There is increasing awareness of boat sound effects on coral reef assemblages. While behavioral disturbances have been found in fishes, the effects on marine invertebrates remain largely unknown. Here, the behavioral effects of recreational boat sound on thorny oysters at two coral reef habitats within the U.S. Virgin Island National Park were assessed. The “treatment” site was characterized by frequent boat traffic, which increased daytime mean particle acceleration levels (PALrms) by more than 6 dB, while mean PALrms at the “control” site were not contaminated by boat sound. Despite these contrasting soundscapes, all oysters showed the same diurnal cycle, with their valves open at night and partially closed during the day. There was no statistical evidence of behavioral responses in oysters exposed to daytime boat sound. This can be explained by low auditory sensitivity, habituation to a noisy environment due to the pervasiveness of boat sound pollution, or that boat sound may not represent an immediate concern for this species. These findings contrast with laboratory studies that have shown behavioral responses in bivalves exposed to boat sound, highlighting the need for more realistic field-based studies when evaluating potential effects of anthropogenic sounds on this group.
REFERENCES
1.
Apprill
,
A.
,
Girdhar
,
Y.
,
Mooney
,
T. A.
,
Hansel
,
C. M.
,
Long
,
M. H.
,
Liu
,
Y.
,
Zhang
,
W. G.
,
Kapit
,
J.
,
Hughen
,
K.
,
Coogan
,
J.
, and
Greene
,
A.
(2023
). “
Toward a new era of coral reef monitoring
,” Environ. Sci. Technol.
57
, 5117
–5124
.2.
Bates
,
D.
,
Mächler
,
M.
,
Bolker
,
B.
, and
Walker
,
S.
(2015
). “
Fitting linear mixed-effects models using lme4
,” J. Stat. Softw.
67
, 1
–48
.3.
Bejder
,
L.
,
Samuels
,
A. M. Y.
,
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
.4.
Chappell
,
D. R.
,
Horan
,
T. M.
, and
Speiser
,
D. I.
(2021
). “
Panoramic spatial vision in the bay scallop Argopecten irradians
,” Proc. R. Soc. B.
288
, 20211730
.5.
Charifi
,
M.
,
Sow
,
M.
,
Ciret
,
P.
,
Benomar
,
S.
, and
Massabuau
,
J. C.
(2017
). “
The sense of hearing in the Pacific oyster, Magallana gigas
,” PLoS One
12
, e0185353
.6.
Charifi
,
M.
,
Miserazzi
,
A.
,
Sow
,
M.
,
Perrigault
,
M.
,
Gonzalez
,
P.
,
Ciret
,
P.
,
Benomar
,
S.
, and
Massabuau
,
J. C.
(2018
). “
Noise pollution limits metal bioaccumulation and growth rate in a filter feeder, the Pacific oyster Magallana gigas
,” PLoS
One
13
, e0194174
.7.
Comeau
,
L. A.
,
Babarro
,
J. M.
,
Longa
,
A.
, and
Padin
,
X. A.
(2018
). “
Valve-gaping behavior of raft-cultivated mussels in the Ría de Arousa, Spain
,” Aquac. Rep.
9
, 68
–73
.8.
Comeau
,
L. A.
,
Mayrand
,
E.
, and
Mallet
,
A.
(2012
). “
Winter quiescence and spring awakening of the Eastern oyster Crassostrea virginica at its northernmost distribution limit
,” Mar. Biol.
159
, 2269
–2279
.9.
Cones
,
S. F.
,
Jézéquel
,
Y.
, and
Mooney
,
T. A.
(2023
). “
Marine bivalve sound detection and associated noise impacts
,” in 2022 International Conference on the Effects of Noise on Aquatic Life
, Berlin, Germany, July 10–15, 2022 (
Springer Science+Business Media
,
LLC
New York
), in press.10.
Dahl
,
P. H.
, and
Bonnel
,
J.
(2022
). “
Vector acoustic and polarization properties of underwater ship noise
,” J. Acoust. Soc. Am.
151
, 3818
–3827
.11.
Dinh
,
J. P.
,
Suca
,
J. J.
,
Lillis
,
A.
,
Apprill
,
A.
,
Llopiz
,
J. K.
, and
Mooney
,
T. A.
(2018
). “
Multiscale spatio-temporal patterns of boat noise on U.S. Virgin Island coral reefs
,” Mar. Pollut. Bull.
136
, 282
–290
.12.
Duarte
,
C. M.
,
Chapuis
,
L.
