Abstract
A new structure, here tentatively named the “frontal gland,” specifically found on frons of male adults of the Asian rice spittlebug, Callitettix versicolor (Fabricius, 1794) (Hemiptera: Auchenorrhyncha: Cercopidae), is reported. Adult C. versicolor is distinctly dimorphic in frons morphology. The frons in female adults, like that in most cercopid species, is normally swollen and nearly bulbose and is covered with short pilosity, while the frons in male adults is visibly different, with the lower 3/5 of the postclypeus and anteclypeus being centrally flat, bare and smooth on the surface. SEM observations revealed that the flat frons surface of the male adults is covered with numerous, very fine pores. In total, each frons has over 4500 pores on the central flat area, with an average density of 55.5 ± 1.50 pores per 100 µm2. The distance among the pores averages 10.63 ± 1.8 µm. Each pore unit is composed of a round, deep cavity in which one central conical process is set. The cavity is delimited by a cuticular rim and the opening of the cavity averages 2.89 ± 0.20 µm in diameter. The central, conical process has a sponge-like apex and measures 2.52–2.70 µm in diameter. In addition, one or two (two in most cases) extremely fine pits (0.42–0.56 µm in diameter) are located on the marginal cuticle rim surrounding the cavity and its central conical process. These cuticular, fine pits are located proximal to the pores, at a distance of 0.98–1.96 µm. These porous structures are not present on the frons in female adults. They are assumed to be an exocrine gland system and are possibly the male sex pheromone-releasing glands, as they are only present in male adults. Observations of mating behavior showed that it is likely that the secretions made by the frontal gland constitute short-range attractants and may fulfil aphrodisiac functions to stimulate mating. The species of Auchenorrhyncha were previously thought to communicate via acoustic signals, but the findings described here suggest that at least one Auchenorrhynchan species also uses chemicals for sexual communication.
References
Aldrich, J.R. (1996) Sex pheromones in Homoptera and Heteroptera. In: Schaefer, C.W. (Ed.), Studies on Hemipteran Phylogeny. Thomas Say Publications in Entomology. Entomological Society of America, Lanham, Maryland, pp. 199–233.
Birch, M.C. & Haynes, K.F. (1982) Insect Pheromones. The Institute of Biology’s Studies in Biology No. 147. Edward Arnold (Publishers) Ltd., London, 57 pp.
Boulard, M. & Boulard, J. (1979) Un organe énigmatique chez les femelles de Locris (Homoptera Cercopidae). Annales de la Société entomologique de France, Nouvelle Série, 15, 513–523.
Carayon, J. (1984) Les androconies de certains Hémiptères Scutelleridae. Annales de la Société entomologique de France, Nouvelle Série, 20, 113–134.
Cardé, R.T. (1997) Insect Pheromone Research: New Directions. Chapman and Hall, New York, 684 pp.
https://doi.org/10.1007/978-1-4615-6371-6
Chen, X. & Liang, A.-P. (2012) Laboratory rearing of Callitettix versicolor (Hemiptera: Cicadomorpha: Cercopidae), with descriptions of the immature stages. Annals of the Entomological Society of America, 105, 664–670.
https://doi.org/10.1603/AN12052
Chen, X. & Liang, A.-P. (2015) Identification of a self-regulatory pheromone system that controls nymph aggregation behavior of rice spittlebug Callitettix versicolor. Frontiers in Zoology, 12, 10. https://doi.org/10.1186/s12983-015-0102-4
Chen, X., Meyer-Rochow, V.B., Fereres, A., Morente, M. & Liang, A.-P. (2018) The role of biofoam in shielding spittlebug nymphs (Insecta, Hemiptera, Cercopidae) against bright light. Ecological Entomology, 43, 273–281.
https://doi.org/10.1111/een.12496
Claridge, M.F. (1985a) Acoustic signals in the Homoptera. Annual Review of Entomology, 30, 297–317.
https://doi.org/10.1146/annurev.en.30.010185.001501
Claridge, M.F. (1985b) Acoustic behaviour of leafhoppers and planthoppers: species problems and speciation. In: Nault, L.R. & Rodriguez, J.G. (Eds.), The Leafhoppers and Planthoppers. John Wiley & Sons, New York, pp. 103–125.
