Skip to main content
SpringerLink
Log in

Auditory Parasitoid Flies Exploiting Acoustic Communication of Insects

  • Chapter
  • First Online:
Insect Hearing and Acoustic Communication

Part of the book series: Animal Signals and Communication ((ANISIGCOM,volume 1))

Abstract

Hearing evolved in flies of both Dipteran families Tachinidae and Sarcophagidae, enabling the parasitic exploitation of singing orthoptera and hemiptera. Guided by acoustic communication signals, these flies identify and localise their singing target, depositing their larvae on or near the host. Larvae then develop as endoparasites, eventually killing the host. In these flies, the mechanosensory auditory organ is located on the prosternum and in most cases is less than one millimetre in size. The frontal facing tympana constitute an extreme example of adaptation in auditory micromechanics. Directional hearing relies on the mechanical coupling between the hemilateral tympana, a purely mechanical process that exploits minute interaural time differences in tympanic vibrations and enhances bilateral oscillation differences to generate a highly directional sensitivity. In tachinid fly species, the frequency response of the ears is adapted to the host communication signals. The auditory organs contain up to 250 scolopidial afferents, which are directly driven by tympanic membrane vibrations. The signals from the auditory afferents are forwarded to auditory neuropils in the three thoracic neuromeres. Further processing of intensity and directional information and also of temporal patterns involves local and also ascending auditory interneurons, which project up to the brain for final sensory-motor integration.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adamo SA, Robert D, Hoy RR (1995a) Effects of a tachinid parasitoid, O. ochracea, on the behaviour and reproduction of its male and female field cricket hosts (Gryllus spp). J Insect Physiol 41:269–277

    Article  CAS  Google Scholar 

  • Adamo SA, Robert D, Perez J, Hoy RR (1995b) 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 (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 new species of Homotrixa Villeneuve (Diptera: Tachinidae: Ormiini) from Southwestern Australia, with data on biology and ecology. Aus J Entomol 35:135–145

    Article  Google Scholar 

  • Bernal XA, Rand S, Ryan MJ (2006) Acoustic preferences and localization performance of blood-sucking flies (Corethrella, Coquillett) to túngara frog calls. Behav Ecol 17:709–715

    Article  Google Scholar 

  • Borkent A, Belton P (2006) Attraction of female Uranotaenia lowii (Diptera: Culicidae) to frog calls in Costa Rica. Can. Entomol. 138:91–94

    Article  Google Scholar 

  • Burk T (1982) Evolutionary significance of predation on sexually signalling males. Fla Entomol 65:90–104

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Dambach M, Rausche G (1985) Low-frequency airborne vibrations in crickets and feed-back control of calling song. In: Kalmring and Elsner (eds) Acoustic and vibrational communication in insects. Parey Verlag Berlin, pp 177–182

    Google Scholar 

  • Dangles O, Ory N, Steinmann T, Christides JP, Casas J (2006) Spider’s attack versus cricket’s escape: velocity modes determine success. Anim Behav 72(3):603–610

    Article  Google Scholar 

  • Edgecomb RS, Robert D, Read MP, Hoy RR (1995) The tympanal hearing organ of a fly: phylogenetic analysis of its morphological origins. Cell Tiss Res 282:251–268

    Article  CAS  Google Scholar 

  • Farris HE, Oshinsky ML, Forrest TG, Hoy RR (2008) Auditory Sensitivity of an acoustic parasitoid (Emblemasoma sp., Sarcophagidae, Diptera) and the calling behavior of potential hosts. Brain Behav Evol 72:16–26

    Article  CAS  PubMed  Google Scholar 

  • Fowler HG (1987) Field confirmation of the phonotaxis of Euphasiopteryx depleta (Diptera: Tachinidae) to calling males of Scapteriscus vicinus (Orthoptera: Gryllotalpidae). Fla Entomol 70:409–410

    Article  Google Scholar 

  • 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 68:225–226

    Article  Google Scholar 

  • Fry SN, Bichsel M, Müller P, Robert D (2000) Three-dimensional tracking of flying insects using pan-tilt cameras. J Neurosci Methodol 101:59–67

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gnatzy W, Heusslein R (1986) Digger wasp against crickets. Naturwissenschaften 73:212–215

