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Growth and Leaf Gas Exchange in Three Birch Species Exposed to Elevated Ozone and CO2 in Summer

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Abstract

We examined the effects of ozone and elevated CO2 concentration in summer on the growth and photosynthetic traits of three representative birch species in Japan (mountain birch, Monarch birch, and white birch). Seedlings of the three birch species were grown in 16 open-top chambers and were exposed to two levels of ozone (6 and 60 nmol mol−1 for 7 h per day) in combination with two levels of CO2 (370–380 and 600 μmol mol−1 for daytime) from July to October. No adverse effects of ozone were found in the Monarch birch or the white birch, but elevated ozone in summer reduced branch biomass and net photosynthesis, and accelerated leaf abscission, in the mountain birch. Elevated CO2 promoted root development and thereby reduced the ratio of shoot dry mass (stem + branch) to root dry mass (S/R ratio) in the mountain birch and white birch. In contrast, there was no difference in dry mass between ambient and elevated CO2 for the Monarch birch, due to downregulation of photosynthesis. Studies of the combined effect of CO2 and ozone revealed that elevated CO2 did not ameliorate the effect of ozone on mountain birch in late summer. In considering the ameliorating effect of CO2 on ozone damage, it is necessary to take account of the species and the season.

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References

  • Ainsworth, E. A., & Rogers, A. (2007). The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant, Cell & Environment, 30, 258–270.

    Article  CAS  Google Scholar 

  • Barnes, J. D., Pfirrmann, T., Steiner, K., Lütz, C., Busch, U., Küchenhoff, H., et al. (1995). Effects of elevated CO2, elevated O3 and potassium deficiency on Norway spruce [Picea abies (L.) Karst.]: seasonal changes in photosynthesis and non-structural carbohydrate content. Plant, Cell & Environment, 18, 1345–1357.

    Article  CAS  Google Scholar 

  • Bernacchi, C. J., Singsaas, E. L., Pimentel, C., Portis, A. R., Jr., & Long, S. P. (2001). Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant, Cell & Environment, 24, 253–259.

    Article  CAS  Google Scholar 

  • Broadmeadow, A., Heath, J., & Randle, T. J. (1999). Environmental limitations to O3 uptake—some key results from young trees growing at elevated CO2 concentrations. Water, Air, and Soil Pollution, 116, 299–310.

    Article  CAS  Google Scholar 

  • Bytnerowicz, A., Omasa, K., & Paoletti, E. (2007). Integrated effects of air pollution and climate change on forests: a northern hemisphere perspective. Environmental Pollution, 147, 438–445.

    Article  CAS  Google Scholar 

  • Eguchi, N., Karatsu, K., Ueda, T., Funada, R., Takagi, K., Hiura, T., et al. (2008). Photosynthetic responses of birch and alder saplings grown in a free air CO2 enrichment system in northern Japan. Trees—Structure and Function, 22, 437–447.

    Article  CAS  Google Scholar 

  • Evans, L. T. (1963). Environmental control of plant growth. New York: Academic press.

    Google Scholar 

  • Farquhar, G. D., von Caemmerer, S., & Berry, J. A. (1980). A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta, 149, 78–90.

    Article  CAS  Google Scholar 

  • Grams, T. E. E., Anegg, S., Haberle, K.-H., Langebartels, C., & Matyssek, R. (1999). Interactions of chronic exposure to elevated CO2 and O3 levels in the photosynthetic light and dark reactions of European beech (Fagus crenata). New Phytologist, 144, 95–107.

    Article  CAS  Google Scholar 

  • Grulke, N. E., Neufeld, H. S., Davison, A. W., Roberts, M., & Chappelka, A. H. (2007). Stomatal behavior of ozone-sensitive and -insensitive coneflowers (Rudbeckia laciniata var. digitata) in Great Smoky Mountains National Park. New Phytologist, 173, 100–109.

