Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-28T06:15:01.190Z Has data issue: false hasContentIssue false

Nymphal antennae and antennal sensilla in Aleurodicus dispersus (Hemiptera: Aleyrodidae)

Published online by Cambridge University Press:  28 May 2014

L.X. Zheng
Affiliation:
Laboratory of Insect Ecology, South China Agricultural University, Guangzhou, China
W.J. Wu*
Affiliation:
Laboratory of Insect Ecology, South China Agricultural University, Guangzhou, China
G.W. Liang
Affiliation:
Laboratory of Insect Ecology, South China Agricultural University, Guangzhou, China
Y.G. Fu
Affiliation:
Environment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Danzhou, Hainan, China
*
*Author for correspondence Phone: +8602085283467 Fax: +8602085283467 E-mail: [email protected]

Abstract

Whiteflies have distinct nymphal stages: their first stage is mobile, whereas the later immature stages are sessile. The developmental and structural changes of antennae and antennal sensilla in whiteflies during these stages have rarely been investigated. This paper describes the morphology of antennae and antennal sensilla in four nymphal stages of Aleurodicus dispersus based on scanning electron microscopy. There were significant differences found in shape and length of the antennae, and differences in type, number, morphological structure and distributional pattern of antennal sensilla in the four nymphal stages of A. dispersus. We found two types of sensilla on the antennae of first-instar nymph, three types on the third-instar nymphal antennae, four types on the second-instar and seven types on the fourth-instar nymphal antennae. Sensilla trichoidea (ST) and elevated sensilla placodea were found on the antennae of each nymphal stage, sensilla chaetica only occurred on the antennae of fourth-instar nymph. Sensilla furcatea occurred on the antennae of second- and third-instar nymphs, and sensilla basiconica were found on the antennae of second- and fourth-instar nymphs. In addition, there were sensilla campaniform and sensilla coeloconica found only on the antennae of fourth-instar nymph, whereas the ST of fourth-instar nymphs included sensilla trichoidea 1 and sensilla trichoidea 2. The possible functions of antennal sensilla are discussed. Our results contribute to a better understanding of the development of the olfactory system of whitefly nymphal stages, and provide a basis for further exploration of chemical communication mechanisms between whiteflies and host plants.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Altner, H. & Loftus, R. (1985) Ultrastructure and function of insect thermo- and hygroreceptors. Annual Review of Entomology 30, 273295.CrossRefGoogle Scholar
Altner, H. & Prillinger, L. (1980) Ultrastructure of invertebrate chemo- thermo-, and hygrareceptors and its functional significance. International Review of Cytology 67, 69139.CrossRefGoogle Scholar
Altner, H., Schaller-Selzer, L., Stetter, H. & 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, 279307.CrossRefGoogle ScholarPubMed
Barlin, M.R. & Vinson, S.B. (1981) Multiporous plate sensilla of the Chalcidoidea (Hymenoptera). International Journal of Insect Morphology and Embryology 10, 2942.CrossRefGoogle Scholar
Basibuyuk, H.H. & Quicke, D.L.J. (1999) Gross morphology of multiporous plate sensilla in the Hymenoptera (Insecta). Zoologica Scripta 28, 5167.CrossRefGoogle Scholar
Bink-Moenen, R.M. (1983) Revision of the African whiteflies (Aleyrodidae) mainly based a collection from Tchad. Monog. Nederlandse Entomologische Vereniging 10, 1211.Google Scholar
