The development of hearing abilities in the shark Scyliorhinus canicula

[en] The few works on audition in sharks and rays concern only adult specimens. We report the hearing abilities in the dogfish Scyliorhinus canicula at different stages, from embryos that still have their yolk sac inside their egg, to juveniles. Hearing development corresponds to an increase in the frequency range from 100−300 Hz in early pre-hatching stages to 100–600 Hz in juveniles. Modifications in hearing abilities correspond to the development of the brain, the increase of the volume of the membranous labyrinth, the growth of the sensory epithelium, and the development of stereocilia in addition to kinocilium before hatching. This work offers solid insights into the development of hearing abilities that usually can only be inferred from the anatomy of vertebrates or after birth/hatching. It shows also that shark can be sensitive to background noise during development.

Research center :

AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège

Disciplines :

Anatomy (cytology, histology, embryology...) & physiology

Author, co-author :

Parmentier, Eric ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive

Banse, Marine ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive

Boistel, Renaud

Compère, Philippe ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive

Bertucci, Frédéric

COLLEYE, Orphal ; Centre Hospitalier Universitaire de Liège - CHU > Unilab > Laboratoire microscopie électronique

Language :

English

Title :

The development of hearing abilities in the shark Scyliorhinus canicula

Publication date :

21 May 2020

Journal title :

American Journal of Anatomy

ISSN :

0002-9106

Publisher :

John Wiley & Sons, Hoboken, United States - New York

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]

Available on ORBi :