    Article  CAS  Google Scholar 

  • Heath, J. (1998). Stomata of trees growing in CO2-enriched air show reduced sensitivity to vapour pressure deficit and drought. Plant, Cell & Environment, 21, 1077–1088.

    Article  Google Scholar 

  • Hokkaido Prefecture. (2011). Forestry statistics of Hokkaido in the fiscal year 2010. http://www.pref.hokkaido.lg.jp/sr/sum/kcs/rin-toukei/22rtk.htm, Accessed 10 Jan 2012. (In Japanese).

  • Hoshika, Y., Watanabe, M., Inada, N., & Koike, T. (2012). Ozone-induced stomatal sluggishness develops progressively in Siebold beech (Fagus crenata). Environmental Pollution, 166, 152–156.

    Article  CAS  Google Scholar 

  • Karnosky, D. E., Oksanen, E., Dickson, R. E., & Isebrands, J. G. (2001). Impact of interacting greenhouse gases on forest ecosystems. In D. F. Karnosky, G. Scarascia-Mugnozza, R. Geulemans, & J. L. Innes (Eds.), The impacts of carbon dioxide and other greenhouse gases on forest ecosystems (pp. 253–267). Wallingford: CABI.

    Chapter  Google Scholar 

  • Karnosky, D. F., Percy, K. E., Chappelka, A. H., Simpson, C., & Pikkarainen, J. M. (2003). Air pollution, global change and forests in the new millennium (p. 469). Amsterdam: Elsevier.

    Google Scholar 

  • 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, 623–636.

    Article  CAS  Google Scholar 

  • Koike, T. (1988). Leaf structure and photosynthetic performance as related to the forest succession of deciduous broad-leaved trees. Plant Species Biology, 3, 77–87.

    Article  Google Scholar 

  • Koike, T. (1995a). Effects of CO2 in interaction with temperature and soil fertility on the foliar phenology of alder, birch, and maple seedlings. Canadian Journal of Botany, 73, 149–157.

    Article  Google Scholar 

  • Koike, T. (1995b). Physiological ecology of the growth characteristics of Japanese mountain birch in northern Japan: a comparison with Japanese mountain white birch. In E. O. Box et al. (Eds.), Vegetation science in forestry: global perspective based on forest ecosystems of East and Southeast Asia (pp. 409–422). The Netherlands: Kluwer Academic Publishers.

    Google Scholar 

  • Koike, T., & Sakagami, Y. (1985). Comparison of the photosynthetic responses to temperature and light of Betula maximowicziana and Betula platyphylla var. japonica. Canadian Journal of Forest Research, 15, 631–635.

    Article  Google Scholar 

  • Kolb, T. E., & Matyssek, R. (2001). Limitation and perspectives about scaling ozone impacts in trees. Environmental Pollution, 115, 373–393.

    Article  CAS  Google Scholar 

  • Larcher, W. (2004). Physiological plant ecology (4th ed.). Heidelberg: Springer.

    Google Scholar 

  • Linder, S. (1987). Responses to water and nutrients in coniferous ecosystems. In. E.-D. Schulze and H.Z. Wolfer (eds.). Potentials and limitations of ecosystems analysis. Ecological Studies, 61, Springer, Heidelberg, pp.180-202.

  • Long, S. P., & Bernacchi, C. J. (2003). Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. Journal of Experimental Botany, 54, 2393–2401.

    Article  CAS  Google Scholar 

  • Long, S. P., Ainsworth, E. A., Rogers, A., & Ort, D. R. (2004). Rising atmospheric carbon dioxide: plants FACE the future. Annual Review of Plant Biology, 55, 591–628.

    Article  CAS  Google Scholar 

  • Lütz, C., Anegg, S., Gerant, D., Alaoui-Sosse, B., Gerard, J., & Dizengremel, P. (2000). Beech trees exposed to high CO2 and to simulated summer ozone levels: effects on photosynthesis, chloroplast components and leaf enzyme activity. Physiologia Plantarum, 109, 252–259.

