Skip to main content
SpringerLink
Log in

Pea Aphids, Acyrthosiphon Pisum, Suppress Induced Plant Volatiles in Broad Bean, Vicia Faba

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

Abstract

Plants defend themselves against herbivory through several means, including the production of airborne volatile organic compounds (VOCs). These VOCs benefit plants by attracting natural enemies of their herbivores. The pea aphid, Acyrthosiphon pisum, is able to feed on its host plant, Vicia faba, without inducing detectable changes in plant VOC emission. Levels of VOCs emission are not significantly different between control plants and those fed upon by aphids for up to 5 days. Using a second herbivore, the beet armyworm caterpillar, Spodoptera exigua, we demonstrate that several expected caterpillar-induced VOCs are reduced when co-infested with pea aphids, thus demonstrating that pea aphids have the ability to inhibit the release of certain VOCs. This study shows, for the first time, that aphids not only avoid triggering plant volatile emission, but also can actively inhibit herbivore-induced volatiles.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Colazza, S., Mcelfresh, J. S., and Millar, J. G. 2004. Identification of volatile synomones, induced by Nezara viridula feeding and oviposition on bean spp., that attract the egg parasitoid Trissolcus basalis. J. Chem. Ecol. 30:945–964.

    Article  PubMed  CAS  Google Scholar 

  • Creelman, R. A., and Mullet, J. E. 1997. Biosynthesis and action of jasmonates in plants. Annu. Rev. Plant Physiol. 48:355–381.

    Article  CAS  Google Scholar 

  • Dawson, G. W., Griffiths, D. C., Pickett, J. A., Smith, M. C., and Woodcock, C. M. 1984. Natural inhibition of the aphid alarm pheromone. Entomol. Exp. Appl. 36:197–199.

    Article  CAS  Google Scholar 

  • Dawson, G. W., Griffiths, D. C., Pickett, J. A., Wadhams, L. J., and Woodcock, C. M. 1987. Plant-derived synergists of alarm pheromone from turnip aphid, Lipaphis (Hyadaphis) erysimi (Homoptera, Aphididae). J. Chem. Ecol. 13(7):1663–1671.

    Article  CAS  Google Scholar 

  • De Boer, J. G., Hordijk, C. A., Posthumus, M. A., and Dicke, M. 2008. Prey and non-prey arthropods sharing a host plant: effects on induced volatile emission and predator attraction. J. Chem. Ecol. 34:281–290.

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • De Vos, M., and Jander, G. 2009. Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana. Plant Cell Environ. 32:1548–1560.

    Article  PubMed  Google Scholar 

  • Degen, T., Dillmann, C., Marion-Poll, F., and Turlings, T. C. J. 2004. High genetic variability of herbivore-induced volatile emission within a broad range of maize inbred lines. Plant Physiol. 135:1928–1938.

    Article  PubMed  CAS  Google Scholar 

  • Delphia, C. M., Mescher, M. C., and De Moraes, C. M. 2007. Induction of plant volatiles by herbivores with different feeding habits and the effects of induced defenses on host-plant selection by thrips. J. Chem. Ecol. 33:997–1012.

    Article  PubMed  CAS  Google Scholar 

  • Dicke, M., Van Loon, J. J. A., and Soler, R. 2009. Chemical complexity of volatiles from plants induced by multiple attack. Nat. Chem. Biol. 5:317–324.

    Article  PubMed  CAS  Google Scholar 

  • Du, Y., Poppy, G. M., Powell, W., Pickett, J. A., Wadhams, L. J., and Woodcock, C. M. 1998. Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi. J. Chem. Ecol. 24:1355–1368.

    Article  CAS  Google Scholar 

  • Felton, G. W., and Tumlinson, J. H. 2008. Plant-insect dialogs: complex interactions at the plant-insect interface. Curr. Opin. Plant Biol. 11:457–463.

    Article  PubMed  CAS  Google Scholar 

  • Gouinguene, S., Degen, T., and Turlings, T. C. J. 2001. Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte). Chemoecology 11:9–16.

