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Ultrastructure of antennal sensilla of female Ceratosolen solmsi marchali (Hymenoptera: Chalcidoidea: Agaonidae: Agaoninae)

Published online by Cambridge University Press:  02 April 2012

Zongbo Li ,
Pei Yang ,
Yanqiong Peng  and
Darong Yang
Zongbo Li
Affiliation:
Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Kunming 650223, People's Republic of China, and Graduate University of the Chinese Academy of Sciences, Beijing 100039, People's Republic of China
Pei Yang
Affiliation:
Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Kunming 650223, People's Republic of China, and Graduate University of the Chinese Academy of Sciences, Beijing 100039, People's Republic of China
Yanqiong Peng
Affiliation:
Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Kunming 650223, People's Republic of China
Darong Yang*
Affiliation:
Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Kunming 650223, People's Republic of China
*
1Corresponding author (e-mail: Yangdr@xtbg.ac.cn).
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Abstract

Fig-pollinating wasps are phytophagous wasps that mainly use olfaction to locate their fig (Ficus L., Moraceae) hosts. To provide a morphological framework for studying agaonid olfaction, we examined the antennal sensilla of female Ceratosolen solmsi marchali Mayr by scanning and transmission electron microscopy. We identified and characterized (ultrastructure, distribution, abundance, and position) 13 types of sensilla: multiporous placoid sensilla (types 1 and 2), basiconic sensilla (types 1 and 2), basiconic capitate peg sensilla, sensilla chaetica (types 1–3), sensilla trichodea, sensilla coeloconica (types 1–3), and one specialized sensillum regarded as a sensillum obscurum. We suggest that five types are chemoreceptors because they are porous and innervated by multiple sensory neurons. Sensilla coeloconica type 1 may also function as chemoreceptors, based on external morphology. Other sensilla may be involved in mechanoreception, thermo- and (or) hygro-reception, or pressure detection. We discuss our results in relation to the lifestyle of C. solmsi marchali.

Résumé

Les guêpes pollinisatrices des figuiers sont des guêpes phytophages qui utilisent surtout l'odorat pour trouver leurs figuiers (Ficus L., Moraceae) hôtes. Nous étudions aux microscopes électroniques à balayage et à transmission les sensilles des antennes des femelles de Ceratosolen solmsi marchali Mayr afin de mettre au point un cadre morphologique pour l'étude de l'olfaction chez les agaonidés. Nous identifions et caractérisons (ultrastructure, répartition, abondance et position) treize types de sensilles: des sensilles placoïdes à pores multiples (types 1 et 2), des sensilles basiconiques (types 1 et 2), des sensilles basiconiques en bâtonnet capité, des sensilles chétiformes (types 1–3), des sensilles trichoïdes, des sensilles coeloconiques (types 1–3) et une sensille spécialisée considérée comme une « sensille obscure ». Nous croyons que cinq des types de sensilles sont des chimiorécepteurs parce qu'elles portent des pores et sont innervées par de nombreux neurones sensoriels. Les sensilles coeloconiques de type 1 fonctionnent peut-être aussi comme chimiorécepteurs, d'après leur morphologie externe. Les autres sensilles sont peut-être impliquées dans la mécanoréception, la thermoréception et (ou) l'hygroréception ou la détection de la pression. Nous discutons de nos résultats en relation avec le mode de vie de C. solmsi marchali.

[Traduit par la Rédaction]

Type
Articles
Information
The Canadian Entomologist , Volume 141 , Issue 5 , October 2009 , pp. 463 - 477
Copyright
Copyright © Entomological Society of Canada 2009

