Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-24T03:40:26.524Z Has data issue: false hasContentIssue false
  • English
  • Français

Hearing in tsetse flies? Morphology and mechanics of a putative auditory organ

Published online by Cambridge University Press:  28 October 2008

E.J. Tuck ,
J.F.C. Windmill  and
D. Robert
E.J. Tuck
Affiliation:
School of Biological Sciences, Woodland Road, University of Bristol, Bristol, UK
J.F.C. Windmill
Affiliation:
School of Biological Sciences, Woodland Road, University of Bristol, Bristol, UK
D. Robert*
Affiliation:
School of Biological Sciences, Woodland Road, University of Bristol, Bristol, UK
*
*Author for correspondence Fax: 117 331 6737 E-mail: D.Robert@bristol.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

Tympanal hearing organs are widely used by insects to detect sound pressure. Such ears are relatively uncommon in the order Diptera, having only been reported in two families thus far. This study describes the general anatomical organization and experimentally examines the mechanical resonant properties of an unusual membranous structure situated on the ventral prothorax of the tsetse fly, Glossina morsitans (Diptera: Glossinidae). Anatomically, the prosternal membrane is backed by an air filled chamber and attaches to a pair of sensory chordotonal organs. Mechanically, the membrane shows a broad resonance around 5.3–7.2 kHz. Unlike previously reported dipteran tympana, a directional response to sound was not found in G. morsitans. Collectively, the morphology, the resonant properties and acoustic sensitivity of the tsetse prothorax are consistent with those of the tympanal hearing organs in Ormia sp. and Emblemasoma sp. (Tachinidae and Sarcophagidae). The production of sound by several species of tsetse flies has been repeatedly documented. Yet, clear behavioural evidence for acoustic behaviour is sparse and inconclusive. Together with sound production, the presence of an ear-like structure raises the enticing possibility of auditory communication in tsetse flies and renews interest in the sensory biology of these medically important insects.

Keywords

DipteraGlossina morsitanshearingprothoracic membranetsetsetympanum
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 99 , Issue 2 , April 2009 , pp. 107 - 119
Copyright
Copyright © 2008 Cambridge University Press

