Download PDF
Plant Biol (Stuttg) 2007; 9(2): 181-190
DOI: 10.1055/s-2006-955915
Review Article

Georg Thieme Verlag Stuttgart KG · New York

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

D. F. Karnosky1 , H. Werner2 , T. Holopainen3 , K. Percy4 , T. Oksanen3 , E. Oksanen3 , 5 , C. Heerdt2 , P. Fabian2 , J. Nagy6 , W. Heilman7 , R. Cox4 , N. Nelson8 , R. Matyssek9
  • 1School of Forest Resources and Environmental Science, Michigan Technological University, 1400 Townsend Drive, Houghton, MI 49931, USA
  • 2Department of Ecology, Ecoclimatology, Technical University of Munich, Am Hochanger 13, 85354 Freising-Weihenstephan, Germany
  • 3Ecological Laboratory, Department of Environmental Science, University of Kuopio, 70211 Kuopio, Finland
  • 4NRCAN Canadian Forest Service - Atlantic Forestry Centre, P.O. Box 4000, Fredericton, New Brunswick E3B 5P7, Canada
  • 5Department of Biology, University of Joensuu, P.O. Box 111, 80101 Joensuu, Finland
  • 6Brookhaven National Laboratory, 30 Bell Avenue, Upton 11973, New York, USA
  • 7USDA Forest Service, 1407 S. Harrison Road, East Lansing, MI 48823, USA
  • 8USDA Forest Service, Forestry Sciences Laboratory, 5985 Hwy. K, Rhinelander, WI 54501, USA
  • 9Department of Ecology, Ecophysiology of Plants, Technical University of Munich, Am Hochanger 13, 85354 Freising-Weihenstephan, Germany
Further Information

Publication History

Received: July 5, 2006

Accepted: October 30, 2006

Publication Date:
13 March 2007 (online)

   Permissions and Reprints

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
    CrossrefPubMedGoogle Scholar
  • 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
    Article in Thieme ConnectPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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); 
    PubMedGoogle Scholar
  • 5 Cox R. M., Malcolm J. W.. Passive ozone monitoring for forest health assessment.  Water, Air, and Soil Pollution. (1999);  116 339-344
    CrossrefPubMedGoogle Scholar
  • 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
    Google Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    Google Scholar
  • 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
    PubMedGoogle Scholar
  • 14 Heerdt C.. Methoden zum Ozonmonitoring in einem Buchen-, Fichten-Mischbestand unter Free-Air-Ozonbegasung. PhD Thesis, Technische Universität München, in prep. (2006)
    Google Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 16 IPCC .A report of working group I of the Intergovernmental Panel on Climate Change. http://www.ipcc.ch/. (2001)
    Google Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    Google Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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); 
    PubMedGoogle Scholar
  • 23 Kolb T. E., Matyssek R.. Limitations and perspectives about scaling ozone impacts in trees.  Environmental Pollution. (2001);  115 373-393
    CrossrefPubMedGoogle Scholar
  • 24 Leuchner M., Fabian P., Werner H.. Spectral multichannel monitoring of radiation within a mature mixed forest.  Plant Biology. (2005);  7 619-627
    Article in Thieme ConnectPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    Article in Thieme ConnectPubMedGoogle Scholar
  • 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
    Google Scholar
  • 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
    Article in Thieme ConnectPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    Article in Thieme ConnectPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    Article in Thieme ConnectPubMedGoogle Scholar
  • 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
    Google Scholar
  • 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); 
    PubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 42 Reich P. B.. Quantifying plant response to ozone: a unifying theory.  Tree Physiology. (1987);  3 63-91
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    Article in Thieme ConnectPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 47 Samuelson L., Kelly J. M.. Scaling ozone effects from seedlings to forest trees.  New Phytologist. (2001);  149 21-41
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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)
    Google Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar

D. F. Karnosky

School of Forest Resources and Environmental Science
Michigan Technological University

1400 Townsend Drive

Houghton, MI 49931

USA

Email: karnosky@mtu.edu

Editor: H. Rennenberg