Hearing capacities and morphology of the auditory system in Serrasalmidae (Teleostei: Otophysi)

[en] Like all otophysan fishes, serrasalmids (piranhas and relatives) possess a Weberian apparatus that improves their hearing capacities. We compared the hearing abilities among eight species of serrasalmids having different life-history traits: herbivorous vs. carnivorous and vocal vs. mute species. We also made 3D reconstructions of the auditory system to detect potential morphological variations associated with hearing ability. The hearing structures were similar in overall shape and position. All the species hear in the same frequency range and only slight differences were found in hearing thresholds. The eight species have their range of best hearing in the lower frequencies (50–900 Hz). In vocal serrasalmids, the range of best hearing covers the frequency spectrum of their sounds. However, the broad overlap in hearing thresholds among species having different life-history traits (herbivorous vs. carnivorous and vocal vs. non-vocal species) suggests that hearing ability is likely not related to the capacity to emit acoustic signals or to the diet, i.e. the ability to detect sounds is not associated with a given kind of food. The inner ear appears to be highly conservative in this group suggesting that it is shaped by phylogenetic history or by other kinds of constraints such as predator avoidance.

Research center :

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

Disciplines :

Environmental sciences & ecology
Zoology

Author, co-author :

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

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

Michel, Christian ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Département de Biologie, Ecologie et Evolution

Herrel, Anthony; Muséum National d'Histoire Naturelle (Paris, France) > Adaptations du vivant

Boyle, Kelly; University of South Alabama > Department of Marine Sciences

Language :

English

Title :

Hearing capacities and morphology of the auditory system in Serrasalmidae (Teleostei: Otophysi)

Publication date :

19 January 2018

Journal title :

Scientific Reports

eISSN :

2045-2322

Publisher :

