Abstract
Animals have evolved a vast diversity of mechanisms to detect sounds. Auditory organs are thus used to detect intraspecific communicative signals and environmental sounds relevant to survival. To hear, terrestrial animals must convert the acoustic energy contained in the airborne sound pressure waves into neural signals. In mammals, spectral quality is assessed by the decomposition of incoming sound waves into elementary frequency components using a sophisticated cochlear system. Some insects like katydids (or bushcrickets) have evolved biophysical mechanisms for auditory processing that are remarkably equivalent to those of mammals. Located on their front legs, katydid ears are small, yet are capable of performing several of the tasks usually associated with mammalian hearing. These tasks include air-to-liquid impedance conversion, signal amplification, and frequency analysis. Impedance conversion is achieved by a lever system, a mechanism functionally analogous to the mammalian middle ear ossicles, yet morphologically distinct. In katydids, the exact mechanisms supporting frequency analysis seem diverse, yet are seen to result in dispersive wave propagation phenomenologically similar to that of cochlear systems. Phylogenetically unrelated katydids and tetrapods have evolved remarkably different structural solutions to common biophysical problems. Here, we discuss the biophysics of hearing in katydids and the variations observed across different species.
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Abbreviations
- AcT:
-
Acoustic trachea
- ATM:
-
Anterior tympanal Membrane
- AV:
-
Auditory vesicle
- CA:
-
Crista acustica
- HC:
-
Hemolymph channel
- LDV:
-
Laser Doppler vibrometry
- PTM:
-
Posterior tympanal Membrane
- TM:
-
Tympanal membrane
- TP:
-
Tympanal plate
References
Ashmore J (2008) Cochlear outer hair cell motility. Physiol Rev 88(1):173–210. doi:10.1152/physrev.00044.2006
Autrum H (1940) Über Lautäusserungen und Schallwahrnehmung bei Arthropoden. II. Das Richtungshören von Locusta ital.; und Versuch einer Hörtheorie für Tympanalorgane vom Locustidentyp. Z Vergl Physiol 28:326–352. doi:10.1007/BF00342439
Autrum H (1963) Anatomy and physiology of sound receptors in invertebrates. In: Busnel RG (ed) Acoustic behaviour of animals. Elsevier, Amsterdam, pp 412–433
Bailey WJ (1990) The ear of the bushcriket. In: Bailey WJ, Rentz DCF (eds) The Tettigoniidae. Biology, systematics and evolution. Crawford House Press, Bathurst, pp 217–247
Bailey WJ, Stephen RO (1978) Directionality and auditory slit function: theory of hearing in bushcrickets. Science 201(4356):633–634. doi:10.1126/science.201.4356.633
Bailey WJ, Stephen RO, Yeoh P (1988) Signal transmission in noisy environments: auditory masking in the tympanic nerve of the bushcricket Metaballus litus (Orthoptera: Tettigoniinae). J Acoust Soc Am 83(5):1828–1832. doi:10.1121/1.396517
Ball E, Field LH (1981) Structure of the auditory system of the weta Hemideina crassidens (Blanchard, 1851) (Orthoptera, Ensifera, Gryllacridoidea, Stenopelmatidae). Cell Tissue Res 217(2):321–344. doi:10.1007/bf00233584
Bangert M, Kalmring K, Sickmann T, Stephen R, Jatho M, Lakes-Harlan R (1998) Stimulus transmission in the auditory receptor organs of the foreleg of bushcrickets (Tettigoniidae) I. The role of the tympana. Hear Res 115(1–2):27–38. doi:10.1016/S0378-5955(97)00177-9
Belwood JJ, Morris GK (1987) Bat predation and its influence on calling behavior in neotropical katydids. Science 238:64–67. doi:10.1126/science.238.4823.64
Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer Associates, Sunderland, Massachusetts
Bruns V, Schmieszek E (1980) Cochlear innervation in the greater horseshoe bat—demonstration of an acoustic fovea. Hear Res 3(1):27–43. doi:10.1016/0378-5955(80)90006-4
