Abstract
Many aquatic organisms use vocalizations for reproductive behavior; therefore, disruption of their soundscape could adversely affect their life history. Male oyster toadfish (Opsanus tau) establish nests in shallow waters during spring and attract female fish with boatwhistle vocalizations. Males exhibit high nest fidelity, making them susceptible to anthropogenic sound in coastal waters, which could mask their vocalizations and/or reduce auditory sensitivity levels. Additionally, the effect of self-generated boatwhistles on toadfish auditory sensitivity has yet to be addressed. To investigate the effect of sound exposure on toadfish auditory sensitivity, sound pressure and particle acceleration sensitivity curves were determined using auditory evoked potentials before and after (0-, 1-, 3-, 6- and 9-day) exposure to 1- or 12-h of continuous playbacks to ship engine sound or conspecific vocalization. Exposure to boatwhistles had no effect on auditory sensitivity. However, exposure to anthropogenic sound caused significant decreases in auditory sensitivity for at least 3 days, with shifts up to 8 dB SPL and 20 dB SPL immediately following 1- and 12-h anthropogenic exposure, respectively. Understanding the effect of self-generated and anthropogenic sound exposure on auditory sensitivity provides an insight into how soundscapes affect acoustic communication.
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References
Amoser S, Ladich F (2003) Diversity in noise-induced temporary hearing loss in otophysine fishes. J Acoust Soc Am 113:2170–2179. https://doi.org/10.1121/1.1557212
Bhandiwad AA, Whitchurch EA, Colleye O et al (2017) Seasonal plasticity of auditory saccular sensitivity in “sneaker” type II male plainfin midshipman fish, Porichthys notatus. J Comp Physiol A 203:211–222. https://doi.org/10.1007/s00359-017-1157-9
Bruintjes R, Radford AN (2013) Context-dependent impacts of anthropogenic noise on individual and social behaviour in a cooperatively breeding fish. Anim Behav 85:1343–1349. https://doi.org/10.1016/j.anbehav.2013.03.025
Cardinal EA, Radford CA, Mensinger AF (2018) Potential role of the anterior lateral line in sound localization in toadfish (Opsanus tau). J Exp Bio 221:jeb180679. https://doi.org/10.1242/jeb.180679
Codarin A, Wysocki LE, Ladich F, Picciulin M (2009) Effects of ambient and boat noise on hearing and communication in three fish species living in a marine protected area (Miramare, Italy). Mar Pollut Bull 58:1880–1887. https://doi.org/10.1016/j.marpolbul.2009.07.011
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 32:1366–1376. https://doi.org/10.1523/JNEUROSCI.4928-11.2012
Colleye O, Vetter BJ, Mohr RA et al (2019) Sexually dimorphic swim bladder extensions enhance the auditory sensitivity of female plainfin midshipman fish, Porichthys notatus. J Exp Bio. https://doi.org/10.1242/jeb.204552
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 276:228–240. https://doi.org/10.1002/jmor.20336
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
Erbe C (2013) Underwater noise of small personal watercraft (jet skis). J Acoust Soc Am 133:EL326–EL330. https://doi.org/10.1121/1.4795220
Faulkner RC, Farcas A, Merchant ND (2018) Guiding principles for assessing the impact of underwater noise. J Appl Ecol 55:2531–2536. https://doi.org/10.1111/1365-2664.13161
Fay RR, Edds-Walton PL (1997a) Directional response properties of saccular afferents of the toadfish, Opsanus tau. Hear Res 111:1–21. https://doi.org/10.1016/S0378-5955(97)00083-X
Fay RR, Edds-Walton PL (1997b) 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
Fine ML (1978) Seasonal and geographical variation of the mating call of the oyster toadfish Opsanus tau L. Oecologia 36:45–57. https://doi.org/10.1007/BF00344570
Fish JF (1972) The effect of sound playback on the toadfish. Behavior of marine animals. Springer, Boston, pp 386–434
Fish JF, Offutt GC (1972) Hearing thresholds from toadfish, Opsanus tau, measured in the laboratory and field. J Acoust Soc Am 51:1318–1321. https://doi.org/10.1121/1.1912977
Flock Å (1965) Transducing mechanisms in the lateral line canal organ receptors. Cold Spring Harb Symp Quant Biol 30:133–145. https://doi.org/10.1101/SQB.1965.030.01.016
