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The metathoracic wing-hinge chordotonal organ of an atympanate moth, Actias luna (Lepidoptera, Saturniidae): a light- and electron-microscopic study

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Summary

The structure of a simple chordotonal organ, the presumed homologue of the noctuoid moth tympanal organ, is described in the atympanate moth, Actias luna. The organ consists of a proximal scolopidial region and a distal strand, which attaches peripherally to the membranous cuticle ventral to the hindwing alula. The strand is composed of elongate, microtubule-rich cells encased in an extracellular connective tissue sheath. The scolopidial region houses three mononematic, monodynal scolopidia, each comprised of a sensory cell, scolopale cell, and attachment cell. The dendritic apex is octagonally shaped in transverse section, its inner membrane lined by a laminated structure reminiscent of the noctuoid tympanal organ ‘collar’. A 9+0-type cilium emerges from the dendritic apex, passes through both the scolopale lumen and cap, and terminates in an extracellular space distal to the latter. Proximal extensions of the attachment cell and distal prolongations of the scolopale cell surrounding the cap are joined by an elaborate desmosome, with which is associated an extensive electron-dense fibrillar plaque. Within the scolopale cell, this plaque constitutes the scolopale ‘rod’ material. The data are discussed in terms of both the organ's potential function, and its significance as the evolutionary proto-type of the noctuoid moth ear.

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References

  • Altner H (1988) The scolopalial organs in the first antennal segment in Allacma fusca (Collembola, Sminthuridae). Zoomorphology 108:173–181

    Google Scholar 

  • Ashhurst DE (1982) The structure and development of insect connective tissues. In: King RC, Akai H (eds) Insect ultrastructure, vol 1, Plenum, New York London

    Google Scholar 

  • Ball EE (1981) Structure of the auditory system of the weta Hemideina crassidens (Blanchard 1851) (Orthoptera, Ensifera, Gryllacridoidea, Stenopelmatidae). 2. Ultrastructure of the auditory sensilla. Cell Tissue Res 217:345–359

    Google Scholar 

  • Bartholomew GA, Casey TM (1978) Oxygen consumption of moths during rest, pre-flight warm-up, and flight in relation to body size and wing morphology. J Exp Biol 76:11–25

    Google Scholar 

  • Blöchl R, Selzer R (1988) Embryogenesis of the connective chordotonal organ in the pedicel of the American cockroach: cell lineage and morphological differentiation. Cell Tissue Res 252:669–678

    Google Scholar 

  • Bloom JW, Zacharuk RY, Holodniuk AE (1981) Ultrastructure of a terminal chordotonal organ sensillum in larval antennae of the yellow mealworm, Tenebrio molitor L. Can J Zool 59:515–524

    Google Scholar 

  • Boyan GS, Fullard JH (1986) Interneurones responding to sound in the tobacco budworm moth Heliothis virescens (Noctuidae): morphological and physiological characteristics. J Comp Physiol A 158:391–404

    Google Scholar 

  • Bromley AK, Dunn JA, Anderson M (1980) Ultrastructure of the antennal sensilla of aphids. II. Trichoid, chordotonal, and campaniform sensilla. Cell Tissue Res 205:493–511

    Google Scholar 

  • Corbière-Tichané G (1971) Ultrastructure des organes chordotonaux des piéces céphaliques chez la larve du Speophyes lucidulus Delar. (Coléoptère Cavernicole de la sous-famille des Bathysciinae). Z Zellforsch 117:275–302

    Google Scholar 

  • Corbière-Tichané G (1975) L'organe de Johnston chez l'imago de Speophys cavernicole de la sous-famille des Bathysciinae) Ultrastructure. J Microsc Biol Cell 22:55–68

    Google Scholar 

  • Coro F, Pérez J (1987) Estructura del órgano timpánico de Empyreuma pugione (Lepidoptera: Arctiidae). Cienc Biol 17:31–41

    Google Scholar 

  • Debauche H (1935) Recherches sur les organes sensoriels antennaires de Hydropsyche longipennis. La Cellule 44:43–83

    Google Scholar 

  • Dethier VG (1963) The physiology of insect senses. Methuen, London

    Google Scholar 

  • Doolan JM, Young D (1981) The organization of the auditory organ of the bladder cicada, Cystosoma saundersii. Philos Trans R Soc Lond (Biol) 291:525–540

    Google Scholar 

  • Dorsett DA (1962) Preparation for flight by hawk-moths. J Exp Biol 39:579–588

    Google Scholar 

  • Elsner N, Popov AV (1978) Neuroethology of acoustic communication. Adv Insect Physiol 13:229–355

    Google Scholar 

  • Faucheux MJ (1985) Structure of the tarso-pretarsal chordotonal organ in the imago of Tineola bisselliella Humm. (Lepidoptera: Tineidae). Int J Insect Morph Embryol 14:147–154

