[en] Adult female and nesting (type I) male midshipman fish (Porichthys notatus) exhibit an adaptive form of auditory plasticity for the enhanced detection of social acoustic signals. Whether this adaptive plasticity also occurs in “sneaker” type II males is unknown. Here, we characterize auditory-evoked potentials recorded from hair cells in the saccule of reproductive and non-reproductive “sneaker” type II male midshipman to determine whether this sexual phenotype exhibits seasonal, reproductive state-dependent changes in auditory sensitivity and frequency response to behaviorally relevant auditory stimuli. Saccular potentials were recorded from the middle and caudal region of the saccule while sound was presented via an underwater speaker. Our results indicate saccular hair cells from reproductive type II males had thresholds based on measures of sound pressure and acceleration (re. 1 μPa and 1 ms−2, respectively) that were ~8–21 dB lower than non-reproductive type II males across a broad range of frequencies, which include the dominant higher frequencies in type I male vocalizations. This increase in type II auditory sensitivity may potentially facilitate eavesdropping by sneaker males and their assessment of vocal type I males for the selection of cuckoldry sites during the breeding season.
Alderks PW, Sisneros JA (2011) Ontogeny of auditory saccular sensitivity in the plainfin midshipman fish, Porichthys notatus. J Comp Physiol A 197(4):387–398
Bass AH, Clark CW (2003) The physical acoustics of underwater sound communication. In: Simmons AM, Popper AN, Fay RR (eds) Acoustic communication. Springer, New York, pp 15–64
Bass AH, Ladich F (2008) Vocal–acoustic communication: from neurons to behavior. In: Webb JF, Popper AN, Fay RR (eds) Fish bioacoustics. Springer, New York, pp 253–278
Bass AH, McKibben JR (2003) Neural mechanisms and behaviors for acoustic communication in teleost fish. Progr Neurobiol 69(1): 1–26.
Bass AH, Bodnar DA, 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, Cambridge, pp 493–514
Blaxter JHS (1981) The swim bladder and hearing. In: Tavolga WN, Popper AN, Fay RR (eds) Hearing and sound communication in fishes. Springer, Berlin, pp 61–72
Brantley RK, Bass AH (1994) Alternative male spawning tactics and acoustic signals in the plainfin midshipman fish Porichthys notatus Girard (Teleostei, Batrachoididae). Ethology 96(3):213–232
Braun CB, Grande T (2008) Evolution of peripheral mechanisms for the enhancement of sound reception. In: Webb JF, Popper AN, Fay RR (eds) Fish bioacoustics, Springer, New York, pp 99–144
Casper BM, Mann DA (2006) Evoked potential audiograms of the nurse shark (Ginglymostoma cirratum) and the yellow stingray (Urobatis jamaicensis). Environ Biol Fish 76(1):101–108
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(1):371–385
Coffin AB, Mohr RA, Sisneros JA (2012) Saccular-specific hair cell addition correlates with reproductive state-dependent changes in the auditory saccular sensitivity of a vocal fish. J Neurosci 32(4):1366–1376
Cohen MJ, Winn HE (1967) Electrophysiological observations on hearing and sound production in the fish, Porichthys notatus. J Exp Zool 165(3):355–369
Coombs S, Popper AN (1979) Hearing differences among Hawaiian squirrelfish (family Holocentridae) related to differences in the peripheral auditory system. J Comp Physiol 132(3):203–207
De Vries HL (1950) The mechanics of the labyrinth otoliths. Acta Otolaryngol 38(3):262–273
Edds-Walton PL, Arruda J, Fay RR, Ketten DR (2015) Computerized tomography of the otic capsule and otoliths in the oyster toadfish, Opsanus tau. J Morphol 276(2):228–240
Fay RR (1984) The goldfish ear codes the axis of acoustic particle motion in three dimensions. Science 225(4665):951–954
Fay RR, Popper AN (1980) Structure and function in teleost auditory systems. In: Popper AN, Fay RR (eds) Comparative studies of hearing in vertebrates. Springer, Berlin, pp 3–42
Fay RR, Popper AN (2012) Fish hearing: new perspectives from two ‘senior’ bioacousticians. Brain Behav Evol 79(4):215–217
Fettiplace R, Fuchs PA (1999) Mechanisms of hair cell tuning. Annu Rev Physiol 61:809–834
Fine ML, Lenhardt ML (1983) Shallow-water propagation of the toadfish mating call. Comp Biochem Physiol A 76:225–231
Fine ML, Parmentier E (2015) Mechanisms of fish sound production. In: Ladich F (ed) Sound communication in fishes. Animal signals and communication, vol 4. Springer, Berlin, pp 77–126
Forlano PM, Sisneros JA, Rohmann KN, Bass AH (2015) Neuroendocrine control of seasonal plasticity in the auditory and vocal systems of fish. Front Neuroendocrinol 37:129–145.
