Skip to main content
SpringerLink
Log in

Attraction of Parastethorus nigripes and other insect species to methyl salicylate and (Z)-3-hexenyl acetate dispensers in a citrus grove and vineyard in south-eastern Australia

  • Published:
Phytoparasitica Aims and scope Submit manuscript

Abstract

Herbivore-induced plant volatiles (HIPVs) play an important role in tritrophic interactions, and have the potential to attract beneficial arthropods into crops to enhance biological control of target pests. We conducted field trials in citrus and grapes to evaluate the response of abundant insect species to two HIPVs, methyl salicylate (MeSa) and (Z)-3-hexenyl acetate. Micromus tasmaniae (Hemerobiidae) showed significant attraction to MeSa, but only in the vineyard trial. Parastethorus nigripes (Coccinellidae) was also attracted to MeSa in the vineyard, but in the second citrus trial the treatment response was just outside the nominal 5% significance level. In the first citrus trial where P. nigripes was not separated taxonomically from the closely related coccinellid Stethorus vagans, a combined analysis was undertaken and significant attraction of both coccinellid species to MeSa was also observed. There was also a significant positive combined response of P. nigripes and S. vagans to (Z)-3-hexenyl acetate in the first citrus trial. Other predatory insect species did not respond to MeSa or (Z)-3-hexenyl acetate. As compared with the vineyard trial, weaker attraction of some insect species in the citrus trials may reflect high levels of background odour in the citrus orchard that could have interfered with normal insect olfactory responses. Our results support previous studies demonstrating coccinellids in the tribe Stethorini are often strongly attracted to MeSa. Deploying MeSa dispensers in vulnerable crops could attract increased numbers of P. nigripes, enhancing the biological control of pest tetranychid mites in Australian horticultural systems and reducing or eliminating the need for miticide applications.

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

Similar content being viewed by others

References

  • Agelopoulos, N., Birkett, M. A., Hick, A. J., Hooper, A. M., Pickett, J. A., Pow, E. M., Smart, L. E., Smiley, D. W. M., Wadhams, L. J., & Woodcock, C. M. (1999). Exploiting semiochemicals in insect control. Pesticide Science, 55, 225–235.

    Article  CAS  Google Scholar 

  • Azeem, M., Rajarao, G. K., Terenius, O., Nordlander, G., Nordenhem, H., Nagahama, K., Norin, E., & Borg-Karlson, A. K. (2015). A fungal metabolite masks the host plant odor for the pine weevil (Hylobius abietis). Fungal Ecology, 13, 103–111.

    Article  Google Scholar 

  • Bianchi, F. J. J. A., Schellhorn, N. A., & Cunningham, S. A. (2013). Habitat functionality for the ecosystem service of pest control: reproduction and feeding sites of pest and natural enemies. Agricultural and Forest Entomology, 15, 12–23.

    Article  Google Scholar 

  • Biddinger, D. J., Weber, D. C., & Hull, L. A. (2009). Coccinellidae as predators of mites: Stethorini in biological control. Biological Control, 51, 268–283.

    Article  Google Scholar 

  • Bruce, T. J. A., Martin, J. L., Pickett, J. A., Pye, B. J., Smart, L. E., & Wadhams, L. J. (2003). cis-jasmone treatment induces resistance in wheat plants against the grain aphid, Sitobion avenae (Fabricius) (Homoptera: Aphididae). Pest Management Science, 59, 1031–1036.

    Article  CAS  PubMed  Google Scholar 

  • Butler, D., Cullis, B. R., Gilmour, A. R., & Gogel, B. J. (2009). Analysis of mixed models for S language environments. ASReml-R reference manual. Queensland Department of Primary Industries and Fisheries, Brisbane / NSW Department of Primary Industries, Orange.

  • Colless, D. H. (1982). Australian Anthomyiidae (Diptera). Australian Journal of Zoology, 30, 81–91.

    Article  Google Scholar 

  • Colless, D. H., & McAlpine, D. K. (1991). Diptera (Flies). in: The Insects of Australia. A Textbook for Students and Research Workers (Vol. 2, 2nd ed.pp. 717–786). Melbourne: CSIRO / Melbourne University Press.

    Google Scholar 

  • Diatloff, A. (1965). Larvae of Rivellia sp. (Diptera : Platystomatidae) attacking the root nodules of Glycine javanica L. Journal of the Entomological Society of Queensland, 4, 86.

    Article  Google Scholar 

  • Dudareva, N., & Negre, F. (2005). Practical applications of research into the regulation of plant volatile emission. Current Opinion in Plant Biology, 8, 113–118.

