Skip to main content
SpringerLink
Log in

Ability of the Oriental Fruit Moth Grapholita molesta (Lepidoptera: Tortricidae) to Detoxify Juglone, the Main Secondary Metabolite of the Non-host Plant Walnut

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Many plant species produce toxic secondary metabolites that limit attacks by herbivorous insects, and may thereby constrain insect expansion to new hosts. Walnut is a host for the codling moth Cydia pomonella, which efficiently detoxifies the main walnut defensive compound juglone (5-hydroxy-1,4-naphthoquinone). The oriental fruit moth Grapholita molesta, which also belongs to the tribe Grapholitini, does not feed on walnut. We tested the performance of G. molesta, a highly invasive species, on artificial diets containing juglone at levels mimicking those found in walnut over the growing season. Juglone-fed G. molesta survived relatively well to adulthood, but larval and adult body weights were reduced, and larval developmental time was prolonged in a dose-dependent fashion. Chemical analysis of frass from larvae that had been fed a juglone-containing diet suggests that G. molesta reduces juglone to non-toxic 1,4,5-trihydroxynaphthalene in its gut. This unexpected tolerance of G. molesta to high levels of juglone may facilitate expansion of the host range beyond the current rosacean fruit trees used by this invasive pest.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Barnes, M. M. 1991. Codling moth occurrence, host race formation, and damage, pp. 313–327, in: L. van der Geest and H. Evenhuis (eds.). World Crop Pests, Vol. 5: Tortricid Pests. Their Biology, Natural Enemies and Control. Elsevier, Amsterdam.

  • Barbehenn, R., Poopat, U., and Spencer, B. 2003. Semiquinone and ascorbyl radicals in the gut fluids of caterpillars measured with EPR spectrometry. Insect Biochem. Molec. Biol. 33:125–130.

    Article  CAS  Google Scholar 

  • Bezemer, T. M. and Mills, N. J. 2001. Walnut development affects chemical composition and codling moth performance. Agric. Forest Entomol. 3:191–199.

    Article  Google Scholar 

  • Campos, F., Atkinson, J., Arnason, J. T., Philogene, B. J. R., Morand, P., Werstiuk, N. H., and Timmins, G. 1988. Toxicity and toxicokinetics of 6-methoxybenzoazolinone (MBOA) in the European corn borer, Ostrinia nubilalis (Hübner). J. Chem. Ecol. 14:989–1002.

    Article  CAS  Google Scholar 

  • Casado, D., Gemeno, C., Avilla, J., and Riba, M. 2008. Diurnal variation of walnut tree volatiles and electrophysiological responses in Cydia pomonella (Lepidoptera: Tortricidae). Pest Manag. Sci. 64:736–747.

    Article  PubMed  CAS  Google Scholar 

  • Chen, M. H. and Dorn, S. 2009. Reliable and efficient discrimination of four internal fruit-feeding Cydia and Grapholita species (Lepidoptera: Tortricidae) by polymerase chain reaction-restriction fragment length polymorphism. J. Econ. Entomol. 102:2209–2216.

    Article  PubMed  CAS  Google Scholar 

  • Chen, M. H. and Dorn, S. 2010. Microsatellites reveal genetic differentiation among populations in an insect species with high genetic variability in dispersal, the codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae). Bull. Entomol. Res. 100:75–85.

    Article  PubMed  CAS  Google Scholar 

  • Cisneros, F. H. and Barnes, M. M. 1974. Contribution to the biological and ecological characterization of apple and walnut host races of codling moth, Laspeyresia pomonella (L.): Moth longevity and oviposition capacity. Environ. Entomol. 3:402–406.

    Google Scholar 

  • Clark, A. M., Jurgens, T. M., and Hufford, C. D. 1990. Antimicrobial activity of juglone. Phytother. Res. 4:11–14.

    Article  Google Scholar 

  • Colaric, M., Veberic, R., Solar, A., Hudina, M., and Stampar, F. 2005. Phenolic acids, syringaldehyde, and juglone in fruits of different cultivars of Juglans regia L. J. Agric. Food Chem. 53:6390–6396.

