Advertisement

Water, Air, and Soil Pollution

, Volume 185, Issue 1–4, pp 239–254 | Cite as

Foliar, Physiologial and Growth Responses of Four Maple Species Exposed to Ozone

  • Vicent CalatayudEmail author
  • Júlia Cerveró
  • María José Sanz
Article

Abstract

The effects of ozone in four maple species, Acer campestre, A. opalus subsp. granatense, A. monspessulanum and A. pseudoplatanus were studied in OTC under two different experimental conditions: in charcoal filtered air (CF), and in non filtered air plus 30 ppb ozone (NF+30). The four species of maple showed contrasting sensitivity to ozone as demonstrated by visible injury development, gas exchange and chlorophyll a fluorescence, and growth measurements. Plant injury index (i.e. a combination of percentage of injured leaves and leaf surface affected) was more consistently related with physiological measurements than the onset of first symptom of visible injury. Differences in ozone sensitivity among species may be partly related to higher stomatal conductances in A. opalus and A. pseudoplatanus. In these two species, ozone produced significant reductions in CO2 assimilation under saturating light conditions (A sat), stomatal conductance (g s), transpiration rate (T r) and Water Use Efficiency (WUE) (the latter also significantly declined in A. campestre) towards the end of summer, while intercellular CO2 concentrations (C i) increased significantly. In asymptomatic leaves of A. opalus, neither stomatal limitation nor photoinhibitory damage (F v/F m) could explain the observed decline of A sat, and photosynthesis was down regulated by reducing the proportion of absorbed energy used in photochemistry (Φ PSII) at expenses of the energy dispersed non-photochemically (NPQ). Leaf N content also declined significantly in A. pseudoplatanus. Plants exposed to ozone showed a tendency to decrease growth, but it was not significant within the exposure period for any of the four species. The most sensitive species were A. opalus and A. pseudoplatanus, while the species with the smallest and more coriaceous leaves, A. monspessulanum, was the most resistant.

Keywords

Ozone Visible injury Oxidative stress Photosynthesis Fluorescence Chlorophyll C/N 

Abbreviations

Asat

light saturated CO2 assimilation

AOT40

accumulated exposure over threshold 40 ppb

Ci

intercellular CO2 concentrations

CSTR

Continuously Stirred Tank Reactors

DSF

days after starting of fumigation

Φexc

quantum efficiency of excitation capture by oxidized reaction centers of PSII

ΦPSII

quantum yield of electron transfer at PSII

Fm

maximum fluorescence

\( F^{\prime }_{{\text{m}}} \)

maximum fluorescence in the light adapted state

Fo

minimal fluorescence

\( F^{\prime }_{{\text{o}}} \)

minimum fluorescence in the light-adapted state

Fs

modulated fluorescence yield at steady state

Fv/Fm

maximum quantum efficiency of photosystem II (PSII) primary photochemistry

gs

stomatal conductance to water vapor

NPQ

quenching due to non-photochemical dissipation of absorved light energy

OTC

open top chamber

PPFD

photosynthetic photon flux density

qp

coefficient for photochemical quenching.

RHGR

relative height growth rate

Tr

transpiration rate

VPD

leaf-to-air water vapor pressure deficit

WUE

water Use Efficiency, calculated as A sat/T r

Notes

Acknowledgements

M.J.S. and V.C. thank the DGCN (MMA), and Conselleria de Territori i Habitatge (project FORMEDOZON, Interreg III B) for funding this study, and to Generalitat Valenciana and Bancaixa for continuous support to Fundación CEAM. This work has been carried out in connection with the activities of the Working Group of Ambient Air Quality of ICP-Forests. Esperanza Calvo is acknowledged for fruitful discussions on the article. Carmen Martín is thanked for taking care of the plants. José Reig-Armiñana and Francisco García-Breijo are also thanked for information on the anatomical traits of the plants. Ana Bucher helped with the C and N analyses.