    Article  Google Scholar 

  • Mao, Q., Watanabe, M., & Koike, T. (2010). Growth characteristics of two promising tree species for afforestation, birch and larch in the northeastern part of Asia. Eurasian Journal of Forest Research, 13, 69–76.

    Google Scholar 

  • Matsumura, H., Mikami, C., Sakai, Y., Murayama, K., Izuta, T., Yonekura, T., et al. (2005). Impacts of elevated O3 and/or CO2 on growth.of Betula platyphylla, Betula ermanii, Fagus crenata, Pinus densiflora and Cryptomeria japonica seedlings. Journal of Agricultural Meteorology, 60, 1121–1124.

    Google Scholar 

  • Matyssek, R. & Sandermann, H. (2003). Impact of ozone on trees: an ecophysiological perspective. In: Esser, K., Lüttge, U., Beyschlag, W. & Hellwig F (eds). An ecophysiological perspective. progress in botany, vol.64. Springer, Heidelberg, pp. 349-404.

  • Matyssek, R., Keller, T., & Koike, T. (1993). Branch growth and leaf gas exchange of Populus tremula exposed to low ozone concentrations throughout two growing seasons. Environmental Pollution, 79, 1–7.

    Article  CAS  Google Scholar 

  • Naja, M., & Akimoto, H. (2004). Contribution of regional pollution and long-range transport to the Asia-Pacific region: analysis of long-term ozonesonde data over Japan. Journal of Geophysical Research, 109, D21306.

    Article  Google Scholar 

  • Nelson, N. D., & Isebrands, J. G. (1983). Late-season photosynthesis and photosynthate distribution in an intensively-cultured Populus nigra × P. laurifolia clone. Photosynthetica, 17, 537–549.

    Google Scholar 

  • Noguchi, I. (2011). Atmospheric condition and forest declining of mountain birch in the somma of Lake Mashu. Northern Forestry 63, 29 (in Japanese).

  • Ohara, T., & Sakata, T. (2003). Long-term variation of photochemical oxidants over Japan. Journal of Japan Society for Atmospheric Environment, 38, 47–54 (in Japanese with English summary).

    Google Scholar 

  • Ohara, T., Uno, I., Wakamatsu, S., & Murano, K. (2001). Numerical simulation of the springtime trans-boundary air pollution in East Asia. Water, Air, and Soil Pollution, 130, 295–300.

    Article  Google Scholar 

  • Ohno, Y., Umeki, K., Yasaka, M., Watanabe, I., & Takiya, M. (2010). Competition as a predisposing factor of crown dieback in a secondary forest of Betula maximowicziana in Hokkaido, northern Japan. Journal of Forest Research, 15, 161–168.

    Article  Google Scholar 

  • Onandia, G., Olsson, A.-K., Barth, S., King, J. S., & Uddling, J. (2011). Exposure to moderate concentrations of tropospheric ozone impairs tree stomatal response to carbon dioxide. Environmental Pollution, 159, 2350–2354.

    Article  CAS  Google Scholar 

  • Paoletti, E., & Grulke, N. E. (2005). Does living in elevated CO2 ameliorate tree response to ozone? A review of stomatal responses. Environmental Pollution, 137, 483–493.

    Article  CAS  Google Scholar 

  • Serengil, Y., Augustaitis, A., Bytnerowicz, A., Grulke, N., Kozovitz, A. R., Matyssek, R., et al. (2011). Adaptation of forest ecosystems to air pollution and climate change: a global assessment on research priorities. iForest—Biogeosciences and Forestry, 4, 44–48.

    Article  Google Scholar 

  • Shimizu, H., & Feng, Y. W. (2007). Ozone and/or water stress could have influenced the Betula ermanii Cham. forest decline observed at Oku-Nikko, Japan. Environmental Monitoring and Assessment, 128, 109–119.

    Article  CAS  Google Scholar 

  • Takeda, M., & Aihara, K. (2007). Effects of ambient ozone concentrations on beech (Fagus crenata) seedlings in the Tanzawa mountains, Kanagawa prefecture Japan. Journal of Japan Society of Atmospheric Environment, 42, 107–117 (in Japanese with English summary).

