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Journal of Comparative Physiology A

, Volume 179, Issue 1, pp 29–44 | Cite as

Directional hearing by mechanical coupling in the parasitoid fly Ormia ochracea

  • D. Robert
  • R. N. Miles
  • R. R. Hoy
Original Papers

Abstract

Sound localization is a basic processing task of the auditory system. The directional detection of an incident sound impinging on the ears relies on two acoustic cues: interaural amplitude and interaural time differences. In small animals, with short interaural distances both amplitude and time cues can become very small, challenging the directional sensitivity of the auditory system. The ears of a parasitoid fly Ormia ochracea, are unusual in that both acoustic sensors are separated by only 520 μm and are contained within an undivided air-filled chamber. This anatomy results in minuscule differences in interaural time cues (ca. 2 μs) and no measurable difference in interaural intensity cues generated from an incident sound wave.

The tympana of both ears are anatomically coupled by a cuticular bridge. This bridge also mechanically couples the tympanana, providing a basis for directional sensitivity. Using laser vibrometry, it is shown that the mechanical response of the tympanal membranes has a pronounced directional sensitivity. Interaural time and intensity differences in the mechanical response of the ears are significantly larger than those available in the acoustic field. The tympanal membranes vibrate with amplitude differences of about 12 dB and time differences on the order of 50 μs to sounds at 90° off the longitudinal body axis. The analysis of the deflection shapes of the tympanal vibrations shows that the interaural differences in the mechanical response are due to the dynamic properties of the tympanal system and reflect its intrinsic sensitivity to the direction of a sound source. Using probe microphones and extracellular recording techniques, we show that the primary auditory afferents encode sound direction with a time delay of about 300 μs. Our data point to a novel mechanism for directional hearing in O. ochracea based on intertympanal mechanical coupling, a process that amplifies small acoustic cues into interaural time and amplitude differences that can be reliably processed at the neural level. An intuitive description of the mechanism is proposed using a simple mechanical model in which the ears are coupled through a flexible lever.

Key words

Insect bioacoustics Sound localization Tympanal ear Laser vibrometry Ormia ochracea 