References

  1. Ashmore, M. R. (2005). Assessing the future global impacts of ozone vegetation. Plant, Cell and Environment, 28, 949–964.CrossRefGoogle Scholar
  2. Baier, M., Kandlbinder, A., Golldack, D., & Dietz, K.-J. (2005). Oxidative stress and ozone: Perception, signalling and response. Plant, Cell and Environment, 28, 1012–1020.CrossRefGoogle Scholar
  3. Baker, T. R., Allen, H. L., Schoeneberger, M. M., & Kress, L. W. (1994). Nutritional response of loblolly pine exposed to ozone and simulated acid rain. Canadian Journal of Forest Research, 24, 453–461.Google Scholar
  4. Barnes, J. D., Balaguer, L., Manrique, E., Elvira, S., & Davison, A. W. (1992). A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants. Environmental and Experimental Botany, 32, 85–100.CrossRefGoogle Scholar
  5. Black, V. J., Black, C. R., Roberts, J. A., & Stewart, C. A. (2000). Impact of ozone on the reproductive development of plants. Tansley Review for New Phytologist, 147, 421–447.CrossRefGoogle Scholar
  6. Brendley, B. W., & Pell, E. J. (1998). Ozone-induced changes in biosynthesis of Rubisco and associated compensation to stress in foliage of hybrid poplar. Tree Physiology, 18, 81–90.Google Scholar
  7. Bussotti, F., Agati, G., Desotgiu, R., Matteini, P., & Tani, C. (2005). Ozone foliar symptoms in woody plant species assessed with ultrastructural and fluorescence analysis. New Phytologist, 166, 941–955.CrossRefGoogle Scholar
  8. Bussotti, F., & Ferretti, M. (1998). Air pollution, forest condition and forest declines in southern europe. An overview. Environmental Pollution, 101, 49–65.CrossRefGoogle Scholar
  9. Cabezudo, B., & Talavera, S. (coordinators) (2005). Lista roja de la flora vascular de Andalucía. Junta de Andalucía, Sevilla, 83 p.Google Scholar
  10. Calatayud, A., Iglesias, D., Talón, M., & Barreno, E. (2003). Effects of 2-month ozone exposure in spinach leaves on photosynthesis, antioxidant systems and lipid peroxidation. Plant Physiology & Biochemistry, 41, 839–845.CrossRefGoogle Scholar
  11. Chappelka, A. H., & Chevone, B. I. (1992). Tree responses to ozone. In A. S. Lefohn (Ed.), Surface-level ozone exposures and their effects on vegetation (pp. 271–324). Chelsea, MI: Lewis.Google Scholar
  12. Chappelka, A. H., & Samuelson, L. J. (1998). Ambient ozone effects on forest trees of the eastern United States: A review. New Phytologist, 139, 91–108.CrossRefGoogle Scholar
  13. Dann, M. S., & Pell, E. J. (1989). Decline of activity and quantity of ribulose bisphosphate carboxylase/oxygenase and net photosynthesis in ozone-treated potato foliage. Plant Physiology, 91, 427–432.Google Scholar
  14. De Kok, L. J., & Tausz, M. (2001). The role of glutathione in plant reaction and adaptation to air pollutants. In D. Grill, M. Tausz, & L. J. De Kok (Eds.), Significance of glutathione to plant adaptation to the environment (pp. 185–208). Amsterdam: Kluwer.Google Scholar
  15. de Vries, W., Reinds, G. J., Posh, M., Sanz, M. J., Krause, G., Calatayud, V., et al. (2003). Intensive monitoring of forest ecosystems in Europe, 2003. Technical Report. EC-UN/ECE, Brussels, Geneva (ISSN 1020-6078).Google Scholar
  16. Enyedi, A. J., Eckardt, N. A., & Pell, E. J. (1992). Activity of ribulose bisphosphate carboxylase/oxygenase from potato cultivars with differential response to ozone stress. New Phytologist, 122, 493–500.CrossRefGoogle Scholar
  17. EU European Union (2002). Directive 2002/3/EC of the European Parliament and of the Council of 12 February 2002 relating to ozone in ambient air. Official Journal of the European Communities, L 67/14–30.Google Scholar
