Operant conditioning as a tool to assess hearing abilities in sharks.
Mustelus lenticulatus
Sphyrna lewini
behavioural audiogram
elasmobranchs
food reward conditioning
rig
scalloped hammerhead
smooth hound
Journal
Journal of fish biology
ISSN: 1095-8649
Titre abrégé: J Fish Biol
Pays: England
ID NLM: 0214055
Informations de publication
Date de publication:
Aug 2023
Aug 2023
Historique:
received:
13
03
2023
accepted:
08
05
2023
medline:
4
8
2023
pubmed:
19
5
2023
entrez:
19
5
2023
Statut:
ppublish
Résumé
Sharks (elasmobranchs) are an ancient, diverse group of fishes, representing a basal stage in the evolution of vertebrate hearing. Yet, our understanding of behavioural measures of hearing abilities in sharks is limited. To address this, an operant conditioning paradigm was designed, and scalloped hammerhead Sphyrna lewini and rig (spotted estuary smooth hound) Mustelus lenticulatus were successfully trained to respond to pure-tone acoustic stimuli from an underwater speaker. After 2-3 weeks of training, both species showed distinctive responses to these acoustic stimuli and retained this behaviour when reinforced. S. lewini responded to a 400 Hz pulsed tone with an abrupt increase in tailbeat frequency (97 beats per 30 s vs. 69 beats for a 2 kHz control and 70 beats for no signal) and sustained vigorous swimming (arousal response) for at least 30 s. In response to a 200 Hz pulsed tone, M. lenticulatus visited a target area under the speaker significantly more frequently (13.4 ± 4.3 times per minute vs. 1.4 ± 1.5 times for a 1.2 kHz control and 0.9 ± 0.01 times for no signal) and swam circles under the speaker to search for food. The authors used S. lewini arousal responses to pure-tone stimuli of 40, 80, 200, 400, 600 and 800 Hz to generate a provisional hearing-threshold curve. The results show that S. lewini adapts to low-frequency hearing (greatest sensitivity at 200 Hz, upper limit 800 Hz), which is like other coastal pelagic sharks that have been investigated so far. Despite challenges operant acoustic conditioning studies are a viable method for revealing auditory capabilities of sharks.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
411-424Subventions
Organisme : Faculty of Medical and Health Sciences, University of Auckland
Organisme : Marsden Fund
ID : UOA1808
Informations de copyright
© 2023 The Authors. Journal of Fish Biology published by John Wiley & Sons Ltd on behalf of Fisheries Society of the British Isles.
Références
Anderson, J. M., Clegg, T. M., Véras, L. V., & Holland, K. N. (2017). Insight into shark magnetic field perception from empirical observations. Scientific Reports, 7, 11042. https://doi.org/10.1038/s41598-017-11459-8.
Aronson, L. R., Aronson, F. R., & Clark, E. (1967). Instrumental conditioning and light-dark discrimination in young nurse sharks. Bulletin of Marine Science, 17(2), 249-256.
Backus, R. H. (1963). Hearing in elasmobranchs. In G. W. Perry (Ed.), Sharks and survival (pp. 243-254). Boston: D. C. Heath and Company.
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 1-48. https://doi.org/10.18637/jss.v067.i01.
Beulig, A. (1982). Social and experiential factors in the responsiveness of sharks to sound. Florida Scientist, 45(1), 2-10.
Bhandiwad, A. A., & Sisneros, J. A. (2016). Revisiting psychoacoustic methods for the assessment of fish hearing. In J. A. Sisneros (Ed.), Fish hearing and bioacoustics: An anthology in honor of Arthur N. Popper and Richard R. Fay (pp. 157-184). Cham: Springer. https://doi.org/10.1007/978-3-319-21059-9_8.
Bres, M. (1993). The behaviour of sharks. Reviews in Fish Biology and Fisheries, 3(2), 133-159. https://doi.org/10.1007/BF00045229.
Brown, C., & Schluessel, V. (2022). Smart sharks: A review of chondrichthyan cognition. Animal Cognition, 26, 175-188. https://doi.org/10.1007/s10071-022-01708-3.
