Abstract
Examination of fish responses to sound stimuli has a rich and varied history but it is not always clear when responses are true measures of hearing or the lateral-line. The central innervation of auditory and lateral-line sensory afferents lie in close proximity in the brainstem and both sets of receptors are, at heart, hair cell-based particle motion detectors. While it is possible to separately measure physiological activity of these two receptor subtypes, many studies of fish “hearing” use whole brain potentials or behavioural assays in complex sound fields where it is not possible to distinguish inputs. We argue here that, as often measured, what is thought of as fish “hearing” is often a multisensory response of both auditory and lateral line receptors. We also argue that in many situations where fish use sound stimuli, the behaviour is also an integrative response of both systems, due to the often close proximity of fish during sound communication. We end with a set of recommendations for better understanding the separate and combined roles of ear and lateral-line hair cells as well as an acknowledgment of the seminal and continuing contributions of Arthur N. Popper and Richard R. Fay to this field.
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References
Akamatsu T, Okumura T, Novarini N, Yan HY (2002) Empirical refinements applicable to the recording of fish sounds in small tanks. J Acoust Soc Am 112:3073–3082
Amorim MCP, Vasconcelos RO (2008) Variability in the mating calls of the Lusitanian toadfish Halobatrachus didactlyus: cues for potential individual recognition. J Fish Biol 73:1267–1283
Au WWL, Hastings MC (2008) Principles of marine bioacoustics. Springer, New York
Brack CL, Ramcharitar J (2012) Assessment of lateral line function: a potential technique for studies in ototoxicity. J Clin Neurosci 19:333–335
Brantley RK, Bass AH (1994) Alternative male spawning tactics and acoustic signals in the plainfin midshipman fish Porichthys notatus Girard (Teleostei, Batrachoididae). Ethology 96:213–232
Braun CB (2002) What is the nature of multisensory interaction between octavolateralis sub-systems. Brain Behav Evol 59:162–176
Brown AD, Mussen TD, Sisneros JA, Coffin AB (2011) Reevaluating the use of aminoglycoside antibiotics in behavioral studies of the lateral line. Hear Res 272:1–2
Caiger PE, Montgomery JC, Bruce M, Lu J, Radford CA (2013) A proposed mechanism for the observed ontogenetic improvement in the hearing ability of hapuka (Polyprion oxygeneios). J Comp Phys A 199:653–661
Canfield JG, Rose GJ (1996) Hierarchical sensory guidance of Mauthner-mediated escape responses in goldfish (Carassius auratus) and cichlids (Haplochromis burtoni). Brain Behav Evol 48:137–156
Chapman CJ (1973) Field studies of hearing in teleost fish. Helgolander wiss Meeresunters 24:371–390
Chapman CJ, Hawkins AD (1973) A field study of hearing in the cod, Gadus morhua. J Comp Physiol 85:147–167
Chapman CJ, Sand O (1974) Field studies of hearing in two species of flatfish Pleuronectes platessa (L.) and Limnada limnada (L.) (Family Pleuronectidae). Comp Biochem Physiol 47A:371–385
Coffin AB, Zeddies DG, Fay RR, Brown AD, Alderks PW, Bhandiwad AA, Mohr RA, Gray MD, Rogers PH, Sisneros JA (2014) Use of the swim bladder and lateral line in near-field sound source localization by fish. J Exp Biol 217:2078–2088
Corwin JT, Bullock TH, Schweitzer J (1982) The auditory brain stem response in five vertebrate classes. Electroencephalogr Clin Neurophysiol 54:629–641
Eaton RC, Popper AN (1995) The octavolateralis system and Mauthner cell: interactions and questions. Brain Behav Evol 46:124–130
Eaton RC, Bombardier RA, Meyer DL (1977) The Mauthner-initiated startle response in teleost fish. J Exp Biol 66:65–81
Eaton RC, Lee RKK, Foreman MB (2001) The Mauthner cell and other identified neurons of the brainstem escape network of fish. Prog Neurobiol 63:467–485
Egner SA, Mann DA (2005) Auditory sensitivity of sergeant major damselfish Abudefduf saxatilis from post-settlement juvenile to adult. Mar Ecol Prog Ser 285:213–222