  18. Evans, G. C. (1972). The quantitative analysis of plant growth. Studies in Ecology 1. Great Britain: Blackwell, 734 p.Google Scholar
  19. Ferretti, M., Bussotti, F., & Calderesi, M. (2004). Ozone, defoliation, of beech (Fagus sylvatica) an visible foliar symptoms on native plants on selected plots of South-Western Europe. In M. Ferretti, M.-J. Sanz, & M. Schaub (Eds.), O 3 SWE-ozone and the forests of South-West Europeern. Final Report (pp. 111–140). Jointly prepared by Corpo Forestale dello Stato, Italia; Ministerio de Medio Ambiente, Dirección General para la Biodiversidad, España; Eidgenössische Forschungsanstalt für Wald, Schnee und Landschaft – WSL, Schweiz; Office National des Forêts, France.Google Scholar
  20. Ferretti, M., Calderisi, M., & Bussotti, F. (2007). Ozone exposure, defoliation of beech (Fagus sylvatica L.) and visible foliar symptoms on native plants in selected plots of South-western Europe. Environmental Pollution, 145, 644–651.CrossRefGoogle Scholar
  21. Fiscus, E. L., Booker, F. L., & Burkey, K. O. (2005). Crop responses to ozone: Uptake, modes of action, carbon assimilation and partitioning. Plant, Cell and Environment, 28, 997–1011.CrossRefGoogle Scholar
  22. Fowler, D., Cape, J. N., Coyle, M., Flechard, C., Kuylenstierna, J., Hicks, K., et al. (1999). The global exposure of forests to air pollutants. Water, Air, & Soil Pollution, 116, 5–32.CrossRefGoogle Scholar
  23. Gaucher, C., Costanzo, N., Afif, D., Mauffette, Y., Chevrier, N. & Dizengremel, P. (2003). The impact of elevated ozone and carbon dioxide on young Acer saccharum seedlings. Physiologia Plantarum, 117, 392–402.CrossRefGoogle Scholar
  24. Genty, B., Briantais, J. M., & Baker, N. R. (1989). The relationship between the quantum yield of photosynthetic electron transport and quenching of Chl fluorescence. Biochimica et Biophysica Acta, 990, 87–92.Google Scholar
  25. Gravano, E., Bussotti, F., Strasser, R. J., Schaub, M., Novak, K., Skelly, K., et al. (2004). Ozone symptoms in leaves of woody plants in open-top chambers: Ultrastructural and physiological characteristics. Physiologia Plantarum, 121, 620–633.CrossRefGoogle Scholar
  26. Guidi, L., Di Cagno, R., & Soldatini, G. F. (2000). Screening of bean cultivars for their response to ozone as evaluated by visible symptoms and leaf chlorophyll fluorescence. Environmental Pollution, 107, 349–355.CrossRefGoogle Scholar
  27. Guidi, L., Nali, C., Ciompi, S., Lorenzini, G., & Franco, G. (1997). The use of chlorophyll fluorescence and leaf gas exchange as methods for studying the different responses to ozone of two bean cultivars. Journal of Experimental Botany, 48, 173–179.CrossRefGoogle Scholar
  28. Günthardt-Goerg, M. S., McQuattie, C. J., Scheidegger, C., Rhiner, C., & Matyssek, R. (1997). Ozone-induced cytochemical and ultra-structural changes in leaf mesophyll cell walls. Canadian Journal of Forest Research, 27, 453–463.CrossRefGoogle Scholar
  29. Heath, R. L. (1987). The biochemistry of ozone attack on the plasma membrane of plant cells. In J. A. Saunders, L. Kosak-Channing, & E. E. Conn (Eds.), Recent advances in phytochemistry. Phytochemical effects of environmental compounds (pp. 29–54). New York, NY: Plenum.Google Scholar
  30. Heath, R. L., & Taylor, G. E., Jr. (1997). Physiological processes and plant responses to ozone exposure. In H. Sandermann, A. R. Wellburn, & R. L. Heath (Eds.), Forest Decline and Ozone: A comparison of controlled chamber and field experiments. Ecological Studies 127 (pp. 317–368). New York: Springer.Google Scholar