Flock Å, Wersäll J (1962) A study of the orientation of the sensory hairs of the receptor cells in the lateral line organ of fish, with special reference to the function of the receptors. J Cell Biol 15:19–27. https://doi.org/10.1083/jcb.15.1.19
Gray G-A, Winn HE (1961) Reproductive ecology and sound production of the toadfish, Opsanus tau. Ecology 42:274–282. https://doi.org/10.2307/1932079
Hamernik RP, Henderson D, Crossley JJ, Salvi RJ (1974) Interaction of continuous and impulse noise: audiometric and histological effects. J Acoust Soc Am 55:117–121. https://doi.org/10.1121/1.1928141
Hatch LT, Clark CW, Parijs SMV et al (2012) Quantifying loss of acoustic communication space for right whales in and around a US national marine sanctuary. Conserv Biol 26:983–994. https://doi.org/10.1111/j.1523-1739.2012.01908.x
Haviland-Howell G, Frankel AS, Powell CM et al (2007) Recreational boating traffic: a chronic source of anthropogenic noise in the Wilmington, North Carolina Intracoastal Waterway. J Acoust Soc Am 122:151–160. https://doi.org/10.1121/1.2717766
Hawkins AD, Pembroke AE, Popper AN (2015) Information gaps in understanding the effects of noise on fishes and invertebrates. Rev Fish Biol Fish 25:39–64. https://doi.org/10.1007/s11160-014-9369-3
Herbert-Read JE, Kremer L, Bruintjes R et al (2017) Anthropogenic noise pollution from pile-driving disrupts the structure and dynamics of fish shoals. Proc Biol Sci. https://doi.org/10.1098/rspb.2017.1627
Higgs DM, Souza MJ, Wilkins HR et al (2002) Age- and size-related changes in the inner ear and hearing ability of the adult zebrafish (Danio rerio). JARO 3:174–184. https://doi.org/10.1007/s101620020035
Holles S, Simpson SD, Radford AN et al (2013) Boat noise disrupts orientation behaviour in a coral reef fish. Mar Ecol Prog Ser 485:295–300. https://doi.org/10.3354/meps10346
Holt MM, Noren DP, Veirs V et al (2008) Speaking up: Killer whales (Orcinus orca) increase their call amplitude in response to vessel noise. J Acoust Soc of Am 125:EL27–EL32. https://doi.org/10.1121/1.3040028
Hudspeth AJ (1985) The cellular basis of hearing: the biophysics of hair cells. Science 230:745–752
Hudspeth AJ, Corey DP (1977) Sensitivity, polarity, and conductance change in the response of vertebrate hair cells to controlled mechanical stimuli. PNAS 74:2407–2411. https://doi.org/10.1073/pnas.74.6.2407
Ladich F (2013) Effects of noise on sound detection and acoustic communication in fishes. In: Brumm H (ed) Animal communication and noise. Springer, Berlin, pp 65–90
Ladich F, Schulz-Mirbach T (2013) Hearing in cichlid fishes under noise conditions. PLoS One 8:e57588. https://doi.org/10.1371/journal.pone.0057588
Lozier NR, Sisneros JA (2019) Reproductive-state dependent changes in saccular hair cell density of the vocal male plainfin midshipman fish. Hear Res 383:107805. https://doi.org/10.1016/j.heares.2019.107805
Marley SA, Kent CPS, Erbe C, Parnum IM (2017) Effects of vessel traffic and underwater noise on the movement, behaviour and vocalisations of bottlenose dolphins in an urbanised estuary. Sci Rep 7:13437. https://doi.org/10.1038/s41598-017-13252-z
Maruska KP, Mensinger AF (2009) Acoustic characteristics and variations in grunt vocalizations in the oyster toadfish Opsanus tau. Environ Biol Fish 84:325–337. https://doi.org/10.1007/s10641-009-9446-y
Maruska KP, Mensinger AF (2015) Directional sound sensitivity in utricular afferents in the toadfish Opsanus tau. J Exp Biol 218:1759–1766. https://doi.org/10.1242/jeb.115345
McCauley RD, Fewtrell J, Popper AN (2003) High intensity anthropogenic sound damages fish ears. J Acoust Soc Am 113:638–642. https://doi.org/10.1121/1.1527962
Mensinger AF (2014) Disruptive communication: stealth signaling in the toadfish. J Exp Biol 217:344–350. https://doi.org/10.1242/jeb.090316
Mensinger AF, Wert JCV, Rogers LS (2019) Lateral line sensitivity in free-swimming toadfish Opsanus tau. J Exp Biol 222:jeb190587. https://doi.org/10.1242/jeb.190587
Nissen AC, Vetter BJ, Rogers LS, Mensinger AF (2019) Impacts of broadband sound on silver (Hypophthalmichthys molitrix) and bighead (H. nobilis) carp hearing thresholds determined using auditory evoked potential audiometry. Fish Physiol Biochem. https://doi.org/10.1007/s10695-019-00657-y
Parvulescu A (1964) Problems of propagation and processing. In: Tavolga WN (ed) Marine BioAcoustics. Pergamon Press, Oxford, pp 87–100