Fay R (2009) Soundscapes and the sense of hearing of fishes. Integr Zool 4:26–32
Fay RR, Feng AS (1987) Mechanisms for directional hearing among nonmammalian vertebrates. In: Yost WA, Gourevitch G (eds) Directional hearing. Springer, New York, pp 179–211
Fay RR, Megela Simmons A (1999) The sense of hearing in fishes and amphibians. In: Fay RR, Popper AN (eds) Comparative hearing: fish and amphibians. Springer, New York, pp 269–318
Fay RR, Popper AN (2012) Fish hearing: new perspectives from two “senior” bioacousticians. Brain Behav Evol 792:215–217
Fine ML, Lehnardt ML (1983) Shallow-water propagation of the toadfish mating call. Comp Biochem Physiol 76A:225–231
Fine ML, Perini MA (1994) Sound production evoked by electrical stimulation of the forebrain in the oyster toadfish. J Comp Physiol A 174:173–185
Forrest TG, Miller GL, Zagar JR (1993) Sound propagation in shallow water: implications for acoustic communication by aquatic animals. Bioacoustics 4:259–270
Gray GA, Winn HE (1961) Reproductive ecology and sound production of the toadfish, Opsanus tau. Ecology 42:274–282
Higgs DM, Lui, Z, Mann DA (2006) Hearing and mechanoreception. In: Evans DH (ed) The physiology of fishes, 3rd edn. CRC Press, pp 391–429
Higgs DM, Radford CA (2013) The contribution of the lateral line to “hearing” in fish. J Exp Biol 216:1484–1490
Higgs DM, Souza MJ, Wilkins HR, Presson JC, Popper AN (2002) Age related changes in the inner ear and hearing ability of the adult zebrafish (Danio rerio). J Assoc Res Otolaryngol 3:174–184
Higgs DM, Rollo AK, Souza MJ, Popper AN (2003) Development of form and function in peripheral auditory structures of the zebrafish (Danio rerio). J Acoust Soc Am 113:1145–1154
Horch K, Salmon M (1973) Adaptations to the acoustic environment by the squirrelfishes Myripristis violaceus and M. pralinius. Mar Behav Physiol 2:121–139
Janssen J (2000) Toxicity of Co2+: implications for lateral line studies. J Comp Physiol A 186:957–960
Johnston CE, Bolling MK, Holt DE, Phillips CT (2008) Production of acoustic signals during aggression in Coosa bass, Micropterus coosae. Environ Biol Fish 82:17–20
Kenyon TN (1996) Ontogenetic changes in the auditory sensitivity of damselfishes (Pomacentridae). J Comp Physiol A 179:553–561
Kenyon TN, Ladich F, Yan HY (1998) A comparative study of hearing ability in fishes: the auditory brainstem response approach. J Comp Physiol A 182:307–318
Ladich F (2004) Sound production and acoustic communication. In: von der Emde G, Mogdans J, Kapoor BG (eds) The senses of fish: adaptations for the reception of natural stimuli. Narosa Publishing, New Delhi, pp 210–230
Ladich F, Fay RR (2013) Auditory evoked potential audiometry in fish. Rev Fish Biol Fish 23:317–364
Leis JM, Carson-Ewart BM (2003) Orientation of pelagic larvae of coral-reef fishes in the ocean. Mar Ecol Prog Ser 252:239–253
Leis JM, Lockett MM (2005) Localization of reef sounds by settlement stage larvae of coral-reef fishes (Pomacentridae). Bull Mar Sci 76:715–724
Leis JM, Carson-Ewart BM, Cato DH (2002) Sound detection in situ by the larvae of a coral-reef damselfish (Pomacentridae). Mar Ecol Prog Ser 232:259–268
Lévêque C, Oberdoff T, Paugy D, Stiassny MLJ, Tedesco PA (2008) Global diversity of fish (Pisces) in freshwater. Hydrobiologia 595:545–567
Lugli M, Fine ML (2003) Acoustic communication in two freshwater gobies: ambient noise and short-range propagation in shallow streams. J Acoust Soc Am 114:512
Lugli M, Fine ML (2007) Stream ambient noise, spectrum and propagation of sounds in the goby Padogobius martensii: sound pressure and particle velocity. J Acoust Soc Am 122:2881–2892
Mann DA, Lobel PS (1997) Propagation of damselfish (Pomacentridae) courtships sounds. J Acoust Soc Am 101:3783
Maruska KP, Boyle KS, Dewan LR, Tricas TC (2007) Sound production and spectral hearing sensitivity in the Hawaiian sergeant damselfish, Abudefduf abdominalis. J Exp Biol 210:3990–4004
