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Acoustic noise has the potential to cause stress, to distract and to mask important sounds, and thus to affect behaviour. Human activities have added considerable noise to both terrestrial and aquatic habitats, and there is growing evidence that anthropogenic noise affects communication and movement patterns in a variety of species. However, there has been relatively little work considering the effect on behaviours that are fundamental to survival, and thus have direct fitness consequences. We conducted a series of controlled tank-based experiments to consider how playback of ship noise, the most common source of underwater noise, affects foraging and antipredator behaviour in the shore crab, Carcinus maenas. Ship noise playback was more likely than ambient-noise playback to disrupt feeding, although crabs experiencing the two sound treatments did not differ in their likelihood of, or speed at, finding a food source in the first place. While crabs exposed to ship noise playback were just as likely as ambient-noise controls to detect and respond to a simulated predatory attack, they were slower to retreat to shelter. Ship noise playback also resulted in crabs that had been turned on their backs righting themselves faster than those experiencing ambient-noise playback; remaining immobile may reduce the likelihood of further predatory attention. Our findings therefore suggest that anthropogenic noise has the potential to increase the risks of starvation and predation, and showcases that the behaviour of invertebrates, and not just vertebrates, is susceptible to the impact of this pervasive global pollutant.
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Noise negatively affects foraging and antipredator behaviour in shore
crabs
Matthew A. Wale
a
, Stephen D. Simpson
b
, Andrew N. Radford
a
,
*
a
School of Biological Sciences, University of Bristol, Bristol, U.K.
b
Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, U.K.
article info
Article history:
Received 25 January 2013
Initial acceptance 6 March 2013
Final acceptance 8 April 2013
Available online 10 June 2013
MS. number: 13-00078R
Keywords:
anthropogenic noise
Carcinus maenas
distraction
environmental change
invertebrate behaviour
pollution
predation risk
shore crab
starvation risk
stress
Acoustic noise has the potential to cause stress, to distract and to mask important sounds, and thus to
affect behaviour. Human activities have added considerable noise to both terrestrial and aquatic habitats,
and there is growing evidence that anthropogenic noise affects communication and movement patterns
in a variety of species. However, there has been relatively little work considering the effect on behaviours
that are fundamental to survival, and thus have direct tness consequences. We conducted a series of
controlled tank-based experiments to consider how playback of ship noise, the most common source of
underwater noise, affects foraging and antipredator behaviour in the shore crab, Carcinus maenas. Ship
noise playback was more likely than ambient-noise playback to disrupt feeding, although crabs expe-
riencing the two sound treatments did not differ in their likelihood of, or speed at, nding a food source
in the rst place. While crabs exposed to ship noise playback were just as likely as ambient-noise
controls to detect and respond to a simulated predatory attack, they were slower to retreat to shelter.
Ship noise playback also resulted in crabs that had been turned on their backs righting themselves faster
than those experiencing ambient-noise playback; remaining immobile may reduce the likelihood of
further predatory attention. Our ndings therefore suggest that anthropogenic noise has the potential to
increase the risks of starvation and predation, and showcases that the behaviour of invertebrates, and not
just vertebrates, is susceptible to the impact of this pervasive global pollutant.
Ó2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
To survive and reproduce successfully, animals must minimize
the risks of starvation and predation. Events that compromise
either the foraging or antipredator behaviour of an individual are
therefore likely to have detrimental consequences for its tness.
Stressful events, for example, can lead to changes in the intensity,
duration or frequency of particular activities as part of an allostatic
response (Broom & Johnson 1993;McEwen & Wingeld 2003;
Wingeld 2005). If this response includes a reduction or cessation
of normal locomotor activity (see Metcalfe et al. 1987), then the
likelihood of successful escape from a predator may be reduced
and, if less time is spent foraging, food intake may decline. Food
acquisition may also be negatively affected if stress results in un-
necessary and costly antipredator responses (Lima & Dill 1990).
Moreover, stress might cause a reduction in appetite, mediated by
peptides associated with the corticotrophin-releasing factor system
(Bernier 2006); animals might be less inclined to search for food
when stressed.
Since foraging and antipredator behaviour involve various
cognitive processes, including detection, classication and decision
making (Shettleworth 2010), events that impair attention could
also pose a problem. Effects on attention might arise as part of a
stress-related allostatic response (as above), but attention might
also be compromised if an animal is distracted (Dukas 2004;Chan &
Blumstein 2011). If attention is narrowed, with animals either
ignoring stimuli or focusing on a smaller spatial scale (Dukas 2002),
then food or predators may be less likely to be detected (Hockey
1970). Distracted animals may also be more likely to respond
inappropriately to an imminent threat and run the risk of losing
current food items, either because they escape or because they are
stolen by others (Dukas 2002). These attention-mediated effects
are driven by a limited capacity to attend simultaneously to mul-
tiple stimuli (Dukas 2004;Chan & Blumstein 2011).
Many animals are alerted to the presence of predators or prey by
auditory cues, such as acts of intraspecic communication or the
sounds inadvertently produced as a consequence of movement
(Barrera et al. 2011;Siemers & Schaub 2011). Moreover, alarm calls
have evolved in a wide range of mammals and birds to warn others
of impending danger (Hollén & Radford 2009), while other vocal-
izations can provide information on the current level of risk (Hollén
*Correspondence: A. N. Radford, School of Biological Sciences, University of
Bristol, Woodland Road, Bristol BS8 1UG, U.K.
E-mail address: andy.radford@bristol.ac.uk (A. N. Radford).
Contents lists available at SciVerse ScienceDirect
Animal Behaviour
journal homepage: www.elsevier.com/locate/anbehav
0003-3472/$38.00 Ó2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.anbehav.2013.05.001
Animal Behaviour 86 (2013) 111e118
et al. 2008;Bell et al. 2009). Thus, predation and starvation may be
more likely if such acoustic information is masked, that is, if the
threshold for detection or discrimination of one sound is increased
in the presence of another (Brumm & Slabbekoorn 2005). Masking
can be complete (energeticmasking), whereby the signal is not
detected at all, or partial (informationalmasking), whereby the
signal is detectable by the listener, but the content is hard to un-
derstand. Either way, there are likely to be tness consequences for
foragers and potential prey from a reduced ability to detect valu-
able auditory information (Brumm & Slabbekoorn 2005;Siemers &
Schaub 2011;Lowry et al. 2012).
Acoustic noise, especially if it is loud, persistent, unexpected or
novel, has the potential to cause stress (Wysocki et al. 2006;Wright
et al. 2007), to distract (Hockey 1970;Chan et al. 2010a) and to
mask important sounds (Brumm & Slabbekoorn 2005;Siemers &
Schaub 2011;Lowry et al. 2012). In recent decades, human activ-
ities such as urban development, expansion of transport networks
and resource extraction have added considerable noise to both
terrestrial and aquatic environments across the globe, and led to
major changes in the acoustic landscape (see McDonald et al. 2006;
Watts et al. 2007;Barber et al. 2009). Consequently, anthropogenic
noise is now recognized as a major pollutant of the 21st century,
appearing in national and international legislation (e.g. US National
Environment Policy Act and European Commission Marine Strategy
Framework Directive). A burgeoning research effort using both
natural sound sources and playback experiments has indicated that
anthropogenic noise can affect the behaviour of species in a variety
of taxonomic groups (reviewed by Tyack 2008;Barber et al. 2009;
Slabbekoorn et al. 2010). However, most of that behavioural work
has focused on vocal communication or movement patterns (see,
e.g. Radford et al. 2012); far less research attention has been paid to
foraging and antipredator behaviour, which are of fundamental
importance to survival (see Chan et al. 2010a,b;Purser & Radford
2011;Siemers & Schaub 2011;Bracciali et al. 2012 for exceptions).
