Anthropogenic activities are causing increased noise levels in the marine environment. To date, few studies have been undertaken to investigate the effects of different noise frequencies on the behaviour of juvenile fish. In this study, the behavioural changes of juvenile gilthead seabream (Sparus aurata) are evaluated when exposed to white noise filtered in third-octave bands centred at 63, 125, 500, and 1000 Hz (sound pressure level, 140–150 dB re 1 μΡa) for 7 h. The group dispersion, motility, and swimming height of the fish were analysed before and during the acoustic emission. Dispersion of the fish was found to reduce immediately upon application of low frequency sound (63 and 125 Hz) with a return to control condition after 2 h (indicative of habituation), whereas at 1 kHz, dispersion increased after 2 h without any habituation. The motility decreased significantly at 63 Hz throughout the 7 h of sound exposure. The swimming height decreased significantly for all frequencies other than 125 Hz. The results of this study highlight significant variations in the behavioural responses of juvenile fish that could have consequences on their fitness and survival.

1.
Anderson
,
P. A.
,
Berzins
,
I. K.
,
Fogarty
,
F.
,
Hamlin
,
H. J.
, and
Guillette
,
L. J.
, Jr.
(
2011
). “
Sound, stress, and seahorses: The consequences of a noisy environment to animal health
,”
Aquaculture
311
,
129
138
.
2.
Bejder
,
L.
,
Samuels
,
A.
,
Whitehead
,
H.
,
Finn
,
H.
, and
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
.
3.
Benhaïm
,
D.
,
Péan
,
S.
,
Lucas
,
G.
,
Blanc
,
N.
,
Chatain
,
B.
, and
Bégout
,
M.-L.
(
2012
). “
Early life behavioural differences in wild caught and domesticated seabass (Dicentrarchus labrax
),”
Appl. Anim. Behav. Sci.
141
,
79
90
.
4.
Blaxter
,
J. H. S.
,
Gray
,
J. A. B.
, and
Denton
,
E. J.
(
1981
). “
Sound and startle responses in herring shoals
,”
J. Mar. Biol. Assoc. U. K.
61
,
851
869
.
5.
Blom
,
E. L.
,
Kvarnemo
,
C.
,
Dekhla
,
I.
,
Schöld
,
S.
,
Andersson
,
M. H.
,
Svensson
,
O.
, and
Amorim
,
M. C. P.
(
2019
). “
Continuous but not intermittent noise has a negative impact on mating success in a marine fish with paternal care
,”
Sci. Rep.
9
(
1
),
5494
.
6.
Borsani
,
J.
,
Faulkner
,
R.
, and
Merchant
,
N.
(
2015
). “
Impacts of noise and use of propagation models to predict the recipient side of noise
,” Report prepared under contract ENV.D.2/FRA/2012/0025 for the European Commission, Centre for Environment, Fisheries and Aquaculture Science, UK.
7.
Brewer
,
M.
(
2000
). “
Research design and issues of validity
,” in
Handbook of Research Methods in Social and Personality Psychology
, edited by
H.
Reis
and
C.
Judd
(
Cambridge University Press
,
Cambridge, UK
), pp.
3
16
.
8.
Bruintjes
,
R.
,
Harding
,
H.
,
Bunce
,
T.
,
Birch
,
F.
,
Lister
,
J.
,
Spiga
,
I.
,
Benson
,
T.
,
Rossington
,
S.
,
Jones
,
D.
,
Tyler
,
C.
,
Radford
,
A.
, and
Simpson
,
S.
(
2017
). “
Shipbuilding docks as experimental systems for realistic assessments of anthropogenic stressors on marine organisms
,”
Bioscience
67
(
9
),
853
859
.
9.
Buscaino
,
G.
,
Filiciotto
,
F.
,
Buffa
,
G.
,
Bellante
,
A.
,
Stefano
,
V. D.
,
Assenza
,
A.
,
Fazio
,
F.
,
Caola
,
G.
, and
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
.
10.
Cachat
,
J.
,
Stewart
,
A.
,
Grossman
,
L.
,
Gaikwad
,
S.
,
Kadri
,
F.
,
Chung
,
K. M.
,
Wu
,
N.
,
Wong
,
K.
,
Roy
,
S.
,
Suciu
,
C.
,
Goodspeed
,
J.
,
Elegante
,
M.
,
Bartels
,
B.
,
Elkhayat
,
S.
,
Tien
,
D.
,
Tan
,
J.
,
Denmark
,
A.
,
Gilder
,
T.
,
Kyzar
,
E.
,
Dileo
,
J.
,
Frank
,
K.
,
Chang
,
K.
,
Utterback
,
E.
,
Hart
,
P.
, and
Kalueff
,
A. V.
(
2010
). “
Measuring behavioral and endocrine responses to novelty stress in adult zebrafish
,”
Nat. Protoc.
5
,
1786
1799
.
11.
Carroll
,
A. G.
,
Przeslawski
,
R.
,
Duncan
,
A.
,
Gunning
,
M.
, and
Bruce
,
B.
