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The influence of volatile semiochemicals from stink bug eggs and oviposition-damaged plants on the foraging behaviour of the egg parasitoid Telenomus podisi

Published online by Cambridge University Press:  14 June 2016

M.F.F. Michereff
Affiliation:
Embrapa Recursos Genéticos e Biotecnologia (Cenargen), Brasília, Brazil
M. Borges
Affiliation:
Embrapa Recursos Genéticos e Biotecnologia (Cenargen), Brasília, Brazil
M.F.S. Aquino
Affiliation:
Embrapa Recursos Genéticos e Biotecnologia (Cenargen), Brasília, Brazil Universidade de Brasília, Brasília, Brazil
R.A. Laumann
Affiliation:
Embrapa Recursos Genéticos e Biotecnologia (Cenargen), Brasília, Brazil
A.C.M. Mendes Gomes
Affiliation:
Embrapa Recursos Genéticos e Biotecnologia (Cenargen), Brasília, Brazil
M.C. Blassioli-Moraes*
Affiliation:
Embrapa Recursos Genéticos e Biotecnologia (Cenargen), Brasília, Brazil
*
*Author for correspondence Phone: +55 (61) 3448-4932 Fax: +55 (61) 3340-3462 E-mail: [email protected]

Abstract

During host selection, physical and chemical stimuli provide important cues that modify search behaviours of natural enemies. We evaluated the influence of volatiles released by eggs and egg extracts of the stink bug Euschistus heros and by soybean plants treated with the eggs and egg extracts on Telenomus podisi foraging behaviour. Responses to volatiles were evaluated in Y-tube olfactometers after exposure to (1) one egg cluster for 24 h; (2) plants with eggs laid by the stink bug, tested at 24, 48, and 72 h after treatment; (3) plants with eggs laid artificially, tested at 24, 48, and 72 h after treatment; and (4) plants treated with acetone or hexane extracts of eggs. Telenomus podisi was attracted to volatiles emitted by one egg cluster and to acetone extracts of one egg cluster, but not to air or acetone controls. There were no responses to odours of plants treated with eggs or egg extracts. Analysis of acetone extracts of egg clusters by gas chromatography revealed the major components were saturated and unsaturated fatty acids, including hexadecanoic acid, linoleic acid, and (Z)-9-octadecenoic acid. Our results suggest that one egg cluster and the acetone extract of one egg cluster contain volatile compounds that can modify T. podisi foraging behaviour, and that the amounts of these compounds, probably together with some minor compounds, are important for host recognition by T. podisi. Also, the oviposition damage or egg extracts on the plant did not elicit indirect defences that attracted Telenomus podisi.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2016 

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References

Aquino, M.F.S., Dias, A.M., Morges, M., Blassioli-Moraes, M.C. & Laumann, R.A. (2012) Influence of visual cues on host-searching and learning behaviour of the parasitoids Telenomus podisi and Trissolcus basalis . Entomologia Experimentalis et Applicata 145, 162174.CrossRefGoogle Scholar
Arakaki, N., Yamazawa, H. & Wakamura, S. (2011) The egg parasitoid Telenomus euproctidis (Hymenoptera: Scelionidae) uses sex pheromone released by immobile female tussock moth Orgyia postica (Lepidoptera: Lymantriidae) as kairomone. Applied Entomology and Zoology 46, 195200.CrossRefGoogle Scholar
Bin, F., Vinson, S.B., Strand, M.R., Colazza, S. & Jones, W.A. (1993) Source of an egg kairomone for Trissolcus basalis, a parasitoid of Nezara viridula . Physiological Entomology 18, 715.Google Scholar
Borges, M. & Aldrich, J.R. (1994) Estudos de semioquímicos para o manejo de Telenominae. Anais da Sociedade Entomológica do Brasil 23, 575577.CrossRefGoogle Scholar