    Article  Google Scholar 

  • Gray DA, Banuelos C, Walker SE, Cade WH, Zuk M (2007) Behavioural specialization among populations of the acoustically orienting parasitoid fly Ormia ochracea utilizing different cricket species as hosts. Anim Behav 73:99–104

    Article  Google Scholar 

  • Hedwig, B Pollack GS (2008) Invertebrate auditory pathways. In: AI Basbaum, Kaneko A, GM Shepherd and G Westheimer editors: The Senses: A Comprehensive Reference, Vol. 3; Audition, P. Dallas and D. Oertel, San Diego Academic Press, pp 525–564

    Google Scholar 

  • Hennig R, Franz A, Stumpner A (2004) Processing of auditory information in insects. Micros Res Tech 63(6):351–374

    Article  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 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lakes-Harlan R, Jacobs K, Allen GR (2007) Comparison of auditory sense organs in parasitoid Tachinidae (Diptera) hosted by Tettigoniidae (Orthoptera) and homologous structures in a non-hearing Phoridae (Diptera). Zoomorphology 126:229–243

    Article  Google Scholar 

  • Lehmann GUC (2003) Review of biogeography, host range and evolution of acoustic hunting in Ormiini (Insecta, 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(4):239–245

    Article  Google Scholar 

  • Lehmann GUC, Heller K-G, Lehmann AW (2001) Male bushcrickets favoured by parasitoid flies when acoustically more attractive for conspecific females (Orthoptera: Phaneropteridae/Diptera: Tachinidae). Entomol Gen 25:135–140

    Google Scholar 

  • Léonide JC (1969) Recherches sur la biologie de divers diptères endoparasites d’Orthoptères. Memoires du Museum National d’histoire Naturelle serie A, Zoologie 53:1–246

    Google Scholar 

  • Mason AC, Oshinsky ML, Hoy RR (2001) Hyperacute directional hearing in a microscale auditory system. Nature 410:686–690

    Article  CAS  PubMed  Google Scholar 

  • Miles R, Robert D, Hoy R, (1995) Mechanically coupled ears for directional hearing in the parasitoid fly Ormia ochracea. J Acoust Soc Am 98(6):3059–3070

    Google Scholar 

  • Miles RN, Hoy RR (2006) The development of a biologically-inspired directional microphone for hearing aids. Audiology and Neurootology 11(2):86–94

    Article  CAS  Google Scholar 

  • Miles RN, Su QT, Cui W, Shetye M, Degertekin FL, Bicen B, Garcia C, Jones SA, Hall NA (2009) A low-noise differential microphone inspired by the ears of the parasitoid fly Ormia ochracea. J Acoust Soc Am 125:2013–2026

    Article  CAS  PubMed  Google Scholar 

  • Montealegre-Z F, Jonsson T, Robson-Brown K, Postles M, Robert D (2012) Convergent evolution between mammalian and insect audition. Science 338:968–971

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Müller P, Robert D (2002) Death comes suddenly to the unprepared: singing crickets, call fragmentation, and parasitoid flies. Behav Ecol 13:598–606

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Ramsauer N, Robert D (2000) Phonotactic orientation in a parasitoid fly. Naturwissenschaften 87:315–319

    Article  CAS  PubMed  Google Scholar 

  • Robert D (2001) Innovative biomechanics for directional hearing in small flies. Biol Bull 200:190–194

    Article  CAS  PubMed  Google Scholar 

  • Robert D (2005) Directional hearing in insects. In: Popper AN, Fay RR: Sound source localization. Springer Handbook of Auditory Research, pp 6–35

    Google Scholar 

  • Robert D (2008). Sound localization in insects. In: Basbaum AL, Kaneko A, Shepherd GM and Westheimer G: The senses: a comprehensive reference, vol 3. Audition P Dallos and D Oertel. San Diego, Academic Press, pp 725–732

    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  CAS  PubMed  Google Scholar 

  • Robert D, Göpfert MC (2002) Novel schemes for hearing and acoustic orientation in insects. Curr Opin Neurobiol 12:715–720

    Article  CAS  PubMed  Google Scholar 

  • Robert D, Read M, Hoy RR (1994) The tympanal hearing organ of the parasitoid fly Ormia ochracea (Diptera, Tachinidae, Ormiini). Cell Tiss Res 275:63–78