(
2017
). “
A critical review of the potential impacts of marine seismic surveys on fish and invertebrates
,”
Mar. Poll. Bull.
114
,
9
24
.
12.
Casper
,
B. M.
,
Smith
,
M. E.
,
Halvorsen
,
M. B.
,
Sun
,
H.
,
Carlson
,
T. J.
, and
Popper
,
A. N.
(
2013
). “
Effects of exposure to pile driving sounds on fish inner ear tissues
,”
Comp. Biochem. Physiol. Part A Mol. Integr. Physiol.
166
,
352
360
.
13.
Castellote
,
M.
,
Clark
,
C. W.
, and
Lammers
,
M. O.
(
2012
). “
Acoustic and behavioural changes by fin whales (Balaenoptera physalus) in response to shipping and airgun noise
,”
Biol. Conserv.
147
,
115
122
.
14.
Celi
,
M.
,
Filiciotto
,
F.
,
Maricchiolo
,
G.
,
Genovese
,
L.
,
Quinci
,
E. M.
,
Maccarrone
,
V.
,
Mazzola
,
S.
,
Vazzana
,
M.
, and
Buscaino
,
G.
(
2016
). “
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
.
15.
Ceraulo
,
M.
,
Bruintjes
,
R.
,
Benson
,
T.
,
Rossington
,
K.
,
Farina
,
A.
, and
Buscaino
,
G.
(
2016
). “
Relationships of underwater sound pressure and particle velocity during pile driving in a flooded dock
,”
Proc. Mtgs. Acoust.
27
, 0
40007
.
16.
Codarin
,
A.
,
Wysocki
,
L. E.
,
Ladich
,
F.
, and
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
.
17.
Cox
,
T. M.
,
Ragen
,
T. J.
,
Read
,
A. J.
,
Vos
,
E.
,
Baird
,
R. W.
,
Balcomb
,
K.
,
Barlow
,
J.
,
Caldwell
,
J.
,
Cranford
,
T.
,
Crum
,
L.
,
D'Amico
,
A.
,
D'Spain
,
G.
,
Fernández
,
A.
,
Finneran
,
J.
,
Gentry
,
R.
,
Gerth
,
W.
,
Gulland
,
F.
,
Hildebrand
,
J.
,
Houser
,
D.
,
Hullar
,
T.
,
Jepson
,
P. D.
,
Ketten
,
D.
,
MacLeod
,
C. D.
,
Miller
,
P.
,
Moore
,
S.
,
Mountain
,
D.
,
Palka
,
D.
,
Ponganis
,
P.
,
Rommel
,
S.
,
Rowles
,
T.
,
Taylor
,
B.
,
Tyack
,
P.
,
Wartzok
,
D.
,
Gisiner
,
R.
,
Mead
,
J.
, and
Benner
,
L.
(
2006
). “
Understanding the impacts of anthropogenic sound on beaked whales
,”
J. Cetacean Res. Manag.
7
,
177
187
.
18.
Day
,
R. D.
,
McCauley
,
R. M.
,
Fitzgibbon
,
Q. P.
,
Hartmann
,
K.
, and
Semmens
,
J. M.
(
2016
). “
Assessing the impact of marine seismic surveys on southeast Australian scallop and lobster fisheries
,” University of Tasmania, Hobart, October.
19.
Dekeling
,
R. P. A.
,
Tasker
,
M. L.
,
Van der Graaf
,
A. J.
,
Ainslie
,
M. A.
,
Andersson
,
M. H.
,
André
,
M.
,
Borsani
,
J. F.
,
Brensing
,
K.
,
Castellote
,
M.
,
Cronin
,
D.
,
Dalen
,
J.
,
Folegot
,
T.
,
Leaper
,
R.
,
Pajala
,
J.
,
Redman
,
P.
,
Robinson
,
S. P.
,
Sigray
,
P.
,
Sutton
,
G.
,
Thomsen
,
F.
,
Werner
,
S.
,
Wittekind
,
D.
, and
Young
,
J. V.
(
2014
). “
Monitoring guidance for underwater noise in European seas, Part II: Monitoring guidance specifications
, JRC Scientific and Policy Report EUR 26555 EN,” Publications Office of the European Union, Luxembourg.
20.
De Quirós
,
J. B.
,
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
,
M.
,
Iñíguez
,
F. M. D.
,
Johnson
,
M.
,
Komnenou
,
A.
,
Koopman
,
H.
,
Pabst
,
D. A.
,
Roe
,
W. D.
,
Sierra
,
E.
,
Tejedor
,
M.
, and
Schorr
,
G.
(
2019
). “
Advances in research on the impacts of anti-submarine sonar on beaked whales
,”
Proc. R. Soc. B
286
,
20182533
.
21.
Doksæter
,
L.
,
Handegard
,
N. O.
,
Godø
,
O. R.
,
Kvadsheim
,
P. H.
, and
Nordlund
,
N.
(
2012
). “
Behavior of captive herring exposed to naval sonar transmissions (1.0–1.6 kHz) throughout a yearly cycle
,”
J. Acoust. Soc. Am.
131
,
1632
1642
.