Perelmuter JT, Wilson AB, Sisneros JA, Forlano PM (2019) Forebrain dopamine system regulates inner ear auditory sensitivity to socially relevant acoustic signals. Curr Biol. https://doi.org/10.1016/j.cub.2019.05.055
Pirotta E, Merchant ND, Thompson PM et al (2015) Quantifying the effect of boat disturbance on bottlenose dolphin foraging activity. Biol Conserv 181:82–89. https://doi.org/10.1016/j.biocon.2014.11.003
Popper AN, Fay RR (2011) Rethinking sound detection by fishes. Hear Res 273:25–36. https://doi.org/10.1016/j.heares.2009.12.023
Popper AN, Hawkins A (eds) (2016) The effects of noise on aquatic life II. Springer, New York
Popper AN, Hawkins AD (2019) An overview of fish bioacoustics and the impacts of anthropogenic sounds on fishes. J Fish Biol 94:692–713. https://doi.org/10.1111/jfb.13948
Popper AN, Smith ME, Cott PA et al (2005) Effects of exposure to seismic airgun use on hearing of three fish species. J Acoust Soc Am 117:3958–3971. https://doi.org/10.1121/1.1904386
Popper AN, Hawkins AD, Sand O, Sisneros JA (2019) Examining the hearing abilities of fishes. J Acoust Soc Am 146:948–955. https://doi.org/10.1121/1.5120185
Putland RL, Mackiewicz AG, Mensinger AF (2018) Localizing individual soniferous fish using passive acoustic monitoring. Ecol Inform 48:60–68. https://doi.org/10.1016/j.ecoinf.2018.08.004
Putland RL, Montgomery JC, Radford CA (2019) Ecology of fish hearing. J Fish Biol 95:39–52. https://doi.org/10.1111/jfb.13867
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. https://doi.org/10.1242/jeb.092510
Radford CA, Stanley JA, Simpson SD, Jeffs AG (2011) Juvenile coral reef fish use sound to locate habitats. Coral Reefs 30:295–305. https://doi.org/10.1007/s00338-010-0710-6
Radford AN, Kerridge E, Simpson SD (2014) Acoustic communication in a noisy world: can fish compete with anthropogenic noise? Behav Ecol 25:1022–1030. https://doi.org/10.1093/beheco/aru029
Ramcharitar J, Popper AN (2004) Masked auditory thresholds in sciaenid fishes: a comparative study. J Acoust Soc Am 116:1687–1691. https://doi.org/10.1121/1.1771614
Ricci SW, Bohnenstiehl DR, Eggleston DB et al (2017) Oyster toadfish (Opsanus tau) boatwhistle call detection and patterns within a large-scale oyster restoration site. PLoS One 12:e0182757. https://doi.org/10.1371/journal.pone.0182757
Rogers PH, Hawkins AD, Popper AN et al (2016) Parvulescu revisited: small tank acoustics for bioacousticians. In: Popper AN, Hawkins A (eds) The effects of noise on aquatic life II. Springer, New York, pp 933–941
Rohmann KN, Andrew BH (2011) Seasonal plasticity of auditory hair cell frequency sensitivity correlates with plasma steroid levels in vocal fish. J Exp Biol 214:1931–1942. https://doi.org/10.1242/jeb.054114
Santulli A, Modica A, Messina C et al (1999) Biochemical responses of european sea bass (Dicentrarchus labrax L.) to the stress induced by off shore experimental seismic prospecting. Mar Pollut Bull 38:1105–1114. https://doi.org/10.1016/S0025-326X(99)00136-8
Sarà G, Dean JM, D’Amato D et al (2007) Effect of boat noise on the behaviour of bluefin tuna Thunnus thynnus in the Mediterranean Sea. Mar Ecol Prog Ser 331:243–253. https://doi.org/10.3354/meps331243
Saunders J, Dooling R (1974) Noise-induced threshold shift in the parakeet (Melopsittacus undulatus). PNAS 71:1962–1965. https://doi.org/10.1073/pnas.71.5.1962
Shannon G, McKenna MF, Angeloni LM et al (2016) A synthesis of two decades of research documenting the effects of noise on wildlife. Biol Rev 91:982–1005. https://doi.org/10.1111/brv.12207
Sierra-Flores R, Atack T, Migaud H, Davie A (2015) Stress response to anthropogenic noise in Atlantic cod Gadus morhua L. Aquac Eng 67:67–76. https://doi.org/10.1016/j.aquaeng.2015.06.003
Simpson SD, Purser J, Radford AN (2015) Anthropogenic noise compromises antipredator behaviour in European eels. Global Change Biol 21:586–593. https://doi.org/10.1111/gcb.12685
Sisneros JA (2007) Saccular potentials of the vocal plainfin midshipman fish, Porichthys notatus. J Comp Physiol A 193:413–424. https://doi.org/10.1007/s00359-006-0195-5
Sisneros JA, Forlano PM, Deitcher DL, Bass AH (2004) Steroid-dependent auditory plasticity leads to adaptive coupling of sender and receiver. Science 305:404–407. https://doi.org/10.1126/science.1097218