Claridge, M.F. (1990) Acoustic recognition signals: barriers to hybridisation in Homoptera Auchenorrhyncha. Canadian Journal of Zoology, 68, 1741–1746.
https://doi.org/10.1139/z90-255
Claridge, M.F., Morgan, J.C. & Moulds, M.S. (1999) Substrate-transmitted acoustic signals of the primitive cicada, Tettigarcta crinita Distant (Hemiptera Cicadoidea, Tettigarctidae). Journal of Natural History, 33, 1831–1834.
https://doi.org/10.1080/002229399299752
Cobben, R.H. (1987) What do we really know about host selection in Auchenorrhyncha? In: Vidano, C. & Arzone, A. (Eds.), Proceedings of the 6th Auchenorrhyncha Meeting, CNR-IPRA, Turin, Italy, 1987, pp. 81–92.
Distant, W.L. (1908) Rhynchota, Homoptera and Appendix (Pt.). In: Bingham, C.T. (Ed.), The Fauna of British India including Ceylon and Burma. Vol. IV. Taylor & Francis, London, pp. i–xv + 1–501.
Fonseca, M.G., Silva, S.E.B., Auad, A.M., Paiva, I.G. & Borges, C.A. (2013) Mating behavior of Mahanarva spectabilis (Hemiptera: Cercopidae) under laboratory conditions. Journal of Insect Behavior, 26, 824–831.
https://doi.org/10.1007/s10905-013-9394-4
Ginzel, M.D. (2010) Olfactory signals. In: Breed, M.D. & Moore, J. (Eds.), Encyclopedia of Animal Behavior. Academic Press, Oxford, pp. 584–588.
https://doi.org/10.1016/B978-0-08-045337-8.00268-0
Goodchild, A.J.P. (1966) Evolution of the alimentary canal in the Hemiptera. Biological Reviews of the Cambridge Philosophical Society, 41, 97–139.
https://doi.org/10.1111/j.1469-185X.1966.tb01540.x
Gough, A.J.E., Games, D.E., Staddon, B.W., Knight, D.W. & Olagbemiro, T.O. (1986) C9 aliphatic adelhydes: possible sex pheromone from male tropical West African shield bug, Sphaerocoris annulus. Zeitschrift für Naturforschung, 41C, 93–96.
https://doi.org/10.1515/znc-1986-11-1221
Guan, S.-Q., Zhang, B.-L. & Zuo, Y.L. (1991) Preliminary study on the occurrence and control of Callitettix versicolor Fabricius and Abidama liuensis Metcalf. Plant Protection, 17 (3), 10–12.
Hoffmann, W.E. (1942) Bugs or Homoptera. The cicadas, plant hoppers, plant lice, scale insects, and others. Special Publication of Lingnan Natural History Survey and Museum, 9, 1–20, pls. 1–30.
Knight, D.W., Staddon, B.W. & Thorne, M.J. (1985) Presumed sex pheromon from androconical glands of male cotton harlequin bug Tectocoris diophthalmus (Heteroptera: Scutelleridae) identified as 3,5-dihydroxy-4-pyrone. Zeitschrift für Naturforschung, 40C, 851–853.
https://doi.org/10.1515/znc-1985-11-1217
Lallemand, V. (1949) Révision des Cercopinae (Hemiptera Homoptera). Première partie. Mémoires d’Institut Royal des Sciences Naturelles de Belgique, Series 2, 32, 1–193.
Li, D.-Y., Liao, G.-H. & He, C.-J. (2010) Growth and decline regulation of Callitettix versicolor and its control in paddy field. Southwest China Journal of Agricultural Sciences, 23, 1370–1373. [in Chinese with English abstract]
Li, J.-Q., Zhao, Z.-M., Wu, S.-Y., Ming, K. & Hou, L.-N. (2001) Biology and ecology of rice spittle bug (Callitettix versicolor). Journal of Southwestern Agricultural University, 23, 156–159. [in Chinese with English abstract]
Liang, A.-P. & Fletcher, M.J. (2002) Morphology of the antennal sensilla in four Australian spittlebug species (Hemiptera: Cercopidae) with implications for phylogeny. Australian Journal of Entomology, 41, 39–44.
https://doi.org/10.1046/j.1440-6055.2002.00266.x
Liang, A.-P. & Webb, M.D. (2002) New taxa and revisionary notes in Rhinaulacini spittlebugs from southern Asia (Homoptera: Cercopidae). Journal of Natural History, 36, 729–756.
https://doi.org/10.1080/00222930110062336
Liao, G.-H., Li, D.-Y. & He, C.-J. (2010) Distribution and injury of Callitettix versicolor in rice. Guizhou Agriculture Science, 38, 96–99. [in Chinese]
Lim, G.T. & Pan, Y.C. (1980) Entomofauna of sugarcane in Malaysia. Proceedings of the International Society of Sugar Cane Technologists, 17, 658–1679.
