Multiple exposure to thunderstorm sound in Nile tilapia (Oreochromis niloticus): physiological response and stress recovery

André M., Solé M., Lenoir M., Durfort M., Quero C., Mas A., Lombarte A., van der Shaar M., López-Bejar M., Morell M., Zaugg S., Houégnian L. (2011). Low-frequency sounds induce acoustic trauma in cephalopods. Front. Ecol. Environ., 10: 18–28. Search in Google Scholar

Andrew R.K., Howe B.M., Mercer J.A. (2002). Ocean ambient sound: Comparing the 1960s with the 1990s for a receiver off the California coast. Acoust. Res. Lett. Online, 3: 65–70. Search in Google Scholar

Bacheler N.M., Shertzer K.W., Cheshire R.T., MacMahan J.J. (2019). Tropical storms influence the movement behavior of a demersal oceanic fish species. Sci. Rep., 9: 1481. Search in Google Scholar

Barton B.A. (2002). Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr. Comp. Biol., 42: 517–525. Search in Google Scholar

Beale C.M., Monaghan P. (2004). Behavioural responses to human disturbance: a matter of choice? Anim. Behav., 68: 1065–1069. Search in Google Scholar

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. Search in Google Scholar

Brown J.A. (1993). Endocrine responses to environmental pollutants. In: Fish Ecophysiology, Rankin J.C., Jensen F.B. (eds). Fish Fisheries Series, 9, Chapman and Hall, London, pp. 276–296. Search in Google Scholar

Bruintjes R., Radford A.N. (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. Search in Google Scholar

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. Search in Google Scholar

Caruso G., Genovese I., Maricchiolo G., Modica A. (2005). Haematological, biochemical and immunological parameters as stress indicators in Dicentrarchus labrax and Sparus aurata farmed in off-shore cages. Aquac. Int., 13: 67–73. Search in Google Scholar

Casper B.M., Halvorsen M.B., Matthews F., Carlson T.J., Popper A.N. (2013). Recovery of Barotrauma injuries resulting from exposure to pile driving sound in two sizes of hybrid striped bass. PLoS One, 8(9): e73844. Search in Google Scholar

CMCCLAIN (2008). Does Lightning Kill Marine Animals? ScienceBlogs Deepseanews. https://scienceblogs.com/deepseanews/2008/03/17/does-lightning-kill-marine-ani. Search in Google Scholar

Culik B.M., Koschinski S., Tregenza N., Ellis G.M. (2001). Reactions of harbor porpoises Phocoena phocoena and herring Clupea harengus to acoustic alarms. Mar. Ecol. Prog. Ser., 211: 255–260. Search in Google Scholar

Dalla Valle A.Z., Rivas-Diaz R., Claireaux G. (2003). Opercular differential pressure as a predictor of metabolic oxygen demand in the starry flounder. J. Fish Biol., 63: 1578–1588. Search in Google Scholar

Davidson J., Frankel A.S., Ellison W.T., Summerfelt S., Popper A.N., Mazik P., Bebak J. (2007). Minimizing noise in fiberglass aquaculture tanks: noise reduction potential of various retrofits. Aquac. Eng., 37: 125–131. Search in Google Scholar

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. Search in Google Scholar

de Jong K., Forland T.N., Amorim M.C.P., Rieucau G., Slabbekoorn H., Sivle L.D. (2020). Predicting the effects of anthropogenic noise on fish reproduction. Rev. Fish Biol. Fish., 30: 245–268. Search in Google Scholar

Emelda M. (2011). Difference between thunder and lightning. Difference between similar terms and objects. http://www.differencebetween.net/science/nature/difference-between-thunder-andlightning/. Search in Google Scholar

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. Search in Google Scholar

Gabriel U.U., Akinrotimi O.A. (2011). Management of stress in fish for sustainable aquaculture development. Researcher, 3: 28–38. Search in Google Scholar

Gibson A.K., 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. Search in Google Scholar

Gornati R., Papis E., Rimoldi S., Terova G., Saroglia M., Bernardini G. (2004). Rearing density influences the expression of stress related genes in sea bass (Dicentrarchus labrax, L.). Gene, 341: 111–118. Search in Google Scholar