Sivle LD, Kvadsheim PH, Fahlman A et al (2012) Changes in dive behavior during naval sonar exposure in killer whales, long-finned pilot whales, and sperm whales. Front Physiol 3:400
Slabbekoorn H, Bouton N, van Opzeeland I et al (2010) A noisy spring: the impact of globally rising underwater sound levels on fish. Trends Ecol Evol 25:419–427. https://doi.org/10.1016/j.tree.2010.04.005
Smith ME, Kane AS, Popper AN (2004) Acoustical stress and hearing sensitivity in fishes: does the linear threshold shift hypothesis hold water? J Exp Biol 207:3591–3602. https://doi.org/10.1242/jeb.01188
Smith ME, Coffin AB, Miller DL, Popper AN (2006) Anatomical and functional recovery of the goldfish (Carassius auratus) ear following noise exposure. J Exp Biol 209:4193–4202. https://doi.org/10.1242/jeb.02490
Tavolga WN (1971) Sound production and detection. In: Hoar WS, Randall DJ (eds) Fish physiology. Academic Press, Cambridge, pp 135–205
Van Wert JC, Mensinger AF (2019) Seasonal and daily patterns of the mating calls of the oyster toadfish, Opsanus tau. Biol Bull. https://doi.org/10.1086/701754
Vasconcelos RO, Amorim MCP, Ladich F (2007) Effects of ship noise on the detectability of communication signals in the Lusitanian toadfish. J Exp Biol 210:2104–2112. https://doi.org/10.1242/jeb.004317
Vetter BJ, Brey MK, Mensinger AF (2018) Reexamining the frequency range of hearing in silver (Hypophthalmichthys molitrix) and bighead (H. nobilis) carp. PLOS One 13:e0192561. https://doi.org/10.1371/journal.pone.0192561
Vetter BJ, Seeley LH, Sisneros JA (2019) Lagenar potentials of the vocal plainfin midshipman fish, Porichthys notatus. J Comp Physiol A. https://doi.org/10.1007/s00359-018-01314-0
Voellmy IK, Purser J, Flynn D et al (2014a) Acoustic noise reduces foraging success in two sympatric fish species via different mechanisms. Anim Behav 89:191–198. https://doi.org/10.1016/j.anbehav.2013.12.029
Voellmy IK, Purser J, Simpson SD, Radford AN (2014b) Increased noise levels have different impacts on the anti-predator behaviour of two sympatric fish species. PLoS One 9:e102946. https://doi.org/10.1371/journal.pone.0102946
Weeg MS, Land BR, Bass AH (2005) Vocal pathways modulate efferent neurons to the inner ear and lateral line. J Neurosci 25:5967–5974. https://doi.org/10.1523/JNEUROSCI.0019-05.2005
Wersäll J, Flock Å, Lundquist P-G (1965) Structural basis for directional sensitivity in cochlear and vestibular sensory receptors. Cold Spring Harb Symp Quant Biol 30:115–132. https://doi.org/10.1101/SQB.1965.030.01.015
Williams R, Wright AJ, Ashe E et al (2015) Impacts of anthropogenic noise on marine life: publication patterns, new discoveries, and future directions in research and management. Ocean Coast Manag 115:17–24. https://doi.org/10.1016/j.ocecoaman.2015.05.021
Wysocki LE, Ladich F (2005) Hearing in fishes under noise conditions. JARO 6:28–36. https://doi.org/10.1007/s10162-004-4043-4
Wysocki LE, Dittami JP, Ladich F (2006) Ship noise and cortisol secretion in European freshwater fishes. Biol Conserv 128:501–508. https://doi.org/10.1016/j.biocon.2005.10.020
Yan HY, Fine ML, Horn NS, Colón WE (2000) Variability in the role of the gasbladder in fish audition. J Comp Physiol A 186:435–445. https://doi.org/10.1007/s003590050443
Acknowledgements
The authors would like to acknowledge the Marine Resources Center staff at the Marine Biological Laboratory for providing toadfish. Funding was provided by National Science Foundation Grants IOS 1354745 and DBI 1359230 and 1659604 to AFM, and by the National Science Foundation Graduate Research Fellowship Program under grant DGE 1804377 to LSR. All experimental procedures conformed to NIH guidelines for animal care and use of animals, and were approved by the University of Minnesota Institutional Animal Care and Use Committee under Protocol ID: 1903-36856A.
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Rogers, L.S., Putland, R.L. & Mensinger, A.F. The effect of biological and anthropogenic sound on the auditory sensitivity of oyster toadfish, Opsanus tau. J Comp Physiol A 206, 1–14 (2020). https://doi.org/10.1007/s00359-019-01381-x
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DOI: https://doi.org/10.1007/s00359-019-01381-x