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Directional hearing in insects with internally coupled ears

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Abstract

Compared to all other hearing animals, insects are the smallest ones, both in absolute terms and in relation to the wavelength of most biologically relevant sounds. The ears of insects can be located at almost any possible body part, such as wings, legs, mouthparts, thorax or abdomen. The interaural distances are generally so small that cues for directional hearing such as interaural time and intensity differences (IITs and IIDs) are also incredibly small, so that the small body size should be a strong constraint for directional hearing. Yet, when tested in behavioral essays for the precision of sound source localization, some species demonstrate hyperacuity in directional hearing and can track a sound source deviating from the midline by only \(1^{\circ }\)–\(2^{\circ }\). They can do so by using internally coupled ears, where sound pressure can act on both sides of a tympanic membrane. Here we describe their varying anatomy and mode of operation for some insect groups, with a special focus on crickets, exhibiting probably one of the most sophisticated of all internally coupled ears in the animal kingdom.

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References

  • Alexander RD (1962) Evolutionary change in cricket acoustical communication. Evolution 16:443–462

    Article  Google Scholar 

  • Autrum H (1940) Über Lautäußerungen und Schallwahrnehmung bei Arthropoden II. Das Richtungshören von Locusta und Versuch einer Hörtheorie für Tympanalorgane vom Locustidentyp. Zeitschrift für vergleichende Physiologie 28:326–352

    Article  Google Scholar 

  • Bailey WJ (1990) The ear of the bushcriket. In: Bailey WJ, Rentz DCF (eds) The Tettigoniidae. Biology, Systematics and Evolution. Crawford House Press, Bathurst, Australia, pp 217–247

  • Boyan GS (1993) Another look at insect audition: the tympanic receptors as an evolutionary specialization of the chordotonal system. J Insect Physiol 39:187–200

    Article  Google Scholar 

  • Conner WE, Corcoran AJ (2012) Sound strategies: the 65-million year-old battle between bats and insects. Annu Rev Entomol 57:21–39

    Article  CAS  PubMed  Google Scholar 

  • Field LH, Matheson T (1998) Chordotonal organs of insects. Adv Insect Physiol 27:1–228

    Article  Google Scholar 

  • Fonseca PJ (1993) Directional hearing of a cicada: biophysical aspects. J Comp Physiol A 172:767–774

    Article  Google Scholar 

  • Fonseca PJ (2014) Cicada acoustic communication. In: Hedwig B (ed) Insect hearing and acoustic communication. Springer, New York, pp 101–121

    Chapter  Google Scholar 

  • Fonseca PJ, Popov AV (1994) Sound radiation in a cicada: the role of different structures. J Comp Physiol A 175:349–361

    Article  Google Scholar 

  • Fonseca PJ, Hennig RM (2004) Directional characteristics of the auditory system of cicadas: is the sound producing tymbal an integral part of directional hearing? Physiol Entomol 29:400–408

    Article  Google Scholar 

  • Fullard JH (1990) The sensory ecology of moths and bats: global lessons in staying alive. In: Evans DL, Schmidt JO (eds) Insect defenses. Adaptive mechanisms and strategies of prey and predators. State University of New York Press, Albany, pp 203–226

    Google Scholar 

  • Gu JJ, Montealegre-Z F, Robert D, Engel MS, Qiao GX, Ren D (2012) Wing stridulation in a Jurassic katydid (Insecta, Orthoptera) produced low-pitched musical calls to attract females. Proc Natl Acad Sci USA 109:3868–3873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heinrich R, Jatho M, Kalmring K (1993) Acoustic transmission characteristics of the tympanal tracheae of bushcrickets (Tettigoniidae). II. Comparative studies of the tracheae of seven species. J Acoust Soc Am 93(6):3481–3489

    Article  Google Scholar 

  • Hill KG, Oldfield BP (1981) Auditory function in Tettigoniidae (Orthoptera: Ensifera). J Comp Physiol A 142:169–180