Nature Publishing Group

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 22 January 2018

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Bibliography

Slabbekoorn, H. et al. A noisy spring: The impact of globally rising underwater sound levels on fish. Trends Ecol. Evolut. 25, 419-427 (2010).
Ladich, F. Acoustic communication and the evolution of hearing in fishes. Philos. Trans. R. Soc. London (Biol.) 355, 1285-1288 (2000).
Vasconcelos, R. O., Fonseca, P. J., Amorim, M. C. P. & Ladich, F. Representation of complex vocalizations in the Lusitanian toadfish auditory system: Evidence of fine temporal, frequency and amplitude discrimination. Proc. R. Soc. Lond. (Biol.) 278, 826-834 (2011).
Remage-Healey, L., Nowacek, D. P. & Bass, A. H. Dolphin foraging sounds suppress calling and elevate stress hormone levels in a prey species, the Gulf toadfish. J. Exp. Biol. 209, 4444-4451, https://doi.org/10.1242/jeb.02525 (2006).
Fay, R. Soundscapes and the sense of hearing of fishes. Integr. Zool. 4, 26-32 (2009).
Parmentier, E. et al. The influence of various reef sounds on coral-fish larvae behaviour. J. Fish Biol. 86, 1507-1518, https://doi.org/10.1111/jfb.12651 (2015).
Simpson, S. D., Meekan, M. G., McCauley, R. D. & Jeffs, A. Attraction of settlement-stage coral reef fishes to reef noise. Mar. Ecol. Prog. Ser. 276, 263-268 (2004).
Ladich, F. Fish bioacoustics. Curr. Opin. Neurobiol. 28, 121-127 (2014).
Weber, E. H. De Aure et Auditu Hominis et Animalium. Pars I. De Aure Animalium Aquatilium. Leipzig; Gerhard Fleischer (1820).
Grande, T. & Young, B. The ontogeny and homology of the Weberian apparatus in the zebrafish Danio rerio (Ostariophysi: Cypriniformes). Zool. J. Linnean Soc. 140, 241-254 (2004).
Diogo, R. Origin, evolution and homologies of the Weberian apparatus: A new insight (Origen, evolución y homologías del aparato Weberiano: Un nuevo acercamiento). Int. J. Morphol. 27, 333-354 (2009).
Chardon, M. & Vandewalle, P. Evolutionary trends and possible origin of the Weberian apparatus. Neth. J. Zool. 47, 383-403 (1997).
Chardon, M., Parmentier, E. & Vandewalle, P. In Catfishes (eds G. Arratia, B. G. Kapoor, M. Chardon, & R. Diogo) 71-120, Science Publishers (2003).
Alexander, R. M. The structure of the Weberian apparatus in the Cyprini. Proc. Zool. Soc. Lond. 139, 451-473, https://doi.org/10.1111/j.1469-7998.1962.tb01839.x (1962).
von Frisch, K. The sense of hearing in fish. Nature 141, 8-11 (1938).
De Pinna, M. & Grande, T. Ontogeny of the Accessory Neural Arch in Pristigasteroid Clupeomorphs and Its Bearing on the Homology of the Otophysan Claustrum (Teleostei). Copeia, 838-845 (2003).
Grande, T. & de Pinna, M. in Mesozoic Fishes 3 - Systematics, Paleoenvironments and Biodiversity (eds G. Arratia & H-P. Schultze) 429-448 (2004).
Finneran, J. J. & Hastings, M. C. A mathematical analysis of the peripheral auditory system mechanics in the goldfish (Carassius auratus). J. Acoust. Soc. Am. 108, 1308-1321, https://doi.org/10.1121/1.1286099 (2000).
Popper, A. N. & Fay, R. R. Rethinking sound detection by fishes. Hear. Res. 273, 25-36 (2011).
Higgs, D. M., Rollo, A. K., Souza, M. J. & Popper, A. N. Development of form and function in peripheral auditory structures of the zebrafish (Danio rerio). J. Acoust. Soc. Am. 113, 1145-1154 (2003).
Lechner, W., Heiss, E., Schwaha, T., Glösmann, M. & Ladich, F. Ontogenetic development of weberian ossicles and hearing abilities in the african bullhead catfish. PLoS ONE 6 (2011).
Ladich, F. & Wysocki, L. E. How does tripus extirpation affect auditory sensitivity in goldfish? Hear. Res. 182, 119-129 (2003).
Yan, H. Y., Fine, M. L., Horn, N. S. & Colón, W. E. Variability in the role of the gasbladder in fish audition. J. Comp. Physiol. (A) 186, 435-445 (2000).
Lechner, W. & Ladich, F. Size matters: Diversity in swimbladders and Weberian ossicles affects hearing in catfishes. J. Exp. Biol. 211, 1681-1689 (2008).
Planquette, P., Keith, P. & Le Bail, P.-Y. Atlas des poissons d'eau douce de Guyane. Tome 1., Publications scientifiques du Muséum national d'Histoire Naturelle (1996).
Anderson, J. T., Rojas, S. J. & Flecker, A. S. High-quality seed dispersal by fruit-eating fishes in Amazonian floodplain habitats. Oecol. 161, 279-290 (2009).
Lucas, C. M. Within flood season variation in fruit consumption and seed dispersal by two characin fishes of the Amazon. Biotropica 40, 581-589 (2008).
Ortí, G., Sivasundar, A., Dietz, K. & Jégu, M. Phylogeny of the Serrasalmidae (Characiformes) based on mitochondrial DNA sequences. Genet. Mol. Biol. 31, 343-351 (2008).