22.
Domjan
,
M.
(
2010
).
The Principles of Learning and Behaviour
, 6th ed. (
Wadsworth, Cengage Learning
,
Belmont, CA
).
23.
Fakan
,
E. P.
, and
McCormick
,
M. I.
(
2019
). “
Boat noise affects the early life history of two damselfishes
,”
Mar. Poll. Bull.
141
,
493
500
.
24.
Ferrari
,
M. C. O.
,
McCormick
,
M. I.
,
Meekan
,
M. G.
,
Simpson
,
S. D.
,
Nedelec
,
S. L.
, and
Chivers
,
D. P.
(
2018
). “
School is out on noisy reefs: The effect of boat noise on predator learning and survival of juvenile coral reef fishes
,”
Proc. R. Soc. B
285
,
20180033
.
25.
Fewtrell
,
J. L.
, and
McCauley
,
R. D.
(
2012
). “
Impact of air gun noise on the behaviour of marine fish and squid
,”
Mar. Pollut. Bull.
64
,
984
993
.
26.
Filiciotto
,
F.
,
Giacalone
,
V. M.
,
Fazio
,
F.
,
Buffa
,
G.
,
Piccione
,
G.
,
Maccarrone
,
V.
,
Di Stefano
,
V.
,
Mazzola
,
S.
, and
Buscaino
,
G.
(
2013
). “
Effects of acoustic environment on gilthead sea bream (Sparus aurata): Sea and onshore aquaculture background noise
,”
Aquaculture.
414–415
,
36
45
.
27.
Filiciotto
,
F.
,
Vazzana
,
M.
,
Celi
,
M.
,
Maccarrone
,
V.
,
Ceraulo
,
M.
,
Buffa
,
G.
,
Di Stefano
,
V.
,
Mazzola
,
S.
, and
Buscaino
,
G.
(
2014
). “
Behavioural and biochemical stress responses of Palinurus elephas after exposure to boat noise pollution in tank
,”
Mar. Poll. Bull.
84
,
104
114
.
28.
Fine
,
M. L.
,
King
,
T. L.
,
Ali
,
H.
,
Sidker
,
N.
, and
Cameron
,
T. M.
(
2016
). “
Wall structure and material properties cause viscous damping of swim bladder sounds in the oyster toadfish Opsanus tau
,”
Proc. R. Soc. London B
283
,
1
9
.
29.
Gerlotto
,
F.
, and
Fréon
,
P.
(
1992
). “
Some elements on vertical avoidance of fish schools to a vessel during acoustic surveys
,”
Fish. Res.
14
,
251
259
.
30.
Gordon
,
J.
,
Gillespie
,
D.
,
Potter
,
J.
,
Frantzis
,
A.
,
Simmonds
,
M. P.
,
Swift
,
R.
, and
Thompson
,
D.
(
2003
). “
A review of the effects of seismic surveys on marine mammals
,”
Mar. Technol. Soc. J.
37
,
16
34
.
31.
Handegard
,
N. O.
,
Michalsen
,
K.
, and
Tjøstheim
,
D.
(
2003
). “
Avoidance behaviour in cod (Gadus morhua) to a bottom-trawling vessel
,”
Aquat. Living Resour.
16
,
265
270
.
32.
Hawkins
,
A.
,
Knudsen
,
F. R.
,
Davenport
,
J.
,
McAllen
,
R.
,
Bloomfield
,
H. J.
,
Schilt
,
C.
, and
Johnson
,
P.
(
2012
). “
Grazing by sprat schools upon zooplankton within an enclosed marine lake
,”
J. Exp. Mar. Biol. Ecol.
411
,
59
65
.
33.
Hawkins
,
A. D.
,
Pembroke
,
A. E.
, and
Popper
,
A. N.
(
2015
). “
Information gaps in understanding the effects of noise on fishes and invertebrates
,”
Rev. Fish Biol. Fish.
25
,
39
64
.
34.
Hawkins
,
A. D.
,
Roberts
,
L.
, and
Cheesman
,
S.
(
2014
). “
Responses of free-living coastal pelagic fish to impulsive sounds
,”
J. Acoust. Soc. Am.
135
,
3101
3116
.
35.
Holles
,
S.
,
Simpson
,
S. D.
,
Radford
,
A. N.
,
Berten
,
L.
, and
Lecchini
,
D.
(
2013
). “
Boat noise disrupts orientation behaviour in a coral reef fish
,”
Mar. Ecol. Prog. Ser.
485
,
295
300
.
36.
Holmes
,
J. L.
,
McWilliam
,
J.
,
Ferrari
,
M. C. O.
, and
McCormick
,
M. I.
(
2017
). “
Juvenile damselfish are affect but desensitize to small motor boat noise
,”
J. Exp. Mar. Biol. Ecol.
494
,
63
68
.
37.
Israeli-Weinstein
,
D.
, and
Kimmel
,
E.
(
1998
). “
Behavioral response of carp (Cyprinus carpio) to ammonia stress
,”
Aquaculture
165
,
81
93
.