    Article  PubMed  CAS  Google Scholar 

  • Dambroski, H. R., Linn, C., Berlocher, S. H., Forbes, A. A., Roelofs, W., and Feder, J. L. 2005. The genetic basis for fruit odor discrimination in Rhagoletis flies and its significance for sympatric host shifts. Evolution 59:1953–1964.

    PubMed  CAS  Google Scholar 

  • Erbout, N., De Meyer, M., Vangestel, C., and Lens, L. U. C. 2009. Host plant toxicity affects developmental rates in a polyphagous fruit fly: Experimental evidence. Biol. J. Linn. Soc. 97:728–737.

    Article  Google Scholar 

  • Faccoli, M., Blaženec, M., and Schlyter, F. 2005. Feeding response to host and nonhost compounds by males and females of the spruce bark bettle Ips typographus in a tunneling microassasy. J. Chem. Ecol. 31:745–759.

    Article  PubMed  CAS  Google Scholar 

  • Ferkovich, S. M. and Norris, D. M. 1971. Naphthoquinone inhibitors of Periplaneta americana and Scolytus multistriatus feeding: Ultraviolet difference spectra of reactions of juglone, menadione, and 1,4-naphthoquinone with amino acids and the indicated mechanism of feeding inhibition. Chem. Biol. Interact. 4:23–30.

    Article  PubMed  CAS  Google Scholar 

  • Hedin, P. A., Collum, D. H., Langhans, V. E., and Graves, C. H. 1980. Distribution of juglone and related compounds in pecan and their effect on Fusicladium effusum. J. Agric. Food Chem. 28:340–342.

    Article  CAS  Google Scholar 

  • Hern, A. and Dorn, S. 1999. Sexual dimorphism in the olfactory orientation of adult Cydia pomonella in response to α-farnesene. Entomol. Exp. Appl. 92:63–72.

    Article  CAS  Google Scholar 

  • Inbaraj, J. J. and Chignell, C. F. 2004. Cytotoxic action of juglone and plumbagin: A mechanistic study using HaCaT keratinocytes. Chem. Res. Toxicol. 17:55–62.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, K. S. and Felton, G. W. 2001. Plant phenolics as dietary antioxidants for herbivorous insects: A test with genetically modified tobacco. J. Chem. Ecol. 27:2579–2597.

    Article  PubMed  CAS  Google Scholar 

  • Keil, S., Gu, H., and Dorn, S. 2001. Response of Cydia pomonella to selection on mobility: Laboratory evaluation and field verification. Ecol. Entomol. 26:495–501.

    Article  Google Scholar 

  • Lindroth, R. L. 1989. Chemical ecology of luna moth: Effects of host plant on detoxification enzyme activity. J. Chem. Ecol. 15:2019–2029.

    Article  CAS  Google Scholar 

  • Lindroth, R. L., Anson, B. D., and Weisbrod, A. V. 1990. Effects of protein and juglone on gypsy moths: Growth performance and detoxification enzyme activity. J. Chem. Ecol. 16:2533–2547.

    Article  CAS  Google Scholar 

  • Louda, S. M., Kendall, D., Connor, J., and Simberloff, D. 1997. Ecological effects of an insect introduced for the biological control of weeds. Science 277:1088–1090.

    Article  CAS  Google Scholar 

  • Martel, C., Rejasse, A., Rousset, F., Bethenod, M. T., and Bourguet, D. 2003. Host-plant-associated genetic differentiation in Northern French populations of the European corn borer. Heredity 90:141–149.

    Article  PubMed  CAS  Google Scholar 

  • Moreau, J., Benrey, B., and Thiery, D. 2006. Assessing larval food quality for phytophagous insects: Are the facts as simple as they appear? Funct. Ecol. 20:592–600.

    Article  Google Scholar 

  • Myers, C. T., Hull, L. A., and Krawczyk, G. 2006. Effects of orchard host plants on the oviposition preference of the oriental fruit moth (Lepidoptera: Tortricidae). J. Econ. Entomol. 99:1176–1183.

