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Zoomorphology

, Volume 126, Issue 4, pp 229–243 | Cite as

Comparison of auditory sense organs in parasitoid Tachinidae (Diptera) hosted by Tettigoniidae (Orthoptera) and homologous structures in a non-hearing Phoridae (Diptera)

  • Reinhard Lakes-Harlan
  • Kirsten Jacobs
  • Geoff R. Allen
Original Paper

Abstract

The dipteran parasitoids Therobia leonidei and Homotrixa alleni (Tachinidae) use acoustic cues to locate their calling tettigoniid (Ensifera, Orthoptera) hosts. The sexually dimorphic tympanal organs of both fly species are located at the prosternum. For comparison a homologous chordotonal organ in the non-hearing fly Phormia regina, Meigen (Phoridae) is also described. The scolopidial sense organs of the ears have approximately 180 sensory cells in Th. leonidei and 250 cells in H. alleni. Interspecific analysis indicates that the cell number and arrangement might be genus specific in Tachinidae. The mononematic scolopidia, each with one sensory cell, are of different sizes and insert at the tympanal membrane. Large scolopidial units (diameter of sensory cells up to 50 μm) extend longitudinally from the centre of the sensory organ towards the ligament, whereas small units (sensory cell diameter up to 10 μm) are arranged sequentially within the sensory organ. This arrangement is discussed to be a possible basis for frequency discrimination. The ultrastructure of the scolopidia is similar in the hearing and non-hearing flies. In both groups, the majority of scolopales has a diameter from 2 to 2.9 μm, although hearing species have additionally wider scolopales. The homologous chordotonal organ of Ph. regina consists of approximately 55 sensory cells of uniform direction. The data are discussed in comparison to the ears of other Diptera.

Keywords

Scolopidial organ Chordotonal organ Diptera Bush crickets Homotrixa alleni Therobia leonidei Phormiaregina 

Notes

Acknowledgments

We are grateful to Prof. Stumpner for valuable discussions and critical reading of the manuscript. We thank Prof. Ehlers for use of the scanning electron microscopy facility, and Prof. Schürmann for use of the transmission electron microscope facility at the University of Göttingen. The support of Prof. Elsner and the technical help of M. Winkler are greatly appreciated.

References

  1. Adamo SA, Robert D, Hoy RR (1995) Effects of a tachinid parasitoid, Ormia ochracea, on behaviour and reproduction of its male and female field cricket hosts (Gryllus spp). J Insect Physiol 41:269–277CrossRefGoogle Scholar
  2. Allen GR (1995a) The biology of the phonotactic parasitoid, Homotrixa sp. (Diptera: Tachinidae), and its impact on the survival of male Sciarasaga quadrata (Orthoptera: Tettigoniidae) in the field. Ecol Entomol 20:103–110Google Scholar
  3. Allen GR (1995b) The calling behaviour and spatial distribution of male bushcrickets (Sciarasaga quadrata) and their relationship to parasitism by acoustically orienting tachinid flies. Ecol Entomol 20:303–310Google Scholar
  4. Allen GR (2000) Call structure variability and field survival among bushcrickets exposed to phonotactic parasitoids. Ethology 106:409–423CrossRefGoogle Scholar
  5. 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 217:345–359PubMedCrossRefGoogle Scholar
  6. Barraclough DA, Allen GR (1996) Two species of Homotrixa Villeneuve (Diptera: Tachinidae: Ormiini) from Southwestern Australia, with data on biology and ecology. Aust J Entomol 35:135–145CrossRefGoogle Scholar
  7. Cade W (1975) Acoustically orienting parasitoids: fly phonotaxis to cricket song. Science 190:1312–1313Google Scholar
  8. Cade WH (1983) Effects of fly parasitoids on nightly calling duration in field crickets. Can J Zool 62:226–228CrossRefGoogle Scholar
  9. Edgecomb RS, Robert D, Read MP, Hoy RR (1995) The tympanal hearing organ of a fly: phylogenetic analysis of its morphological origin. Cell Tissue Res 282:251–268PubMedGoogle Scholar
  10. Field LH, Matheson T (1998) Chordotonal organs of insects. Adv Ins Physiol 27:1–228CrossRefGoogle Scholar
  11. Fonseca PJ, Münch D, Hennig RM (2000) How cicadas interpret acoustic signals. Nature 405:297–298PubMedCrossRefGoogle Scholar
  12. Fowler HG (1987) Field behavior of Euphasiopteryx depleta (Diptera: Tachinidae): phonotactically orienting parasitoids of mole crickets (Orthoptera: Gryllotalpidae: Scapteriscus). J N YEntomol Soc 95:474–480Google Scholar
  13. Fowler HG, Kochalka JN (1985) New record of Euphasiopteryx depleta (Diptera: Tachinidae) from Paraguay: attraction to broadcast calls of Scapteriscus acletus (Orthoptera: Gryllotalpidae). Fla Entomol 68:225–226CrossRefGoogle Scholar
  14. Fullard JH, Yack JE (1993) The evolutionary biology of insect hearing. Trends Ecol Evol 8:248–252CrossRefGoogle Scholar
  15. Füller H, Ernst A (1981) Die Ultrastruktur der femoralen Chordotonalorgane von Carausius morosus. Zool J Anat 91:574–601Google Scholar
  16. Ghiradella H (1971) Fine structure of the noctuid moth ear. I. The transducer area and connections to the tympanic membrane of Feltia subgothia Hawthorn. J Morphol 134:21–45PubMedCrossRefGoogle Scholar
  17. Gray EG (1960) The fine structure of the insect ear. Philos Trans R Soc Lond B 243:75–94CrossRefGoogle Scholar
  18. Hengstenberg R (1991) Gaze control in the blowfly Calliphora: a multisensory, two-stage integration process. Semin Neurosci 3:19–30CrossRefGoogle Scholar
  19. Hennig W (1974) Diptera. In: Helmcke J-G, Starck D, Wermuth H (eds) Handbuch der Zoologie. Walter de Gruyter, Berlin, 1–331Google Scholar
  20. Hertweck H (1931) Anatomie und Variabilität des Nervensystems und der Sinnesorgane von Drosophila melanogaster (Meigen). Z Wiss Zool 139:560–664Google Scholar
  21. Hoy RR, Robert D (1996) Tympanal hearing in insects. Annu Rev Entomol 41:433–450PubMedCrossRefGoogle Scholar
  22. Kalmring K, Rössler W, Ebendt R, Ahi J, Lakes R (1993) The auditory receptor organs in the forelegs of bushcrickets: physiology, receptor cells arrangement, and morphology of the tympanal and intermediate organs of three closely related species. Zool J Physiol 97:75–94Google Scholar
  23. Lakes R, Schikorski T (1990) Neuroanatomy of the Tettigoniids. In: Bailey WJ, Rentz DCF (eds) The Tettigoniidae: biology, systematics and evolution. Crawford House, Bathurst, pp 166–190Google Scholar
  24. Lakes-Harlan R, Heller K-G (1992) Ultrasound-sensitive ears in a parasitoid fly. Naturwissenschaften 79:224–226CrossRefGoogle Scholar
  25. Lakes-Harlan R, Stölting H, Stumpner A (1998) Phonotaxis of the parasitoid fly Colcondamyia auditrix (Sarcophagidae, Diptera). In: Elsner N, Wehner R (eds) Göttingen Neurobiology Report 1998. Thieme Verlag, Stuttgart, p 285Google Scholar
  26. Lakes-Harlan R, Stumpner A, Allen G (1995) Functional adaptations of the auditory system of two parasitoid fly species, Therobia leonidei and Homotrixa spec. In: Burrows M, Matheson T, Newland P, Schuppe H (eds) Nervous systems and behaviour. Thieme Verlag, Stuttgart, p 358Google Scholar
  27. Lakes-Harlan R, Stölting H, Stumpner A (1999) Convergent evolution of insect hearing organs from a preadaptive structure. Proc R Soc Lond B 266:1161–1167CrossRefGoogle Scholar
  28. Lehmann GUC (2003) Review of biogeography, host range and evolution of acoustic hunting in Ormiini (Insects, Diptera, Tachinidae), parasitoids of night-calling bushcrickets and crickets (Insecta, Orthoptera, Ensifera). Zool Anz 242:107–120CrossRefGoogle Scholar
  29. Lehmann GUC, Heller K-G (1998) Bushcricket song structure and predation by the acoustically orienting parasitoid fly Therobia leonidei (Diptera: Tachinidae: Ormiini). Behav Ecol Sociobiol 43:239–245CrossRefGoogle Scholar
  30. Leonide JC (1963) Sur l’acridiophagie des larves de Tachinaires. Comptes Rendus d’Acad Sci Paris 256:1591–1593Google Scholar
  31. Michel K (1974) Das Tympanalorgan von Gryllus bimaculatus De Geer (Saltatoria, Gryllidae). Z Morph Tiere 77:285–315CrossRefGoogle Scholar
  32. Oldfield B (1985) The tuning of auditory receptors in bushcrickets. Hearing Res 17:25–35CrossRefGoogle Scholar
  33. Oshinsky ML, Hoy RR (1995) Response properties of auditory afferents in the fly Ormia ochracea. In: Burrows M, Matheson T, Newland PL, Schuppe H (eds) Nervous systems and behaviour. Thieme Verlag, Stuttgart, p 369Google Scholar
  34. Oshinsky ML, Hoy RR (2002) Physiology of the auditory afferents in an acoustic parasitoid fly. J Neurosci 22:7254–7263PubMedGoogle Scholar
  35. Pflüger H-J, Field LH (1999) A locust chordotonal organ coding for proprioceptive and acoustic stimuli. J Comp Physiol A 184:169–183CrossRefGoogle Scholar
  36. Robert D, Willi D (2000) The histological architecture of the auditory organs in the parasitoid fly Ormia ochracea. Cell Tissue Res 301:447–457PubMedCrossRefGoogle Scholar
  37. Robert D, Amoroso J, Hoy RR (1992) The evolutionary convergence of hearing in a parasitoid fly and its cricket host. Science 258:1135–1137PubMedCrossRefGoogle Scholar
  38. Robert D, Read MP, Hoy RR (1994) The tympanal hearing organ of the parasitoid fly Ormia ochracea (Diptera, Tachinidae, Ormiini). Cell Tissue Res 275:63–78PubMedCrossRefGoogle Scholar
  39. Robert D, Edgecomb RS, Read MP, Hoy RR (1996) Tympanal hearing in tachinid flies (Diptera, Tachinidae, Ormiini): the comparative morphology of an innovation. Cell Tissue Res 284:435–448PubMedCrossRefGoogle Scholar
  40. Römer H, Bailey W (1998) Strategies for hearing in noise: peripheral control over auditory sensitivity in the bushcricket Sciarasaga quadrata (Austrosaginae: Tettigoniidae). J Exp Biol 201:1023–1033PubMedGoogle Scholar
  41. Shanbhag SR, Singh K, Singh RN (1992) Ultrastructure of the femoral chordotonal organs and their novel synaptic organization in the legs of Drosophila melanogaster Melgen (Diptera: Drosophilidae). Int J Insect Morphol Embryol 21:311–322CrossRefGoogle Scholar
  42. Stumpner A (1996) Tonotopic organization of the hearing organ in an bushcricket. Naturwissenschaften 83:81–84Google Scholar
  43. Stumpner A, Lakes-Harlan R (1996) Auditory interneurons in a hearing fly (Therobia leonidei, Ormiini, Tachinidae, Diptera). J Comp Physiol A 178:227–233CrossRefGoogle Scholar
  44. Stumpner A, Allen GR, Lakes-Harlan R (2006) Hearing and frequency dependence of auditory interneurons in the parasitoid fly Homotrixa alleni (Tachinidae: Ormiini). J Comp Physiol A 193:113–125CrossRefGoogle Scholar
  45. Walker TJ (1993) Phonotaxis in female Ormia ochracea (Diptera: Tachinidae), a parasitoid of field crickets. J Insect Behav 6:389–410CrossRefGoogle Scholar
  46. Walker TJ, Wineriter A (1991) Hosts of a phonotactic parasitoid and levels of parasitism (Diptera: Tachinidae: Ormia ochracea). Fla Entomol 74:554–559CrossRefGoogle Scholar
  47. Yager DD (1990) Sexual dimorphism of auditory function in praying mantis. J Morphol 221:517–537Google Scholar
  48. Yager DD (1999) Structure, development, and evolution of insect auditory systems. Microsc Res Tech 47:380–400PubMedCrossRefGoogle Scholar
  49. Young D, Ball E (1974) Structure and development of the auditory system in the prothoracic leg of the cricket Teleogryllus commodus (Walker). I. Adult structure. Z Zellforsch 147:293–312PubMedCrossRefGoogle Scholar
  50. Zuk M, Simmons LW, Cupp L (1993) Calling characteristics of parasitized and unparasitized populations of the field cricket Teleogryllus oceanicus. Behav Ecol Sociobiol 33:339–343Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Reinhard Lakes-Harlan
    • 1
  • Kirsten Jacobs
    • 2
  • Geoff R. Allen
    • 3
  1. 1.Institut für TierphysiologieUniversität GiessenGiessenGermany
  2. 2.Institut für Zoologie und Anthropologie, AG NeurobiologieGöttingenGermany
  3. 3.School of Agricultural Science/TIARUniversity of TasmaniaHobartAustralia

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