In this study, we used a series of controlled tank-based experi-
ments to explore how additional noise affected foraging and anti-
predator behaviour of a common marine crustacean, the shore crab,
Carcinus maenas. As our experimental sound to be added, we used
playback of ship noise. While underwater anthropogenic noise ari-
ses from many sources, including seismic surveys, mining activity,
sonar, wind farms and acoustic deterrent devices (Tasker et al. 2010),
ship noise is the most common (Vasconcelos et al. 2007) and has
alone led to a 10e100-fold increase in low-frequency (20e200 Hz)
ambient aquatic noise over the past century (Tyack 2008). To date,
the vast majority of studies investigating potential impacts of un-
derwater anthropogenic noise have been conducted on vertebrates
(Nowacek et al. 2007;Popper & Hastings 2009;Slabbekoorn et al.
2010). However, crustaceans and other marine invertebrates are
capable of hearing (Salmon 1971;Goodall et al. 1990) and use sound
for a variety of reasons (e.g. Jeffs et al. 2003;Stanley et al. 2010;
Simpson et al. 2011); thus they are likely to be vulnerable to the
impact of anthropogenic noise (see Wale et al. 2013).
In two separate foraging experiments, we examined the likeli-
hood and speed with which individuals located a food source and
whether their feeding behaviour was disrupted. We predicted that
ship noise playback would reduce the likelihood of crabs nding a
food item or would result in their taking longer to do so, and that it
might lead to an interruption in feeding behaviour. In an additional
two experiments, we probed antipredator behaviour. We simulated
a predatory attack, and predicted that ship noise playback might
make individuals less likely to detect the attack, respond differently
or take longer to retreat to shelter. We also investigated the
response of crabs to being unrighted (turned on their backs);
immobility is a well-documented antipredator behaviour (OBrien
& Dunlap 1975), potentially reducing the likelihood of further
predatory attention, and thus the most appropriate response might
be to remain in that position. If ship noise playback impairs deci-
sion making, we predicted that crabs would right themselves faster
than during playback of ambient noise.
METHODS
Ethical Note
All experiments in this study were approved by the University of
Bristol Animal Services Ethical Committee (University Investigation
Number: UB/10/034). The research adhered to the legal re-
quirements of the country (U.K.) in which the work was carried out,
and all institutional guidelines. Crabs showed no signs of adverse
reactions to the test set-ups; all tested individuals appeared to
return to normal pretrial behaviour when inspected and fed at the
end of each test day. At the end of the experiments, animals were
either kept for further study or given to the Bristol Aquarium.
Study Animals and Husbandry
All crabs were collected from Newquay harbour, U.K. (50
25
0
N
5
5
0
W), using a seine net, on 9 and 10 February 2012 (rst cohort)
and on 2 and 3 May 2012 (second cohort). Inside Newquay harbour
itself, there is sporadic trafc noise from pleasure craft, shing and
angling boat trips, and speed boats; noise from larger ships further
aeld is also likely, although those vessels do not enter the harbour
itself. Crabs were held for a maximum of 48 h in salt-water tanks at
the Blue Reef Aquarium, Newquay before transfer to Bristol
Aquarium by courier. During the transfer (265 km; 3.5 h), crabs
were out of water, but covered in damp cloths and newspaper, and
were maintained at their usual 12e14
C by the use of surrounding
ice packs; this method was adapted from Ingle (1999). Holding
tanks (48 32 cm and 28 cm high) in Bristol were made of poly-
styrene, to reduce noise transmission, and received water from one
of the Aquarium display tanks, which were plumbed into advanced
ltration facilities. Holding tanks were tted with a subsurface
inow pipe to prevent noise from water falling or collision with the
tank oor; the ow was adjusted to allow complete tank ush-
through every 30 min and thus ensure the maintenance of high
water quality. Sound levels in holding tanks were kept as low as
possible and were comparable to those for ambient-noise playback
during experiments (holding tank: 116 dB RMS re 1
m
Pa peaking at
1 kHz; ambient noise recording during playback: 111 dB RMS re
1
m
Pa peaking at 1.8 kHz; Fig. 1a).
Holding tanks contained sand on the oor and two shelters
made with inverted plastic ower pots weighted down with a layer
of pea gravel secured around the base with Milliput epoxy putty
(The Milliput Company, Gwynedd, U.K.). Holding tank lids included
a mesh window to allow light to reach the animals; this light did
not, however, cover all areas of the tank or reach into shelters and
thus animals had a choice of light/dark conditions. Water temper-
ature was kept at 12e14
C, salinity at 32e35 ppt and water qual-
ities within safe parameters (NO
2
:<0.3 mg/litre; NO
3
: 0 mg/
litre; NH
3þ
:0.25 mg/litre; pH: 7.4e7.9). Crabs were fed every 48 h
(except when part of foraging experiments; see below) on a variety
of previously frozen meats (cockle, mussel, shrimp, krill, sand eel,
mackerel) or dry composite marine pellets (New Era Aquaculture
Ltd., Thorne, U.K.), with any excess cleared from the holding tank
during tank maintenance no more than 8 h after feeding. Although
there was a constant water change within the holding tank (see
above), 25% of water was removed by siphon with excess food and
waste; this water was replaced by normal tank ow-through.
Water changes and the ow-through system ensured
M. A. Wale et al. / Animal Behaviour 86 (2013) 111e118112
maintenance of constant oxygen levels and the removal of any
water that had become trappedin the tank corners.
Noise Treatments
The sounds used as playbacks were from three major U.K. ports
(Gravesend, Plymouth, Portsmouth). In each location, recordings
were made of both ambient noise and noise generated by a single
passing ship at ca. 200 m distance (Gravesend: Rio de la Plata,
a 286 m long, 64 730 tonne container ship; Plymouth: Bro
Distributor, a 14 m long, 14 500 tonne LPG tanker; Portsmouth:
Commodore Goodwill, a 126 m long, 5215 tonne ferry). Ships were
travelling at constant, relatively slow speeds (<10 knots), as
enforced by port authorities for vessels entering and leaving
estuarine areas. All recordings were made with a calibrated
omnidirectional hydrophone (HiTech HTI-96-MIN with inbuilt
preamplier, High Tech Inc., Gulfport, MS, U.S.A.) and an Edirol R09-
HR 24-Bit recorder (44.1 kHz sampling rate, Roland Systems Group,
Bellingham, WA, U.S.A.). The recording level was calibrated for the
R09-HR using pure sine wave signals, measured in line with an
oscilloscope, produced by a function generator. Intensity (root
mean square, RMS) and power spectral density (units normalized
to 1 Hz, Hann evaluation, 50% overlap, FFT size 1024; averaged from
2 min of recording) were calculated for each recording in Avisoft
SASLab Pro v4.5.2 (Avisoft Bioacoustics, Berlin, Germany). This
analysis found some variation in average noise levels between re-
cordings: ambient tracks between 92 and 106 dB RMS re 1
m
Pa, and
ship noise tracks between 126 and 136 dB RMS re 1
m
Pa.
