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Ozone alters the feeding behavior of the leaf beetle Agelastica coerulea (Coleoptera: Chrysomelidae) into leaves of Japanese white birch (Betula platyphylla var. japonica)

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Abstract

High mixing ratios of ground-level O3 threaten trophic interactions. In the present study, we conducted laboratory assays, where insect larvae and adults were not directly exposed to O3, to test the feeding behavior and attraction of the coleopteran leaf beetle Agelastica coerulea to early and late leaves of Japanese white birch (Betula platyphylla var. japonica) treated with ambient or elevated O3 levels. We found that overwintered adults were not deterred from grazing elevated O3-treated leaves, but rather preferred them than ambient O3-treated ones. We also found that the feeding behavior of 2nd instar larvae fed on early or late leaves was not influenced by the O3 treatment of the leaves when larvae could choose leaves. These observations of the adults and larvae feeding preferences contradict prior observations in the field conditions where the insects avoided leaves in O3-enriched atmosphere. Since adults preferred elevated O3-exposed leaves in the present laboratory assays, it is worthy of further investigations whether adults change their grazing preference so as to ensure the leaf palatability as a feeding source for their larvae. Hence, new direction towards detailed ovipositional behavior surveys under field conditions is encouraged.

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References

  • Agathokleous E, Saitanis CJ, Koike T (2015) Tropospheric O3, the nightmare of wild plants: a review study. J Agric Meteorol 71:142–152

    Article  Google Scholar 

  • Agathokleous E, Saitanis CJ, Wang X, Watanabe M, Koike T (2016) A review study on past 40 years of research on effects of tropospheric O3 on belowground structure, functioning and processes of trees: a linkage with potential ecological implications. Wat Air Soil Pollut 227:33

    Article  Google Scholar 

  • Agrell J, Kopper B, McDonald EP, Lindroth RL (2005) CO2 and O3 effects on host plant preferences of the forest tent caterpillar (Malacosoma disstria). Glob Chang Biol 11:588–599

    Article  Google Scholar 

  • Akimoto H (2003) Global air quality and pollution. Science 302:1716–1719

    Article  CAS  Google Scholar 

  • Barbehenn RV, Constabel CP (2011) Tannins in plant-herbivore interactions. Phytochemistry 72:1551–1565

    Article  CAS  Google Scholar 

  • Bate-Smith EC (1977) Astringent tannins of acer species. Phytochemistry 16:1421–1426

    Article  CAS  Google Scholar 

  • Baur R, Binder S, Benz G (1991) Nonglandular leaf trichomes as short-term inducible defense of the grey alder, Alnus incana (L.), against the chrysomelid beetle, Agelastica alni L. Oecologia 87:219–226

    Article  CAS  Google Scholar 

  • Blande JD, Holopainen JK, Niinemets Ü (2014) Plant volatiles in polluted atmospheres: stress responses and signal degradation. Plant Cell Environ 37:1892–1904

    Article  CAS  Google Scholar 

  • Bolsinger M, Lier ME, Hughes PR (1992) Influence of ozone air pollution on plant-herbivore interactions. Part 2: effects of ozone on feeding preference, growth and consumption rates of monarch butterflies (Danaus plexippus). Environ Pollut 77:31–37

    Article  CAS  Google Scholar 

  • Booker FL, Burkey KO, Jones AM (2012) Re-evaluating the role of ascorbic acid and phenolic glycosides in ozone scavenging in the leaf apoplast of Arabidopsis thaliana L. Plant Cell Environ 35:1456–1466

    Article  CAS  Google Scholar 

  • Box GEP, Cox DR (1964) An analysis of transformations. J R Stat Soc B 26:211–252

    Google Scholar 

  • Bryant JP, Chapin FS III, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368

    Article  CAS  Google Scholar 

  • Cape JN (2008) Surface ozone concentrations and ecosystem health: past trends and a guide to future projections. Sci Total Environ 400:257–269