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References

  1. Bennet-Clark HC (1984) Insect hearing: Acoustics and transduction. In: Lewis T (ed) Insect communication. Academic Press, LondonGoogle Scholar
  2. Cade WH (1975) Acoustically orienting parasitoid: fly phonotaxis to cricket song. Science 190: 1312–1313Google Scholar
  3. Calford MB, Piddington RW (1988) Avian interaural canal enhances interaural delay. J Comp Physiol A 162: 503–510Google Scholar
  4. Coles RB, Guppy A (1988) Directional hearing in the barn owl (Tyto alba). J Comp Physiol A 163: 117–133Google Scholar
  5. Coles RB, Gower DM, Boyd PJ, Lewis DB (1982) Acoustic transmission through the head of the common mole, Talpa europaea. J Exp Biol 101: 337–341Google Scholar
  6. Edgecomb RS, Robert D, Read M, Hoy RR (1995) The tympanal hearing organ of a fly: phylogenetic analysis of its morphological origins. Cell Tissue Res 282: 251–268Google Scholar
  7. Eggermont JJ (1988) Mechanisms of sound localization in anurans. In: Fritzsch B, Ryan MJ, Wilczynski W, Hetherington TE, Walkowiak W (eds) The evolution of the amphibian auditory system. John Wiley, New York Chichester Brisbane Toronto Singapore, pp 307–336Google Scholar
  8. Fletcher NH (1992) Acoustic systems in biology. Oxford University PressGoogle Scholar
  9. Fonseca P (1993) Directional hearing of a cicada: biophyical aspects. J Comp Physiol A 172: 767–774Google Scholar
  10. Henson OW (1974) Comparative anatomy of the middle ear. In: Keidel WD, Neff WD (eds) Handbook of sensory physiology, vol V/1. Springer, Berlin Heidelberg New York, pp 39–110Google Scholar
  11. Hill KG, Boyan GS (1977) Sensitivity to frequency and direction of sound in the auditory system of crickets. J Comp Physiol 121: 79–97Google Scholar
  12. Hill KG, Lewis DB, Hutchings ME, Coles RB (1980) Directional hearing in the Japanese quail (Coturnix coturnix japonica) I. Acoustic properties of the auditory system. J Exp Biol 86: 135–151Google Scholar
  13. Hoy RR, Robert D (1996) Tympanal hearing in insects. Ann Rev Entomol 41: 433–450Google Scholar
  14. Knudsen EI (1980) Sound localization in birds. In: Popper AN, Fay RR (eds) Comparative studies of hearing in vertebrates. Springer, Berlin Heidelberg New York, pp 289–322Google Scholar
  15. Lakes-Harlan R, Heller K-G (1992) Ultrasound sensitive ears in a parasitoid fly. Naturwissenschaften 79: 224–226Google Scholar
  16. Löhe G, Kleindienst HU (1994) The role of the medial septum in the acoustic trachea of the cricket Gryllus bimaculatus. II. Influence on directionality of the auditory system. J. Comp Physiol A 174: 601–606Google Scholar
  17. Michel K (1974) Das Tympanalorgan von Gryllus bimaculatus Degeer (Saltatoria: Gryllidae). Z Morph Tiere 77: 285–315Google Scholar
  18. Michel K (1975) Das tympanalorgan von Cicada omi (Cicadina, Homoptera). Zoomorphologie 82: 63–78Google Scholar
  19. Michelsen A (1994) Directional hearing in crickets and other small animals. In: Schildberger K, Elsner N (eds) Fortschritte der Zoologie, vol 39: Neural basis of behavioural adaptations. Fischer, Stuttgart, pp 195–207Google Scholar
  20. Michelsen A, Larsen ON (1985) Hearing and sound. In: Kerkut G, Gilbert L (eds) Comprehensive insect physiology, biochemistry, and pharmacology, vol 6. Pergamon, New York, pp 495–556Google Scholar
  21. Michelsen A, Popov AV, Lewis B (1994) Physics of directional hearing in the cricket Gryllus bimaculatus. J Comp Physiol A 175: 153–164Google Scholar
  22. Middlebrooks JC, Green DM (1991) Sound localization by human listeners. Annu Rev Psychol 42: 135–159Google Scholar
  23. Middlebrooks JC, Makous JC, Green DM (1989) Directional sensitivity of sound pressure levels in the human ear canal. J Acoust Soc Am 86: 89–108Google Scholar
  24. Miles RN, Robert D, Hoy RR (1995) Mechanically coupled ears for directional hearing in the parasitoid fly O. ochracea. J Acoust Soc Am 98(6): 3059–3070Google Scholar
  25. Moiseff A, Konishi M (1981) Neuronal and behavioral sensitivity to binaural time differences in the owl. J Neurosci 1: 40–48Google Scholar
  26. Mörchen A, Rheinländer J, Schwartzkopff J (1978) Latency shift in insect auditory fibers. Naturwissenschaften 65: 657Google Scholar
  27. Morse PM, Ingard KU (1968) Theoretical acoustics. McGraw Hill, New York, pp 418–422Google Scholar
  28. Narins PM, Ehret G, Tautz J (1988) Accessory pathway for sound transfer in a neotropical frog. Proc Natl Acad Sci USA 85: 1508–1512Google Scholar
  29. Oshinsky ML, Hoy RR (1995) Response properties of auditory afferents in the fly O. ochracea. In: Burrows M, Matheson T, Newland PL, Schuppe H (eds) Nervous systems and behaviour. Thieme, Stuttgart New York, p 359Google Scholar
  30. Rayleigh Lord (1907) On our perception of sound direction. Philos Mag 13: 214–232Google Scholar
  31. Robert D (1989) The auditory behaviour of flying locusts. J Exp Biol 147: 279–301Google Scholar
  32. Robert D, Amoroso J, Hoy RR (1992) The evolutionary convergence of hearing in a parasitoid fly and its cricket host. Science 258: 1135–1137Google Scholar
  33. Robert D, Read MP, Hoy RR (1994a) The tympanal hearing organ of the parasitoid fly Ormia ochracea (Diptera, Tachinidae, Ormiini). Cell Tissue Res 275: 63–78Google Scholar
  34. Robert D, Miles RN, Hoy RR (1994b) A novel mechanism for directional hearing in a parasitoid fly. J Acoust Soc Am 96: 3296Google Scholar
  35. Schlegel PA (1994) Azimuth estimates by human subjects under free-field and headphone conditions. Audiology 33: 93–116Google Scholar
  36. Walker TJ (1986) Monitoring the flights of the field crickets (Gryllus spp.) and a tachinid fly (Euphasiopterix ochracea) in north Florida. Florida Entomol 69: 678–685Google Scholar
  37. Walker TJ, Wineriter SA (1991) Hosts of a phonotactic parasitoid and levels of parasitism (Diptera: Tachinidae: Ormia ochracea). Fla Entomol 74: 554–559Google Scholar
  38. Wendler G, Löhe G (1993) The role of the median septum in the acoustic trachea of the cricket Gryllus bimaculatus. I. Importance for efficient phonotaxis. J Comp Physiol A 173: 557–564Google Scholar
  39. Wineriter SA, Walker TJ (1990) Rearing parasitoid flies (Diptera: Tachinidae Ormiini, Ormia spp.) Entomophaga 35: 621–632Google Scholar
  40. Young D, Hill KG (1977) Structure and function of the auditory system of the cicada, Cystosoma saundersii. J Comp Physiol 117: 23–45Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • D. Robert
    • 1
  • R. N. Miles
    • 2
  • R. R. Hoy
    • 1
  1. 1.Section of Neurobiology and Behavior, S.G. Mudd HallCornell UniversityIthacaUSA
  2. 2.Department of Mechanical EngineeringState University of New YorkBinghamtonUSA

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