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Volatile Emissions from Aesculus hippocastanum Induced by Mining of Larval Stages of Cameraria ohridella Influence Oviposition by Conspecific Females

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Abstract

Larval stages of the horse chestnut leafminer Cameraria ohridella can completely destroy the surface of horse chestnut leaves, Aesculus hippocastanum. This study investigated the effect of the degree of leaf browning caused by the insect’s larvae on olfactory detection, aggregation, and oviposition of C. ohridella adults. The influence of A. hippocastanum flower scent on oviposition of the first generation was also evaluated. Utilizing gas chromatography coupled with parallel detection by mass spectrometry and electroantennography (GC-MS/EAD), more than 30 compounds eliciting responses from antennae of C. ohridella were detected. Oviposition and mining by C. ohridella caused significant changes in the profile of leaf volatiles of A. hippocastanum. After oviposition and subsequent mining by early larval stages (L1–L3), substances such as benzaldehyde, 1,8-cineole, benzyl alcohol, 2-phenylethanol, methyl salicylate, (E)-β-caryophyllene, and (E,E)-α-farnesene were emitted in addition to the compounds emitted by uninfested leaves. Insects were able to detect these compounds. The emitted amount of these substances increased with progressive larval development. During late larval stages (L4, L5) and severe loss of green leaf area, (E,E)-2,4-hexadienal, (E/Z)-linalool oxide (furanoid), nonanal, and decanal were also released by leaves. These alterations of the profile of volatiles caused modifications in aggregation of C. ohridella on leaves. In choice tests, leaves in early infestation stages showed no significant effect on aggregation, whereas insects avoided leaves in late infestation stages. Further choice tests with leaves treated with single compounds led to the identification of substances mediating an increase or decrease in oviposition.

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References

  • Bernays, E. A. and Chapman, R. F. 1994. Host-Plant Selection by Phytophagous Insects. Chapman & Hall. London, New York.

  • Boland, W., Ney, P., Jaenicke, L., and Gassmann, G. 1984. A “closed-loop-stripping” technique as a versatile tool for metabolic studies of volatiles, pp. 371–380, in P. Schreier (ed.). Analysis of Volatiles. Walter de Gruyter, Berlin.

    Google Scholar 

  • Bolter, C. J., Dicke, M., Van Loon, J. J. A., Visser, J. H., and Posthumus, M. A. 1997. Attraction of Colorado potato beetle to herbivore-damaged plants during herbivory and after its termination. J. Chem. Ecol. 23:1003–1023.

    Article  CAS  Google Scholar 

  • De Moraes, C. M., Lewis, W. J., Paré, P. W., Alborn, H. T., and Tumlinson, J. H. 1998. Herbivory-infested plants selectively attract parasitoids. Nature 393:570–573.

    Article  Google Scholar 

  • De Prins, J., De Prins, W., and De Coninck, E. 2003. The pupal morphology of Cameraria ohridella compared with that of the genus Phyllonorycter (Lep. Gracillariidae). J. Pest Sci. 76:145–150.

    Google Scholar 

  • Deschka, G. 1994. Die Roßkastanien-Miniermotte: Lebensbild eines blattminierenden Schädlings. Ökol. (Linz) 16:32–36.

    Google Scholar 

  • Deschka, G. and Dimic, N. 1986. Cameraria ohridella n. sp. aus Mazedonien, Jugoslawien (Lepidoptera, Lithocelletidae). Acta Entomol. Jugosl. 22:11–23.

    Google Scholar 

  • Dicke, M. 1999. Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? Entomol. Exp. Appl. 91:131–142.

    Article  CAS  Google Scholar 

  • Dicke, M. and Vet, L. E. M. 1999. Plant–carnivore interactions: Evolutionary and ecological consequences for plant, herbivore and carnivore, pp. 483–520, in H. Olff, V. K. Brown, and R. H. Drent (eds.). Herbivores: Between Plants and Predators. Blackwell, Oxford, UK.

    Google Scholar 

  • Dicke, M., van Beek, T. A., Posthumus, M. A., Dom, N. B., van Bokhoven, H., and de Groot, A. 1990. Isolation and identification of volatile kairomone that affects acarine predator–prey interaction: Involvement of host plant in its production. J. Chem. Ecol. 16:381–396.