    Article  CAS  Google Scholar 

  • Han, B. Y., and Chen, Z. M. 2002a. Composition of the volatiles from intact and mechanically pierced tea aphid-tea shoot complexes and their attraction to natural enemies of the tea aphid. J. Agr. Food Chem. 50:2571–2575.

    Article  CAS  Google Scholar 

  • Han, B. Y., and Chen, Z. M. 2002b. Composition of the volatiles from intact and tea aphid-damaged tea shoots and their allurement to several natural enemies of the tea aphid. J. Appl. Entomol.-Zeitschrift Fur Angewandte Entomologie 126:497–500.

    CAS  Google Scholar 

  • Harmel, N., Almohamad, R., Fauconnier, M. L., Du Jardin, P., Verheggen, F., Marlier, M., Haubruge, E., and Francis, F. 2007. Role of terpenes from aphid-infested potato on searching and oviposition behavior of Episyrphus balteatus. Insect Sci. 14:57–63.

    Article  CAS  Google Scholar 

  • James, D. G. 2003. Field evaluation of herbivore-induced plant volatiles as attractants for beneficial insects: methyl salicylate and the green lacewing, Chrysopa nigricornis. J. Chem. Ecol. 29:1601–1609.

    Article  PubMed  CAS  Google Scholar 

  • Jimenez-Martinez, E. S., Bosque-Perez, N. A., Berger, P. H., Zemetra, R., Ding, H. J., and Eigenbrode, S. D. 2004. Volatile cues influence the response of Rhopalosiphum padi (Homoptera : Aphididae) to barley yellow dwarf virus-infected transgenic and untransformed wheat. Environ. Entomol. 33:1207–1216.

    Article  CAS  Google Scholar 

  • Kovats, E. S. 1988. Citation classic—gas-chromatographic characterization of organic-substances in the retention index system. CC/Phys. Chem. Earth 14–14.

  • Kunert, G., and Weisser, W. W. 2003. The interplay between density- and trait-mediated effects in predator-prey interactions: a case study in aphid wing polymorphism. Oecologia 135:304–312.

    PubMed  Google Scholar 

  • Loughrin, J. H., Manukian, A., Heath, R. R., and Tumlinson, J. H. 1995. Volatiles emitted by different cotton varieties damaged by feeding beet armyworm larvae. J. Chem. Ecol. 21:1217–1227.

    Article  CAS  Google Scholar 

  • Pareja, M., Mohib, A., Birkett, M. A., Dufour, S., and Glinwood, R. T. 2009. Multivariate statistics coupled to generalized linear models reveal complex use of chemical cues by a parasitoid. Anim. Behav. 77:901–909.

    Article  Google Scholar 

  • Poelman, E. H., Van Loon, J. J. A., and Dicke, M. 2008. Consequences of variation in plant defense for biodiversity at higher trophic levels. Trends Plant Sci. 13:534–541.

    Article  PubMed  CAS  Google Scholar 

  • Prado, E., and Tjallingii, W. F. 2007. Behavioral evidence for local reduction of aphid-induced resistance. J. Insect Sci. 7:1–8.

    Article  PubMed  Google Scholar 

  • Quiroz, A., Pettersson, J., Pickett, J. A., Wadhams, L. J., and Niemeyer, H. M. 1997. Semiochemicals mediating spacing behavior of bird cherry-oat aphid, Rhopalosiphum padi feeding on cereals. J. Chem. Ecol. 23:2599–2607.

    Article  CAS  Google Scholar 

  • Rodriguez-Saona, C., Crafts-Brandner, S. J., Williams, L., and Pare, P. W. 2002. Lygus hesperus feeding and salivary gland extracts induce volatile emissions in plants. J. Chem. Ecol. 28:1733–1747.

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Saona, C., Crafts-Brandner, S. J., and Canas, L. A. 2003. Volatile emissions triggered by multiple herbivore damage: beet armyworm and whitefly feeding on cotton plants. J. Chem. Ecol. 29:2539–2550.