Sound samples of 60e140 s, incorporating the highest ampli-
tude of the ship passes (in which amplitude did not vary by more
than one quarter in magnitude) and the most stable levels of
ambient noise (where there were no events such as boats passing
or sounds of objects striking each other under the water) were used
to create experimental tracks in Audacity 1.3.13 (http://audacity.
sourceforge.net/). Each track included a 30 s fade in, 6.5 min of
ambient or ship noise and a 30 s fade out; one sample of ambient or
ship noise was looped to create a given playback track. Experi-
mental tracks were played back as WAV les using a similar set-up
to Purser & Radford (2011) and Wale et al. (2013): WAV/MP3
Player (Ultradisk DVR2 560 h; frequency range 20e20 000 Hz);
amplier (Kemo Electronic GmbH; 18 W; frequency response: 40e
20 000 Hz); potentiometer (set to minimum resistance; Omeg Ltd;
10 K logarithmic); and Aqua 30 underwater speaker (DNH; effective
frequency range 80e20 000 Hz). To give consistency between the
three exemplars in each treatment, tracks were re-recorded (using
the same hydrophone set-up as above) in the centre of the
experimental tank and modied (uniform amplication or atten-
uation); received sound levels for that tank position were therefore
103 e108 dB RMS re 1
m
Pa for ambient noise (chosen to be higher
than the noise oor in the experimental tank at low frequencies)
and 148e155 dB RMS re 1
m
Pa for ship noise (Fig. 1b, c). Exact sound
levels will differ throughout the tank, but our aim in this study was
to consider the potential behavioural impact of additional noise in
the environment, not establish the precise links between given
sound levels and responses.
The noise playbacks presented a range of frequencies that are
likely to fall within the hearing range of shore crabs, inferred from
studies on ddler crabs, Uca rapax and U. pugilator (Salmon 1971),
but the ship noise playbacks peaked at lower frequencies than the
ambient-noise playbacks. It is likely that crabs are primarily sen-
sitive to particle motion (Salmon 1971;Goodall et al. 1990), but, for
technical reasons, sound levels are given throughout in terms of
sound pressure; we do not attempt to establish absolute values for
sensitivity, but rather provide an indication of the behaviours that
can potentially be affected by the addition of noise to the
environment.
General Experimental Design
We chose to conduct our experiments in tanks to control care-
fully the conditions and contexts of the study animals, and to allow
detailed data collection. Care must of course be taken when
extrapolating results from tank-based experiments to meaningful
implications for free-ranging animals in open water. From a bio-
logical perspective, captive animals are usually more constrained
than in the wild, although in some of our experiments the
60
70
80
90
100
110
120
130
140
0 0.2 0.4 0.6 0.8 1.2 1.4 1.6 1.8 2 2.2 2.4 2.6 2.8 3
60
70
80
90
100
110
120
140
150
0 0.2 0.4 0.6 0.8 1 1.2 1.4 1.6 1.8 2 2.2 2.4 2.6 2.8
60
70
80
90
100
110
120
130
140
150
0 0.2 0.4 0.6 0.8 1.2 1.4 1.6 1.8 2 2.2 2.4 2.6 2.8 3
Holding-tank noise
Ambient-noise playback
Ship noise playback
Ambient-noise playback
Experimental-tank noise
Ship noise playback
Ambient-noise playback
Experimental-tank noise
130
(a)
(b)
(c)
3
1
1
Fre
q
uenc
y
(kHz)
150
Power spectral density (dB re 1µPa2 Hz-1)
Figure 1. Variation in sound proles for (a) holding tanks and ambient-noise play-
backs, (b) playbacks in the tank used for both foraging experiments and the simulated
predatory attack experiment, and (c) playbacks in the tank used for the unrighted crab
experiment. Shown are illustrative power spectrographic examples from recordings
made in the centre of the relevant tank.
M. A. Wale et al. / Animal Behaviour 86 (2013) 111e118 113
behavioural response measured was localized. Moreover, captive
individualsfeeding regimes may not be replicated naturally. From
an acoustics perspective, playbacks cannot perfectly replicate nat-
ural sound sources and the sound eld in a tank is complex
(Parvulescu 1964,1967;Okumura et al. 2002). However, our pri-
mary aim was to determine for the rst time whether addition of
noise can potentially affect various key life history variables in
marine invertebrates; future work can then establish the precise
effects in natural conditions.
Both foraging experiments and the simulated predatory attack
experiment were conducted in a tank (40 30 cm and 30 cm high)
with walls 4 mm thick; the experiment in which the crab was
unrighted took place in a tank (60 30 cm and 40 cm high) with
walls 6 mm thick. In the former, the playback speaker was placed
behind a vertical partition situated 10 cm from one short side; in
the latter, the speaker was beneath a platform (Fig. 2). Both
experimental tanks were placed on 5 cm thick foam pipe lagging, to
minimize sound transfer, and had the sides covered with opaque
black paint to half the height, to minimize distraction from visual
reections.
All crabs used in experiments weighed between 40 and 60 g,
and were randomly allocated to one of the two sound treatments
(ambient or ship noise). Experiments used an independent-
samples design to avoid any potential carryover effects. Separate
groups of crabs were used for each experiment, to remove any
compounding effects from repetitive handling stress and/or expo-
sure to sound (see Wale et al. 2013). Two cohorts of animals were
tested within each experiment, the rst occurring 1e3 months
before the second; experiments in each cohort were conducted at
the same time of day to remove any bias caused by the circadian
rhythm of the crabs (see Bojsen & Witthøfft 1998). Each animal was
randomly assigned one of the three playback tracks in each treat-
ment. Thirty-six animals were tested in each experiment in coun-
terbalanced blocks of six (ambient and ship noise from each of
three harbours).
Foraging Experiments
Prior to both foraging experiments, crabs were food deprived for
96 h. After placement in the holding area of the experimental tank
(Fig. 2a), crabs in both experiments were given 30 s to acclimatize.
The food source in both cases was a mussel, Mytilus edulis, which
had been drilled through and attached to a stainless steel washer
on the tank oor (as per Jensen et al. 2002). In the food search
experiment, the playback track was rst started and the divider
between the holding area and the experimental area then removed.
Each crab was given a maximum of 7.5 min (equivalent to a single
ship pass in the playback tracks) to nd the food source, after which
individuals were noted as having been successful or not. For those
that were successful, the time taken to locate the food source was
recorded.
In the feeding-disruption experiment, the divider was rst
removed and the crab allowed to nd the food source without any
playback of noise. Once the food was found and the animal had
begun eating, the playback track was started and any reaction
recorded in real time by the observer. Feeding was considered
disrupted if the animal ceased eating, indicated by a cessation in
maxilliped movement (normally ca. 5 beats/s; cessation scored if at
least 5 s with no beats), complete freezing of the animal or move-
ment away from the food. After 1 min of noise, a lack of any such
response was recorded as no apparent distraction.