Luo, Q.Y. & Xu, S.M. (2011) The occurrence and integrated control of Callitettix versicolor (Fabricius). Hubei Plant Protection, 2011 (2), 29–30. [in Chinese]
Machado, F.E.L., Peck, D.C. & Lerma, J.M. (2001) Importancia de la comunicación vibracional en el comportamiento reproductivo del salivazo de los pastos (Homoptera: Cercopidae). Revista Colombiana de Entomologia, 29, 9–15.
McGavin, G.C. (1993) Bugs of the World. Blandford, London, 192 pp.
Metcalf, Z.P. (1961) General Catalogue of the Homoptera. Fasc. VII. Cercopoidea. Part 2. Cercopidae, Paper No. 1278. North Carolina State College, Raleigh, North Carolina, pp. 1–607.
Metcalf, Z.P. & Horton, G. (1934) The Cercopidae (Homoptera) of China. Lingnan Science Journal, 13, 367–429, pls. 37–43.
Morgan, J.C. & Claridge, M.F. (1993) Acoustic signals and life history of Machaerota rastrata. In: Drosopoulos, S., Petrakis, P.V., Claridge, M.F. & de Vrijer, P.W.F. (Eds.), Proceedings of the 8th Auchenorrhyncha Congress, Delphi, Greece, 9–13 August 1993, pp. 91–92.
Morris, H. & Waterhouse, D.F. (2001) The Distribution and Importance of Arthropod Pests and Weeds of Agriculture in Myanmar. ACIAR, Canberra, 73 pp.
Ossiannilsson, F. (1949) Insect drummers. A study on the morphology and function of the sound-producing organ of Swedish Homoptera Auchenorrhyncha. Opuscula Entomologica, 10 (Supplementum), 1–146.
Pawar, A.D. & Bhalla, O.P. (1976 [1974)) Pest complex of rice in Himachal Pradesh. Indian Journal of Entomology, 36, 358–359.
Peck, D.C. & Thompson, V. (2008) Spittlebugs (Hemiptera: Cercopoidea). In: Capinera, J.L. (Ed.), Encyclopedia of Entomology. Springer, Dordrecht, pp. 3512–3516.
Percy-Cunningham, J.E. & MacDonald, J.A. (1987) Biology and ultrastructure of sex pheromone-producing glands. In: Prestwich, G.D. & Blomquist, G.J. (Eds.), Pheromone Biochemistry. Academic Press, Orlando, Florida, pp. 27–69.
https://doi.org/10.1016/B978-0-12-564485-3.50007-5
Schneider, C.A., Rasband, W.S. & Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671–675.
https://doi.org/10.1038/nmeth.2089
Staddon, B.W., Abdollahi, A., Parry, G., Rissiter, M. & Knight, D.W. (1994) Major component in male sex pheromone of cereal pest Eurygaster integriceps Puton (Heteroptera: Scutelleridae) identified as a homosesquiterpenoid. Journal of Chemical Ecology, 20, 2721–2731.
https://doi.org/10.1007/BF02036203
Stål, C. (1865) Homoptera nova vel minus cognita. Öfversigt af Kongl. Vetenskaps‑Akademiens Förhandlingar, Stockholm, 22, 145–165.
Thompson, V. (1994) Spittlebug indicators of nitrogen-fixing plants. Ecological Entomology, 19, 391–398.
https://doi.org/10.1111/j.1365-2311.1994.tb00257.x
Thompson, V. (1997) Spittlebug nymphs (Homoptera: Cercopidae) in Heliconia flowers (Zingiberales: Heliconiaceae): preadaptation and evolution of the first aquatic Homoptera. Revista de Biologia Tropical, 45, 905–912.
Ubik, K., Vrkoc, J., Zdárek, J. & Kontev, C. (1975) Vanillin: possible sex pheromone of an insect. Naturwissenschaften, 62, 348.
https://doi.org/10.1007/BF00608902
Vrkoc, J., Ubik, K., Zdárek, J. & Kontev, C. (1977) Ethyl acrylate and vanillin as components of the male sex pheromone complex in Eurygaster integriceps (Heteroptera: Scutelleridae). Acta Entomologica Bohemoslov, 74, 205–206.
Yuan, F. (1986) Family Cercopidae. In: Deng, G.-F. (Ed.), Agricultural Insects of China. Science Press, Beijing, pp. 154–157. [in Chinese]
Zdárek, J. & Kontev, C. (1975) Some ethological aspects of reproduction in Eurygaster integriceps (Heteroptera: Scutelleridae). Acta Entomologica Bohemoslov, 72, 239–248.