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Antennal Sensilla and Sexual Dimorphism of the Parasitoid Trichospilus pupivorus (Hymenoptera: Eulophidae)

Published online by Cambridge University Press:  14 July 2016

Isabel Moreira da Silva ,
Kleber de Sousa Pereira ,
Thomas Spranghers ,
José Cola Zanuncio  and
José Eduardo Serrão
Isabel Moreira da Silva*
Affiliation:
Departamento de Fitotecnia, Universidade Federal de Viçosa, Viçosa, Minas Gerais 36570-900, Brasil
Kleber de Sousa Pereira*
Affiliation:
Departamento de Entomologia/BIOAGRO, Universidade Federal de Viçosa, Viçosa, Minas Gerais 36570-900, Brasil
Thomas Spranghers
Affiliation:
Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, B-9000 Gent, Belgium
José Cola Zanuncio
Affiliation:
Departamento de Entomologia/BIOAGRO, Universidade Federal de Viçosa, Viçosa, Minas Gerais 36570-900, Brasil
José Eduardo Serrão
Affiliation:
Departamento de Biologia Geral, Universidade Federal de Viçosa, Viçosa, Minas Gerais 36570-900, Brasil
*
*Corresponding author. [email protected]; [email protected]
*Corresponding author. [email protected]; [email protected]
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Abstract

Sensory structures (sensilla) of insects are present in high number in the antennae are important for perceiving environmental cues. Thus, sensilla play an important role in the localization, discrimination, and acceptance of a possible host by parasitoid insects. The sensilla, classified according to their shape, size, and distribution, may also show sexual dimorphism in insects. The types and distribution of antennal sensilla in female and male parasitoid Trichospilus pupivorus (Ferriere, 1930) (Hymenoptera: Eulophidae) were evaluated. T. pupivorus females had longer antennae than males. Both males and females have ten sensilla types with higher abundance of placoid sensilla in females, which suggest a possible functional dimorphism.

Keywords

antennal sensillaparasitoidsscanning electron microscopyTrichospilus pupivorus
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 22 , Issue 4 , August 2016 , pp. 913 - 921
Copyright
© Microscopy Society of America 2016 

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Footnotes

a

Isabel Moreira da Silva and Kleber de Sousa Pereira equally contributed to this work.