  31. Hörtensteiner, S., & Feller, U. (2002). Nitrogen metabolism and remobilization during senescence. Journal of Experimental Botany, 53, 927–937.CrossRefGoogle Scholar
  32. Innes, J. L., Skelly, J. M., & Schaub, M. (2001). Ozone and broadleaved species. A guide to the identification of ozone-induced foliar injury. [Ozon, Laubholz- und Krautpflanzen. Ein Führer zum Bestimmen von Ozonsymptomen]. Haupt, Bern, Stuttgart, Wien.Google Scholar
  33. IPCC (2001) Climate Change 2001: Synthesis Report. Geneva, Switzerland: Intergovernmental Panel on Climate Change.Google Scholar
  34. Jensen, K. F. (1973). Response of nine forest tree species to chronic ozone fumigation. Plant Disease Reporter, 57, 914–917.Google Scholar
  35. Jensen, K. F. (1983). Growth relationship in silver maple fumigated with O3 and SO2. Canadian Journal of Forest Research, 13, 298–302.CrossRefGoogle Scholar
  36. Kangasjärvi, J., Talvinen, J., Utriainen, M., & Karjalainen, R. (1994). Plant defense systems induced by ozone: Commissioned Review. Plant, Cell and Environment, 17, 783–794.CrossRefGoogle Scholar
  37. Karnosky, D. F., Zak, D., Pregnitzer, K., Awmack, C., Bockheim, J., Dickson, R., et al. (2003). 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, 17, 289–304.CrossRefGoogle Scholar
  38. Kersteins, G., & Lendzian, K. J. (1989). Interactions between ozone and plant cuticules 1. Ozone deposition and permeability. New Phytologist, 112, 13–19.CrossRefGoogle Scholar
  39. Keutgen, A. J., Noga, G., & Pawelzik, E. (2005) Cultivar-specific impairment of strawberry growth, photosynthesis, carbohydrate and nitrogen accumulation by ozone. Environmental and Experimental Botany, 53, 271–280.CrossRefGoogle Scholar
  40. King, J. S., Kubiske, M. E., Pregitzer, K. S., Hendrey, G. R., McDonald, E. P., Giardina, C. P., et al. (2005). Tropospheric O3 compromises net primary production in young stands of trembling aspen, paper birch and sugar maple in response to elevated atmospheric CO2. New Phytologist, 168, 623–635.CrossRefGoogle Scholar
  41. Kress, L. W., & Skelly, J. M. (1982). Response of several eastern forest trees to chronic doses of ozone and nitrogen dioxide. Plant Disease, 66, 1149–1152.CrossRefGoogle Scholar
  42. Krupa, S., & Manning, W. J. (1988). Atmospheric ozone: Formation and effects on vegetation. Environmental Pollution, 50, 101–137.CrossRefGoogle Scholar
  43. Krupa, S., McGrath, M. T., Andersen, C. P., Booker, F. L., Burkey, K. O., Chappelka, A. H., et al. (2001). Ambient ozone and plant health. Plant Disease, 85, 5–12.CrossRefGoogle Scholar
  44. Lindroth, R. L., Kopper, B. J., Parsons, F. J., Bockheim, J. G., Karnosky, D. F., Hendrey, G. R., et al. (2002). Consequences of elevated carbon dioxide and ozone for foliar chemical composition and dynamics in trembling ozone for foliar chemical composition and dynamics in trembling aspen (Populus tremuloides) and paper birch (Betula papyrifera). Environmental Pollution, 115, 395–404.CrossRefGoogle Scholar
  45. Lorenzini, G., Guidi, L., Nali, C., & Soldatini, G. F. (1999). Quenching analysis in poplar clones exposed to ozone. Tree Physiology, 19, 607–612.Google Scholar
  46. Matyssek, R., Bytnerowicz, A., Karlsson, P.-E., Paoletti, E., Sanz, M. J., Schaub, M., et al. (2007) Promoting the O3 flux concept for European forest trees. Environmental Pollution, 146, 587–607.CrossRefGoogle Scholar
  47. Matyssek, R., & Innes, J. L. (1999). Ozone – a risk factor for trees and forests in Europe?. Water, Air & Soil Pollution, 116, 199–226.CrossRefGoogle Scholar
