Abstract
This study examined the effects of boat noise pollution on the stress indices of gilthead sea bream (Sparus aurata, Linnaeus 1758). To assess the stress response in these fish, biometric values and plasma parameters such as ACTH, cortisol, glucose, lactate, haematocrit, Hsp70, total protein, cholesterol, triglycerides and osmolarity were analysed. After acclimatization of the animals, the experiment was carried out in a tank fitted with underwater speakers where the fish were exposed to sound treatments (in duplicate) consisting of: 10 days of no sound (control treatment; the animals were only exposed to the experimental tank’s background noise) and 10 days of noise derived from original recordings of motor boats, including recreational boats, hydrofoil, fishing boat and ferry boat (vessel noise treatment). The exposure to noise produced significant variations in almost all the plasma parameters assessed, but no differences were observed in weights and fork lengths. A PERMANOVA analysis highlighted significantly increased values (p < 0.05) of ACTH, cortisol, glucose, lactate, haematocrit, Hsp70, cholesterol, triglycerides and osmolarity in the fish exposed to vessel noise for 10 days. This study clearly highlights that anthropogenic noise negatively affects fish, and they are valuable targets for detailed investigations into the effects of this global pollutant. Finally, these experimental studies could represent part of the science that is able to improve the quality of the policies related to management plans for maritime spaces (Marine Strategy Framework Directive 56/2008 CE) that are aimed at stemming this pollutant phenomenon.
Similar content being viewed by others
Abbreviations
- ACTH:
-
Adrenocorticotropic hormone
- BPL:
-
Band pressure level
- ELISA:
-
Enzyme-linked immunosorbent assay
- GES:
-
Good Environmental Status
- HPI:
-
Hypothalamic–pituitary–interrenal
- Hsp:
-
Heat-shock protein
- MDS:
-
Multidimensional scaling
- MSFD:
-
Marine Strategy Framework Directive
- OOB:
-
Classification accuracy for out-of-bag
- PC:
-
Total protein concentrations
- PERMANOVA:
-
Univariate permutational multivariate analysis of variance
- SC:
-
Sympathetico-chromaffin
- SPL:
-
Sound pressure level
- RF:
-
Random forest
References
Banner A, Hyatt M (1973) Effects of noise on eggs and larvae of two estuarine fishes. Trans Am Fish Soc 1:134–136
Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42:517–525
Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annu Rev Fish Dis 1:13–26
Barton BA, Schreck CB, Sigismondi LA (1986) Multiple acute disturbances evoke cumulative physiological stress responses in juvenile chinook salmon. Trans Am Fish Soc 115:245–251
Breen P, Robinson LA, Rogers SI et al (2012) An environmental assessment of risk in achieving good environmental status to support regional prioritisation of management in Europe. Mar Policy 36:1033–1043
Bruintjes R, Radford AN (2013) Context-dependent impacts of anthropogenic noise on individual and social behaviour in a cooperatively breeding fish. Anim Behav 85:1343–1349. doi:10.1016/j.anbehav.2013.03.025
Bruintjes R, Radford AN (2014) Chronic playback of boat noise does not impact hatching success or post-hatching larval growth and survival in a cichlid fish. PeerJ 2:e594. doi: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
Cammarata M, Vazzana M, Accardi D, Parrinello N (2012) Seabream (Sparus aurata) long-term dominant-subordinate interplay affects phagocytosis by peritoneal cavity cells. Brain Behav Immun 26:580–587. doi:10.1016/j.bbi.2012.01.008
Celi M, Filiciotto F, Parrinello D, Buscaino G, Damiano A, Cuttitta A, D’Angelo S, Mazzola S, Vazzana M (2013) Physiological and agonistic behavioural response of Procambarus clarkii to an acoustic stimulus. J Exp Biol 216:709–718
Celi M, Filiciotto F, Vazzana M, Arizza V, Maccarrone V, Ceraulo M, Mazzola S, Buscaino G (2015) Shipping noise affecting immune responses of European spiny lobster Palinurus elephas (Fabricius, 1787). Can J Zool 93:113–121
Clark CW, Ellison WT, Southall BL, Hatch L, Van Parijs SM, Frankel A, Ponirakis D (2009) Acoustic masking in marine ecosystems: intuitions, analysis, and implication. Mar Ecol Prog Ser 395:201–222
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 52:1880–1887
Coeurdacier JL, Dutto G, Gasset E, Blancheton JP (2011) Is total serum protein a good indicator for welfare in reared sea bass (Dicentrarchus labrax)? Aquat Living Resour 24:121–127