Faure PA, Hoy RR (2000) The sounds of silence: cessation of singing and song pausing are ultrasound-induced acoustic startle behaviors in the katydid Neoconocephalus ensiger (Orthoptera; Tettigoniidae). J Comp Physiol A 186(2):129–142. doi:10.1007/s003590050013
Field LH, Matheson T (1998) Chordotonal organs of insects. Adv Insect Physiol 27:1–230. doi:10.1016/S0065-2806(08)60013-2
Field LH, Hill KG, Ball EE (1980) Physiological and biophysical properties of the auditory system of the New Zealand weta Hemideina crassidens (Blanchard, 1851) (Ensifera: Stenopelmatidae). J Comp Physiol 141(1):31–37. doi:10.1007/bf00611875
Heinrich R, Jatho M, Kalmring K (1993) Acoustic transmission characteristics of the tympanal tracheas of bushcrickets (Tettigoniidae). II. Comparative studies of the tracheas of 7 species. J Acoust Soc Am 93(6):3481–3489. doi:10.1121/1.405678
Heller K-G (1995) Acoustic signalling in Palaeotropical bush-crickets (Orthoptera, Tettigonioidea, Pseudophyllidae): does predation pressure by eavesdropping enemies differ in the Palaeotropics and Neotropics. J Zool (Lond) 237:469–485
Hill KG, Oldfield BP (1981) Auditory function in tettigoniidae (Orthoptera:Ensifera). J Comp Physiol 142(2):169–180. doi:10.1007/bf00605735
Hirtenlehner S, Römer H, Schmidt AD (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. doi:10.1007/s00359-013-0869-8
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. doi:10.1121/1.413371
Hummel J, Kössl M, Nowotny M (2011) Sound-induced tympanal membrane motion in bushcrickets and its relationship to sensory output. J Exp Biol 214(21):3596–3604. doi:10.1242/jeb.054445
Isobe K, Motokawa K (1955) Functional structure of the retinal fovea and maxwell’s spot. Nature 175(4450):306–307. doi:10.1038/175306a0
Klowden MJ (2008) Physiological systems in Insects. 2nd ed. Elsevier Inc.
Lang AB, Kalko EKV, Römer H, Bockholdt C, Dechmann DKN (2006) Activity levels of bats and katydids in relation to the lunar cycle. Oecologia 146(4):659–666. doi:10.1007/s00442-005-0131-3
Lewis DB (1974) The physiology of the tettigoniid ear. II. The response characteristics of the ear to differential inputs: lesion and blocking experiments. J Exp Biol 60:839–851
Lomas K, Montealegre-Z F, Parsons S, Field LH, Robert D (2011) Mechanical filtering for narrow-band hearing in the weta. J Exp Biol 214(5):778–785. doi:10.1242/jeb.050187
Lomas KF, Greenwood DR, Windmill JFC, Jackson JC, Corfield J, Parsons S (2012) Discovery of a lipid synthesising organ in the auditory system of an Insect. PLoS One 7(12):e51486. doi:10.1371/journal.pone.0051486
Mason AC, Morris GK, Wall P (1991) High ultrasonic hearing and tympanal slit function in rainforest katydids. Naturwissenschaften 78(8):365–367. doi:10.1007/BF01131611
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(5):453–462. doi:10.1007/s00359-009-0423-x
Michelsen A (1971) The physiology of the locust ear. J Comp Physiol A 71(1):102–128. doi:10.1007/BF01245156
Michelsen A, Larsen ON (1978) Biophysics of the ensiferan ear. I: tympanal vibrations in bushcriekets (Tettigoniidae) studied with Laser vibrometry. J Comp Physiol A 123(3):193–203. doi:10.1007/BF00656872
Michelsen A, Larsen ON (2008) Pressure difference receiving ears. Bioinspir Biomim 3 (1). doi:10.1088/1748-3182/3/1/011001
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(2):145–151. doi:10.1007/BF00215110
Michelsen A, Popov AV, Lewis B (1994b) Physics of directional hearing in the cricket Gryllus bimaculatus. J Comp Physiol A 175(2):153–164. doi:10.1007/BF00215111
Montealegre-Z F (2009) Scale effects and constraints for sound production in katydids (Orthoptera: Tettigoniidae): generator morphology constrains signal parameters. J Evol Biol 22:355–366. doi:10.1111/j.1420-9101.2008.01652.x
Montealegre-Z F (2014) Biofísica- El refinado oído del saltamontes: un caso de evolución convergente con el oído de los mamíferos. Investigación y Ciencia (Spanish edition of Scientific American) 452:50–56
