Behavioral guidance systems are commonly used in freshwater fish conservation. The biological relevance of sound to fish and recorded responses to human-generated noise supports the viability of the use of acoustics as an effective stimulus in such technologies. Relatively little information exists on the long-term responses and recovery of fish to repeated acoustic exposures. In a controlled laboratory study, the response and tolerance of Eurasian minnow (Phoxinus phoxinus) shoals to tonal signals (150 Hz of 1 s pulse duration) differing only in temporal characteristics (“continuous,” “slow,” “intermediate,” or “fast” pulse repetition rate) were investigated. In comparison to independent control groups, fish increased their mean group swimming speed, decreased inter-individual distance, and became more aligned in response to the onset of all four acoustic treatments. The magnitude of response, and time taken to develop a tolerance to a treatment differed according to pulse repetition rate. Groups were found to have the greatest and longest lasting response to tone sequences tested in this study when they were pulsed at an intermediate rate of 0.2 s−1. This study illustrates the importance of understanding the response of fish to acoustic signals, and will assist toward the development of longer-term effective acoustic guidance systems.
References
1.
Akamatsu
, T.
, Okumura
, T.
, Novarini
, N.
, and Yan
, H. Y.
(2002
). “Empirical refinements applicable to the recording of fish sounds in small tanks
,” J. Acoust. Soc. Am.
112
, 3073
–3082
.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.
Blumstein
, D. T.
(2016
). “Habituation and sensitization: New thoughts about old ideas
,” Anim. Behav.
120
, 255
–262
.4.
Burner
, C. J.
, and Moore
, H. L.
(1962
). “Attempts to guide small fish with underwater sound
,” U.S. Fish Wildl. Ser., Spec. Sci Rep. Fish.
403
, 1
–30
.5.
Currie
, H. A. L.
, White
, P. R.
, Leighton
, T. G.
, and Kemp
, P. S.
(2020
). “Collective behavior of the European minnow (Phoxinus phoxinus) in response to signals of differing acoustic complexity
,” (in press).6.
de Jong
, K.
, Amorim
, M. C. P.
, Fonseca
, P. J.
, Fox
, C. J.
, and Heubel
, K. U.
(2018
). “Noise can affect acoustic communication and subsequent spawning success in fish
,” Environ. Pollut.
237
, 814
–823
.7.
Deleau
, M. J. C.
, White
, P. R.
, Peirson
, G.
, Leighton
, T. G.
, and Kemp
, P. S.
(2019
). “Use of acoustics to enhance the efficiency of physical screens designed to protect downstream moving European eel (Anguilla Anguilla)
,” Fish. Manag. Ecol.
27
, 1
–9
.8.
Dunning
, D. J.
, Ross
, Q. E.
, Geoghegan
, P.
, Reichle
, J. J.
, Menezes
, J. K.
, and Watson
, J. K.
(1992
). “Alewives avoid high-frequency sound
,” N. Am. J. Fish. Manag.
12
(3
), 407
–416
.9.
Geffroy
, B.
, Samia
, D. S. M.
, Bessa
, E.
, and Blumstein
, D. T.
(2015
). “How nature-based tourism might increase prey vulnerability to predators
,” Trends Ecol. Evolut.
30
(12
), 755
–765
.10.
Gray
, M.
, Rogers
, P. H.
, and Zeddies
, D. G.
(2016
). “Acoustic particle motion measurement for bioacousticians: Principles and pitfalls
,” Proc. Mtgs. Acoust.
27
, 010022
.11.
Greenhouse
, S. W.
, and Geisser
, S.
(1959
). “On methods in the analysis of profile data
,” Psychometrika.
24
, 95
–112
.12.
Handegard
, N. O.
, Boswall
, K. M.
, Ioannou
, C. C.
, Leblanc
, S. P.
, Tjøstheim
, D. B.
, and Couzin
, I. D.
(2012
). “The dynamics of coordinated group hunting and collective information transfer among schooling prey
,” Curr. Biol.
22
(13
), 1213
–1217
.13.