Díaz-Uriarte R, Alvarez de Andrés S (2006) Gene selection and classification of microarray data using random forest. BMC Bioinformatics 7(1):3. doi:10.1186/1471-2105-7-3
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 414–415:36–45
Filiciotto F, Vazzana M, Celi M, Maccarrone V, Ceraulo M, Buffa G, Di Stefano V, Mazzola S, Buscaino G (2014) Behavioural and biochemical stress responses of Palinurus elephas after exposure to boat noise pollution in tank. Mar Pollut Bull 84:104–114
Graham AL, Cooke SJ (2008) The effects of noise disturbance from various recreational boating activities common to inland waters on the cardiac physiology of a freshwater fish, the largemouth bass (Micropterus salmoides). Aquat Conserv 18:1315–1324. doi:10.1002/aqc.941
Green DM, Deferrari HA, McFadden D, Pearse JS, Popper AN, Richardson WJ, Ridgway SH, Tyack PL (1994) Low-frequency sound and marine mammals: current knowledge and research needs. National Research Council, Washington
Gronquist D, Berges JA (2013) Effects of aquarium-related stressors on the zebrafish: a comparison of behavioral, physiological, and biochemical indicators. J Aquat Anim Health 25:53–65. doi:10.1080/08997659.2012.747450
Hadi AA, Shokr AE, Alwan SF (2009) Effect of aluminium on the biochemical parameters of freshwater fish, Tilapia zilli. J Sci Appl 3:33–41
Heath AG (1990) Summary and perspectives. Am Fish Soc Symp 8:183–191
Hildebrand JA (2009) Anthropogenic and natural sources of ambient noise in the ocean. Mar Ecol Prog Ser 395:5–20
Holles S, Simpson SD, Radford AN, Berten L, Lecchini D (2013) Boat noise disrupts orientation behaviour in a coral reef fish. Mar Ecol Prog Ser 485:295–300. doi:10.3354/meps10346
Jones DR, Randall DJ (1978) The respiratory and circulatory systems during exercise. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 7. Academic Press, New York, pp 425–501
Kight CR, Swaddle JP (2011) How and why environmental noise impacts animals: an integrative, mechanistic review. Ecol Lett 14:1052–1061. doi:10.1111/j.1461-0248.2011.01664.x
Kori-Siakpere O, Ikomi BR, Ogbe MG (2011) Biochemical response of the African catfish: Clarias gariepinus (Burchell, 1822) to sublethal concentrations of potassium permanganate. Ann Biol Res 2:1–10
Lagardère JP (1982) Effects of noise on growth and reproduction of Crangon crangon in rearing tanks. Mar Biol 71:177–185
Liaw A, Wiener M (2002) Classification and regression by random forest. R News 2:18–22
Lowe CJ, Davison W (2005) Plasma osmolarity, glucose concentration and erythrocyte responses of two Antarctic nototheniid fishes to acute and chronic thermal change. J Fish Biol 67:752–766
Martinez-Porchas M, Martinez-Cordova LR, Ramos-Enriquez R (2009) Cortisol and glucose: reliable indicators of stress? Pan Am J Aquat Sci 4:158–178
Maule AG, Schreck CB, Kaattari SL (1987) Changes in the immune system of coho salmon (Oncorhynchus kisutch) during the parr-to-smolt transformation and after implantation of cortisol. Can J Fish Aquat Sci 44:161–166
Mc Donald DG, Hope H, Wood CM (1980) The influence of calcium on the physiological responses of the rainbow trout, Salmo gairdneri, to low environmental pH. J Exp Biol 88:109–131
McDonald JI, Wilkens SL, Stanley JA, Jeffs AG (2014) Vessel generator noise as a settlement cue for marine biofouling species. Biofouling 30:741–749
Mesa MG (1994) Effects of multiple acute stressors on the predator avoidance ability and physiology of juvenile chinook salmon. Trans Am Fish Soc 123:786–793
Morley EL, Jones G, Radford AN (2014) The importance of invertebrates when considering the impacts of anthropogenic noise. Proc R Soc B Biol Sci 281(1776):20132683. doi:10.1098/rspb.2013.2683
Muazzez O, Atli G, Canli M (2009) Effects of metal (Ag, Ad, Cr, Cu, Zn) exposures on some enzymatic and non-enzymatic indicators in the liver of Oreochromis niloticus. Bull Environ Contam Toxicol 82:317–321
Mugnier C, Fostier A, Guezou S, Gaignon JL, Quemener L (1998) Effect of some repetitive factors on turbot stress response. Aquacult Int 6:33–45
Okumura T, Akamatsu T, Yan HY (2002) Analyses of small tank acoustics: empirical and theoretical approaches. Bioacoustics 12:330–332
Panigada S, Pavan G, Borg J, Bella A, Galil S, Vallini C (2008) Biodiversity impacts of ship movement noise, grounding and anchoring. In: Abdulla A, Linden O (eds) Maritime traffic effects on biodiversity in the Mediterranean Sea: review of impacts, priority areas and mitigation measures. IUCN Centre for Mediterranean Cooperation, Malaga, p 184