Bourdais, D., Vernon, P., Krespi, L., Lelannic, J. & Van Baaren, J. (2006) Antennal structure of male and female Aphidius rhopalosiphi DeStefani-Peres (Hymenoptera: Braconidae): description and morphological alterations after cold storage or heat exposure. Microscopy Research and Technique 69, 10051013.CrossRefGoogle ScholarPubMed
Bromley, A.K., Dunn, J.A. & Anderson, M. (1979) Ultrastructure of the antennal sensilla of aphids. I. Coeloconic and placoid sensilla. Cell and Tissue Research 203, 427442.CrossRefGoogle ScholarPubMed
Bromley, A.K., Dunn, J.A. & Anderson, M. (1980) Ultrastructure of the antennal sensilla of aphids. Cell and Tissue Research 205, 493511.CrossRefGoogle ScholarPubMed
Cave, R.D. & Gaylor, M.J. (1987) Antennal sensilla of male and female Telenomus reynoldsi Gordh and Coker (Hymenoptera: Scelionidae). International Journal of Insect Morphology and Embryology 16(1), 2739.CrossRefGoogle Scholar
Chapman, R.F. (1982) The Insects: Structure and Function. London, Edward Arnold.Google Scholar
Chapman, R.F. (1998) The Insects: Structure and Function. 4th edn. UK, Cambridge University Press.CrossRefGoogle Scholar
DeVaney, J.A., Eddy, G.W., Handke, B.D. & Lopez, E. (1970) Olfactory responses of the adult screw-worm after removal of the antennae, mouthparts, tarsi and legs. Journal of Economic Entomology 63, 18161819.CrossRefGoogle ScholarPubMed
Dietz, A. & Humphreys, W.J. (1971) Scanning electron microscopic studies of antennal receptors of the worker honey bee, including sensilla campaniformia. Annals of the Entomological Society of America 64, 919925.CrossRefGoogle Scholar
Domenichini, G. (1981) Structure di Trialeurodes vaporariorum (Westw) e loro funzioni (Homoptera: Aleyrodidae). Memorie della Società Entomologica Italiana 60, 169176.Google Scholar
Eichmuller, S. & Schafer, S. (1995) Sensory neuron development revealed by taurine immunocytochemistry in the honeybee. Journal of Comparative Neurology 352, 297307.CrossRefGoogle ScholarPubMed
Gao, Y., Luo, L.Z. & Hammond, A. (2007) Antennal morphology, structure and sensilla distribution in Microplitis pallidipes (Hymenoptera: Braconidae). Micron 38, 684693.CrossRefGoogle ScholarPubMed
Gill, R.J. (1990) The morphology of whiteflies. pp. 1346in Gerling, G. (Ed.) Whiteflies: Their Bionomics, Pest Status and Management. Andover, UK, Intercept.Google Scholar
Greenberg, B. (1970) Species distribution of new structures on fly antennae. Nature 228, 13381339.CrossRefGoogle ScholarPubMed
Gullan, P.J. & Cranston, P.S. (2000) The Insects: An Outline of Entomology. 2nd edn. Oxford, Blackwell.Google Scholar
Hashimoto, Y. (1990) Unique features of sensilla on the antennae of Formicidae (Hymenoptera). Journal of Applied Entomology and Zoology 25, 491501.CrossRefGoogle Scholar
Hays, D.B. & Vinson, S.B. (1971) Acceptance of Heliothis virescences (F.) (Lepidoptera: Noctuidae) as a host by parasitic Cardichiles nigriceps Viereck (Hymenoptera: Braconidae). Animal Behaviour 19, 344352.CrossRefGoogle Scholar
Kleineidam, C., Romani, R., Tautz, J. & Izidoro, N. (2000) Ultrastructure and physiology of the CO2 sensitive sensillum ampullaceum in the leaf-cutting ant Atta sexdens. Arthropod Structure and Development 29, 4355.CrossRefGoogle ScholarPubMed
Kristoffersen, L., Hallberg, E., Wallén, R. & Anderbrant, O. (2006) Sparse sensible array on Trios apicalis (Homoptera: Triozidae) antennae–an adaptation to high stimulus level. Arthropod Structure and Development 35, 8592.CrossRefGoogle Scholar