Harpaz
, R.
, Tkačik
, G.
, and Schneidman
, E.
(2017
). “Discrete modes of social information processing predict individual behaviour of fish in a group
,” Proc. Natl. Acad. Sci.
114
(38
), 10149
–10154
.14.
Hasan
, M. R.
, Crane
, A. L.
, Ferrari
, M. C. O.
, and Chivers
, D. P.
(2018
). “A cross-modal effect of noise: The disappearance of the alarm reaction of a freshwater fish
,” Anim. Cogn.
21
(3
), 419
–424
.15.
Hawkins
, A. D.
, and Myrberg
, A. A.
(1983
). “Hearing and sound communication underwater
,” in Bioacoustics, a Comparative Approach
, edited by B.
Lewis
(Academic
, London
), pp. 347
–405
.16.
Hawkins
, A. D.
, and Popper
, A. N.
(2018
). “Directional hearing and sound source localization by fishes
,” J. Acoust. Soc. Am.
144
, 3329
–3350
.17.
Herbert-Read
, H. E.
, Kremer
, L.
, Bruintjes
, R.
, Radford
, A. N.
, and Ioannou
, C. C.
(2017
). “Anthropogenic noise pollution from pile-driving disrupts the structure and dynamics of fish shoals
,” Proc. R. Soc. London, Ser. B
284
(1863
), 20171627
.18.
Huynh
, H.
, and Feldt
, L. S.
(1976
). “Estimation of the box correction for degrees of freedom from sample data in randomized block and split-plot designs
,” J. Ed. Stat.
1
, 69
–82
.19.
Huynh
, H.
, and Mandeville
, G. K.
(1979
). “Validity conditions in repeated measures designs
,” Psych. Bull.
86
(5
), 964
–973
.20.
Katsnelson
, B.
, Petnikov
, V.
, and Lynch
, J.
(2012
). “Fundamentals of shallow water acoustics
,” in The Underwater Acoustics Series
(Springer
, New York
).21.
Kent
, M. I. A.
, Lukeman
, R.
, Lizier
, J. T.
, and Ward
, A. J. W.
(2019
). “Speed-mediated properties of schooling
,” R. Soc. Open. Sci.
6
(2
), 181482
.22.
Maes
, J.
, Turnpenny
, A. W. H.
, Lambert
, D. R.
, Nedwell
, J. R.
, Parmentier
, A.
, and Ollevier
, F.
(2004
). “Field evaluation of a sound system to reduce estuarine fish intake rates at a power plant cooling water inlet
,” J. Fish Biol.
64
, 938
–946
.23.
Mann
, D. A.
, and Lobel
, P. S.
(1997
). “Propagation of damselfish (Pomacentridae) courtship sounds
,” J. Acoust. Soc. Am.
101
, 3783
–3791
.24.
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
.25.
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 (Gadus morhua
),” Proc. R. Soc. B
282
, 20151943
.26.
Neo
, Y. Y.
, Hubert
, J.
, Bolle
, L.
, 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
, 369
–374
.27.
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
.28.
Neo
, Y. Y.
, Parie
, L.
, Bakker
, F.
, Snelderwaard
, P.
, Tudorache
, C.
, Schaaf
, M.
, and Slabbekoorn
, H.
(2015a
). “Behavioural changes in response to sound exposure and no spatial avoidance of noisy conditions in captive zebrafish
,” Front. Behav. Neurosci.
9
, 28
.29.
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
.30.
Neo
, Y. Y.
, Ufkes
, E.
, Kastelein
, R. A.
, Winter
, H. V.
, ten Cate
, C.
, and Slabbekoorn
, H.
(2015b
). “Impulsive sounds change European seabass swimming patterns: Influence of pulse repetition interval
,” Mar. Pollut. Bull.
97
(1-2
), 111
–117
.31.
Popper
, A. N.
, and Carlson
, T. J.
(1998
). “Application of sound and other stimuli to control fish behaviour
,” Trans. Am. Fish. Soc.