38.
Kastelein
,
R. A.
,
van der Heul
,
S.
,
Verboom
,
W. C.
,
Jennings
,
N.
,
van der Veen
,
J.
, and
de Haan
,
D.
(
2008
). “
Startle response of captive North Sea fish species to underwater tones between 0.1 and 64 kHz
,”
Mar. Environ. Res.
65
,
369
377
.
39.
Ketten
,
D. R.
,
Lien
,
J.
, and
Todd
,
S.
(
1993
). “
Blast injury in humpback whale ears: Evidence and implications
,”
J. Acoust. Soc. Am.
94
(
3
),
1849
1850
.
40.
Koolhaas
,
J. M.
,
Bartolomucci
,
A.
,
Buwalda
,
B.
,
de Boer
,
S. F.
,
Flügge
,
G.
,
Korte
,
S. M.
,
Meerlo
,
P.
,
Murison
,
R.
,
Olivier
,
B.
,
Palanza
,
P.
,
Sgoifo
,
A.
,
Steimer
,
T.
,
Stiedl
,
O.
,
van Dijk
,
G.
,
Wöhr
,
M.
, and
Fuchs
,
E.
(
2011
). “
Stress revisited: A critical evaluation of the stress concept
,”
Neurosci. Biobehav. Rev.
35
,
1291
1301
.
41.
Kunc
,
H. P.
,
McLaughlin
,
K. E.
, and
Schmidt
,
R.
(
2016
). “
Aquatic noise pollution: Implications for individuals, populations, and ecosystems
,”
Proc. R. Soc. B Biol. Sci.
283
,
20160839
.
42.
Kuwada
,
H.
,
Masuda
,
R.
,
Shiozawa
,
S.
,
Kogane
,
T.
,
Imaizumi
,
K.
, and
Tsukamoto
,
K.
(
2000
). “
Effect of fish size, handling stresses and training procedure on the swimming behavior of hatchery-reared striped jack: Implications for stock enhancement
,”
Aquaculture
185
,
245
256
.
43.
Lecchini
,
D.
,
Bertucci
,
F.
,
Gache
,
C.
,
Khalife
,
A.
,
Besson
,
M.
,
Roux
,
N.
,
Berthe
,
C.
,
Singh
,
S.
,
Parmentier
,
E.
,
Nugues
,
M. M.
,
Brooker
,
R. M.
,
Dixson
,
D. L.
, and
Hédouin
,
L.
(
2018
). “
Boat noise prevents soundscape based habitat selection by coral planulae
,”
Sci. Rep.
8
,
9283
.
44.
Lepage
,
O.
,
Øverli
,
Ø.
,
Petersson
,
E.
,
Järvi
,
T.
, and
Winberg
,
S.
(
2000
). “
Differential stress coping in wild and domesticated sea trout
,”
Brain Behav. Evol.
56
,
259
268
.
45.
Lloris
,
D.
(
2005
). “
Sparus aurata
,” in A World Overview of Species of Interest to Fisheries, available at www.fao.org/figis/servlet/species?fid=2384. 3p, FIGIS Species Fact Sheets, Species Identification and Data Programme-SIDP, FAO-FIGIS (Last viewed 8 July 2005).
46.
Luca
,
R. M.
, and
Gerlai
,
R.
(
2012
). “
In search of optimal fear inducing stimuli: Differential behavioral responses to computer animated images in zebrafish
,”
Behav. Brain Res.
226
,
66
76
.
47.
Lyamin
,
O. I.
,
Korneva
,
S. M.
,
Rozhnov
,
V. V.
, and
Mukhametov
,
L. M.
(
2011
). “
Cardiorespiratory changes in beluga in response to acoustic noise
,”
Dokl. Biol. Sci.
440
,
257
258
.
48.
Martín López
,
L. M.
,
Miller
,
P. J. O.
,
Aguilar de Soto
,
N.
, and
Johnson
,
M.
(
2015
). “
Gait switches in deep-diving beaked whales: Biomechanical strategies for longduration dives
,”
J. Exp. Biol.
218
,
1325
1338
.
49.
McCauley
,
R. D.
,
Day
,
R. D.
,
Swadling
,
K. M.
,
Fitzgibbon
,
Q. P.
,
Watson
,
R. A.
, and
Semmens
,
J. M.
(
2017
). “
Widely used marine seismic survey air gun operations negatively impact zooplankton
,”
Nat. Ecol. Evol.
1
(
7
),
195
.
50.
McCauley
,
R. D.
,
Fewtrell
,
J.
,
Duncan
,
A. J.
,
Jenner
,
C.
,
Jenner
,
M.-N.
,
Penrose
,
J. D.
,
Prince
,
R. I. T.
,
Adhitya
,
A.
,
Murdoch
,
J.
, and
McCabe
,
K.
(
2000
). “
Marine seismic surveys—A study of environmental implications
,”
APPEA J.
40
,
692
706
.
51.
McCauley
,
R. D.
,
Fewtrell
,
J.
