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Anastrepha egg deposition induces volatiles in fruits that attract the parasitoid Fopius arisanus

Published online by Cambridge University Press:  07 December 2012

J. Pérez ,
J.C. Rojas ,
P. Montoya ,
P. Liedo  and
A. Castillo
J. Pérez*
Affiliation:
Departamento de Entomología Tropical, El Colegio de la Frontera Sur (ECOSUR), Carretera Antiguo Aeropuerto km 2.5, 30700 Tapachula, Chiapas, México
J.C. Rojas
Affiliation:
Departamento de Entomología Tropical, El Colegio de la Frontera Sur (ECOSUR), Carretera Antiguo Aeropuerto km 2.5, 30700 Tapachula, Chiapas, México
P. Montoya
Affiliation:
Programa Moscafrut SAGARPA-IICA, Central Poniente 14, 30700 Tapachula, Chiapas, México
P. Liedo
Affiliation:
Departamento de Entomología Tropical, El Colegio de la Frontera Sur (ECOSUR), Carretera Antiguo Aeropuerto km 2.5, 30700 Tapachula, Chiapas, México
A. Castillo
Affiliation:
Programa Moscafrut SAGARPA-IICA, Central Poniente 14, 30700 Tapachula, Chiapas, México
*
* Author for correspondence Fax: +52 9626289806 E-mail: [email protected]
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Abstract

Fopius arisanus is a solitary egg–pupal endoparasitoid that attacks several species of tephritid fruit flies, particularly Bactrocera spp. This species, indigenous from the Indo-Australian region, was introduced into Mexico for biological control purposes. From the standpoint of the ‘new associations’ concept this parasitoid has been evaluated against fruit flies in the Anastrepha complex. We investigated the specificity of F. arisanus responses to fruits infested with two species of Anastrepha. We examined whether fruit volatiles attractive to this parasitoid are induced as a result of fruit fly oviposition. We also investigated whether F. arisanus females are able to discriminate between the oviposition-induced volatiles from host eggs parasitised by conspecifics and volatiles from unparasitised eggs. All experiments were performed in a wind tunnel. Results showed that mango fruits infested with A. ludens eggs (2–3 days after egg deposition) were significantly more attractive to naïve F. arisanus females compared with non-infested fruits or fruits infested with larvae. In addition, guava fruits harbouring A. striata eggs were significantly more attractive to the parasitoid than non-infested fruits or fruits infested with larvae. Thus, the parasitoid was attracted to fruits with eggs, but fruit and fly species did not influence the parasitoid attraction. We also found that F. arisanus females were more attracted to fruits exposed to fertile A. ludens females (i.e. fruits with eggs inside) compared with fruits exposed to sterile females (i.e. fruits with no eggs inside) or fruits with mechanical damage. Parasitoid females were not attracted to A. ludens eggs. The results suggest that the presence of eggs induces volatiles that attract parasitoids. Finally, we found that F. arisanus was able to discriminate between fruits with unparasitised eggs vs. eggs parasitised by conspecifics, indicating that host discrimination could be mediated by olfactory cues.

Keywords

host searching behaviournew associationsBraconidaeTephritidaeAnastrephaMexico
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 103 , Issue 3 , June 2013 , pp. 318 - 325
Copyright
Copyright © Cambridge University Press 2012