    Article  CAS  Google Scholar 

  • Da Rosa Santos AC, Furlan CM (2013) Levels of phenolic compounds in Tibouchina pulchra after fumigation with ozone. Atmos Pollut Res 4:250–256

    Article  Google Scholar 

  • De Rezende FM, Furlan CM (2009) Anthocyanins and tannins in ozone-fumigated guava trees. Chemosphere 76:1445–1450

    Article  Google Scholar 

  • Endress AG, Jeffords MR, Case LJ, Smith LM (1991) Ozone induced acceptability of yellow poplar and black cherry to gypsy moth larvae. J Environ Hort 9:221–225

    CAS  Google Scholar 

  • Fares S, Oksanen E, Lännenpää M, Julkunen-Tiitto R, Loreto F (2010) Volatile emissions and phenolic compound concentrations along a vertical profile of Populus nigra leaves exposed to realistic ozone concentrations. Photosynth res 104:61–74

    Article  CAS  Google Scholar 

  • Farré-Armengol G, Peñuelas J, Li T, Yli-Pirilä P, Filella I, Llusia J, Blande JD (2016) Ozone degrades floral scent and reduces pollinator attraction to flowers. New Phytol 209:152–160

    Article  Google Scholar 

  • Feng Z, Kobayashi K, Ainsworth EA (2008) Impact of elevated ozone concentration on growth, physiology, and yield of wheat (Triticum aestivum L.): a meta-analysis. Glob Chang Biol 14:2696–2708

    Google Scholar 

  • Freiwald V, Häikiö E, Julkunen-Tiitto R, Holopainen JK, Oksanen E (2008) Elevated ozone modifies the feeding behaviour of the common leaf weevil on hybrid aspen through shifts in developmental, chemical, and structural properties of leaves. Entomol Exp App 128:66–72

    Article  CAS  Google Scholar 

  • Fuentes JD, Roulston TH, Zenker J (2013) Ozone impedes the ability of a herbivore to find its host. Environ Res Let 8:014048

    Article  Google Scholar 

  • Fuhrer J, Booker F (2003) Ecological issues related to ozone: agricultural issues. Environ Int 29:141–154

    Article  CAS  Google Scholar 

  • Hara H (2015) Leaf beetle (Agelastica coerulea). In: Forest Insect Library of Forestry Research Institute, HRO, http://www.fri.hro.or.jp/zukan/konchu/00data/kochu/hamusi/hannoki/note.html

  • Hillstrom ML, Lindroth RL (2008) Atmospheric carbon dioxide and ozone alter forest insect abundance and community composition. Ins Cons Div 1:233–241

    Article  Google Scholar 

  • Hoshika Y, Watanabe M, Inada N, Mao Q, Koike T (2013) Photosynthetic response of early and late leaves of white birch (Betula platyphylla var. japonica) grown under free-air ozone exposure. Environ Pollut 182:242–247

    Article  CAS  Google Scholar 

  • Inoue W, Vanderstock A, Sakikawa T, Nakamura M, Saito H, Shibuya M, Koike T (2016) The interaction between insects and deciduous broadleaved trees under different O3 concentrations and soil fertilities. Boreal For Res 64 (In Japanese)

  • Jones CG, Coleman JS (1988) Plant stress and insect behavior: cottonwood, ozone and the feeding and oviposition preference of a beetle. Oecologia 76:51–56

    Article  Google Scholar 

  • Jordan DN, Green TH, Chappelka AH, Lockaby BG, Meldahl RS, Gjerstad DH (1991) Response of total tannins and phenolics in loblolly pine foliage exposed to ozone and acid rain. J Chem Ecol 17:505–513

    Article  CAS  Google Scholar 

  • Julkunen-Tiitto R (1985) Phenolic constituents in the leaves of northern willows: methods for the analysis of certain phenolics. J Agric Food Chem 33:213–217

    Article  CAS  Google Scholar 

  • Kalabokas PD, Cammas J-P, Thouret V, Volz-Thomas A, Boulanger D, Reparis CC (2013) Examination of the atmospheric conditions associated with high and low summer ozone levels in the lower troposphere over the eastern Mediterranean. Atmos Chem Phys Dis 13:2457–2491