Kumashiro, B.R., Lai, P.Y., Funasaki, G.Y. & Teramoto, K.K. (1983) Efficacy of Nephaspis amnicola and Encarsia haitiensis in controlling Aleurodicus dispersus in Hawaii. Proceedings of the Hawaiian Entomological Society 24, 261269.Google Scholar
Mani, M. & Krishnamoorthy, A. (2002) Classical biological control of the spiralling whitefly, Aleurodicus dispersus Russell – an appraisal. Insect Science and its Application 22(4), 263273.Google Scholar
Mellor, H.E. & Anderson, M. (1995) Antennal sensilla of whiteflies: Trialeurodes vaporariorum (Westwood), the glasshouse whitefly, Aleyrodes proletella (Linnaeus), the cabbage whitefly, and Bemisia tabaci (Gennadius), the tobacco whitefly (Homoptera: Aleyrodidae). Part 1: external morphology. International Journal of Insect Morphology and Embryology 24(2), 133143.CrossRefGoogle Scholar
Merivee, E., Ploomi, A., Rahi, M., Bresciani, J., Ravn, H.P., Luik, A. & Sammelselg, V. (2002) Antennal sensilla of the ground beetle Bembidion properans Steph. (Coleoptera, Carabidae). Micron 33, 429440.CrossRefGoogle ScholarPubMed
Norton, W.N. & Vinson, S.B. (1974 a) Antennal sensilla of three parasitic Hymenoptera. International Journal of Insect Morphology and Embryology 3, 305316.CrossRefGoogle Scholar
Norton, W.N. & Vinson, S.B. (1974 b) A comparative ultrastructural and behavioural study of the antennal sensory sensilla of the parasitoid Cardiochiles nigriceps (Hymenoptera: Braconidae). Journal of Morphology 142, 329350.CrossRefGoogle ScholarPubMed
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 Structure and Development 29, 231240.CrossRefGoogle ScholarPubMed
Olson, D.M. & 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, 507520.CrossRefGoogle Scholar
Onagbola, E.O., Meyer, W.L., Boina, D.B. & Stelinski, L.L. (2008) Morphological characterization of the antennal sensilla of the Asian citrus psylli, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), with reference to their probable function. Micron 39, 11841191.CrossRefGoogle Scholar
Pettersson, E.M., Hallberg, E. & Bigersson, G. (2001) Evidence for the importance of odour perception in the parasitoid Rhopalicus tutela (Walker) (Hym.: Pteromalidae). Journal of Applied Entomology 125, 293301.CrossRefGoogle Scholar
Pophf, B. (1997) Olfactory responses record from sensilla coeloconica of the silkmoth Bombyx mori. Physiological Entomology 22, 239248.CrossRefGoogle Scholar
Roux, O., Van Baaren, J., Gers, C., Arvanitakis, L. & Legal, L. (2005) Antennal structure and oviposition behavior of the specialist parasitoid: Cotesia plutellae. Microscopy Research and Technique 68, 3644.CrossRefGoogle ScholarPubMed
Ruchty, M., Romani, R., Kuebler, L.S., Ruschioni, S., Roces, F., Isidoro, N. & Kleineidam, C.J. (2009) The thermo-sensitive sensilla coeloconica of leaf-cutting ants (Atta volleneideri). Arthropod Structure and Development 38, 195205.CrossRefGoogle Scholar
Russell, L.M. (1965) A new species of Aleurodicus douglas and two close relatives. Florida Entomologist 48, 4755.CrossRefGoogle Scholar
Schmidt, K. & Kuhbandner, B. (1983) Ontogeny of the sensilla placodea on the antennae of Aulacus striatus Jurine (Hymenoptera: Aulacidae). International Journal of Insect Morphology and Embryology 12, 4357.CrossRefGoogle Scholar
Schneider, D. (1964) Insect antennae. Annual Review of Entomology 9, 103122.CrossRefGoogle Scholar