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References

Altuzar, A., Montoya, P. & Rojas, J.C. (2004) Response of Fopius arisanus (Hymenoptera: Braconidae) to fruit volatiles in a wind tunnel. Florida Entomologist 87, 616–618.Google Scholar
Aluja, M., Guillén, J., de la Rosa, G., Cabrera, M., Celedonio, H., Liedo, P. & Hendrichs, J. (1987) Natural host plant survey of the economically importance fruit flies (Diptera: Tephritidae) of Chiapas, Mexico. Florida Entomologist 70, 329–338.Google Scholar
Bautista, R.C., Mochizuki, N., Spencer, J.P., Harris, E.J. & Ichimura, D.M. (1999) Mass-rearing of the tephritid fruit fly parasitoid Fopius arisanus (Hymenoptera: Braconidae). Biological Control 15, 137–144.Google Scholar
Baranowski, R., Glenn., H. & Sivinski, J. (1993) Biological control of the Caribbean fruit fly (Diptera: Tephritidae). Florida Entomologist 76, 245–251.Google Scholar
Colazza, S., Fucarino, A., Peri, E., Salerno, G., Conti, E. & Bin, F. (2004) Insect oviposition induces volatile emission in herbaceous plants that attracts egg parasitoids. Journal of Experimental Biology 207, 47–53.Google Scholar
Dicke, M. (1999) Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods. Entomologia Experimentalis et Applicata 91, 131–142.Google Scholar
Dicke, M. & van Loon, J.J.A. (2000) Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomologia Experimentalis et Applicata 97, 237–249.Google Scholar
Domínguez, J., Artiaga-López, T., Solís, E. & Hernández, E. (2010) Métodos de colonización y cría masiva. pp. 259–276 in Montoya, P., Toledo, J. & Hernández, E. (Eds) Moscas de la Fruta: Fundamentos y Procedimientos para su Manejo. Mexico, S y G Editores.Google Scholar
Doutt, R. L. & DeBach, P. (1964) Some biological control concepts and questions. pp. 118–142 in DeBach, P. (Ed.) Biological Control of Insect Pests and Weeds. London, Chapman & Hall.Google Scholar
Fatouros, N.E., van Loon, J.J.A., Hordijk, K.A., Smid, H.M. & Dicke, M. (2005) Herbivore-induced plant volatiles mediate in flight host discrimination by parasitoids. Journal of Chemical Ecology 31, 2033–2047.Google Scholar
Fatouros, N.E., Dicke, M., Mumm, R., Meiners, T. & Hilker, M. (2008) Foraging behavior of egg parasitoids exploiting chemical information. Behavioral Ecology 19, 677–689.Google Scholar
Godfray, H.C.J. (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princeton, New Jersey, Princeton University Press.CrossRefGoogle Scholar
Harris, E.J., Bautista, R.C. & Spencer, J.P. (2000) Utilization of the egg–larval parasitoid, Fopius (Biosteres) arisanus, for augmentative control of tephritid fruit flies. pp. 725–732 in Tan, K.H. (Ed.) Area-Wide Control of Fruit Flies and Other Insect Pests. Penang, Malaysia, Penerbit Universiti Sains Malaysia.Google Scholar
Hernández-Ortiz, V. (1992) El Género Anastrepha Schiner en México (Diptera: Tephritidae): Taxonomía, Distribución y sus Plantas Huéspedes. Xalapa, México, Instituto de Ecología y Sociedad Mexicana de Entomología.Google Scholar
Hilker, M. & Meiners, T. (2006) Early herbivore alert: insect eggs induce plant defense. Journal of Chemical Ecology 32, 1379–1397.Google Scholar
Hilker, M. & Meiners, T. (2011) Plants and insect eggs: How do they affect each other? Phytochemistry 72, 1612–1623.Google Scholar
Hilker, M., Kobs, C., Varama, M. & Schrank, K. (2002) Insect egg deposition induces Pinus sylvestris to attract egg parasitoids. Journal of Experimental Biology 205, 455–461.Google Scholar
