Skip to main content Accessibility help

Chemical investigations of volatile kairomones produced by Hyphantria cunea (Drury), a host of the parasitoid Chouioia cunea Yang

  • G. Zhu (a1), L. Pan (a1), Y. Zhao (a1), X. Zhang (a1), F. Wang (a1), Y. Yu (a2), W. Fan (a1), Q. Liu (a1), S. Zhang (a3) and M. Li (a1)...


In tritrophic ‘plants–herbivores–natural enemies’ systems, there are relatively few reports concerning the role(s) of kairomones in pupal parasitism. Chouioia cunea Yang (Hymenoptera: Eulophidae), an endoparasitic chalcid wasp, parasitizes pupae of the fall webworm (Hyphantria cunea Drury). The role of host-related kairomones was investigated using electroantennogram (EAG) and behavioral techniques. Chemicals from some host stages (pupae) and host by-products (frass), induced arrestment behavior of female parasitoids, while chemicals from prepupae, were inactive. Gas chromatography–mass spectrometry analysis of volatiles collected from pupae, frass and prepupae using solid-phase microextration revealed seven compounds with carbon chain lengths ranging from C4 to C20. All of the chemicals elicited significant EAG responses in C. cunea. Y-tube olfactometer bioassays demonstrated a significant positive response of mated female C. cunea to 1-dodecene. These data provide a better understanding of the host location mechanisms of pupal parasitoid.


Corresponding author

*Author for correspondence Phone: 86-022-23766394 Fax: 86-022-23766539 E-mail:


Hide All
† These authors contributed equally to this work.