    Article  CAS  PubMed  Google Scholar 

  • Field, R. P. (1979). Integrated pest control in Victorian peach orchards: the role of Stethorus spp. (Coleoptera: Coccinellidae). Journal of the Australian Entomological Society, 18, 315–322.

    Article  Google Scholar 

  • Flint, H. M., Salter, S. S., & Walters, S. (1979). Caryophyllene: an attractant for the green lacewing. Environmental Entomology, 8, 1123–1125.

    Article  CAS  Google Scholar 

  • Gadino, A. N., Walton, V. M., & Lee, J. C. (2012). Evaluation of methyl salicylate lures on populations of Typhlodromus pyri (Acari: Phytoseiidae) and other natural enemies in western Oregon vineyards. Biological Control, 63, 48–55.

    Article  CAS  Google Scholar 

  • Gencer, N. S., Kumral, N. A., Sivritepe, H. O., Seidi, M., Susurluk, H., & Senturk, B. (2009). Olfactory response of the ladybird beetle Stethorus gilvifrons to two preys and herbivore-induced plant volatiles. Phytoparasitica, 37, 217–224.

    Article  Google Scholar 

  • Gouinguene, S. P., & Turlings, T. C. J. (2002). The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiology, 129, 1296–1307.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harper, D. B., Hamilton, J. T. G., Kennedy, J. T., & McNally, K. J. (1989). Chloromethane, a novel methyl donor for biosynthesis of esters and anisoles in Phellinus pomaceus. Applied and Environmental Microbiology, 55, 1981–1989.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heil, M. (2004). Induction of two indirect defences benefits lima bean (Phaseolus lunatus, Fabaceae) in nature. Journal of Ecology, 92, 527–536.

    Article  Google Scholar 

  • van Herk, W. G., Vernon, R. S., Cronin, E. M. L., & Gaimari, S. D. (2015). Predation of Thereva nobilitata (Fabricius) (Diptera: Therevidae) on Agriotes obscurus L. (Coleoptera: Elateridae). Journal of Applied Entomology, 139, 154–157.

    Article  Google Scholar 

  • Hunter, M. D. (2002). A breath of fresh air: beyond laboratory studies of plant volatile – natural enemy interactions. Agricultural and Forest Entomology, 4, 81–86.

    Article  Google Scholar 

  • James, D. G. (2003a). Field evaluation of herbivore-induced plant volatiles as attractants for beneficial insects: methyl salicylate and the green lacewing, Chrysopa nigricornis. Journal of Chemical Ecology, 29, 1601–1609.

    Article  CAS  PubMed  Google Scholar 

  • James, D. G. (2003b). Synthetic herbivore-induced plant volatiles as field attractants for beneficial insects. Environmental Entomology, 32, 977–982.

    Article  CAS  Google Scholar 

  • James, D. G. (2005). Further field evaluation of synthetic herbivore-induced plant volatiles as attractant for beneficial insects. Journal of Chemical Ecology, 31, 481–495.

    Article  CAS  PubMed  Google Scholar 

  • James, D. G., & Grasswitz, T. W. (2005). Synthetic herbivore-induced plant volatiles increase field captures of parasitic wasps. BioControl, 50, 871–880.

    Article  CAS  Google Scholar 

  • James, D. G., & Price, T. S. (2004). Field testing of methyl salicylate for recruitment and retention of beneficial insects in grapes and hops. Journal of Chemical Ecology, 30, 1613–1628.

    Article  CAS  PubMed  Google Scholar 

  • Kanchiswamy, C. N., Malnoy, M., & Maffei, M. E. (2015). Chemical diversity of microbial volatiles and their potential for plant growth and productivity. Frontiers in Plant Science, 6, 151. https://doi.org/10.3389/fpls.2015.00151.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaplan, I. (2012). Trophic complexity and the adaptive value of damage-induced plant volatiles. PLoS Biology, 10, e1001437. https://doi.org/10.1371/journal.pbio.1001437.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karl, T., Guenther, A., Turnipseed, A., Patton, E. G., & Jardines, K. (2008). Chemical sensing of plant stress at the ecosystem scale. Biogeosciences, 5, 1287–1294.

    Article  CAS  Google Scholar 

  • Kenward, M. G., & Roger, J. H. (1997). The precision of fixed effects estimates from restricted maximum likelihood. Biometrics, 53, 983–997.