    Article  Google Scholar 

  • Hirtenlehner S, Römer H, Schmidt AKD (2014) Out of phase: relevance of the medial septum for directional hearing and phonotaxis in the natural habitat of field crickets. J Comp Physiol A 200(2):139–148

    Article  Google Scholar 

  • Hirtenlehner S, Römer H (2014) Selective phonotaxis of female crickets under natural outdoor conditions. J Comp Physiol A 200:239–250

    Article  Google Scholar 

  • Hoffmann E, Jatho M (1995) The acoustic trachea of Tettigoniids as an exponential horn: theoretical calculations and bioacoustical measurements. J Acoust Soc Am 98(4):1845–1851

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hoy RR (1992) The evolution of hearing in insects as adaptations to predation from bats. In: Webster DB, Fay RR, Popper AN (eds) The evolutionary biology of hearing. Springer, Heidelberg, pp 115–129

    Chapter  Google Scholar 

  • Jeram S, Rössler W, Cokl A, Kalmring K (1995) Structure of atympanate tibial organs in legs of the cave-living Ensifera, Troglophilus neglectus (Gryllacridoidea, Raphidophoridae). J Morphol 223:109–118

    Article  Google Scholar 

  • Kostarakos K, Hennig M, Römer H (2009) Two matched filters and the evolution of mating signals in four species of cricket. Front Zool 6:22

    Article  PubMed  PubMed Central  Google Scholar 

  • Kostarakos K, Römer H (2010) Sound transmission and directional hearing in field crickets: neurophysiological studies outdoors. J Comp Physiol A 196:669–681

    Article  Google Scholar 

  • Lewis DB (1974) The physiology of the Tettigoniide ear. I. The implications of the anatomy of the ear to its function in sound reception. J Exp Biol 60:821–837

    CAS  PubMed  Google Scholar 

  • Lewis DB (1983) Directional cues for auditory localization. In: Lewis DB (ed) Bioacoustics: a comparative approach. Academic Press, London, pp 233–260

    Google Scholar 

  • Mhatre N, Montealegre-Z F, Balakrishnan R, Robert D (2009) Mechanical response of the tympanal membranes of the tree cricket Oecanthus henryi. J Comp Physiol A 195:453–462

    Article  Google Scholar 

  • Michelsen A (1998) Biophysical basis of sound localization in insects. In: Hoy RR, Popper AN, Fay RR (eds) Comparative hearing: insects. Springer, New York, pp 18–22

    Chapter  Google Scholar 

  • Michelsen A, Heller KG, Stumpner A, Rohrseitz K (1994a) A new biophysical method to determine the gain of the acoustic trachea in bushcrickets. J Comp Physiol A 175:145–152

    Article  CAS  PubMed  Google Scholar 

  • Michelsen A, Popov AV, Lewis B (1994b) Physics of directional hearing in the cricket Gryllus bimaculatus. J Comp Physiol A 175:153–164

    Article  Google Scholar 

  • Michelsen A, Löhe G (1995) Tuned directionality in cricket ears. Nature 375:639

  • Michelsen A, Rohrseitz K (1995) Directional sound processing and interaural sound transmission in a small and large grasshopper. J Exp Biol 198:1817–1827

    PubMed  Google Scholar 

  • Michelsen A, Larsen ON (2008) Pressure difference receiving ears. Bioinspir Biomimet 3:1–18

    Article  Google Scholar 

  • Montealegre-Z F, Robert D (2015) Biomechanics of hearing in katydids. J Comp Physiol A 201:5–18

    Article  Google Scholar 

  • Morse PM, Ingard KU (1968) Theoretical Acoustics. Princeton University Press, Princeton, NJ

  • Nilsson DE (2009) The evolution of eyes and visually guided behaviour. Philos Trans R Soc Lond B 364:2833–2847

    Article  Google Scholar 

  • Robert D (2005) Directional hearing in insects. In: Popper AN, Fay RR (eds) Sound source localization. Springer, New York, pp 6–35

