[en] In oceans, the noise generated by human activities has reached phenomenal proportions, with considerable harmful effects on marine life. Measuring this impact to achieve a sustainable balance for highly vulnerable marine ecosystems, such as coral reefs, is a critical environmental policy objective. Here, we demonstrate that anthropogenic noise alters the interactions of a coral reef fish with its environment and how this behavioural response to noise impairs foraging. In situ observations on the Moorea reef revealed that the damselfish Dascyllus emamo reacts to boat passage by moving closer to its coral bommie, considerably reducing the volume of water available to search for prey. Using boat noise playback experiments in microcosms, we studied D. emamo's behaviour and modeled its functional response (FR), which is the relationship between resource use and resource density, when feeding on juvenile shrimps. Similar to field observations, noise reduced D. emamo's spatial occupancy, accompanied by a lower FR, indicating a reduction in predation independent of prey density. Overall, noise-induced behavioural changes are likely to influence predator-prey interaction dynamics and ultimately the fitness of both protagonists. While there is an urgent need to assess the effect of anthropogenic noise on coral reefs, the ecological framework of the FR approach combined with behavioural metrics provides an essential tool for evaluating the cascading effects of noise on nested ecological interactions at the community level.
Research Center/Unit :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Disciplines :
Zoology
Author, co-author :
Minier, Lana ; PSL Research University: EPHE-UPVD-CNRS, UAR 3278 CRIOBE, Moorea, French Polynesia, Polynésienne des Eaux, Vitale, Bora-Bora, French Polynesia. Electronic address: lanaminier@gmail.com
Bertucci, Frédéric ; UMR MARBEC, University of Montpellier, CNRS, IFREMER, IRD, Sète, France
Gay, Tamatoa; PSL Research University: EPHE-UPVD-CNRS, UAR 3278 CRIOBE, Moorea, French Polynesia
Chamot, Zoé ; PSL Research University: EPHE-UPVD-CNRS, UAR 3278 CRIOBE, Moorea, French Polynesia
Turco, Théophile ; ENES Bioacoustics Research Laboratory, University of Saint-Etienne, CRNL, CNRS UMR 5292, Inserm UMR_S 1028, Saint-Etienne, France
Schligler, Jules ; PSL Research University: EPHE-UPVD-CNRS, UAR 3278 CRIOBE, Moorea, French Polynesia
Mills, Suzanne C; PSL Research University: EPHE-UPVD-CNRS, UAR 3278 CRIOBE, Moorea, French Polynesia, Laboratoire d'Excellence "CORAIL", Perpignan, France, Institut universitaire de France, France
Vidal, Manuel; Institut de Neurosciences de la Timone, UMR 7289, Aix-Marseille Université, CNRS, Marseille, France
Parmentier, Eric ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive
Sturny, Vincent; Polynésienne des Eaux, Vitale, Bora-Bora, French Polynesia
Mathevon, Nicolas ; ENES Bioacoustics Research Laboratory, University of Saint-Etienne, CRNL, CNRS UMR 5292, Inserm UMR_S 1028, Saint-Etienne, France, Institut universitaire de France, France, Ecole Pratique des Hautes Etudes, CHArt Lab, PSL University, Paris, France
Beauchaud, Marilyn ; ENES Bioacoustics Research Laboratory, University of Saint-Etienne, CRNL, CNRS UMR 5292, Inserm UMR_S 1028, Saint-Etienne, France
Lecchini, David; PSL Research University: EPHE-UPVD-CNRS, UAR 3278 CRIOBE, Moorea, French Polynesia
Médoc, Vincent; ENES Bioacoustics Research Laboratory, University of Saint-Etienne, CRNL, CNRS UMR 5292, Inserm UMR_S 1028, Saint-Etienne, France
We would like to thank the staff of Polyn\u00E9sienne des Eaux. This work was supported by the Fondation de France (2019\u201308602), the Office Fran\u00E7ais de la Biodiversit\u00E9 (AFB/2019/385 \u2013 OFB.20.0888), the Polyn\u00E9sienne des Eaux, the projects ANR-19-CE34-0006-Manini and ANR-19-CE14-0010-SENSO, the ANRT grant (CIFRE 2021/1268), the University of Saint-Etienne and the Institut universitaire de France.We would like to thank the staff of Polyn\u00E9sienne des Eaux. This work was supported by the Fondation de France (2019-08602), the Office Fran\u00E7ais de la Biodiversit\u00E9 (AFB/2019/385 \u2013 OFB.20.0888), the Polyn\u00E9sienne des Eaux, the projects ANR-19-CE34-0006-Manini and ANR-19-CE14-0010-SENSO, the ANRT grant (CIFRE 2021/1268), the University of Saint-Etienne and the Institut universitaire de France.