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References

Altner, H., Schaller-Selzer, L., Stetter, H., and Wohlrab, I. 1983. Poreless sensilla with inflexible sockets: a comparative study of a fundamental type of insect sensilla probably comprising thermo- and hygroreceptors. Cell and Tissue Research, 234: 279–307. PMID:6196120 doi:10.1007/BF00213769.CrossRefGoogle ScholarPubMed
Ameismeier, F. 1985. Embryonic development and molting of the antennal coeloconic no pore- and double-walled wall pore sensilla in Locusta migratoria (Insecta, Orthopteroidea). Zoomorphology, 105: 356–366. doi:10.1007/BF00312279.CrossRefGoogle Scholar
Amornsak, W., Cribb, B., and Gordh, G. 1998. External morphology of antennal sensilla of Trichogramma australicum Girault (Hymenoptera: Trichogrammatidae). International Journal of Insect Morphology and Embryology, 27: 67–82. doi:10.1016/S0020-7322(98)00003-8.CrossRefGoogle Scholar
Barlin, M.R., and Vinson, B.S. 1981. Multiporous plate sensilla in antennae of the Chalcidoidea (Hymenoptera). International Journal of Insect Morphology and Embryology, 10: 29–42. doi:10.1016/0020-7322(81)90011-8.CrossRefGoogle Scholar
Barlin, M.R., Vinson, S.B., and Piper, G.L. 1981. Ultrastructure of the antennal sensilla of the cockroach-egg parasitoid Tetrastichus hagenowii (Hymenoptera: Eulophidae). Journal of Morphology, 168: 97–108. doi:10.1002/jmor.1051680110.CrossRefGoogle ScholarPubMed
Basibuyuk, H.H., and Quicke, D.L.J. 1999. Gross morphology of multiporous plate sensilla in the Hymenoptera (Insecta). Zoologica Scripta, 28(1–2): 51–67. doi:10.1046/j.1463-6409.1999.00007.x.CrossRefGoogle Scholar
Bleeker, M.A.K., Smid, H.M., Van Aelst, A.C., Van Loon, J.J.A., and Vet, L.E.M. 2004. Antennal sensilla of two parasitoid wasps: a comparative scanning electron microscopy study. Microscopy Research and Technique, 63: 266–273. PMID: 15170756 doi:10.1002/jemt.20038.CrossRefGoogle ScholarPubMed
Calvello, M., Brandazza, A., Navarrini, A., Dani, F.R., Turillazzi, S., Felicioli, A., and Pelosi, P. 2005. Expression of odorant-binding proteins and chemosensory proteins in some Hymenoptera. Insect Biochemistry and Molecular Biology, 35: 297–307. PMID:15763466 doi:10.1016/j.ibmb.2005.01.002.CrossRefGoogle ScholarPubMed
Chapman, R.F. 1998. The insects: structure and function. 4th ed. Cambridge University Press, London, United Kingdom.CrossRefGoogle Scholar
Chen, C., and Song, Q. 2008. Responses of the pollinating wasp Ceratosolen solmsi marchali to odor variation between two floral stages of Ficus hispida. Journal of Chemical Ecology, 34: 1536–1544. PMID:19015920 doi:10.1007/s10886-008-9558-4.CrossRefGoogle ScholarPubMed
Chiappini, E., Solinas, C., and Solinas, M. 2001. Antennal sensilla of Anagrus atomus (L.) (Hymenoptera: Mymaridae) female and their possible behavioural significance. Entomologica (Bari), 35: 51–76.Google Scholar
Compton, S.G., Ellwood, M.D.F., Davis, A.J., and Welch, K. 2000. The flight heights of chalcid wasps (Hymenoptera, Chalcidoidea) in a lowland Bornean rain forest: fig wasps are the high fliers. Biotropica, 32: 515–522.CrossRefGoogle Scholar
Dahms, E.C. 1984. An interpretation of the structure and function of the antennal sense organs of Melittobia australica (Hymeneoptera: Eulophidae) with the discovery of a large dermal gland in the male scape. Memoirs of the Queensland Museum, 21: 361–385.Google Scholar
Den Otter, C.J., Schuil, H.A., and Sander-van Oosten, A. 1978. Reception of host-plant odours and female sex pheromone in Adoxophyes orana (Lepidoptera: Tortricidae): electrophysiology and morphology. Entomologia Experimentalis et Applicata, 24: 570–578. doi:10.1007/BF02385110.CrossRefGoogle Scholar
Faucheux, M.J., Kristensen, N.P., and Yen, S.-H. 2006. The antennae of neopseustid moths: morphology and phylogenetic implications with special reference to the sensilla (Insecta, Lepidoptera, Neopseustidae). Zoologischer Anzeiger, 245: 131–142. doi:10.1016/j.jcz.2006.05.004.CrossRefGoogle Scholar
