Abstract
Tympanate hearing has evolved in at least 6 different orders of insects, but had not been reported until recently in the Diptera. This study presents a newly discovered tympanal hearing organ, in the parasitoid tachinid fly, Ormia ochracea. The hearing organ is described in terms of external and internal morphology, cellular organization of the sensory organ and preliminary neuroanatomy of the primary auditory afferents. The ear is located on the frontal face of the prothorax, directly behind the head capsule. Conspicuously visible are a pair of thin cuticular membranes specialized for audition, the prosternal tympanal membranes. Directly attached to these membranes, within the enlarged prosternal chamber, are a pair of auditory sensory organs, the bulbae acusticae. These sensory organs are unique among all auditory organs known so far because both are contained within an unpartitioned acoustic chamber. The prosternal chamber is connected to the outside by a pair of tracheae. The cellular anatomy of the fly's scolopophorous organ was investigated by light and electron microscopy. The bulba acustica is a typical chordotonal organ and it contains approximately 70 receptor cells. It is similar to other insect sensory organs associated with tympanal ears. The similarity of the cellular organization and tympanal morphology of the ormiine ear to the ears of other tympanate insects suggests that there are potent constraints in the design features of tympanal hearing organs, which must function to detect high frequency auditory signals over long distances. Each sensory organ is innervated by a branch of the frontal nerve of the fused thoracic ganglia. The primary auditory afferents project to each of the pro-, meso-, and metathoracic neuropils. The fly's hearing organ is sexually dimorphic, whereby the tympanal membranes are larger in females and the spiracles larger in males. The dimorphism presumably reflects differences in the acoustic behavior in the two sexes.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Bailey WJ, Römer H (1991) Sexual differences in auditory sensitivity: mismatch of hearing threshold and call frequency in a tettigoniid (Orthoptera, Tettigoniidae: Zaprochilinae) J Comp Physiol [A] 169:349–353
Bennet-Clark HC, Ewing AW (1967) Stimuli provided by courtship of male Drosophila melanogaster. Nature 215:669–671
Bennet-Clark HC, Ewing AW (1968) The wing mechanism involved in the courtship of Drosophila. J Exp Biol 49:117–128
Boo KS, Richards AG (1975) Fine structure of the scolopidia in the Johnston's organ of male Aedes aegyptii (L.) (Diptera: Culicidae) Int J Insect Morphol Embryol 4:549–566
Cade WH (1975) Acoustically orienting parasitoids: fly phonotaxis to cricket song. Science 190:1312–1313
Cardone B, Fullard JH (1988) Auditory characteristics and sexual dimorphism in the gypsy moth. Physiol Entomol 13:9–14
Dethier VG (1963) The physiology of insect senses. Methuen, London
Eggers F (1919) Das thorakale bitympanale Organ einer Gruppe der Lepidoptera Heterocera. Zool Jahrb 41:273–376
Ghiradella H (1971) Fine structure of the noctuid moth ear. J Morphol 134:21–46
Gray EG (1960) The fine structure of the insect ear. Philos Trans R Soc Lond (Biol) 243:75–94
Haskell PT, Belton P (1957) Electrical responses of certain lepidopterous tympanal organs. Nature 177:139–140
Hengstenberg R (1991) Gaze control in the blowfly Calliphora: a multisensory, two-stage integration process. Sem Neurosci 3:19–29
Hertweck H (1931) Anatomie und Variabilität des Nervensystems und der Sinnesorgane von Drosophila melanogaster (Meigen) Z Wiss Zool 139:559–663
Hoikkala A, Hoy RR, Kaneshiro KY (1989) High-frequency clicks of Hawaiian picture-winged Drosophila species. Anim Behav 37:927–934
Howse PE (1968) The fine structure and organization of chordotonal organs. Symp Zool Soc (Lond) 23:167–198
Hoy RR (1989) Startle, categorical response, and attention in acoustic behavior of insects. Annu Rev Neurosci 12:355–375
Johnston C (1855) Auditory apparatus of the Culex mosquito. Q J Microsc Sci 3:97–102
Lakes-Harlan R, Heller K-G (1992) Ultrasound sensitive ears in a parasitoid fly. Naturwissenschaften 79:224–226
Mangold JR (1978) Attraction of Euphasiopterix ochracea, Corothrella sp. and gryllids to broadcast songs of the southern mole cricket. Fla Entomol 61:57–61
Markl H (1973) Leistungen des Vibrationssinnes bei wirbellosen Tieren. Fortschr Zool 21:100–120
Mayer AM (1874) Experiments on the supposed auditory apparatus of the mosquito. Am Nat 8:577–592