Parvathi K, Sivakumar P, Sarasu Ramesh M (2011) Sublethal effects of chromium on some biochemical profiles of the fresh water teleost, Cyprinus carpio. Int J Appl Biol Pharm Technol 2:295–300
Parvulescu A (1964) Problems of propagation and processing. In: Tavolga WN (ed) Marine bio-acoustics. Pergamon Press, Oxford, pp 87–100
Parvulescu A (1967) The acoustics of small tanks. In: Tavolga WN (ed) Marine bio-acoustics, vol 2. Pergamon Press, Oxford
Picciulin M, Sebastianutto L, Codarin A, Farina A, Ferrero EA (2010) In situ behavioural responses to boat noise exposure of Gobius cruentatus (Gmelin, 1789; fam Gobiidae) and Chromis chromis (Linnaeus, 1758; fam Pomacentridae) living in a marine protected area. J Exp Mar Biol Ecol 386:125–132
Pickering AD (1981) Introduction: the concept of biological stress. In: Pickering AD (ed) Stress and fish. Academic Press, New York, pp 1–7
Pickering AD, Pottinger TG, Carragher J, Sumpter JP (1987) The effects of acute and chronic stress on the levels of reproductive hormones in the plasma of mature male brown trout, Salmo trutta L. Gen Comp Endocrinol 68:249–259
Popper AN, Fay RR, Platt C, Sand O (2003) Sound detection mechanism and capabilities of teleost fishes. In: Collin SP, Marshall NJ (eds) Sensory processing in aquatic environments. Springer, New York, pp 3–38
Ross D (2005) Ship sources of ambient noise. IEEE J Ocean Eng 30:257–261
Sandström A, Eriksson BK, Karås P, Isaeus M, Schreiber H (2005) Boating and navigation activities influence the recruitment of fish in a Baltic Sea archipelago area. J Hum Environ 34:125–130
Sarà G, Dean JM, D’Amato D, Buscaino G, Oliveri A, Genovese S, Ferro S, Buffa G, Lo Martire M, Mazzola S (2007) Effect of shipping traffic on behaviour of bluefin tuna Thunnus thynnus. Mar Ecol Prog Ser 331:243–253
Scholik AR, Yan HY (2001) Effects of underwater noise on auditory sensitivity of a cyprinid fish. Hear Res 152:17–24
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
Smith ME, Kane AS, Popper AN (2004) Noise-induced stress response and hearing loss in goldfish (Carassius auratus). J Exp Biol 207:427–435
Sumpter JP, Dye HM, Benfey TJ (1986) The effects of stress on plasma ACTH, alpha-MSH, and cortisol levels in salmonid fishes. Gen Comp Endocrinol 62:377–385
Voellmy IK, Purser J, Flynn D, Kennedy P, Simpson SD, Radford AN (2014a) Acoustic noise reduces foraging success via different mechanisms in two sympatric fish species. Anim Behav 89:191–198
Voellmy IK, Purser J, Simpson SD, Radford AN (2014b) Increased noise levels have different impacts on the anti-predator behaviour of two sympatric fish species. PLoS ONE 9:e102946. doi:10.1371/journalpone0102946
Wale MA, Simpson SD, Radford AN (2013) Noise negatively affects foraging and antipredator behaviour in shore crabs. Anim Behav 86:111–118
Weilgart LS (2007) The impacts of anthropogenic ocean noise on cetaceans and implications for management. Can J Zool 85:1091–1116
Wells RMG, Pankhurst NW (1999) Evaluation of simple instruments for the measurement of blood glucose and lactate, and plasma protein as stress indicators in fish. J World Aquac Soc 30:276–284
Wells RMG, Weber RE (1990) The spleen in hypoxic and exercised rainbow trout. J Exp Biol 150:461–466
Wysocki LE, Dittami JP, Ladich F (2006) Ship noise and cortisol secretion in European freshwater fishes. Biol Conserv 128:501–508
Yamamoto K, Itazawa Y, Kobayashi H (1980) Supply of erythrocytes into the circulating blood from the spleen of exercised fish. Comp Biochem Physiol A65:5–11
Acknowledgments
The authors thank Valentina Corrias and Giovanni de Vincenzi for their valuable assistance in field organization and technical support. This work has been funded by the Flagship Project RITMARE—the Italian Research for the Sea coordinated by the Italian National Research Council and funded by the Italian Ministry of Education, University and Research within the National Research Program 2011–2013.
Author information
Authors and Affiliations
Corresponding author
Additional information
Mirella Vazzana and Giuseppa Buscaino have contributed equally to this work.
Rights and permissions
About this article
Cite this article
Celi, M., Filiciotto, F., Maricchiolo, G. et al. Vessel noise pollution as a human threat to fish: assessment of the stress response in gilthead sea bream (Sparus aurata, Linnaeus 1758). Fish Physiol Biochem 42, 631–641 (2016). https://doi.org/10.1007/s10695-015-0165-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-015-0165-3