Berendt, R.D., Corliss, E.L.R., Ojalvo, M.S., Quieting: a practical guide to noise control. U.S. Department of Commerce, 1976, National Bureau of Standards.
Bernaldo de Quirós, Y., Fernandez, A., Baird, R.W., Brownell, R.L., Aguilar de Soto, N., Allen, D., Arbelo, M., Arregui, M., Costidis, A., Fahlman, A., Frantzis, A., Gulland, F.M.D., Iñíguez, M., Johnson, M., Komnenou, A., Koopman, H., Pabst, D.A., Roe, W.D., Sierra, E., Tejedor, M., Schorr, G., Advances in research on the impacts of anti-submarine sonar on beaked whales. Proc. Biol. Sci., 286, 2019, 20182533, 10.1098/rspb.2018.2533.
Buckingham, M.J., Wave propagation, stress relaxation, and grain-to-grain shearing in saturated, unconsolidated marine sediments. J. Acoust. Soc. Am. 108 (2000), 2796–2815, 10.1121/1.1322018.
Chan, A.A.Y.-H., Giraldo-Perez, P., Smith, S., Blumstein, D.T., Anthropogenic noise affects risk assessment and attention: the distracted prey hypothesis. Biol. Lett. 6 (2010), 458–461, 10.1098/rsbl.2009.1081.
Coblentz, K.E., DeLong, J.P., Estimating predator functional responses using the times between prey captures. Ecology, 102, 2021, e03307, 10.1002/ecy.3307.
Di Franco, E., Pierson, P., Di Iorio, L., Calò, A., Cottalorda, J.M., Derijard, B., Di Franco, A., Galvé, A., Guibbolini, M., Lebrun, J., Micheli, F., Priouzeau, F., Risso-de Faverney, C., Rossi, F., Sabourault, C., Spennato, G., Verrando, P., Guidetti, P., Effects of marine noise pollution on Mediterranean fishes and invertebrates: a review. Mar. Pollut. Bull., 159, 2020, 111450, 10.1016/j.marpolbul.2020.111450.
Dick, J.T.A., Gallagher, K., Avlijas, S., Clarke, H.C., Lewis, S.E., Leung, S., Minchin, D., Caffrey, J., Alexander, M.E., Maguire, C., Harrod, C., Reid, N., Haddaway, N.R., Farnsworth, K.D., Penk, M., Ricciardi, A., Ecological impacts of an invasive predator explained and predicted by comparative functional responses. Biol. Invasions 15 (2013), 837–846, 10.1007/s10530-012-0332-8.
Dinh, J.P., Suca, J.J., Lillis, A., Apprill, A., Llopiz, J.K., Mooney, T.A., Multiscale spatio-temporal patterns of boat noise on U.S. Virgin Island coral reefs. Mar. Pollut. Bull. 136 (2018), 282–290, 10.1016/j.marpolbul.2018.09.009.
Duarte, C.M., Chapuis, L., Collin, S.P., Costa, D.P., Devassy, R.P., Eguiluz, V.M., Erbe, C., Gordon, T.A.C., Halpern, B.S., Harding, H.R., Havlik, M.N., Meekan, M., Merchant, N.D., Miksis-Olds, J.L., Parsons, M., Predragovic, M., Radford, A.N., Radford, C.A., Simpson, S.D., Slabbekoorn, H., Staaterman, E., Van Opzeeland, I.C., Winderen, J., Zhang, X., Juanes, F., The soundscape of the Anthropocene ocean. Science, 371, 2021, eaba4658, 10.1126/science.aba4658.