Antipredator Experiments
The simulated predator attack experiment began when an ani-
mal was taken from the pre-experimental holding tank and placed
into the shelter provided in the experimental tank (Fig. 2b). The
shelter was identical to that in the holding tanks (see above).
The playback was started when the crab rst ventured out of the
shelter. After the 30 s fade in on the playback track, a wooden dowel
was plunged by hand into the water and straight out again (only the
dowel touched the water), directly in front of the crab; this was
used to simulate the action of a bird attempting to catch the crab.
The initial reaction of the crab to the predator stimulus was
recorded as either running (movement away from the stimulus) or
freezing (cessation of all movement). After the dowel was removed,
the time taken for the crab to return to the shelter was recorded.
Crabs were classied as returning to shelter either when they
entered it or stopped in the gap between it and the back of the
experimental tank.
To examine the righting behaviour of crabs when unrighted
(placed on their back), the playback track was started and after 15 s
an animal was placed inverted on the sand tray in the experimental
tank (Fig. 2c). The crab was then pinned in this position using a
3 cm diameter stainless steel washer, mounted on a brass rod at 20
(a)
(b)
(c)
Insulation
Speaker
Speaker holder
Direction of sound
Food source Divider
Speaker holder
Speaker
Insulation
Shelter
Direction of sound
Speaker
Insulation
Direction of sound
Experimental platform
Figure 2. Tank set-ups for (a) both foraging experiments, (b) the simulated predatory
attack experiment, and (c) the unrighted crab experiment.
M. A. Wale et al. / Animal Behaviour 86 (2013) 111e118114
with Milliput (see OBrien & Dunlap 1975). The crab was held in this
position for 15 s, since pinning for 30 s or longer can trigger an
immobility response (OBrien & Dunlap 1975). The restraint was
then removed and the time until the crab had completely turned
over and its second pereiopod touched the sand was recorded.
Data Analysis
Statistical analyses were conducted in R version 2.14.2 (The R
Foundation for Statistical Computing, Vienna, Austria, http://www.
r-project.org). Data tted the assumptions of normality and ho-
moscedasticity for parametric testing. In some cases, two-sample
ttests were adjusted accordingly for unequal variances, resulting
in altered degrees of freedom. Owing to external events or unusual
behaviour, data from six individuals across the four experiments
were not available for analysis; nal sample sizes were therefore 35
for the food search experiment, 36 for the feeding-disruption
experiment, 34 for the simulated predatory attack experiment,
and 33 for the experiment in which the crab was unrighted. We
conducted more than one test on each experimental data set.
However, since application of sequential Bonferroni corrections
(Rice 1989) does not qualitatively alter any of our ndings, and
since there is considerable debate about whether such corrections
should actually be made for multiple testing using the same data
set (see Nakagawa 2004), we present the uncorrected statistical
output in the Results.
RESULTS
Foraging Experiments
The two cohorts of crabs used for each of the foraging experi-
ments did not differ signicantly in their likelihood of nding the
food source (chi-square test:
c
2
1
¼0:01, P¼0.927), their search
times (two-sample ttest: t
33
¼0.21, P¼0.837) or their likelihood of
being disrupted from feeding (chi-square test:
c
2
1
¼0:11,
P¼0.739); cohorts were therefore combined for an assessment of
the effect of ship noise playback. The ability of crabs to nd the food
item was not impaired by the playback of ship noise compared to
ambient noise: crabs in the two sound treatments did not differ
signicantly in either their likelihood of locating the food in the
available time (chi-square test:
c
2
1
¼2:90, P¼0.089; Fig. 3a) or in
the time taken to nd the food source (two-sample ttest, only
individuals that found the food: t
25
¼0.75, P¼0.458; Fig. 3b).
Sound treatment did, however, have a signicant effect on the
behaviour of feeding crabs (chi-square test:
c
2
1
¼16:05, P<0.001).
Individuals exposed to ship noise playback were more likely to
suspend feeding than were those experiencing ambient-noise
playback (Fig. 3c).
Antipredator Experiments
All tested individuals in both sound treatments responded to the
simulated predatory attack by freezing or running; no individuals
failed to detect the attack. The two cohorts of crabs used did not
differ signicantly in the type of initial reaction (chi-square test:
c
2
1
¼2:03, P¼0.154) or in their time to nd shelter (two-sample
ttest: t
32
¼0.46, P¼0.650); samples were therefore combined for
an assessment of the effect of ship noise playback. There was no
signicant difference in the initial reaction to the predator stimulus
depending on whether ambient or ship noise was playing (chi-
square test:
c
2
1
¼0:15, P¼0.699; Fig. 4a). However, crabs exposed
to ship noise playback took signicantly longer to return to shelter
than those experiencing ambient-noise playback (two-sample
ttest: t
19
¼3.95, P¼0.001; Fig. 4b). This was true of both those
individuals that initially reacted by freezing (t
6
¼2.97, P¼0.030)
and those that ran in response to the simulated predatory attack
(t
15
¼4.12, P¼0.001).
In the experiment in which crabs were unrighted, there was no
signicant difference between the two cohorts in the time that
individuals took to right themselves (two-sample ttest: t
31
¼0.23,
P¼0.817); samples were therefore combined to assess the effect of
ship noise playback. Crabs experiencing ship noise playback turned
over signicantly faster than those played back ambient noise
(t
17
¼5.97, P<0.001; Fig. 4c).
DISCUSSION
Single exposure to the playback of noise from an individual ship
resulted in a variety of behavioural changes in shore crabs: their
feeding was disrupted, they were slower to return to shelter
following a simulated predatory attack, and they righted them-
selves faster when inverted. Previous work has shown that
anthropogenic noise, including that from ships, can affect the
behaviour of marine mammals (e.g. Parks et al. 2007;Castellote
et al. 2012). Of more direct relevance, given the shared ability to
detect particle motion, is the recent work demonstrating that such
0
2
4
6
8
10
12
14
20
Ship noise (N=18)
Found food
Did not find food
(a)
(b)
(c)
NS
0
50
100
150
200
250
Ship noise (N=16)
NS
0
2
4
6
8
10
12
14
16
18
20
22
Ship noise (N=18)
Number of individuals
Not distracted
Distracted
***
18
Number of individuals
Ambient noise (N=17)
Ambient noise (N=11)
Time (s)
Ambient noise (N=18)
Pla
y
back treatment
16
Figure 3. Results of the foraging experiments. (a) Number of crabs that did or did not
nd a food source, (b) mean SE time taken to nd the food source, and (c) number of
crabs that were or were not disrupted from their feeding during playback of ambient
or ship noise. Sample sizes are provided in parentheses. ***P<0.001.
M. A. Wale et al. / Animal Behaviour 86 (2013) 111e118 115
noise could also affect sh behaviour (e.g. Purser & Radford 2011;
Bracciali et al. 2012;Bruintjes & Radford 2013). However, our
ndings represent the rst indication that marine decapods can be
affected behaviourally by underwater anthropogenic noise (see
Wale et al. 2013 for a physiological response); studies have shown
this is also true of terrestrial decapods, with evidence for increased
distraction and decreased antipredator responses when exposed to
playback of anthropogenic noise (Chan et al. 2010a,b;Stahlman
et al. 2011). Future work needs to ascertain whether the demon-
strated responses occur in natural conditions, and the scale of likely
impact in response to real sources of anthropogenic noise.
