Fish biophony in a Mediterranean submarine canyon

[en] Although several bioacoustics investigations have shed light on the acoustic communication of Mediterranean fish species, the occurrence of fish sounds has never been reported below −40 m depth. This study assessed the occurrence of fish sounds at greater depths by monitoring the soundscape of a Mediterranean submarine canyon (Calvi, France) thanks to a combination of Static Acoustic Monitoring (three stations, from −125 to −150 m depth, 3 km from coastline) and of hydrophone-integrated gliders (Mobile Acoustic Monitoring; from −60 to −900 m depth, 3–6 km from coastline). Biological sounds were detected in 38% of the audio files; ten sound types (for a total of more than 9.000 sounds) with characteristics corresponding to those emitted by vocal species, or known as produced by fish activities, were found. For one of these sound types, emitter identity was inferred at the genus level (Ophidion sp.). An increase of from 10 to 15 dB re 1 μPa in sea ambient noise was observed during daytime hours due to boat traffic, potentially implying an important daytime masking effect. This study shows that monitoring the underwater soundscape of Mediterranean submarine canyons can provide holistic information needed to better understand the state and the dynamics of these heterogeneous, highly diverse environments

Research center :

FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège

Disciplines :

Zoology

Author, co-author :

Bolgan, Marta ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive

Gervaise, Cédric

Di Iorio, Lucia

Lossent, Julie

Lejeune, Pierre ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique

Raick, Xavier ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive

Parmentier, Eric ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive

Language :

English

Title :

Fish biophony in a Mediterranean submarine canyon

Publication date :

22 April 2020

Journal title :

Journal of the Acoustical Society of America

ISSN :

0001-4966

eISSN :

1520-8524

Publisher :

