Hostname: page-component-76fb5796d-zzh7m Total loading time: 0 Render date: 2024-04-26T15:30:16.183Z Has data issue: false hasContentIssue false
  • English
  • Français

Ultrastructure of Antennal Morphology and Sensilla of Teak Skeletonizer, Eutectona machaeralis Walker (Lepidoptera: Crambidae)

Part of: Micrographia Collection

Published online by Cambridge University Press:  14 October 2020

Laijiao Lan Open the ORCID record for Laijiao Lan [Opens in a new window] ,
Shengkun Wang ,
Keyan Hu ,
Tao Ma  and
Xiujun Wen
Laijiao Lan
Affiliation:
Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, College of Forestry and Landscape Architecture, South China Agricultural University, 483 Wushan Road, Tianhe District, Guangzhou 510642, China
Shengkun Wang
Affiliation:
Research Institute of Tropical Forestry of CAF, Guangzhou 510520, China
Keyan Hu
Affiliation:
Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, College of Forestry and Landscape Architecture, South China Agricultural University, 483 Wushan Road, Tianhe District, Guangzhou 510642, China
Tao Ma*
Affiliation:
Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, College of Forestry and Landscape Architecture, South China Agricultural University, 483 Wushan Road, Tianhe District, Guangzhou 510642, China
Xiujun Wen*
Affiliation:
Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, College of Forestry and Landscape Architecture, South China Agricultural University, 483 Wushan Road, Tianhe District, Guangzhou 510642, China
*
*Authors for correspondence: Tao Ma, Email: matao@scau.edu.cn; Xiujun Wen, Email: wenxiujun@scau.edu.cn
*Authors for correspondence: Tao Ma, Email: matao@scau.edu.cn; Xiujun Wen, Email: wenxiujun@scau.edu.cn
Get access

Abstract

The leaf skeletonizer, Eutectona machaeralis (Walker) (Lepidoptera: Crambidae), is a severe insect pest of teak trees (Tectona grandis L.f.) in China. To provide some basic evidence for future semiochemical-based management strategies of E. machaeralis, the morphology, ultrastructure, and distribution of antennal sensilla of adults were observed under scanning and transmission electron microscopy. The shape and structure of antenna were similar between males and females, both being filiform. However, the antennal length of males was significantly longer than that of females. Eight morphological sensilla types were observed in both sexes: Böhm's bristles, sensilla trichodea, sensilla basiconica, sensilla chaetica, sensilla styloconica, sensilla coeloconica, sensilla auricillica, and sensilla squamiformia. Significant sexual dimorphism of the sensilla dimensions was found, especially in sensillar length. The putative and potential functions of the different sensilla types are discussed based on the fine structures of the cuticular walls and dendrites of the different sensilla types. We expect these results to help lay a solid foundation for future functional research and develop further investigations of E. machaeralis.

Keywords

chemical communicationolfactionSEMsexual dimorphismTEM
Type
Micrographia
Information
Microscopy and Microanalysis , Volume 26 , Issue 6 , December 2020 , pp. 1274 - 1282
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press on behalf of the Microscopy Society of America

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.)

Footnotes

a

L-J. Lan and S-K. Wang contributed equally to this work.