Borges, M., Schmidt, F.G.V., Sujii, E.R., Medeiros, M.A., Mori, K., Zarbin, P.H.G. & Ferreira, J.T.B. (1998) Field responses of stink bugs to the natural and synthetic pheromone of the Neotropical brown stink bug, Euschistus heros (Heteroptera: Pentatomidae). Physiological Entomology 23, 202207.Google Scholar
Borges, M., Costa, M.L.M., Sujii, E.R., Cavalcanti, M.G., Redígolo, G.F., Resck, I.S. & Vilela, E.F. (1999) Semiochemical and physical stimuli involved in host recognition by Telenomus podisi (Hymenoptera: Scelionidae) toward Euschistus heros (Heteroptera: Pentatomidae). Physiological Entomology 24, 227233.CrossRefGoogle Scholar
Borges, M., Colazza, S., Ramirez-Lucas, P., Chauhan, K.R., Moraes, M.C.B. & Aldrich, J.R. (2003) Kairomonal effect of walking traces from Euschistus heros (Heteroptera: Pentatomidae) on two strains of Telenomus podisi (Hymenoptera: Scelionidae). Physiological Entomology 28, 349355.Google Scholar
Bruce, T.J.A., Midega, C.A.O., Birkett, M.A., Pickett, J.A. & Khan, Z.R. (2010) Is quality more important than quantity? Insect behavioural responses to changes in a volatile blend after stemborer oviposition on an African grass. Biology Letters 6, 314317.Google Scholar
Bruessow, F., Gouhier-Darimont, C., Buchala, A., Metraux, J.P. & Reymond, P. (2010) Insect egg suppress plant defence against chewing herbivores. Plant Journal 62, 876885.Google Scholar
Büchel, K., Malskies, S., Mayer, M., Fenning, T.M., Gershenzon, J., Hilker, M. & Meiners, T. (2011) How plants give early herbivore alert: volatile terpenoids attract parasitoids to egg-infested elms. Basic Applied Ecology 12, 403412.CrossRefGoogle Scholar
Colazza, S., Mcelfresh, J.S., & Millar, J.G. (2004 a) Identification of volatile synomones, induced by Nezara viridula feeding and oviposition on bean spp., that attract the egg parasitoid Trissolcus basalis . Journal of Chemical Ecology 30, 945964.Google Scholar
Colazza, S., Fucarino, A., Peri, E., Salerno, G., Conti, E. & Bin, F. (2004 b) Insect oviposition induces volatile emission in herbaceous plants that attracts egg parasitoids. Journal of Experimental Biology 207, 4753.Google Scholar
Cusumano, A., Weldegergis, B.T., Colazza, S., Dicke, M. & Fatouros, N. (2015) Attraction of egg-killing parasitoids toward induced plant volatiles in a multi-herbivore context. Oecologia 179, 163174.CrossRefGoogle Scholar
Fatouros, N.E., Dicke, M., Mumm, R., Meiners, T. & Hilker, M. (2008) Foraging behavior of egg parasitoids exploiting chemical informations. Behavioral Ecology 19, 677689.Google Scholar
Fatouros, N.E., Lucas-Barbosa, D., Weldegergis, B.T., Pashalidou, F.G., Van Loon, J.J.A., Dicke, M., Harvey, J.A., Gols, R. & Huigens, M.E. (2012) Plant volatiles induced by herbivore egg deposition affect insects of different trophic levels. PLoS ONE 7, 114.Google Scholar
Hilker, M. & Meiners, T. (2006) Early herbivore alert: insect eggs induce plant defense. Journal of Chemical Ecology 32, 13791397.CrossRefGoogle ScholarPubMed
Hilker, M. & Meiners, T. (2010) How do plants “notice” attack by herbivorous arthropods? Biological Review 85, 267280.Google Scholar
Hilker, M. & Meiners, T. (2011) Plants and insect eggs: how do they affect each other? Phytochemistry 72, 16121623.Google Scholar
Hilker, M., Stein, C., Schröder, R., Varama, M. & Mumm, R. (2005) Insect egg deposition induces defence responses in Pinus sylvestris: characterisation of the elicitor. Journal of Experimental Biology 208, 18491854.Google Scholar