Acoustical Society of America, United States - New York

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 05 May 2020

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Bibliography

Ali, H. A., Mok, H. K., and Fine, M. L. (2016). "Development and sexual dimorphism of the sonic system in deep sea neobythitine fishes: The upper continental slope," Deep Sea Res. Pt I 115, 293-308. 10.1016/j.dsr.2016.07.010
Alves, D., Amorim, M. C. P., and Fonseca, P. J. (2016). "Boat noise reduces acoustic active space in the lusitanian toadfish Halobatrachus didactylus," Proc. Mtg. Acoust. 27, 010033. 10.1121/2.0000325
Beguery, L., Lossent, J., Tricarico, R., Gervaise, C., Iorio, L. D., Valentini Poirier, C. A., and Boissery, P. (2018). "Mapping underwater noise, detection of ships and cetaceans using a SeaExplorer glider at a basin level: Feedback from the first 1000 km-long acoustic exploration of the Western French Mediterranean Sea," J. Acoust. Soci. Am. 144 (3), 1807-1807. 10.1121/1.5067977
Bolgan, M., O'Brien, J., Chorazyczewska, E., Winfield, I. J., McCullough, P., and Gammell, M. (2017). "The soundscape of Arctic Charr spawning grounds in lotic and lentic environments: Can passive acoustic monitoring be used to detect spawning activities?," Bioacoustics 4622, 1-29. 10.1080/09524622.2017.1286262
Carriço, R., Silva, M. A., Menezes, G. M., Fonseca, P. J., and Amorim, M. C. P. (2019). "Characterization of the acoustic community of vocal fishes in the Azores," PeerJ 7, e7772. 10.7717/peerj.7772
Casadevall, M., Matallanas, J., Carrasson, M., and Munoz, M. (1996). "Morphometric, meristic and anatomical differences between Ophidion barbatum L., 1758 and O. rochei Muller, 1845 (Pisces, Ophidiidae)," Publicaciones Especial Instuto Espanol de Oceanografia 21, 45-61.ISSN:0214-7378; ISBN 84-491-0240-5
Codina, E., Kéver, L., Compere, P., Dragičević, B., Dulčić, J., and Parmentier, E. (2012). "The barbel-like specialization of the pelvic fins in Ophidion rochei (Ophidiidae)," J. Morphol. 273 (12), 1367-1376. 10.1002/jmor.20066
Danovaro, R., Company, J. B., Corinaldesi, C., D'Onghia, G., Galil, B., Gambi, C., Gooday, A. J., Lampadariou, N., Luna, G. M., Morigi, C., Olu, K., Polymenakou, P., Ramirez-Llodra, E., Sabbatini, A., Sardà, F., Sibuet, M., and Tselepides, A. (2010). "Deep-sea biodiversity in the Mediterranean Sea: The known, the unknown and the unknowable," PloS One 5 (8), e11832. 10.1371/journal.pone.0011832
de Jong, K., Amorim, M. C. P., Fonseca, P. J., Klein, A., and Heubel, K. U. (2016). "Noise affects acoustic courtship behavior similarly in two species of gobies," Proc. Mtg. Acoust. 27, 010018. 10.1121/2.0000272
Desiderà, E., Guidetti, P., Panzalis, P., Navone, A., Valentini-Poirrier, C. A., Boissery, P., Gervaise, C., and Di Iorio, L. (2019). "Acoustic fish communities: Sound diversity of rocky habitats reflects fish species diversity," Mar. Ecol. Progr. Ser. 608, 183-197. 10.3354/meps12812
D'Onghia, G., Politou, C. Y., Bozzano, A., Lloris, D., Rotllant, G., Sion, L. E., and Mastrototaro, F. (2004). "Deep-water fish assemblages in the Mediterranean Sea," Sci. Mar. 68 (S3), 87-99. 10.3989/scimar.2004.68s387
Erbe, C., Verma, A., McCauley, R., Gavrilov, A., and Parnum, I. (2015). "The marine soundscape of the Perth Canyon," Prog. Oceanogr. 137, 38-51. 10.1016/j.pocean.2015.05.015
Fine, M. L., Lin, H., Nguyen, B. B., Rountree, R. A., Cameron, T. M., and Parmentier, E. (2007). "Functional morphology of the sonic apparatus in the fawn cusk-eel Lepophidium profundorum (Gill, 1863)," J. Morphol. 268 (11), 953-966. 10.1002/jmor.10551
Fine, M. L., and Thorson, R. F. (2008). "Use of passive acoustics for assessing behavioral interactions in individual toadfish," Trans. Am. Fish. Soc. 137, 627-637. 10.1577/T04-134.1