Hoffmeister, T.S. & Roitberg, B.D. (1997) To mark the host or the patch: decisions of a parasitoid searching for concealed host larvae. Evolutionary Ecology 11, 145–168.CrossRefGoogle Scholar
Hokkanen, H.M.T. & Pimentel, D. (1984) New approach for selecting biological control agents. Canadian Entomologist 116, 1109–1121.Google Scholar
Kessler, A & Baldwin, I.T. (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291, 2141–2144.Google Scholar
Liquido, N.J. (1991) Effect of ripeness and location of papaya fruits on the parasitization rates of Oriental fruit fly and melon fly (Diptera: Tephritidae) by braconid (Hymenoptera) parasitoids. Environmental Entomology 20, 1732–1736.Google Scholar
López-Muñoz, L. (2004) Efecto de la irradiación en el desarrollo gonadal de Anastrepha ludens (Loew) y Anastrepha obliqua (Macquart). Campaña contra Moscas de la Fruta. Metapa de Domínguez, México, Programa MOSCAMED-MOSCAFRUT/Subdirección de Desarrollo de Métodos.Google Scholar
Meiners, T. & Hilker, M. (1997) Host location in Oomyzus gallerucae (Hymenoptera: Eulophidae), an egg parasitoid of the elm leaf beetle Xanthogaluruca luteola (Coleoptera: Chrysomelidae). Oecologia 112, 87–93.Google Scholar
Montoya, P., Suárez, A., López, F. & Cancino, J. (2009) Fopius arisanus oviposition in four Anastrepha fruit fly species of economic importance in Mexico. BioControl 54, 437–444.CrossRefGoogle Scholar
Nufio, C.R. & Papaj, D.R. (2001) Host marking behavior in phytophagous insects and parasitoids. Entomologia Experimentalis et Applicata 99, 273–293.Google Scholar
Obonyo, M., Schulthess, F., Gerald, J., Wanyama, O., Le Ru, B. & Calatayud, P.A. (2008) Location, acceptance and suitability of lepidopteran stemborers feeding on a cultivated and wild host-plant to the endoparasitoid Cotesia flavipes Cameron (Hymenoptera: Braconidae). Biological Control 45, 36–47.Google Scholar
Ovruski, S., Aluja, M., Sivinski, J. & Wharton, R. (2000) Hymenopteran parasitoids on fruit-infesting Tephritidae (Diptera) in Latin America and the southern United States: Diversity, distribution, taxonomic status and their use in fruit fly biological control. Integrated Pest Management Reviews 5, 81–107.Google Scholar
Pashalidou, F.G., Huigens, M.E., Dicke, M. & Fatouros, N.E. (2010) The use of oviposition-induced plant cues by Trichogramma egg parasitoids. Ecological Entomology 35, 748–753.Google Scholar
Pérez, J., Rojas, J.C., Montoya, P., Liedo, P., González, F.J. & Castillo, A. (2012) Size, shape and hue modulate attraction and landing responses of the braconid parasitoid Fopius arisanus to fruit odour-baited visual targets. BioControl 57, 405–414.Google Scholar
Quimio, G.M. & Walter, G.H. (2001) Host preference and host suitability in an egg-pupal fruit fly parasitoid, Fopius arisanus (Sonan) (Hym., Braconidae). Journal of Applied Entomology 125, 135–140.Google Scholar
Rousse, P., Harris, E.J. & Quilici, S. (2005) Fopius arisanus, an egg-pupal parasitoid of Tephritidae. Overview. Biocontrol News and Information 26, 59–69.Google Scholar
Rousse, P., Gourdon, F. & Quilici, S. (2006) Host specificity of the egg pupal parasitoid Fopius arisanus (Hymenoptera: Braconidae) in La Reunion. Biological Control 37, 284–290.CrossRefGoogle Scholar
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, 313–321.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.CrossRefGoogle ScholarPubMed
van Baaren, J. & Nénon, J.P. (1996) Host location and discrimination mediated through olfactory stimuli in two species of Encyrtidae. Entomologia Experimentalis et Applicata 81, 61–69.Google Scholar