    Article  CAS  Google Scholar 

  • Dicke, M., Van Poecke, R. M. P., and De Boer, J. G. 2003. Inducible indirect defence of plants: From mechanisms to ecological function. Basic Appl. Ecol. 4:27–42.

    Article  CAS  Google Scholar 

  • Färbert, P., Koch, U. T., Färbert, A., Staten, R. T., and Cardé, R. T. 1997. Pheromone concentration measured with electroantennogram in cotton fields treated for mating disruption of Pectinophora gossypiella (Lepidoptera: Gelechiidae). Environ. Entomol. 26:1105–1116.

    Google Scholar 

  • Freise, J. F. 2001. Untersuchungen zur Biologie und Ökologie der Rosskastanien-Miniermotte, Cameraria ohridella Desch. & Dim. (Lep., Gracillariidae). PhD dissertation, Technical University of Munich, Germany.

  • Freise, J. F., Heitland, W., and Tosevski, I. 2002. Parasitism of the horse chestnut leaf miner, Cameraria ohridella Deschka and Dimic (Lep., Gracillariidae), in Serbia and Macedonia. Anz. Schaedlingskd. 75:152–157.

    Article  Google Scholar 

  • Gilbert, M. and Grégoire, J. C. 2003. Visual, semi-quantitative assessments allow accurate estimates of leafminer population densities: An example comparing image processing and visual evaluation of damage by the horse chestnut leafminer C. ohridella (Lep. Gracillariidae). J. Appl. Entomol. 127:354–359.

    Article  Google Scholar 

  • Grabenweger, G. 2003. Parasitism of different larval stages of Cameraria ohridella. BioControl 48:671–684.

    Article  Google Scholar 

  • Grabenweger, G., Avtzis, N., Girardoz, S., Hrasovec, B., Tomov, R., and Kenis, M. 2005. Parasitism of Cameraria ohridella (Lep. Gracillariidae) in natural and artificial horse-chestnut stands in the Balkans. J. Agric. For. Entomol. 7:291–296.

    Article  Google Scholar 

  • Hellrigl, K. 1999. Die Verbreitung der Roßkastanien-Miniermotte Cameraria ohridella Deschka & Dimic 1986 (Lepidoptera, Gracillariidae) in Südtirol. Veroeffentl. Tiroler Landesmus. Ferdinandeum 79:265–300.

    Google Scholar 

  • Hellrigl, K. 2001. Neue Untersuchungen über die Rosskastanien-Miniermotte C. ohridella (Deschka & Dimic), 1986 (Lep., Gracillariidae). Gredleriana 1:9–81.

    Google Scholar 

  • Hobson, K. R., Wood, D. L., Cool, L. G., White, P. R., Ohtsuka, T., Kubo, I., and Zavarin, E. 1993. Chiral specificity in responses by the bark beetle Dendroctonus valens to host kairomones. J. Chem. Ecol. 19:1837–1846.

    Article  CAS  Google Scholar 

  • Hochmuth, D. H. 2004. MassFinder für Windows [Software zur Analyse chemischer Verbindungen] Version http://www.massfinder.com.

  • Hopke, J., Donath, J., Blechert, S., and Boland, W. 1994. Herbivore-induced volatiles: The emission of acyclic homoterpenes from leaves of Phaseolus and Zea mays can be triggered by a β-glucosidase and jasmonic acid. FEBS Lett. 352:146–150.

    Article  PubMed  CAS  Google Scholar 

  • Johne, A. B. 2001. Ein Beitrag zum Auftreten und zur Verbreitung der Kastanienminiermotte (Cameraria ohridella Deschka & Dimic). Diploma thesis, University of Applied Science, Dresden.

  • Johne, A. B., Füldner, K., Weißbecker, B., and Schütz, S. 2003. Kopplung der phänologischen Entwicklung der Rosskastanie A. hippocastanum mit Lebenszyklus und Verhalten der Kastanienminiermotte C. ohridella. Nachrichtenbl. Dtsch. Pflanzenschutz. 55:213–220, 299.

    Google Scholar 

  • Johne, B., Schütz, S., and Füldner K. 2005. Hinweise zur Morphologie und Entwicklung der Kastanienminiermotte Cameraria ohridella (Lep.: Gracillariidae) im südlichen Niedersachsen (NW-Deutschland). Philippia Ottoneum Kassel 12:137–146.