Gervaise, C., Lossent, J., Di Iorio, L., Beguery, L., Tricarico, R., Boissery, P., and Valentini-Poirier, C. A. (2019). "Mapping underwater noise with a SeaExplorer glider at a basin level: Feedback from the first 1000 km-long acoustics exploration of the Western French Mediterranean Sea," in Proceedings of OCEANS 2019, June 17-20, Marseille, France.
Goren, M., and Galil, B. S. (2002). "Record of Cataetyx laticeps and Ophidion barbatum (Ophidiiformes) in the Eastern Mediterranean, with comments to deep sea ichthyofauna," Cybium 26 (2), 150-152. ISSN 0399-0974
Hallacher, L. E. (1974). "The comparative morphology of extrinsic gasbladder musculature in the scorpionfish genus Sebastes (Pisces: Scorpaenidae)," Proc. Calif. Acad. Sci. 40, 59-86.
Hawkins, A. D., and Picciulin, M. (2019). "The importance of underwater sounds to gadoid fishes," J. Acoust. Soc. Am. 146 (5), 3536-3551. 10.1121/1.5134683
IUCN Centre for Mediterranean Cooperation (2004). The Mediterranean Deep-Sea Ecosystems: An Overview of Their Diversity, Structure, Functioning and Anthropogenic Impacts, With a Proposal for Their Conservation (IUCN, Rome, Italy).
Kéver, L., Boyle, K. S., Bolen, G., Dragičević, B., Dulčić, J., and Parmentier, E. (2014). "Modifications in call characteristics and sonic apparatus morphology during puberty in Ophidion rochei (Actinopterygii: Ophidiidae)," J. Morphol. 275, 650-660. 10.1002/jmor.20245
Kéver, L., Boyle, K. S., Dragičević, B., Dulčić, J., Casadevall, M., and Parmentier, E. (2012). "Sexual dimorphism of sonic apparatus and extreme intersexual variation of sounds in Ophidion rochei (Ophidiidae): First evidence of a tight relationship between morphology and sound characteristics in Ophidiidae," Front. Zool. 9, 1-16. 10.1186/1742-9994-9-34
Lembke, C., Lowerre-Barbieri, S., Mann, D. A., and Taylor, J. C. (2018). "Using three acoustic technologies on underwater gliders to survey fish," Mar. Tech. Soc. J. 52 (6), 39-52. 10.4031/MTSJ.52.6.1
Lindseth, A., and Lobel, P. (2018). "Underwater soundscape monitoring and fish bioacoustics: A review," Fishes 3 (3), 36. 10.3390/fishes3030036
Locascio, J. V., and Mann, D. A. (2008). "Diel patterns of fish sound production in Charlotte Harbor, FL," Trans. Am. Fish. Soc. 137, 606-615. 10.1577/T06-069.1
Luczkovich, J. J., Pullinger, R. C., and Johnson, S. E. (2008). "Identifying sciaenid critical spawning habitats by the use of passive acoustics," Trans. Am. Fish. Soc. 137, 576-605. 10.1577/T05-290.1
Mann, D. A., Bowers-Altman, J., and Rountree, R. A. (1997). "Sounds produced by the striped cusk-eel Ophidion marginatum (Ophidiidae) during courtship and spawning," Copeia 3, 610-612. 10.2307/1447568
Mann, D., and Jarvis, S. M. (2004). "Potential sound production by a deep-sea fish," J. Acoust. Soc. Am. 115 (5), 2331-2333. 10.1121/1.1694992
Mann, D. A., and Lobel, P. S. (1995). "Passive acoustic detection of sounds produced by the damselfish, Dascyllus albisella (Pomacentridae)," Bioacoustics 6 (3), 199-213. 10.1080/09524622.1995.9753290
Mann, D., Locascio, J., and Wall, C. (2016). "Listening in the ocean: New discoveries and insights on marine life from autonomous passive acoustic recorders," in Listening in the Ocean (Springer, New York), pp. 309-324.
Marshall, N. B. (1967). "Sound-producing mechanisms and the biology of deep-sea fishes," in Marine Bio-Acoustics, edited by W. M. Tavolga (Pergamon, Oxford, UK), pp. 123-133.
Marshall, N. B. (1973). "Family Macrouridae," in Fishes of the Western North Atlantic, edited by D. Cohen (Sears Foundation for Marine Research Publications, New Haven, CT), pp. 496-665.