Gao, Y., Luo, L.Z., and Hammond, A. 2007. Antennal morphology, structure and sensilla distribution in Microplitis pallidipes (Hymenoptera: Braconidae). Micron (Oxford, England), 38: 684–693.CrossRefGoogle ScholarPubMed
Grison-Pigé, L., Bessière, J.M., and Hossaert-McKey, M. 2002. Specific attraction of figpollinating wasps: role of volatile compounds released by tropical figs. Journal of Chemical Ecology, 28: 283–295. PMID:11925068 doi:10.1023/A:1017930023741.CrossRefGoogle ScholarPubMed
Harrison, R.D. 2003. Fig wasp dispersal and the stability of a keystone plant resource in Borneo. Proceedings of the Royal Society of London, Series B, Biological Sciences, 270: S76–S79. doi:10.1098/rsbl.2003.0018.Google ScholarPubMed
Harrison, R.D., and Rasplus, J.Y. 2006. Dispersal of fig pollinators in Asian tropical rain forests. Journal of Tropical Ecology, 22: 631–639. doi:10.1017/S0266467406003488.CrossRefGoogle Scholar
Hossaert-McKey, M., Gibernau, M., and Frey, J. 1994. Chemosensory attraction of fig wasps to substances produced by receptive figs. Entomologia Experimentalis et Applicata, 70: 185–191. doi:10.1007/BF02380526.CrossRefGoogle Scholar
Hunger, T., and Steinbrecht, R.A. 1998. Functional morphology of a double-walled multiporous olfactory sensillum: the sensillum coeloconicum of Bombyx mori (Insecta, Lepidoptera). Tissue and Cell, 30: 14–29. PMID:18627836 doi:10. 1016/S0040-8166(98)80003-7.CrossRefGoogle ScholarPubMed
Isidoro, N., Bin, F., Colazza, S., and 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. Journal of Hymenoptera Research, 5: 206–239.Google Scholar
Keil, T.A. 1999. Morphology and development of the peripheral olfactory organs. In Insect olfaction. Edited by Hansson, B.S., Springer-Verlag, , New York. pp. 5–47.CrossRefGoogle Scholar
Kjellberg, F., Doumesche, B., and Bronstein, J. 1988. Longevity of a fig wasp (Blastophaga psenes). Proceeding of the Koninklijke Nederlandse Akademie van Wetenschappen, Series C, 91: 117–122.Google Scholar
Kjellberg, F., Jousselin, E., Hossaert-McKey, M., and Rasplus, J.Y. 2005. Biology, ecology, and evolution of fig-pollinating wasps (Chalcidoidea, Agaonidae). In Biology, ecology, and evolution of gall-inducing arthropods. Edited by Raman, A., Schaefer, C.W., and Withers, T.M.. Science Publishers, Inc., Enfield, New Hampshire, and Plymouth, United Kingdom. pp. 539–572.Google Scholar
Navasero, R.C., and Elzen, G.W. 1991. Sensilla on the antennae, foretarsi and palpi of Microplitis croceipes (Cresson) (Hymenoptera: Braconidae). Proceedings of the Entomological Society of Washington, 93: 737–747.Google Scholar
Norton, W.N., and Vinson, S.B. 1974. Antennal sensilla of three parasitic Hymenoptera. International Journal of Insect Morphology and Embryology, 3(3–4): 305–316. doi:10.1016/0020-7322(74)90025-7.CrossRefGoogle Scholar
Ochieng, S.A., Park, K.C., Zhu, J.W., and Baker, T.C. 2000. Functional morphology of antennal chemoreceptors of the parasitoid Microplitis croceipes (Hymenoptera: Braconidae). Arthropod Structure and Development, 29: 231–240. PMID: 18088929 doi:10.1016/S1467-80390(01)0008-1.CrossRefGoogle ScholarPubMed
Olson, D.M., and Andow, D.A. 1993. Antennal sensilla of female Trichogramma nubilale (Ertle and Davis) (Hymenoptera: Trichogrammatidae) and comparisons with other parasitic Hymenoptera. International Journal of Insect Morphology and Embryology, 22: 507–520. doi:10.1016/0020-7322(93)90037-2.CrossRefGoogle Scholar
Onagbola, E.O., and Fadamiro, H.Y. 2008. Scanning electron microscopy studies of antennal sensilla of Pteromalus cerealellae (Hymenoptera: Pteromalidae). Micron (Oxford, England), 39: 526–535.Google ScholarPubMed
Pettersson, E.M., Hallberg, E., and Birgersson, G. 2001. Evidence for the importance of odour-perception in the parasitoid Rhopalicus tutela (Walker) (Hym., Pteromalidae). Journal of Applied Entomology, 125: 293–301. doi:10.01046/j.1439-0418.2001.00550.x.CrossRefGoogle Scholar