  48. Matyssek, R., Reich, P., Oren, R., & Winner, R. E. (1995). Response mechanisms of conifers to air pollutants. In W. K. Smith & T. M. Hinckley (Eds.), Ecophysiology of coniferous forests (pp. 255–308). San Diego: Academic.Google Scholar
  49. Matyssek, R., Wieser, G., Nunn, A. J., Kozovits, A. R., Reiter, I. M., Heerdt, C., et al. (2004). Comparison between AOT40 and ozone uptake in forest trees of different species, age and site conditions. Atmospheric Environment, 38, 2271–2281.CrossRefGoogle Scholar
  50. Mehlhorn, H., Tabner, B. J., & Wellburn, A. R. (1990). Electron spin resonance: Evidence for the formation of free radicals in plants exposed to ozone. Physiologia Plantarum, 79, 377–383.CrossRefGoogle Scholar
  51. Mikkelsen, T. N. (1995). Physiological responses of Fagus sylvatica L. exposed to low levels of ozone in open-top chambers. Trees, 9, 355–361.CrossRefGoogle Scholar
  52. Mikkelsen, T. N., Dodell, B., & Lutz, C. (1995). Changes in pigment concentration and composition in Norway spruce induced by long-term exposure to low levels of ozone. Environmental Pollution, 87, 197–205.CrossRefGoogle Scholar
  53. Mikkelsen, T. N., & Heide-Jørgensen, H. S. (1996). Acceleration of leaf senescence in Fagus sylvatica L. by low levels of tropospheric ozone demonstrated by leaf colour, chlorophyll fluorescence and chloroplast ultrastructure. Trees, 10, 145–156.Google Scholar
  54. Millán, M. M., Mantilla, E., Salvador, R., Carratalá, A., Sanz, M. J., Alonso, L., et al. (2000). Ozone cycles in the Western Mediterranean Basin: Interpretation of monitoring data in complex coastal terrain. Journal of Applied Meteorology, 39, 487–508.CrossRefGoogle Scholar
  55. Millán, M. M., Salvador, R., Mantilla, E., & Kallos, G. (1997). Photo-oxidant dynamics in the Mediterranean Basin in summer: Results from European research projects. Journal of Geophysical Research, 102(D7), 8811–8823.CrossRefGoogle Scholar
  56. Mills (2004). Mapping critical levels for vegetation. In: UNECE Convention on Long-rate Transboundary Air Pollution. Manual on Methodologies and Criteria for Modelling and Mapping Critical Loads and Levels and Air Pollution Effects, Risks and Trends. Retrieved from http://www.oekodata.com/icpmapping/.
  57. Musselmann, R. C., & Massmann, W. J. (1999) Ozone flux to vegetation and its relationship to plant response and ambient air quality standards. Atmospheric Environment, 33, 65–73.CrossRefGoogle Scholar
  58. Novak, K., Schaub, M., Fuhrer, J., Skelly, J. M., Hug, C., & Landolt, W. (2005). Seasonal trends in reduced leaf gas exchange and ozone-induced foliar injury in three ozone sensitive woody plant species. Environmental Pollution, 136, 33–45.CrossRefGoogle Scholar
  59. Novak, K., Skelly, J. M., Schaub, M., Kräuchi, N., Hug, C. & Landolt, W. (2003). Ozone air pollution and foliar injury development on native plants of Switzerland. Environmental Pollution, 125, 41–52.CrossRefGoogle Scholar
  60. Orendovici, T., Skelly, J. M., Ferdinand, J. A., Savage, J. E., Sanz, M. J., & Smith, G. C. (2003). Response of native plants of northeastern United States and southern Spain to ozone exposures; determining exposure/response relationships. Environmental Pollution, 125, 31–40.CrossRefGoogle Scholar
  61. Paoletti, E. (2006). Impact of ozone on Mediterranean forests: A review. Environmental Pollution, 144, 463–474.CrossRefGoogle Scholar
  62. Paoletti, E., & Grulke, N. E. (2005). Does living in elevated CO2 ameliorate tree response to ozone? A review on stomatal responses. Environmental Pollution, 137, 483–493.CrossRefGoogle Scholar