Hu, J.S., Gelman, D.B. & Bell, R.A. (1999) Effects of selected physical and chemical treatments of Colorado potato beetle eggs on host acceptance and development of the parasitic wasp, Edovum puttleri . Entomologia Experimentalis et Applicata 90, 237245.Google Scholar
Jorge, L.A.C., Laumann, R.A., Borges, M., Moraes, M.C.B., Cruz, R.A., Milare, B.N. & Palhares, L. (2005) Software para avaliação do comportamento de insetos. Circular Técnica n. 30, 7p. São Carlos, SP: Embrapa Instrumentação Agropecuária.Google Scholar
Kaloshian, I. & Walling, L.L. (2005) Hemipterans as plant pathogens. Annual Review of Phytopathology 43, 491521.Google Scholar
Laumann, R.A., Moraes, M.C.B., Cokl, A. & Borges, M. (2007) Eavesdropping on the sexual vibratory communication of stink bugs (Hemiptera: Pentatomidae) by the egg parasitoid Telenomus podisi . Animal Behaviour 73, 637649.Google Scholar
Laumann, R.A., Aquino, M.F.S., Moraes, M.C.B., Pareja, M. & Borges, M. (2009) Response of the egg parasitoids Trissolcus basalis and Telenomus podisi to compounds from defensive secretions of stink bugs. Journal of Chemical Ecology 35, 819.Google Scholar
Laumann, R.A., Cokl, A., Lopes, A.P.S., Ferreira, J.B.C., Moraes, M.C.B. & Borges, M. (2011) Silent singers are not safe: selective response of a parasitoid to substrate-borne vibratory signals of stink bugs. Animal Behaviour 82, 11751183.Google Scholar
Leonard, D.E., Wu, Z-Xe., Ferro, D.N. (1987) Responses of parasite Edovum puttleri to kairomone from eggs of Colorado potato beetle, Leptinotarsa decemlineata . Journal of Chemical Ecology 13, 335344.CrossRefGoogle Scholar
Liu, M., Yu, H. & Li, G. (2008) Oviposition deterrents from eggs of the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae): chemical identification and analysis by electroantennogram. Journal of Insect Physiology 54, 656662.Google Scholar
Medeiros, M.A., Schimidt, F.V.G., Loiácono, M.S., Carvalho, V.F. & Borges, M. (1997) Parasitismo e predação de ovos de Euschistus heros (Fab.) (Heteroptera: Pentatomidae) no Distrito Federal, Brasil. Anais da Sociedade Entomológica do Brasil 26, 397401.CrossRefGoogle Scholar
Medeiros, M.A., Loiácono, M.S., Borges, M. & Schimidt, F.V.G. (1998) Incidência natural de parasitóides em ovos de percevejos (Hemiptera: Pentatomidae) encontrados na soja no Distrito Federal. Pesquisa Agropecuária Brasileira 33, 14311435.Google Scholar
Melo Machado, R.C., Sant'Ana, J., Blassioli-Moraes, M.C., Laumann, R.A. & Borges, M. (2014) Herbivory-induced plant volatiles from Oryza sativa and their influence on chemotaxis behaviour of Tibraca limbativentris stal. (Hemiptera: Pentatomidae) and egg parasitoids. Bulletin of Entomological Research 104, 347356.Google Scholar
Michereff, M.F.F., Laumann, R.A., Borges, M., Michereff Filho, M., Diniz, I.R., Farias Neto, A.L. & Moraes, M.C.B. (2011) Volatiles mediating plant-herbivory-natural enemy interaction in resistant and susceptible soybean cultivars. Journal of Chemical Ecology 37, 273285.Google Scholar
Michereff, M.F.F., Borges, M., Laumann, R.A., Diniz, I.R. & Moraes, M.C.B. (2013) Influence of volatile compounds from herbivore-damaged soybean plants on searching behavior of the egg parasitoid Telenomus podisi . Entomologia Experimentalis et Applicata 147, 917.Google Scholar
Michereff, M.F.F., Michereff Filho, M., Blassioli-Moraes, M.C., Laumann, R.A., Diniz, I.R. & Borges, M. (2015) Effect of resistant and susceptible soybean cultivars on the attraction of egg parasitoids in field conditions. Journal of Applied Entomology 139, 207216.CrossRefGoogle Scholar