, and
Popper
,
A. N.
(
2003
). “
High intensity anthropogenic sound damages fish ears
,”
J. Acoust. Soc. Am.
113
,
638
642
.
52.
McCormick
,
M. I.
, and
Lönnstedt
,
O. M.
(
2013
). “
Degrading habitats and the effect of topographic complexity on risk assessment
,”
Ecol. Evol.
3
,
4221
4229
.
53.
McCormick
,
M. I.
,
Makey
,
L.
, and
Dufour
,
V.
(
2002
). “
Comparative study of metamorphosis in tropical reef fishes
,”
Mar. Biol.
141
,
841
853
.
54.
McCormick
,
S. D.
,
Shrimpton
,
J. M.
,
Carey
,
J. B.
,
O'Dea
,
M. F.
,
Sloan
,
K. E.
,
Moriyama
,
S.
, and
Björnssonc
,
B. Th.
(
1998
). “
Repeated acute stress reduces growth rate of Atlantic salmon parr and alters plasma levels of growth hormone, insulin-like growth factor I and cortisol
,”
Aquaculture
168
,
221
235
.
55.
Mesa
,
M. G.
(
1994
). “
Effects of multiple acute stressors on the predator avoidance ability and physiology of juvenile chinook salmon
,”
Trans. Am. Fish. Soc.
123
,
786
793
.
56.
Mueller-Blenkle
,
C.
,
McGregor
,
P. K.
,
Gill
,
A. B.
,
Andersson
,
M. H.
,
Metcalfe
,
J.
,
Bendall
,
V.
,
Sigray
,
P.
,
Wood
,
D. T.
, and
Thomsen
,
F.
(
2010
). “
Effects of pile-driving noise on the behaviour of marine fish
,” Tech. Report, COWRIE Ref: Fish 06−08.
57.
Munday
,
P. L.
,
Dixson
,
D. L.
,
McCormick
,
M. I.
,
Meekan
,
M. G.
,
Ferrari
,
M. C. O.
, and
Chivers
,
D. P.
(
2010
). “
Replenishment of fish populations is threatened by ocean acidification
,”
Proc. Natl. Acad. Sci. U.S.A.
107
,
12930
12934
.
58.
Nedelec
,
S. L.
,
Mills
,
S. C.
,
Lecchini
,
D.
,
Nedelec
,
B.
,
Simpson
,
S. D.
, and
Radford
,
A. N.
(
2016
). “
Repeated exposure to noise increases tolerance in a coral reef fish
,”
Environ. Pollut.
216
,
428
436
.
59.
Nedelec
,
S. L.
,
Radford
,
A. N.
,
Pearl
,
L.
,
Nedelec
,
B.
,
McCormick
,
M. I.
,
Meekan
,
M. G.
, and
Simpson
,
S. D.
(
2017
). “
Motorboat noise impacts parental behaviour and offspring survival in a reef fish
,”
Proc. R. Soc. B
284
,
20170143
.
60.
Nedelec
,
S. L.
,
Radford
,
A. N.
,
Simpson
,
S. D.
,
Nedelec
,
B.
,
Lecchini
,
D.
, and
Mills
,
S. C.
(
2014
). “
Anthropogenic noise playback impairs embryonic development and increases mortality in a marine invertebrate
,”
Sci. Rep.
4
,
5891
.
61.
Nedelec
,
S. L.
,
Simpson
,
S. D.
,
Morley
,
E. L.
,
Nedelec
,
B.
, and
Radford
,
A. N.
(
2015
). “
Impacts of regular and random noise on the behaviour, growth and development of larval Atlantic cod (Gadusmorhua
),”
Proc. R. Soc. B
282
,
20151943
.
62.
Nelson
,
D.
, and
Johnson
,
R.
(
1972
). “
Acoustic attraction of Pacific reef sharks: Effect of pulse intermittency and variability
,”
Comp. Biochem. Physiol. Part A Physiol.
42
,
85
95
.
63.
Neo
,
Y. Y.
,
Hubert
,
J.
,
Bolle
,
L. J.
,
Winter
,
H. V.
, and
Slabbekoorn
,
H.
(
2018
). “
European seabass respond more strongly to noise exposure at night and habituate over repeated trials of sound exposure
,”
Environ. Pollut.
239
,
367
374
.
64.
Neo
,
Y. Y.
,
Hubert
,
J.
,
Bolle
,
L.
,
Winter
,
H. V.
,
ten Cate
,
C.
, and
Slabbekoorn
,
H.
(
2016
). “
Sound exposure changes European seabass behaviour in a large outdoor floating pen: Effects of temporal structure and a ramp-up procedure
,”
Environ. Pollut.
214
,
26
34
.
65.
Neo
,
Y. Y.
,
Seitz
,
J.
,
Kastelein
,
R. A.
,
Winter
,
H. V.
,
ten Cate
,
C.
, and
Slabbekoorn
,
H.
(
2014
). “
Temporal structure of sound affects behavioural recovery from noise impact in European seabass
,”
Biol. Conserv.
178
,
65
73
.