Guerriero G., Di Finizio A., Ciarcia G. (2002). Stress-induced changes of plasma antioxidants in aquacultured sea bass, Dicentrarchus labrax. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol., 132: 205–211. Search in Google Scholar

Hawkins A.D., Johnson C., Popper A.N. (2020). How to set sound exposure criteria for fishes. J. Acoust. Soc. Am., 147: 1762–1777. Search in Google Scholar

Kammerer B.D., Cech J.J., Kultz D. (2010). Rapid changes in plasma cortisol, osmolality, and respiration in response to salinity stress in tilapia (Oreochromis mossambicus). Comp. Biochem. Physiol. Part A Mol. Integr. Physiol., 157: 260–265. Search in Google Scholar

Kayali 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. Technol., 19: 681–685. Search in Google Scholar

Kubilay A., Uluköy G. (2002). The effects of acute stress on Rainbow trout (Oncorhynchus mykiss). Turk. J. Zool., 26: 249–254. Search in Google Scholar

Kuo C.M., Hsieh S.L. (2006). Comparisons of physiological and biochemical responses between milkfish (Chanos chanos) and grass carp (Ctenopharyngodon idella) to cold shock. Aquaculture, 251: 525–536. Search in Google Scholar

Kusku H. (2020). 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. Search in Google Scholar

Kusku H., Yigit M., Ergün S., Yigit Ü., Taylor N. (2018 a). Acoustic noise pollution from marine industrial activities: Exposure and impacts. Aquat. Res., 1: 148–161. Search in Google Scholar

Kusku H., Ergün S., Yilmaz S., Güroy B., Yigit M. (2018 b). Impacts of urban noise and musical stimuli on growth performance and feed utilization of Koi fish (Cyprinus carpio) in recirculating water conditions. Turkish J. Fish. Aquat. Sci., 19: 513–523. Search in Google Scholar

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., 51: 3166–3174. Search in Google Scholar

Laidley C.W., Leatherland J.F. (1988). Cohort sampling, anaesthesia and stocking density effects on plasma cortisol, thyroid hormone, metabolite and ion levels in rainbow trout, Salmo gairdneri Richardson. J. Fish Biol., 33: 73–88. Search in Google Scholar

Lee W.S., Monaghan P., Metcalfe N.B. (2013). Experimental demonstration of the growth rate – lifespan trade-off. Proc. R. Soc. B: Biol. Sci., 280: 20122370. Search in Google Scholar

Marino G., Di Marco P., Mandich A., Finora M.G., Cataudella S. (2001). Changes in serum cortisol, metabolites, osmotic pressure and electrolytes in response to different blood sampling procedures in cultured sea bass (Dicentrarchus labrax L.). J. Appl. Ichthyol., 17: 115–120. Search in Google Scholar

Martínez-Porchas M., Martínez-Córdova L.R., Ramos-Enrıquez R. (2009). Cortisol and glucose: Reliable indicators of fish stress? Pan-Am. J. Aquat. Sci., 4: 158–178. Search in Google Scholar

McLaughlin K.E., Kunc H.P. (2013). Experimentally increased noise levels change spatial and singing behaviour. Biol. Lett., 9: 20120771. Search in Google Scholar

McLean M.F., Hanson K.C., Cooke S.J., Hinch S.G., Patterson D.A., Nettles T.L., Litvak M.K., Crossin G.T. (2016). Physiological stress response, reflex impairment and delayed mortality of white sturgeon Acipenser transmontanus exposed to simulated fisheries stressors. Conserv. Physiol., 4: cow031. Search in Google Scholar

Metcalfe N.B., Huntingford F.A., Thorpe J.E. (1987). The influence of predation risk on the feeding motivation and foraging strategy of juvenile Atlantic salmon. Anim. Behav., 35: 901–911. Search in Google Scholar

MGM (2020). Turkish Ministry of Agriculture and Forestry, General Directorate of Meteorology. In: 2019 Yılı Meteorolojik Afetler Değerlendirmesi, Eroğlu H., Çetin S., Erkan M.A., Çamalan G., Güser Y., Odabaşı E., Soydam M., Arabacı H. (eds). Tarım ve Orman Bakanlığı, Meteoroloji Genel Müdürlüğü, 2020 Ankara. https://mgm.gov.tr/FILES/genel/raporlar/2019MeteorolojikAfetlerDegerlendirmesi.pdf. Search in Google Scholar