127
(5
), 673
–707
.32.
Popper
, A. N.
, and Hastings
, M. C.
(2009
). “Effects of anthropogenic sources of sound on fishes
,” J. Fish Biol.
75
, 455
–489
.33.
Piper
, A. T.
, White
, P. R.
, Wright
, R. M.
, Leighton
, T. G.
, and Kemp
, P. S.
(2019
). “Response of seaward migrating European eel (Anguilla anguilla) to an infrasound deterrent
,” Ecol. Eng.
127
, 480
–486
.34.
Rankin
, C. H.
, Abrams
, T.
, Barry
, R. J.
, Bhatnagar
, S.
, Clayton
, D.
, Colombo
, J.
, Coppola
, G.
, Geyer
, M. A.
, Glanzman
, D. L.
, Marsland
, S.
, McSweeney
, F.
, Wilson
, D. A.
, Wu
, C.-F.
, and Thompson
, R. F.
(2009
). “Habituation revisited: An updated and revised description of the behavioural characteristics of habituation
,” Neurobiol. Learn. Mem.
92
(2
), 135
–138
.35.
Sabet
, S. S.
, Neo
, Y. Y.
, and Slabbekoorn
, H.
(2015
). “The effect of temporal variation in sound exposure on swimming and foraging behaviour of captive zebrafish
,” Anim. Behav.
107
, 49
–60
.36.
Salas
, A. K.
, Wilson
, P. S.
, and Ryan
, M. J.
(2018
). “Acoustic communication in the Bocon toadfish (Amphichthys cryptocentrus)
,” Environ. Biol. Fish.
101
, 1175
–1193
.37.
Scruton
, D. A.
, McKinley
, R. S.
, Kouwen
, N.
, Eddy
, W.
, and Booth
, R. K.
(2003
). “Improvement and optimization of fish guidance efficiency (FGE) at a behavioural fish protection system for downstream migrating Atlantic salmon (Salmo salar) smolts
,” River Res. Appl.
19
(5-6
), 605
–617
.38.
Simpson
, S. D.
, Meekan
, M.
, Montgomery
, J.
, McCauley
, R.
, and Jeffs
, A.
(2005
). “Homeward sound
,” Science.
308
, 221
.39.
Smith
, M. E.
, Kane
, A. S.
, and Popper
, A.
(2004
). “Noise-induced stress response and hearing loss in goldfish (Carassius auratus)
,” J. Exp. Biol.
207
, 427
–435
.40.
The R Foundation for Statistical Computing
(2015
). http://www.r-project.org/ (Last viewed 9/20/2015)41.
Tonolla
, D.
, Acuña
, V.
, Lorang
, M. S.
, Heutschi
, K.
, and Tockner
, K.
(2010
). “A field-based investigation to examine underwater soundscapes of five common river habitats
,” Hydrol. Process.
24
, 3146
–3156
.42.
43.
Vetter
, B. J.
, Cupp
, A. R.
, Fredricks
, K. T.
, Gaikowski
, M. P.
, and Mensinger
, A. F.
(2015
). “Acoustical deterrence of Silver Carp (Hypophthalmichthys molitrix)
,” Biol. Invasions.
17
(12
), 3383
–3392
.44.
Voellmy
, I. K.
, Purser
, J.
, Simpson
, S. D.
, and Radford
, A. N.
(2016
). “Effects of previous acoustic experience on behavioural response to experimental sound stimuli and implications for research
,” in The Effects of Noise on Aquatic Life II
, Vol. 875
of Advances in Experimental Medicine and Biology, edited by A.
Popper
and A.
Hawkins
(Springer
, New York
).45.
Ward
, D.
, Morison
, F.
, Morrissey
, E.
, Jenks
, K.
, and Watson
, W. H.
(2011
). “Evidence that potential fish predators elicit the production of carapace vibrations by the American lobster
,” J. Exp. Biol.
214
, 2641
–2648
.© 2020 Acoustical Society of America.
2020
Acoustical Society of America
You do not currently have access to this content.
