Abstract
Evidence suggests that the capacity for sound source localization is common to mammals, birds, reptiles, and amphibians, but surprisingly it is not known whether fish locate sound sources in the same manner (e.g., combining binaural and monaural cues) or what computational strategies they use for successful source localization. Directional hearing and sound source localization in fishes continues to be important topics in neuroethology and in the hearing sciences, but the empirical and theoretical work on these topics have been contradictory and obscure for decades. This chapter reviews the previous behavioral work on directional hearing and sound source localization in fishes including the most recent experiments on sound source localization by the plainfin midshipman fish (Porichthys notatus), which has proven to be an exceptional species for fish studies of sound localization. In addition, the theoretical models of directional hearing and sound source localization for fishes are reviewed including a new model that uses a time-averaged intensity approach for source localization that has wide applicability with regard to source type, acoustic environment, and time waveform.
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References
Bass AH, Clark CW (2003) The physical acoustics of underwater sound communication. In: Simmons AM, Fay RR, Popper AN (eds) Acoustic communication. Springer, New York, pp 1–64
Bass AH, McKibben JR (2003) Neural mechanisms and behaviors for acoustic communication in teleost fish. Prog Neurobiol 69:1–26
Bass AH, Bodnar D, Marchaterre MA (1999) Complementary explanations for existing phenotypes in an acoustic communication system. In: Hauser MD, Konishi M (eds) The design of animal communication. MIT Press, Cambridge, pp 493–514
Beranek LL (1954) Acoustics. McGraw-Hill, New York
Brantley RK, Bass AH (1994) Alternative male spawning tactics and acoustic signals in the plainfin midshipman fish Porichthys notatus. Girard (teleostei, Batrachoididae). Ethology 96:212–232
Bregman AS (1990) Auditory scene analysis. The perceptual organisation of sound. MIT Press, Cambridge
Brown AD, Mussen TD, Sisneros JA, Coffin AB (2011) Reevaluating the use of aminoglycoside antibiotics in behavioral studies of the lateral line. Hear Res 272:1–4
Buwalda RJA (1981) Segregation of directional and nondirectional acoustic information in the cod. In: Tavolga WN, Popper AN, Fay RR (eds) Hearing and sound communication in fishes. Springer, New York, pp 139–171
Buwalda RJA, Schuijf A, Hawkins AD (1983) Discrimination by the cod of sounds from opposing directions. J Comp Physiol A 150:175–184
Chapman CJ (1973) Field studies of hearing in teleost fish. Helgoländer wiss Meeresunters 24:371–390
Chapman CJ, Hawkins AD (1973) A field study of hearing in the cod, Gadus morhua L. J Comp Physiol 85:147–167
Chapman CJ, Johnstone ADF (1974) Some auditory discrimination experiments on marine fish. J Exp Biol 61:521–528
Chapman CJ, Sand O (1974) Field studies of hearing in two species of flatfish Pleuronectes platessa (L.) and Limanda limanda (L.) (family pleuronectidae). Comp Biochem Physiol A 47:371–385
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 fishes. J Exp Biol 217:2078–2088
de Vries HL (1950) The mechanics of the labyrinth otoliths. Acta Otolaryngol 38:262–273
Delco EA (1960) Sound discrimination by males of two cyprinid fishes. Tex J Sci 12:48–54
Dijkgraaf S (1960) Hearing in bony fishes. Proc R Soc B 152:51–54
Edds-Walton PL, Fay RR, Highstein SM (1999) Dendritic arbors and central projections of auditory fibers from the saccule of the toadfish (Opsanus tau). J Comp Neurol 411:212–238
Fay RR (1984) The goldfish ear codes the axis of acoustic particle motion in three dimensions. Science 225(951):954
Fay RR (1998) Auditory stream segregation in goldfish (Carassius auratus). Hear Res 120:69–76
Fay RR (2000) Frequency contrasts underlying auditory stream segregation in goldfish. J Assoc Res Otolaryngol 1:20–128
Fay RR (2005) Sound source localization in fishes. In: Fay RR, Popper AN (eds) Springer handbook of auditory research: sound source localization. Springer, New York, pp 36–66
Fay RR, Edds-Walton PL (1997) Directional response properties of saccular afferents of the toadfish, Opsanus tau. Hear Res 111:1–21
Fine ML, Winn HE, Joest L, Perkins PJ (1977) Temporal aspects of calling behavior in the oyster toadfish, Opsanus tau. Fish Bull 75:871–874
Fraenkel GS, Gunn DL (1961) The orientation of animals. Dover, New York
Furshpan EJ, Furukawa T (1962) Intracellular and extracellular responses of the several regions of the Mauthner cell of the goldfish. J Neurophysiol 25:732–771
Gerald JW (1971) Sound production during courtship in six species of sunfish (Centrachidae). Evolution 25:75–87