McCauley, R. D., and Cato, D. H. (2016). "Evening choruses in the Perth Canyon and their potential link with Myctophidae fishes," J. Acoust. Soc. Am. 140 (4), 2384-2398. 10.1121/1.4964108
Morato, T., Watson, R., Pitcher, T. J., and Pauly, D. (2006). "Fishing down the deep," Fish Fisheries 7 (1), 24-34. 10.1111/j.1467-2979.2006.00205.x
Nguyen, T. K., Lin, H., Parmentier, E., and Fine, M. L. (2008). "Seasonal variation in sonic muscles in the fawn cusk-eel Lepophidium profundorum," Biol. Lett. 4 (6), 707-710. 10.1098/rsbl.2008.0383
Nichols, B. (2005). "Characterizing sound production in nearshore rockfishes (Sebastes spp.)," M.S. thesis, University of Florida, Gainesville, FL.
Nielsen, J. G., Cohen, D. M., Markle, D. F., and Robins, C. R. (1999). "Ophidiiform fishes of the world (Order Ophidiiformes). An annotated and illustrated catalogue of pearlfishes, cusk-eels, brotulas and other ophidiiform fishes known to date," in FAO Species Catalogue (FAO Fisheries, Rome, Italy).
Parmentier, E., Bahri, M. A., Plenevaux, A., Fine, M. L., and Estrada, J. M. (2018). "Sound production and sonic apparatus in deep-living cusk-eels (Genypterus chilensis and Genypterus maculatus)," Deep Sea Res. Pt I 141, 83-92. 10.1016/j.dsr.2018.09.009
Parmentier, E., Bouillac, G., Dragicevic, B., Dulcic, J., and Fine, M. L. (2010). "Call properties and morphology of the sound-producing organ in Ophidion rochei (Ophidiidae)," J. Exp. Biol. 213, 3230-3236. 10.1242/jeb.044701
Parmentier, E., and Fine, M. L. (2016). "Fish sound production: Insights," in Vertebrate Sound Production and Acoustic Communication, edited by Suthers, R. A., Fitch, W. T., Fay, R. R., and Popper, A. N. (Springer, New York), pp. 19-49.
Parmentier, E., Fontenelle, N., Fine, M. L., Vandewalle, P., and Henrist, C. (2006). "Functional morphology of the sonic apparatus in Ophidion barbatum (Teleostei, Ophidiidae)," J. Morphol. 267, 1461-1468. 10.1002/jmor.10496
Picciulin, M., Bolgan, M., Codarin, A., Fiorin, R., Zucchetta, M., and Malavasi, S. (2013). "Passive acoustic monitoring of Sciaena umbra on rocky habitats in the Venetian littoral zone," Fish. Res. 145, 76-81. 10.1016/j.fishres.2013.02.008
Picciulin, M., Kéver, L., Parmentier, E., and Bolgan, M. (2018). "Listening to the unseen: Passive acoustic monitoring reveals the presence of a cryptic fish species," Aquat. Conserv. 29 (2), 2-10. 10.1002/aqc.2973
Priede, I. G. (2017). Deep-Sea Fishes: Biology, Diversity, Ecology and Fisheries (Cambridge University Press, Cambridge, UK).
Rako-Gospić, N., and Picciulin, M. (2018). "Underwater noise: Sources and effects on marine life," in World Seas: An Environmental Evaluation (Academic Press, New York), pp. 367-389.
Rountree, R. A., and Bowers-Altman, J. (2002). "Soniferous behaviour of the striped cusk-eel Ophidion marginatum," Bioacoustics 12 (2-3), 240-242. 10.1080/09524622.2002.9753709
Rountree, R. A., Gilmore, R. G., Goudey, C. A., Hawkins, A. D., Luczkovich, J. J., and Mann, D. A. (2006). "Listening to fish: Applications of passive acoustics to fisheries science," Fisheries 31 (9), 433-446. 10.1577/1548-8446(2006)31[433:LTF]2.0.CO;2
Rountree, R. A., and Juanes, F. (2010). "First attempt to use a remotely operated vehicle to observe soniferous fish behavior in the Gulf of Maine, Western Atlantic Ocean," Cur. Zool. 56 (1), 90-99. 10.1093/czoolo/56.1.90
Rountree, R. A., Juanes, F., Goudey, C. A., and Ekstrom, K. E. (2012). "Is biological sound production important in the deep sea?," in The Effects of Noise on Aquatic Life (Springer, New York), pp. 181-183.
Rountree, R. A., Bolgan, M., and Juanes, F. (2018a). "How can we understand freshwater soundscapes without fish sound descriptions?," Fisheries 44 (3), 137-143. 10.1002/fsh.10190
