Consistency of spatiotemporal sound features supports the use of passive acoustics for long-term monitoring

Parmentier, Eric; Di Iorio, Lucia; Picciulin, Marta; Malavasi, Stefano; Lagardère, Jean-Paul; Bertucci, Frédéric

doi:10.1111/acv.12362

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Consistency of spatiotemporal sound features supports the use of passive acoustics for long-term monitoring

Parmentier, Eric; Di Iorio, Lucia; Picciulin, Marta et al.

2018 • In Animal Conservation

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https://hdl.handle.net/2268/213060

DOI
10.1111/acv.12362

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Keywords :

acoustic monitoring; Sciaenidae; conservation; sentinel species

Abstract :

[en] Many studies stress the usefulness of fish calls as effective indicators of distinct species occurrence. However, most of these studies have been undertaken in a given area and during restricted periods of time. There is a need to show passive acoustic monitoring is a reliable method to study vocal species over space and time. This study aims to use passive acoustic methods to follow the brown meagre Sciaena umbra at relevant temporal and spatial scales. Specimens of S. umbra were recorded in both aquarium and in the field. In situ recordings were made at two regions (Corsica and Sardinia) during four summers (2008–2012–2013–2015). Temporal and frequency parameters of the fish calls were collected by different teams and compared to test the ability to unequivocally identify the fish sound. The comparison between our data and the bibliography highlights the capability to identify S. umbra during a period of 17 years in different Mediterranean regions, clearly supporting the usefulness of acoustic monitoring to discover and protect aggregation sites of this endangered species. The sound producing mechanism in S. umbra consists of high-speed sonic muscles surrounding dorsally the posterior end of the swim bladder, which can explain the low acoustic variability that helps in the species identification. Similar mechanisms are found in other Sciaenidae, suggesting that a similar conclusion can be drawn for many other adult sciaenids that could be used as sentinel species. This study should be of high interest to policymakers and scientists because it shows passive acoustic can be confidently used in resource management.

Research center :

AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège

Disciplines :

Zoology

Author, co-author :

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

Di Iorio, Lucia

Picciulin, Marta

Malavasi, Stefano

Lagardère, Jean-Paul

Bertucci, Frédéric

Language :

English

Title :

Consistency of spatiotemporal sound features supports the use of passive acoustics for long-term monitoring

Publication date :

2018

Journal title :

Animal Conservation

ISSN :

1367-9430

eISSN :

1469-1795

Publisher :

Blackwell Publishing, Oxford, United Kingdom

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]

Available on ORBi :