66.
Neo
,
Y. Y.
,
Ufkes
,
E.
,
Kastelein
,
R. A.
,
Winter
,
H. V.
,
ten Cate
,
C.
, and
Slabbekoorn
,
H.
(
2015
). “
Impulsive sounds change European seabass swimming patterns: Influence of pulse repetition interval
,”
Mar. Pollut. Bull.
97
,
111
117
.
67.
Nilsson
,
G. E.
,
Ostlund-Nilsson
,
S.
,
Penfold
,
R.
, and
Grutter
,
A. S.
(
2007
). “
From record performance to hypoxia tolerance: Respiratory transition in damselfish larvae settling on a coral reef
,”
Proc. R. Soc. B
274
,
79
85
.
68.
Parmentier
,
E.
, and
Fine
M. L.
(
2016
). “
Fish sound production: Insights
,” in
Vertebrate Sound Production and Acoustic Communication
, edited by
R. A.
Suthers
and
T.
Fitch
(
Springer
,
New York
), pp.
19
49
.
69.
Pearson
,
W. H.
,
Skalski
,
J. R.
, and
Malme
,
C. I.
(
1992
). “
Effects of sounds from a geophysical survey device on behavior of captive rockfish (Sebastes spp
.),”
Can. J. Fish. Aquat. Sci.
49
,
1343
1356
.
70.
Picciulin
,
M.
,
Sebastianutto
,
L.
,
Codarin
,
A.
,
Farina
,
A.
, and
Ferrero
,
E. A.
(
2010
). “
In situ behavioural responses to boat noise exposure of Gobiuscruentatus (Gmelin, 1789; fam. Gobiidae) and Chromischromis (Linnaeus, 1758; fam. Pomacentridae) living in a Marine protected area
,”
J. Exp. Mar. Biol. Ecol.
386
,
125
132
.
71.
Popper
,
A. N.
,
Fay
,
R. R.
,
Platt
,
C.
, and
Sand
,
O.
(
2003
). “
Sound detection mechanism and capabilities of teleost fishes
,” in
Sensory Processing in Aquatic Environments
, edited by
S. P.
Collin
and
N. J.
Marshall
(
Springer
,
New York
), pp.
3
38
.
72.
Popper
,
A. N.
, and
Hawkins
,
A. D.
(
2018
). “
The importance of particle motion to fishes and invertebrates
,”
J. Acoust. Soc. Am.
143
,
470
486
.
73.
Popper
,
A. N.
, and
Hawkins
,
A. D.
(
2019
). “
An overview of fish bioacoustics and the impacts of anthropogenic sounds on fishes
,”
J. Fish Biol.
94
,
692
713
.
74.
Purser
,
J.
, and
Radford
,
A. N.
(
2011
). “
Acoustic noise induces attention shifts and reduces foraging performance in three-spined sticklebacks (Gasterosteus aculeatus
),”
PLoS One
6
,
e17478
.
75.
Rankin
,
C. H.
,
Abrams
,
T.
,
Barry
,
R. J.
,
Bhatnagar
,
S.
,
Clayton
,
D. F.
,
Colombo
,
J.
,
Coppola
,
G.
,
Geyer
,
M. A.
,
Glanzman
,
D. L.
,
Marsland
,
S.
,
McSweeney
,
F. K.
,
Wilson
,
D. A.
,
Wu
,
C.-F.
, and
Thompson
,
R. F.
(
2009
). “
Habituation revisited: An updated and revised description of the behavioral characteristics of habituation
,”
Neurobiol. Learn. Memory.
92
,
135
138
.
76.
Rankin
,
C. H.
, and
Broster
,
B. S.
(
1992
). “
Factors affecting habituation and recovery from habituation in the nematode Caenorhabditis elegans
,”
Behav. Neurosci.
106
,
239
249
.
77.
Rolland
,
R. M.
,
Parks
,
S. E.
,
Hunt
,
K. E.
,
Castellote
,
M.
,
Corkeron
,
P. J.
,
Nowacek
,
D. P.
, and
Kraus
,
S. D.
(
2012
). “
Evidence that ship noise increases stress in right whales
,”
Proc. R. Soc. B: Biolog. Sci.
279
(
1737
),
2363
2368
.
78.
Romano
,
T. A.
,
Keogh
,
M. J.
,
Kelly
,
C.
,
Feng
,
P.
,
Berk
,
L.
,
Schlundt
,
C. E.
,
Carder
,
D. A.
, and
Finneran
,
J. J.
(
2004
). “
Anthropogenic sound and marine mammal health: Measures of the nervous and immune systems before and after intense sound exposure
,”
Can. J. Fish. Aquat. Sci.
61
,
1124
1134
.
79.
Salas
,
A. K.
,
Wilson
,
P. S.
, and
Fuiman
,
L. A.
(
2019
). “
Ontogenetic change in predicted acoustic pressure sensitivity in larval red drum (Sciaenops ocellatus
),”
J. Exp. Biol.
222
,
1
12
.
80.
Santulli
,
A.
,
Modica
,
A.