    Article  Google Scholar 

  • Kanoun M, Goulas MJP, Biolley J-P (2001) Effect of a chronic and moderate ozone pollution on the phenolic pattern of bean leaves (Phaseolus vulgaris L. cv Nerina): relations with visible injury and biomass production. Biochem Syst Ecol 29:443–457

    Article  CAS  Google Scholar 

  • Karabourniotis G, Liakopoulos G, Nikolopoulos D, Bresta P, Stavroulaki V, Sumbelle S (2014) “Carbon gain vs. water saving, growth vs. defence”: Two dilemmas with soluble phenolics as a joker. Plant Sci 227:21–27

  • Koike T (1995) Physiological ecology of the growth characteristics of Japanese mountain birch in Northern Japan: a comparison with Japanese white birch. In: Box E, et al. (eds.) Vegetation Science in Forestry, Elsevier, pp 409–422

  • Koike T, Tobita H, Shibata T, Matsuki S, Konno K, Kitao M, Yamashita N, Maruyama Y (2006) Defense characteristics of seral deciduous broad-leaved tree seedlings grown under differing levels of CO2 and nitrogen. Popul Ecol 48:23–29

  • Koike T, Watanabe M, Hoshika Y, Kitao M, Matsumura H, Funada R, Izuta T (2013) Effects of ozone on forest ecosystems in east and Southeast Asia. In: Matyssek R, Clarke N, Cudlin P, Mikkelsen TN, Tuovinen J-P, Wieser G, Paoletti E (eds) Climate change, air pollution and global challenges: understanding and perspectives from forest research. Elsevier, Oxford, pp 371–390

    Chapter  Google Scholar 

  • Kopanakis I, Glytsos T, Kouvarakis G, Gerasopoulos E, Mihalopoulos N, Lazaridis M (2016) Variability of ozone in the eastern Mediterranean during a 7-year study. Air Qual Atmos Health 9:461

    Article  CAS  Google Scholar 

  • Li T, Blande JD, Holopainen JK (2016) Atmospheric transformation of plant volatiles disrupts host plant finding. Sci Rep 6:33851

    Article  CAS  Google Scholar 

  • Lindroth RL (2010) Impacts of elevated atmospheric CO2 and O3 on forests: Phytochemistry, trophic interactions, and ecosystem dynamics. J Chem Ecol 36:2–21

    Article  CAS  Google Scholar 

  • Matsuki S, Sano Y, Koike T (2004) Chemical and physical defense in the early and late leaves in three heterophyllous birch species native to northern Japan. Ann Bot 93:141–147

    Article  CAS  Google Scholar 

  • Peltonen PA, Vapaavuori E, Julkunen-Tiitto R (2005) Accumulation of phenolic compounds in birch leaves is changed by elevated carbon dioxide and ozone. Glob Chang Biol 11:1305–1324

    Article  Google Scholar 

  • Saitanis C, Panagopoulos G, Dasopoulou V, Agathokleous E, Papatheohari Y (2015) Integrated assessment of ambient ozone phytotoxicity in Greece’s Tripolis plateau. J Agric Meteorol 71(2):55–64

    Article  Google Scholar 

  • Sakikawa T, Oikawa M, Watanabe M, Mao Q, Koike T (2014) The effect of ozone on leaf phenology of white birch (Betula platyphylla var. japonica) grown under free-air ozone exposure. Boreal For Res 62:59–60 (in Japanese)

    Google Scholar 

  • Sakikawa T, Nakamura M, Watanabe M, Oikawa M, Satoh F, Koike T (2016) Leaf phenology and insect grazing of Japanese white birch saplings grown under free-air ozone exposure. J Agric Meteorol 72:80–84

    Article  Google Scholar 

  • Schoonhoven LM, Van Loon JJA, Dicke M (2005) Insect-plant biology, 2nd edn. Oxford University Press, New York, p 421