Mccormick CA (1999) Anatomy of the central auditory pathways of fish and amphibians. In: Comparative hearing: fish and amphibians. Springer, New York, pp 155–217
Mirjany M, Preuss T, Faber DS (2011) Role of the lateral line mechanosensory system in directionality of goldfish auditory evoked escape response. J Exp Biol 214:3358–3367
Montgomery J, Coombs SL, Halstead M (1995) Biology of the mechanosensory lateral line in fishes. Rev Fish Biol Fish 5:399–416
Montgomery JC, Tolimieri N, Haine OS (2001) Active habitat selection by pre-settlement reef fishes. Fish Fish 2:261–277
Montgomery JC, Jeffs A, Simpson SD, Meekan M, Tindle C (2006) Sound as an orientation cue for the pelagic larvae of reef fishes and decapod crustaceans. Adv Mar Biol 51:143–196
Moulton JM, Dixon RH (1967) Directional hearing in fishes. Mar Bioacoust 2:187–228
Myrber AA, Spires JY (1972) Sound discrimination by the bicolor damselfish, Eupomacentrus partitus. J Exp Biol 57:727–735
Myrberg AA (1981) Sound communication and interception in fishes. In: Popper AN, Fay RR (eds) Hearing and sound communication in fishes. Springer, New York, pp 395–426
Myrberg AA, Banner A, Richard JD (1969) Shark attraction using a video-acoustic system. Mar Biol 2:264–276
Nelson EM, Gruber SH (1963) Sharks: attraction by low-frequency sounds. Science 142:975–977
Niemiller ML, Higgs DM, Soares D (2013) Evidence for hearing loss in amblyopsid cavefishes. Biol Lett 9. doi:10.1098/rsbl.2013.0104
Parvulescu A (1967) The acoustics of small tanks. Mar Bioacoust 2:7–13
Popper AN, Fay RR (1973) Sound production and processing by teleost fishes: a critical review. J Acoust Soc Am 53:1515–1529
Popper AN, Fay RR (1993) Sound detection and processing by fish: critical review and major research questions. Brain Behav Evol 41:14–38
Popper AN, Fay RR (1997) Evolution of the ear and hearing: issues and questions. Brain Behav Evol 50:213–221
Popper AN, Fay RR (1999) Comparative hearing: fish and amphibians. Springer, New York
Radford CA, Mensinger AF (2014) Anterior lateral line nerve encoding to tones and play-back vocalisations in free-swimming oyster toadfish, Opsanus tau. J Exp Biol 217:1570–1579
Radford CA, Tindle CT, Montgomery JC, Jeffs AG (2011) Modelling a reef as an extended sound source increases the predicted range at which reef noise may be heard by fish larvae. Mar Ecol Prog Ser 438:167–174
Radford CA, Montgomery JC, Caiger P, Higgs DM (2012) Pressure and particle motion detection thresholds in fish: a re-examination of salient auditory cues in teleosts. J Exp Biol 215:3429–3435
Radford CA, Montgomery JC, Caiger P, Johnston P, Lu J, Higgs DM (2013) A novel hearing specialization in the New Zealand bigeye, Pempheris adspersa. Biol Lett 9:21020163
Rogers PH, Cox M (1988) Underwater sound as a biological stimulus. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, New York, pp 131–149
Sand O, Bleckmann H (2008) Orientation to auditory and lateral line stimuli. In: Webb JF, Popper AN, Fay RR (eds) Fish bioacoustics. Springer, New York, pp 183–231
Simpson SD, Meekan MG, McCauley RD, Jeffs A (2004) Attraction of settlement-stage coral reef fishes to reef noise. Mar Ecol Prog Ser 276:263–268
Simpson SD, Meekan MG, Montgomery JC, McCauley RD, Jeffs A (2005) Homeward sound. Science 308:221
Tavolga WN (1958) Underwater sounds produced by two species of toadfish, Opsanus tau and Opsanus beta. Bull Mar Sci 8:278–284
Tolimieri N, Jeffs A, Montgomery JC (2000) Ambient sound as a cue for navigation by the pelagic larvae of reef fishes. Mar Ecol Prog Ser 207:219–224
Tolimieri N, Haine O, Montgomery JC, Jeffs A (2002) Ambient sound as a navigational cue for larval reef fish. Bioacoustics 12:214–217
Tolimieri N, Haine O, Jeffs A, McCauley R, Montgomery JC (2004) Directional orientation of pomacentrid larvae to ambient reef sound. Coral Reefs 23:184–191
Torricelli P, Romani R (1986) Sound production in the Italian freshwater goby, Padogobius martensi. Copeia 1986:213–216
Torricelli P, Lugli M, Pavan G (1990) Analysis of sounds produced by male Padogobius martensi (Pisces, Gobiidae) and factors affecting their structural properties. Bioacoustics 2:261–275