,
Messina
,
C.
,
Ceffa
,
L.
,
Curatolo
,
A.
,
Rivas
,
G.
,
Fabi
,
G.
, and
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
.
81.
Sarà
,
G.
,
Dean
,
J. M.
,
D'Amato
,
D.
,
Buscaino
,
D.
,
Oliveri
,
A.
,
Genovese
,
S.
,
Ferro
,
S.
,
Buffa
,
G.
,
Lo Martire
,
M.
, and
Mazzola
,
S.
(
2007
). “
Effect of boat noise on the behaviour of bluefin tuna Thunnus thynnus in the mediterranean sea
,”
Mar. Ecol. Prog. Ser.
331
,
243
253
.
82.
Shi
,
W.
,
Han
,
Y.
,
Guan
,
X.
,
Rong
,
J.
,
Du
,
X.
,
Zha
,
S.
,
Tang
,
Y.
, and
Liu
,
G.
(
2019
). “
Anthropogenic noise aggravates the toxicity of cadmium on some physiological characteristics of the blood clam Tegillarca granosa
,”
Front. Physiol.
10
,
377
.
83.
Silva
,
P. I. M.
,
Martins
,
C. I. M.
,
Engrola
,
S.
,
Marino
,
G.
,
Øverli
,
Ø.
, and
Conceicao
,
L. E. C.
(
2010
). “
Individual differences in cortisol levels and behaviour of Senegalese sole (Solea senegalensis) juveniles: Evidence for coping styles
,”
Appl. Anim. Behav. Sci.
124
,
75
81
.
84.
Simpson
,
S. D.
,
Meekan
,
M. G.
,
Larsen
,
N. J.
,
McCauley
,
R. D.
, and
Jeffs
,
A.
(
2010
). “
Behavioral plasticity in larval reef fish: Orientation is influenced by recent acoustic experiences
,”
Behav. Ecol.
21
(
5
),
1098
1105
.
85.
Simpson
,
S. D.
,
Radford
,
A. N.
,
Nedelec
,
S. L.
,
Ferrari
,
M. C.
,
Chivers
,
D. P.
,
McCormick
,
M. I.
, and
Meekan
,
M. G.
(
2016
). “
Anthropogenic noise increases fish mortality by predation
,”
Nat. Commun.
7
,
10544
.
86.
Skilbrei
,
O.
, and
Holst
,
J.
(
2009
). “
Vertical movements of ‘escaped’ farmed Atlantic salmon (Salmo salar L.)—A simulation study in a western Norwegian fjord
,”
ICES J. Mar. Sci.
66
,
278
288
.
87.
Slabbekoorn
,
H.
,
Bouton
,
N.
,
van Opzeeland
,
I.
,
Coers
,
A.
,
ten Cate
,
C.
, and
Popper
,
A. N.
(
2010
). “
A noisy spring: The impact of globally rising underwater sound levels on fish
,”
Trends Ecol. Evol.
25
,
419
427
.
88.
Slotte
,
A.
,
Hansen
,
K.
,
Dalen
,
J.
, and
Ona
,
E.
(
2004
). “
Acoustic mapping of pelagic fish distribution and abundance in relation to a seismic shooting area off the Norwegian west coast
,”
Fish. Res.
67
,
143
150
.
89.
Smith
,
M. E.
,
Kane
,
A. S.
, and
Popper
,
A. N.
(
2004a
). “
Noise-induced stress response and hearing loss in goldfish (Carassius auratus)
,”
J. Exp. Biol.
207
(
3
),
427
435
.
90.
Smith
,
M. E.
,
Kane
,
A. S.
, and
Popper
,
A. N.
(
2004b
). “
Acoustical stress and hearing sensitivity in fishes: Does the linear threshold shift hypothesis hold water?
,”
J. Exp. Biol.
207
,
3591
3602
.
91.
Sogard
,
S. M.
(
1997
). “
Size-selective mortality in the juvenile stage of teleost fishes: A review
,”
Bull. Mar. Sci.
60
,
1129
1157
.
92.
Solé
,
M.
,
Lenoir
,
M.
,
Durfort
,
M.
,
López-Bejar
,
M.
,
Lombarte
,
A.
, and
André
,
M.
(
2013b
). “
Ultrastructural damage of Loligo vulgaris and Illexcoindetii statocysts after low frequency sound exposure
,”
PLoS One
8
(
10
),
e78825
.
93.
Solé
,
M.
,
Lenoir
,
M.
,
Durfort
,
M.
,
López-Bejar
,
M.
,
Lombarte
,
A.
,
van der Schaar
,
M.
, and
André
,
M.
(
2013a
). “
Does exposure to noise from human activities compromise sensory information from cephalopod statocysts?
,”
Deep Sea Res., Part II
95
,
160
181
.
94.
Spiga
,
I.
,
Aldreda
,
N.
, and
Caldwella
,
G. S.
(
2017
). “
Anthropogenic noise compromises the anti-predator behaviour of the European seabass, Dicentrarchus labrax (L.
),”
Mar. Poll. Bull.
