[en] In the Mediterranean Sea, the seagrass Posidonia oceanica plays a key ecological
role, and is protected by a range of legislation. Standard Posidonia monitoring
programmes generally focus on the plant at different spatial and short temporal
scales, without considering the organisms dependent on the ecosystem. Passive
acoustic monitoring (PAM) has a high potential to non-intrusively monitor
biological activities and biodiversity at high temporal resolution, and to assess
ecosystem health. This is particularly relevant considering that Posidonia meadows
host numerous sound-producing fish species. In this study, bottommoored
hydrophones were deployed in nine Western Mediterranean meadows
covering a distance of more than 200 km to identify acoustic features potentially
relevant to monitor this critical habitat. Among eight identified fish sound
categories, we found a single type of sound (that we will refer to as /kwa/)
dominating the soundscape of Posidonia meadows over a time span of 7
months. Compared to other low-frequency sounds, the /kwa/ presented unique
characteristics that suggest it is produced by a fish via fast contracting muscles.
The /kwa/ was the only sound detectable under anthropogenic noise conditions,
and little affected by it. Cluster analyses performed on 13 acoustic features
revealed a high degree of call diversity. /Kwa/ diversity, combined with its
large-scale (all meadows), long-term (7 months) occurrence and low noise
interference, make the /kwa/ a promising candidate for PAM of Posidonia
meadows. Furthermore, variability in acoustic features suggests a central role of
the /kwa/ in communication. Overall, this work sets the basis for establishing
the relevance of the /kwa/ in monitoring P. oceanica meadows and developing
PAM techniques for this critical habitat.
Disciplines :
Aquatic sciences & oceanology
Author, co-author :
Di Iorio, Lucia ✱; Chorus Research Institute
Raick, Xavier ✱; Chair Chorus, Foundation of the Grenoble Institute of Technology
Parmentier, Eric ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive
Boissery, Pierre; Agence de l’Eau Rhone Méditerranée Corse
Valentini-Poirier, Cathy-Anna; Agence de l’Eau Rhone Méditerranée Corse
Gervaise, Cédric; Chorus Research Institute
✱ These authors have contributed equally to this work.
Language :
English
Title :
‘Posidonia meadows calling’: a ubiquitous fish sound with monitoring potential
Alternative titles :
[fr] 'L'appel de l'herbier de posidonies" : un son omniprésent avec un potentiel de monitoring [es] 'La llamada de la pradera de posidonia" : un sonido omnipresente con un potencial de monitoreo
Publication date :
January 2018
Journal title :
Remote Sensing in Ecology and Conservation
eISSN :
2056-3485
Publisher :
y John Wiley & Sons Ltd on behalf of Zoological Society of London
Amorim, M. C. P., and R. O. Vasconcelos. 2008. Variability in the mating calls of the Lusitanian toadfish Halobatrachus didactylus: cues for potential individual recognition. J. Fish Biol. 73, 1267–1283. https://doi.org/10.1111/j.1095-8649.2008.01974.x.
Amorim, M. C. P., Y. Stratoudakis, and A. D. Hawkins. 2004. Sound production during competitive feeding in the grey gurnard. J. Fish Biol. 65, 182–194. https://doi.org/10.1111/j.0022-1112.2004.00443.x.
Amorim, M. C. P., R. O. Vasconcelos, J. F. Marques, and F. Almada. 2006. Seasonal variation of sound production in the Lusitanian toadfish, Halobatrachus didactylus. J. Fish Biol. 69, 1892–1899. https://doi.org/10.1111/j.1095-8649.2006.01247.x.
Amorim, M. C. P., J. M. Simões, and P. J. Fonseca. 2008. Acoustic communication in the Lusitanian toadfish, Halobatrachus didactylus: evidence for an unusual large vocal repertoire. J. Mar. Biol. Assoc. U.K. 88, 1069–1073.https://doi.org/10.1017/S0025315408001677
Andromède Océanologie (2015). Plaquette de présentation de TEMPO, un réseau de surveillance des herbiers de posidonie en mer Méditerrané (Andromède & Agence de l'eau RMC, Eds.). http://www.observatoire-mer.fr/img/tempo.pdf
Ardizzone, G., A. Belluscio, and L. Maiorano. 2006. Long-term change in the structure of a Posidonia oceanica landscape and its reference for a monitoring plan. Mar. Ecol. 27, 299–309. https://doi.org/10.1111/j.1439-0485.2006.00128.x.