Mickle M.F., Higgs D.M. (2018). Integrating techniques: a review of the effects of anthropogenic noise on freshwater fish. Can. J. Fish. Aquat. Sci., 75: 1534–1541. Search in Google Scholar

Moberg G.P. (1985). Biological response to stress: key to assessment of animal well being? In: Animal Stress, Moberg G.P. (ed.). American Physiological Society, Bethesda-Maryland, pp. 27–49. Search in Google Scholar

Nedelec S.L., Mills S.C., Lecchini D., Nedelec B., Simpson S.D., Radford A.N. (2016). Repeated exposure to noise increases tolerance in a coral reef fish. Environ. Pollut., 216: 428–436. Search in Google Scholar

Nichols T.A., Anderson T.W., Širović A. (2015). Intermittent noise induces physiological stress in a coastal marine fish. PLoS One, 10(9): e0139157. Search in Google Scholar

Pickering A.D., Pottinger T.G., 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. Search in Google Scholar

PIDP (2001). Pile Installation Demonstration Project, San Francisco – Oakland Bay Bridge East Span Seismic Safety Project, Fisheries Impact Assessment. Report PIDP EA 012081 on CalTrans Contract 04A0148. Task Order 205.10.90, PIDP 04-ALA-80–0.0/0.5 (pp. 1–68). https://www.nrc.gov/docs/ML1434/ML14345A579.pdf. Search in Google Scholar

Popper A.N., Smith M.E., Cott P.A., Hanna B.W., MacGillivray A.O., Austin M.E., Mann D.A. (2005). Effects of exposure to seismic airgun use on hearing of three fish species. J. Acoust. Soc. Am., 117: 3958–3971. Search in Google Scholar

Popper A.N., Hawkins A.D., Fay R.R., Mann D., Bartol S., Carlson T., Coombs S., Ellison W.T., Gentry R., Halvorsen M.B., Lokkeborg S., Rogers P., Southall B.L., Zeddies D.G., Tavolga W.N. (2014). ASA S3/SC1.4 TR-2014 Sound exposure guidelines for fishes and sea turtles: A technical report prepared by ANSI – Accredited Standards Committee S3/SC1 and registered with ANSI. Springer Nature, New York. Search in Google Scholar

Popper A.N., Hawkins A.D., Thomsen F. (2020). Taking the animals’ perspective regarding anthropogenic underwater sound. Trends Ecol. Evol., 35: 787–794. Search in Google Scholar

Prabu E., Rajagopalsamy C.B.T., Ahilan B., Jegan Michael Andro Jeevagan I., Renuhadevi M. (2019). Tilapia – an excellent candidate species for world aquaculture: A review. Annu. Res. Rev. Biol., 31: 1–14. Search in Google Scholar

Radford A.N., Lèbre L., Lecaillon G., Nedelec S.L., Simpson S.D. (2016). Repeated exposure reduces the response to impulsive noise in European seabass. Glob. Change Biol., 22: 3349–3360. Search in Google Scholar

Santulli A., Modica A., Messina C., Ceffa L., Curatolo A., Rivas G., Fabi G., D’Amelio V. (1999). Biochemical responses of European sea bass (Dicentrarchus labrax L.) to the stress induced by off shore experimental seismic prospecting. Mar. Pollut. Bull., 38: 1105–1114. Search in Google Scholar

Siddik M.A.B., Nahar A., Ahamed F., Hossain M. (2014). Over-wintering growth performance of mixed-sex and mono-sex Nile tilapia Oreochromis niloticus in the northeastern Bangladesh. Croat. J. Fish., 72: 70–76. Search in Google Scholar

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. Search in Google Scholar

Simpson S.D., Purser J., Radford A.N. (2015). Anthropogenic noise compromises antipredator behaviour in European eels. Glob. Change Biol., 21: 586–593. Search in Google Scholar

Skjervold P.O., Fjæra S.O., Østby P.B., Einen O. (2001). Live-chilling and crowding stress before slaughter of Atlantic salmon (Salmo salar). Aquaculture, 192: 265–280. Search in Google Scholar