    Google Scholar 

  • Friedman MH (1972) A light and electron microscopic study of sensory organs and associated structures in the foreleg tibia of the cricket, Gryllus assimilis. J Morphol 138:263–328

    Google Scholar 

  • Fullard JH (1988) The tuning of moth ears. Experientia 44:423–428

    Google Scholar 

  • Fuller H, Ernst A (1973) Die Ultrastruktur der femoralen Chordotonalorgane von Carausius morosus. Br Zool J (Anat) 91:547–601

    Google Scholar 

  • Ghiradella H (1971) Fine structure of the noctuid moth ear. I. The transducer area and connections to the tympanic membrane in Feltia subgothica Hawthorn. J Morphol 134:21–45

    Google Scholar 

  • Glauert AM (1975) Fixation, dehydration and embedding of biological specimens. Elsevier, New York

    Google Scholar 

  • Graber V (1882) Die chordotonalen Sinnesorgane und das Gehör der Insekten. Arch Mikrosk Anat Entw Mech 20:506–640

    Google Scholar 

  • Gray EG (1960) The fine structure of the insect ear. Philos Trans R Soc Lond (Biol) 243:75–94

    Google Scholar 

  • Hallberg E (1981) Johnston's organ in Neodiprion sertifer (Insecta: Hymenoptera) J Morphol 167:305–312

    Google Scholar 

  • Haskell PT (1961) Insect sounds Witherby, London

    Google Scholar 

  • Howse PE (1968) The fine structure and functional organization of chordotonal organs. Symp Zool Soc (Lond) 23:167–198

    Google Scholar 

  • Hustert R (1974) Morphologie und Atmungsbewegungen des 5. Abdominalsegmentes von Locusta migratoria migratorioides. Zool Jb Physiol Bd 78:157–174

    Google Scholar 

  • Kennel J von, Eggers F (1933) Die abdominalen Tympanalorgane der Lepidopteren. Zool Jahrb Abt Anat 57:1–104

    Google Scholar 

  • Kühne R (1982) Neurophysiology of the vibration sense in locusts and bushcrickets: response characteristics of single receptor units. J Insect Physiol 28:155–163

    Google Scholar 

  • Lane NJ, Flores V (1990) The cytoskeketal components in the maintenance of intercellular junctions in an insect. Cell Tissue Res 262:373–385

    Google Scholar 

  • Lane NJ, Skaer H leB (1980) Intercellular junctions in insect tissues. Adv Insect Physiol 15:35–213

    Google Scholar 

  • Locke M, Huie P (1975) Staining of the elastic fibers in insect connective tissue after tannic acid/glutaraldehyde fixation. Tissue Cell 7:211–216

    Google Scholar 

  • Madsen BM, Miller LA (1987) Auditory input to motor neurons of the dorsal longitudinal flight muscles in a noctuid moth (Barathra brassicae L.). J Comp Physiol A 160:23–31

    Google Scholar 

  • Matsuda R (1976) Morphology and evolution of the insect abdomen. Pergamon, New York

    Google Scholar 

  • Meier T, Reichert H (1990) Embryonic development and evolutionary origin of the orthopteran auditory organs. J Neurobiol 21:592–610

    Google Scholar 

  • Michel K (1977) Feinstrukturelle Besonderheiten im mesothorakalen Tympanalorgan der Ruderwanze Callicorixa praeusta (Heteroptera: Corixidae). Entomol Germ 3:316–323

    Google Scholar 

  • Miller LA (1983) How insects detect and avoid bats. In: Huber F, Markl H (eds) Neuroethology and behavioral physiology. Springer, Berlin Heidelberg New York, pp 250–266

    Google Scholar 

  • Miller TA (1979) Insect neurophysiological techniques. Springer, New York Heidlerberg Berlin pp 241–242

    Google Scholar 

  • Moran DT, Rowley JC III (1975) The fine structure of the cockroach subgenual organ. Tissue Cell 7:91–106

    Google Scholar 

  • Moran DT, Rowley JC III, Varela FG (1975) Ultrastructure of the grasshopper proximal femoral chordotonal organ. Cell Tissue Res 161:445–457

    Google Scholar 

  • Moran DT, Varela FJ, Rowley JC III (1977) Evidence for active role of cilia in sensory transduction. Proc Natl Acad Sci USA 74:793–797

    Google Scholar 

  • Moulins M (1976) Ultrastructure of chordotonal organs. In: Mill PJ (ed) Structure and function of proprioceptors in the invertebrates. Chapman and Hall, London, pp 387–426

    Google Scholar 

  • Nüesch H (1953) The morphology of the thorax of Telea polyphemus (Lepidoptera). I. Skeleton and muscles. J Morphol 93:589–608