    Google Scholar 

  • Kindl, J., Kanlinová, B., Freise, J., Heitland, W., Augustin, S., Guichard, S., Avtzis, N., and Svatoš, A. 2002. Monitoring the population dynamics of the horse chestnut leafminer Cameraria ohridella with a synthetic pheromone in Europe. Plant Protect. Sci. 38:131–138.

    Google Scholar 

  • König, W. A., Joulain, D., and Hochmuth, D. H. 2004. Terpenoids and Related Constituents of Essential Oils [database], http://www.massfinder.com.

  • Langenheim, J. H. 1994. Higher plant terpenoids: A phytocentric overview of their ecological roles. J. Chem. Ecol. 20:1223–1280.

    Article  CAS  Google Scholar 

  • Lozán, J. L. and Kausch, H. 1998. Angewandte Statistik für Naturwissenschaftler. Parey Verlag, Berlin.

    Google Scholar 

  • Maeda, T. and Takabayashi, J. 2001. Production of herbivore-induced plant volatiles and their attractiveness to Phytoseius persimilis (Acari: Phytoseiidae) with changes of Tetranychus urticae (Acari: Tetranychidae) density on a plant. Appl. Entomol. Zool. 36:47–52.

    Article  Google Scholar 

  • Matsuki, M., Clarke, B., Ebbers, M., Eschler, B., Foley, W., Lawler, I., Moore, B., Watson M., and Floyd R. B. 2001. Herbivory by Christmas beetles in Southeast Australia in relation to intra specific variation in Eucalyptus leaf chemistry, pp. 29–53, in R. B. Floyd and W. J. Foley (eds.). Identifying Pest Resistant Eucalyptus Using Near-infrared Spectroscopy. Rural Industries Research and Development Corporation, Australia.

    Google Scholar 

  • OriginLab, 2002. ORIGIN für Windows [Software für Datenanalyse und Technische Graphiken] Version 7, http://www.OriginLab.com.

  • Pschorn-Walcher, H. 1994. Freiland Biologie der eingeschleppten Roßkastanien-Miniermotte Cameraria ohridella Deschka and Dimic (Lep., Gracillariidae) im Wienerwald. Linzer Biol. Beitr. 26:633–642.

    Google Scholar 

  • Röse, U. S. R., Manukian, A., Heath, R. R., and Tumlinson, J. H. 1996. Volatile semichemicals released from undamaged cotton leaves. Plant Physiol. 111:487–495.

    PubMed  Google Scholar 

  • Schütz, S. 2001. Der Einfluss verletzungsinduzierter Emissionen der Kartoffelpflanze (S. tuberosum) auf die geruchliche Wirtspflanzenfindung und -auswahl durch den Kartoffelkäfer (L. decemlineata). Habilitation. Justus Liebig University, Gießen.

    Google Scholar 

  • Schütz, S., Weißbecker, B., Klein, A., and Hummel, H. E. 1997. Host plant selection of the Colorado potato beetle as influenced by damage-induced volatiles of the potato plant. Naturwissenschaften 84:212–217.

    Article  Google Scholar 

  • Schütz, S., Weissbecker, B., Koch, U. T., and Hummel, H. E. 1999. Detection of volatiles released by diseased potato tubers using a biosensor on the basis of intact insect antennae. Biosens. Bioelectron. 14:221–228.

    Article  Google Scholar 

  • Scutareanu, P., Drukker, B., Bruin, J., Posthumus, M. A., and Sabelis, M. W. 1997. Volatiles from psylla-infested pear trees and their possible involvement in attraction of anthocorid predators. J. Chem. Ecol. 23:2241–2260.

    Article  CAS  Google Scholar 

  • Šefrová, H. 2003. Invasions of Lithocolletinae species in Europe—causes, kinds, limits and ecological impact (Lepidoptera, Gracillariidae). Ecólogia (Bratislava) 22:132–124.

    Google Scholar 

  • Šefrová, H. and Skuhravý, V. 2000. The larval morphologie of Cameraria ohridella Deschka & Dimic compared with the Phyllonorycter Hübner (Lepidoptera, Gracillariidae). Acta Univ. Agric. Silvic. Mendel. Brun. 4:23–30.

    Google Scholar 

  • Shulaev, V., Silverman, P., and Raskin, I. 1997. Airborne signalling by methyl salicylate in plant pathogen resistance. Nature 385:718–721.