Shanbhag, S.R., Müller, B. & Steinbrecht, R.A. (1999) Atlas of olfactory organs of Drosophila melanogaster 1. Types, external organization, innervation and distribution of olfactory sensilla. International Journal of Insect Morphology and Embryology 28, 377397.CrossRefGoogle Scholar
Slifer, E.H. & Sekhon, S.S. (1961) Fine structure of the sense organs on the antennal flagellum of the honey bee, Apis mellifera. Linnaeus. Journal of Morphology 109, 351381.CrossRefGoogle Scholar
Snodgrass, R.E. (1956) Anatomy of the Honey Bee. 1st edn. New York, Comstock Publishing Associate.Google Scholar
Srinivasa, M.V. (2000) Host plants of the spiraling whitefly Aleurodicus dispersus Russell (Hemiptera: Aleyrodidae). Pest Management in Horticultural Ecosystems 6, 79105.Google Scholar
Steinbrecht, R.A. (1984) Arthropods: chemo-, thermo-, and hygroreceptors. pp. 523553in Hahn, J.B., Matoltsy, A.G. & Richards, K.S. (Eds) Biology of the Integument, Vol. 1. Berlin, Springer-Verlag.CrossRefGoogle Scholar
Steinbrecht, R.A. (1997) Pore structures in insect olfactory sensilla: a review of data and concepts. International Journal of Insect Morphology and Embryology 26, 229245.CrossRefGoogle Scholar
Steiner, C. & Keil, T.A. (1995) Morphogenesis of the antenna of the male silkmoth, Antheraea polyphemus. V. Development of the peripheral nervous system. Tissue Cell 27, 275288.CrossRefGoogle ScholarPubMed
Stort, C.A. & Barelli, N. (1981) Genetic study of olfactory structures in the antennae of two Apis mellifera subspecies. Journal of the Kansas Entomological Society 54, 352.Google Scholar
Van Baaren, J., Barbier, R. & Nénon, J.P. (1996) Female antennal sensilla of Epidinocarsis lopezi and Leptomastix dactylopii (Hymenoptera: Encyrtidae), parasitoids of pseudo coccid mealybugs. Canadian Journal of Zoology 74, 710720.CrossRefGoogle Scholar
Van Baaren, J., Boivin, G., Lelannic, J. & Nénon, J.P. (1999) Comparison of antennal sensilla of Anaphes victus and A. listronoti (Hymenoptera: Mymaridae), egg parasitoids of Curculionidae. Zoomorphology 199, 18.CrossRefGoogle Scholar
Voegelé, J., Cals-Usciati, J., Pihan, J.P. & Daumal, J. (1975) Structure de l'antenne female des trichogrammes. Entomophaga 20, 161169.CrossRefGoogle Scholar
Weseloh, R.M. (1972) Sense organs of the hyperparasite Cheiloneurus noxius (Hymenoptera: Encyrtidae) important in hosts election processes. Annals of the Entomological Society of America 65, 4146.CrossRefGoogle Scholar
Whitman, D.W. & Eller, F.J. (1990) Parasitic wasps orient to green leaf volatiles. Chemoecology 1(2), 4146.CrossRefGoogle Scholar
Yang, H., Yan, S.C. & Liu, D. (2009) Ultrastructural observations on antennal sensilla of Coleophora obducta (Meyrick) (Lepidoptera: Coleophoridae). Micron 40, 231238.CrossRefGoogle ScholarPubMed
Zacharuk, R.Y. (1980) Ultrastructure and function of insect chemosensilla. Annual Review of Entomology 25, 2747.CrossRefGoogle Scholar
Zacharuk, R.Y. (1985) Antennae and sensilla. pp. 169in Kerkut, G.A. & Gilbert, L.I. (Eds) Comprehensive Insect Physiology, Biochemistry and Pharmacology, Vol. 6. Oxford, Pergamon Press.Google Scholar
Zacharuk, R.Y. & Shields, V.D. (1991) Sensilla of immature insects. Annual Review of Entomology 36, 331354.CrossRefGoogle Scholar
Zheng, L.X., Wu, W.J. & Fu, Y.G. (2010) Sensilla on the antenna of adult spiraling whitefly Aleurodicus dispersus. Chinese Bulletin of Entomology 47(3), 525528.Google Scholar
Zimmermann, B. (1991) Differentiation of the thermo-hygrosensitive (no-pore) sensilla on the antenna of Antheraea pernyi (Lepidoptera: Saturniidae): a study of cryofixed material. Cell and Tissue Research 266, 427440.CrossRefGoogle Scholar