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The auditory system of cartilaginous fishes

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Abstract

Cartilaginous fishes (Chondrichthyes), including sharks, skates, rays, elephant fishes and chimaeras, have been in existence for over 400 million years and represent early stages of the evolution of extant jawed vertebrates. The sensory systems of cartilaginous fishes, including their hearing apparatus, have adapted to a diverse range of ecosystems, from the deep ocean to freshwater rivers, revealing high levels of morphological diversity. Since sound travels such long distances underwater, this environmental cue may represent an important signal in the behavior and survival of this group of fishes but there are still many gaps in our understanding of their hearing system. Based on current knowledge, cartilaginous fishes are most sensitive to low frequency sounds (< 1500 Hz) and there is abundant support that their inner ears use only particle displacement detection rather than the detection of sound pressure, but further studies are needed to corroborate the observations of long distance detection of sound sources that might be based on the detection of pressure oscillations. This review investigates the diversity and functional significance of the inner ear of chondrichthyans from a range of habitats and explores what is known about their hearing capabilities. How underwater sounds are processed by the central nervous system, the impacts of sound on acoustic ecology and behavior, and the potential effects of anthropogenic sound are also examined. Some suggestions for future work are presented to fill the large gaps in our knowledge of the hearing abilities of this important group of vertebrates.

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adapted from Retzius (1881) and Maisey (2001)). Not to scale. aa, anterior ampulla; asc, anterior semicircular canal; ed, endolymphatic duct; ha, horizontal ampulla; hsc, horizontal semicircular canal; l, lagena; lm, lagenar macula; mn, macula neglecta; pa, posterior ampulla; psc, posterior semicircular canal; s, saccule; sm, saccular macula; ss, sinus superior; u, utricle; um, utricular macula

Fig. 4

adapted from Barber and Emerson (1980) and Lovell et al. (2007). Arrows indicate orientation of the hair cells across the macular surface. A, anterior; D, dorsal; L, lateral

Fig. 5

modified from Fay et al. (1974). ant, anterior; cr, cranium; cu, cupula; ed, endolymphatic duct; ep, endolymphatic pore; fo, fenestra ovalis; hc, hair cell; ki, kinocilium; mn, macula neglecta; ot, otoconia; pf, parietal fossa; post, posterior; psc, posterior semicircular canal; s, saccule; sk, skin; sm, saccular macula; st, stereocilia; um, utricular macula

Fig. 6

adapted from Barry (1987)). Ant, nucleus octavus anterioris; Aur, cerebellar auricle; Cb, cerebellum; CC(ND), cerebellar crest overlying nucleus dorsalis; CC(NI), cerebellar crest overlying nucleus intermedius; Desc, nucleus octavus descendens; Di, diencephalon; Mag, nucleus octavus magnocellularis; Med, medulla; Mes, mesencephalon; ND, nucleus dorsalis octavolateralis, nI, nucleus intermedius octavolateralis, nIII, occulomotor nerve; nIV, trochlear nerve; nIX, glossopharyngeal nerve; nLLa, anterior lateral line nerve; nLLad anterior lateral line nerve dorsal root; nLLav, anterior lateral line ventral root; nLLp, posterior lateral line nerve; NPv nucleus octavus pericentricularis; NV, trigeminal nerve; nVII, facial nerve; nVIII, octaval nerve; nVIIIa, octaval nerve anterior branch; nVIIIp, octaval nerve posterior branch; nX, vagus nerve; Post, nucleus octavus posterioris; Tel, telencephalon

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Fig. 8

Modified from Evangelista et al. (2010). l, lagena; s, saccule; u, utricle. Scale bars = 2 mm. Illustrations are not to scale

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Acknowledgements

We sincerely thank three anonymous reviewers for providing in depth, critical feedback. We are also grateful to Kara Yopak, Nathan Hart and Caroline Kerr for their involvement in earlier experimental work and useful discussions. This work was supported by Sea World Research and Rescue Foundation (SWR/3/2013). LC was supported by the University of Western Australia through a Scholarship for International Research Fees.

Funding

This work was supported by Sea World Research and Rescue Foundation (SWR/3/2013). LC was supported by the University of Western Australia through a Scholarship for International Research Fees.

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Correspondence to Lucille Chapuis.

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Chapuis, L., Collin, S.P. The auditory system of cartilaginous fishes. Rev Fish Biol Fisheries 32, 521–554 (2022). https://doi.org/10.1007/s11160-022-09698-8

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