since 19 July 2017

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Bibliography

Alós, J. & Cabanellas-Reboredo, M. (2012). Experimental acoustic telemetry experiment reveals strong site fidelity during the sexual resting period of wild brown meagre, Sciaena umbra. J. Appl. Ichthyol. 28, 606–611.
Amorim, M.C.P., Fonseca, P.J. & Almada, V.C. (2003). Sound production during courtship and spawning of Oreochromis mossambicus : male – female and male – male interactions. J. Fish Biol. 62, 658–672.
Amorim, M.C.P., Simoes, J.M., Mendonça, N., Bandarra, N.M., Almada, V.C. & Fonseca, P.J. (2010). Lusitanian toadfish song reflects male quality. J. Exp. Biol. 213, 2997–3004.
Amorim, M.C.P., Simões, J.M., Almada, V.C. & Fonseca, P.J. (2011). Stereotypy and variation of the mating call in the Lusitanian toadfish, Halobatrachus didactylus. Behav. Ecol. Sociobiol. 65, 707–716.
Amorim, M.C.P., Pedroso, S.S., Bolgan, M., Jordão, J.M., Caiano, M. & Fonseca, P.J. (2013). Painted gobies sing their quality out loud: acoustic rather than visual signals advertise male quality and contribute to mating success. Funct. Ecol. 27, 289–298.
Bee, M.A., Kozich, C.E., Blackwell, K.J. & Gerhardt, H.C. (2001). Individual variation in advertisement calls of territorial male green frogs, Rana clamitans: implications for individual discrimination. Ethology 107, 65–84.
Bertucci, F., Lejeune, P., Payrot, J. & Parmentier, E. (2015). Sounds produced by the dusky grouper (Epinephelus marginatus) during its spawning season in the Mediterranean Sea. J. Fish Biol. 87, 400–421.
Bonacito, C., Costantini, M., Picciulin, M., Ferrero, E.A. & Hawkins, A.D. (2001). Acoustical and temporal features of Sciaena umbra (Sciaenidae) in the Miramare marine reserve (Gulf of Trieste, Italy). In Proceeding of the XVIII IBAC, International Bioacoustics Council Meeting, Cogne.
Bonacito, C., Costantini, M., Picciulin, M., Ferrero, E.A. & Hawkins, A.D. (2002). Passive hydrophone census of Sciaena umbra (Sciaenidae) in the Gulf of Trieste (Northern Adriatic sea, Italy). Bioacoustics 12, 292–294.
Boyle, K.S., Colleye, O. & Parmentier, E. (2014). Sound production to electric discharge: sonic muscle evolution in progress in Synodontis spp. catfishes (Mochokidae). Proc. R. Soc. B Biol. Sci. 281, 1197.
Boyle, K.S., Bolen, G. & Parmentier, E. (2015a). Agonistic sounds and swim bladder morphology in a malapterurid electric catfish. J. Zool. (Lond.) 296, 249–260.
Boyle, K.S., Riepe, S., Bolen, G. & Parmentier, E. (2015b). Variation in swim bladder drumming sounds from three doradid catfish species with similar sonic morphologies. J. Exp. Biol. 218, 2881–2891.
Budka, M. & Osiejuk, T.S. (2013). Formant frequencies are acoustic cues to caller discrimination and are a weak indicator of the body size of corncrake males. Ethology 119, 960–969.
Ceugniet, M., Aubin, T., Bernard-Laurent, A. & Soyez, D. (1999). Vocal signatures of the rally call of red-legged and rock partridges and of their hybrids. C.R. Acad. Sci. 322, 887–895.
Chakroun-Marzouk, N. & Ktari, M.H. (2003). Le corb des côtes tunisiennes Sciaena umbra (Sciaenidae): cycle sexuel, âge et croissance. Cybium 27, 211–225.
Chao, L.N. (1986). Sciaenidae. In Fishes of the Eastern Atlantic and Mediterranean: 865–874. Whitehead, P.J.P., Bauchot, M.-L., Hureau, J.C. & Tortonese, E. (Eds). Paris: UNESCO.
Chauvet, C. (1991). Le corb ou brown meagre (Sciaena umbra – Linnaeus, 1758) quelques éléments de sa biologie. In Les Espèces Marines à Protéger en Méditerranée: 229–231. Boudouresque, C.F., Avon, M. & Gravez, V. (Eds). France: GIS Posidonie.
Codarin, A., Picciulin, M., Sebastianutto, L., Calcagno, G., Spoto, M. & Ferrero, E.A. (2012). Nocturnal acoustic activity in the shallow waters of WWF-Miramare Natural Marine Reserve (Trieste, Italy). In Effects of Noise on Aquatic Life, Advances in Experimental Medicine and Biology, 730: 161–164. Popper, A.N. & Hawkins, A.D. (Eds). New York: Springer Science + Business Media, LLC.
Connaughton, M.A. & Taylor, M.H. (1995). Seasonal and daily cycles in sound production associated with spawning in weakfish, Cynoscion regalis. Environ. Biol. Fishes 42, 233–240.
Connaughton, M.A., Fine, M.L. & Taylor, M.H. (1997). The effects of seasonal hypertrophy and atrophy on fiber morphology, metabolic substrate concentration and sound characteristics of the weakfish sonic muscle. J. Exp. Biol. 200, 2449–2457.