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

Adamo, S.A., Robert, D., Perez, J. & Hoy, R.R. (1995) The response of an insect parasitoid, Ormia ochracea (Tachinidae), to the uncertainty of larval success during infestation. Behavioral Ecology and Sociobiology 36, 111–118.CrossRefGoogle Scholar
Allen, G.R., Kamien, D., Berry, O., Byrne, P. & Hunt, J. (1999) Larviposition, host cues and planidial behaviour in the sound-locating parasitoid fly Homotrixa alleni (Diptera: Tachinidae). Journal of Insect Behavior 12, 67–79.CrossRefGoogle Scholar
Bennet-Clark, H.C. & Ewing, A.W. (1967) Stimuli provided by courtship of male Drosophila melanogaster. Nature 215, 669–671.CrossRefGoogle Scholar
Briceño, R.D., Eberhard, W.G. & Robinson, A.S. (2007) Copulation behaviour of Glossina pallidipes (Diptera: Muscidae) outside and inside the female, with a discussion of genitalic evolution. Bulletin of Entomological Research 97, 471–488.CrossRefGoogle ScholarPubMed
Cade, W. (1975) Acoustically orienting parasitoids: Fly phonotaxis to cricket song. Science 190, 1312–1312.CrossRefGoogle Scholar
Cocroft, R.B., Tieu, T.D., Hoy, R.R. & Miles, R.N. (2000) Directionality in the mechanical response to substrate vibration in a treehopper (Hemiptera: Memracidae: Umbonia crassicornis). Journal of Comparative Physioliology A 186, 695–705.CrossRefGoogle Scholar
Colvin, J. & Gibson, G. (1992) Host-seeking behavior and management of tsetse. Annual Review of Entomology 37, 21–40.CrossRefGoogle ScholarPubMed
Denlinger, D.L., Saini, R.K. & Chaudhury, M.F.B. (1983) Parturition in the tsetse fly Glossina morsitans: Pattern of activity, sound production and evidence for control by the mother's brain. Journal of Insect Physiology 29, 715–721.CrossRefGoogle Scholar
Dethier, V.G. (1954) Notes on the biting response of tsetse flies. American Journal of Tropical Medicine and Hygiene 3, 160–171.CrossRefGoogle ScholarPubMed
Edgecomb, R.S., Robert, D., Read, M.P. & Hoy, R.R. (1995) The tympanal hearing organ of a fly: phylogenetic analysis of its morphological origins. Cell tissue research 282, 251–268.CrossRefGoogle ScholarPubMed
Erickson, E.I.C. & Moller, A.R. (1975) Sound production in the tsetse fly Glossina morsitans morsitans. Journal of the Acoustical Society of America 57, 984–986.CrossRefGoogle ScholarPubMed
Fullard, J.H. & Yack, J.E. (1993) The evolutionary biology of insect hearing. Trends in Ecology and Evolution 8, 248–252.CrossRefGoogle ScholarPubMed
Gibson, G. & Torr, S.J. (1999) Visual and olfactory responses of haematophagous Diptera to host stimuli. Medical and Veterinary Entomology 13, 2–23.CrossRefGoogle ScholarPubMed
Gooding, R.H. & Krafsur, E.S. (2005) Tsetse genetics: Contributions to biology, systematics and control of tsetse flies. Annual Review of Entomology 50, 101–123.CrossRefGoogle ScholarPubMed
Göpfert, M.C. & Robert, D. (2001) Active auditory mechanics in mosquitoes. Proceedings of the Royal Society of London, Series B 268, 333–339.CrossRefGoogle ScholarPubMed
Green, C.H. & Cosens, D. (1983) Spectral response of the tsetse fly, Glossina morsitans morsitans. Journal of Insect Physiology 29, 795–800.CrossRefGoogle Scholar
Howe, M.A. & Lehane, M.J. (1986) Post-feed buzzing in the tsetse, Glossina morsitans morsitans, is an endothermic mechanism. Physiological Entomology 11, 279–286.CrossRefGoogle Scholar
Hoy, R.R. & Robert, D. (1996) Tympanal hearing in insects. Annual Review of Entomology 41, 433–450.CrossRefGoogle ScholarPubMed
Jackson, J.C. & Robert, D. (2006) Nonlinear auditory mechanism enhances female sounds for male mosquitoes. The Proceedings of the National Academy of Sciences USA 103, 16734–16739.CrossRefGoogle ScholarPubMed
Kohler, U. & Lakes-Harlan, R. (2001) Auditory behaviour of a parasitoid fly (Emblemasoma auditrix, Sarcophagidae, Diptera). Journal of Comparative Physiology A 187, 581–587.Google ScholarPubMed
Kreyszig, E. (1999). Advanced Engineering Mathematics. pp. 626–634. 8th edn. New York, USA, John Wiley & Son.Google Scholar
Kristjanson, P.M., Swallow, B.M., Rowlands, G.J., Kruska, R.L. & Leeuw, P.N. (1999) Measuring the costs of African animal trypanosomosis, the potential benefits of control and returns to research. Agricultural Systems 59, 79–98.CrossRefGoogle Scholar
Lakes-Harlan, R. & Heller, K.G. (1992) Ultrasound-sensitive ears in a parasitoid fly. Naturwissenschaften 79, 224–226.CrossRefGoogle Scholar
Lakes-Harlan, R., Stölting, H. & Stumpner, A. (1999) Convergent evolution of insect hearing organs from a preadaptive structure. Proceedings of the Royal Society London, Series B 266, 1161–1167.CrossRefGoogle Scholar
Leonard, D.E. & Saini, R.K. (1993) Semiochemicals from anal exudate of larvae of tsetse flies Glossina morsitnas morsitans Westwood and G. morsitans centralis Machado attract gravid females. Journal of Chemical Ecology 19, 2039–2046.CrossRefGoogle Scholar
Moloo, S.K. (1971) An artificial feeding technique for Glossina. Parasitology 63, 507–512.CrossRefGoogle ScholarPubMed
Müller, P. & Robert, D. (2001). A shot in the dark: the silent quest of a free-flying phonotactic fly. Journal of Experimental Biology 204, 1039–1052.CrossRefGoogle ScholarPubMed
Nash, T.A.M. (1969) The establishment and value of large self-maintaining colonies of tsetse flies (Glossina spp.). Tropical Animal Health and Production 1, 1–6.CrossRefGoogle Scholar