Bullock, T. H., & Corwin, J. T. (1979). Acoustic evoked activity in the brain in sharks. Journal of Comparative Physiology A, 129(3), 223-234. https://doi.org/10.1007/BF00657658.
Casper, B. M. (2011). Hearing and lateral line: The ear and hearing in sharks, skates, and rays. In A. P. Farrell (Ed.), Encyclopedia of fish physiology (pp. 262-269). Academic Press. https://doi.org/10.1016/B978-0-12-374553-8.00013-7.
Chapuis, L., Collin, S. P., Yopak, K. E., McCauley, R. D., Kempster, R. M., Ryan, L. A., & Egeberg, C. A. (2019). The effect of underwater sounds on shark behaviour. Scientific Reports, 9(1), 1-11. https://doi.org/10.1038/s41598-019-43078-w.
Chapuis, L., & Collin, S. P. (2022). The auditory system of cartilaginous fishes. Reviews in Fish Biology and Fisheries, 32(72), 521-554. https://doi.org/10.1007/s11160-022-09698-8.
Clark, E. (1959). Instrumental conditioning of lemon sharks. Science, 130(3369), 217-218. https://doi.org/10.1126/science.130.3369.217.b.
Clark, E. (1963). Visual discrimination in lemon sharks. Tenth Pacific science congress. Honolulu.
Corwin, J. T. (1978). The relation of inner ear structure to the feeding behavior in sharks and rays. In O. Johari (Ed.), Scanning electron microscopy (pp. 1105-1112). Chicago: S.E.M. Inc.
Corwin, J. T., Bullock, T. H., & Schweitzer, J. (1982). The auditory brain stem response in five vertebrate classes. Electroencephalography and Clinical Neurophysiology, 54(6), 629-641. https://doi.org/10.1016/0013-4694(82)90117-1.
Davies, D., Lochner, J., & Smith, E. (1963). Preliminary investigations on the hearing of sharks (Investigational Report No. 7). Durban, Republic of South Africa: Oceanographic Research Institute.
Evangelista, C., Mills, M., Siebeck, U. E., & Collin, S. P. (2010). A comparison of the external morphology of the membranous inner ear in elasmobranchs. Journal of Morphology, 271(4), 483-495. https://doi.org/10.1002/jmor.10812.
Fay, R. R., Kendall, J. I., Popper, A. N., & Tester, A. L. (1974). Vibration detection by the macula neglecta of sharks. Comparative Biochemistry and Physiology Part A: Physiology, 47(4), 1235-1240. https://doi.org/10.1016/0300-9629(74)90097-8.
Frisch, K. (1938). The sense of hearing in fish. Nature, 141(1), 8-11. https://doi.org/10.1038/141008a0.
Fritzsch, B. (1999). Hearing in two worlds: Theoretical and actual adaptive changes of the aquatic and terrestrial ear for sound reception. In R. R. Fay & A. N. Popper (Eds.), Comparative hearing: Fish and amphibians (pp. 15-42). New York, NY, USA: Springer. https://doi.org/10.1007/978-1-4612-0533-3_2.
Fuss, T., Bleckmann, H., & Schluessel, V. (2014). Visual discrimination abilities in the gray bamboo shark (Chiloscyllium griseum). Zoology, 117(2), 104-111. https://doi.org/10.1016/j.zool.2013.10.009.
Graeber, C. R., Schroeder, D. M., Jane, J. A., & Ebbesson, S. O. (1978). Visual discrimination following partial telencephalic ablations in nurse sharks (Ginglymostoma cirratum). Journal of Comparative Neurology, 180(2), 325-344. https://doi.org/10.1002/cne.901800209.
Guttridge, T. L., & Brown, C. (2014). Learning and memory in the port Jackson shark, Heterodontus portusjacksoni. Animal Cognition, 17(2), 415-425. https://doi.org/10.1007/s10071-013-0673-4.
Guttridge, T. L., Myrberg, A. A., Porcher, I. F., Sims, D. W., & Krause, J. (2009). The role of learning in shark behaviour. Fish and Fisheries, 10(4), 450-469. https://doi.org/10.1111/j.1467-2979.2009.00339.x.