Meier T, Reichert H (1990) Embryonic development and evolutionary origin of the orthopteran auditory organs. J Neurobiol 21:592–610
Michel K (1974) Das Tympanalorgan von Gryllus bimaculatus Degeer (Saltatoria, Gryllidae). Z Morphol Tiere 77:285–315
Michelsen A, Nocke H (1974) Biophysical aspects of sound communication in insects. Adv Insect Physiol 10:247–296
Michelsen A, Larsen ON (1985) Hearing and sound. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol 6. Pergamon Press, New York, pp 495–556
Miller LA (1970) Structure of the green lacewing tympanal organ (Chrysopa carnea, Neuroptera). J Morphol 131:359–382
Miller LA (1977) Directional hearing in the locust Schistocerca gregaria Forskål (Acrididae: Orthoptera). J Comp Physiol [A] 119:85–98
Moulins M (1976) Ultrastructure of chordotonal organs. In: Mill PJ (ed) Structure and function of proprioceptors in invertebrates. Chapman and Hall, London, pp 387–426
Narins PM, Capranica RR (1976) Sexual differences in the auditory system of the tree frog Eleutherodactylus coqui. Science 192:378–380
Pantin CFA (1946) Notes on microscopical techniques for zoologists. Cambridge University Press, New York
Preuss T, Hengstenberg R (1992) Structure and kinematics of the prosternal organs and their influence on head position in the blowfly Calliphora erythrocephala Meig. J Comp Physiol [A] 171:483–493
Risler H, Schmidt K (1967) Der Feinbau der Scolopidien im Johnstonschen Organ von Aedes aegypti (L.). Z Natuforsch [B] 22:759–62
Robert D, Amoroso J, Hoy RR (1992) The evolutionary convergence of hearing in a parasitoid fly and its cricket host. Science 258:1135–1137
Roeder KD (1967) Nerve cells and insect behavior, 2nd ed. Harvard University Press, Cambridge
Roth LM (1948) A study of mosquito behavior. Am Midland Nat 40:265–352
Sandeman DC, Markl H (1980) Head movements in flies (Calliphora) produced by deflection of the halteres. J Exp Biol 85:43–60
Schwabe J (1906) Beiträge zur Morphologie und Histologie der tympanalen Sinnesapparate der Orthopteren. Zoologica 50:1–154
Sivinsky T, Webb JC (1986) Changes in a Caribbean fruit fly acoustic signal with social situation (Diptera: Tephritidae). Ann Entomol Soc Am 79:146–149
Soper RS, Shewell GE, Tyrrell D (1976) Colcondamyia auditrix nov. sp. (Diptera: Sarcophagidae), a parasite which is attracted by the mating song of its host, Okanagana rimosa (Homoptera: Cicadidae). Can Entomol 108:61–68
Strausfeld NJ, Seyan HS (1985) Convergence of visual, haltere and prosternal inputs at neck motor neurons. Cell Tissue Res 240:601–615
Venable JH, Coggeshall R (1965) A simplified lead citrate stain for use in electron microscopy. J Cell Biol 25:407
Walker TJ (1986) Monitoring the flights of field crickets (Gryllus spp.) and a tachnid fly (Euphasiopterix ochracea) in north Florida. Fla Entomol 69:678–685
Webb JC, Burk T, Sivinsky J (1983) Attraction of female Caribbean fruit flies Anastrepha suspensa (Diptera: Tephritidae) to the presence of males and male produced stimuli in field cages. Ann Entomol Soc Am 76:996–998
Wineriter SA, Walker TJ (1990) Rearing phonotactic parasitoid flies (Diptera: Tachinidae, Ormiini, Ormia spp.) Entomophaga 35:621–632
Wood DM (1987) Tachinidae. In: Manual of nearctic diptera. (Research Branch Agriculture Canada Monograph 28, vol 2) pp 1193–1270
Yack JE, Fullard JH (1990) The mechanoreceptive origin of insect tympanal organs: a comparative study of similar nerves in tympanate and atympanate moths. J Comp Neurol 300:523–534
Yack JE, Roots BI (1992) 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
Yager DD (1990) Sexual dimorphism of auditory function and structure in praying mantises (Mantodea; Dictyoptera). J Zool (Lond) 221:517–537
Yager DD, Hoy RR (1986) The cyclopean ear: a new sense for the praying mantis. Science 231:727–729
Yager DD, Hoy RR (1987) The midline metathoracic ear of the praying mantis, Mantis religiosa. Cell Tissue Res 250:531–541
Young D (1973) Fine structure of the sensory cilium of an insect auditory receptor. J Neurocytol 2:47–58
Young D, Hill KG (1977) Structure and function of the auditory system of the cicada, Cystosoma saundersii. J Comp Physiol [A] 117:23–45
Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice-Hall, New Jersey
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Robert, D., Read, M.P. & Hoy, R.R. The tympanal hearing organ of the parasitoid fly Ormia ochracea (Diptera, Tachinidae, Ormiini). Cell Tissue Res 275, 63–78 (1994). https://doi.org/10.1007/BF00305376
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/BF00305376