Smith M.E., Kane A.S., Popper A.N. (2004). Noise-induced stress response and hearing loss in goldfish (Carassius auratus). J. Exp. Biol., 207: 427–435. Search in Google Scholar

Southall B.L., Bowles A.E., Ellison W.T., Finneran J.J., Gentry R.L., Greene C.R., Kastak D., Ketten D.R., Miller J.H., Nachtigall P.E., Richardson W.J., Thomas J.A., Tyack P.L. (2007). Marine mammal noise exposure criteria: Initial scientific recommendations. Bioacoustics, 17: 273–275. Search in Google Scholar

Southall B.L., Finneran J.J., Reichmuth C., Nachtigall P.E., Ketten D.R., Bowles A.E., Ellison W.T., Nowacek D.P., Tyack P.L. (2019). Marine mammal noise exposure criteria: Updated scientific recommendations for residual effects. Aquat. Mamm., 45: 125–232. Search in Google Scholar

Spiga I., Aldred N., Caldwell G.S. (2017). Anthropogenic noise compromises the anti-predator behaviour of the European seabass, Dicentrarchus labrax (L.). Mar. Pollut. Bull., 122: 297–305. Search in Google Scholar

Sun Y., Song Y., Zhao J., Chen J., Yuan Y., Jiang S., Zhang D. (2001). Effect of drilling noise and vibration on growth of carp (Cyprinus carpio) by cut-fin marking. Mar. Fish. Res. / Haiyang Shiuchan Yanjiu, 22: 62–68. Search in Google Scholar

Tantarpale V.T., Rathod S.H., Kapil S. (2012). Temperature stress on opercular beats and respiratory rate of freshwater fish Channa punctatus. Int. J. Sci. Res. Publ., 2: 1–5. Search in Google Scholar

Terhune J.M., Friars G.W., Bailey J.K., O’Flynn F.M. (1990). Noise levels may influence Atlantic salmon smolting rates in tanks. J. Fish Biol., 37: 185–197. Search in Google Scholar

Thomsen F., Erbe C., Hawkins A., Lepper P., Popper A.N., Scholik-Schlomer A., Sisneros J. (2020). Introduction to the special issue on the effects of sound on aquatic life. J. Acoust. Soc. Am., 148: 934–938. Search in Google Scholar

Vazzana M., Cammarata M., Cooper E.L., Parrinello N. (2002). Confinement stress in sea bass (Dicentrarchus labrax) depresses peritoneal leukocyte cytotoxicity. Aquaculture, 210: 231–243. Search in Google Scholar

Wale M.A., Simpson S.D., Radford A.N. (2013). Size-dependent physiological responses of shore crabs to single and repeated playback of ship noise. Biol. Lett., 9: 20121194. Search in Google Scholar

Wang M., Lu M. (2016). Tilapia polyculture: a global review. Aquac. Res., 47: 2363–2374. Search in Google Scholar

Wedemeyer G. (1976). Physiological response of juvenile coho salmon and rainbow trout to handling and crowding stress in intensive fish culture. J. Fish. Res. Board Can., 33: 2699–2702. Search in Google Scholar

Wells R.M.G., Tetens V., Devries A.L. (1984). Recovery from stress following capture and anaesthesia of Antarctic fish: haematology and blood chemistry. J. Fish Biol., 25: 567–576. Search in Google Scholar

Wendelaar Bonga S.E. (1997). The stress response in fish. Physiol. Rev., 77: 591–625. Search in Google Scholar

Wenz G.M. (1962). Acoustic ambient noise in the ocean: spectra and sources. J. Acoust. Soc. Am., 34: 1936–1956. Search in Google Scholar

Wysocki L.E., Davidson III J.W., Smith M.E., Frankel A., Ellison W.T., Mazik P.M., Popper A.N., Bebak J. (2007). Effects of aquaculture production noise on hearing, growth, and disease resistance of rainbow trout Oncorhynchus mykiss. Aquaculture, 272: 687–697. Search in Google Scholar

Xu J.Y., Miao X.W., Liu Y., Cui S.R. (2005). Behavioral response of tilapia (Oreochromis niloticus) to acute ammonia stress monitored by computer vision. J. Zhejiang Univ. Sci., 6B: 812–816. Search in Google Scholar

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. Search in Google Scholar