,
Collin
,
S. P.
,
Costa
,
D. P.
,
Devassy
,
R. P.
,
Eguiluz
,
V. M.
,
Erbe
,
C.
,
Gordon
,
T. A.
,
Halpern
,
B. S.
,
Harding
,
H. R.
, and
Havlik
,
M. N.
(2021
). “
The soundscape of the Anthropocene ocean
,” Science
371
, eaba4658
.13.
Duncan
,
A. J.
,
Lucke
,
K.
,
Erbe
,
C.
, and
McCauley
,
R. D.
(2016
). “
Issues associated with sound exposure experiments in tanks
,” Proc. Mtgs. Acoust.
27
, 070008
.14.
Feifarek
,
B. P.
(1987
). “
Spines and epibionts as antipredator defenses in the thorny oyster Spondylus americanus Hermann
,” J. Exp. Mar. Biol. Ecol.
105
, 39
–56
.15.
Flamant
,
J.
, and
Bonnel
,
J.
(2023
). “
Broadband properties of potential and kinetic energies in an oceanic waveguide
,” J. Acoust. Soc. Am.
153
, 3012
–3024
.16.
Hubert
,
J.
,
van der Burg
,
A. D.
,
Witbaard
,
R.
, and
Slabbekoorn
,
H.
(2023
). “
Separate and combined effects of boat noise and a live crab predator on mussel valve gape behavior
,” Behav. Ecol.
34
, 495
–505
.17.
Hughes
,
T. P.
,
Kerry
,
J. T.
,
Baird
,
A. H.
,
Connolly
,
S. R.
,
Dietzel
,
A.
,
Eakin
,
C. M.
,
Heron
,
S. F.
,
Hoey
,
A. S.
,
Hoogenboom
,
M. O.
,
Liu
,
G.
, and
McWilliam
,
M. J.
(2018
). “
Global warming transforms coral reef assemblages
,” Nature
556
, 492
–496
.18.
Jézéquel
,
Y.
,
Bonnel
,
J.
,
Aoki
,
N.
, and
Mooney
,
T. A.
(2022a
). “
Tank acoustics substantially distort broadband sounds produced by marine crustaceans
,” J. Acoust. Soc. Am.
152
, 3747
–3755
.19.
Jézéquel
,
Y.
,
Cones
,
S.
,
Jensen
,
F. H.
,
Brewer
,
H.
,
Collins
,
J.
, and
Mooney
,
T. A.
(2022b
). “
Pile driving repeatedly impacts the giant scallop (Placopecten magellanicus)
,” Sci. Rep.
12
, 15380
.20.
Jézéquel
,
Y.
,
Cones
,
S.
, and
Mooney
,
T. A.
(2023
). “
Sound sensitivity of the giant scallop (Placopecten magelanicus) is life stage, intensity, and frequency dependent
,” J. Acoust. Soc. Am.
153
, 1130
–1137
.21.
Jones
,
I. T.
,
Gray
,
M. D.
, and
Mooney
,
T. A.
(2022
). “
Soundscapes as heard by invertebrates and fishes: Particle motion measurements on coral reefs
,” J. Acoust. Soc. Am.
152
, 399
–415
.22.
Kaplan
,
M. B.
, and
Mooney
,
T. A.
(2015
). “
Ambient noise and temporal patterns of boat activity in the US Virgin Islands National Park
,” Mar. Pollut. Bull.
98
, 221
–228
.23.
Kaplan
,
M. B.
, and
Solomon
,
S.
(2016
). “
A coming boom in commercial shipping? The potential for rapid growth of noise from commercial ships by 2030
,” Mar. Policy
73
, 119
–121
.24.
Ledoux
,
T.
,
Clements
,
J.
,
Comeau
,
L.
,
Cervello
,
G.
,
Tremblay
,
R.
,
Olivier
,
F.
,
Chauvaud
,
L.
,
Bernier
,
R. Y.
, and
Lamarre
,
S. G.
(2023
). “
Effects of anthropogenic sounds on the behavior and physiology of the Eastern oyster (Crassostrea virginica)
,” Front. Mar. Sci.
10
, 1104526
.25.
Levitan
,
D. R.
,
Best
,
R. M.
, and
Edmunds
,
P. J.
(2023
). “
Sea urchin mass mortalities 40 y apart further threaten Caribbean coral reefs
,” Proc. Natl. Acad. Sci. U.S.A.
120
, e2218901120
.26.
Merchant
,
N. D.
,
Witt
,
M. J.
,
Blondel
,
P.