Bertucci, F., E. Parmentier, G. Lecellier, A. D. Hawkins, and D. Lecchini. 2016. Acoustic indices provide information on the status of coral reefs: an example from Moorea Island in the South Pacific. Sci. Rep. 6, 33326. https://doi.org/10.1038/srep33326.
Blom, E. L., I. Mück, K. Heubel, and O. Svensson. 2016. Acoustic and visual courtship traits in two sympatric marine Gobiidae species – Pomatoschistus microps and Pomatoschistus minutus. Environ. Biol. Fishes 99, 999–1007. https://doi.org/10.1007/s10641-016-0550-5.
Bonacorsi, M., C. Pergent-Martini, N. Breand, and G. Pergent. 2013. Is Posidonia oceanica regression a general feature in the Mediterranean Sea? Mediterr. Mar. Sci. 14, 193–203.
Boudouresque, C. F., E. Charbonel, A. Meinesz, G. Pergent, C. Pergent-Martini, G. Cadiou, et al. 2000. A monitoring network based on the seagrass Posidonia oceanica in the Northwestern Mediterranean Sea. Biol. Mar. Mediterr. 7, 328–331.
Boudouresque, C. F., G. Bernad, P. Bonhomme, E. Charbonnel, L. Le Diréach, and S. Ruitton. 2007. Monitoring methods for Posidonia oceanica seagrass meadows in Provence and the French Riviera. Sci. Rep. Port-Cros Natl. Park 22, 17–38.
Boudouresque, C.-F., G. Bernard, P. Bonhomme, E. Charbonnel, G. Diviacco, A. Meinesz, et al. 2012. Pp. 1–202. Protection and conservation of Posidonia oceanica meadows. RAMOGE and RAC/SPA publisher, Tunis.
Boyle, K. S., S. Riepe, G. Bolen, and E. Parmentier. 2015. Variation in swim bladder drumming sounds from three doradid catfish species with similar sonic morphologies. J. Exp. Biol. https://doi.org/10.1242/jeb.123414.10.1242/jeb.123414.
Brumm, H, and M. Naguib. 2009. Chapter 1 Environmental Acoustics and the Evolution of Bird Song. Vol 40, Pp. 1–33. Advances in the Study of Behavior. Academic Press, London.
Cato, D. H. 1978. Marine biological choruses observed in tropical waters near Australia. J. Acoust. Soc. Am. 64, 736. https://doi.org/10.1121/1.382038.
Connaughton, M. A. 2004. Sound generation in the searobin (Prionotus carolinus), a fish with alternate sonic muscle contraction. J. Exp. Biol. 207, 1643–1654. https://doi.org/10.1242/jeb.00928.
Connaughton, M. A., and M. Taylor. 1995. Seasonal and daily cycles in sound production associated with spawning in the weakfish, Cynoscion regalis. Environ. Biol. Fishes 42, 233–240. https://doi.org/10.1007/BF00004916.
Connaughton, M. A., M. L. Fine, and M. H. Taylor. 2002. Review. Weakfish sonic muscle: influence of size, temperature and season. J. Exp. Biol. 205, 2183–2188.
Coquereau, L., J. Grall, L. Chauvaud, C. Gervaise, J. Clavier, A. Jolivet, et al. 2016. Sound production and associated behaviors of benthic invertebrates from a coastal habitat in the north-east Atlantic. Mar. Biol. 163, 127. https://doi.org/10.1007/s00227-016-2902-2.
Descamp, P., F. Holon, L. Ballesta, A. Guilbert, M. Guillot, P. Boissery, et al. 2011. Fast and easy method for seagrass monitoring: Application of acoustic telemetry to precision mapping of Posidonia oceanica beds. Mar. Pollut. Bull. 62, 284–292. https://doi.org/10.1016/j.marpolbul.2010.10.012.
Farina, A., and S. H. Gage. 2017. Ecoacoustics: The Ecological Role of Sounds. in A. Farina S. H. Gage, eds. John Wiley & Sons, Ltd, Oxford.
Gerhardt, H. C. 1981. Mating call recognition in the green treefrog (Hyla cinerea): importance of two frequency bands as a function of sound pressure level. J. Comp. Physiol. A. 144, 9–16. https://doi.org/10.1007/BF00612792.
