Abstract
Human-made impacts on the acoustic environment from marine industries is becoming a more significant issue with increasing public concern of environmental consequences. Even though there are several reports with scientific evidences on harmful influences of anthropogenic underwater sounds on the aquatic ecosystem, most of the studies so far dealt with trigger effects of short term noise impacts on aquatic animals. In the present study, however, long-term experimentation was conducted with Nile tilapia (Oreochromis niloticus) in order to figure out how fish may respond to long-term exposure of underwater sounds and if the level of response may change (increase or decline) over time. A startle reflex as a sign of stress was seen immediately at the start of the playbacks of ship noise or urban sounds in this study. Peaks of elevated respiratory movements of ventilation (opercula beats and pectoral wing rates) retained high over the following 30 days of sound initiation and underwent a declining trend over the following 90 days of exposure. At the end of the 120-day study period, the lowered response of fish after long-term sound exposure is likely due to the increased tolerance of fish to human-generated underwater sounds of urban and shipping noises. Different than short-term noise impacts, information on long-term exposure of anthropogenic underwater sounds is important for environmental management and setting new regulations for the sustainable use of water resources in the world.
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References
André M (2009) The sperm whale sonar: monitoring and use in mitigation of anthropogenic noise effects in the marine environment. Nucl Instrum Methods Phys Res Sect A 602:262–267. https://doi.org/10.1016/j.nima.2008.12.223
Andrew RK, Howe BM, Mercer JA, Dzieciuch MA (2002) Ocean ambient sound: comparing the 1960s with the 1990s for a receiver off the California coast. Acoust Res Lett 3:65–70. https://doi.org/10.1121/1.1461915
Barber JR, Crooks KR, Fristrup KM (2009) The costs of chronic noise exposure for terrestrial organisms. Trends Ecol Evol 25:180–189. https://doi.org/10.1016/j.tree.2009.08.002
Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42:517–525. https://doi.org/10.1093/icb/42.3.517
Beale CM, Monaghan P (2004) Behavioural responses to human disturbance: a matter of choice? Anim Behav 68:1065–1069. https://doi.org/10.1016/j.anbehav.2004.07.002
Bejder L, Samuels A, Whitehead H, Finn H, Allen S (2009) Impact assessment research: use and misuse of habituation, sensitisation and tolerance in describing wildlife responses to anthropogenic stimuli. Mar Ecol Prog Ser 395:177–185. https://doi.org/10.3354/meps07979
Bruintjes R, Radford AN (2014) Chronic playback of boat noise does not impact hatching success or posthatching larval growth and survival in a cichlid fish. Peer J 2:e594. https://doi.org/10.7717/peerj.594
Buscaino G, Filiciotto F, Buffa G, Bellante A, di Stefano V, Assenza A, Fazio F, Caola G, Mazzola S (2010) Impact of an acoustic stimulus on the motility and blood parameters of European sea bass (Dicentrarchus labrax L.) and gilthead sea bream (Sparus aurata L.). Mar Environ Res 69:136–142. https://doi.org/10.1016/j.marenvres.2009.09.004
Clark J, Young J, Bart, A, Zohar Y (1996). Underwater ambient noise measurements. In 30th Proceedings of the Acoustical Society of America. St. Louis, MO, November 27, 13
Codarin A, Wysocki LE, Ladich F, Picciulin M (2009) Effects of ambient and boat noise on hearing and communication in three fish species living in a marine protected area (Miramare, Italy). Mar Pollut Bull 58:1880–1887. https://doi.org/10.1016/j.marpolbul.2009.07.011
Davidson J, Frankel AS, Ellison WT, Summerfelt S, Popper AN, Mazik P, Bebak J (2007) Minimizing noise in fiberglass aquaculture tanks: noise reduction potential of various retrofits. Aquac Eng 37(2):125–131. https://doi.org/10.1016/j.aquaeng.2007.03.003
Davidson J, Bebak J, Mazik P (2009) The effects of aquaculture production noise on the growth, condition factor, feed conversion, and survival of rainbow trout, Oncorhynchus mykiss. Aquaculture 288:337–343. https://doi.org/10.1016/j.aquaculture.2008.11.037
de Jong K, Forland TN, Amorim MCP, Rieucau G, Slabbekoorn H, Sivle LD (2020) Predicting the effects of anthropogenic noise on fish reproduction. Rev Fish Biol Fisheries 30:245–268. https://doi.org/10.1007/s11160-020-09598-9