Grothe B, Pecka M, McAlpine D (2010) Mechanisms of sound localization in mammals. Physiol Rev 90:983–1012
Harris GG, van Bergeijk WA (1962) Evidence that the lateral line organ responds to near-field displacements of sound sources in water. J Acoust Soc Am 34:1831–1841
Hawkins AD, Sand O (1977) Directional hearing in the median vertical plane by the cod. J Comp Physiol A 122:1–8
Hirsh IJ (1948) The influence of interaural phase on interaural summation and inhibition. J Acoust Soc Am 20:536–544
Hulse SH, MacDougall-Shackleton SA, Wisniewski AB (1997) Auditory scene analysis by songbirds: stream segregation of birdsong by European starlings (Sturnus vulagris). J Comp Psychol 111:3–13
Ibara RM, Penny LT, Ebeling AW, van Dykhuizen G, Cailliet G (1983) The mating call of the plainfin midshipman fish, Porichthys notatus. In: Noakes DGL, Lindquist DG, Helfman GS, Ward JA (eds) Predators and prey in fishes. Junk Press, The Hague, pp 205–212
Janssen J (2000) Toxicity of Co2+: implications for lateral line studies. J Comp Physiol A 186:957–960
Jensen FB, Kuperman WA, Porter MB, Schmidt H (2011) Computational ocean acoustics, 2nd edn. Eq. 2.205. Springer, New York
Kalmijn AJ (1997) Electric and near-field acoustic detection, a comparative study. Acta Physiol Scand 161(Suppl 638):25–38
Kaus S (1987) The effect of aminoglycoside antibiotics on the lateral line organ of Aplocheilus lineatus (Cyprinodontidae). Acta Otolaryngol 103:291–298
Ladich F, Myrberg AA (2006) Agonistic behaviour and acoustic communication. In: Ladich F, Collin SP, Moller P, Kapoor BG (eds) Communication in fishes. Science Publishers, Enfield, pp 122–148
Lu Z, Xu Z, Buchser WJ (2003) Acoustic response properties of lagenar nerve fibers in the sleeper goby, Dormitator latifrons. J Comp Physiol A 189:889–905
Lu Z, Xu Z, Buchser WJ (2004) Coding of acoustic particle motion by utricular afferents of the sleeper goby, Dormitator latifrons. J Comp Physiol A 190:923–938
Mann DA, Lu Z, Popper AN (1997) Ultrasound detection by a teleost fish. Nature 389:341
Mann DA, Lu Z, Hastings MC, Popper AN (1998) Detection of ultrasonic tones and simulated dolphin echolocation clicks by a teleost fish, the American shad (Alosa sapidissima). J Acoust Soc Am 104:562–568
McKibben JR, Bass AH (1998) Behavioral assessment of acoustic parameters relevant to signal recognition and preference in a vocal fish. J Acoust Soc Am 104:3520–3533
McKibben JR, Bass AH (2001) Effects of temporal envelope modulation on acoustic signals in a vocal fish: harmonic and beat stimuli. J Acoust Soc Am 109:2934–2943
Meyer M, Fay RR, Popper AN (2010) Frequency tuning and intensity coding of sound in the auditory periphery of the lake sturgeon, Acipenser fulvescens. J Exp Biol 213:1567–1578
Meyer M, Popper AN, Fay RR (2012) Coding of sound direction in the auditory periphery of the lake sturgeon, Acipenser fulvescens. J Neurophysiol 107:658–665
Montgomery JC, Baker CF, Carton AG (1997) The lateral line can mediate rheotaxis in fish. Nature 38:960–963
Moulton JM, Dixon RH (1967) Directional hearing in fishes. In: Tavolga WN (ed) Marine bioacoustics, vol 2. Pergamon Press, New York, pp 187–228
Myrberg AA (1981) Sound communication and interception in fishes. In: Tavolga WN, Popper AN, Fay RR (eds) Hearing and sound communication in fishes. Springer, New York, pp 395–426
Myrberg AA, Lugli M (2006) Reproductive behavior and acoustical interactions. In: Ladich F, Collin SP, Moller P, Kapoor BG (eds) Communication in fishes, vol 1. Science Publishers, Enfield, NH, pp 149–176
Myrberg AA, Spires JY (1972) Sound discrimination by the bicolor damselfish, Eupomacentrus partitus. J Exp Biol 57:727–735
Nelson DR, Gruber SH (1963) Sharks: attraction by low-frequency sounds. Science 142:975–977
Nelson DR, Johnson RH (1972) Acoustic attraction of pacific reef sharks: effect of pulse intermittency and variability. Comp Biochem Physiol A 42:85–90
Pierce AD (1981) Acoustics: an introduction to its physical principles and applications. McGraw-Hill, NY
Platt C, Popper AN (1981) Fine structure and function of the ear. In: Tavolga WN et al (eds) Hearing and sound communication in fishes. Spring-Verlag, New York, pp 3–38
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, Salmon A, Parvulescu A (1973) Sound localization by the Hawaiian squirrelfishes, Myripristis berndti and M. argyromus. Anim Behav 21:86–97
Reinhardt F (1935) Uber Richtungswharnehmung bei Fischen, besonders bei der Elritze (Phoxinus laevis L.) und beim Zwergwels (Amiurus nebulosus Raf.). Z Vergl Physiol 22:570–603
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 Verlag, New York, pp 131–149
Rogers PH, Zeddies DG (2008) Multipole mechanisms for directional hearing in fish. In: Webb JF, Popper AN, Fay RR (eds) Fish bioacoustics. Springer, New York, pp 233–252