Gobert, S., S. Sartoretto, V. Rico-Raimondino, B. Andral, A. Chery, P. Lejeune, et al. 2009. Assessment of the ecological status of Mediterranean French coastal waters as required by the water framework directive using the Posidonia oceanica rapid easy index: PREI. Mar. Pollut. Bull. 58, 1727–1733. https://doi.org/10.1016/J.MARPOLBUL.2009.06.012.
Grava, T. 2006. Effect of habitat quality on communication and signalling in the black-capped chickadee. Thesis at the University of Northern British Columbia. Accessed from https://www.unbc.ca/sites/default/files/sections/ken-otter/phdthesis-thibaultgravafinal.pdf
Guillén, J. E., J. L. Sanchez Lizaso, S. Jiménez, J. Martinez, A. Codina, M. Montero, et al. 2013. Evolution of Posidonia oceanica seagrass meadows and its implications for management. J. Sea Res. 83, 65–71. https://doi.org/10.1016/j.seares.2013.04.012.
Hastings, P., and A. Širović. 2015. Soundscapes offer unique opportunities for studies of fish communities. Proc. Natl Acad. Sci. USA 112, 5866–5867.
Holon, F., P. Boissery, A. Guilbert, E. Freschet, and J. Deter. 2015a. The impact of 85 years of coastal development on shallow seagrass beds (Posidonia oceanica L. (Delile)) in South Eastern France: a slow but steady loss without recovery. Estuar. Coast. Shelf Sci. 165, 204–212. https://doi.org/10.1016/j.ecss.2015.05.017.
Holon, F., N. Mouquet, P. Boissery, M. Bouchoucha, G. Delaruelle, A. S. Tribot, et al. 2015b. Fine-scale cartography of human impacts along French Mediterranean coasts: a relevant map for the management of marine ecosystems. PLoS ONE 10, e0135473. https://doi.org/10.1371/journal.pone.0135473.
Kalogirou, S., M. Corsini-Foka, A. Sioulas, H. Wennhage, and L. Pihl. 2010. Diversity, structure and function of fish assemblages associated with Posidonia oceanica beds in a biodiversity enrichment in a diverse world area of the eastern Mediterranean Sea and the role of non-indigenous species. J. Fish Biol. 77, 2338–2357. https://doi.org/10.1111/j.1095-8649.2010.02817.x.
Kéver, L., K. S. Boyle, and E. Parmentier. 2015. Effects of seawater temperature on sound characteristics in Ophidion rochei (Ophidiidae). J. Fish Biol. 87, 502–509. https://doi.org/10.1111/jfb.12730.
Kéver, L., P. Lejeune, L. N. Michel, and E. Parmentier. 2016. Passive acoustic recording of Ophidion rochei calling activity in Calvi Bay (France). Mar. Ecol. 37, 1315–1324. https://doi.org/10.1111/maec.12341.
Kinda, G. B., Y. Simard, C. Gervaise, J. I. Mars, and L. Fortier. 2013. Under-ice ambient noise in Eastern Beaufort Sea, Canadian Arctic, and its relation to environmental forcing. J. Acoust. Soc. Am. 134(1), 77–87. https://doi.org/10.1121/1.4808330.
Ladich, F. 2015. Sound communication in fishes. in F. Ladich, ed. Sprienger-Verlag, Wien.
Ladich, F., and G. Schleinzer. 2014. Effect of temperature on acoustic communication: sound production in the croaking gourami (labyrinth fishes). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 182, 8–13. https://doi.org/10.1016/j.cbpa.2014.11.013.
Laiolo, P. 2010. The emerging significance of bioacoustics in animal species conservation. Biol. Cons. 143, 1635–1645. https://doi.org/10.1016/J.BIOCON.2010.03.025.
Laiolo, P., and J. L. Tella. 2007. Erosion of animal cultures in fragmented landscapes. Front. Ecol. Environ. 5, 68–72. https://doi.org/10.1890/1540-9295(2007)5[68:EOACIF]2.0.CO;2.
Laiolo, P., M. Vögeli, D. Serrano, and J. L. Tella. 2008. Song diversity predicts the viability of fragmented bird populations. PLoS ONE 3, e1822. https://doi.org/10.1371/journal.pone.0001822.