Connaughton, M.A., Taylor, M.H. & Fine, M.L. (2000). Effects of fish size and temperature on weakfish disturbance calls: implications for the mechanism of sound generation. J. Exp. Biol. 203, 1503–1512.
Connaughton, M.A., Fine, M.L. & Taylor, M.H. (2002). Weakfish sonic muscle: influence of size, temperature and season. J. Exp. Biol. 205, 2183–2188.
Dijkgraaf, S. (1947). Ein Tone erzeugender Fisch im Neapler Aquarium. Experientia 3, 493–494.
Engin, S. & Seyhan, K. (2009). Biological characteristics of rock goby, Gobius paganellus (Actinopterygii: Perciformes: Gobiidae), in the south-eastern Black sea. Acta Ichthyol. Piscat. 39, 111–118.
Fine, M.L. & Parmentier, E. (2015). Mechanisms of sound production. In Sound communication in fishes: 77–126. Ladich, F. (Ed). Wien: Springer.
Fish, J.F. & Cummings, W.C. (1972). A 50-dB increase in sustained ambient noise from fish (Cynoscion xanthulus). J. Acoust. Soc. Am. 52, 1266–1270.
Fish, M.P. & Mowbray, H.M. (1970). Sounds of Western North Atlantic Fishes. Baltimore: The Johns Hopkins Press.
Francescon, A. & Barbaro, A. (1999). Umbrina cirrosa produzione e allevamento in cattività. Manuale di divulgazione, Serie Acquacultura. Verona: Veneto Agricoltura. Corella Poligrafica.
Gerhardt, H.C. (1991). Female mate choice in treefrogs: static and dynamic acoustic criteria. Anim. Behav. 42, 615–635.
Grau, A., Linde, M. & Grau, A.M. (2009). Reproductive biology of the vulnerable species Sciaena umbra Linnaeus, 1758 (Pisces: Sciaenidae). Sci. Mar. 73, 67–81.
Guest, W.C. & Lasswell, J.L. (1978). A note on courtship behavior and sound production of Red Drum. Copeia 1978, 337–338.
Hernandez, K.M., Risch, D., Cholewiak, D.M., Dean, M.J., Hatch, L.T., Hoffman, W.S., Rice, A.N., Zemeckis, D. & Van Parijs, S.M. (2013). Acoustic monitoring of Atlantic cod (Gadus morhua) in Massachusetts Bay: implications for management and conservation. ICES J. Mar. Sci. J. du Cons. 70, 628–635.
Hill, G.L., Fine, M.L. & Musick, J.A. (1987). Ontogeny of the sexually dimorphic sonic muscle in three sciaenid species. Copeia 3, 708–713.
Holt, G.J., Holt, S.A. & Arnold, C.R. (1985). Diel periodicity of spawning in sciaenids. Mar. Ecol. Prog. Ser. 27, 1–7.
Ladich, F. & Myrberg, A.A.J. (2006). Agonistic behavior and acoustic communication. In Communication in fishes: 122–148. Ladich, F., Collin, S.P., Moller, P. & Kapoor, B.G. (Eds). Enfield: Science Publishers.
Lagardère, J.P. & Mariani, A. (2006). Spawning sounds in meagre Argyrosomus regius recorded in the Gironde estuary, France. J. Fish Biol. 69, 1697–1708.
Lagardère, J.-P. & Parmentier, É. (2014). Les sons de contact de l'ombrine côtière – Umbrina cirrosa (Linné, 1758). Bull. Soc. Borda 514, 214–217.
Lengagne, T. (2001). Temporal stability in the individual features in the calls of eagle owls (Bubo bubo). Behaviour 138, 1407–1419.
Luczkovich, J.J., Sprague, M.W., Johnson, S.E. & Pullinger, R.C. (1999). Delimiting spawning areas of weakfish, Cynoscion regalis (family Sciaenidae) in Pamlico Sound, North Carolina using passive hydroacoustic surveys. Bioacoustics 10, 143–160.
Luczkovich, J.J., Mann, D.A. & Rountree, R.A. (2008). Passive acoustics as a tool in fisheries science. Trans. Am. Fish. Soc. 137, 533–541.
Mann, D.A. & Grothues, T.M. (2009). Short-term upwelling events modulate fish sound production at a mid-Atlantic ocean observatory. Mar. Ecol. Prog. Ser. 375, 65–71.
Mann, D.A., Bowers-Altman, J. & Rountree, R.A. (1997). Sounds produced by the striped cusk-eel Ophidion marginatum (Ophidiidae) during courtship and spawning. Copeia 3, 610–612.
Millot, S. & Parmentier, E. (2014). Development of the ultrastructure of sonic muscles : a kind of neoteny? BMC Evol. Biol. 14, 1–9.
Millot, S., Vandewalle, P. & Parmentier, E. (2011). Sound production in red-bellied piranhas (Pygocentrus nattereri, Kner): an acoustical, behavioural and morphofunctional study. J. Exp. Biol. 214, 3613–3618.
Mok, H.K. & Gilmore, R.G. (1983). Analysis of sound production in estuarine aggregations of Pogonias cromis, Bairdiella chrysoura, and Cynoscion nebulosus (Sciaenidae). Bull. Inst. Zool. Acad. Sin. 22, 157–186.