van Bergeijk WA (1964) Directional and nondirectional hearing in fish. Mar Bioacoust 1:281–299
Webb JF (1998) Laterophysic connection: a unique link between the swimbladder and the lateral line system in Chaetodon (Perciformes: Chaetodontidae). Copeia 1998:1032–1036
Webb JF, Smith WL (2000) The laterophysic connection in chaetodontid butterflyfish: morphological variation and speculations on sensory function. Philos Trans R Soc B 355:1125–1129
Weeg MS, Bass AH (2002) Frequency response properties of lateral line superficial neuromasts in a vocal fish, with evidence for acoustic sensitivity. J Neurophysiol 88:1252–1262
Wilson CJ, Wilson PS, Greene CA, Dunton KH (2013) Seagrass meadows provide an acoustic refuge for estuarine fish. Mar Ecol Prog Ser 472:117–127
Wright K, Higgs DM, Belanger AJ, Leis J (2005) Auditory and olfactory abilities of pre-settlement larvae and post-settlement juveniles of a coral reef damselfish (Pisces: Pomacentridae). Mar Biol 147:1425–1434
Wright K, Higgs DM, Leis J (2008) Auditory and olfactory abilities of larvae of the Indo-Pacific Coral Trout Plectropomus leopardus (Pisces: Serranidae) at settlement. J Fish Biol 72:2543–2556
Wright K, Higgs DM, Leis J (2011) Ontogenetic and interspecific variation in hearing ability in marine fish larvae. Mar Ecol Prog Ser 424:1–13
Wysocki LE, Ladich F (2003) The representation of conspecific sounds in the auditory brainstem of teleost fishes. J Exp Biol 206:2229–2240
Yan HY, Fine ML, Horn NS, Colón WE (2000) Variability in the role of the gasbladder in fish audition. J Comp Physiol 186:435–445
Zeddies DG, Fay RR, Alderks PW, Shaub KS, Sisneros JA (2010) Sound source localization by the plainfin midshipman fish, Porichthys notatus. J Acoust Soc Am 127:3104–3113
Zeddies DG, Fay RR, Gray MD, Alderks PW, Acob A, Sisneros JA (2012) Local acoustic particle motion guides sound-source localization behavior in the plainfin midshipman fish, Porichthyes notatus. J Exp Biol 215:152–160
Zelick R, Mann DA, Popper AN (1999) Acoustic communication in fishes and frogs. In: Fay RR, Popper AN (eds) Comparative hearing: fish and amphibians. Springer, New York, pp 363–411
Acknowledgements
Drs. Arthur Popper and Richard Fay have been the guiding influence for much of the field of fish bioacoustics throughout their careers and have advanced the field by their own primary research work as well as by the numerous commentary papers and compendia they have put together over the years. Art was a valued mentor for DH during a critical phase of his scientific career and acted as a true mentor as a scientist and as an academic. The time spent in Popper’s lab continues to influence DH and contribute to his approach to science and mentoring. Dr. Fay was also an important sounding board for DH during his time as a postdoctoral fellow and, while DH never had the opportunity to work directly in Fay’s lab he always appreciated the feedback and assistance when their paths crossed. While CR has not had the opportunity to work directly with either of Dr. Popper or Fay, they have really provided the foundation behind his work in understanding how larval marine fish use underwater sound as an orientation cue. In saying that, Dr. Popper has always supported CR’s work through invitations and support to attend conferences.
The authors also gratefully appreciate the work of Ms. Meghan Donovan for drawing images for Figs. 3 and 4, Mr. Peter Johnston (MD) for the work on the CT-Scan images and two anonymous reviewers for many constructive comments on an earlier draft of this manuscript.
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Higgs, D.M., Radford, C.A. (2016). The Potential Overlapping Roles of the Ear and Lateral Line in Driving “Acoustic” Responses. In: Sisneros, J. (eds) Fish Hearing and Bioacoustics. Advances in Experimental Medicine and Biology, vol 877. Springer, Cham. https://doi.org/10.1007/978-3-319-21059-9_12
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