Fakan, E.P., McCormick, M.I., Boat noise affects the early life history of two damselfishes. Mar. Pollut. Bull. 141 (2019), 493–500, 10.1016/j.marpolbul.2019.02.054.
Fernandez-Declerck, M., Rojas, E., Prosnier, L., Teulier, L., Dechaume-Moncharmont, F.-X., Médoc, V., Adding insult to injury: anthropogenic noise intensifies predation risk by an invasive freshwater fish species. Biol. Invasions 25 (2023), 2775–2785, 10.1007/s10530-023-03072-w.
Ferrier-Pagès, C., Leal, M.C., Calado, R., Schmid, D.W., Bertucci, F., Lecchini, D., Allemand, D., Noise pollution on coral reefs? — a yet underestimated threat to coral reef communities. Mar. Pollut. Bull., 165, 2021, 112129, 10.1016/j.marpolbul.2021.112129.
Frédérich, B., Fabri, G., Lepoint, G., Vandewalle, P., Parmentier, E., Trophic niches of thirteen damselfishes (pomacentridae) at the grand récif of toliara, Madagascar. Ichthyol. Res. 56 (2009), 10–17, 10.1007/s10228-008-0053-2.
Frédérich, B., Lehanse, O., Vandewalle, P., Lepoint, G., Trophic niche width, shift, and specialization of Dascyllus aruanus in toliara lagoon, Madagascar. Copeia, 2010, 218–226, 10.1643/CE-09-031 2010.
Frédérich, B., Parmentier, E., Biology of Damselfishes, 2016, CRC Press, Taylor & Fracis, Boca Rator.
Gentleman, W.C., Neuheimer, A.B., Functional responses and ecosystem dynamics: how clearance rates explain the influence of satiation, food-limitation and acclimation. J. Plankton Res. 30 (2008), 1215–1231, 10.1093/plankt/fbn078.
Gerritsen, J., Strickler, J.R., Encounter probabilities and community structure in zooplankton: a mathematical model. J. Fish. Res. Board Can. 34 (1977), 73–82, 10.1139/f77-008.
Gonson, C., Pelletier, D., Gamp, E., Preuss, B., Jollit, I., Ferraris, J., Decadal increase in the number of recreational users is concentrated in no-take marine reserves. Mar. Pollut. Bull. 107 (2016), 144–154, 10.1016/j.marpolbul.2016.04.007.
Halfwerk, W., Slabbekoorn, H., Pollution going multimodal: the complex impact of the human-altered sensory environment on animal perception and performance. Biol. Lett., 11, 2015, 20141051, 10.1098/rsbl.2014.1051.
Hanache, P., Spataro, T., Firmat, C., Boyer, N., Fonseca, P., Médoc, V., Noise-induced reduction in the attack rate of a planktivorous freshwater fish revealed by functional response analysis. Freshw. Biol. 65 (2020), 75–85, 10.1111/fwb.13271.
Harding, H.R., Gordon, T.a.C., Wong, K., McCormick, M.I., Simpson, S.D., Radford, A.N., Condition-dependent responses of fish to motorboats. Biol. Lett., 16, 2020, 20200401, 10.1098/rsbl.2020.0401.
Hildebrand, J.A., Anthropogenic and natural sources of ambient noise in the ocean. Mar. Ecol. Prog. Ser. 395 (2009), 5–20, 10.3354/meps08353.
Holling, C.S., Some characteristics of simple types of predation and parasitism. Can. Entomol. 91 (1959), 385–398, 10.4039/Ent91385-7.
Holling, C.S., The components of predation as revealed by a study of small-mammal predation of the European pine sawfly. Can. Entomol. 91 (1959), 293–320, 10.4039/Ent91293-5.
Juliano, S.A., Nonlinear Curve Fitting: Predation and Functional Response Curves. Cheiner, S.M., Gurven, J., (eds.) Design and Analysis of Ecological Experiments, 2nd Edition, 2001, Chapman and Hall, London, 178–196.
Kalinkat, G., Schneider, F.D., Digel, C., Guill, C., Rall, B.C., Brose, U., Body masses, functional responses and predator–prey stability. Ecol. Lett. 16 (2013), 1126–1134, 10.1111/ele.12147.