Hide All
Aak, A. & Knudsen, G.K. (2012) Egg developmental status and the complexity of synthetic kairomones combine to influence attraction behaviour in the blowfly Calliphora vicina . Physiological Entomology 37, 127135.
Afsheen, S., Wang, X., Li, R., Zhu, C.S. & Lou, Y.G. (2008) Differential attraction of parasitoids in relation to specificity of kairomones from herbivores and their by-products. Insect Science 15, 381397.
Azandeme-Hounmalon, G.Y., Torto, B., Fiaboe, K.K.M., Subramanian, S., Kreiter, S. & Martin, T. (2016) Visual, vibratory, and olfactory cues affect interactions between the red spider mite Tetranychus evansi and its predator Phytoseiulus longipes . Journal of Pest Science 89, 137152.
Bukovinszky, T., Poelman, E.H., Kamp, A., Hemerik, L., Prekatsakis, G. & Dicke, M. (2012) Plants under multiple herbivory: consequences for parasitoid search behaviour and foraging efficiency. Animal Behaviour 83(2), 501509.
Chiu-Alvarado, P., Barrera, J.F. & Rojas, J.C. (2009) Attraction of Prorops nasuta (Hymenoptera: Bethylidae) a parasitoid of the coffee berry borer (Coleoptera: Curculionidae), to host-associated olfactory cues. Annals of the Entomological Society America 102, 166171.
Costa, A. & Reeve, J.D. (2011) Olfactory experience modifies semiochemical responses in a bark beetle predator. Journal of Chemical Ecology 37, 11661176.
Dicke, M. & Baldwin, I.T. (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends in Plant Science 15(3), 167175.
Gao, B.J., Du, J., Gao, S.H. & Liu, J.X. (2010) Genetic diversity and differentiations of fall webworm (Hyphantria cunea) populations. Scientia Silvae Sinicae 8(46), 120124.
Giunti, G., Benelli, G., Conte, G., Mele, M., Caruso, G., Gucci, R., Flamini, G. & Canale, A. (2016) VOCs-mediated location of olive fly larvae by the braconid parasitoid Psyttalia concolor: a multivariate comparison among VOC bouquets from three olive cultivars. Biomed Research International 2016, ID, 7827615. DOI: 10.1155/2016/7827615.
Gonzalez, J.M., Cusumano, A., Williams, H.J., Colazza, S. & Vinson, S.B. (2011) Behavioral and chemical investigations of contact kairomones released by the mud dauber wasp Trypoxylon politum, a host of the parasitoid Melittobia digitata . Journal of Chemical Ecology 37, 629639.
Hofstetter, R.W., Gaylord, M.L., Martinson, S. & Wagner, M.R. (2012) Attraction to monoterpenes and beetle-produced compounds by syntopic Ips and Dendroctonus bark beetles and their predators. Agricultural and Forest Entomology 14, 207215.
Hou, Z.Y. & Yan, F.S. (1995) Electroantennogram response of Lysiphlebia japonica Ashmead (Homoptera: Aphidiidae) to some cotton plant volatiles and cotton aphid pheromones. Entomologia Sinica 2, 253264.
Ji, R., Xie, B.Y., Li, X.H., Gao, Z.X. & Li, D.M. (2007) Research progress on the invasive species, Hyphantria cunea. Entomological Knowledge 40(01), 1318.
Kashima, Y. & Miyazawa, M. (2014) Chemical composition and aroma evaluation of essential oils from Evolvulus alsinoides L. Chemical & Biodiversity 11(3), 396407.
Kong, X.B., Liu, K.W., Wang, H.B., Zhang, S.F. & Zhang, Z. (2012) Identification and behavioral evaluation of sex pheromone components of the Chinese pine caterpillar moth, Dendrolimus tabulaeformis . PLoS ONE 7, e33381.
Liu, S.H., Norris, D.M. & Lyne, P. (1989) Volatiles from the foliage of soybean, Glycine max, and lima bean, Phaseolus lunatus: their behavioral effects on the insects Trichoplusia ni and Epilachna varivestis . Journal of Agricultural and Food Chemistry 37, 496501.
Lo Giudice, D., Riedel, M., Rostas, M., Peri, E. & Colazza, S. (2011) Host sex discrimination by an egg parasitoid on brassica leaves. Journal of Chemical Ecology 37, 622628.
Malik, U., Karmakar, A. & Barik, A. (2016) Attraction of the potential biocontrol agent Galerucella placida (Coleoptera: Chrysomelidae) to the volatiles of Polygonum orientale (Polygonaceae) weed leaves. Chemoecology 26, 4558.
Martin, J. & Lopez, P. (2012) Supplementation of male pheromone on rock substrates attracts female rock lizards to the territories of males: a field experiment. PLoS ONE 7, e30108.
Moon, J.K. & Shibamoto, T. (2009) Role of roasting conditions in the profile of volatile flavor chemicals formed from coffee beans. Journal of Agricultural and Food Chemistry 57(13), 58235831.
Mukherjee, A., Sarkar, N. & Barik, A. (2015) Momordica cochinchinensis (Cucurbitaceae) leaf volatiles: semiochemicals for host location by the insect pest, Aulacophora foveicollis (Coleoptera: Chrysomelidae). Chemoecology 25, 93104.
Norris, D.M. & Liu, S.H. (1991) Insect repellent containing 1-dodecene. US Patent 5030660.
Onagbola, E.O. & Fadamiro, H.Y. (2011) Electroantennogram and behavioral responses of Pteromalus cerealellae to odor stimuli associated with its host, Callosobruchus maculatus . Journal of Stored Product Research 47, 123129.
Penaflor, M.F.G.V., Erb, M., Miranda, L.A., Werneburg, A.G. & Bento, J.M.S. (2011) Herbivore-induced plant volatiles can serve as host location cues for a generalist and a specialist egg parasitoid. Journal of Chemical Ecology 37, 13041313.
Rani, P.U., Kumari, S.I., Sriramakrishna, T. & Sudhakar, T.R. (2007) Kairomones extracted from rice yellow stem borer and their influence on egg parasitization by Trichogramma japonicum Ashmead. Journal of Chemical Ecology 33, 5973.