Rountree, R. A., Juanes, F., and Bolgan, M. (2018b). "Air movement sound production by alewife, white sucker, and four salmonid fishes suggests the phenomenon is widespread among freshwater fishes," PloS One 13 (9), e0204247. 10.1371/journal.pone.0204247
Rowell, T. J., Demer, D. A., Aburto-Oropeza, O., Cota-Nieto, J. J., Hyde, J. R., and Erisman, B. E. (2017). "Estimating fish abundance at spawning aggregations from courtship sound levels," Sci. Rep. 7 (1), 3340. 10.1038/s41598-017-03383-8
Ruppé, L., Clément, G., Herrel, A., Ballesta, L., Décamps, T., Kéver, L., and Parmentier, E. (2015). "Environmental constraints drive the partitioning of the soundscape in fishes," PNAS 112 (19), 6092-6097. 10.1073/pnas.1424667112
Sierra-Flores, R., Atack, T., Migaud, H., and Davie, A. (2015). "Stress response to anthropogenic noise in Atlantic cod Gadus morhua L," Aquacult. Eng. 67, 67-76. 10.1016/j.aquaeng.2015.06.003
Širović, A., Cutter, G. R., Butler, J. L., and Demer, D. A. (2009). "Rockfish sounds and their potential use for population monitoring in the Southern California Bight," ICES J. Mar. Sci. 66 (6), 981-990. 10.1093/icesjms/fsp064
Širović, A., and Demer, D. A. (2009). "Sounds of captive rockfishes," Copeia 3, 502-509. 10.1643/CP-08-121
Skliris, N., Goffart, A., Hecq, J. H., and Djenidi, S. (2001). "Shelf-slope exchanges associated with a steep submarine canyon off Calvi (Corsica, NW Mediterranean Sea): A modeling approach," J. Geophys. Res. 106, 19883-19901, https://doi.org/10.1029/2000JC000534.
Slabbekoorn, H., Bouton, N., van Opzeeland, I., Coers, A., ten Cate, C., and Popper, A. N. (2010). "A noisy spring: The impact of globally rising underwater sound levels on fish," Trends Ecol. Evol. 25 (7), 419-427. 10.1016/j.tree.2010.04.005
Stefanescu, C., Morales-Nin, B., and Massuti, E. (1994). "Fish assemblage on the slope in the Catalan Sea (western Mediterranean): Influence of a submarine canyon," J. Mar. Biol. Assoc. UK 74 (3), 499-512. 10.1017/S0025315400047627
Straight, C. A., Freeman, B. J., and Freeman, M. C. (2014). "Passive acoustic monitoring to detect spawning in large-bodied catostomids," Trans. Am. Fish. Soc. 143, 595-605. 10.1080/00028487.2014.880737
Wahlberg, M., and Westerberg, H. (2003). "Sounds produced by herring (Clupea harengus) bubble release," Aquat. Res. 3, 271-275. 10.1016/S0990-7440(03)00017-2
Wall, C. C., Mann, D. A., Lembke, C., Taylor, C., He, R., and Kellison, T. (2017). "Mapping the soundscape off the southeastern USA by using passive acoustic glider technology," Mar. Coastal Fish. 9 (1), 23-37. 10.1080/19425120.2016.1255685
Wall, C. C., Rountree, R. A., Pomerleau, C., and Juanes, F. (2014). "An exploration for deep-sea fish sounds off Vancouver Island from the NEPTUNE Canada ocean observing system," Deep Sea Res. Pt I 83, 57-64. 10.1016/j.dsr.2013.09.004
Wall, C. C., Simard, P., Lembke, C., and Mann, D. A. (2013). "Large-scale passive acoustic monitoring of fish sound production on the West Florida Shelf," Mar. Ecol. Progr. Ser. 484, 173-188. 10.3354/meps10268
Wang, Z. T., Nowacek, D. P., Akamatsu, T., Wang, K. X., Liu, J. C., Duan, G. Q., Cao, H. J., and Wang, D. (2017). "Diversity of fish sound types in the Pearl River Estuary, China," PeerJ 5, e3924. 10.7717/peerj.3924
Wilson, B., Batty, R. S., and Dill, L. M. (2004). "Pacific and Atlantic herring produce burst pulse sounds," Proc. R. Soc. Lond. B: Biol. Sci. 271 (3), 95-97. 10.1098/rsbl.2003.0107
Würtz, M. (2012). Mediterranean Submarine Canyons. Ecology and Governance (IUCN, Málaga, Spain), p. 193.
Zhang, X., Guo, H., Zhang, S., and Song, J. (2015). "Sound production in marbled rockfish (Sebastiscus marmoratus) and implications for fisheries," Integrat. Zool. 10 (1), 152-158. 10.1111/1749-4877.12105