Lamb, J. B., van de Water J. A. J. M., D. G. Bourne, C. Altier, M. Y. Hein, E. A. Fiorenza, et al. 2017. Seagrass ecosystems reduce exposure to bacterial pathogens of humans, fishes, and invertebrates. Science 355: 731–733.https://doi.org/10.1126/science.aal1956
Le Bot, O., J. I. Mars, C. Gervaise, and Y. Simard. 2015. Rhythmic analysis for click train detection and source separation with examples on beluga whales. Appl. Acoust. 95, 37–49. https://doi.org/10.1016/j.apacoust.2015.02.005.
Lin, M., H. C. J. Lucas, and G. Shmueli. 2013. Too big to fail: large samples and the p-value problem. Inf. Syst. Res. 24, 906–917. https://doi.org/10.1287/isre.2013.0480.
Lopez y Royo, C., G. Pergent, C. Pergent-Martini, and G. Casazza. 2010. Seagrass (Posidonia oceanica) monitoring in western Mediterranean: implications for management and conservation. Environ. Monit. Assess. 171(1–4), 365–380.
Mathias, D., C. Gervaise, and L. Di Iorio. 2016. Wind dependence of ambient noise in a biologically rich coastal area. J. Acoust. Soc. Am. 139, 839–850. https://doi.org/10.1121/1.4941917.
McCauley, R. D., and D. H. Cato. 2000. Patterns of fish calling in a nearshore environment in the Great Barrier Reef. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355, 1289–93. https://doi.org/10.1098/rstb.2000.0686.
McGregor, P. K. 2005. Animal Communication Networks.PK McGregor, eds. Cambridge University Press, Cambridge.
McLachlan, G, Peel, D. 2000. Finite Mixture Models. John Wiley & Sons, Inc: Hoboken, NJ.
Mellinger, D., K. Stafford, S. Moore, R. Dziak, and H. Matsumoto. 2007. An overview of fixed passive acoustic observation methods for cetaceans. Oceanography 20, 36–45.https://doi.org/10.5670/oceanog.2007.03
Nguyen, T. K., H. Lin, E. Parmentier, and M. L. Fine. 2008. Seasonal variation in sonic muscles in the fawn cusk-eel Lepophidium profundorum. Biol. Lett. 4, 707–710. https://doi.org/10.1098/rsbl.2008.0383.
Noël, C., P. Boissery, N. Quelin, and V. Raimondino. 2012. Cahier Technique du Gestionnaire: analyse comparée des méthodes de surveillance des herbiers de posidonies, Pp. 96 CartOcean. Dreal PACA, France, Agence de l'eau RMC.
van Oort, H., K. A. Otter, K. T. Fort, and C. I. Holschuh. 2006. Habitat quality, social dominance and dawn chorus song output in black-capped chickadees. Ethology 112, 772–778. https://doi.org/10.1111/j.1439-0310.2006.01228.x.
Parmentier, E., L. Kéver, K. Boyle, Y. E. Corbisier, L. Sawelew, and S. Malavasi. 2013. Sound production mechanism in Gobius paganellus (Gobiidae). J. Exp. Biol. 216, 3189–3199. https://doi.org/10.1242/jeb.087205.
Parmentier, E., M. L. Fine, and H. K. Mok. 2016. Sound production by a recoiling system in the Pempheridae and Terapontidae. J. Morphol. 277, 717–724. https://doi.org/10.1002/jmor.20529.
Parmentier, E., L. Di Iorio, M. Picciulin, S. Malavasi, J. P. Lagardère, and F. Bertucci. 2017. Consistency of spatiotemporal sound features supports the use of passive acoustics for long-term monitoring. Anim. Conserv. https://doi.org/10.1111/acv.12362.
Pedroso, S. S., M. Bolgan, J. M. Jordão, P. J. Fonseca, and M. C. P. Amorim. 2012. Acoustic communication in Pomatoschistus spp.: a comparison between closely related species. Pp. 113–115. The Effects of Noise on Aquatic Life. Springer, New York, NY. doi.org/10.1007/978-1-4419-7311-5_25
Penny, W. D., J. Mattout, and N. Trujillo-Barreto. 2007. Bayesian model selection and averaging. In Statistical Parametric Mapping. Pp. 454–467. Elsevier, London.
Personnic, S., C. F. Boudouresque, P. Astruch, E. Ballesteros, S. Blouet, D. Bellan-Santini, et al. 2014. An Ecosystem-Based Approach to Assess the Status of a Mediterranean Ecosystem, the Posidonia oceanica Seagrass Meadow. PLoS ONE 9, e98994. https://doi.org/10.1371/journal.pone.0098994.