References

Ahmed, T., Zhang, T.T., Wang, Z.Y., He, K.L. & Bai, S.X. (2013). Morphology and ultrastructure of antennal sensilla of Macrocentrus cingulum Brischke (Hymenoptera: Braconidae) and their probable functions. Micron 50, 35–43.Google Scholar
Altner, H. & Prillinger, L. (1980). Ultrastructure of invertebrate chemo-, thermo-, and hygroreceptors and its functional significance. Int Rev Cytol 61, 69–139.Google Scholar
Amornsak, W., Cribb, B. & Gordh, G. (1998). External morphology of antennal sensilla of Trichogranna australicum Girault (Hymenoptera: Trichogrammatidae). Int J Insect Morphol Embryol 27, 67–82.Google Scholar
Barbarossa, I.T., Muroni, P., Dardani, M., Casula, P. & Angioy, A.M. (1998). New insight into the antennal chemosensory function of Opius concolor (Hymenoptera: Braconidae). Ital J Zool 65, 367–370.CrossRefGoogle Scholar
Barlin, M.R. & Vinson, S.B. (1981). Multiporous plate sensilla in antennae of Chalcidoidea (Hymenoptera). Insect Morphol Embryol 10, 29–42.Google Scholar
Battaglia, D., Isidoro, N., Romani, R., Bin, F. & Pennacchio, F. (2002). Mating behaviour of Aphidius ervi (Hymenoptera: Braconidae): The role of antennae. Eur J Entomol 99, 451–456.Google Scholar
Bleeker, M.A.K., Smid, H.M., Van Aelst, A.C., Van Loon, J.J. & Vet, L.E. (2004). Antennal sensilla of two parasitoid wasps: A comparative scanning electron microscopy study. Microsc Res Tech 63, 266–273.Google Scholar
Borden, J.H., Chong, L. & Rose, A. (1978). Morphology of the elongate placoid sensillum on the antennae of Itoplectis conquisitor . Ann Entomol Soc Am 71, 223–227.Google Scholar
Borden, J.H., Miller, G.E. & Richerson, J.V. (1973). A nossible new sensillum on the antennae of Itoplectis conqzkitor (Hymenoptera: Ichneumonidae). Can Entomol 105, 1363–1367.CrossRefGoogle Scholar
Bouček, Z. (1976). The African and Asiatic species of Trichospilus and Cotterellia (Hymenoptera: Eulophidae). Bull Entomol Res 65, 669–681.Google Scholar
Bruyne, M. & Baker, T.C. (2008). Odor detection in insects: Volatile codes. J Chem Ecol 34, 882–897.Google Scholar
Chapman, R.F. (2013). The Insects: Structure and Function, 5th ed. Cambridge: Cambridge University Press, 929 pp.Google Scholar
Chen, L. & Fadamiro, H.Y. (2008). Antennal sensilla of the decapitating phorid fly, Pseudacteon tricuspis (Diptera: Phoridae). Micron 39, 517–525.Google Scholar
Cônsoli, F.L., Kitajima, E.W. & Parra, J.R.P. (1999). Sensilla on the antenna and ovipositor of the parasitic wasps Trichogramma galloi Zucchi and T. pretiosum Riley (Hymenoptera: Trichogrammatidae). Microsc Res Tech 45, 313–324.Google Scholar
Delvare, G. & Lasalle, J.A. (1993). New genus of Tetrastichinae (Hymenoptera: Eulophidae) from the Neotropical region, with the description of a new species parasitica on key pests of oil palm. J Nat Hist 27, 435–444.CrossRefGoogle Scholar
Dieudonne, A., Daniel, T.L. & Sane, S.P. (2014). Encoding properties of the mechanosensory neurons in the Johnston’s organ of the hawk moth, Manduca sexta . J Exp Biol 217, 3045–3056.Google ScholarPubMed
Dweck, H.K.M. (2009). Antennal sensory receptors of Pteromalus puparum female (Hymenoptera: Pteromalidae), a gregarious pupal endoparasitoid of Pieris rapae . Micron 40, 769–774.CrossRefGoogle ScholarPubMed
Dweck, H.K.M. & Gadallah, N.S. (2008). Description of the antennal sensilla of Habrobracon hebetor . BioControl 53, 841–856.CrossRefGoogle Scholar
Gao, Y., Luo, L.Z. & Hammond, A. (2007). Antennal morphology, structure and sensilla distribution in Microplitis pallidipes (Hymenoptera: Braconidae). Micron 38, 684–693.Google Scholar