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Saona, C., Chalmers, J. A., Raj, S., and Thaler, J. S. 2005. Induced plant responses to multiple damagers: differential effects on an herbivore and its parasitoid. Oecologia 143:566–577.

    Article  PubMed  Google Scholar 

  • Rodriguez-Saona, C. R., Musser, R. O., Vogel, H., Hum-Musser, S. M., and Thaler, J. S. 2010. Molecular, biochemical, and organismal analyses of tomato plants simultaneously attacked by herbivores from two feeding guilds. J. Chem. Ecol. 36:1043–1057.

    Article  PubMed  CAS  Google Scholar 

  • Runyon, J. B., Mescher, M. C., and De Moraes, C. M. 2008. Parasitism by Cuscuta pentagona attenuates host plant defenses against insect herbivores. Plant Physiol. 146:987–995.

    Article  PubMed  CAS  Google Scholar 

  • Tjallingii, W. F. 1995. Aphid-plant interactions: what goes on in the depth of the tissues? Proc/Section Exper. Appl. Entomol. Netherlands Entomological Society 6:163–169.

    Google Scholar 

  • Tjallingii, W. F., and Gabrys, B. 1999. Anomalous stylet punctures of phloem sieve elements by aphids. Entomol. Exp. Appl. 91:97–103.

    Article  Google Scholar 

  • Tooker, J. F., Rohr, J. R., Abrahamson, W. G., and De Moraes, C. M. 2008. Gall insects can avoid and alter indirect plant defenses. New Phytol. 178:657–671.

    Article  PubMed  CAS  Google Scholar 

  • Turlings, T. C. J., Bernasconi, M., Bertossa, R., Bigler, F., Caloz, G., and Dorn, S. 1998. The induction of volatile emissions in maize by three herbivore species with different feeding habits: possible consequences for their natural enemies. Biol. Control 11:122–129.

    Article  Google Scholar 

  • Zhang, P. J., Zheng, S. J., Van Loon, J. J. A., Boland, W., David, A., Mumm, R., and Dicke, M. 2009. Whiteflies interfere with indirect plant defense against spider mites in lima bean. Proc. Natl. Acad. Sci. USA. 106:21202–21207.

    Article  PubMed  CAS  Google Scholar 

  • Zhu, J. W., and Park, K. C. 2005. Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata. J. Chem. Ecol. 31:1733–1746.

    Article  PubMed  CAS  Google Scholar 

  • Zhu, J., Obrycki, J. J., Ochieng, S. A., Baker, T. C., Pickett, J. A., and Smiley, D. 2005. Attraction of two lacewing species to volatiles produced by host plants and aphid prey. Naturwissenschaften 92:277–281.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Mr. Bryan Banks of Volatile Assay Systems for equipment and technical assistance. Nathaniel McCartney assisted with maintenance and expertise in experimental and chemical procedures. Matthew Gordon, Chouc Vo, and John Mano provided essential procedural assistance as well as plant and aphid colony maintenance.

Author information

Author notes

  1. Ezra G. Schwartzberg

    Present address: Department of Entomology, University of Wisconsin-Madison, Madison, WI, 53703, USA

  2. Katalin Böröczky

    Present address: Department of Entomology, North Carolina State University, Raleigh, NC, 27695, USA

Authors and Affiliations

  1. Department of Entomology, Center for Chemical Ecology, The Pennsylvania State University, University Park, PA, 16802, USA

    Ezra G. Schwartzberg, Katalin Böröczky & James H. Tumlinson

Authors
  1. Ezra G. Schwartzberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Katalin Böröczky
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. James H. Tumlinson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ezra G. Schwartzberg.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schwartzberg, E.G., Böröczky, K. & Tumlinson, J.H. Pea Aphids, Acyrthosiphon Pisum, Suppress Induced Plant Volatiles in Broad Bean, Vicia Faba . J Chem Ecol 37, 1055–1062 (2011). https://doi.org/10.1007/s10886-011-0006-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-011-0006-5

Key Words

Search

Navigation