  • Vanderstock A, Agathokleous E, Inoue W, Eguchi N, Nakamura M, Satoh F, Kanie S, Koike T (2016) Preliminary survey on insect grazing in white birch stands under free-air O3 fumigation. Boreal For Res 64:27–30

    Google Scholar 

  • Watanabe M, Hoshika Y, Inada N, Wang X, Mao W, Koike T (2013) Photosynthetic traits of Siebold’s beech and oak saplings grown under free air ozone exposure in northern Japan. Environ Pollut 174:50–56

    Article  CAS  Google Scholar 

  • Yamaji K, Julkunen-Tiitto R, Rousi M, Freiwald V, Oksanen E (2003) Ozone exposure over two growing seasons alters root-to-shoot ratio and chemical composition of birch (Betula pendula Roth). Glob Chang Biol 9:1363–1377

    Article  Google Scholar 

  • Yli-Pirilä P, Copolovici L, Kännaste A, Noe S, Blande JD, Mikkonen S, Klemola T, Pulkkinen J, Virtanen A, Laaksonen A, Joutsensaari J, Niinemets Ü, Holopainen JK (2016) Herbivory by an outbreaking moth increases emissions of biogenic volatiles and leads to enhanced secondary organic aerosol formation capacity. Environ Sci Technol 50:11501–11510

    Article  Google Scholar 

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Acknowledgements

The authors are grateful to Dr. Elena Paoletti and Dr. Yasutomo Hoshika of the Institute of Sustainable Plant Protection, Florence, Italy, for kind suggestions. Evgenios Agathokleous is an International Research Fellow (ID No: P17102) of the Japan Society for the Promotion of Science (JSPS).

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Author notes

  1. Tomoki Mochizuki

    Present address: Graduate Division of Nutritional and Environmental Sciences, University of Shizuoka, Shizuoka, 422-8526, Japan

  2. Makoto Watanabe

    Present address: Agriculture Institute, Tokyo University of Agriculture and Technology, Tokyo, 183-8509, Japan

  3. Kimitaka Kawamura

    Present address: Chubu Institute for Advanced Studies, Chubu University, Kasugai, 487-8501, Japan

Authors and Affiliations

  1. Research Faculty of Agriculture, School of Agriculture, Hokkaido University, Sapporo, 060-85889, Japan

    Evgenios Agathokleous, Tetsuichi Sakikawa, Shahenda A. Abu ElEla, Makoto Watanabe & Takayoshi Koike

  2. Hokkaido Research Center, Forestry and Forest Products Research Institute (FFPRI), 7 Hitsujigaoka, Sapporo, Hokkaido, 062-8516, Japan

    Evgenios Agathokleous

  3. Entomology Department, Faculty of Science, Cairo University, Giza, Egypt

    Shahenda A. Abu ElEla

  4. Institute of Low Temperature Science, Hokkaido University, Sapporo, 060-0814, Japan

    Tomoki Mochizuki & Kimitaka Kawamura

  5. Hokkaido University Forests, Sapporo, 060-0809, Japan

    Masahiro Nakamura

Authors
  1. Evgenios Agathokleous
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  2. Tetsuichi Sakikawa
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Corresponding authors

Correspondence to Evgenios Agathokleous or Takayoshi Koike.

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Funding

This study was funded in part by Grant-in-Aid from JSPS through Type B program (26292075 to T. Koike; 26450188 to M. Nakamura). JSPS is a nonprofit organization.

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The authors declare that they have no conflict of interest.

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Responsible editor: Philippe Garrigues

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Agathokleous, E., Sakikawa, T., Abu ElEla, S.A. et al. Ozone alters the feeding behavior of the leaf beetle Agelastica coerulea (Coleoptera: Chrysomelidae) into leaves of Japanese white birch (Betula platyphylla var. japonica). Environ Sci Pollut Res 24, 17577–17583 (2017). https://doi.org/10.1007/s11356-017-9369-7

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