References

Altner, H, Sass, H & Altner, I (1977). Relationship between structure and function of antennal chemo-, hygro-, and thermoreceptive sensilla in Periplaneta americana. Cell Tissue Res 176, 389–405.CrossRefGoogle ScholarPubMed
Altner, H, Schaller-Selzer, L, Stetter, H & Wohlrabo, I (1983). Poreless sensilla with inflexible sockets: A comparative study of a fundamental type of insect sensilla probably comprising thermo- and hygroreceptors. Cell Tissue Res 234, 279–307.CrossRefGoogle ScholarPubMed
Amornsak, W, Cribb, B & Gordh, G (1998). External morphology of antennal sensilla of Trichogramma australicum Girault (Hymenoptera: Trichogrammatidae). Int J Insect Morphol Embryol 27, 67–82.CrossRefGoogle Scholar
Anderson, P & Hallberg, E (1990). Structure and distribution of tactile and bimodal taste/tactile sensilla on the ovipositor, tarsi and antennae of the flour moth, Ephestia kuehniella (Zeller) (Lepidoptera: Pyralidae). Int J Insect Morphol Embryol 19, 13–23.CrossRefGoogle Scholar
Anderson, P, Hallberg, E & Subchev, M (2000). Morphology of antennal sensilla auricillica and their detection of plant volatiles in the Herald moth, Scoliopteryx libatrix L. (Lepidoptera: Noctuidae). Arthropod Struct Dev 29, 33–41.CrossRefGoogle ScholarPubMed
Anfora, G, Vitagliano, S, Larsson, MC, Witzgall, P, Tasin, M, Germinara, GS & De Cristofaro, A (2014). Disruption of Phthorimaea operculella (Lepidoptera: Gelechiidae) oviposition by the application of host plant volatiles. Pest Manag Sci 70, 628–635.CrossRefGoogle ScholarPubMed
Ansebo, L, Ignell, R, Löfqvist, J & Hansson, BS (2005). Responses to sex pheromone and plant odours by olfactory receptor neurons housed in sensilla auricillica of the codling moth, Cydia pomonella (Lepidoptera: Tortricidae). J Insect Physiol 51, 1066–1074.CrossRefGoogle ScholarPubMed
Baker, TC, Ochieng’, SA, Cossé, AA, Lee, SG, Todd, JL, Quero, C & Vickers, NJ (2004). A comparison of responses from olfactory receptor neurons of Heliothis subflexa and Heliothis virescens to components of their sex pheromone. J Comp Physiol A 190, 155–165.CrossRefGoogle ScholarPubMed
Bartlet, E, Romani, R, Williams, IH & Isidoro, N (1999). Functional anatomy of sensory structures on the antennae of Psylliodes chrysocephala L. (Coleoptera: Chrysomelidae). Int J Insect Morphol Embryol 28, 291–300.CrossRefGoogle Scholar
Bawin, T, Collard, F, De Backer, L, Yarou, BB, Compère, P, Francis, F & Verheggen, FJ (2017). Structure and distribution of the sensilla on the antennae of Tuta absoluta (Lepidoptera: Gelechiidae). Micron 96, 16–28.CrossRefGoogle ScholarPubMed
Beeson, CFC (1941). The Ecology and Control of the Forest Insects of India and the Neighbouring Countries, p. 767. New Delhi: Vasant Press Dehra Dun India.Google Scholar
Binyameen, M, Anderson, P, Ignell, R, Seada, MA, Hansson, BS & Schlyter, F (2012). Spatial organization of antennal olfactory sensory neurons in the female Spodoptera littoralis moth: Differences in sensitivity and temporal characteristics. Chem Senses 37, 613–629.CrossRefGoogle ScholarPubMed
Bleeker, MAK, Smid, HM, Van Aelst, AC, Van Loon, JJA & Vet, LEM (2004). Antennal sensilla of two parasitoid wasps: A comparative scanning electron microscopy study. Microsc Res Tech 63, 266–273.CrossRefGoogle ScholarPubMed
Böhm, LK (1911). Die antennalen Sinnesorgane der Lepidopteren. Arb Zool Inst Universiltät Wien 19, 219–246.Google Scholar
Bruce, TJA, Wadhams, LJ & Woodcock, CM (2005). Insect host location: A volatile situation. Trends Plant Sci 10, 269–274.CrossRefGoogle ScholarPubMed
Callahan, PS (1975). Insect antennae with special reference to the mechanism of scent detection and the evolution of sensilla. Int J Insect Morphol Embryol 4, 381–430.CrossRefGoogle Scholar