Guttridge, T. L., van Dijk, S., Stamhuis, E. J., Krause, J., Gruber, S. H., & Brown, C. (2013). Social learning in juvenile lemon sharks, Negaprion brevirostris. Animal Cognition, 16(1), 55-64. https://doi.org/10.1007/s10071-012-0550-6.
Guttridge, T. L., Yopak, K. E., & Schluessel, V. (2018). Sharks-elasmobranch cognition. In N. Bueno-Guerra & F. Amici (Eds.), Field and laboratory methods in animal cognition: A comparative guide (p. 354). Cambridge: Cambridge University Press. https://doi.org/10.1017/9781108333191.018.
Hartig, F. (2017). Package ‘DHARMa’. Regensburg, Germany: University of Regensburg. Retrieved from http://florianhartig.github.io/DHARMa/
Hawkins, A. D. (1981). The hearing abilities of fish. In W. N. Tavolga, A. N. Popper, & R. R. Fay (Eds.), Hearing and sound communication in fishes (pp. 109-137). New York, NY, USA: Springer. https://doi.org/10.1007/978-1-4615-7186-5_6.
Hawkins, A. D., & Popper, A. N. (2018). Directional hearing and sound source localization by fishes. The Journal of the Acoustical Society of America, 144(6), 3329-3350. https://doi.org/10.1121/1.5082306.
Hobson, E. S. (1963). Feeding behavior in three species of sharks. Pacific Science, 17(2), 171-194.
Jacoby, D. M., Croft, D. P., & Sims, D. W. (2012). Social behaviour in sharks and rays: Analysis, patterns, and implications for conservation. Fish and Fisheries, 13(4), 399-417. https://doi.org/10.1111/j.1467-2979.2011.00436.x.
Johnson, C., Scronce, B., & McManus, M. (1984). Detection of DC electric dipoles in background fields by the nurse shark. Journal of Comparative Physiology A, 155(5), 681-687. https://doi.org/10.1007/BF00610854.
Kajiura, S. M., & Holland, K. N. (2002). Electroreception in juvenile scalloped hammerhead and sandbar sharks. Journal of Experimental Biology, 205(23), 3609-3621. https://doi.org/10.1242/jeb.205.23.3609.
Kalmijn, A. J. (1982). Electric and magnetic field detection in elasmobranch fishes. Science, 218(4575), 916-918. https://doi.org/10.1126/science.7134985.
Kalmijn, A. J. (1988). Hydrodynamic and acoustic field detection. In J. Atema, R. R. Fay, A. N. Popper, & W. N. Tavolga (Eds.), Sensory biology of aquatic animals (pp. 83-130). New York, NY, USA: Springer. https://doi.org/10.1007/978-1-4612-3714-3_4.
Kalmijn, A. J. (2000). Detection and processing of electromagnetic and near-field acoustic signals in elasmobranch fishes. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 355(1401), 1135-1141. https://doi.org/10.1098/rstb.2000.0654.
Kelly, J. C., & Nelson, D. R. (1975). Hearing thresholds of the horn shark, Heterodontus francisci. The Journal of the Acoustical Society of America, 58(4), 905-909. https://doi.org/10.1121/1.380742.
Kenyon, T. N., Ladich, F., & Yan, H. Y. (1998). A comparative study of hearing ability in fishes: The auditory brainstem response approach. Journal of Comparative Physiology A, 182(3), 307-318. https://doi.org/10.1007/s003590050181.
Ketten, D. R. (1997). Structure and function in whale ears. Bioacoustics, 8(1-2), 103-135. https://doi.org/10.1080/09524622.1997.9753356.
Kimber, J. A., Sims, D. W., Bellamy, P. H., & Gill, A. B. (2011). The ability of a benthic elasmobranch to discriminate between biological and artificial electric fields. Marine Biology, 158(1), 1-8. https://doi.org/10.1007/s00227-010-1537-y.