Animals disturbed while foraging, especially if they move away
from the food source, run the risk of losing the item, either because
the prey escapes or because it is stolen; food acquisition is highly
competitive in decapod crustaceans (Smallegange et al. 2009). Lost
food would increase the amount of foraging time required to satisfy
energetic needs, at the cost to other essential behaviours
(Abrahams & Dill 1989) and potentially an increased predation risk;
animals often have to trade off vigilance with time spent foraging
(Lima & Dill 1990). Moreover, selection of more items to ensure the
same food intake increases the likelihood of foraging errors, such as
the consumption of toxic or harmful food, especially since perfor-
mance mistakes may be more likely in noisy conditions (see Purser
& Radford 2011). If individuals persistently or frequently had to
increase their foraging effort or compensation is not possible, then
there would be likely consequences for growth, reproductive suc-
cess and survival; individuals might also be at a competitive
disadvantage (Pintor & Sih 2008), although that depends on the
relative impact of noise on different species.
Noise also appears to have a negative impact on important
antipredator behaviours in the shore crab. Retreating into a shelter,
where the prey becomes inaccessible, is a well-known defence
mechanism (Guerra-Bobo & Brough 2010;Rossong et al. 2011), and
extra time spent in exposed conditions before reaching safety in-
creases the chances of predation. Of course, the vulnerability to
predation depends on how predators are affected by noise, since
not all species are affected similarly (see Francis et al. 2011). Crabs
placed on their backs and exposed to ship noise playback also
righted themselves faster than those experiencing ambient noise.
From a functional perspective, a faster righting could be perceived
as benecial, with the crabs able to escape predation quicker,
spending shorter periods of time on their back with their weak
undersides exposed. However, because remaining motionless may
reduce the likelihood of further predatory attack (OBrien & Dunlap
1975), ceasing this behaviour sooner could further increase the
predation likelihood, with ultimate consequence for survival.
It is possible thatanimals might habituateto continuous exposure
to the same noise, or become more tolerant of it (Smith et al. 2004;
Bejder et al. 2009). If so, the potential impacts discussed above would
be lessened over time. However, variable or unpredictable exposure
or the occurrence of novel noise might prevent this (for example,
various sh species produced increased cortisol in response to vari-
able boat noise but not to continuous Gaussian noise; Wysocki et al.
2006) and could even lead to a sensitized response to such distur-
bances. The processes of habituation and sensitization to noise
exposure are only just beginning to be explored (Masini et al. 2008;
Wale et al. 2013) and the implications are far from simple (Bejder
et al. 2009), so further research is certainly warranted.
Our study did not explicitly explore whether stress, distraction,
masking or a combination of these underpins the demonstrated
behavioural responses to noise playback. Masking is perhaps un-
likely as an explanation for our results, because there were no
obvious acoustic cues or signals available, certainly in the two
foraging experiments (which utilized pinned mussels) or the
experiment when the crab was unrighted. Previous work has sug-
gested that exposure to noise can reduce attention to a primary
task, such as foraging or the detection of predators (Chan et al.
2010a;Purser & Radford 2011), because attention capacity is
limited (Mendl 1999;Dukas 2002). However, crabs in our experi-
ments did not take longer to nd a food item and were no less likely
to respond to the simulated predator attack during ship noise
playback, which does not lend any support to the distraction hy-
pothesis (see Chan et al. 2010a;Chan & Blumstein 2011). It is
possible that our set-up was too simple to allow any such effects to
be determined: for instance, the limited connes of the tank may
have made nding the food item rather too easy. Future work needs
to test explicitly between potential underlying mechanisms for
noise-induced differences in behavioural responses (see Chan et al.
2010a;Siemers & Schaub 2011).
In general, studies of anthropogenic noise both on land and
underwater have tended to focus on vertebrates (Tyack 2008;
Barber et al. 2009;Slabbekoorn et al. 2010;Radford et al. 2012). The
0
2
4
6
8
12
Ship noise (N=16)
Number of individuals
Run
Freeze
(a) NS
0
20
40
60
80
100
120
Ship noise (N=16)
(b)
(c)
**
0
1
2
3
4
5
6
Ship noise (N=17)
Time (s)
***
10
Ambient noise (N=18)
Ambient noise (N=18)
Time (s)
Ambient noise (N=16)
Pla
y
back treatment
Figure 4. Results of the antipredator experiments. (a) Number of crabs that ran or
froze as an initial response to a simulated predatory attack, (b) mean SE time taken
to return to a shelter in the immediate aftermath of the simulated attack, and (c)
mean SE time taken to right themselves from an inverted position during playback
of ambient or ship noise. Sample sizes are provided in parentheses. **P<0.01;
***P<0.001.
M. A. Wale et al. / Animal Behaviour 86 (2013) 111e118116
paucity of attention on invertebrates is not commensurate with
their abundance and diversity (they make up 60% of marine species,
for example), their importance ecologically (as essential compo-
nents of food webs) and economically (especially in light of
changing sheries), or their value in terms of new natural products
(Cesar et al. 2003;Ausubel et al. 2010;Leal et al. 2012). Care is
clearly needed when interpreting our results from tank-based
playback experiments (chosen to ensure tight control of potential
confounding factors) in a real-world context. Tank playbacks
cannot replicate natural sound elds perfectly (Parvulescu 1964,
1967;Okumura et al. 2002) and crustaceans probably detect
sounds using particle motion (Goodall et al. 1990). However, given
the paucity of studies examining the impact of anthropogenic noise
on foraging and antipredator behaviour in any taxa, even pre-
liminary indications in this regard are potentially valuable. More-
over, our study highlights both that invertebrates are likely to be
susceptible to the impacts of anthropogenic noise and that they
provide a tractable option for detailed investigations into the im-
pacts of this pervasive global pollutant.
Acknowledgments
We are grateful to the Bristol Aquarium for housing the study
animals and to members of the Bioacoustics and Behavioural
Ecology Research Group at the University of Bristol for discussions
about the impacts of anthropogenic noise. We thank Irene Voellmy
and Sophie Holles for making the original sound recordings and
Nick Roberts, Vincent Janik, Dan Blumstein and two anonymous
referees for comments on the manuscript. Funding for this project
was provided by Defra.
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M. A. Wale et al. / Animal Behaviour 86 (2013) 111e118118
... Specifically, in crustaceans, anthropogenic noise directly affects different behavioral, physiological and biochemical parameters such as the predatory and foraging behavior (Yim-Hol Chan et al., 2010;Wale et al., 2013), immune response (Celi et al., 2015), locomotor activity, territorial behavior, and hemolynphatic parameters such as a higher glucose and total protein concentration (Celi et al., 2013;Filiciotto et al., 2014Filiciotto et al., , 2016. One of the most studied biochemical processes involving cellular stress is oxidative stress. ...
... For example, in squids and cuttlefish, it was demonstrated that they showed similar response behaviors after habituation to artificial sounds (Mooney et al., 2016;Samson et al., 2014). Similarly, in the crab Carcinus maenas it was showed that repetitive exposure to motorboat sound did not affect physiological parameters of this crab, probably, because of sound habituation (Wale et al., 2013). In the present study, the biochemical analysis of CAT activity was modified in the presence of boat stimuli compared to the control condition, thus, it is suggested that although potential habituation to sound in the behavioral response may occur, this anthropogenic stimuli equally promotes physiological stress in N. granulata. ...