122
,
297
305
.
95.
Thorpe
,
W. H.
(
1963
).
Learning and Instinct in Animals
(
Methuen
,
London
),
61
pp.
96.
Van Parijs
,
S. M.
, and
Corkeron
,
P. J.
(
2001
). “
Boat traffic affects the acoustic behaviour of Pacific humpback dolphins, Sousa chinensis
,”
J. Mar. Biol. Assoc. U. K.
81
,
533
538
.
97.
Vasconcelos
,
R. O.
,
Amorim
,
M. C. P.
, and
Ladich
,
F.
(
2007
). “
Effects of ship noise on the detectability of communication signals in the Lusitanian toadfish
,”
J. Exp. Biol.
210
,
2104
2112
.
98.
Vazzana
,
M.
,
Celi
,
M.
,
Arizza
,
V.
,
Calandra
,
G.
,
Buscaino
,
G.
,
Ferrantelli
,
V.
,
Bracciali
,
C.
, and
Sará
,
G.
(
2017
). “
Noise elicits haematological stress parameters in Mediterranean damselfish (Chromis chromis, perciformes): A mesocosm study
,”
Fish Shellfish. Immun.
62
,
147
152
.
99.
Vazzana
,
M.
,
Celi
,
M.
,
Genovese
,
L.
,
Corrias
,
V.
,
Quinci
,
E. M.
,
De Vincenzi
,
G.
,
Maccarrone
,
V.
,
Cammilleri
,
G.
,
Mazzola
,
S.
,
Buscaino
,
G.
, and
Filiciotto
,
F.
(
2016
). “
Are mussels able to distinguish underwater sounds? Assessment of the reactions of Mytilus galloprovincialis after exposure to lab-generated acoustic signals
,”
Compar. Bioch. Phys, A
201
,
61
70
.
100.
Vazzana
,
M.
,
Ceraulo
,
M.
,
Mauro
,
M.
,
Papale
,
E.
,
Dioguardi
,
M.
,
Mazzola
,
S.
,
Arizza
,
V.
,
Chiaramonte
,
M.
, and
Buscaino
,
G.
(
2020b
). “
Effects of acoustic stimulation on biochemical parameters in the digestive gland of Mediterranean mussel Mytilus galloprovincialis (Lamark, 1819)
,”
J. Acoust. Soc. Am.
147
(
4
),
2414
2422
.
101.
Vazzana
,
M.
,
Mauro
,
M.
,
Ceraulo
,
M.
,
Dioguardi
,
M.
,
Papale
,
E.
,
Mazzola
,
S.
,
Arizza
,
V.
,
Beltrame
,
F.
,
Ingugli
,
L.
, and
Buscaino
,
G.
(
2020a
). “
Underwater high frequency noise: Biological responses in sea urchin Arbacia lixula (Linnaeus, 1758
),”
Comp. Bioch. Phys-Part A: Mol. Integr. Phys.
242
,
110650
.
102.
Wardle
,
C. S.
,
Carter
,
T. J.
,
Urquhart
,
G. G.
,
Johnstone
,
A. D. F.
,
Ziolkowski
,
A. M.
,
Hampson
,
G.
, and
Mackie
,
D.
(
2001
). “
Effects of seismic air guns on marine fish
,”
Cont. Shelf Res.
21
,
1005
1027
.
103.
Weilgart
,
L. S.
(
2007
). “
The impacts of anthropogenic ocean noise on cetaceans and implications for management
,”
Can. J. Zool.
85
,
1091
1116
.
104.
Wilson
,
B.
, and
Dill
,
L. M.
(
2002
). “
Pacific herring respond to simulated odontocete echolocation sounds
,”
Can. J. Fish. Aquat. Sci.
59
,
542
553
.
105.
Wood
,
S. N.
,
Pya
,
N.
, and
Säfken
,
B.
(
2016
). “
Smoothing parameter and model selection for general smooth models
,”
J. Am. Stat. Assoc.
111
,
1548
1563
.
106.
Woodley
,
C. M.
, and
Peterson
,
M. S.
(
2003
). “
Measuring responses to simulated predation threat using behavioral and physiological metrics: The role of aquatic vegetation
,”
Oecologia
136
,
155
160
.
107.
Wysocki
,
L. E.
,
Dittami
,
J. P.
, and
Ladich
,
F.
(
2006
). “
Ship noise and cortisol secretion in European freshwater fishes
,”
Bio. Conserv.
128
,
501
508
.
108.
Wysocki
,
L. E.
, and
Ladich
,
F.
(
2005
). “
Effects of noise exposure on click detection and the temporal resolution ability of the goldfish auditory system
,”
Hear. Res.
201
,
27
36
.
109.
Zhou
,
W.
,
Huang
,
X.
, and
Xu
,
X.
(
2018
). “
Changes of movement behavior and HSP70 gene expression in the hemocytes of the mud crab (Scylla paramamosain) in response to acoustic stimulation
,”
Mar. Fresh. Beh. Phys.
51
,
3
14
.
You do not currently have access to this content.