    Article  CAS  Google Scholar 

  • Robert D, Miles RN, Hoy RR (1996) Directional hearing by mechanical coupling in the parasitoid fly Ormia ochracea. J Comp Physiol A 179:29–44

    Article  CAS  PubMed  Google Scholar 

  • Robert D, Hoy RR (2007) Auditory systems in insects. Invertebrate Neurobiology. Eds. R. Greenspan, G. North. Cold Spring Harbour Laboratory Press., In, pp 155–184

    Google Scholar 

  • Robert D, Miles R, Hoy RR (1998) Tympanal mechanics in the parasitoid fly Ormia ochracea: intertympanal coupling during mechanical vibration. J Comp Physiol A 183:443–452

    Article  Google Scholar 

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

    CAS  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). JEB 201:1023–1033

    Google Scholar 

  • Römer H, Spickermann M, Bailey W (1998) Sensory basis for sound intensity discrimination in the bushcricket Requena verticalis (Tettigoniidae, Orthoptera). J Comp Physiol A 182:595–607

    Article  Google Scholar 

  • SchniederkÓ§tter K, Lakes-Harlan R (2004) Infection behavior of a parasitoid fly, Emblemasoma auditrix, and its host cicada Okanagana rimosa. J Ins Sci 4(36):1–7

    Google Scholar 

  • Shewell GE (1987) Sarcophagidae. In: Manual of nearctic diptera. Research Branch Agriculture Canada. Monogr 28, vol 2, pp 1159–1186

    Google Scholar 

  • Soper R, Shewell G, 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). The Can Entomol 108:61–68

    Article  Google Scholar 

  • Stölting H, Stumpner A, Lakes-Harlan R (2007) Morphology and physiology of the prosternal chordotonal organ of the sarcophagid fly Sarcophaga bullata (Parker). J Insect Physiol 53:444–454

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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, Allen GR, Lakes-Harlan R (2007) Hearing and frequency dependence of auditory interneurons in the parasitoid fly Homotrixa alleni (Tachinidae: Ormiini). J Comp Physiol A 193:113–125

    Article  Google Scholar 

  • Tinghitella RM, Wang JM, Zuk M (2009) Preexisting behavior renders a mutation adaptive: flexibility in male phonotaxis behavior and the loss of singing ability in the field cricket. Behav Ecol 20:722–728

    Article  Google Scholar 

  • Tuck EJ, Windmill JFC and D. Robert D (2009) Hearing in tsetse flies? Morphology and mechanics of a putative auditory organ. Bull Entomol Res 99: 107–119

    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 SA (1991) Hosts of a phonotactic parasitoid and levels of parasitism (Diptera: Tachinidae: Ormia ochracea). Fla Entomol 74:554–559

    Article  Google Scholar 

  • Wineriter SA, Walker TJ (1990) Rearing phonotactic parasitoid flies (Diptera: Tachinidae), Ormiini, Ormia spp.). Entomophaga 35:621–632

    Article  Google Scholar 

  • Yager DD (1999) Structure, development, and evolution of insect auditory systems. Microsc Res Tech 47(6):380–400

    Google Scholar 

  • Zuk M, Simmons LW, Cupp L (1993) Calling characteristics of parasitized and unparasitized populations of the field cricket Teleogryllus oceanicus. Behav Ecol Sociobiol 33:339–343

    Google Scholar 

  • Zuk M, Rotenberry JT, Tinghitella RM (2006) Silent night: adaptive disappearance of a sexual signal in a parasitized population of field crickets. Biol Letts 2:521–524

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, Cambridge, UK

    Berthold Hedwig

  2. School of Biological Sciences, Bristol, UK

    Daniel Robert

Authors
  1. Berthold Hedwig
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel Robert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Berthold Hedwig .

Editor information

Editors and Affiliations

  1. Department of Zoology, University of Cambridge, Cambridge, United Kingdom

    Berthold Hedwig

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Hedwig, B., Robert, D. (2014). Auditory Parasitoid Flies Exploiting Acoustic Communication of Insects. In: Hedwig, B. (eds) Insect Hearing and Acoustic Communication. Animal Signals and Communication, vol 1. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-40462-7_4

Download citation

Publish with us

Policies and ethics

Search

Navigation