Thompson, A. W., Betancur-R, R., Lopez-Fernandez, H. & Orti, G. A time-calibrated, multi-locus phylogeny of piranhas and pacus (Characiformes: Serrasalmidae) and a comparison of species tree methods. Mol. Phylogenet. Evol. 81, 242-257 (2014).
Millot, S., Vandewalle, P. & Parmentier, E. Sound production in red-bellied piranhas (Pygocentrus nattereri, Kner): An acoustical, behavioural and morphofunctional study. J. Exp. Biol. 214, 3613-3618 (2011).
Markl, H. Sound production in piranhas (Serrasalminae, Characidae). Z. vergl. Physiologie 74, 39-56 (1971).
Mélotte, G., Vigouroux, R., Michel, C. & Parmentier, E. Interspecific variation of warning calls in piranhas: A comparative analysis. Sci. Rep. 6, https://doi.org/10.1038/srep36127 (2016).
Popper, A. N., Ramcharitar, J. & Campana, S. E. Why otoliths? Insights from inner ear physiology and fisheries biology. Mar. Freshwater Res. 56, 497-504 (2005).
Higgs, D. M., Souza, M. J., Wilkins, H. R., Presson, J. C. & Popper, A. N. Age- and size-related changes in the inner ear and hearing ability of the adult zebrafish (Danio rerio). JARO - J. Assoc. Res. Otolaryngol. 3, 174-184 (2001).
Stabentheiner, A. Correlations between hearing and sound production in piranhas. J. Comp. Physiol. (A) 162, 67-76 (1988).
Ladich, F. Did auditory sensitivity and vocalization evolve independently in otophysan fishes? Brain Behav. Evol. 53, 288-304 (1999).
Wysocki, L. E. & Ladich, F. Can fishes resolve temporal characteristics of sounds? New insights using auditory brainstem responses. Hear. Res. 169, 36-46 (2002).
Ladich, F. & Popper, A. N. Comparison of the inner ear ultrastructure between teleost fishes using different channels for communication. Hear. Res. 154, 62-72, https://doi.org/10.1016/S0378-5955(01)00217-9 (2001).
Markl, H. Aggression and prey capture in piranhas (Serrasalminae, Characidae). Z. Tierpsychol. 30, 190-216 (1972).
Andersen, R. A. & Enger, P. S. Microphonic potentials from the sacculus of a teleost fish. Comp. Biochem. Physiol. 27, 879-881 (1968).
Enger, P. S., Hawkins, A. D., Sand, O. & Chapman, C. J. Directional sensitivity of saccular microphonic potentials in the haddock. J. Exp. Biol. 59, 425-433 (1973).
Fay, R. R. & Edds-Walton, P. L. Diversity in frequency response properties of saccular afferents of the toadfish. Opsanus tau. Hear. Res. 113, 235-246, https://doi.org/10.1016/S0378-5955(97)00148-2 (1997).
Popper, A. N. & Schilt, C. R. In Fish Bioacoustics Vol. 32 (eds J. Webb, R. Fay, & A. Popper) 17-48, Springer Handbook of Auditory Research (2008).
Schulz-Mirbach, T., Ladich, F., Plath, M., Metscher, B. D. & Heß, M. Are accessory hearing structures linked to inner ear morphology? Insights from 3D orientation patterns of ciliary bundles in three cichlid species. Front. Zool. 11 (2014).
Bird, N. C. & Hernandez, L. P. Morphological variation in the Weberian apparatus of cypriniformes. J. Morphol. 268, 739-757 (2007).
Watson, J. M. The development of the Weberian ossicles and anterior vertebrae in the goldfish. Proc. R. Soc. Lond. (Biol.) 127, 452-472 (1939).
Radermaker, F., Surlemont, C., Sanna, P., Chardon, M. & Vandewalle, P. Ontogeny of the Weberian apparatus of Clarias gariepinus (Pisces Siluriformes). Can. J. Zool. 67, 2090-2097 (1989).
Popper, A. N. The effects of size on auditory capacities of the goldfish. J. Aud. Res. 11, 239-247 (1971).
Jégu, M., Keith, P. & Belmonte-Jégu, E. A new species of Tometes (Teleostei: Characidae: Serrasalminae) from the Guianian shield, Tometes lebaili n. sp. BFPP - Bull. Fr. Peche Prot. Milieux Aquat., 23-48 (2002).
Jégu, M., Dos Santos, G. M., Keith, P. & Le Bail, P. Y. Supplementary description and rehabilitation of Tometes trilobatus Valenciennes, 1850, type-species of Tometes Valenciennes (Characidae: Serrasalminae). Cybium 26, 99-122 (2002).
Lugli, M. The tradeoff between signal detection and recognition rules auditory sensitivity under variable background noise conditions. J. Theor. Biol. 386, 1-6, https://doi.org/10.1016/j.jtbi.2015.08.033 (2015).
Kenyon, T. N., Ladich, F. & Yan, H. Y. A comparative study of hearing ability in fishes: The auditory brainstem response approach. J. Comp. Physiol. (A) 182, 307-318 (1998).
Corwin, J. T., Bullock, T. H. & Schweitzer, J. The auditory brain stem response in five vertebrate classes. Electroencephalogr. Clin. Neurophysiol. 54, 629-641, https://doi.org/10.1016/0013-4694(82)90117-1 (1982).
Parmentier, E., Colleye, O. & Mann, D. Hearing ability in three clownfish species. J. Exp. Biol. 212, 2023-2026 (2009).
Colleye, O., Kéver, L., Lecchini, D., Berten, L. & Parmentier, E. Auditory evoked potential audiograms in post-settlement stage individuals of coral reef fishes. J. Exp. Mar. Biol. Ecol. 483, 1-9 (2016).