Montealegre-Z F, Morris GK (2004) The spiny devil katydids, Panacanthus Walker (Orthoptera : Tettigoniidae): an evolutionary study of acoustic behaviour and morphological traits. Syst Entomol 29(1):21–57. doi:10.1111/j.1365-3113.2004.00223.x
Montealegre-Z F, Postles M (2010) Resonant sound production in Copiphora gorgonensis (Tettigoniidae: Copiphorini), an endemic species from Parque Nacional Natural Gorgona Colombia. J Orthoptera Res 19(2):347–355. doi:10.1665/034.019.0223
Montealegre-Z F, Jonsson T, Robson-Brown KA, Postles M, Robert D (2012) Convergent evolution between insect and mammalian audition. Science 338(6109):968–971. doi:10.1126/science.1225271
Morris GK (1999) Song in arthropods. In: Davey KG (ed) Encyclopedia of reproduction, vol 4. Academic Press, San Diego, pp 508–517
Morris GK (2008) Size and carrier in the bog katydid, Metrioptera sphagnorum (Orthoptera: Ensifera, Tettigoniidae). J Orthoptera Res 17(2):333–342. doi:10.1665/1082-6467-17.2.333
Morris GK, Mason AC, Wall P, Belwood JJ (1994) High ultrasonic and tremulation signals in neotropical katydids (Orthoptera, Tettigoniidae). J Zool (Lond) 233:129–163. doi:10.1111/j.1469-7998.1994.tb05266.x
Mugleston JD, Song H, Whiting MF (2013) A century of paraphyly: A molecular phylogeny of katydids (Orthoptera: Tettigoniidae) supports multiple origins of leaf-like wings. Mol Phylogenet Evol 69(3):1120–1134. doi:10.1016/j.ympev.2013.07.014
Nowotny M, Hummel J, Weber M, Moeckel D, Koessl M (2010) Acoustic-induced motion of the bushcricket (Mecopoda elongata, Tettigoniidae) tympanum. J Comp Physiol A 196(12):939–945. doi:10.1007/s00359-010-0577-6
Oldfield BP (1982) Tonotopic organization of auditory receptors in Tettigoniidae (Orthoptera, Ensifera). J Comp Physiol 147(4):461–469. doi:10.1007/BF00612011
Oldfield BP (1985) The role of the tympanal membrane in the tuning of auditory receptors in Tettigoniidae (Orthoptera: Ensifera). J Exp Biol 116:493–497
Palghat Udayashankar A, Kössl M, Nowotny M (2012) Tonotopically arranged traveling waves in the miniature hearing organ of bushcrickets. PLoS One 7(2):e31008. doi:10.1371/journal.pone.0031008
Palghat Udayashankar A, Kössl M, Nowotny M (2014) Lateralization of travelling wave response in the hearing organ of bushcrickets. Plos One 9(1):e86090
Purves D, Augustine GJ, Fitzpatrick D, Hall WC, LaMantia AS, White LE (2013). Neuroscience. 5rd edition, Chapter 13. Sinauer Associates, Sunderland
Rajaraman K, Mhatre N, Jain M, Postles M, Balakrishnan R, Robert D (2013) Low-pass filters and differential tympanal tuning in a paleotropical bushcricket with an unusually low frequency call. J Exp Biol 216:777–787. doi:10.1242/jeb.078352
Ramsier MA, Cunningham AJ, Moritz GL, Finneran JJ, Williams CV, Ong PS, Gursky-Doyen SL, Dominy NJ (2012) Primate communication in the pure ultrasound. Biol Lett 8(4):508–511. doi:10.1098/rsbl.2011.1149
Ratcliffe JM, Fullard JH, Arthur BJ, Hoy RR (2011) Adaptive auditory risk assessment in the dogbane tiger moth when pursued by bats. Proc R Soc B-Biol Sci 278(1704):364–370. doi:10.1098/rspb.2010.1488
Robert D (2005) Directional hearing in insects. In: Popper AN, Fay RR (eds) Sound source localization, vol 25. Springer-Verlag New York, pp 6–35. doi: 10.1007/0-387-28863-5_2
Robinson DJ, Hall MJ (2002) Sound signalling in Orthoptera. Adv Insect Physiol 29:151–278. doi:10.1016/S0065-2806(02)29003-7
Robles L, Ruggero MA (2001) Mechanics of the mammalian cochlea. Physiol Rev 81(3):1305–1352
Römer H (1983) Tonotopic organization of the auditory neuropil in the bushcricket Tettigonia viridissima. Nature 306(5938):60–62. doi:10.1038/306060a0
Rössler W, Hubschen A, Schul J, Kalmring K (1994) Functional morphology of bushcricket ears: comparison between two species belonging to the Phaneropterinae and Decticinae (Insecta, Ensifera). Zoomorphology 114(1):39–46. doi:10.1007/BF00574913