,
Godley
,
B. J.
, and
Smith
,
G. H.
(2012
). “
Assessing sound exposure from shipping in coastal waters using a single hydrophone and Automatic Identification System (AIS) data
,” Mar. Pollut. Bull.
64
, 1320
–1329
.27.
Mills
,
S. C.
,
Beldade
,
R.
,
Henry
,
L.
,
Laverty
,
D.
,
Nedelec
,
S. L.
,
Simpson
,
S. D.
, and
Radford
,
A. N.
(2020
). “
Hormonal and behavioural effects of motorboat noise on wild coral reef fish
,” Environ. Pollut.
262
, 114250
.28.
Nagai
,
K.
,
Honjo
,
T.
,
Go
,
J.
,
Yamashita
,
H.
, and
Oh
,
S. J.
(2006
). “
Detecting the shellfish killer Heterocapsa circularisquama (Dinophyceae) by measuring bivalve valve activity with a Hall element sensor
,” Aquaculture
255
, 395
–401
.29.
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
.30.
Nedelec
,
S. L.
,
Radford
,
A. N.
,
Gatenby
,
P.
,
Davidson
,
I. K.
,
Velasquez Jimenez
,
L.
,
Travis
,
M.
,
Chapman
,
K. E.
,
McCloskey
,
K. P.
,
Lamont
,
T. A.
,
Illing
,
B.
,
McCormick
,
M. I.
, and
Simpson
,
S. D.
(2022
). “
Limiting motorboat noise on coral reefs boosts fish reproductive success
,” Nat. Commun.
13
, 2822
.31.
Peng
,
C.
,
Zhao
,
X.
,
Liu
,
S.
,
Shi
,
W.
,
Han
,
Y.
,
Guo
,
C.
,
Jiang
,
J.
,
Wan
,
H.
,
Shen
,
T.
, and
Liu
,
G.
(2016
). “
Effects of anthropogenic sound on digging behavior, metabolism, Ca2+/Mg2+ ATPase activity, and metabolism-related gene expression of the bivalve Sinonovacula constricta
,” Sci. Rep.
6
, 24266
.32.
Popper
,
A. N.
, and
Hawkins
,
A. D.
(2018
). “
The importance of particle motion to fishes and invertebrates
,” J. Acoust. Soc. Am.
143
, 470
–488
.33.
Putland
,
R. L.
,
Constantine
,
R.
, and
Radford
,
C. A.
(2017
). “
Exploring spatial and temporal trends in the soundscape of an ecologically significant embayment
,” Sci. Rep.
7
, 5713
.34.
Roberts
,
L.
,
Cheesman
,
S.
,
Breithaupt
,
T.
, and
Elliott
,
M.
(2015
). “
Sensitivity of the mussel Mytilus edulis to substrate-borne vibration in relation to anthropogenically generated noise
,” Mar. Ecol. Prog. Ser.
538
, 185
–195
.35.
Roberts
,
L.
, and
Elliott
,
M.
(2017
). “
Good or bad vibrations? Impacts of anthropogenic vibration on the marine epibenthos
,” Sci. Total Environ.
595
, 255
–268
.36.
Robson
,
A. A.
,
Chauvaud
,
L.
,
Wilson
,
R. P.
, and
Halsey
,
L. G.
(2012
). “
Small actions, big costs: The behavioural energetics of a commercially important invertebrate
,” J. R. Soc. Interface
9
, 1486
–1498
.37.
Rogers
,
P. H.
,
Hawkins
,
A. D.
,
Popper
,
A. N.
,
Fay
,
R. R.
, and
Gray
,
M. D.
(2016
). “
Parvulescu revisited: Small tank acoustics for bioacousticians
,” in The Effects of Noise on Aquatic Life II
, edited by
A. N.
Popper
and
A. D.
Hawkins
(
Springer
,
New York
), pp. 933
–941
.38.
Souter
,
D. W.
, and
Lindén
,
O.
(2000
). “
The health and future of coral reef systems
,” Ocean Coast. Manag.
43
, 657
–688
.39.
Viana
,
M. G.
, and
Rocha-Barreira
,
C. D. A.
(2007
). “
The sensorial structures of Spondylus americanus Hermann, 1781 (Mollusca: Bivalvia, Spondylidae)
,” Braz. Arch. Biol. Technol.
50
, 815
–819
.40.
Wale
,
M. A.
,
Briers
,
R. A.
,
Hartl
,
M. G.
,
Bryson
,
D.
, and
Diele
,
K.
(2019
). “
From DNA to ecological performance: Effects of anthropogenic noise on a reef-building mussel
,” Sci. Total Environ.
689
, 126
–132
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