Filiciotto F, Giacalone VM, Fazio F, Buffa G, Piccione G, Maccarrone V, Di Stefano V, Mazzola S, Buscaino G (2013) Effect of acoustic environment on gilthead sea bream (Sparus aurata): sea and onshore aquaculture background noise. Aquaculture 414:36–45. https://doi.org/10.1016/j.aquaculture.2013.07.042
Filiciotto F, Cecchini S, Buscaino G, Maccarrone V, Piccione G, Fazio F (2017) Impact of aquatic acoustic noise on oxidative status and some immune parameters in gilthead sea bream Sparus aurata (Linnaeus, 1758) juveniles. Aquac Res 48:1895–1903. https://doi.org/10.1111/are.13027
Gibson AK, Mathis A (2006) Opercular beat rate for rainbow darters Etheostoma caeruleum exposed to chemical stimuli from conspecific and heterospecific fishes. J Fish Biol 69:224–232. https://doi.org/10.1111/j.1095-8649.2006.01102.x
Halfwerk W, Slabbekoorn H (2009) A behavioural mechanism explaining noisedependent frequency use in urban birdsong. Anim Behav 78:1301–1307. https://doi.org/10.1016/j.anbehav.2009.09.015
Kammerer BD, Cech JJ, Kultz D (2010) Rapid changes in plasma cortisol, osmolality, and respiration in response to salinity stress in tilapia (Oreochromis mossambicus). Comp Biochem Physiol A Physiol 157:260–265. https://doi.org/10.1016/j.cbpa.2010.07.009
Kayalı B, Yigit M, Bulut M (2011) Evaluation of the recovery time of sea bass Dicentrarchus labrax Linnaeus 1758 juveniles from transport and handling stress using ammonia nitrogen excretion rates as a stress indicator. J Mar Sci Tech-Taiw 16(6):681–685
Kusku H, Yigit M, Ergün S, Yigit Ü, Taylor N (2018) Acoustic noise pollution from marine industrial activities: exposure and impacts. Aquat Res 1(4):148–161. https://doi.org/10.3153/AR18017
Kusku H, Ergün S, Yilmaz S, Güroy B, Yigit M (2019) Impacts of urban noise and musical stimuli on growth performance and feed utilization of koi fish (Cyprinus carpio) in recirculating water conditions. Turk J Fish Aquat Sci 19(6):513–523. https://doi.org/10.4194/1303-2712-v19_6_07
Kusku H, Yigit Ü, Yilmaz S, Yigit M, Ergün S (2020) Acoustic effects of underwater drilling and piling noise on growth and physiological response of Nile tilapia (Oreochromis niloticus). Aquac Res 00:1–9. https://doi.org/10.1111/are.14652
Lagardère J (1982) Effects of noise on growth and reproduction of Crangon crangon in rearing tanks. Mar Biol 71:177–185. https://doi.org/10.1007/BF00394627
McDonald MA, Hildebrand JA, Wiggins SM, Ross D (2008) A 50 year comparison of ambient ocean noise near San Clemente Island: a bathymetrically complex coastal region off Southern California. J Acoust Soc Am 124:1985–1992. https://doi.org/10.1121/1.2967889
McLaughlin KE, Kunc HP (2013) Experimentally increased noise levels change spatial and singing behaviour. Biol Lett 9:20120771. https://doi.org/10.1098/rsbl.2012.0771
Morley EL, Jones G, Radford AN (2014) The importance of invertebrates when considering the impacts of anthropogenic noise. Proc R Soc Ser B 281:20132683. https://doi.org/10.1098/rspb.2013.2683
Nedelec SL, Mills SC, Lecchini D, Nedelec B, Simpson SD, Radford AN (2016) Repeated exposure to noise increases tolerance in a coral reef fish. Environ Pollut 216:428–436. https://doi.org/10.1016/j.envpol.2016.05.058
Neo Y, Seitz J, Kastelein R, Winter H, Ten Cate C, Slabbekoorn H (2014) Temporal structure of sound affects behavioral recovery from noise impact in European seabass. Biol Conserv 178:65–73. https://doi.org/10.1016/j.biocon.2014.07.012
Nichols TA, Anderson TW, Širović A (2015) Intermittent noise induces physiological stress in a coastal marine fish. PLoS One 10(9):1–13. https://doi.org/10.1371/journal.pone.0139157
Papoutsoglou SE, Karakatsouli N, Skouradakis C, Papoutsoglou ES, Batzina A, Leondaritis G, Sakellaridis N (2013) Effect of musical stimuli and white noise on rainbow trout (Oncorhynchus mykiss) growth and physiology in recirculating water conditions. Aquac Eng 55:16–22. https://doi.org/10.1016/j.aquaeng.2013.01.003
Pickering AD, Pottinger TG, Christie P (1982) Recovery of the Brown trout, Salmo trutta L., from acute handling stress: a time-course study. J Fish Biol 20:229–244. https://doi.org/10.1111/j.1095-8649.1982.tb03923.x
Popper AN, Fay RR (2011) Rethinking sound detection by fishes. Hear Res 273:25–36. https://doi.org/10.1016/j.heares.2009.12.023
Radford AN, Purser J, Bruintjes R et al (2015) Beyond a simple effect: variable and changing responses to anthropogenic noise. In: Popper AN, Hawkins AD (eds) The effects of noise on aquatic life, 2rd edn. Springer Science+Business Media, New York, pp 901–907