Khomich, M., Måge, I., Rud, I., Berget, I., Analysing microbiome intervention design studies: comparison of alternative multivariate statistical methods. PLoS One, 16, 2021, e0259973, 10.1371/journal.pone.0259973.
Kooijman, S.A.L.M., Social interactions can affect feeding behaviour of fish in tanks. Journal of Sea Research, Metabolic organization: 30 years of DEB applications and developments 62 (2009), 175–178, 10.1016/j.seares.2009.06.003.
Kuşku, H., Yiğit, M., Ergün, S., Yiğit, Ü., Taylor, N., Acoustic noise pollution from marine industrial activities: exposure and impacts. Aquat Res, 2018, 148–161, 10.3153/AR18017.
Maierdiyali, A., Wang, L., Luo, Y., Li, Z., Effect of tank size on zebrafish behavior and physiology. Animals, 10, 2020, 2353, 10.3390/ani10122353.
Mann, D.A., Lobel, P.S., Acoustic behavior of the damselfish Dascyllus albisella: behavioral and geographic variation. Environ. Biol. Fish. 51 (1998), 421–428, 10.1023/A:1007410429942.
McCann, K., Hastings, A., Huxel, G.R., Weak trophic interactions and the balance of nature. Nature 395 (1998), 794–798, 10.1038/27427.
McCormick, M.I., Allan, B.J.M., Harding, H., Simpson, S.D., Boat noise impacts risk assessment in a coral reef fish but effects depend on engine type. Sci. Rep., 8, 2018, 3847, 10.1038/s41598-018-22104-3.
McCormick, M.I., Fakan, E.P., Nedelec, S.L., Allan, B.J.M., Effects of boat noise on fish fast-start escape response depend on engine type. Sci. Rep., 9, 2019, 6554, 10.1038/s41598-019-43099-5.
McCormick, M.I., Watson, S.-A., Simpson, S.D., Allan, B.J.M., Effect of elevated CO2 and small boat noise on the kinematics of predator–prey interactions. Proc. Biol. Sci., 285, 2018, 20172650, 10.1098/rspb.2017.2650.
Mills, S.C., Beldade, R., Henry, L., Laverty, D., Nedelec, S.L., Simpson, S.D., Radford, A.N., Hormonal and behavioural effects of motorboat noise on wild coral reef fish. Environ. Pollut., 262, 2020, 114250, 10.1016/j.envpol.2020.114250.
Murdoch, W.W., Oaten, A., Predation and population stability. MacFadyen, A., (eds.) Advances in Ecological Research, 1975, Academic Press, 1–131, 10.1016/S0065-2504(08)60288-3.
Nanninga, G.B., Côté, I.M., Beldade, R., Mills, S.C., Behavioural acclimation to cameras and observers in coral reef fishes. Ethology 123 (2017), 705–711, 10.1111/eth.12642.
Nedelec, S.L., Mills, S.C., Lecchini, D., Nedelec, B., Simpson, S.D., Radford, A.N., Repeated exposure to noise increases tolerance in a coral reef fish. Environ. Pollut. 216 (2016), 428–436, 10.1016/j.envpol.2016.05.058.
Parmentier, E., Donaldson, T., Banse, M., Cleaning of coral reef fishes by the humbug damselfish Dascyllus aruanus. Mar. Biodivers., 52, 2022, 39, 10.1007/s12526-022-01275-3.
Parmentier, E., Kéver, L., Casadevall, M., Lecchini, D., Diversity and complexity in the acoustic behaviour of Dacyllus flavicaudus (Pomacentridae). Mar. Biol. 157 (2010), 2317–2327, 10.1007/s00227-010-1498-1.
Parmentier, E., Lecchini, D., Frederich, B., Brie, C., Mann, D., Sound production in four damselfish (Dascyllus) species: phyletic relationships?. Biol. J. Linn. Soc. 97 (2009), 928–940, 10.1111/j.1095-8312.2009.01260.x.