Kimber, J. A., Sims, D. W., Bellamy, P. H., & Gill, A. B. (2014). Elasmobranch cognitive ability: Using electroreceptive foraging behaviour to demonstrate learning, habituation, and memory in a benthic shark. Animal Cognition, 17(1), 55-65. https://doi.org/10.1007/s10071-013-0637-8.
Kritzler, H., & Wood, L. (1961). Provisional audiogram for the shark Carcharhinus leucas. Science, 133(3463), 1480-1482. https://doi.org/10.1126/science.133.3463.1480.
Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. (2017). lmerTest package: Tests in linear mixed effects models. Journal of Statistical Software, 82(1), 1-26. https://doi.org/10.18637/jss.v082.i13.
Ladich, F., & Fay, R. R. (2013). Auditory evoked potential audiometry in fish. Reviews in Fish Biology and Fisheries, 23(3), 317-364. https://doi.org/10.1007/s11160-012-9297-z.
Lara, R. A., Breitzler, L., Lau, L. H., Gordillo-Martinez, F., Chen, F., Fonseca, P. J., & Vasconcelos, R. O. (2022). Noise-induced hearing loss correlates with inner ear hair cell decrease in larval zebrafish. Journal of Experimental Biology, 225, 1-9. https://doi.org/10.1242/jeb.243743.
Magnusson, A., Skaug, H., Nielsen, A., Berg, C., Kristensen, K., Maechler, M., … Brooks, M. (2020). Package ‘glmmTMB.’. https://cran.r-project.org/web/packages/glmmTMB/glmmTMB.pdf.
Maisey, J. G., & Lane, J. A. (2010). Labyrinth morphology and the evolution of low-frequency phonoreception in elasmobranchs. Comptes Rendus Palevol, 9(6-7), 289-309. https://doi.org/10.1016/j.crpv.2010.07.021.
McFadden, S. L., Simmons, A. M., Erbe, C., & Thomas, J. A. (2022). Behavioral and physiological audiometric methods for animals. In C. Erbe & J. A. Thomas (Eds.), Exploring animal behavior through sound (pp. 355-387). Springer. https://doi.org/10.1007/978-3-030-97540-1_10.
McManus, M., Johnson, C., & Jeffries, M. (1984). Training nurse sharks using operant conditioning (Technical Report No. 977, 12 pp.). San Diego, CA, USA: Naval Ocean Systems Center.
Meyer, C. G., Holland, K. N., & Papastamatiou, Y. P. (2004). Sharks can detect changes in the geomagnetic field. Journal of the Royal Society Interface, 2(2), 129-130. https://doi.org/10.1098/rsif.2004.0021.
Mickle, M. F., Pieniazek, R. H., & Higgs, D. M. (2020). Field assessment of behavioural responses of southern stingrays (Hypanus americanus) to acoustic stimuli. Royal Society Open Science, 7(1), 191544. https://doi.org/10.1098/rsos.191544.
Mickle, M. F., & Higgs, D. M. (2022). Towards a new understanding of elasmobranch hearing. Marine Biology, 169(1), 1-13. https://doi.org/10.1007/s00227-021-03996-8.
Mooney, A. T., Samson, J. E., Schlunk, A. D., & Zacarias, S. (2016). Loudness-dependent behavioral responses and habituation to sound by the longfin squid (Doryteuthis pealeii). Journal of Comparative Physiology A, 202(7), 489-501. https://doi.org/10.1007/s00359-016-1092-1.
Myrberg, A. A., Banner, A., & Richard, J. (1969). Shark attraction using a video-acoustic system. Marine Biology, 2(3), 264-276. https://doi.org/10.1007/BF00351149.
Myrberg, A. A., & Gruber, S. H. (1974). The behavior of the bonnethead shark, Sphyrna tiburo. Copeia, 1974(2), 358-374. https://doi.org/10.2307/1442530.
Nelson, D. R. (1967). Hearing thresholds, frequency discrimination, and acoustic orientation in the lemon shark, Negaprion brevirostris (Poey). Bulletin of Marine Science, 17(3), 741-768.