Petersen, F.T., Meier, R., Kutty, S.N. & Wiegmann, B.M. (2007) The phylogeny and evolution of host choice in the Hippoboscoidea (Diptera) as reconstructed using four molecular markers. Molecular and Phylogenetic Evolution 45, 111–122.CrossRefGoogle ScholarPubMed
Popham, E.J., Parr, M.J. & Chowdhury, V. (1977) Specific differences in tsetse fly sounds and their behavioural significance. Experientia. 34, 1152–1154.CrossRefGoogle Scholar
Ramsauer, N. & Robert, D. (2000) Phonotactic orientation in a parasitoid fly. Naturwissenschaften 87, 315–319.CrossRefGoogle Scholar
Reinouts Van Haga, H.A. & Mitchell, B.K. (1975) Temperature receptors on tarsi of the tsetse fly Glossina morsitans West. Nature 255, 225–226.CrossRefGoogle ScholarPubMed
Robert, D. & Hoy, R.R. (2007) Auditory systems in insects. pp. 155–184in North, G. & Greenspan, R.J. (Eds) Invertebrate Neurobiology. New York, USA, Cold Spring Harbor Laboratory Press.Google Scholar
Robert, D., Amoroso, J. & Hoy, R.R. (1992) The evolutionary convergence of hearing in a parasitoid fly and its cricket host. Science 258, 1135–1137.CrossRefGoogle Scholar
Robert, D., Read, M.P. & Hoy, R.R. (1994) The tympanal hearing organ of the parasitoid fly Ormia ochracea (Diptera, Tachninidae, Ormiini). Cell Tissue Research 275, 63–78.CrossRefGoogle ScholarPubMed
Robert, D., Edgecomb, R.S., Read, M.P. & Hoy, R.R. (1996a) Tympanal hearing in tachinid flies (Diptera, Tachinidae, Ormiini): the comparative morphology of an innovation. Cell Tissue Reearch 284, 435–448.CrossRefGoogle ScholarPubMed
Robert, D., Miles, R.N. & Hoy, R.R. (1996b) Directional hearing by mechanical coupling in the parasitoid fly Ormia ochracea. Journal of Comparative Physiology A 179, 29–44.CrossRefGoogle ScholarPubMed
Robert, D., Miles, R.N. & Hoy, R.R. (1998) Tympanal mechanics in the parasitoid fly Ormia ochracea intertympanal coupling during mechanical vibration. Journal of Comparative Physiology A 183, 443–452.CrossRefGoogle Scholar
Robert, D., Miles, R.N. & Hoy, R.R. (1999) Tympanal hearing in the Sarcophagid parasitoid fly Emblemasoma sp.: The biomechanics of directional hearing. Journal of Experimental Biology 202, 1865–1876.CrossRefGoogle ScholarPubMed
Rohlf, F.J. (2001) TPS-DIG (Software for acquiring landmarks), v.1.4. Published by the authors. Available at http://www.life.bio.sunysb.edu/morph/ (accessed 19 November 2007).Google Scholar
Saini, R.K. (1981) Communication by sound in tsetse? Journal of the South Pacific Association for Commonwealth Literature and Language Studies 24, 98–99.Google Scholar
Saini, R.K. (1983a) Sound production associated with feeding behaviour of the tsetse, Glossina m. morsitans. Entomologia Experimentalis et Applicata 34, 1–8.CrossRefGoogle Scholar
Saini, R.K. (1983b) Acoustic emissions of tsetse. Insect Science and Its Application 5, 341–344.Google Scholar
Saini, R.K. (1985) Sound production associated with sexual behaviour of the tsetse, Glossina morsitans morsitans. Insect Science and Its Application 6, 637–644.Google Scholar
Smith, D.H., Pepin, J. & Stich, A.H.R. (1998) Human African trypanosomiasis: an emerging public health crisis. British Medical Bulletin 54, 341–355.CrossRefGoogle ScholarPubMed
Soper, R.S., Shewell, G.E. & Tyrell, D. (1976) Colcondamyia auditrix nov. sp. (Diptera: Sarcophagidae), a parasite which is attracted by the mating sound of its host, Okanagan rimosa (Homoptera: Cicadidae). The Canadian Entomologist 108, 61–68.CrossRefGoogle Scholar
Stölting, H., Stumpner, A. & Lakes-Harlan, R. (2007) Morphology and physiology of the prosternal chordotonal organ of the sarcophagid fly Sarcophaga bullata (Parker). Journal of Insect Physiology 53, 444–454.CrossRefGoogle ScholarPubMed
Stumpner, A. & Lakes-Harlan, R. (1996) Auditory interneurons in a hearing fly (Therobia leonidei, Ormiini, Tachinidae, Diptera). Journal of Comparative Physiology A 178, 227–233.CrossRefGoogle Scholar
Stumpner, A., Allen, G.R. & Lakes-Harlan, R. (2007) Hearing and frequency dependence of auditory interneurons in the parasitoid fly Homotrixa alleni (Tachinidae: Ormiini). Journal of Comparative Physiology A 193, 113–125.CrossRefGoogle ScholarPubMed
Van Der Goes Van Naters, W.M. & Den Otter, C.J. (1998) Amino acids as taste stimuli for tsetse flies. Physiological Entomology 23, 278–284.CrossRefGoogle Scholar
Voskamp, K.E., Everaarts, E. & Den Otter, C.J. (1999) Olfactory responses to attractants and repellents in tsetse. Medical and Veterinary Entomology 13, 386–392.CrossRefGoogle ScholarPubMed
Vreysen, M.J.B., Saleh, K.M., Ali, M.Y., Abdulla, A.M., Zhu, Z.-R., Juma, K.G., Dyck, V.A., Msang, A.R., Mkonyi, P.A. & Feldmann, H.U. (2000) Glossina austeni (Diptera: Glossinidae) eradicated on the Island of Unguja, Zanzibar, using the sterile insect technique. Journal of Economic Entomology 93, 123–135.CrossRefGoogle ScholarPubMed
Wall, R. & Langley, P. (1991) From behaviour to control: the development of trap and target techniques for tsetse fly population management. Agricultural Zoology Reviews 4, 137–159.Google Scholar
WHO (2006) African trypanosomiasis (Sleeping sickness). WHO Fact Sheet 259. Available at http://www.who.int/mediacentre/factsheets/fs259/en/ (accessed 19 November 2007).Google Scholar
Yack, J.E. (2004) The structure and function of auditory chordotonal organs in insects. Microscopy Research and Technique 63, 315–337.CrossRefGoogle ScholarPubMed
Yager, D.D. (1999) Structure, development and evolution of insect auditory systems. Microscopy Research and Technique 47, 380–400.3.0.CO;2-P>CrossRefGoogle ScholarPubMed