    Google Scholar 

  • Nüesch H (1957) Die Morphologie des Thorax von Telea polyphemus Cr. (Lepid.). II. Nervensystem. Zool Jahrb Abt Anat 75:615–642

    Google Scholar 

  • Pantin CFA (1946) Notes on microscopical techniques for zoologists. Cambridge University Press, Cambridge

    Google Scholar 

  • Pappas LG, Larsen JR (1976) Labellar chordotonal organs of the mosquito, Culiseta inornata (Williston) (Diptera: Culicidae). Int J Insect Morphol Embryol 5:145–150

    Google Scholar 

  • Paul DH (1974) Responses to acoustic stimulation of thoracic interneurones in noctuid moths. J Insect Physiol 20:2205–2218

    Google Scholar 

  • Pillsbury N (1980) Electron microscopy. In: Sheehan DC, Hrapchak BP (eds) Theory and practice of histotechnology. Mosby, St. Louis Toronto London, pp 327–346

    Google Scholar 

  • Pumphrey RJ (1940) Hearing in insects. Biol Rev 15:107–132

    Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at a high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    Google Scholar 

  • Roeder KD (1966) Acoustic sensitivity of the noctuid tympanic organ and its range for the cries of bats. J Insect Physiol 12:843–859

    Google Scholar 

  • Roeder KD (1967) Nerve cells and insect behavior. Harvard University Press, Cambridge

    Google Scholar 

  • Schmidt K (1969) Der Feinbau der stiftführenden Sinnesorgane im Pedicellus der Florfliege Chrysopa Leach (Chrysopidae, Planipennia). Z Zellforsch 99:357–388

    Google Scholar 

  • Slifer EH, Sekhon SS (1975) The femoral chordotonal organs of a grasshopper, Orthoptera, Acrididae. J Neurocytol 4:419–438

    Google Scholar 

  • Spangler HG (1988) Moth hearing, defense, and communication. Annu Rev Entomol 33:59–81

    Google Scholar 

  • Theophilidis G (1986) The femoral chordotonal organs of Decticus albifrons (Orthoptera: Tettigoniidae). I. Structure Comp Biochem Physiol 84:529–536

    Google Scholar 

  • Toh Y (1981) Fine structure of sense organs on the antennal pedicel and scape of the male cockroach, Periplaneta americana. J Ultrastruct Res 77:119–132

    Google Scholar 

  • Toh Y, Yokohari F (1985) Structure of the antennal chordotonal sensilla of the American cockroach. J Ultrastruct Res 90:124–134

    Google Scholar 

  • Uga S, Kuwabara M (1965) On the fine structure of the chordotonal sensillum in antenna of Drosophila melanogaster. J Electronmicrosc 14:173–181

    Google Scholar 

  • Vande Berg JS (1971) Fine structural studies of Johnston's organ in the tobacco hornworm moth, Manduca sexta (Johannson). J Morphol 133:439–456

    Google Scholar 

  • Wolfrum U (1990) Actin filaments: the main components of the scolopale in insect sensilla. Cell Tissue Res 261:85–96

    Google Scholar 

  • Yack JE, Fullard JH (1990) The mechanoreceptive origin of insect tympanal organs: a comparative study of similar nerves in tampanate and atympanate moths J Comp Neurol 300:523–534

    Google Scholar 

  • Yager DD, Hoy RR (1987) The midline metathoracic ear of the praying mantis, Mantis religiosa. Cell Tissue Res 250:531–541

    Google Scholar 

  • Young D (1970) The structure and function of a connective chordotonal organ in the cockroach leg. Philos Trans Roy Soc (Biol) 256:401–428

    Google Scholar 

  • Young D (1973) Fine structure of the sensory cilium of an insect auditory receptor. J Neurocytol 2:47–58

    Google Scholar 

  • Young D, Ball E (1974a) Structure and development of the auditory system in the prothoracic leg of the cricket Teleogryllus commodus (Walker). I. Adult structure. Z Zellforsch 147:293–312

    Google Scholar 

  • Young D, Ball E (1974b) Structure and development of the tracheal organ in the mesothoracic leg of the cricket Teleogryllus commodus (Walker). Z Zellforsch 147:325–334

    Google Scholar 

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Authors and Affiliations

  1. Department of Zoology, Erindale College, University of Toronto, L5L 1C6, Mississauga, Ontario, Canada

    J. E. Yack

  2. Department of Zoology, University of Toronto, M5S 1A1, Toronto, Ontario, Canada

    B. I. Roots

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Yack, J.E., Roots, B.I. The metathoracic wing-hinge chordotonal organ of an atympanate moth, Actias luna (Lepidoptera, Saturniidae): a light- and electron-microscopic study. Cell Tissue Res 267, 455–471 (1992). https://doi.org/10.1007/BF00319368

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  • DOI: https://doi.org/10.1007/BF00319368

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