Castrejón Gómez, VR, Nieto, G, Valdes, J, Castrejón, F & Rojas, JC (2003). The antennal sensilla of Zamagiria dixolophella Dyar (Lepidoptera: Pyralidae). Ann Entomol Soc Am 96(5), 672–678.CrossRefGoogle Scholar
Chang, XQ, Shu, Z, Liang, L & Wang, MQ (2015). Insight into the ultrastructure of antennal sensilla of Mythimna separata (Lepidoptera: Noctuidae). J Insect Sci 15(1), 124.CrossRefGoogle ScholarPubMed
Chiappini, E, Solinas, C & Solinas, M (2001). Antennal sensilla of Anagrus atomus (L.) (Hymenoptera: Mymaridae) female and their possible behavioural significance. Entomologica 35, 51–76.Google Scholar
Cossé, AA, Todd, JL & Baker, TC (1998). Neurons discovered in male Helicoverpa zea antennae that correlate with pheromone-mediated attraction and interspecific antagonismo. J Comp Physiol A 182, 585–594.Google Scholar
Cuperus, PL (1983). Distribution of antennal sense organs in male and female ermine moth Yponomeuta vigintipunctatus (Retzius) (Lepidoptera: Yponomeutidae). Int J Insect Morphol Embryol 12, 59–66.CrossRefGoogle Scholar
David, BV & Ananthakrishnan, TN (2004). General and Applied Entomology, p. 1161. New Delhi: Tata Mc Graw Hill Publishing Company Limited.Google Scholar
Derby, CD & Steullet, P (2001). Why do animals have so many receptors? The role of multiple chemosensors in animal perception. Biol Bull 200, 211–215.CrossRefGoogle ScholarPubMed
Du, JW (1988). Insect Pheromone and Application, 1st ed. Beijing: China Forestry Publishing House.Google Scholar
Faucheux, MJ (1999). Biodiversity and Unity of Sensory Organs in Insecta Lepidoptera. Nantes: Société des Sciences Naturelles de l'Ouest de la France.Google Scholar
Forstner, M, Gohl, T, Gondesen, I, Raming, K, Breer, H & Krieger, J (2008). Differential expression of SNMP-1 and SNMP-2 proteins in pheromone-sensitive hairs of moths. Chem Senses 33, 291–299.CrossRefGoogle ScholarPubMed
Gadenne, C, Barrozo, RB & Anton, S (2016). Plasticity in insect olfaction: To smell or not to smell? Annu Rev Entomol 61, 317–333.CrossRefGoogle ScholarPubMed
Gao, Y, Luo, LZ & Hammond, A (2007). Antennal morphology, structure and sensilla distribution in Microplitis pallidipes (Hymenoptera: Braconidae). Micron 38(6), 684–693.CrossRefGoogle ScholarPubMed
Gill, KP, Wilgenburg, EV, Macmillan, DL & Elgar, MA (2013). Density of antennal sensilla influences efficacy of communication in a social insect. Am Nat 182, 834–840.CrossRefGoogle Scholar
Hallberg, E (1979). The fine structure of the antennal sensilla of the pine sawfly Neodiprion sertifer (Insecta: Hymenoptera). Protoplasma 101, 111–126.CrossRefGoogle Scholar
Hallberg, E, Hansson, BS & Steinbrecht, RA (1994). Morphological characteristics of antennal sensilla in the European corn borer Ostrinia nubilalis (Lepidoptera: Pyralidae). Tissue Cell 26, 489–502.CrossRefGoogle Scholar
Hansson, BS, van der Pers, JNC, Hedenstriim, E, Hogberg, HE, Anderbrant, O & Liifqvist, J (1991). Sex pheromone perception in male pine sawflies, Neodiprion sertifer (Hymenoptera: Diprionidae). J Comp Physiol A 168, 533–538.CrossRefGoogle ScholarPubMed
Isidoro, N, Bin, F, Colazza, S & Vinson, SB (1996). Morphology of antennal gustatory sensilla and glands in some parasitoids Hymenoptera with hypothesis on their role in sex and host recognition. J Hym Res 5, 206–239.Google Scholar
Jerez-Rico, M & Quintero, M (2017). Heuristic forest planning model for optimizing timber production and carbon sequestration in teak plantations. iForest 10(2), 30–39.Google Scholar
Jung, CH, Park, JW & Boo, KS (1999). Types of antennal sensilla of the asian corn borer, Ostrinia furnacalis (Guenee). J Asia-Pac Entomol 2, 51–60.CrossRefGoogle Scholar
Keil, TA (1989). Fine structure of the pheromone sensitive sensilla on the antenna of the hawk moth, Manduca sexta. Tissue Cell 21, 139–151.CrossRefGoogle Scholar
Keil, TA (1999). Morphology and development of the peripheral olfactory organs. In Insect Olfaction, Hansson, BS (Ed.), pp. 5–47. Berlin, Heidelberg: Springer.CrossRefGoogle Scholar
Krieger, J, Gondesen, I, Forstner, M, Gohl, T, Dewer, Y & Breer, H (2009). HR11 and HR13 receptor-expressing neurons are housed together in pheromone-responsive sensilla trichodea of male Heliothis virescens. Chem Senses 34, 469–477.CrossRefGoogle ScholarPubMed
Krishnan, A, Prabhakar, S, Sudarsan, S & Sane, SP (2012). The neural mechanisms of antennal positioning in flying moths. J Exp Biol 215, 3096–3105.Google ScholarPubMed
Kulkarni, N, Paunikar, S & Hussaini, SS (2011). Susceptibility of teak skeletonizer, Eutectona machaeralis (Walker) to the EPN, Heterorhabditis indica Poinar. World J Zool 6, 33–39.Google Scholar
Lavoie-Dornik, J & McNeil, JN (1987). Sensilla of the antennal flagellum in Pseudaletia unipuncta (Haw.) (Lepidoptera: Noctuidae). Int J Insect Morphol Embryol 16, 153–167.CrossRefGoogle Scholar
Li, X & Bai, SF (2004). Ultrastructural studies on the antennal sensilla of Diadegma semiclausum Hellen (Hym., Ichneumonidae). J Henan Agri Univer 38(1), 45–48. (in Chinese)Google Scholar
Lopes, O, Barata, EN, Mustaparta, H & Araújo, J (2002). Fine structure of antennal sensilla basiconica and their detection of plant volatiles in the eucalyptus wood borer, Phoracantha semipunctata Fabricius (Coleoptera: Cerambycidae). Arthropod Struct Dev 31, 1–13.CrossRefGoogle Scholar
Ma, T, Zhang, YY, Wang, SK, Lan, LJ, Lin, N, Wang, C, Wu, YJ, Chang, MS, Sun, ZH, Wang, CL & Wen, XJ (2018). Reproductive behavior and sex pheromone production in Eutectona machaeralis (Lepidoptera: Crambidae). Fla Entomol 101(2), 189–194.CrossRefGoogle Scholar
Merivee, E, Rahi, M & Luik, A (1999). Antennal sensilla of the click beetle, Melanotus villosus (Geoffroy) (Coleoptera: Elateridae). Int J Insect Morphol Embryol 28, 41–51.CrossRefGoogle Scholar
Mo, SS & Zhao, DX (2006). Observationon antennal sensilla of Chlunetia transversa with scanning electron microscopy. Entomol J East China 15(2), 96–98 (in Chinese).Google Scholar
Nair, KSS (1988). The teak defoliator in Kerala, India. In Dynamics of Forest Insect Populations, Berryman, AA (Ed.), pp. 267–289. New York: Plenum Press.CrossRefGoogle Scholar
Nair, KSS (2007). Tropical Forest Insect Pests: Ecology, Impact and Management, p. 404. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Nair, KSS, Sudheendrakumar, VV, Varma, RV, Chako, KC & Jayaraman, K (1996). Effect of defoliation by Hyblaea puera and Eutectona machaeralis (Lepidoptera) on volume increment of teak. In Impact of Diseases and Insect Pests in Tropical Forests, Nair, KSS, Sharma, JK & Varma, RV (Eds.), pp. 23–26. Peechi, Kerala, India: Kerala Forest Research Institute, IUFRO Symposium Proceedings.Google Scholar
Ndomo-Moualeu, AF, Ulrichs, C, Radek, R & Adler, C (2014). Structure and distribution of antennal sensilla in the Indianmeal moth, Plodia interpunctella (Hübner, 1813) (Lepidoptera: Pyralidae). J Stored Prod Res 59, 66–75.CrossRefGoogle Scholar
Ochieng, SA, Park, KC, Zhu, JW & Baker, TC (2000). Functional morphology of antennal chemoreceptors of the parasitoid Microplitis croceipes (Hymenoptera: Braconidae). Arthropod Struct Dev 29, 231–240.CrossRefGoogle ScholarPubMed
Onagbola, EO & Fadamiro, HY (2008). Scanning electron microscopy studies of antennal sensilla of Pteromalus cerealellae (Hymenoptera: Pteromalidae). Micron 39, 526–535.CrossRefGoogle ScholarPubMed
Reis, CAF & Paludzyszyn Filho, E (2011). Estado da Arte de Plantios com Espécies Florestais de Interesse Comercial Para o Mato Grosso, p. 65. Colombo: Embrapa Florestas, (Embrapa Florestas. Documentos, 215).Google Scholar
Ren, LL, Wu, Y, Shi, J, Zhang, L & Luo, YQ (2014). Antenna morphology and sensilla ultrastructure of Tetrigus lewisi Candèze (Coleoptera: Elateridae). Micron 60, 29–38.CrossRefGoogle ScholarPubMed
Romero-López, A, Morón, M & Valdez, J (2010). Sexual dimorphism in antennal receptors of Phyllophaga ravida Blanchard (Coleoptera: Scarabaeoidea: Melolonthidae). Neotrop Entomol 39, 957–966.CrossRefGoogle Scholar
Ross, KTA & Anderson, M (1991). Ultrastructure of the funicular sensilla of the cabbage root fly, Delia radicum L. (Diptera: Anthomyiidae). Int J Insect Morphol Embryol 20, 83–101.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Roychoudhury, N (2012). Deployment of resistance in teak to key insect pests. Indian Forester 138(2), 123–130.Google Scholar
Schneider, D (1964). Insect antennae. Annu Rev Entomol 9, 103–122.CrossRefGoogle Scholar
Sen, A & Mitchell, BK (2001). Olfaction in the Colorado potato beetle: Ultrastructure of antennal sensilla in Leptinotarsa sp. J Biosci 26, 233–246.CrossRefGoogle ScholarPubMed
Shen, J, Lou, BG, Shen, YL & Gao, QK (2005). Scanning electron microscopy observation on antennal sensilla of Opogona sacchari. J Zhejiang For Sci Technol 25(6), 27–30 (in Chinese).Google Scholar
Shukla, PK, Jamaluddin, K & Roychoudhury, N (2001). Diseases and Insect Pests of Teak, p. 86. ICFRE Brochure No. 68. Jabalpur: Tropical Forest Research Institute.Google Scholar
Slifer, EH (1970). The structure of arthropod chemoreceptors. Annu Rev Entomol 15, 121–142.CrossRefGoogle Scholar
Steinbrecht, RA, Laue, M & Ziegelberger, G (1995). Immunolocalization of pheromone-binding protein and general odorant-binding protein in olfactory sensilla of the silk moths Antheraea and Bombyx. Cell Tissue Res 282, 203–217.CrossRefGoogle Scholar
Steinbrecht, RA & Müller, B (1991). The thermo-/hygrosensitive sensilla of the silkmoth Bombyx mori: Morphological changes after dry- and moist-adaptation. Cell Tissue Res 266, 441–456.CrossRefGoogle Scholar
Van Baaren, J, Boivin, G, Le Lannic, J & Nénon, JP (1999). Comparison of antennal sensilla of Anaphes victus and A. listronoti (Hymenoptera, Mymaridae), egg parasitoids of Curculionidae. Zoomorphology 119, 1–8.CrossRefGoogle Scholar
Wall, C (1978). Morphology and histology of the antenna of Cydia nigricana (F.) (Lepidoptera: Tortricidae). Int J Insect Morphol Embryol 7, 237–250.CrossRefGoogle Scholar
Wee, SL, Oh, HW & Park, KC (2016). Antennal sensillum morphology and electrophysiological responses of olfactory receptor neurons in trichoid sensilla of the diamondback moth (Lepidoptera: Plutellidae). Fla Entomol 99, 146–158.CrossRefGoogle Scholar
Wu, SX, Chen, ZQ & Wang, TH (1979). A preliminary study on the teak defoliator, Pyrausta machaeralis Walker. Acta Entomol Sin 22, 156–163 (in Chinese).Google Scholar
Yan, XZ, Deng, CP, Xie, JX, Wu, LJ, Sun, XJ & Hao, C (2017). Distribution patterns and morphology of sensilla on the antennae of Plutella xylostella (L.)—A scanning and transmission electron microscopic study. Micron 103(5), 1–11.CrossRefGoogle Scholar
Yang, H, Yan, SC & Liu, D (2009). Ultrastructural observations on antennal sensilla of Coleophora obducta (Meyrick) (Lepidoptera: Coleophoridae). Micron 40(2), 231–238.CrossRefGoogle ScholarPubMed
Yuan, X, Zhang, SF, Zhang, Z, Kong, XB, Wang, HB, Shen, GC & Zhang, HJ (2013). Antennal morphology and sensilla ultrastructure of the web-spinning sawfly Acantholyda posticalis Matsumura (Hymenoptera: Pamphiliidae). Micron 50, 20–28.CrossRefGoogle ScholarPubMed
Zacharuk, RY (1985). Sensory organs: cuticular sensilla. In Comparative Insect Physiology, Biochemistry and Pharmacology, vol. 6, Kerkut, GA & Gilbert, LI (Eds.), pp. 1–69. Oxford: Pergamon Press.Google Scholar