Montie, E.W., Vega, S. & Powell, M. (2015). Seasonal and spatial patterns of fish sound production in the May River, South Carolina. Trans. Am. Fish. Soc. 144, 705–716.
Montie, E.W., Kehrer, C., Yost, J., Brenkert, K., O'Donnell, T. & Denson, M. R. (2016). Long-term monitoring of captive red drum Sciaenops ocellatus reveals that calling incidence and structure correlate with egg deposition. J. Fish Biol. 88, 1776–1795.
Mooney, T.A., Kaplan, M.B., Izzi, A., Lamoni, L. & Sayigh, L. (2016). Temporal trends in cusk eel sound production at a proposed US wind farm site. Aquat. Biol. 24, 201–210.
Myrberg, J.A.A. & Lugli, M. (2006). Reproductive behavior and acoustic communication. In Communication in Fishes: 149–176. Ladich, F., Collin, S.P., Moller, P. & Kapoor, B.G. (Eds). Endfield: Science Publishers.
Ono, R.D. & Poss, S.G. (1982). Structure and innervations of the swimbladder musculature in the weakfish, Cynoscion regalis (Teleostei: Sciaenidae). Can. J. Zool. 60, 1955–1967.
Parmentier, E. & Fine, M.L. (2016). Fish sound production: insight. In Vertebrate sound production and acoustic communication: 19–49. Suthers, R., Tecumseh, F., Popper, A.N. & Fay, R.R. (Eds). New York: Springer.
Parmentier, E., Tock, J., Falguière, J.-C. & Beauchaud, M. (2014). Sound production in Sciaenops ocellatus: preliminary study for the development of acoustic cues in aquaculture. Aquaculture 432, 204–211.
Pedroso, S.S., Barber, I., Svensson, O., Fonseca, P.J. & Amorim, M.C.P. (2013). Courtship sounds advertise species identity and male quality in sympatric Pomatoschistus spp. gobies. PLoS ONE 8, e64620.
Picciulin, M., Calcagno, G., Sebastianutto, L., Bonacito, C., Codarin, A., Constantini, M. & Ferrero, E.A. (2012a). Diagnostics of nocturnal calls of Sciaenia umbra (L., fam. Sciaenidae) in a near shore Mediterranean marine reserve. Bioacoustics 2012, 1–12.
Picciulin, M., Sebastianutto, L., Codarin, A., Calcagno, G. & Ferrero, E.A. (2012b). Brown meagre vocalization rate increases during repetitive boat noise exposures: a possible case of vocal compensation. J. Acoust. Soc. Am. 132, 3118–3124.
Picciulin, M., Bolgan, M., Codarin, A., Fiorin, R., Zucchetta, M. & Malavasi, S. (2013). Passive acoustic monitoring of Sciaena umbra on rocky habitats in the Venetian littoral zone. Fish. Res. 145, 76–81.
Picciulin, M., Bolgan, M., Coro, A.B., Calcagno, G. & Malavasi, S. (2016). Sound production by the Shi drum Umbrina cirrosa and comparison with the brown meagre Sciaena umbra: a passive acoustic monitoring perspective. J. Fish Biol. 88, 1655–1660.
R Core Team (2014). R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. Available at: http://www.R-project.org/.
Ramcharitar, J.U., Gannon, D.P. & Popper, A.N. (2006). Bioacoustics of fishes of the family Scianidae (croackers and drums). Trans. Am. Fish. Soc. 135, 1409–1431.
Ruppé, L., Clément, G., Herrel, A., Ballesta, L., Décamps, T., Kéver, L. & Parmentier, E. (2015). Environmental constraints drive the partitioning of the soundscape in fishes. Proc. Natl Acad. Sci. USA 112, 6092–6097.
Saucier, M.H. & Baltz, D.M. (1993). Spawning site selection by spotted seatrout, Cynoscion nebulosus, and black drum, Pogonias cromis, in Louisiana. Environ. Biol. Fishes 36, 257–272.
Sprague, M.W. (2000). The single sonic muscle twitch model for the sound-production mechanism in the weakfish, Cynoscion regalis. J. Acoust. Soc. Am. 108, 2430–2437.
Tellechea, J.S., Martinez, C., Fine, M.L. & Norbis, W. (2010). Sound production in the whitemouth croaker and relationship between fish size and disturbance call characteristics. Environ. Biol. Fishes 89, 163–172.
Tellechea, J.S., Fine, M.L. & Norbis, W. (2017). Passive acoustic monitoring, development of disturbance calls and differentiation of disturbance and advertisement calls in the Argentine croaker Umbrina canosai (Sciaenidae). J. Fish Biol. 90, 1631–1643.
Tower, R.W. (1908). The production of sound in the drumfishes, the searobin and the toadfish. Ann. N. Y. Acad. Sci. 18, 149–180.
Tricas, T. & Boyle, K. (2014). Acoustic behaviors in Hawaiian coral reef fish communities. Mar. Ecol. Prog. Ser. 511, 1–16.
Vasconcelos, R.O., Carricço, R., Ramos, A., Modesto, T., Fonseca, P.J. & Amorim, M.C.P. (2012). Vocal behavior predicts reproductive success in a teleost fish. Behav. Ecol. 23, 375–383.