Rousse, P., Chiroleu, F., Veslot, J. & Quilici, S. (2007) The host- and microhabitat olfactory location by Fopius arisanus suggests a broad potential host range. Physiological Entomology 32(4), 313321.
Sacchetti, P., Rossi, E., Bellini, L., Vernieri, P., Cioni, P.L. & Flamini, G. (2015) Volatile organic compounds emitted by bottlebrush species affect the behaviour of the sweet potato whitefly. Arthropod-Plant Interactions 9, 393403.
Schoonhoven, L.M., van Loon, J.J.A. & Dicke, M. (2005) Host-plant selection: how to find a host plant. pp. 136160, Insect-Plant Biology. 2nd edn. Oxford, Oxford University Press.
Seenivasagan, T. & Paul, A.V.N. (2011) Electroantennogram and flight orientation response of Cotesia plutellae to hexane extract of cruciferous host plants and larvae of Plutella xylostella . Entomological Research 41, 717.
Selli, S., Canbas, A., Varlet, V., Kelebek, H., Prost, C. & Serot, T. (2008) Characterization of the most odor-active volatiles of orange wine made from a Turkish cv. Kozan (Citrus sinensis L. osbeck). Journal of Agricultural and Food Chemistry 56(1), 227234.
Shamilov, A.S. (2008) American white moth in Dagestan. Zashchita I Karantin Rastenii 8, 29.
Snyder, J.C., Antonious, G.F. & Thacker, R. (2011) A sensitive bioassay for spider mite (Tetranychus urticae) repellency: a double bond makes a difference. Experimental and Applied Acarology 55(3), 215224.
Sullivan, G.T., Karaca, I., Ozman-Sullivan, S.K. & Yang, Z.Q. (2011) Chalcidoid parasitoids of overwintered pupae of Hyphantria cunea (Lepidoptera: Arctiidae) in hazelnut plantations of Turkey's central Black Sea region. Canadian Entomologist 143, 411414.
Vinson, S.B. (1991) Chemical signals used by parasitoids. Redia 74, 1542.
Vinson, S.B. (1998) The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biological Control 11, 7996.
Van Tol, R.W.H.M., Bruck, D.J., Griepink, F.C. & De Kogel, W.J. (2012) Field attraction of the vine weevil Otiorhynchus sulcatus to kairomones. Journal of Economic Entomology 105, 169175.
Vet, L.E.M. & Dicke, M. (1992) Infochemical use by natural enemies of herbivores in a tritrophic context. Annual Review of Entomology 37, 141172.
Webster, B., Bruce, T., Dufour, S., Birkemeyer, C., Birkett, M., Hardie, J.& Pickett, J. (2008) Identification of volatile compounds used in host location by the black bean aphid, Aphis fabae . Journal of Chemical Ecology 34, 11531161.
Willmer, P.G., Nuttman, C.V., Raine, N.E., Stone, G.N., Pattrick, J.G., Henson, K., Stillman, P., Mcilroy, L., Potts, S.G. & Knudsen, J.T. (2009) Floral volatiles controlling ant behaviour. Function Ecology 23, 888900.
Yang, Z.Q. (1989) A new genus and species of Eulophidae (Hymenoptera: Chalcidoidea) parasitizing Hyphantria cunea (Drury) (Lepidoptera: Arctiidae) in China. Entomotaxonomia 11(1–2), 117130.
Yang, Z.Q. (1990) Anatomy of internal reproductive system of Chouioia cunea (Hymenoptera, Chalcidoidea, Eulophidae). Scientia Silvae Sinicae 31(1), 2326.
Yang, Z.Q. (2004) Advance in bio-control researches of the important forest insect pests with natural enemies in China. Chinese Journal of Biological Control 20(4), 221227.
Yang, Z.Q. & Zhang, Y.A. (2007) Researches on techniques for biocontrol of the fall webworm, Hyphantria cunea, a severe invasive insect pest to China. Chinese Bulletin of Entomology 44(4), 465471.
Yang, X.Q., Wei, J.R. & Yang, Z.Q. (2001) A survey on insect natural enemies of Hyphantria cunea in Da lian District, Liaoning Province. Chinese Journal of Biological Control 17(1), 4042.
Yang, Z.Q., Wei, J.R. & Wang, X.Y. (2006) Mass rearing and augmentative releases of the native parasitoid Chouioia cunea for biological control of the introduced fall webworm Hyphantria cunea in China. Biocontrol 51, 401418.
Yang, Z.Q., Wang, X.Y., Wei, J.R., Qu, H.R. & Qiao, X.R. (2008) Survey of the native insect natural enemies of Hyphantria cunea (Drury) (Lepidoptera: Arctiidae) in China. Bulletin of Entomological Research 98, 293302.
Zhang, X.X. & Wang, Z.J. (2009) Research progress on the Hyphantria cunea (Drury) of alien invasive species. Journal of Anhui Agricultural Sciences 37(1), 215219.
Zhao, Y.N., Wang, F.Z., Zhang, X.Y., Zhang, S.H., Guo, S.L., Zhu, G.P., Liu, Q. & Li, M. (2016) Transcriptome and Expression Patterns of Chemosensory Genes in Antennae of the Parasitoid Wasp Chouioia cunea. PLoS ONE 11(2), e0148159. doi: 10.1371/journal.pone.0148159.
Zheng, Y.N., Qi, J.Y., Sun, S.H. & Yang, C.C. (2012) Advance in research of Chouioia cunea Yang (Hymenoptera: Eulophidade) and its biocontrol application in China. Chinese Journal of Biological Control 28(2), 275281.
Zheng, L.X., Wu, W.J. & Fu, Y.G. (2014) (±)-2-Hexanol from Pterocarpus indicus leaves as attractant for female Aleurodicus dispersus (Hemiptera: Aleyrodidae). African Entomology 22, 267272.
Zong, S., Luo, Y., Zhou, J. & Liu, S. (2012) Volatile compounds of healthy and insect-damaged Hippophae rhamnoides sinensis in natural and planted forests. Zeitschrift fur Naturforschung C 67(5–6), 244248.
Zvereva, E.L., Rank, N.E. (2004) Fly parasitoid Megaselia opacicornis uses defensive secretions of the leaf beetle Chrysomela lapponica to locate its host. Oecologia 140, 516522.



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed