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Hearing and frequency dependence of auditory interneurons in the parasitoid fly Homotrixa alleni (Tachinidae: Ormiini)

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Abstract

The parasitoid tachinid fly Homotrixa alleni detects its hosts by their acoustic signals. The tympanal organ of the fly is located at the prothorax and contains scolopidial sensory units of different size and orientation. The tympanal membrane vibrates in the frequency range of approximately 4–35 kHz, which is also reflected in the hearing threshold measured at the neck connective. The auditory organ is not tuned to the peak frequency (5 kHz) of the main host, the bush cricket Sciarasaga quadrata. Auditory afferents project in the three thoracic neuromeres. Most of the ascending interneurons branch in all thoracic neuromeres and terminate in the deutocerebrum of the brain. The interneurons do not differ considerably in frequency tuning, but in their sensitivity with lowest thresholds around 30 dB SPL. Suprathreshold responses of most neurons depend on frequency and intensity, indicating inhibitory influence at higher intensities. Some neurons respond particularly well at low frequency sounds (around 5 kHz) and high intensities (80–90 dB SPL), and thus may be involved in detection of the primary host, S. quadrata. The auditory system of H. alleni contains auditory interneurons reacting in a wide range of temporal patterns from strictly phasic to tonic and with clear differences in frequency responses.

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References

  • Adam TJ, Finlayson PG, Schwarz DWF (2001) Membrane properties of principal neurons of the lateral superior olive. J Neurophysiol 86:922–934

    PubMed  CAS  Google Scholar 

  • Adamo SA, Robert D, Perez J, Hoy RR (1995) The response of an insect parasitoid, Ormia ochracea (Tachinidae), to the uncertainty of larval success during infestation. Behav Ecol Sociobiol 36:111–118

    Article  Google Scholar 

  • Allen GR (1995) The calling behaviour and spatial distribution of male bushcrickets (Sciarasaga quadrata) and their relationship to parasitism by acoustically orienting tachinid flies. Ecol Entomol 20:303–310

    Google Scholar 

  • Allen GR (2000) Call structure variability and field survival among bushcrickets exposed to phonotactic parasitoids. Ethology 106:409–423

    Article  Google Scholar 

  • Allen GR, Kamien D, Berry O, Byrne P, Hunt J (1999) Larviposition, host cues, and planidial behavior in the sound-locating parasitoid fly Homotrixa alleni (Diptera: Tachinidae). J Insect Behav 12:67–79

    Article  Google Scholar 

  • 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 35:135–145

    Article  Google Scholar 

  • Belshaw R (1993) Tachinid flies (Diptera: Tachinidae). Handbook for the identification of British insects 10, London, pp 169

  • Cade W (1975) Acoustically orienting parasitoids: fly phonotaxis to cricket song. Science 190:1312–1313

    Google Scholar 

  • Fullard JH, Yack JE (1993) The evolutionary biology of insect hearing. Trends Ecol Evol 8:248–252

    Article  Google Scholar 

  • Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans: common problems and divers solutions. Chicago University Press, Chicago

    Google Scholar 

  • Hedwig B, Knepper M (1992) NEUROLAB, a comprehensive program for the analysis of neurophysiological and behavioural data. J Neurosci Meth 45:135–148

    Article  CAS  Google Scholar 

  • Hennig RM (1988) Ascending auditory interneurons in the cricket Teleogryllus commodus (Walker): comparative physiology and direct connections with afferents. J Comp Physiol A 163:135–143

    Article  PubMed  CAS  Google Scholar 

  • Hoy RR, Robert D (1996) Tympanal hearing in insects. Annu Rev Entomol 41:433–450

    Article  PubMed  CAS  Google Scholar 

  • Köhler U, Lakes-Harlan R (2001) Auditory behaviour of a parasitoid fly (Emblemasoma auditrix, Sarcophagidae, Diptera). J Comp Physiol A 187:581–587

    Article  PubMed  Google Scholar 

  • Kössl M, Boyan GS (1998) Acoustic distortion products from the ear of a grasshopper. J Acoust Soc Am 104:326–335

    Article  Google Scholar 

  • Lakes R, Schikorski T (1990) Neuroanatomy of the Tettigoniids. In: Bailey WJ, Rentz DCF (eds) The Tettigoniidae: biology, systematics and evolution. Crawford House Press, Bathurst, pp 166–190

    Google Scholar 

  • Lakes-Harlan R, Heller K-G (1992) Ultrasound-sensitive ears in a parasitoid fly. Naturwissenschaften 79:224–226

    Article  Google Scholar 

  • 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) Thieme-Verlag, Stuttgart, 358

  • Lakes-Harlan R, Stölting H, Stumpner A (1999) Convergent evolution of insect hearing organs from a preadaptive structure. Proc R Soc London B 266:1161–1167

    Article  Google Scholar 

  • Lakes-Harlan R, Stölting H, Moore TE (2000) Phonotactic behavior of a parasitoid (Emblemasoma auditrix, Sarcophagidae, Diptera) in response to the calling song of the host (Okanagana rimosa, Cicada, Homoptera). Zoology 103:31–39

    Google Scholar 

  • Lang F, Brandt G, Glahe M (1993) A versatile multichannel acoustic stimulator controlled by a personal computer. In: Elsner N, Heisenberg M (eds) Gene-Brain–Behaviour. Thieme-Verlag, Stuttgart, pp 892

    Google Scholar 

  • 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 242:107–120

    Article  Google Scholar 

  • Lehmann GUC, Heller KG (1998) Bushcricket song structure and predation by the acoustically-orienting parasitoid fly Therobia leonidei (Diptera: Tachinidae: Ormiini). Behav Ecol Sociobiol 43:239–245

    Article  Google Scholar 

  • Manley GA (2000) Cochlear mechanisms from a phylogenetic viewpoint. Proc Natl Acad Sci USA 97:11736–11743

    Article  PubMed  CAS  Google Scholar 

  • Marsh RA, Nataraj K, Gans D, Portfors CV, Wenstrup JJ (2006) Auditory responses in the cochlear nucleus of awake mustached bats: precursors to spectral integration in the auditory midbrain. J Neurophysiol 95:88–105

    Article  PubMed  Google Scholar 

  • Meyer J, Elsner N (1996) How well are frequency sensitivities of grasshopper ears tuned to species-specific song spectra? J Exp Biol 199:1631–1642

    PubMed  Google Scholar 

  • Milde JJ, Strausfeld NJ (1988) Cluster organization and response characteristics of the giant fiber pathway of the blowfly, Calliphora erythrocephala. J Comp Neurol 294:59–75

    Article  Google Scholar 

  • Mücke A, Lakes-Harlan R (1995) Central projections of sensory cells of the midleg of the locust, Schistocerca gregaria. Cell Tiss Res 280:391–400

    Google Scholar 

  • Müller P, Robert D (2001) A shot in the dark: the silent quest of a free-flying phonotactic fly. J Exp Biol 204:1039–1052

    PubMed  Google Scholar 

  • Oldfield B (1985) The tuning of auditory receptors in bushcrickets. Hearing Res 17:25–35

    Article  Google Scholar 

  • Oshinsky ML, Hoy RR (2002) Physiology of the auditory afferents in an acoustic parasitoid fly. J Neurosci 22:7254–7263

    PubMed  CAS  Google Scholar 

  • Pfeiffer RR (1966) Classification of response patterns of spike discharges for units in the cochlear nucleus: tone-burst stimulation. Exp Brain Res 1:220–235

    Article  PubMed  CAS  Google Scholar 

  • Robert D, Willi D (2000) The histological architecture of the auditory organs in the parasitoid fly Ormia ochracea. Cell Tiss Res 301:447–457

    Article  CAS  Google Scholar 

  • Robert D, Amoroso J, Hoy RR (1992) The evolutionary convergence of hearing in a parasitoid fly and its cricket host. Science 258:1135–1137

    Article  PubMed  CAS  Google Scholar 

  • Robert D, Miles RN, Hoy RR (1999) Tympanal hearing in the sarcophagid parasitoid fly Emblemasoma sp.: the biomechanics of directional hearing. J Exp Biol 202:1865–1876

    PubMed  CAS  Google Scholar 

  • Römer H (1987) Representation of auditory distance within a central neuropil of the bushcricket Mygalopsis marki. J Comp Physiol A 161:33–42

    Article  Google Scholar 

  • Römer H, Marquart V (1984) Morphology and physiology of auditory interneurons in the metathoracic ganglion of the locust. J Comp Physiol A 155:249–262

    Article  Google Scholar 

  • Römer H, Marquart V, Hardt M (1988) Organisation of a sensory neuropile in the auditory pathway of two groups of orthopterans. J Comp Neurol 275:201–215

    Article  PubMed  Google Scholar 

  • 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 201:1023–1033

    PubMed  Google Scholar 

  • Sandow JD (1980) The morphology, distribution and acoustic repertoire of the genus Mygalopsis (Orthoptera, Tettigoniidae). Master-Thesis: University of Western Australia, Nedlands