since 25 May 2020

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Bibliography

Abramoff, M.D., Magalhaes, P.J. and Ram, S.J. (2014) Image processing with ImageJ. Biophotonics International, 11, 36–42.
Ballard, W., Mellinger, J. and Lechenault, H. (1993) A series of normal stages for development of Scyliorhinus canicula the lesser spotted dogfish (Chondrichthyes : Scyliorhinidae). Journal of Experimental Zoology, 267, 318–336.
Barber, V.C. and Emerson, C.J. (1980) Cell and tissue scanning electron microscopic observations on the inner ear of the skate, Raja oceilata. Cell and Tissue Research, 215, 199–215.
Boistel, R., Swoger, J., Krzic, U., Fernandez, V., Gillet, B. and Reynaud, E.G. (2011) The future of three-dimensional microscopic imaging in marine biology. Marine Ecology, 32, 438–452.
Bullock, T.H. and Corwin, J.T. (1979) Acoustic evoked activity in the brain in sharks. Journal of Comparative Physiology A, 129, 223–234.
Casper, B.M. and Mann, D.A. (2006) Evoked potential audiograms of the nurse shark (Ginglymostoma cirratum) and the yellow stingray (Urobatis jamaicensis). Environmental Biology of Fishes, 76, 101–108.
Colleye, O., Ovidio, M., Salmon, A. and Parmentier, E. (2013) Contribution to the study of acoustic communication in two Belgian river bullheads (Cottus rhenanus and C. perifretum) with further insight into the sound-producing mechanism. Zoology, 10, 1–14.
Corwin, J.T. (1981a) Peripheral auditory physiology in the lemon shark: Evidence of parallel otolithic and non-otolithic sound detection. Journal of Comparative Physiology A, 142, 379–390.
Corwin, J.T. (1981b) Postembryonic production and aging of inner ear hair cells in sharks. The Journal of Comparative Neurology, 201, 541–553.
Corwin, J.T. (1983) Postembryonic growth of the macula neglecta auditory detector in the ray, Raja clavata: continual increases in hair cell number, neural convergence, and physiological sensitivity. The Journal of Comparative Neurology, 217, 345–356.
Corwin, J.T. (1989) Functional anatomy of the auditory system in sharks and rays. Journal of Experimental Zoology, 252, 62–74.
Corwin, J.T. and Northcutt, G. (1982) Auditory centers in the elasmobranch brain stem: deoxyglucose autoradiography and evoked potential recording. Brain Research, 236, 261–273.
Demski, L.S., Gerald, J.W. and Popper, A.N. (1973) Central and peripheral mechanisms of teleost sound production. American Zoologist, 13, 1141–1167.
Diez, J.M. and Davenport, J. (1987) Embryonic respiration in the dogfish (Scyliorhinus canicula L.). Journal of the Marine Biological Association of the United Kingdom, 67, 249–261.
Egner, S.A. and Mann, D.A. (2005) Auditory sensitivity of sergeant major damselfish Abudefduf saxatilis from post-settlement juvenile to adult. Marine Ecology Progress Series, 285, 213–222.
Foulley, M.-M. and Mellinger, J. (1980). Etude chronologique, structurale et biométrique de l’œuf et de son développement chez la petite roussette (Scyliorhinus canicula) élevée en eau de mer artificielle. Reproduction Nutrition Développement, 26, 1835–1848.
Gans, C. (1992) An overview of the evolutionary biology of hearing. In: The Evolutionary Biology of Hearing (eds Webster, D.B., Fay, R.R. and Popper, A.N.), pp. 3–13. New York: Springer.
Hanson, M., Westerberg, H. and Öblad, M. (1990) The role of magnetic statoconia in dogfish (Squalus Acanthias). The Journal of Experimental Biology, 151, 205–218.
Higgs, D.M. and Radford, C.A. (2013) The contribution of the lateral line to 'hearing' in fish. Journal of Experimental Biology, 216(8), 1484–1490.
Ho, J., Tumkaya, T., Aryal, S., Choi, H. and Claridge-Chang, A. (2019) Moving beyond P values: data analysis with estimation graphics. Nature Methods, 16, 565–566.
Hueter, R.E., Mann, D.A., Maruska, K.P., Sisneros, J.A. and Demski, L.S. (2004) Sensory biology of elasmobranchs. In: Biology of Sharks and Their Relatives (eds Carrier, J.C., Musick, J.A. and Heithaus, M.R.), pp. 325–368. Boca Raton, Florida: CRC Press.
Kéver, L., Colleye, O., Herrel, A., Romans, P. and Parmentier, E. (2014) Hearing capacities and otolith size in two ophidiiform species (Ophidion rochei and Carapus acus). Journal of Experimental Biology, 217, 2517–2525.
Kormanik, G.A. (1993) Ionic and osmotic environment of developing elasmobranch embryos. Environmental Biology of Fishes, 38, 233–240.
Ladich, F. and Fay, R.R. (2013) Auditory evoked potential audiometry in fish. Review in Fish Biology and Fisheries, 23, 317–364.
Lovell, J.M., Findlay, M.M., Harper, G.M. and Moate, R.M. (2007) The polarization of hair cells from the inner ear of the lesser spotted dogfish Scyliorhinus canicula. Journal of Fish Biology, 70, 362–373.
Lowenstein, O. and Roberts, T.D.M. (1951) The localization and analysis of the responses to vibration from the isolated elasmobranch labyrinth; a contribution to the problem of the evolution of hearing in vertebrates. Journal of Physiology, 114, 471–489.
Löwenstein, O. and Sand, A. (1940) The individual and integrated activity of the semicircular canals of the elasmobranch labyrinth. Journal of Physiology, 99, 89–101.
Lychakov, D.V., Boyadzhieva-Mikhailova, A., Christov, I. and Evdokimov, I.I. (2000) Otolithic apparatus in Black Sea elasmobranchs. Fisheries Research, 46, 27–38.
Maisey, J.G. (2001) Remarks on the inner ear of elasmobranchs and its interpretation from skeletal labyrinth morphology. Journal of Morphology, 250, 236–264.
Mann, D.A., Higgs, D.M., Tavolga, W.N., Souza, M.J. and Popper, A.N. (2001) Ultrasound detection by clupeiform fishes. Journal of the Acoustical Society of America, 109, 3048–3054.
Mellinger, J. (1994) L’oeuf de roussette (Scyliorhinus canicula) incubé au laboratoire : un matériel de recherche pour l’embryologiste, l’éthologiste, le physiologiste. Ichtyophysiologica Acta, 17, 9–27.
Mills, M., Rasch, R., Siebeck, U.E. and Collin, S.P. (2011) Exogenous material in the inner ear of the adult Port Jackson shark, Heterodontus portusjacksoni (Elasmobranchii). Anatomical Record, 294, 373–378.
Montgomery, J.C., Jeffs, A., Simpson, S.D., Meekan, M.G. and Tindle, C. (2006) Sound as an orientation clue for the pelagic larvae of reef fish and crustaceans. Advances in Marine Biology, 51, 143–196.
Nedelec, S.L., Campbell, J., Radford, A.N., Simpson, S.D. and Merchant, N.D. (2016) Particle motion: the missing link in underwater acoustic ecology. Methods in Ecology and Evolution, 7, 836–842.
Parmentier, E., Colleye, O. and Mann, D. (2009) Hearing ability in three clownfish species. Journal of Experimental Biology, 212, 2023–2026.
Popper, A.N. and Fay, R.R. (2011) Rethinking sound detection by fishes. Hearing Research, 273, 25–36.
Popper, A.N., Hawkins, A.D., Sand, O. and Sisneros, J.A. (2019) Examining the hearing abilities of fishes. Journal of the Acoustical Society of America, 146, 948–955.
Retzius, G. (1884). Das Gehörorgan der Reptilien, der Vögel und der Säu-gethiere (Vol. 2). In: Das Gehörorgan der Wirbelthiere: Morphologisch-histologischeStudien. Stockholm: Samson & Wallin.
Rogers, P.H., Hawkins, A.D., Popper, A.N., Fay, R.R. and Gray, M.D. (2016) Parvulescu revisited: small tank acoustics for bioacousticians BT. In: The Effects of Noise on Aquatic Life II (eds Popper, A.N. and Hawkins, A.), pp. 933–941. New York: Springer.
Simpson, S.D., Yan, H.Y., Wittenrich, M.L. and Meekan, M.G. (2005) Response of embryonic coral reef fishes (Pomacentridae: Amphiprion spp.) to noise. Marine Ecology Progress Series, 287, 201–208.
Tester, A.L., Kendall, J.I. and Milisen, W.B. (1972) Morphology of the ear of the shark genus Carcharhinus, with particular reference to the macula neglecta. Pacific Science, 26, 264–274.
Zanette, I., Daghfous, G., Weitkamp, T., Gillet, B. and Adriaens, D. (2014) Looking Inside marine organisms with magnetic resonance and X-ray imaging. In: Imaging Marine Life: Macrophotography and Microscopy Approaches for Marine Biology (ed. Reynaud, E.G.), pp. 123–184. Hoboken: Wiley-Blackwell.