    Article  CAS  Google Scholar 

  • Skuhravý, V. 1999. Zusammenfassende Betrachtung der Kenntnisse über die Rosskastanienminiermotte, Cameraria ohridella Deschka & Dimic (Lep., Gracillariidae). Anz. Schädlingskund. 72:95–99.

    Google Scholar 

  • StatSoft, Inc., 2003. STATISTICA für Windows [Software-System für Datenanalyse] Version 6, http://www.statsoft.com.

  • Steinbauer, M. J. and Wanjura, W. J. 2002. Christmas beetles (Anoplognathus spp., Coleoptera: Scarabaeidae) mistake peppercorn trees for eucalyptus. J. Nat. Hist. 36:119–125.

    Article  Google Scholar 

  • Svatoš, A., Kalinova, B., Hoskovec, M., Hovorka, O., and Hrdy, I. 1999. Identification of a new lepitopteran sex pheromone in picogram quantities using an antennal biodetector: (8E,10Z)-Tetradeca-8,10-dienal from Cameraria ohridella. Tetrahedron Lett. 40:7011–7014.

    Article  CAS  Google Scholar 

  • Tomiczek, C. and Krehan, H. 1998. The horsechestnut leafmining moth (Cameraria ohridella): A new pest in Central Europa. J. Arboric. 24:144–148.

    Google Scholar 

  • Visser, J. H. 1986. Host odor perception in phytophagous insects. Annu. Rev. Entomol. 31:121–44.

    Article  Google Scholar 

  • Visser, J. H. and A, D. A. 1978. General green leaf volatiles in the olfactory orientation of the Colorado beetle Leptinotarsa decemlineata. Entonol. Exp. Appl. 24:538–549.

    Google Scholar 

  • Weissbecker, B., Holighaus, G., and Schütz, S. 2004. Gas chromatography with mass spectrometric and electroantennographic detection: Analysis of wood odorants by direct coupling of insect olfaction and mass spectrometry. J. Chromatogr. A. 1056:209–216.

    Article  PubMed  CAS  Google Scholar 

  • Weissbecker, B., Van Loon, J. J. A., and Dicke, M. 1999. Electroantennogram responses of a predator, Perillus bioculatus, and its prey, Leptinotarsa decemlineata, to plant volatiles. J. Chem. Ecol. 25:313–2325.

    Article  Google Scholar 

  • Zhang, Q. H., Schlyter, F., Battisti, A., Birgersson, G., and Anderson, P. 2003. Electrophysiological responses of Thaumetopoea pityocampa females to host volatiles: Implications for host selection of active and inactive terpenes. J. Pest Sci. 76:103–107.

    Google Scholar 

  • Zhu, S., Yang, Y., Yu, H., Yue, Y., and Zou, G. 2005. Chemical composition and antimicrobial activity of the essential oils of Chrysanthemum indicum. J. Ethnopharmacol. 96:151–158.

    Article  CAS  Google Scholar 

  • Zunke, U. and Doobe, G. 2003. Neue Erkenntnisse zur Rosskastanien-Miniermotte durch das Hamburger Cameraria-Projekt, pp. 176–193, in D. Dujesiefken and P. Kockerbeck (eds.). Jahrbuch der Baumpflege 2003. Thalacker Medien, Braunschweig, Germany.

    Google Scholar 

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Acknowledgments

A.B. Johne was supported by the evangelisches Studienwerk “e. V. Villigst”. We are grateful to Wolfgang Gieße (City of Goettingen), Volker Meng (forest botanical garden of Georg August University), and Martin Levin (Revierförsterei Hainberg) for appropriation of trees, to Roman Kaiser, Givaudan, Switzerland, for the gift of (E,E)-α-farnesene, and to Wilhelm Boland, Max Planck Institute Jena, Germany, for the gift of (E)-4,8-dimethyl-1,3,7-nonatriene. We thank the members of our Institute Miriam Rameckers, Jörg Berger, Kira Duntemann, Reinhold Dankworth, and Ulrike Eisenwiener for their assistance. Moreover, thanks to Stefan Schwab for literature. We also appreciate the useful suggestions of the anonymous reviewers.

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Johne, A.B., Weissbecker, B. & Schütz, S. Volatile Emissions from Aesculus hippocastanum Induced by Mining of Larval Stages of Cameraria ohridella Influence Oviposition by Conspecific Females. J Chem Ecol 32, 2303–2319 (2006). https://doi.org/10.1007/s10886-006-9146-4

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