Picciulin, M., M. Bolgan, A. Codarin, R. Fiorin, M. Zucchetta, and S. Malavasi. 2013. Passive acoustic monitoring of Sciaena umbra on rocky habitats in the Venetian littoral zone. Fish. Res. 145, 76–81. https://doi.org/10.1016/j.fishres.2013.02.008.
Picciulin, M., M. Bolgan, A. B. Corò, G. Calcagno, and S. Malavasi. 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. https://doi.org/10.1111/jfb.12926.
Pillsbury, F. C., and J. R. Miller. 2008. Habitat and landscape characteristics underlying anuran community structure along an urban-rural gradient. Ecol. Appl. 18, 1107–1118. https://doi.org/10.1890/07-1899.1.
Price, T., P. Wadewitz, D. L. Cheney, R. M. Seyfarth, K. Hammerschmidt, and J. Fischer. 2015. Vervets revisited: a quantitative analysis of alarm call structure and context specificity. Sci. Rep. 5, 1–11. https://doi.org/10.1038/srep13220.
Radford, A. N., E. Kerridge, and D. Simpson. 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.
Rice, A. N., and A. H. Bass. 2009. Novel vocal repertoire and paired swimbladders of the three-spined toadfish, Batrachomoeus trispinosus: insights into the diversity of the Batrachoididae. J. Exp. Biol. 212, 1377–1391. https://doi.org/10.1242/jeb.028506.
Riede, K. 1998. Acoustic monitoring of Orthoptera and its potential for conservation. J. Insect Conserv. 2(3/4), 217–223. https://doi.org/10.1023/A:1009695813606.
Rosenthal, G. G., and D. Stuart-Fox. 2012. Environmental disturbance and animal communication. Pp. 16–31 in U. Candolin and B. B. M. Wong, eds. Behavioural Responses to a Changing World. Oxford University Press, Oxford.
Rountree, R. A., R. G. Gilmore, C. A. Goudey, A. D. Hawkins, J. J. Luczkovich, and D. A. Mann. 2006. Listening to fish: applications of passive acoustics to fisheries science. Fisheries 31, 443–446.https://doi.org/10.1577/1548-8446(2006)31[433:LTF]2.0.CO;2
Rowe, S., and J. A. Hutchings. 2004. The function of sound production by Atlantic cod as inferred from patterns of variation in drumming muscle mass. Revue canadienne de zoologie 82, 1391–1398. https://doi.org/10.1139/z04-119.
Ruppé, L., G. Clément, A. Herrel, L. Ballesta, T. Décamps, L. Kéver, et al. 2015. Environmental constraints drive the partitioning of the soundscape in fishes. Proc. Natl Acad. Sci. USA 112, 6092–7. https://doi.org/10.1073/pnas.1424667112.
Searby, A., P. Jouventin, and T. Aubin. 2004. Acoustic recognition in macaroni penguins: an original signature system. Anim. Behav. 67, 615–625. https://doi.org/10.1016/j.anbehav.2003.03.012.
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.
Staaterman, E., C. B. Paris, H. A. DeFerrari, D. A. Mann, A. N. Rice, and E. K. D'Alessandro. 2014. Celestial patterns in marine soundscapes. Mar. Ecol. Prog. Ser. 508, 17–32. https://doi.org/10.3354/meps10911.
Sueur, J., S. Pavoine, O. Hamerlynck, S. Duvail, and J. Fjeldså. 2008. Rapid acoustic survey for biodiversity appraisal. PLoS ONE 3, e4065. https://doi.org/10.1371/journal.pone.0004065.
Tucker, S., and G. J. Brown. 2005. Classification of transient sonar sounds using perceptually motivated features. IEEE J. Ocean Eng. 30, 588–600. https://doi.org/10.1109/JOE.2005.850910.
Watkins, W. A. 1968. The harmonic interval: fact or artefact in spectral analysis of pulse trains. Woods Hole Oceanographic Institution, Woods Hole, MA.
Zelick, R., D. A. Mann, and A. N. Popper. 1999. Acoustic communication in fishes and frogs. in R. R. Fay and A. N. Popper, eds. Comparative hearing: fish and amphibians. Springer, New-York.