Moraes, M.C.B., Laumann, R.A., Pires, C.S.S., Sujii, E.R. & Borges, M. (2005) Induced volatiles in soybean and pigeon pea plants artificially infested with the Neotropical brown stink bug, Euschistus heros, and their effect on the egg parasitoid, Telenomus podisi . Entomologia Experimentalis et Applicata 115, 227237.CrossRefGoogle Scholar
Moraes, M.C.B., Pareja, M., Laumann, R.A., Hoffmann-Campo, C.B. & Borges, M. (2008) Response of the parasitoid Telenomus podisi to induced volatiles from soybean damaged by stink bug herbivory and oviposition. Journal of Plant Interaction 3, 17421756.Google Scholar
Moujahed, R., Frati, F., Cusumano, A., Salerno, G., Conti, E., Peri, E. & Colazza, S. (2014) Egg parasitoid attraction toward induced plant volatile is disrupted by a non-host herbivore attacking above or belowground plant organs. Frontiers in Plant Science 5, 110.Google Scholar
Pacheco, D.J.P. & Corrêa-Ferreira, B.S. (2000) Parasitismo de Telenomus podisi Ashmead (Hymenoptera: Scelionidae) em populações de percevejos pragas da soja. Anais da Sociedade Entomológica do Brasil 29, 295302.Google Scholar
Rasmann, S. & Turlings, T.C.J. (2007) Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies. Ecology Letters 10, 926936.Google Scholar
R Development Core Team (2009) R: A Language and Environment for Statistical Computing. Vienna, Austria, R Foundation for Statistical Computing. ISBN 3-900051-07-0. Available online at http://www.R-project.org Google Scholar
Renou, M., Nagnan, P., Berthier, A. & Durier, C. (1992) Identification of compounds from the eggs of Ostrinia nubilalis and Mamestra brassicae having kairomone activity on Trichogramma brassicae . Entomologia Experimentalis et Applicata 63, 291303.Google Scholar
Sales, F.M. (1979) Responsiveness and threshold for host-seeking stimulation of the female, Trissolcus basalis (Wollaston) by the eggs of the host, Nezara viridula (L.). Fitossanidade 3, 3639.Google Scholar
Takasu, K. & Nordlund, D.A. (2001) Host recognition kairomones for Anaphes iole Girault, an egg parasitoid of the Western tarnished plant bug. Biological Control 22, 6065.Google Scholar
Tamiru, A., Bruce, T.J.A., Woodcock, C.M., Caufiled, J.C., Midega, C.A.O., Ogol, C.K.P., Mayon, P., Birkett, M.A., Pickett, J.A. & Khan, Z.R. (2011) Maize landraces recruit egg and larval parasitoids in response to egg deposition by a herbivore. Ecology Letters 14, 10751083.Google Scholar
Tamiru, A., Bruce, T.J.A., Midega, C.A., Woodcock, C.M., Birkett, M.A., Pickett, J.A. & Khan, Z.R. (2012) Oviposition induced volatile emission from Africa smallholder farmers’ maize varieties. Journal of Chemical Ecology 38, 231234.CrossRefGoogle Scholar
Tognon, R., Sant'Ana, J. & Jahnke, S.M. (2014) Influence of original host on chemotaxic behaviour and parasitism in Telenomus podisi Ashmead (Hymenoptera: Platygastridae). Bulletin of Entomological Research 104, 781787.Google Scholar
Tooker, J.F. & De Moraes, C.M. (2007) Jasmonate, salicylate and benzoate in insect eggs. Journal of Chemical Ecology 33, 331343.Google Scholar
Vinson, S.B. (1998) The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilizes by larvaphagous and oophagus species. Biological Control 11, 7996.Google Scholar
Walling, L.L. (2000) The myriad plant responses to herbivores. Journal of Plant Growth Regulation 19, 195216.Google Scholar
Wegener, R., Schulz, S., Meiners, T., Hadwich, K. & Hilker, M. (2001) Analysis of volatiles induced by oviposition of elm leaf beetle Xanthogaleruca luteola on Ulmus minor . Journal of Chemical Ecology 27, 499515.Google Scholar
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