... In the common prawn Palaemon serratus, fewer encounters among individuals and more time resting were found . In the crab Carcinus maenas, it was demonstrated that the boat sound affected the feeding behavior and the response to retreat into a shelter to a simulated predator (Wale et al., 2013). The hermit crab Coenobita clypeatus showed a slower response that allowed a simulated predator to approach closer before they hid (Yim-Hol Chan et al., 2010). ...
... These behaviors induce the transport and mixing of sediment in and around the burrow. Shore crabs (Carcinus maenas) were shown to suspend feeding when ship noise was played (Wale et al., 2013), which might explain why bioturbation rates were reduced if this response holds true in C. volutator. Although sound perception in amphipods is largely unknown, it is also possible that amphipods perceive LFN as vibrations via structures such as a lateral line organ or sensory setae (Beermann et al., 2015;Platvoet et al., 2007), which could be used to detect the presence of potential predators. ...
... This contrasts with the results produced by the setup of the current study if the particle burial depth does correlate with burrow depth. Shore crabs in the study by Wale et al. (2013) also took longer to flee from simulated predator attacks while exposed to ship noise. More recently, young-of-the-year lobsters exposed to 3 h of constant low-frequency noise using the same source were shown to spend less time hiding in the presence of predators (e.g. ...
... This scenario would be dire since amphipods such as C. volutator have been shown to only contribute meaningfully to sediment reworking when abundant (De Backer et al., 2011). However, the ship noise in the setup by Wale et al. (2013) was employed over minutes and not days like in the current study; habituation to LFN by animals may be possible (Carroll et al., 2017;Day et al., 2020) depending on intensity, duration, frequency, and many other factors. The mortality of C. volutator was not affected by LFN, therefore the reduction in bioturbation rates and mean luminophore burial depth cannot be attributed to a loss of experimental animals in the treatments (Table S2). ...
Article
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Sounds from human activities such as shipping and seismic surveys have been progressively invading natural soundscapes and pervading oceanic ambient sounds for decades. Benthic invertebrates are important ecosystem engineers that continually rework the sediment they live in. Here, we tested how low-frequency noise (LFN), a significant component of noise pollution, affects the sediment reworking activities of selected macrobenthic invertebrates. In a controlled laboratory setup, the effects of acute LFN exposure on the behavior of three abundant bioturbators on the North Atlantic coasts were explored for the first time by tracking their sediment reworking and bioirrigation activities in noisy and control environments via luminophore and sodium bromide (NaBr) tracers, respectively. The amphipod crustacean Corophium volutator was negatively affected by LFN, exhibiting lower bioturbation rates and shallower luminophore burial depths compared to controls. The effect of LFN on the polychaete Arenicola marina and the bivalve Limecola balthica remained inconclusive, although A. marina displayed greater variability in bioirrigation rates when exposed to LFN. Furthermore, a potential stress response was observed in L. balthica that could reduce bioturbation potential. Benthic macroinvertebrates may be in jeopardy along with the crucial ecosystem-maintaining services they provide. More research is urgently needed to understand, predict, and manage the impacts of anthropogenic noise pollution on marine fauna and their associated ecosystems.
... Experiments with anthropogenic noise and white noise (noise with equal energy across the spectrum) (Quinn et al. 2006, Ware et al. 2015, Evans et al. 2018, suggest that foraging and vigilance behaviors in noise match those seen in areas with increased predator presence or riskier aspects of cover (Lima 1987, Skinner and Hunter 1998, Caro 2005. Crabs are more likely to stop feeding when exposed to ship noise (Wale et al. 2013), while prairie dogs (Cynomys ludovicianus) increase vigilance and decrease foraging in traffic noise (Shannon et al. 2014). The same trade-off can be seen in chaffinches (Fringilla coelebs) and zebra finches (Taeniopygia guttata) when foraging in white noise (Quinn et al. 2006, Evans et al. 2018). ...
... Additionally, birds largely behaved the same regardless of the variation in spectral or temporal structure we presented, indicating that high sound pressure levels of any noise type could be detrimental in the context of the foraging-vigilance trade-off. Our findings of increased antipredator behavior in noisy anthropogenic environments matches results from similar studies across several listening taxa, including birds, mammals, and invertebrates (Krebs et al. 1997, Quinn et al. 2006, Wale et al. 2013, Klett-Mingo et al. 2016, Evans et al. 2018. Likewise, vigilance increases have been described in wild populations of black-headed grosbeaks (Pheucticus melanocephalus; Sweet et al. in progress) and California ground squirrels (Otospermophilus beecheyi; Le et al. 2019) in response to broadcast of whitewater river noise. ...
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Animals glean information about risk from their habitat. The acoustic environment is one such source of information, and is an important, yet understudied ecological axis. Although anthropogenic noise has become recently ubiquitous, risk mitigation behaviors have likely been shaped by natural noise over millennia. Listening animals have been shown to increase vigilance and decrease foraging in both natural and anthropogenic noise. However, direct comparisons could be informative to conservation and understanding evolutionary drivers of behavior in noise. Here, we used 27 song sparrows (Melospiza melodia) and 148 laboratory behavioral trials to assess foraging and vigilance behavior in both anthropogenic and natural noise sources. Using five acoustic environments (playbacks of roadway traffic, a whitewater river, a whitewater river shifted upwards in frequency, a river with the amplitude modulation of roadway traffic, and an ambient control), we attempt to parse out the acoustic characteristics that make a foraging habitat risky. We found that sparrows increased vigilance or decreased foraging in 4 of 6 behaviors when foraging in higher sound levels regardless of the noise source or variation in frequency and amplitude modulation. These responses may help explain previously reported declines in abundance of song sparrows exposed to playback of intense river noise. Our results imply that natural soundscapes have likely shaped behavior long before anthropogenic noise, and that high sound levels negatively affect the foraging-vigilance trade-off in most intense acoustic environments. Given the ever-increasing footprint of noise pollution, these results imply potential negative consequences for bird populations.
... However, the sound field can be difficult to control in a tank setup. Previous exposure experiments (Celi et al., 2013;Wale, Simpson & Radford, 2013a;Wale, Simpson & Radford, 2013b;Filiciotto et al., 2014;Celi et al., 2015;Walsh, Arnott & Kunc, 2017), while suitably replicating the animal's natural environment, may have inadvertently induced an uneven sound field. A sound source positioned at the side of a tank may produce unknown artifacts due to asymmetric reflection-based interference patterns. ...
... Work in other crustaceans, like the crayfish Procambarus clarkii, did show a difference in aggressive and active behaviors during acoustic stimulus (Celi et al., 2013). Furthermore, the observed reduction in feeding among exposed adult animals could theoretically produce a delayed physiological response similar to that detected in the 7-day mid-frequency exposure samples, as is suggested for crabs (Wale, Simpson & Radford, 2013b) and lobsters (Fitzgibbon et al., 2017). Activities which either damage hearing or mask important auditory cues could have detrimental impact on survival. ...