    Article  PubMed  Google Scholar 

  • Natale, D., Mattiacci, L., Hern, A., Pasqualini, E., and Dorn, S. 2003. Response of female Cydia molesta (Lepidoptera: Tortricidae) to plant derived volatiles. Bull. Entomol. Res. 93:335–342.

    Article  PubMed  CAS  Google Scholar 

  • Natale, D., Mattiacci, L., Pasqualini, E., and Dorn, S. 2004. Apple and peach fruit volatiles and the apple constituent butyl hexanoate attract female oriental fruit moth, Cydia molesta, in the laboratory. J. Appl. Entomol. 128:22–27.

    Article  Google Scholar 

  • Notter-Hausmann, C., and Dorn, S. 2010. Relationship between behavior and physiology in an invasive pest species: Oviposition site selection and temperature-dependent development of the oriental fruit moth (Lepidoptera: Tortricidae). Environ. Entomol. 39:561–569.

    Article  PubMed  Google Scholar 

  • Phillips, P. A. and Barnes, M. M. 1975. Host race formation among sympatric apple, walnut, and plum populations of the codling moth, Laspeyresia pomonella. Ann. Entomol. Soc. Am. 68:1053–1060.

    Google Scholar 

  • Piñero, J. C. and Dorn, S. 2009. Response of female oriental fruit moth to volatiles from apple and peach trees at three phenological stages. Entomol. Exp. Appl. 131:67–74.

    Article  Google Scholar 

  • Piskorski, R. and Dorn, S. 2011. How the oligophage codling moth Cydia pomonella survives on walnut despite its secondary metabolite juglone. J. Insect Physiol. 57:744–750.

    Article  PubMed  CAS  Google Scholar 

  • Piskorski, R., Hanus, R., Vašíčková, S., Cvačka, J., Šobotník, J., Svatoš, A., and Valterová, I. 2007. Nitroalkenes and sesquiterpene hydrocarbons from the frontal gland of three Prorhinotermes termite species. J. Chem. Ecol. 33:1787–1794.

    Article  PubMed  CAS  Google Scholar 

  • Piskorski, R., Trematerra, P., and Dorn, S. 2010. Cuticular hydrocarbon profiles of the codling moth larvae, Cydia pomonella (Lepidoptera: Tortricidae), reflect those of their host plant species. Biol. J. Linn. Soc. 101:376–384.

    Article  Google Scholar 

  • Praz, C. J., Müller, A., and Dorn, S. 2008. Specialized bees fail to develop on non-host pollen: Do plants chemically protect their pollen? Ecology 89:795–804.

    Article  PubMed  Google Scholar 

  • Radix, P., Bastien, C., Jay-Allemand, C., Charlot, G., and Seigle-Murandi, F. 1998. The influence of soil nature on polyphenols in walnut tissues. A possible explanation of differences in the expression of walnut blight. Agronomie 18:627–637.

    Google Scholar 

  • Rodríguez, J., Olea-Azar, C., Cavieres, C., Norambuena, E., Delgado-Castro, T., Soto-Delgado, J., and Araya-Maturana, R. 2007. Antioxidant properties and free radical-scavenging reactivity of a family of hydroxynaphthalenones and dihydroxyanthracenones. Bioorg. Med. Chem. 15:7058–7065.

    Article  PubMed  Google Scholar 

  • Rothschild, G. and Vickers, R. 1991. Biology, ecology and control of the oriental fruit moth, pp. 389–412, in: L. van der Geest and H. Evenhuis (eds.). World Crop Pests, Vol. 5: Tortricid Pests. Their Biology, Natural Enemies and Control. Elsevier, Amsterdam.

  • Sedivy, C., Müller, A., and Dorn, S. 2011. Closely related pollen generalist bees differ in their ability to develop on the same pollen diet: Evidence for physiological adaptations to digest pollen. Funct. Ecol. 25:718–725.

    Article  Google Scholar 

  • Solar, A., Colarič, M., Usenik, V., and Stampar, F. 2006. Seasonal variations of selected flavonoids, phenolic acids and quinones in annual shoots of common walnut (Juglans regia L.). Plant Sci. 170:453–461.