Radford AN, Lèbre L, Lecaillon G, Nedelec SL, Simpson SD (2016) Repeated exposure reduces the response to impulsive noise in European seabass. Glob Chang Biol 22:3349–3360. https://doi.org/10.1111/gcb.13352
Sapozhnikova Yu.P, Gasarov PV, Makarov MM et al (2018). The effects of sound pollution as a stress factor for the Baikal coregonid fish. Limnol Freshw Biol 2: 135-140. https://doi.org/10.31951/2658-3518-2018-A-2-135
Shannon G, McKenna MF, Angeloni LM et al (2016) A synthesis of two decades of research documenting the effects of noise on wildlife. Biol Rev 91:982–1005. https://doi.org/10.1111/brv.12207
Simontacchi C, Poltronieri C, Carraro C, Bertotto D, Xiccato G, Trocino A, Radaelli G (2008) Alternative stress indicators in sea bass Dicentrarchus labrax, L. J Fish Biol 72:747–752. https://doi.org/10.1111/j.1095-8649.2007.01717.x
Simpson SD, Purser J, Radford AN (2015) Anthropogenic noise compromises antipredator behaviour in European eels. Glob Chang Biol 21:586–593. https://doi.org/10.1111/gcb.12685
Simpson SD, Radford AN, Nedelec SL, Ferrari MCO, Chivers DP, McCormick MI, Meekan MG (2016) Anthropogenic noise increases fish mortality by predation. Nat Commun 7:10544. https://doi.org/10.1038/ncomms10544
Slabbekoorn H, Bouton N, van Opzeeland I, Coers A, ten Cate C, Popper AN (2010) A noisy spring: the impact of globally rising underwater sound levels on fish. Trends Ecol Evol 25:419–427. https://doi.org/10.1016/j.tree.2010.04.005
Spiga I, Aldred N, Caldwell GS (2017) Anthropogenic noise compromises the anti-predator behaviour of the European seabass, Dicentrarchus labrax (L.). Mar Pollut Bull 122(1–2):297–305. https://doi.org/10.1016/j.marpolbul.2017.06.067
Szabo TM, Weiss SA, Faber DS, Preuss T (2006) Representation of auditory signals in the M-cell: role of electrical synapses. J Neurophysiol 95(4):2617–2629. https://doi.org/10.1152/jn.01287.2005
Tantarpale VT, Rathod SH, Kapil S (2012) Temperature stress on opercular beats and respiratory rate of freshwater fish Channa punctatus. Int J Sci Res Pub 2(12):1–5
Tyack P (2008). Implications for marine mammals of large-scale changes in the marine acoustic environment. J Mammalogy 89(3): 549–558.
Wale MA, Simpson SD, Radford AN (2013) Size-dependent physiological responses of shore crabs to single and repeated playback of ship noise. Biol Lett 9:20121194. https://doi.org/10.1098/rsbl.2012.1194
Wales SC, Heitmeyer RM (2002) An ensemble source spectramodel for merchant shipradiated noise. J Acoust Soc Am 111:1211–1231. https://doi.org/10.1121/1.1427355
Wendelaar Bonga SE (1997) The stress response in fish. Phys Rev 77:591–625. https://doi.org/10.1152/physrev.1997.77.3.591
Wenz GM (1962) Acoustic ambient noise in the ocean: spectra and sources. J Acoust Soc Am 34(12):1936–1956. https://doi.org/10.1121/1.1909155
Worldometer (2020). https://www.worldometers.info/world-population/world-population-projections/ (From 1950 to current year: elaboration of data by United Nations, Department of Economic and Social Affairs, Population Division. World Population Prospects: The 2019 Revision
Wysocki LE, Dittami JP, Ladich F (2006) Ship noise and cortisol secretion in European freshwater fishes. Biol Conserv 128(4):501–508. https://doi.org/10.1016/j.biocon.2005.10.020
Yavuzcan-Yıldız H, Kırkağaç-Uzbilek M (2001) The evaluation of secondary stress response of grass carp (Ctenopharyngodon idella, Val. 1844) after exposing to the saline water. Fish Physiol Biochem 25:287–290. https://doi.org/10.1023/A:1023279604975
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Faculty of Marine Science and Technology, Canakkale Onsekiz Mart University (Turkey), is acknowledged for the support of experimental facilities used in this study.
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Guidelines of Regulations of Animal Behavior Society were followed throughout the experimental procedures applied in this study, which are in agreement with the approval of the Ethical Committee of Canakkale Onsekiz Mart University (Ethical Commission Approval Number: 2019/09-07).
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Kusku, H. Acoustic sound–induced stress response of Nile tilapia (Oreochromis niloticus) to long-term underwater sound transmissions of urban and shipping noises. Environ Sci Pollut Res 27, 36857–36864 (2020). https://doi.org/10.1007/s11356-020-09699-9
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DOI: https://doi.org/10.1007/s11356-020-09699-9