Isidoro, N., Bin, F., Colazza, S. & Vinson, S.B. (1996). Morphology of antennal gustatory sensilla and glands in some parasitoid Hymenoptera with hypothesis on their role in sex and host recognition. J Hymenopt Res 5, 206–239.Google Scholar
Keil, T.A. (1997). Comparative morphogenesis of sensilla: A review. Int J Insect Morphol Embryol 26, 151–160.CrossRefGoogle Scholar
Klomp, H. & Teerink, B.J. (1962). Host selection and number of eggs per oviposition in the egg-parasite Trichgramma ernbryophagum Htg. Nature 195, 1020–1021.Google Scholar
Li, J., Guo, Q., Han, S., Jiang, L. & Liang, G. (2013). Types, morphologies and distributions of antennal sensilla of Quadrastichus erythrinae (Hymenptera: Eulophidae). Fla Entomol 96, 1288–1297.CrossRefGoogle Scholar
Marques-Silva, S., Matiello-Guss, C.P., Delabie, J.H., Mariano, C.S., Zanuncio, J.C. & Serrão, J.E. (2006). Sensilla and secretory glands in the antennae of a primitive ant: Dinoponera lucida (Formicidae: Ponerinae). Microsc Res Tech 69, 885–890.Google Scholar
Matsuo, E., Yamada, D., Ishikawa, Y., Asai, T., Ishimoto, H. & Kamikouchi, A. (2014). Identification of novel vibration- and deflection-sensitive neuronal subgroups in Johnston’s organ of the fruit fly. Front Physiol 5, 179.CrossRefGoogle ScholarPubMed
Meyhöfer, R., Casas, J. & Dorn, S. (1997). Mechano- and chemoreceptors and their possible role in host location behavior of Sympiesis sericeicornis (Hymenoptera: Eulophidae). Ann Entomol Soc Am 90, 208–219.Google Scholar
Muralimohan, K. & Srinivasa, Y.B. (2008). Natural parasitization and biological control: Case of the coconut caterpillar. Curr Sci 95, 1478–1482.Google Scholar
Navasaro, R.C. & Elzen, G.W. (1991). Sensilla on the antennae, foretarsi and palpi of Microplitis croceipes (Cresson) (Hymenoptera: Braconidae). Proc Entomol Soc Wash 93, 737–747.Google Scholar
Norton, W.N. & Vinson, S.B. (1974). Antennal sensilla of three parasitic Hymenoptera. Int J Insect Morphol Embryol 3, 305–316.Google Scholar
Ochieng, S.A., Park, K.C., Zhu, J.W. & Baker, T.C. (2000). Functional morphology of antennal chemoreceptors of the parasitoid Microplitis croceipes (Hymenoptera: Braconidae). Arthropod Struct Dev 29, 231–240.Google Scholar
Olson, D.M. & Andow, D.A. (1993). Antennal sensilla of female Trichogramma nubilale (Ertle and Davis) (Hymenoptera: Trichogrammatidae) and comparisons with other parasitic hymenoptera. Int J Insect Morphol Embryol 22, 507–520.Google Scholar
Onagbola, E.O., Boina, D.R., Hermann, S.L. & Stelinski, L.L. (2009). Antennal sensilla of Tamarixia radiata (Hymenoptera: Eulophidae), a parasitoid of Diaphorina citri (Hemiptera: Psyllidae.). Ann Entomol Soc Am 102, 523–531.CrossRefGoogle Scholar
Onagbola, E.O. & Fadamiro, H.Y. (2008). Scanning eléctron microscopy studies of antennal sensilla of Pteromalus cerealellae (Hymenoptera: Pteromalidae). Micron 39, 526–535.Google Scholar
Peña-Carrillo, K.I., González-Hernández, A., López-Arroyo, J.I., Mercado-Hernández, R. & Favela-Lara, S. (2015). Morphological and genetic variation in Mexican wild populations of Tamarixia radiata (Hymenoptera: Eulophidae). Fla Entomol 98, 1093–1100.Google Scholar
Pettersson, E.M., Hallberg, E. & Bigersson, G. (2001). Evidence for the importance of odour-perception in the parasitoid Rhopalicus tutela (Walker) (Hym., Pteromalidae). J Appl Entomol 125, 293–301.Google Scholar
Roux, O., Van Baaren, J., Gers, C., Arvanitakis, L. & Legal, L. (2005). Antennal structure and oviposition behavior of the Plutella xylostella specialist parasitoid: Cotesia plutellae . Microsc Res Tech 68, 36–44.Google Scholar