Rogers PH, Popper AN, Cox M, Saidel WM (1988) Processing of acoustic signals in the auditory system of bony fish. J Acoust Soc Am 83:338–349
Sand O (1974) Directional sensitivity of microphonic potentials from the perch ear. J Exp Biol 60:881–899
Sand O, Enger PS (1973) Evidence for an auditory function of the swimbladder in the cod. J Exp Biol 59:405–414
Schellart NAM, de Munck JC (1987) A model for directional and distance hearing in swim bladder-bearing fish based on the displacement orbits of the hair cells. J Acoust Soc Am 82:822–829
Schuijf A (1975) Directional hearing of cod (Gadus morhua) under approximate free field conditions. J Comp Physiol A 98:307–332
Schuijf A, Buwalda RJA (1975) On the mechanism of directional hearing in cod (Gadus morhua). J Comp Physiol A 98:333–344
Schuijf A, Hawkins AD (1983) Acoustic distance discrimination by the cod. Nature 302:143–144
Schuijf A, Baretta JW, Wildschut JT (1971) A field investigation on the discrimination of sound direction in Labrus berggylta (Pisces: Perciformes). Netherl J Zool 22:81–105
Schuijf A, Visser C, Willers A, Buwalda RJ (1977) Acoustic localization in an ostariophysine fish. Experientia 33:1062–1063
Tavolga WN (1958) The significance of underwater sounds produced by males of the gobiid fish, Bathygobius soporator. Physiol Zool 31:259–271
Tytler P, Blaxter JHS (1977) The effect of swimbladder deflation on pressure sensitivity in the saithe Pollachius virens. J Mar Biol Assoc UK 57:1057–1064
Urick R (1967) Principles of underwater sound for engineers. McGraw Hill, New York
van Bergeijk WA (1964) Directional and nondirectional hearing in fish. In: Tavolga WA (ed) Marine bioacoustics. Pergamon Press, London, pp 269–301
van Bergeijk WA (1967) The evolution of vertebrate hearing. In: Neff WD (ed) Contributions to sensory physiology, vol 2. Academic, New York, pp 1–49
Van Trump WJ, Coombs S, Duncan K, McHenry MJ (2010) Gentamicin is ototoxic to all hair cells in the fish lateral line system. Hear Res 261:42–50
von Frisch K, Dijkgraaf S (1935) Can fish perceive sound direction? Z Vergl Physiol 22:641–655
Winn HE (1972) Acoustic discrimination by the toadfish with comments on signal systems. In: Winn HE, Olla BL (eds) Behavior of marine animals volume 2: vertebrates. Plenum, New York, pp 361–385
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(5):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, Porichthys notatus. J Exp Biol 215:152–160
Acknowledgements
The authors would like to thank Drs. Arthur Popper and Richard Fay for their support, mentorship, and collegiality over the course of our collective careers. Both of the authors (JAS and PHR) have had the privilege to work with Dick and Art through various projects and conferences and we are very grateful for their guidance and patience.
Art Popper has been a good friend and biology guru to PHR for over 35 years. (It could have been over 50 years since Art and PHR attended the same NYC high school at the same time.) Back in 1980 Art contacted John Munson, the Superintendent of the NRL Acoustics Division, seeking some help with a tank-acoustics issue. As fate would have it, of the some 200 acousticians at NRL, Munson chose PHR to help with Art’s problem. When PHR visited his lab at Georgetown University, Art explained how a fish’s ear consisted of orthogonal dipole sensors and a collocated monopole sensor. PHR immediately recognized this as being identical to a Navy DIFAR sonar and PHR became obsessed with the idea that since fish were apparently 600 million years ahead of the Navy in sonar design that perhaps they had come up with other concepts that the Navy had yet to discover. From then on PHR was hooked on fish bioacoustics.
Dick Fay has been a great friend and mentor to JAS ever since the first day JAS met Dick outside the Rowe Laboratory at the Marine Biological Laboratory (MBL) in Woods Hole, MA during a smoking break in the summer of 2003. Dick provided the mentorship that allowed JAS to co-PI an NSF grant to investigate sound source localization by the midshipman fish at the Bodega Marine Lab from 2007 to 2011. In addition, JAS had the fortunate opportunity to collaborate with Dick at the Parmly Hearing Institute in Chicago, IL during the spring of 2008 and 2010 and at the MBL in Woods Hole, MA during the summers of 2011 and 2012. During these wonderful times of collaboration, JAS learned from Dick not only how to become a better scientist but also how to appreciate fine food and music, especially the jazz music of Art Tatum.
Research in the Sisneros Lab was supported by an NSF grant (IOS 0642214).
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Sisneros, J.A., Rogers, P.H. (2016). Directional Hearing and Sound Source Localization in Fishes. 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_7
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