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Human usage of coastal water bodies continues to increase and many invertebrates face a broad suite of anthropogenic stressors ( e.g ., warming, pollution, acidification, fishing pressure). Underwater sound is a stressor that continues to increase in coastal areas, but the potential impact on invertebrates is not well understood. In addition to masking natural sound cues which may be important for behavioral interactions, there is a small but increasing body of scientific literature indicating sublethal physiological stress may occur in invertebrates exposed to high levels of underwater sound, particularly low frequency sounds such as vessel traffic, construction noise, and some types of sonar. Juvenile and sub-adult blue crabs ( Callinectes sapidus ) and American lobsters ( Homarus americanus ) were exposed to simulated low-frequency vessel noise (a signal was low-pass filtered below 1 kHz to ensure low-frequency content only) and mid-frequency sonar (a 1-s 1.67 kHz continuous wave pulse followed by a 2.5 to 4.0 kHz 1-s linear frequency modulated chirp) and behavioral response (the animal’s activity level) was quantified during and after exposure using EthoVision XT™ from overhead video recordings. Source noise was quantified by particle acceleration and pressure. Physiological response to the insults (stress and recovery) were also quantified by measuring changes in hemolymph heat shock protein (HSP27) and glucose over 7 days post-exposure. In general, physiological indicators returned to baseline levels within approximately 48 h, and no observable difference in mortality between treatment and control animals was detected. However, there was a consistent amplified hemolymph glucose signal present 7 days after exposure for those animals exposed to mid-frequency sound and there were changes to C. sapidus competitive behavior within 24 h of exposure to sound. These results stress the importance of considering the impacts of underwater sound among the suite of stressors facing marine and estuarine invertebrates, and in the discussion of management actions such as protected areas, impact assessments, and marine spatial planning efforts.
... Exposure to noise has resulted in a few reports of immediate (Lagardère, 1982;McCauley et al., 2017a;Fields et al., 2019) or delayed mortality. Behavioural impacts, such as disrupted feeding, slowed retreat from predators, more rapid righting (Wale et al., 2013a;Nousek-McGregor and Mei, 2016), faster and more frequent movement Zhou et al., 2018), breakdown of social grouping (Buscaino et al., 2011) and increased aggression (Celi et al., 2013) have been reported. A range of physiological impacts have been observed, including stress biochemistry and immune system disruptions (Celi et al., 2013;Celi et al., 2014;Filiciotto et al., 2014), decreases (Wale et al., 2019) or increases in metabolic rate (Wale et al., 2013b), damage to sensory systems (André et al., 2011;Solé et al., 2013a;Solé et al., 2013b;Day et al., 2019;Day et al., 2020) and DNA damage and associated biochemical changes (Wale et al., 2019). ...
Article
Anthropogenic aquatic noise is recognised as an environmental pollutant with the potential to negatively affect marine organisms. Seismic surveys, used to explore subseafloor oil reserves, are a common source of aquatic noise that have garnered attention due to their intense low frequency inputs and their frequent spatial overlap with coastal fisheries. Commercially important Southern Rock Lobster (Jasus edwardsii) adults have previously shown sensitivity to signals from a single seismic air gun. Here, the sensitivity of J. edwardsii juveniles and puerulus to the signals of a full-scale seismic survey were evaluated to determine if early developmental stages were affected similarly to adults, and the range of impact. To quantify impact, lobster mortality rates, dorsoventral righting reflex and progression through moult cycle were evaluated following exposure. Exposure did not result in mortality in either developmental stage, however, air gun signals caused righting impairment to at least 500 m in lobsters sampled immediately following exposure, as had previously been reported in adults with corresponding sensory system damage following exposure. Impairment resulting from close range (0 m) exposure appeared to be persistent, as previously reported in adults, whereas juveniles exposed at a more distant range (500 m) showed recovery, indicating that exposure at a range of 500 m may not cause lasting impairment to righting. Intermoult duration was (time between moults) significantly increased in juveniles exposed at 0 m from the source, indicating the potential for slowed development, growth, and physiological stress. These results demonstrate that exposure to seismic air gun signals have the potential to negatively impact early life history stages of Southern Rock Lobsters. The similarity of both the impacts and the sound exposure levels observed here compared to previous exposure using a single air gun offer validation for the approach, which opens the potential for accessible field-based experimental work into the impact of seismic surveys on marine invertebrates.
... In conclusion, our study shows the impact noise has on resource acquisition of A. octospinosus, which corresponds to noise reduced efficiency in other invertebrate taxa [35,37,47]. Masking of communication during noise treatments may have impacted resource acquisition. ...
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We investigate the impact of anthropogenic noise on the foraging efficiency of leafcutter ants (Acromyrmex octospinosus) in a controlled laboratory experiment. Anthropogenic noise is a widespread, pervasive and increasing environmental pollutant and its negative impacts on animal fitness and behaviour have been well documented. Much of this evidence has come from studies concerning vertebrate species with very little evidence for terrestrial invertebrates, especially social living invertebrates. We compare movement speed, forage fragment size, and colony activity levels of ants exposed to intermittent elevated noise and in ambient noise conditions. We use intermittent and temporally unpredictable bursts of white noise produced from a vibration speaker to create the elevated noise profile. Ant movement speed increased under elevated noise conditions when travelling to collect forage material and when returning to the colony nest. The size of individually measured foraged material was significantly reduced under elevated noise conditions. Colony activity, the number of ants moving along the forage route, was not affected by elevated noise and was consistent throughout the foraging events. Increased foraging speed and smaller forage fragments suggests that the ants had to make more foraging trips over an extended period, which is likely to affect energy expenditure and increases exposure to predators. This is likely to have significant fitness impacts for the colony over time.
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Small recreational boats are an omnipresent source of sound pollution in shallow coastal habitats, which can impact the behavior and physiology of a wide array of taxa. However, effective monitoring of this stressor is currently limited by a lack of tools. The present study coupled passive acoustic monitoring (PAM) with timelapse imagery to provide a comprehensive analysis of sound pollution at two coastal sites varying in habitat structure: Goat (rocky reef) and Kawau (sandy bay) Islands. A convolutional neural network (CNN) was used to automatically count boats in each image, and the relationship between the soundscape and number of boats present was analysed using power spectral density and adaptive threshold analyses. Small boat activity was positively correlated with third octave level (TOL) root mean squared sound pressure levels (SPLRMS 63 – 5011 Hz), and this effect was frequency dependent, at both Goat (F7,9704 = 5.665, p < 0.001) and Kawau (F7,42488 = 325.33, p < 0.001) Islands. However, at Goat Island this interaction effect was driven by a significant difference between 63 Hz and all other TOLs (p < 0.05), whereas at Kawau Island the interaction effect of TOL and boat number was more variable. Furthermore, low frequency (∼50 – 300 Hz) biophony was found to influence the likelihood of boat sound being detected at Goat Island. Small boat impacts are contextual, likely due to habitat specific propagation conditions and the presence/absence of vocalising animals. As such, monitoring of sound pollution in coastal habitats requires a tailored approach which accounts for the localised nature of shallow coastal soundscapes. These findings demonstrate the potential for timelapse imagery to elucidate variability in boat sound, which may be particularly useful for remote sites which are ecologically rich, yet have no acoustic protections, such as many marine protected areas.
