Skip to main content
SpringerLink
Log in

Parasitoid flies exploiting acoustic communication of insects—comparative aspects of independent functional adaptations

  • Review
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Two taxa of parasitoid Diptera have independently evolved tympanal hearing organs to locate sound producing host insects. Here we review and compare functional adaptations in both groups of parasitoids, Ormiini and Emblemasomatini. Tympanal organs in both groups originate from a common precursor organ and are somewhat similar in morphology and physiology. In terms of functional adaptations, the hearing thresholds are largely adapted to the frequency spectra of the calling song of the hosts. The large host ranges of some parasitoids indicate that their neuronal filter for the temporal patterns of the calling songs are broader than those found in intraspecific communication. For host localization the night active Ormia ochracea and the day active E. auditrix are able to locate a sound source precisely in space. For phonotaxis flight and walking phases are used, whereby O. ochracea approaches hosts during flight while E. auditrix employs intermediate landings and re-orientation, apparently separating azimuthal and vertical angles. The consequences of the parasitoid pressure are discussed for signal evolution and intraspecific communication of the host species. This natural selection pressure might have led to different avoidance strategies in the hosts: silent males in crickets, shorter signals in tettigoniids and fluctuating population abundances in cicadas.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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, Hunt J (2001) Larval competition, adult fitness and reproductive strategies in the acoustically-orienting ormiine Homotrixa alleni (Diptera: Tachinidae). J Ins Behav 14:283–297

    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 Ins Behav 12:67–79

    Article  Google Scholar 

  • Arthur B, Hoy R (2006) The ability of the parasitoid fly Ormia ochracea to distinguish sounds in the vertical plane. J Acoust Soc Am 120:1546–1549

    Article  PubMed  Google Scholar 

  • Bailey WJ (1991) Acoustic behaviour of insects. An evolutionary perspective. Chapman and Hall, London

    Google Scholar 

  • Bailey WJ (1998) Do large bushcrickets have more sensitive ears? Natural variation in hearing thresholds within populations of the bushcricket Requena verticalis (Listroscelidinae: Tettigoniidae). Physiol Entomol 23:105–112

    Article  Google Scholar 

  • Bailey N, Zuk M (2008) Acoustic experience shapes female mate choice in field crickets. Proc Roy Soc Biol Sci 275:2645–2650

    Article  Google Scholar 

  • Boulard M (2006) Acoustic signals, diversity and behaviour of cicadas (Cicadidae, Hemiptera). In: Drosopoulos S, Claridge MF (eds) Insect sound and communication. CRC Press, Boca Raton, pp 331–349

    Google Scholar 

  • deVries T, Lakes-Harlan R (2005) Phonotaxis of Emblemasoma auditrix (Sarcophagidae, Diptera) in relation to number of larvae and age. Zoology 108:239–246

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Farris HE, Oshinsky ML, Forrest TG, Hoy R (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 Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Godfray H (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, New Jersey

    Google Scholar 

  • Goles E, Schulz O, Markus M (2001) Prime number selection of cycles in a predator-prey model. Complexity 6:33–38

    Article  Google Scholar 

  • Gray DA, Banuelos C, Walker SS, 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 

  • Greenfield M (2002) Signallers and receivers: mechanisms and evolution of arthropod communication. Oxford University Press, Oxford

    Google Scholar 

  • Gwynne D, Bailey WJ (1999) Female–female competition on katydids: sexual selection for increased sensitivity to a male signal? Evolution 53:546–551

    Article  Google Scholar 

  • Hedwig B, Robert D (2014) Auditory parasitoid flies exploiting acoustic commuincation of insects. In: Hedwig B (ed) Insect hearing and acoustic communication. Animal signals and communication. Springer, New York, pp 45–65

    Chapter  Google Scholar 

  • Heller K-G (1988) Bioakustik der europäischen Laubheuschrecken. Margraf Verlag, Weikersheim

    Google Scholar 

  • Heller K-G, Von Helversen O (1993) Calling behavior in bushcrickets of the genus Poecilimon with differing communication systems (Orthoptera: Tettigonioidea, Phaneropteridae). J Ins Behav 6:361–377

    Article  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 K-G (1992) Ultrasound-sensitive ears in a parasitoid fly. Naturwissenschaften 79:224–226

    Article  Google Scholar 

  • Lakes-Harlan R, Köhler U (2003) Influence of habitat structure on phonotactic strategy of a parasitoid fly (Emblemasoma auditrix, Sarcophagidae, Diptera). Ecol Entomol 28:758–765

    Article  Google Scholar 

  • Lakes-Harlan R, Stölting H, Stumpner A (1999) Convergent evolution of insect hearing organs from a preadaptive structure. Proc Roy Soc Biol Sci 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 

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

    Article  Google Scholar 

  • Lakes-Harlan R, deVries T, Stölting H, Stumpner A (2014) Useless hearing in male Emblemasoma auditrix (Diptera, Sarcophagidae)–A case of intralocus sexual conflict during evolution of a complex sense organ? PLoS ONE 9:e87211

    Article  PubMed Central  PubMed  Google Scholar 

  • Lee N, Elias DO, Mason AC (2009) A precedence effect resolves phantom sound source illusions in the parasitoid fly Ormia ochracea. Proc Nat Acad Sci USA 106:6357–6362

    Article  CAS  PubMed Central  PubMed  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 (2008) How different host species influence parasitism pattern and larval competition of acoustically-orienting parasitoid flies (Tachinidae: Ormiini). In: Krause L, Weber E (eds) Animal behavior: new research. Nova Science Publishers, New York, pp 93–132