    Article  CAS  PubMed  Google Scholar 

  • Koethe, R. W., & Van Duyn, J. W. (1989). Soybean nodule fly, Rivellia quadrifasciata (Diptera: Platystomatidae): observations on adult food sources and responses to baits and traps. Journal of Agricultural Entomology, 6, 83–90.

    Google Scholar 

  • Kost, C., & Heil, M. (2008). The defensive role of volatile emission and extrafloral nectar secretion for lima bean in nature. Journal of Chemical Ecology, 34, 2–13.

    Article  CAS  Google Scholar 

  • Lee, J. C. (2010). Effect of methyl salicylate-based lures on beneficial and pest arthropods in strawberry. Environmental Entomology, 39, 653–660.

    Article  CAS  PubMed  Google Scholar 

  • Lentz, C., Petersen, G., Mölck, G., & Wyss, U. (2004). Olfactory orientation of the spider mite predator Stethorus punctillum. Mitteilungen der Deutschen Gesellschaft für Allgemeine und Angewandte Entomologie, 14, 191–194.

    Google Scholar 

  • Maeda, T., Kishimoto, H., Wright, L. C., & James, D. G. (2015). Mixture of synthetic herbivore-induced plant volatiles attracts more Stethorus punctum picipes (Casey) (Coleoptera: Coccinellidae) than a single volatile. Journal of Insect Behaviour, 28, 126–137.

    Article  Google Scholar 

  • Michereff, M. F. F., Laumann, R. A., Borges, M., Michereff-Filho, M., Diniz, I. R., Neto, A. L. F., & Moraes, M. C. B. (2011). Volatiles mediating a plant-herbivore-natural enemy interaction in resistant and susceptible soybean cultivars. Journal of Chemical Ecology, 37, 273–285.

    Article  CAS  PubMed  Google Scholar 

  • Paré, P. W., & Tumlinson, J. H. (1996). Plant volatile signals in response to herbivore feeding. Florida Entomologist, 79, 93–103.

    Article  Google Scholar 

  • Paré, P. W., & Tumlinson, J. H. (1999). Plant volatiles as a defence against insect herbivores. Plant Physiology, 121, 325–331.

    Article  PubMed  PubMed Central  Google Scholar 

  • R Development Core Team. (2016). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. https://www.R-project.org/.

    Google Scholar 

  • Rasgado, M. A., Malo, E. A., Crux-López, L., Rojas, J. C., & Toledo, J. (2009). Olfactory response of the Mexican fruit fly (Diptera: Tephritidae) to Citrus aurantium volatiles. Journal of Economic Entomology, 102, 585–594.

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Saona, C., Kaplan, I., Braasch, J., Chinnasamy, D., & Williams, L. (2011). Field responses of predaceous arthropods to methyl salicylate: a meta-analysis and case study in cranberries. Biological Control, 59, 294–303.

    Article  CAS  Google Scholar 

  • Sabelis, M., Janssen, A., Pallini, A., Venzon, M., Bruin, J., Drukker, B., & Scutareanu, P. (1999). Behavioural responses of predatory and herbivorous arthropods to induced plant volatiles: from evolutionary ecology to agricultural applications. In A. A. Agrawal, S. Tuzun, & E. Bent (Eds.), Induced plant defenses against pathogens and herbivores. Biochemistry, ecology and Agriculture (pp. 269–296). St Paul: APS Press.

    Google Scholar 

  • Schröder, R., & Hilker, M. (2008). The relevance of background odor in resource location by insects: a behavioural approach. Bioscience, 58, 308–316.

    Article  Google Scholar 

  • Simpson, M., Gurr, G. M., Simmons, A. T., Wratten, S. D., James, D. G., Leeson, G., & Nicol, H. I. (2011). Insect attraction to synthetic herbivore-induced plant volatile-treated field crops. Agricultural and Forest Entomology, 13, 45–57.

    Article  Google Scholar 

  • Skuhravá, M., Martinex, M., & Roques, A. (2010). Diptera. Chapter 10. In Roques, A., Kenis, M., Lees, D., Lopez-Vaamonde, C., Rabitsch, W., Rasplus, J-Y., & Roy, D. (Eds.). Alien terrestrial arthropods of Europe. BioRisk 4, 553–602. https://doi.org/10.3897/biorisk.4.53.

  • Ślipiński, A. (2007). Australian ladybird beetles (Coleoptera: Coccinellidae). Their biology and classification. Australian Biological Resources Study: Canberra.