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Coral reef soundscapes are increasingly studied for their ecological uses by invertebrates and fishes, for monitoring habitat quality, and to investigate effects of anthropogenic noise pollution. Few examinations of aquatic soundscapes have reported particle motion levels and variability, despite their relevance to invertebrates and fishes. In this study, ambient particle acceleration was quantified from orthogonal hydrophone arrays over several months at four coral reef sites, which varied in benthic habitat and fish communities. Time-averaged particle acceleration magnitudes were similar across axes, within 3 dB. Temporal trends of particle acceleration corresponded with those of sound pressure, and the strength of diel trends in both metrics significantly correlated with percent coral cover. Higher magnitude particle accelerations diverged further from pressure values, potentially representing sounds recorded in the near field. Particle acceleration levels were also reported for boat and example fish sounds. Comparisons with particle acceleration derived audiograms suggest the greatest capacity of invertebrates and fishes to detect soundscape components below 100 Hz, and poorer detectability of soundscapes by invertebrates compared to fishes. Based on these results, research foci are discussed for which reporting of particle motion is essential, versus those for which sound pressure may suffice.
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Soundscapes are characterized by a combination of natural and anthropogenic sounds. This study evaluated the stress effect of biological and anthropogenic sounds characterizing a Man and Biosphere UNESCO wetland, by assessing the protein content, oxidative biomarkers, and behavior of a key crab species (Neohelice granulata), through a tank-laboratory experiment. Biological sounds corresponded to predators of N. granulata (fish and crustacean stimuli), while anthropogenic ones belonged to motorboat passages (boat stimulus). Biochemical results showed differences depending on the sound stimuli used and the crab tissue analyzed. Protein content was higher in hemolymph when crabs were exposed to fish and boat stimuli, and in gills when exposed to boat stimulus. The enzymatic activity in hemolymph showed a decreased GST (fish stimulus) and CAT (fish and boat stimuli) activity, in hepatopancreas a higher GST (crustacean stimulus) and CAT (crustacean and boat stimuli) activity was found, and in gills a higher CAT activity was also observed (crustacean and boat stimuli). Lipid peroxidation was higher only in hemolymph (fish and crustacean stimuli). Protein oxidation was higher in gills (fish stimulus) and hepatopancreas (crustacean stimulus). Behavioral analysis demonstrated that the crab locomotion activity diminished when exposed to diverse sound stimuli. Thus, both sound sources caused physiological and behavioral stress in this species. The results contribute important data to be used in the development of management plans considering the habitat importance in terms of biodiversity, the ecosystem services provided and the role of the studied species.
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Mechanical noise plays a key role in ship acoustic performance design as an important component of underwater sound radiation. In this paper, a numerical method for predicting ship mechanical noise, energy-averaged method, is proposed considering coupling mechanism, numerical model and kinematic excitation in full frequencies. In the method, vibroacoustic BEM coupling equations are established by the equivalent generalized force converted from kinematic loads based on the energy-averaged method in low-mid frequencies, and the vibroacoustic transfer functions obtained by SEA are modified in high frequencies, which can reduce computational errors resulting from an offset of natural frequency between a numerical model and a real structure, kinematic loads with incomplete information, and pathological matrices. The accuracy and reliability of the energy-averaged method are verified by the hydroacoustic experiments. The simulated and experimental results are comprehensively evaluated by overall errors, correlation coefficients, and standard deviations. The errors between the simulation and the experiment are 0.75 dB, 0.51 dB, and 1.21 dB in different frequency regions for the shaker case, respectively, while those are 0.41 dB and 0.82 dB in the different diesel engine cases. Additionally, the phenomenon of acoustic cavity resonances cannot be neglected in low frequencies, and the acoustic cavity must be modelled to predict mechanical noise.
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The influence of predation risk on patch choice was measured by examining the spatial distribution of 10 guppies (Poecilia reticulata) between two feeders, at one of which there was a risk of predation. The distribution was assumed to be ideal free. Nine unique situations were examined using all possible combinations of three risk levels and three diet levels, for each sex of guppy separately. Both sex and diet level influenced the effect of predation risk on patch choice. For the females the effect of risk was highest at the intermediate diet level. However, the males exhibited the opposite response: the effect of risk of predation was lowest at the intermediate diet level. A simple equation was then used to predict how much extra food (representing the energetic equivalent of risk) must be added to the risky patch for the guppies to become indifferent to the risk differences between the two types of patches. This manipulation caused a similar number of guppies to use both the risky and safe feeders, reducing or offsetting the influence of risk of predation. However, the male guppies were less influenced by this manipulation than were the females. The different results for the two sexes are consistent with known differences in their life histories, indicating that a knowledge of an animal's life history will often be necessary to understand how it makes trade-offs when choosing were to forage.
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Several studies have suggested that underwater sound may provide an orientation cue for the pelagic stages of coastal crustacea, such as crabs and lobsters, to find their way from the open ocean to the coast where they can settle. Yet, there has been no field evidence to support this phenomenon and it is unclear whether pelagic crustacean stages even have the ability to orient towards sources of underwater sound, such as that which emanates from reefs. Artificial sources of natural underwater sound were deployed offshore in conjunction with light traps to determine if the larval and post-larval stages of coastal crabs were attracted to coastal reef sound. The results demonstrated that the pelagic stages of crabs respond to underwater sounds and that they may use underwater sound to orient towards the coast. The orientation behaviour was modulated by lunar phase, being evident only during first- and last-quarter moon phases, at the time of neap tides. Active orientation during neap tides may take advantage of these incoming night-time tides for predator avoidance or may permit more effective directed swimming activity than is possible during new and full moon spring tides.
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The behavioural responses of Nephrops noruegicus (L.) to acoustic stimuli have been investigated under laboratory and free field conditions. In the laboratory a distinct set of postural motor responses elicited, by sound frequencies of 20–180Hz, was identified. This set of responses was then exploited during free field experiments conducted in a Scottish sea loch to determine the acoustic response threshold. Nephrops were found to be displacement rather than pressure sensitive with a response threshold of 0.888μm which was independent of frequency within the range 20–200Hz.
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Non-lethal behavioural effects of underwater noise in marine mammals are difficult to measure. Here we report acoustic and behavioural changes by fin whales in response to two different types of anthropogenic noise: shipping and airgun noise. Acoustic features of fin whale 20-Hz song notes recorded in the Mediterranean Sea and Northeast Atlantic Ocean were compared for areas with different shipping noise levels, different traffic intensities in the Strait of Gibraltar and during a seismic airgun array survey. In high noise conditions 20-Hz note duration shortened, bandwidth decreased, centre frequency decreased and peak frequency decreased. Similar results were obtained in 20-Hz song notes recorded during a 10-day seismic survey. During the first 72 h of the survey, a steady decrease in song received levels and bearings to singers indicated that whales moved away from the airgun array source and out of our detection area, and this displacement persisted for a time period well beyond the 10-day duration of seismic airgun activity. This study provides evidence that male fin whales from two different subpopulations modify song characteristics under increased background noise conditions, and that under seismic airgun activity conditions they leave an area for an extended period. We hypothesize that fin whale acoustic communication is modified to compensate for increased background noise and that a sensitization process may play a role in the observed temporary displacement. The observed acoustic and behavioural changes of this endangered species are discussed in the context of reproduction success and population survival.