  63. Pell, E. J., Eckardt, N., & Glick, R. E. (1994). Biochemical and molecular basis for the impairment of photosynthetic potential. Photosynthesis Research, 39, 453–462.CrossRefGoogle Scholar
  64. Pell, E. J., Schlagnhaufer, C. D., & Arteca, R. N. (1997). Ozone-induced oxidative stress: Mechanisms of action and reaction. Physiologia Plantarum, 100, 264–273.CrossRefGoogle Scholar
  65. Pleijel, H., Skärby, L., Ojanperä, K., & Selldén, G. (1994). Exposure of oats, Avena sativa L. to filtered and unfiltered air in open-top chambers: Effects on grain yield and quality. Environmental Pollution, 86, 129–134.CrossRefGoogle Scholar
  66. Reddy, G. N., Aeteca, R. N., Dai, Y. R., Flores, H. E., Negram, F. B., & Pell, E. J. (1993). Changes in ethylene and polyamines in relation to mRNA levels of the large and small subunits of ribulose biphosphate/oxygenase in ozone-stressed potato foliage. Plant, Cell and Environment, 120, 819–826.CrossRefGoogle Scholar
  67. Reich, P. B. (1987). Quantifying plant response to ozone: A unifying theory. Tree Physiology, 3, 63–91.Google Scholar
  68. Reich, P. B., & Amudson, R. G. (1985). Ambient levels of ozone reduce net photosynthesis in tree and crop species. Science, 230, 566–570.CrossRefGoogle Scholar
  69. Reich, P. B., Schoettle, A. W., & Amudson, R. G. (1986). Effects of O3 and acidic rain on photosynthesis and growth in sugar maple and northern red oak seedlings. Environmental Pollution, 40, 1–15.CrossRefGoogle Scholar
  70. Reich, P. B., Schoettle, A. W., Stroo, H. F., & Amundson, R. G. (1988). Effects of ozone and acid rain on white pine (Pinus strobus) seedlings grown in five soils. III. Nutrient relations. Canadian Journal of Botany, 66, 1517–1531.Google Scholar
  71. Reichenauer, T. G., & Bolhàr-Nordenkampf, H. R. (1999). Mechanisms of impairment of the photosynthetic apparatus in intact leaves by ozone. Zeitschrift für Naturforschung, 54c, 824–829.Google Scholar
  72. Reig-Armiñana, J., Calatayud, V., Cerveró, J., García-Breijo, F. J., Ibars, A., & Sanz, M. J. (2004). Effects of ozone on the foliar histology of the mastic plant (Pistacia lentiscus L.). Environmental Pollution, 132, 321–331.CrossRefGoogle Scholar
  73. Runeckles, V. C., & Chevone, B. I. (1992). Crop responses to ozone. In A. S. Lefohn (Ed.), Surface level ozone exposures and their effects on vegetation (pp. 189–270). Chelsea, MI: LewisGoogle Scholar
  74. Saitanis, C. J., Riga-Karandinos, A. N., & Karandinos, M. G. (2001). Effects of ozone on chlorophyll and quantum yield of tobacco (Nicotiana tabacum L.) varieties. Chemosphere, 42, 909–917.CrossRefGoogle Scholar
  75. Samuelson, L. J., & Kelly, J. M. (1997). Ozone uptake in Prunus serotina, Acer rubrum and Quercus rubra forest trees of different sizes. New Phytologist, 136, 255–264.CrossRefGoogle Scholar
  76. Samuelson, L. J., Kelly, J. M., Mays, P. A., & Edwards, G. S. (1996). Growth and nutrition of Quercus rubra L. seedlings and mature trees after three seasons of ozone exposure. Environmental Pollution, 91, 317–323.CrossRefGoogle Scholar
  77. Sanz, M. J., & Millán, M. (1998). The dynamics of aged air mases and ozone in the western Mediterranean: Relevance to forest ecosystems. Chemosphere, 98, 1089–1094.CrossRefGoogle Scholar
  78. Sanz, M. J., Sánchez, G., Calatayud, V., Minaya, M. T., & Cerveró, J. (2001). La contaminación atmosférica en los bosques. Guía para la identificación de daños visibles causados por ozono. Organismo Autónomo de Parques Nacionales, 163 p.Google Scholar
  79. Sanz, M. J., Calatayud, V., & Sanchez, G. (2007a). Measures of ozone concentrations using passive sampling in forests of South Western Europe. Environmental Pollution, 145, 620–628.CrossRefGoogle Scholar