Nelson, D. R., & Johnson, R. H. (1972). Acoustic attraction of Pacific reef sharks: effect of pulse intermittency and variability. Comparative Biochemistry and Physiology Part A: Physiology, 42(1), 85-95. https://doi.org/10.1016/0300-9629(72)90370-2.
Newton, K. C., & Kajiura, S. M. (2017). Magnetic field discrimination, learning, and memory in the yellow stingray (Urobatis jamaicensis). Animal Cognition, 20(4), 603-614. https://doi.org/10.1007/s10071-017-1084-8.
Newton, K. C., & Kajiura, S. M. (2020). The yellow stingray (Urobatis jamaicensis) can discriminate the geomagnetic cues necessary for a bicoordinate magnetic map. Marine Biology, 167(10), 1-13. https://doi.org/10.1007/s00227-020-03763-1.
Northcutt, G. R. (1977). Elasmobranch central nervous system organization and its possible evolutionary significance. American Zoologist, 17(2), 411-429. https://doi.org/10.1093/icb/17.2.411.
Olla, B. L. (1962). The perception of sound in small hammerhead sharks, Sphyrna lewini (Unpublished master's thesis). Honolulu, HI, USA: University of Hawaii.
Osorio, F. (2019). Package ‘heavy.’ Robust estimation using heavy-tailed distributions. https://doi.org/10.13140/RG.2.2.17668.42886.
Parvulescu, A. (1964). Problems of propagation and processing. In W. N. Tavolga (Ed.), Marine bioacoustics (pp. 87-100). PE, USA: Pennsylvania State University.
Poppelier, T., Bonsberger, J., Berkhout, B. W., Pollmanns, R., & Schluessel, V. (2022). Acoustic discrimination in the grey bamboo shark Chiloscyllium griseum. Scientific Reports, 12, 6520. https://doi.org/10.1038/s41598-022-10257-1.
Popper, A. N., & Fay, R. R. (1977). Structure and function of the elasmobranch auditory system. American Zoologist, 17(2), 443-452. https://doi.org/10.1093/icb/17.2.443.
Popper, A. N., & Fay, R. R. (2011). Rethinking sound detection by fishes. Hearing Research, 273(1-2), 25-36. https://doi.org/10.1016/j.heares.2009.12.023.
Popper, A. N., & Hawkins, A. D. (2021). Fish hearing and how it is best determined. ICES Journal of Marine Science, 78(7), 2325-2336. https://doi.org/10.1093/icesjms/fsab115.
Popper, A. N., Hawkins, A. D., Sand, O., & Sisneros, J. A. (2019). Examining the hearing abilities of fishes. The Journal of the Acoustical Society of America, 146(2), 948-955. https://doi.org/10.1121/1.5120185.
Popper, A. N., Hawkins, A. D., & Sisneros, J. A. (2021). Fish hearing “specialization”-a re-evaluation. Hearing Research, 425, 108393. https://doi.org/10.1016/j.heares.2021.108393.
Popper, A. N., Platt, C., & Saidel, W. M. (1982). Acoustic functions in the fish ear. Trends in Neurosciences, 5, 276-280. https://doi.org/10.1016/0166-2236(82)90171-0.
Pouca, C. V., & Brown, C. (2018). Food approach conditioning and discrimination learning using sound cues in benthic sharks. Animal Cognition, 21(4), 481-492. https://doi.org/10.1007/s10071-018-1183-1.
Retzius, G. (1881). Das Gehörorgan der Fische und Amphibien. Stockholm, Sweden: Samson & Wallin.
Rogers, P. H., & Cox, M. (1988). Underwater sound as a biological stimulus. In J. Atema, R. R. Fay, A. N. Popper, & W. N. Tavolga (Eds.), Sensory biology of aquatic animals (pp. 131-149). New York, NY, USA: Springer. https://doi.org/10.1007/978-1-4612-3714-3_5.
Ryan, L. A., Chapuis, L., Hemmi, J. M., Collin, S. P., McCauley, R. D., Yopak, K. E., & Kerr, C. C. (2018). Effects of auditory and visual stimuli on shark feeding behaviour: The disco effect. Marine Biology, 165(1), 11. https://doi.org/10.1007/s00227-017-3256-0.