  • Schäffer S, Lakes-Harlan R (2001) Embryonic development of the central projection of auditory afferents (Schistocerca gregaria, Orthoptera, Insecta). J Neurobiol 46:97–112

    Article  PubMed  Google Scholar 

  • Schildberger K (1984) Temporal selectivity of identified auditory neurons in the cricket brain. J Comp Physiol A 155:171–185

    Article  Google Scholar 

  • Schildberger K, Huber F, Wohlers DW (1989) Central auditory pathway: neuronal correlates of phonotactic behavior. In: Huber F, Moore TE, Loher W (eds) Cricket behaviour and neurobiology. Cornell University Press, Ithaca, pp 423–458

    Google Scholar 

  • Schul J (1997) Neuronal basis of phonotactic behaviour in Tettigonia viridissima: processing of behaviourally relevant signals by auditory afferents and thoracic interneurons. J Comp Physiol A 180:573–583

    Article  Google Scholar 

  • Strausfeld NJ, Obermayer M (1980) Resolution of intraneuronal and transsynaptic migration of cobalt in the insect visual and central nervous system. J Comp Physiol 110:1–12

    Google Scholar 

  • Stumpner A (1999) An interneurone of unusual morphology is tuned to the female song frequency in the bushcricket Ancistrura nigrovittata (Orthoptera, Phaneropteridae). J Exp Biol 202:2071–2081

    PubMed  CAS  Google Scholar 

  • Stumpner A, Ronacher B (1991) Auditory interneurons in the metathoracic ganglion of the grasshopper Chorthippus biguttulus. I. Morphological and physiological characterization. J Exp Biol 158:391–410

    Google Scholar 

  • Stumpner A, Lakes-Harlan R (1996) Auditory interneurons in a hearing fly (Therobia leonidei, Ormiini, Tachinidae, Diptera). J Comp Physiol A 178:227–233

    Article  Google Scholar 

  • Stumpner A, von Helversen D (2001) Evolution and function of auditory system in insects. Naturwissenschaften 88:159–170

    Article  PubMed  CAS  Google Scholar 

  • deVries T, Stölting H, Stumpner A, Lakes-Harlan R (2003) Is the auditory sense of male Emblemasoma auditrix (Diptera) useless? In: Elsner N, Zimmermann H (eds) The neurosciences from basic research to therapy. Thieme-Verlag, Stuttgart, pp 409–410

    Google Scholar 

  • Walker TJ (1993) Phonotaxis in female Ormia ochracea (Diptera: Tachinidae), a parasitoid of field crickets. J Insect Behav 6:389–410

    Article  Google Scholar 

  • Walker TJ, Wineriter A (1991) Hosts of a phonotactic parasitoid and levels of parasitism (Diptera: Tachinidae: Ormia ochracea). Fla Ent 74:554–559

    Article  Google Scholar 

  • Yager DD (1999) Structure, development, and evolution of insect auditory systems. Microsc Res Tech 47:380–400

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

AS and RLH were supported by the Deutsche Forschungsgemeinschaft. GRA was supported by an ARC grant from the Australian Research Council. We want to thank two anonymous referees for many helpful comments. The experiments comply with the “Principles of animal care”, publication No. 86–23, revised 1985 of the National Institute of Health, and with the current laws in Germany.

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  1. Geoff R. Allen

    Present address: School of Agricultural Science/TIAR, University of Tasmania, Private Bag 54, Hobart, TAS, 7001, Australia

  2. Reinhard Lakes-Harlan

    Present address: Institut für Tierphysiologie, AG Integrative Sinnesphysiologie, Justus-Liebig Universität Giessen, Wartweg 92, 35392, Giessen, Germany

Authors and Affiliations

  1. Johann-Friedrich-Blumenbach-Institut für Zoologie und Anthropologie, Abt. Neurobiologie, Georg-August Universität Göttingen, Berliner Str. 28, 37073, Göttingen, Germany

    Andreas Stumpner, Geoff R. Allen & Reinhard Lakes-Harlan

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Correspondence to Reinhard Lakes-Harlan.

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Stumpner, A., Allen, G.R. & Lakes-Harlan, R. Hearing and frequency dependence of auditory interneurons in the parasitoid fly Homotrixa alleni (Tachinidae: Ormiini). J Comp Physiol A 193, 113–125 (2007). https://doi.org/10.1007/s00359-006-0174-x

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