van Lenteren, J.C. (1981) Host discrimination by parasitoids. pp. 153–179 in Nordlund, D.A. Jones, R.L. & Lewis, W.J. (Eds) Semiochemicals their Role in Pest Control. New York, Chapman & Hall.Google Scholar
Vargas, R.I., Stark, J.D., Prokopy, R.J. & Green, T.I. (1991) Response of oriental fruit fly (Diptera: Tephritidae) and associated parasitoids (Hymenoptera: Braconidae) to different-color sticky balls. Journal of Economic Entomology 84, 1503–1507.Google Scholar
Vargas, R.I., Stark, J.D., Uchida, G.K. & Purcell, M. (1993) Opiine parasitoids (Hymenoptera: Braconidae) of Oriental fruit fly (Diptera: Tephritidae) on Kauai Island, Hawaii: Island wide relative abundance and parasitism rates in wild and orchard guava habitats. Environmental Entomology 22, 246–253.Google Scholar
Vargas, R.I., Peck, S.L., McQuate, G.T., Jackson, C.G., Stark, J.D. & Amstrong, J.W. (2001) Potential for area-wide integrated management of Mediterranean fruit fly (Diptera: Tephritidae) with a braconid parasitoid and a novel bait spray. Journal of Economic Entomology 94, 817–825.CrossRefGoogle Scholar
Vargas, R.I., Leblanc, L., Putoa, R. & Eitam, A. (2007) Impact of introduction of Bactrocera dorsalis (Diptera: Tephritidae) and classical biological control releases of Fopius arisanus (Hymenoptera: Braconidae) on economically important fruit flies in French Polynesia. Journal of Economic Entomology 100, 670–679.Google Scholar
Vargas, R.I., Leblanc, L., Putoa, R. & Pinero, J.C. (2012). Population dynamics of three Bactrocera spp. fruit flies (Diptera: Tephritidae) and two introduced natural enemies, Fopius arisanus (Sonan) and Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae), after an invasion by Bactrocera dorsalis (Hendel) in Tahiti. Biological Control 60, 199–206.Google Scholar
Vet, L.E.M. & Dicke, M. (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Entomology 37, 141–172.CrossRefGoogle Scholar
Vinson, S.B. (1976) Host selection by insect parasitoids. Annual Review of Entomology 21, 109–133.CrossRefGoogle Scholar
Wang, X.G. & Messing, R.H. (2003a) Foraging behavior and patch time allocation by Fopius arisanus (Hymenoptera: Braconidae) an egg-larval parasitoid of Tephritid fruit flies. Journal of Insect Behavior 16, 593–612.Google Scholar
Wang, X.G. & Messing, R.H. (2003b) Intra and interspecfic competition by Fopius arisanus (Hymenoptera: Braconidae) and Diachasmimorpha tryoni (Hymenoptera: Braconidae), parasitoids of the Mediterranean fruit fly Ceratitis capitata (Diptera: Tephritidae). Biological Control 27, 251–259.Google Scholar
Wang, X.G. & Messing, R.H. (2008) Role of egg-laying experience in avoidance of superparasitism by fruit fly parasitoid Fopius arisanus (Hymenoptera: Braconidae). Annals of Entomological Society of America 101, 656–663.Google Scholar
Wharton, R., Gilstrap, F., Rhode, R., Fischel, M.M. & Hart, W. (1981) Hymenopterous egg-pupal and larval-pupal parasitoids of Ceratitis capitata and Anastrepha spp. (Dip.: Tephritidae) in Costa Rica. Entomophaga 26, 285–290.CrossRefGoogle Scholar
Wong, T.T.Y., Mochizuki, N. & Nishimoto, J.I. (1984) Seasonal abundance of parasitoids of the Mediterranean and Oriental fruit flies (Diptera: Tephritidae) in the Kula area of Maui, Hawaii. Environmental Entomology 13, 140–145.Google Scholar
Zenil, M., Liedo, P., Williams, T., Valle, J., Cancino, J. & Montoya, P. (2004) Reproductive biology of Fopius arisanus (Hymenoptera: Braconidae) on Ceratitis capitata and Anastrepha spp. (Diptera: Tephritidae). Biological Control 29, 169–178.Google Scholar