    Article  CAS  Google Scholar 

  • Stampar, F., Solar, A., Hudina, M., Veberic, R., and Colaric, M. 2006. Traditional walnut liqueur - cocktail of phenolics. Food Chem. 95:627–631.

    Article  CAS  Google Scholar 

  • Summers, C. B. and Felton G. W. 1994. Prooxidant effects of phenolic acids on the generalist herbivore Helicoverpa zea (Lepidoptera: Noctuidae): Potential mode of action for phenolic compounds in plant anti-herbivore chemistry. Insect Biochem. Molec. Biol. 24:943–953.

  • Sun, M., Wang, Y., Song, Z., and Fang, G. 2007. Insecticidal activities and active components of the alcohol extract from green peel of Juglans mandshurica. J. Forestry Res. 18:62–64.

    Article  CAS  Google Scholar 

  • Thiboldeaux, R. L., Lindroth, R. L., and Tracy, J. W. 1994. Differential toxicity of juglone (5-hydroxy-1,4-naphthoquinone) and related naphthoquinones to saturniid moths. J. Chem. Ecol. 20:1631–1641.

    Article  CAS  Google Scholar 

  • Thiboldeaux, R. L., Lindroth, R. L., and Tracy, J. W. 1998. Effects of juglone (5-hydroxy-1,4-naphthoquinone) on midgut morphology and glutathione status in Saturniid moth larvae. Comp. Biochem. Physiol. C 120:481–487.

    PubMed  CAS  Google Scholar 

  • Torriani, M. V. G., Mazzi, D., Hein, S., and Dorn, S. 2010. Direct and correlated responses to artificial selection on flight activity in the oriental fruit moth (Lepidoptera: Tortricidae). Biol. J. Linn. Soc. 100:879–889.

    Article  Google Scholar 

  • Vallat, A. and Dorn, S. 2005. Changes in volatile emissions from apple trees and associated response of adult female codling moths over fruit-growing season. J. Agric. Food Chem. 53:4083–4090.

    Article  PubMed  CAS  Google Scholar 

  • Velten, G., Rott, A. S., Cardona, C., and Dorn, S. 2007. The inhibitory effect of the natural seed storage protein arcelin on the development of Acanthoscelides obtectus. J. Stored Prod. Res. 43:550–557.

    Article  CAS  Google Scholar 

  • Witzgall, P., Ansebo, L., Yang, Z., Angeli, G., Sauphanor, B., and Bengtsson, M. 2005. Plant volatiles affect oviposition by codling moths. Chemoecology 15:77–83.

    Article  CAS  Google Scholar 

  • Yu, S. J. 1987. Quinone reductase of phytophagous insects and its induction by allelochemicals. Comp. Biochem. Physiol. B 87:621–624.

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to Dominique Mazzi for helpful comments on the manuscript, and to Fabienne Hatt and Adriana Najar-Rodriguez for providing the insects. We thank the anonymous reviewers for their valuable comments.

Author information

Author notes

  1. Rafal Piskorski

    Present address: Innovative Environmental Services (IES) Ltd., Benkenstrasse 260, 4108, Witterswil, Switzerland

Authors and Affiliations

  1. Institute of Agricultural Sciences, Applied Entomology, ETH Zurich, Schmelzbergstrasse 9/LFO, 8092, Zurich, Switzerland

    Rafal Piskorski, Simon Ineichen & Silvia Dorn

Authors
  1. Rafal Piskorski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Simon Ineichen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Silvia Dorn
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Silvia Dorn.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Piskorski, R., Ineichen, S. & Dorn, S. Ability of the Oriental Fruit Moth Grapholita molesta (Lepidoptera: Tortricidae) to Detoxify Juglone, the Main Secondary Metabolite of the Non-host Plant Walnut. J Chem Ecol 37, 1110–1116 (2011). https://doi.org/10.1007/s10886-011-0015-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-011-0015-4

Key Words

Search

Navigation