    Google Scholar 

  • 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 43:239–245

    Article  Google Scholar 

  • Lehmann GUC, Lehmann AW (2000) Female bushcrickets mated with parasitized males show rapid remating and reduced fecundity (Orthoptera: Phaneropteridae: Poecilimon mariannae). Naturwissenschaften 87:404–407

    Article  CAS  PubMed  Google Scholar 

  • Lehmann GUC, Lehmann AW (2006) Potential lifetime reproductive success of male bushcrickets parasitized by a phonotactic fly. Anim Behav 71:1103–1110

    Article  Google Scholar 

  • Lehmann GUC, Lehmann AW (2008) Bushcricket song as a clue for spermatophore size? Behav Ecol Sociobiol 62:569–578

    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: Phanopteridae/Diptera: Tachinidae). Entomol Gen 25:135–140

    Article  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 

  • Mason AC, Lee N, Oshinsky ML (2005) The start of phonotactic walking in the fly Ormia ochracea: a kinematic study. J Exp Biol 208:4699–4708

    Article  PubMed  Google Scholar 

  • Michelsen A (1992) Directional hearing in crickets and other small animals. In: Schildberger E, Elsner N (eds) Neural basis of behavioural adaptations, vol 19. Fortschritte der Biologie. pp 195–207

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

    Article  CAS  PubMed  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 

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

    CAS  PubMed  Google Scholar 

  • Pascoal S, Cezard T, Eik-Nes A, Gharbi K, Majewska J, Payne E, Ritchie MG, Zuk M, Bailey NW (2014) Rapid convergent evolution in wild crickets. Curr Biol 24:1369–1374

    Article  CAS  PubMed  Google Scholar 

  • Ramsauer N, Robert D (2000) Free-flight phonotaxis in a parasitoid fly: behavioural thresholds, relative attraction and susceptibility to noise. Naturwissenschaften 87:315–319

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Robert D, Edgecomb RS, Read MP, Hoy RR (1996a) Tympanal hearing in tachinid flies (Diptera, Tachinidae, Ormiini): the comparative morphology of an innovation. Cell Tiss Res 284:435–448

    Article  CAS  Google Scholar 

  • Robert D, Miles RN, Hoy RR (1996b) 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, 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 fly Emblemasoma sp.: the biomechanics of directional hearing. J Exp Biol 202:1865–1876

    CAS  PubMed  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, 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 

  • Rosen MJ, Levin EG, Hoy RR (2009) The cost of assuming life history of a host: acoustic startle in the parasitoid fly Ormia ochracea. J Exp Biol 212:4056–4064

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schniederkötter K, Lakes-Harlan R (2004) Infection behavior of a parasitoid fly, Emblemasoma auditrix and its host cicada Okanagana rimosa. J Ins Sci 4:36–37

    Article  Google Scholar 

  • Stölting H (2000) Morphologie und Physiologie der tympanalen auditorischen Systeme und des evolutionären Vorläuferorgans bei Fliegen. Dissertation, University Göttingen

  • Stölting H, Moore TA, Lakes-Harlan R (2004) Acoustic communication of Okanagana rimosa (Say) (Homoptera: Cicadidae). Zoology 107:243–257

    Article  PubMed  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 

  • Strauß J, Lakes-Harlan R (2014) Evolutionary and phylogenetic origins of tympanal hearing organs in insects. In: Hedwig B (ed) Insect hearing and acoustic communication. Animal signals and communication. Springer, New York, pp 5–26

    Chapter  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 G, 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 

  • Walker TJ (1993) Phonotaxis in female Ormia ochracea (Diptera: Tachinidae), a parasitoid of field crickets. J Ins 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 

  • Williams KS, Simon C (1995) The ecology, behavior, and evolution of periodical cicadas. Annu Rev Entomol 40:269–295

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zuk M, Kolluru GR (1998) Exploitation of sexual signals by predators and parasitoids. Quart Rev Biol 73:415–438

    Article  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, Simmons LW, Rotenberry JT (1995) Acoustically-orienting parasitoids in calling and silent males of the field cricket Teleogryllus oceanicus. Ecol Entomol 20:380–383

    Article  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 Lett 2:521–524

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful for the invitation of the editors to contribute to this special issue. We thank Dr. Michael Reichert for helpful comments and careful language editing. We thank the two reviewers for helpful comments. RLH also thanks the Biological Station of the University of Michigan where studies on the biology of Emblemasoma auditrix have been performed. The authors declare that they have no conflict of interest. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Author information

Authors and Affiliations

  1. Institute for Animal Physiology, AG Integrative Sensory Physiology, Justus-Liebig-Universität Gießen, IFZ, Heinrich-Buff-Ring 26, 35392, Giessen, Germany

    Reinhard Lakes-Harlan

  2. Department of Biology, Behavioral Physiology, Humboldt Universität zu Berlin, Invalidenstraße 43, 10115, Berlin, Germany

    Gerlind U. C. Lehmann

Authors
  1. Reinhard Lakes-Harlan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gerlind U. C. Lehmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Reinhard Lakes-Harlan.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lakes-Harlan, R., Lehmann, G.U.C. Parasitoid flies exploiting acoustic communication of insects—comparative aspects of independent functional adaptations. J Comp Physiol A 201, 123–132 (2015). https://doi.org/10.1007/s00359-014-0958-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-014-0958-3

Keywords

Search

Navigation