Forlano PM, Maruska KP, Sisneros JA, Bass AH (2016) Hormone-dependent plasticity of auditory systems in fishes. In: Bass AH, Sisneros JA, Popper AN, Fay RR (eds) Hearing and hormones. Springer International, New York, pp 15–51
Greenwood PH (1970) Skull and swimbladder connections in the fishes of the family Megalopidae. Bull British Mus Nat Hist (Zool) 14:121–135
Grober MS, Fox SH, Laughlin C, Bass AH (1994) GnRH cell size and number in a teleost fish with two male reproductive morphs: sexual maturation, final sexual status and body size allometry. Brain Behav Evol 43(2):61–78
Hawkins AD (1993) Underwater sound and fish behavior. In: Pitcher TJ (ed) The behaviour of teleost fishes. Chapman and Hall, London, pp 114–151
Horodysky AZ, Brill RW, Fine ML, Musick JA, Latour RJ (2008) Acoustic pressure and particle motion thresholds in six sciaenid fishes. J Exp Biol 211(9):1504–1511
Jerko H, Turunen-Rise I, Enger PS, Sand O (1989) Hearing in the eel (Anguilla anguilla). J Comp Phys A 165(4):455–459
Kelley DB, Bass AH (2010) Neurobiology of vocal communication: mechanisms for sensorimotor integration and vocal patterning. Curr Opin Neurobiol 20(6):748–753
Ladich F (2004) Sound production and acoustic communication. In: von der Emde G, Mogdans J, Kapoor BG (eds) The senses of fishes: adaptations for the reception of natural stimuli. Narosa Publishing House Pvt Ltd, New Delhi, pp 210–230
Lewis RS, Hudspeth AJ (1983) Voltage-and ion-dependent conductances in solitary vertebrate hair cells. Nature 304:538–541
Maruska KP, Sisneros JA (2015) Sex steroid-dependent modulation of acoustic communication systems in fishes. In: Ladich F (ed) Sound communication in fishes. Springer, New York, pp 207–233
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(6):3520–3533
McKibben JR, Bass AH (1999) Peripheral encoding of behaviorally relevant acoustic signals in a vocal fish: single tones. J Comp Physiol A 184(6):563–576
McKibben JR, Bass AH (2001) Peripheral encoding of behaviorally relevant acoustic signals in a vocal fish: harmonic and beat stimuli. J Comp Physiol A 187(4):271–285
Popper AN, Fay RR (1993) Sound detection and processing by fish: critical review and major research questions. Brain Beh Evol 41:14–25
Popper AN, Fay RR (2011) Rethinking sound detection by fishes. Hear Res 273(1):25–36
Roberts WM, Howard J, Hudspeth AJ (1988) Hair cells: transduction, tuning, and transmission in the inner ear. Ann Rev Cell Biol 4(1):63–92
Rogers PH, Cox M (1988) Underwater sound as a biological stimulus. In: Atema J, Fay RR, Popper AN, Tavolga WN, Sensory biology of aquatic animals. Springer, New York, pp 131–149
Rohmann KN, Bass AH (2011) Seasonal plasticity of auditory hair cell frequency sensitivity correlates with plasma steroid levels in vocal fish. J Exp Biol 214(11):1931–1942
Rohmann KN, Fergus DJ, Bass AH (2013) Plasticity in ion channel expression underlies variation in hearing during reproductive cycles. Curr Biol 23(8):678–683
Schellart NAM, Popper AN (1992) Functional aspects of the evolution of the auditory system of actinopterygian fish. In: Webster DB, Fay RR, Popper AN (eds) The evolutionary biology of hearing. Springer, New York, pp 295–322
Sisneros JA (2007) Saccular potentials of the vocal plainfin midshipman fish, Porichthys notatus. J Comp Physiol A 193:413–424
Sisneros JA (2009a) Adaptive hearing in the vocal plainfin midshipman fish: getting in tune for the breeding season and implications for acoustic communication. Integr Zool 4:33–42
Sisneros JA (2009b) Seasonal plasticity of auditory saccular sensitivity in the vocal plainfin midshipman fish, Porichthys notatus. J Neurophysiol 102(2):1121–1131
Sisneros JA, Bass AH (2003) Seasonal plasticity of peripheral auditory frequency sensitivity. J Neurosci 23:1049–1058
Sisneros JA, Bass AH (2005) Ontogenetic changes in the response properties of individual, primary auditory afferents in the vocal plainfin midshipman fish Porichthys notatus Girard. J Exp Biol 208(16):3121–3131
Sisneros JA, Rogers PH (2016) Directional Hearing and Sound Source Localization in Fishes. In: Sisneros JA (ed) Fish hearing and bioacoustics. Springer International, New York, pp 121–155
Sisneros JA, Forlano PM, Knapp R, Bass AH (2004) Seasonal variation of steroid hormone levels in an intertidal-nesting fish, the vocal plainfin midshipman. Gen Comp Endocrinol 136:101–116
Steinacker A, Romero A (1991) Characterization of voltage-gated and calcium-activated potassium currents in toadfish saccular hair cells. Brain Res 556(1):22–32
Steinacker A, Romero A (1992) Voltage-gated potassium current and resonance in the toadfish saccular hair cell. Brain Res 574:229–236
Tomkins JL, Simmons LW (2002). Measuring relative investment: a case study of testes investment in species with alternative male reproductive tactics. Anim Behav 63(5):1009–1016
Tricas TC, Boyle KS (2015) Sound pressure enhances the hearing sensitivity of Chaetodon butterfly fishes on noisy coral reefs. J Exp Biol 218:1585–1595
Vasconcelos RO, Sisneros JA, Amorim MCP, Fonseca PJ (2011) Auditory saccular sensitivity of the vocal Lusitanian toadfish: low frequency tuning allows acoustic communication throughout the year. J Comp Physiol A 197(9):903–913
Weeg M, Fay RR, Bass AH (2002) Directionality and frequency tuning of primary saccular afferents of a vocal fish, the plainfin midshipman (Porichthys notatus). J Comp Physiol A 188(8):631–641
Whitchurch EA, Ketten DR, Forlano PM, Fay RR, Sisneros JA (2012) Swim bladder sexual dimorphism in the plainfin midshipman fish: Implications for acoustic communication in this species. Program No. 296.11/CCC73. 2012 Neuroscience Meeting Planner. Society for Neuroscience, New Orleans (online)
Wysocki LE, Codarin A, Ladich F, Picciulin M (2009) Sound pressure and particle acceleration audiograms in three marine fish species from the Adriatic Sea. J Acoust Soc Am 126(4):2100–2107