plant Biology. (2005);  7 619-627
• 25 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);  20 539-548
• 26 Matyssek R., Schnyder H., Elstner E.-F., Munch J.-C., Pretzsch H., Sandermann H.. Growth and parasite defence in plants: the balance between resource sequestration and retention.  Plant Biology. (2002);  4 133-136
• 27 Matyssek R., Häberle K.-H.. Freising canopy crane, Germany. Mitchell, A. M., Secoy, K., and Jackson, T., eds. The Global Canopy Handbook. Oxford, UK; GCP Publisher (2002): 47-50
• 28 Matyssek R., Agerer R., Ernst D., Munch J.-C., Osswald W., Pretzsch H., Priesack H., Schnyder H., Treutter D.. The plant's capacity in regulating resource demand.  Plant Biology. (2005);  7 560-580
• 29 Matyssek R., Innes J. L.. Ozone - a risk factor for forest trees and forests in Europe?.  Water, Air and Soil Pollution. (1999);  116 199-226
• 55 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
• 30 Norby R. J., Wullschleger S. D., Gunderson C. A., Johnson D. W., Ceulemans R.. Tree responses to rising CO₂ in field experiments: implications for the future forests.  Plant, Cell and Environment. (1999);  22 683-714
• 31 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
• 32 Nunn A. J., Reiter I. M., Häberle K.-H., Langebartels C., Bahnweg G., Pretzsch H., Sandermann H., Matyssek R.. Response pattern in adult forest trees to chronic ozone stress: identification of variations and consistencies.  Environmental Pollution. (2005 a);  136 365-369
• 33 Nunn A. J., Kozovits A. R., Reiter I. M., Heerdt C., Leuchner M., Lütz C., Liu X., Winkler J. B., Grams T. E. E., Häberle K.-H., Werner H., Fabian P., Rennenberg G. H., Matyssek R.. Comparison of ozone uptake and responsiveness between a phytotron study with young and a field experiment with adult beech (Fagus sylvatica).  Environmental Pollution. (2005 b);  137 494-506
• 34 Nunn A. J., Anegg S., Betz G., Simons S., Kalisch G., Seidlitz H. K., Grams T. E. E., Häberle K.-H., Matyssek R., Bahnweg S., Sandermann H., Langebartels C.. Role of ethylene in the regulation of cell death and leaf loss in ozone-exposed European beech.  Plant, Cell and Environment. (2005 c);  28 886-897
• 35 Nunn A. J., Wieser G., Reiter I. M., Häberle K.-H., Grote R., Havranek W. M., Matyssek R.. Testing the “unifying theory” for O₃ sensitivity with mature forest tree responses (Fagus sylvatica and Picea abies). .  Tree Physiology. (2006);  26 1391-1403
• 36 Oksanen E.. 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.  Tree Physiology. (2003 a);  23 603-614
• 37 Oksanen E.. Responses of selected birch (Betula pendula Roth.) clones to ozone change over time.  Plant, Cell and Environment. (2003 b);  26 875-886
• 38 Oksanen E., Kontunen-Soppela S., Riikonen J., Peltonen P., Uddling J., Vapaavuori E.. Northern environment predisposes birches to ozone damage.  Plant Biology. (2007);  9 191-196
• 39 Percy K. E., Legge A. H., Krupa S. V.. Tropospheric ozone: a continuing threat to global forests?. Karnosky, D. F., Percy, K. E., Chappelka, A. H., Simpson, C., and Pikkarainen, J., eds. Air Pollution, Global Change and Forests in the New Millennium, Vol. 3. Amsterdam; Elsevier (2003): 85-118
• 40 Percy K., Nosal M., Heilman W., Dann T., Sober J., Legge A., Karnosky D. F.. New exposure-based metric for evaluating O₃ risk to North American aspen forests.  Environmental Pollution. (2006); 
• 41 Pretzsch H., Kahn M., Grote R.. Die Fichten-Buchen-Mischbestände des Sonderforschungsbereiches „Wachstum oder Parasitenabwehr?“ im Kranzberger Forst.  Forstwissenschaftliches Centralblatt. (1998);  117 241-257
• 42 Reich P. B.. Quantifying plant response to ozone: a unifying theory.  Tree Physiology. (1987);  3 63-91
• 43 Reiter I. M., Häberle K.-H., Nunn A. J., 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
• 44 Reitmayer H., Werner H., Fabian P.. A novel system for spectral analysis of solar radiation within a mixed beech-spruce stand.  Plant Biology. (2002);  4 228-233
• 45 Samuelson L. J., Edwards G. S.. A comparison of sensitivity to ozone in seedlings and trees of Quercus rubra L.  New Phytologist. (1993);  128 373-379
• 46 Samuelson L. J., Kelly J. M.. Carbon partitioning and allocation in northern red oak seedlings and mature trees in response to ozone.  Tree Physiology. (1996);  16 853-858
• 47 Samuelson L., Kelly J. M.. Scaling ozone effects from seedlings to forest trees.  New Phytologist. (2001);  149 21-41
• 48 Schaub M., Skelly J. M., Zhang J. W., Ferdinand J. A., Savage J. E., Stevenson R. E., Davis D. D., Steiner K. C.. Physiological and foliar symptom response in the crowns of Prunus serotina, Fraxinus americana, and Acer rubrum canopy trees to ambient ozone under forest conditions.  Environmental Pollution. (2005);  133 553-567
• 49 Uddling J., Günthardt-Goerg M. S., Matyssek R., Oksanen E., Pleijel H., Selldén G., Karlsson P. E.. Biomass reductions of juvenile birch were more strongly related to stomatal uptake of ozone than to ozone indices based on external exposure.  Atmospheric Environment. (2004);  38 4709-4719
• 50 Utriainen J., Holopainen T.. The influence of nitrogen and phosphorus availability in ozone stress of Norway spruce seedlings.  Tree Physiology. (2001 a);  21 447-456
• 51 Utriainen J., Holopainen T.. Nitrogen availability modifies the ozone responses of Scots pine seedlings exposed in open field system.  Tree Physiology. (2001 b);  21 1205-1213
• 52 Werner H.. Das Indigopapier. Sensitives Element zum Aufbau von Passivsammlern zur Messung von Ozonimmissionen. Schriftenreihe der Forstwissenschaftlichen Fakultät der Universität München und der Bayerischen Landesanstalt für Wald und Forstwirtschaft. Forstl. Forschungsberichte München. (1992)
• 53 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. (2002);  9 117-121
• 54 Wieser G., Tegischer K., Tausz M., Häberle K.-H., Grams T. E. E., Matyssek R.. Age effects on Norway spruce (Picea abies) susceptibility to ozone uptake: a novel approach relating stress avoidance to defense.  Tree Physiology. (2002);  22 583-590

Editor: H. Rennenberg