  80. Sanz, M. J., Sanz, F., Calatayud, V., Sánchez-Peña, G. (2007b). Ozone in Spain’s National Parks and Protected Forests. TheScientificWorldJOURNAL 21, 67–77.Google Scholar
  81. Schaub, M., Skelly, J. M., Steiner, K. C., Davis, D. D., Pennypacker, S. P., Zhang, J., et al. (2003). Physiological and foliar injury responses of Prunus serotina, Fraxinus americana and Acer rubrum seedlings to varying soil moisture and ozone. Environmental Pollution, 124, 307–320.CrossRefGoogle Scholar
  82. Scherzer, A. J., Rebbeck, J., & Boerner, R. E. J. (1998). Foliar nitrogen dynamics and decomposition of yellow-poplar and eastern white pine during four seasons of exposure to elevated ozone and carbon dioxide. Forest Ecology and Management, 109, 355–366.CrossRefGoogle Scholar
  83. Schier, G. A. (1990). Response of yellow-poplar (Liriodendron tulipifera L.) seedlings to simulated acid rain and ozone: 2. Effect on throughfall chemistry and nutrients in the leaves. Environmental and Experimental Botany, 30, 325–331.CrossRefGoogle Scholar
  84. Schreiber, U., Schliwa, U., & Bilger, W. (1986). Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynthesis Research, 10, 51–62.CrossRefGoogle Scholar
  85. Skelly, J. M., Innes, J. L., Savage, J. E., Snyder, K. R., Vanderheyden, D., Zhang, J., et al. (1999). Observation and confirmation of foliar ozone symptoms of native plant species of Switzerland and southern Spain. Water, Air, and Soil Pollution, 116, 227–234.CrossRefGoogle Scholar
  86. Taylor, G. E., Jr., & Tingey, D. T. (1982). Flux of ozone to Glycine max: Sites of regulation and relationship to leaf injury. Oecologia, 53, 179–186.CrossRefGoogle Scholar
  87. Temple, P. J., & Riechers, G. H. (1995). Nitrogen allocation in ponderosa pine seedlings exposed to interacting ozone and drought stresses. New Phytologist, 130, 97–104.CrossRefGoogle Scholar
  88. Vanderheyden, D., Skelly, J., Innes, J., Hug, C., Zhang, J., Landolt, W., et al. (2001). Ozone exposure thresholds and foliar injury on forest plants in Switzerland. Environmental Pollution, 111, 321–331.CrossRefGoogle Scholar
  89. Vollenweider, P., Ottiger, M., & Günthardt-Goerg, M. S. (2003). Validation of leaf ozone symptoms in natural vegetation using microscopical methods. Environmental Pollution, 124, 101–118.CrossRefGoogle Scholar
  90. Wieser, G. (1997) Ozone impact on photosynthetic capacity of mature and young Norway spruce (Picea abies (L.) Karst.): External versus internal exposure. Phyton, 37, 279–302.Google Scholar
  91. Wieser, G., Häsler, R., Götz, B., Koch, W., & Havranek, W. M. (2000). Role of climate, crown position, tree age and altitude in calculated ozone flux into needles of Picea abies and Pinus cembra: A synthesis. Environmental Pollution, 109, 415–422.CrossRefGoogle Scholar
  92. Wohlgemuth, H., Mittelstrass, K., Kschieschan, S., Bender, J., Weigel, H.-J., Overmyer, K., et al. (2002). Activation of an oxidative burst is a general feature of sensitive plants exposed to the air pollutant ozone. Plant, Cell and Environment, 25, 717–726.CrossRefGoogle Scholar
  93. Zhang, J., Ferdinand, J. A., Vanderheyden, D., Skelly, J., & Innes, J. (2001). Variation of gas exchange within native species of Switzerland and relationships with ozone injury: An open-top experiment. Environmental Pollution, 113, 177–185.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Vicent Calatayud
    • 1
    Email author
  • Júlia Cerveró
    • 1
  • María José Sanz
    • 1
  1. 1.Fundación CEAM, Parc TecnològicValenciaSpain

Personalised recommendations