    Google Scholar 

  • Soleyman-Nezhadiyan, E., & Laughlin, R. (1998). Voracity of larvae, rate of development in eggs, larvae and pupae, and flight seasons of adults of the hoverflies Melangyna viridiceps Macquart and Symosyrphus grandicornis Macquart (Diptera: Syrphidae). Australian Journal of Entomology, 37, 243–248.

    Article  Google Scholar 

  • Takabayashi, J., Dicke, M., & Posthumus, M. A. (1994). Volatile herbivore-induced terpenoids in plant-mite interactions: variation caused by biotic and abiotic factors. Journal of Chemical Ecology, 20, 1329–1354.

    Article  CAS  PubMed  Google Scholar 

  • Takabayashi, J., Sabelis, M. W., Janssen, A., Shiojiri, K., & Van Wijk, M. (2006). Can plants betray the presence of multiple herbivore species to predators and parasitoids? The role of learning in phytochemical information networks. Ecological Research, 21, 3–8.

    Article  Google Scholar 

  • Takahashi, H., Takafuji, A., Takabayashi, J., Yano, S., & Shimoda, T. (2001). Seasonal occurrence of specialist and generalist insect predators of spider mites and their response to volatiles from spider-mite-infested plants in Japanese pear orchards. Experimental and Applied Acarology, 25, 393–402.

    Article  CAS  PubMed  Google Scholar 

  • Thaler, J. S. (1999). Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature, 399, 686–688.

    Article  CAS  Google Scholar 

  • Tooker, J. F., Crumrin, A. L., & Hanks, L. M. (2005). Plant volatiles are behavioural cues for adult females of the gall wasp Antistrophus rufus. Chemoecology, 15, 85–88.

    Article  CAS  Google Scholar 

  • Turlings, T. C. J., Tumlinson, J. H., & Lewis, W. J. (1990). Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science, 250, 1251–1253.

    Article  CAS  PubMed  Google Scholar 

  • Waelti, M. O., Muhlemann, J. K., Widmer, A., & Schiestl, F. P. (2008). Floral odour and reproductive isolation in two species of Silene. Journal of Evolutionary Biology, 21, 111–121.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Woods, J. L., James, D. G., Lee, J. C., & Gent, D. H. (2011). Evaluation of airborne methyl salicylate for improved conservation biological control of two-spotted spider mite and hop aphid in Oregon hop yards. Experimental and Applied Acarology, 55, 401–416.

    Article  CAS  PubMed  Google Scholar 

  • Yu, H., Zhang, Y., Wu, K., Gao, X. W., & Guo, Y. Y. (2008). Field-testing of synthetic herbivore-induced plant volatiles as attractants for beneficial insects. Environmental Entomology, 37, 1410–1415.

    Article  CAS  PubMed  Google Scholar 

  • Zhu, J., & Park, K.-C. (2005). Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata. Journal of Chemical Ecology, 31, 1733–1746.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Robert Fiumara of Lillypilly Wines, Leeton for access to his vineyard. Peter Gillespie (NSW DPI), Dr. David Yeates and Dr. Adam Ślipiński (CSIRO Entomology) are thanked for providing assistance with insect identifications, and Dr. Shaun Winterton, California Department of Food and Agriculture, is thanked for providing information on the feeding biology of Therevidae. Glen Warren and Michelle Hallam provided invaluable assistance with the trapping program.

Author information

Authors and Affiliations

  1. NSW Department of Primary Industries, Yanco Agricultural Institute, Private Mail Bag, Yanco, NSW, 2703, Australia

    Mark M. Stevens, Richard J. Faulder, Jianhua Mo & Elizabeth M. Mudford

  2. Graham Centre for Agricultural Innovation (NSW Department of Primary Industries and Charles Sturt University), Wagga Wagga, NSW, Australia

    Mark M. Stevens, Richard J. Faulder, Jianhua Mo & Elizabeth M. Mudford

  3. NSW Department of Primary Industries, Wollongbar Primary Industries Institute, 1243 Bruxner Highway, Wollongbar, NSW, 2477, Australia

    Stephen G. Morris

Authors
  1. Mark M. Stevens
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Richard J. Faulder
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jianhua Mo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elizabeth M. Mudford
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stephen G. Morris
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark M. Stevens.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stevens, M.M., Faulder, R.J., Mo, J. et al. Attraction of Parastethorus nigripes and other insect species to methyl salicylate and (Z)-3-hexenyl acetate dispensers in a citrus grove and vineyard in south-eastern Australia. Phytoparasitica 45, 639–649 (2017). https://doi.org/10.1007/s12600-017-0619-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12600-017-0619-5

Keywords

Search

Navigation