Sarria-S FA, Morris GK, Windmill JFC, Jackson J, Montealegre-Z F (2014) Shrinking wings for ultrasonic pitch production: hyperintense ultra-short-wavelength calls in a new genus of neotropical katydids (Orthoptera: Tettigoniidae). Plos One 9 (6). doi: e9870810.1371/journal.pone.0098708
Schiolten P, Larsen ON, Michelsen A (1981) Mechanical time resolution in some insect ears. I. Impulse responses and time constants. J Comp Physiol 143:289–295. doi:10.1007/BF00611164
Schnitzler H-U, Denzinger A (2011) Auditory fovea and Doppler shift compensation: adaptations for flutter detection in echolocating bats using CF-FM signals. J Comp Physiol A 197(5):541–559. doi:10.1007/s00359-010-0569-6
Schuller G, Pollak G (1979) Disproportionate frequency representation in the inferior colliculus of Doppler-compensating greater horseshoe bats-evidence for an acoustic fovea. J Comp Physiol 132(1):47–54. doi:10.1007/BF00617731
Schumacher R (1973) Morphologische Untersuchungen der tibialen Tympanalorgane von neun einheimischen Laubheuschrecken-Arten (Orthoptera, Tettigonioidea). Z Morphol Tiere 75:267–282. doi:10.1007/BF00288474
Schumacher R (1975) Scanning-Electron-Microscope description of the tibial tympanal organ of the Tettigonioidea (Orthoptera, Ensifera). Z Vergl Physiol 81:209–219. doi:10.1007/BF00278370
Shen JX (1993) A peripheral mechanism for auditory directionality in the bushcricket Gampsocleis gratiosa acoustic tracheal system. J Acoust Soc Am 94(3):1211–1217. doi:10.1121/1.408174
Stephen RO, Bailey WJ (1982) Bioacoustics of the ear of the bushcricket Hemisaga (Sagenae). J Acoust Soc Am 72(1):13–25. doi:10.1121/1.387997
Stephen RO, Bennet-Clark HC (1982) The anatomical and mechanical basis of stimulation and frequency analysis in the locust ear. J Exp Biol 99 (AUG):279-314
Stolting H, Stumpner A (1998) Tonotopic organization of auditory receptors of the bushcricket Pholidoptera griseoaptera (Tettigoniidae, Decticinae). Cell Tissue Res 294(2):377–386. doi:10.1007/s004410051187
Stumpner A, Nowotny M (2014) Neural processing in the bush-cricket auditory pathway. In: Hedwig B (ed) Insect hearing and acoustic communication, vol 1. Animal signals and communication. Springer Berlin Heidelberg, pp 143–166. doi: 10.1007/978-3-642-40462-7_9
Vater M, Kössl M (2011) Comparative aspects of cochlear functional organization in mammals. Hear Res 273(1–2):89–99. doi:10.1016/j.heares.2010.05.018
Vogel S (2013) Comparative biomechanics: life’s physical world, 2nd edn. Princeton University Press, New Jersey
von Békésy G (1960) Experiments in hearing. McGraw-Hill, New York
Vondran T, Apel KH, Schmitz H (1995) The infrared receptor of Melanophila acuminata De Geer (Coleoptera: Buprestidae): ultrastructural study of a unique insect thermoreceptor and its possible descent from a hair mechanoreceptor. Tissue Cell 27(6):645–658. doi:10.1016/S0040-8166(05)80020-5
Windmill JFC, Göpfert MC, Robert D (2005) Tympanal travelling waves in migratory locusts. J Exp Biol 208(1):157–168. doi:10.1242/jeb.01332
Yack JE (2004) The structure and function of auditory chordotonal organs in insects. Microsc Res Tech 63(6):315–337. doi:10.1002/jemt.20051
Acknowledgments
This work was sponsored by the Human Frontier Science Program (Cross Disciplinary Fellowship LT00024/2008-C to F.M.-Z.). The authors are currently sponsored by the Royal Society, and by the Leverhulme Trust (grant No. RPG-2014-284). The Colombian Ministry of Environment granted a permit for fieldwork at Gorgona National Park (decree DTS0-G-31 11/07). We would like to thank two anonymous referees for discussions and comments on earlier versions of the manuscript. We also thank Ben Chivers for proof-reading the final version on English grammar. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
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Montealegre-Z, F., Robert, D. Biomechanics of hearing in katydids. J Comp Physiol A 201, 5–18 (2015). https://doi.org/10.1007/s00359-014-0976-1
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DOI: https://doi.org/10.1007/s00359-014-0976-1