One more step toward a push-pull strategy combining both a trap crop and plant volatile organic compounds against the cabbage root fly Delia radicum
The “push-pull” strategy aims at manipulating insect pest behavior using a combination of attractive and repulsive stimuli using either plants derived volatile organic compounds or insect host plant preferences. In a field experiment using broccoli as a crop, we combined in a “push-pull” context the oviposition deterrent effect of dimethyl disulfide and the attractive effect of a Chinese cabbage strip enhanced with Z-3-hexenyl-acetate. The push component dimethyl disulfide reduced Delia radicum L. (Diptera: Anthomyiidae) oviposition on broccoli by nearly 30%, and applying Z-3-hexenyl-acetate in the pull component of Chinese cabbage increased it by 40%. Moreover, pest infestation was 40% higher in Chinese cabbage compared to broccoli and parasitism by Trybliographa rapae Westwood (Hymenoptera: Figitidae) was four times higher on this trap plant. In addition, lab experiments confirmed that Chinese cabbage is a more suitable host plant than broccoli for the cabbage root fly. Taken together, our results demonstrate the technical possibility of using a push-pull strategy to manipulate the egg-laying behavior of D. radicum in the field.
KeywordsBehavioral manipulation Plant-insect interactions Volatile organic compounds Brassicaceae Delia radicum L. (Diptera: Anthomyiidae) Parasitoid
Volatile organic compound
We thank the staff of the “Domaine experimental de la Motte au Vicomte UE0787” (INRA Center, Le Rheu, France) and especially Gabriel Nedelec for his advice and help with the field experiment. The authors acknowledge Valentin Gaudu and Chloe Guyot for the precious help provided during the monitoring of the field experiment.
AMC, DP, SD, and FL conceived and designed research. VF helped designing the field experiment. DP and SD conducted laboratory experiments. FL and VC conducted field experiments. FL and DP analyzed data. FL wrote the manuscript. All authors commented and approved the manuscript.
Compliance with ethical standards
This work was financed by the project “PURE” and a grant of the French Ministry for Research (MESR) to FL.
Conflict of interest
Authors declare that they have no conflict of interest.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
- Ameye M, Audenaert K, De Zutter N, Steppe K, Van Meulebroek L, Vanhaecke L, De Vleesschauwer D, Haesaert G, Smagghe G (2015) Priming of wheat with the green leaf volatile Z-3-hexenyl acetate enhances defense against Fusarium graminearum but boosts deoxynivalenol production. Plant Physiol 167:1671–1684. doi: 10.1104/pp.15.00107 CrossRefGoogle Scholar
- Badenes-Perez FR, Reichelt M, Gershenzon J, Heckel DG (2014) Using plant chemistry and insect preference to study the potential of Barbarea (Brassicaceae) as a dead-end trap crop for diamondback moth (Lepidoptera: Plutellidae). Phytochemistry 98:137–144. doi: 10.1016/j.phytochem.2013.11.009 CrossRefGoogle Scholar
- Baur R, Birch ANE, Hopkins RJ, Griffiths DW, Simmonds MSJ, Stadler E (1996) Oviposition and chemosensory stimulation of the root flies Delia radicum and D. floralis in response to plants and leaf surface extracts from resistant and susceptible Brassica genotypes. Entomol Exp Appl 78:61–75. doi: 10.1111/j.1570-7458.1996.tb00765.x CrossRefGoogle Scholar
- Blackmore MS, Lord CC (2000) The relationship between size and fecundity in Aedes albopictus. Journal of Vector Ecology 25:212–217Google Scholar
- Coaker TH, Finch S (1971) The cabbage root fly, Erioischia brassicae (Bouché). Report of the National Vegetable Research Station for 1970:23–42Google Scholar
- Curtis J (1860) Farm insects. Blackie & Son, GlasgowGoogle Scholar
- den Ouden H, Theunissen J (1988) Preference and non-preference in monitoring cabbage root fly, Delia radicum/D. Brassicae/, oviposition by traps. Acta Hortic 11–14. doi: 10.17660/ActaHortic.1988.219.1
- Dugravot S, Grolleau F, Macherel D, Rochetaing A, Hue B, Stankiewicz M, Huignard J, Lapied B (2003) Dimethyl disulfide exerts insecticidal neurotoxicity through mitochondrial dysfunction and activation of insect K(ATP) channels. J Neurophysiol 90:259–270. doi: 10.1152/jn.01096.2002 CrossRefGoogle Scholar
- Ferry A (2007) Écologie chimique appliquée à la lutte contre Delia radicum, la mouche du chou. PhD in Biology, Université de Rennes 1Google Scholar
- Ferry A, Dugravot S, Delattre T, Christides JP, Auger J, Bagneres AG, Poinsot D, Cortesero AM (2007) Identification of a widespread monomolecular odor differentially attractive to several Delia radicum ground-dwelling predators in the field. J Chem Ecol 33:2064–2077. doi: 10.1007/s10886-007-9373-3 CrossRefGoogle Scholar
- Freuler J, Fischer S (1982) Description d'un piège à oeufs pour la mouche du chou, Delia brassicae Wiedemann. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 55:77–85Google Scholar
- Ikeshoji T, Ishikawa Y, Matsumoto Y (1981) Ecological and chemical interactions between onion and onion maggot, Hylemya antiqua (Diptera: Anthomyiidae). Review of Plant Protection Research 14:141–149Google Scholar
- Kergunteuil A, Dugravot S, Danner H, van Dam NM, Cortesero AM (2015) Characterizing volatiles and attractiveness of five brassicaceous plants with potential for a ‘push-pull’ strategy toward the cabbage root fly, Delia radicum. J Chem Ecol 41:330–339. doi: 10.1007/s10886-015-0575-9 CrossRefGoogle Scholar
- Khan ZR, Pickett JA, van den Berg J, Wadhams LJ, Woodcock CM (2000) Exploiting chemical ecology and species diversity: stem borer and striga control for maize and sorghum in Africa. Pest Manag Sci 56:957–962. doi: 10.1002/1526-4998(200011)56:11<957::aid-ps236>3.0.co;2-t CrossRefGoogle Scholar
- Lenth RV (2014) lsmeans: least-squares means. http://CRAN.R-project.org/package=lsmeans. Accessed: Nov 2015
- Pyke B, Rice M, Sabine B, Zalucki MP (1987) The push-pull strategy—behavioural control of Heliothis. Aust Cotton Grower May–July:7–9Google Scholar
- R_Core_Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
- Roessingh P, Stadler E, Baur R, Hurter J, Ramp T (1997) Tarsal chemoreceptors and oviposition behaviour of the cabbage root fly (Delia radicum) sensitive to fractions and new compounds of host-leaf surface extracts. Physiol Entomol 22:140–148. doi: 10.1111/j.1365-3032.1997.tb01151.x CrossRefGoogle Scholar
- Stern VM, Mueller A, Sevacher V, Way M (1969) Lygus bug control in cotton through alfalfa interplanting. Calif Agric 23:8–10Google Scholar
- Varis A-L (1967) Studies on the biology of the cabbage root fly (Hylemya brassicae Bouché) and the turnip root fly (Hylemya floralis Fall.) Ann Agr Fenn 6:1–13Google Scholar