    Chapter  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

  • Schmidt AKD, Riede K, Römer H (2011) High background noise shapes selective auditory filters in a tropical cricket. J Exp Biol 214:1754–1762

    Article  PubMed  PubMed Central  Google Scholar 

  • Schmidt AKD, Römer H (2013) Diversity of acoustic tracheal system and its role for directional hearing in crickets. Front Zool 10:61

    Article  PubMed  PubMed Central  Google Scholar 

  • Schöneich S, Hedwig B (2010) Hyperacute directional hearing and phonotactic steering in the cricket (Gryllus bimaculatus deGeer). PLoS One 5:e15141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schul J, Holderied M, Helversen DV, Helversen OV (1999) Directional hearing in grasshoppers: neurophysiological testing of a bioacoustic model. J Exp Biol 202:121–133

  • Shaw S (1994) Detection of airborne sound by a cockroach ‘vibration’ detector: a possible missing link in insect auditory evolution. J Exp Biol 193:13–47

    PubMed  Google Scholar 

  • Song H, Amedegnato C, Cicliano MM, Desutter-Grandcolas L, Heads SW, Huang Y, Otte D, Whiting MF (2015) 300 million years of diversification: elucidating the patterns of orthopteran evolution based on comprehensive taxon and gene sampling. Cladistics. doi:10.1111/cla.12116

    Google Scholar 

  • Strauß J, Stritih N, Lakes-Harlan R (2014) The subgenual organ complex in the cave cricket Troglophilus neglectus (Orthoptera: Rhaphidophoridae): comparative innervation and sensory evolution. R Soc Open Sci 1:140240

    Article  PubMed  PubMed Central  Google Scholar 

  • Strauß J, Stumpner A (2015) Selective forces on origin, adaptation and reduction of tympanal ears in insects. J Comp Physiol A 201:155–169

    Article  CAS  Google Scholar 

  • Stritih N, Stumpner A (2009) Vibratory interneurons in the non-hearing cave cricket indicate evolutionary origin of sound processing elements in ensifera. Zoology 112:48–68

    Article  PubMed  Google Scholar 

  • van Staaden MJ, Römer H (1998) Evolutionary transition from stretch to hearing in ancient grasshoppers. Nature 394:773–776

    Article  CAS  Google Scholar 

  • Wendler G, Löhe G (1993) The role of the medial septum in the acoustic trachea of the cricket Gryllus bimaculatus. J Comp Physiol A 173:557–564

    Google Scholar 

  • Yack JE (2004) The structure and function of auditory chordotonal organs in insects. Microsc Res Tech 63:315–337

    Article  PubMed  Google Scholar 

  • Yack JE, Fullard JH (1993) What is an insect ear? Ann Entomol Soc Am 86:677–682

    Article  Google Scholar 

  • Yack JE, Dawson J (2008) Insect ears. In: Hoy RR, Shepherd GM, Basbaum AI, Kaneko A, Westheimer G (eds) The senses: a comprehensive reference, vol 3. Elsevier, Philadelphia, pp 35–54

    Chapter  Google Scholar 

Download references

Acknowledgments

We are grateful to the Smithsonian Tropical Research Institute (STRI) and the National Authority for the Environment (ANAM) for providing research permits and logistical support, which ensured that all work was conducted in conformity with current Panamanian laws. This work was supported by the Austrian Science Fund (FWF): Project P26072-B25to HR.

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  1. Institute of Zoology, University of Graz, Universitaetsplatz 2, Graz, Austria

    Heiner Römer & Arne K. D. Schmidt

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  1. Heiner Römer
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  2. Arne K. D. Schmidt
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Correspondence to Heiner Römer.

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This article belongs to a Special Issue on Internally Coupled Ears (ICE).

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Römer, H., Schmidt, A.K.D. Directional hearing in insects with internally coupled ears. Biol Cybern 110, 247–254 (2016). https://doi.org/10.1007/s00422-015-0672-4

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