    CAS  Google Scholar 

  • Takigawa, M., Niwano, M., Akimoto, H., & Takahashi, M. (2007). Development of a one-way nested global-regional air quality forecasting model. Sola, 3, 81–84.

    Article  Google Scholar 

  • Uddling, J., Teclaw, R. M., Pregitzer, K. S., & Ellsworth, D. S. (2009). Leaf and canopy conductance in aspen and aspen-birch forests under free-air enrichment of carbon dioxide and ozone. Tree Physiology, 29, 1367–1380.

    Article  CAS  Google Scholar 

  • Watanabe, M., Umemoto-Yamaguchi, M., Koike, T., & Izuta, T. (2010). Growth and photosynthetic response of Fagus crenata seedlings to ozone and/or elevated carbon dioxide. Landscape and Ecological Engineering, 6, 181–190.

    Article  Google Scholar 

  • Watanabe, M., Matsuo, N., Yamaguchi, M., Matsumura, H., Kohno, Y., & Izuta, T. (2010). Risk assessment of ozone impact on the carbon absorption of Japanese representative conifers. European Journal of Forest Research, 129, 421–430.

    Article  Google Scholar 

  • Watanabe, M., Watanabe, Y., Kitaoka, S., Utsugi, H., Kita, K., & Koike, T. (2011). Growth and photosynthetic traits of hybrid larch F1 (Larix gmelinii var. japonica × L. kaempferi) under elevated CO2 concentration with low nutrient availability. Tree Physiology, 31, 965–975.

    Article  CAS  Google Scholar 

  • Watanabe, M., Mao, Q., Novriyanti, E., Ito, H., Ueda, T., Takagi, K., et al. (2011). Photosynthetic activity of 3 birches grown under free air CO2 enrichment system. Boreal Forest Research, 59, 39–40 (in Japanese).

    Google Scholar 

  • Watanabe, M., Yamaguchi, M., Matsumura, H., Kohno, Y., & Izuta, T. (2012). Risk assessment of ozone impact on Fagus crenata in Japan: consideration of atmospheric nitrogen deposition. European Journal of Forest Research, 131, 475–484.

    Article  CAS  Google Scholar 

  • Yamaguchi, M., Watanabe, M., Matsumura, H., Kohno, Y., & Izuta, T. (2011). Experimental studies on the effects of ozone on growth and photosynthetic activity of Japanese forest species. Asian Journal of Atmospheric Environment, 5, 65–78.

    Article  Google Scholar 

  • Yamaji, K., Ohara, T., Uno, I., Kurokawa, J., Pochanart, P., & Akimoto, H. (2008). Future prediction of surface ozone over east Asia using models-3 community multiscale air quality modeling system and regional emission inventory in Asia. Journal of Geophysical Research, 113, D08306. doi:10.1029/2007JD008663.

    Article  Google Scholar 

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Acknowledgments

Thanks for financial support are due to the Environment Research and Technology Development Fund of Japan (B-1105) and for a grant-in-aid from the Japanese Society for Promotion of Science (type B 23380078, and Young Scientists B 24710027 and ditto B 24780239).

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Authors and Affiliations

  1. Silviculture and Forest Ecological Studies, Hokkaido University, Sapporo, 060-8689, Japan

    Yasutomo Hoshika, Makoto Watanabe, Naoki Inada & Takayoshi Koike

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  1. Yasutomo Hoshika
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  2. Makoto Watanabe
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  3. Naoki Inada
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  4. Takayoshi Koike
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Correspondence to Takayoshi Koike.

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Hoshika, Y., Watanabe, M., Inada, N. et al. Growth and Leaf Gas Exchange in Three Birch Species Exposed to Elevated Ozone and CO2 in Summer. Water Air Soil Pollut 223, 5017–5025 (2012). https://doi.org/10.1007/s11270-012-1253-y

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  • DOI: https://doi.org/10.1007/s11270-012-1253-y

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