Salas, C., Broglio, C., Durán, E., Gómez, A., Ocana, F. M., Jimenez-Moya, F., & Rodriguez, F. (2006). Neuropsychology of learning and memory in teleost fish. Zebrafish, 3(2), 157-171. https://doi.org/10.1089/zeb.2006.3.157.
Schluessel, V. (2015). Who would have thought that ‘Jaws’ also has brains? Cognitive Functions in Elasmobranchs. Animal Cognition, 18(1), 19-37. https://doi.org/10.1007/s10071-014-0762-z.
Schluessel, V., Beil, O., Weber, T., & Bleckmann, H. (2014). Symmetry perception in bamboo sharks (Chiloscyllium griseum) and Malawi cichlids (Pseudotropheus sp.). Animal Cognition, 17(5), 1187-1205. https://doi.org/10.1007/s10071-014-0751-2.
Schluessel, V., Herzog, H., & Scherpenstein, M. (2015). Seeing the forest before the trees-spatial orientation in freshwater stingrays (Potamotrygon motoro) in a hole-board task. Behavioural Processes, 119, 105-115. https://doi.org/10.1016/j.beproc.2015.08.001.
Schluessel, V., Rick, I. P., & Plischke, K. (2014). No rainbow for grey bamboo sharks: evidence for the absence of colour vision in sharks from behavioural discrimination experiments. Journal of Comparative Physiology A, 200(11), 939-947. https://doi.org/10.1007/s00359-014-0940-0.
Siciliano, A. M., Kajiura, S. M., Long, J. H., & Porter, M. E. (2013). Are you positive? Electric dipole polarity discrimination in the yellow stingray, Urobatis jamaicensis. The Biological Bulletin, 225(2), 85-91. https://doi.org/10.1086/BBLv225n2p85.
Sims, D., & Davies, S. (1994). Does specific dynamic action (SDA) regulate return of appetite in the lesser spotted dogfish, Scyliorhinus canicula? Journal of Fish Biology, 45(2), 341-348. https://doi.org/10.1111/j.1095-8649.1994.tb01313.x.
Tester, A. L., & Kato, S. (1966). Visual target discrimination in blacktip sharks (Carcharhinus melanopterus) and grey sharks (C. menisorrah). Pacific Science, 20(1), 461-471.
Tolentino, V. A., Cabello, M. G., Linares, F. A., & Mendoza, C. R. (2008). Age and growth of the scalloped hammerhead shark, Sphyrna lewini (Griffith & Smith, 1834) from the southern coast of Sinaloa, México. Hidrobiológica, 18(1), 31-40. Retrieved from https://www.scielo.org.mx/scielo.php?script=sci_arttext&pid=S0188-88972008000100004.
Wickham, H. (2016). ggplot2: Elegant graphics for data analysis (2nd ed.). New York, NY, USA: Springer. https://doi.org/10.1007/978-0-387-98141-3.
Wisby, W. J., Richard, J. D., Nelson, D. R., & Gruber, S. H. (1964). Sound perception in elasmobranchs. In W. N. Tavolga (Ed.), Marine bioacoustics (pp. 255-268). PE, USA: Pennsylvania State University.
Yan, H. Y. (2004). The role of gas-holding structures in fish hearing: An acoustically evoked potentials approach. In E. Gerhard, M. Joachim, & B. G. Kapoor (Eds.), The senses of fish (pp. 189-209). Dordrecht, Netherlands: Springer. https://doi.org/10.1007/978-94-007-1060-3_9.
Yan, H. Y., & Popper, A. N. (1991). An automated positive reward method for measuring acoustic sensitivity in fish. Behavior Research Methods, Instruments, & Computers, 23(3), 351-356. https://doi.org/10.3758/BF03203396.
Young, F. A., Kajiura, S. M., Visser, G. J., Correia, J. P., & Smith, M. F. (2002). Notes on the long-term transport of the scalloped hammerhead shark (Sphyrna lewini). Zoo Biology, 21(3), 243-251. https://doi.org/10.1002/zoo.10019.