Schneider, D. (1964). Insect antennae. Annu Rev Entomol 9, 103–122.Google Scholar
Sivan-Loukianova, E. & Eberl, D.F. (2005). Synaptic ultrastructure of Drosophila Johnston’s organ axon terminals as revealed by an enhancer trap. J Comp Neurol 491, 46–55.Google Scholar
Stefanini, M., De Martino, C. & Zamboni, L. (1967). Fixation of ejaculated spermatozoa for electron microscopy. Nature 216, 173–174.Google Scholar
Steinbrecht, R.A. (1997). Pore structures in insect olfactory sensilla: A review of data and concepts. Int J Insect Morphol Embryol 26, 229–245.Google Scholar
Tavares, W.S., Hansson, C., Serrão, J.E. & Zanuncio, J.C. (2011). First report of Trichospilus pupivorus (Hymenoptera: Eulophidae) parasitizing pupae of Anticarsia gemmatalis (Lepidoptera: Noctuidae). Entomol Gen 33, 281–282.Google Scholar
Taylor, G.J., Luu, T., Ball, D. & Srinivasan, M.V. (2013). Vision and air flow combine to streamline flying honeybees. Sci Rep 3, 2614.Google Scholar
Ubaidillah, R. (2006). Eulophine parasitoids of the genus Trichospilus in Indonesia, with the description of two new species (Hymenoptera: Eulophidae). Entomol Sci 9, 217–222.CrossRefGoogle Scholar
Van Baaren, J., Boivin, G., Bourdais, D. & Roux, O. (2007). Antennal sensilla of hymenopteran parasitic wasps: Variations linked to host exploitation behaviour. In Modern Research and Educational Topics in Microscopy, Méndez-Vilas A. & Díaz J. (Eds.), pp. 345–352. Badajoz, Spain: Formatex.Google Scholar
Viggiani, G. (1982). New species and host records of African Aphelinids. J Entomol Soc South Afr 45, 27–32.Google Scholar
Voegelé, J., Cals-Usciati, J., Pihan, J.P. & Daumal, J. (1975). Structure de l’antenne des Trichogrammes. Entomophaga 20, 161–169.Google Scholar
Wenninger, E.J., Hall, D.G. & Mankin, R.W. (2009). Vibrational communication between the sexes in Diaphorina citri (Hemiptera: Psyllidae). Ann Entomol Soc Am 102, 547–555.CrossRefGoogle Scholar
Weseloh, R.M. (1972). Sense organs of hyperparasite Cheiloneurus noxius (Hymenoptera: Encyrtidae) important in host selection processes. Ann Entomol Soc Am 65, 41–46.Google Scholar
Wibel, R.G., Cassidy, J.D., Bushe, H.E. Jr, Cummings, M.R., Bindokas, V.P., Charlesworth, J. & Buumgartner, D.L. (1984). Scanning electron microscopy of antennal sense organs of Nasonia vitripennis (Hymenoptera: Pteromalidae). Trans Am Microsc Soc 103, 329–340.Google Scholar
Zhang, L., Feng, Y.-Q., Ren, L.-L., Luo, Y.-Q., Wang, F. & Zong, S.-X. (2014). Sensilla on antenna, ovipositor and leg of Eriborus applicitus (Hymenoptera: Ichneumonidae), a parasitoid wasp of Holcocerus insularis staudinger (Lepidoptera: Cossidae). Acta Zool 96, 253–263.Google Scholar
Zhou, H., Wu, W.J., Zang, F.P. & Fu, Y.G. (2013 a). Scanning electron microscopy studies of the antennal sensilla of Metaphycus parasaissetiae Zhang & Huang (Hymenoptera: Encyrtidae). Neotrop Entomol 42, 278–287.Google Scholar
Zhou, H., Wu, W.-J., Zhnag, Z.-F. & Zhnag, Y. (2011). Antennal sensilla of Apanteles cypris Nixon (Hymenoptera: Braconidae), a larval endoparasitoid of Cnaphalocrocismedinalis Guenée (Lepidoptera: Pyralidae). Microsc Res Tech 74, 1199–1208.Google Scholar
Zhou, H., Wua, W.W.J., Niub, L.M. & Fu, Y.G. (2013 b). Antennal sensilla of female Encarsia guadeloupae Viggiani (Hymenoptera: Aphelinidae), a nymphal parasitoid of the spiraling whitefly Aleurodicus dispersus (Hemiptera: Aleyrodidae). Micron 44, 365–372.Google Scholar