Pophof, B. 1997. Olfactory responses recorded from sensilla coeloconica of the silkmoth Bombyx mori. Physiological Entomology, 22: 239–248. doi:10.1111/j.1365-3032.1997.tb01164.x.CrossRefGoogle Scholar
Roux, O., van Baaren, J., Gers, C., Arvanitakis, L., and Legal, L. 2005. Antennal structure and oviposition behavior of the Plutella xylostella specialist parasitoid: Cotesia plutellae. Microscopy Research and Technique, 68: 36–44. PMID:16208718 doi:10.1002/jemt.20220.CrossRefGoogle ScholarPubMed
SAS Institute Inc. 1999. SAS/STAT. Version 8.0. User's guide. SAS Institute Inc., Cary, North Carolina.Google Scholar
Schneider, D. 1964. Insect antennae. Annual Review of Entomology, 9: 103–122. doi:10.01146/annurev.en.09.010164.000535.CrossRefGoogle Scholar
Song, Q.S., Yang, D.R., Zhang, G.G., and Yang, C.R. 2001. Volatiles from Ficus hispida and their attractiveness to fig wasps. Journal of Chemical Ecology, 27: 1929–1942. PMID:11710602 doi:10.01023/A:1012226400586.CrossRefGoogle ScholarPubMed
Steinbrecht, R.A. 1997. Pore structures in insect olfactory sensilla: a review of data and concepts. International Journal of Insect Morphology and Embryology, 26(3–4): 229–245. doi:10.1016/S00020-7322(97)00024-X.Google Scholar
van Baaren, J., Boivin, G., Lannic, J.L., and Nénon, J.-P. 1999. Comparison of antennal sensilla of Anaphes victus and A. listronoti (Hymenoptera: Mymaridae), egg parasitoids of Curculionidae). Zoomorphology, 119: 1–8 doi: 010.01007/s004350050076.CrossRefGoogle Scholar
van Noort, S., Ware, A.B., and Compton, S.G. 1989. Pollinator-specific volatile attractants released from the figs of Ficus burtt-davyi. South African Journal of Science, 85: 323–324.Google Scholar
Ware, A.B., and Compton, S.G. 1992. Repeated evolution of elongate multiporous plate sensilla in female fig wasps (Hymenoptera: Agaonidae: Agaoninae). Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, Series C, 95: 275–292.Google Scholar
Ware, A.B., and Compton, S.G. 1994. Responses of fig wasps to host plant volatile cues. Journal of Chemical Ecology, 20: 785–802. doi:10.1007/BF02059613.CrossRefGoogle ScholarPubMed
Ware, A.B., Kaye, P.T., Compton, S.G., and Noort, S. 1993. Fig volatiles: their role in attracting pollinators and maintaining pollinator specificity. Plant Systematics and Evolution, 186(3–4): 147–156. doi:10.1007/BF00940794.CrossRefGoogle Scholar
Weiblen, G.D. 2002. How to be a fig wasp. Annual Review of Entomology, 47: 299–330. PMID: 011729077 doi:10.1146/annurev.ento.47.091201.0145213.CrossRefGoogle ScholarPubMed
Wiebes, J.T. 1979. Co-evolution of figs and their insect pollinators. Annual Review of Ecology and Systematics, 10: 1–12. doi:10.1146/annurev.es.10.110179.000245.CrossRefGoogle Scholar
Wu, Z.Y., Zhou, Z.K., and Gilbert, M.G. 2003. Moraceae. In Flora of China. Volume 5 (Ulmaceae through Basellaceae). Edited by Wu, Z.Y., Raven, P.H., and Hong, D.Y.. Science Press, Beijing, China, and Missouri Botanical Garden Press St. Louis, Missouri. pp. 37–71.Google Scholar
Yang, D.R., Peng, Y.Q., Song, Q.S., Zhang, G.M., Wang, R.W., Zhao, T.Z., and Wang, Q.Y. 2002. Pollination biology of Ficus hispida in the tropical rainforests of Xishuangbanna, China. Journal of Integrative Plant Biology, 44: 519–526.Google Scholar
Yang, H., Yan, S.C., and Liu, D. 2009. Ultra-structural observations on antennal sensilla of Coleophora obducta (Meyrick) (Lepidoptera: Coleophoridae). Micron (Oxford, England), 40: 231–238.CrossRefGoogle Scholar
Yokohari, F., Tominaga, Y., and Tateda, H. 1982. Antennal hygroreceptors of the honey bee, Apismellifera L. Cell and Tissue Research, 226: 63–73. PMID:7127426 doi:10.1007/BF00217082.Google Scholar
Zacharuk, R.Y. 1989. Antennae and sensilla. In Comprehensive insect physiology, biochemistry, and pharmacology. Volume 6. Nervous system: sensory. Edited by Kerkut, G.A. and Gilbert, L.J.. Pergamon Press, Oxford, United Kingdom. pp. 1–69.Google Scholar