Parmentier, E., Scalbert, R., Raick, X., Gache, C., Frédérich, B., Bertucci, F., Lecchini, D., First use of acoustic calls to distinguish cryptic members of a fish species complex. Zool. J. Linn. Soc. 195 (2022), 964–975, 10.1093/zoolinnean/zlab056.
Polverino, G., Ruberto, T., Staaks, G., Mehner, T., Tank size alters mean behaviours and individual rank orders in personality traits of fish depending on their life stage. Anim. Behav. 115 (2016), 127–135, 10.1016/j.anbehav.2016.03.013.
Popper, A.N., Hawkins, A.D., An overview of fish bioacoustics and the impacts of anthropogenic sounds on fishes. J. Fish. Biol. 94 (2019), 692–713, 10.1111/jfb.13948.
Pritchard, D.W., Paterson, R.A., Bovy, H.C., Barrios-O'Neill, D., FRAIR: an R Package for Fitting and Comparing Consumer Functional Responses. 2017.
Prosnier, L., Loeuille, N., Hulot, F.D., Renault, D., Piscart, C., Bicocchi, B., Deparis, M., Lam, M., Médoc, V., Parasites make hosts more profitable but less available to predators. Oikos, 2024, 2024, e10469, 10.1111/oik.10469.
Randall, H.A., Allen, G.R., A revision of the damselfish genus Dascyllus (Pomacentridae) with the description of a new species. Record Aust. Mus. 31 (1977), 349–385, 10.3853/j.0067-1975.31.1977.217.
Rogers, D., Random search and insect population models. J. Anim. Ecol. 41 (1972), 369–383, 10.2307/3474.
Rojas, E., Prosnier, L., Pradeau, A., Boyer, N., Médoc, V., Anthropogenic noise does not strengthen multiple-predator effects in a freshwater invasive fish. J. Fish. Biol. 102 (2023), 1470–1480, 10.1111/jfb.15397.
Rojas, E., Thévenin, S., Montes, G., Boyer, N., Médoc, V., From distraction to habituation: ecological and behavioural responses of invasive fish to anthropogenic noise. Freshw. Biol. 66 (2021), 1606–1618, 10.1111/fwb.13778.
Rooney, N., McCann, K.S., Integrating food web diversity, structure and stability. Trends Ecol. Evol. 27 (2012), 40–46, 10.1016/j.tree.2011.09.001.
Ross, D., Ship sources of ambient noise. IEEE J. Ocean. Eng. 30 (2005), 257–261, 10.1109/JOE.2005.850879.
Saccenti, E., Hoefsloot, H.C.J., Smilde, A.K., Westerhuis, J.A., Hendriks, M.M.W.B., Reflections on univariate and multivariate analysis of metabolomics data. Metabolomics 10 (2014), 361–374, 10.1007/s11306-013-0598-6.
Sale, P.F., Extremely limited home range in a coral reef fish, Dascyllus aruanus (pisces; pomacentridae). Copeia, 1971, 324–327, 10.2307/1442839 1971.
Sarà, G., Dean, J.M., D'Amato, D., Buscaino, G., Oliveri, A., Genovese, S., Ferro, S., Buffa, G., Martire, M.L., Mazzola, S., Effect of boat noise on the behaviour of bluefin tuna Thunnus thynnus in the Mediterranean Sea. Mar. Ecol. Prog. Ser. 331 (2007), 243–253, 10.3354/meps331243.
Solomon, M.E., The natural control of animal populations. J. Anim. Ecol. 18 (1949), 1–35, 10.2307/1578.
Spurgeon, J.P.G., The economic valuation of coral reefs. Mar. Pollut. Bull. 24 (1992), 529–536, 10.1016/0025-326X(92)90704-A.
Vetter, B., Casper, A., Mensinger, A., Characterization and management implications of silver carp (Hypophthalmichthys molitrix) jumping behavior in response to motorized watercraft. MBI 8 (2017), 113–124, 10.3391/mbi.2017.8.1.11.
Villalobos-Jiménez, G., Dunn, A.M., Hassall, C., Environmental noise reduces predation rate in an aquatic invertebrate. J. Insect Conserv. 21 (2017), 839–847, 10.1007/s10841-017-0023-y.