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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 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 expe-
riencing 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.
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 fitness.
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 & Wingfield 2003;
Wingfield 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, classification 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 intraspecific 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 (‘energetic’masking), whereby the signal is not
detected at all, or partial (‘informational’masking), whereby the
signal is detectable by the listener, but the content is hard to un-
derstand. Either way, there are likely to be fitness 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 finding 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 (O’Brien
& 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 (first cohort)
and on 2 and 3 May 2012 (second cohort). Inside Newquay harbour
itself, there is sporadic traffic noise from pleasure craft, fishing and
angling boat trips, and speed boats; noise from larger ships further
afield 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
filtration facilities. Holding tanks were fitted with a subsurface
inflow pipe to prevent noise from water falling or collision with the
tank floor; the flow was adjusted to allow complete tank flush-
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 floor and two shelters
made with inverted plastic flower 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 flow-through.
Water changes and the flow-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 ‘trapped’in 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
preamplifier, 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 files 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);
amplifier (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 modified (uniform amplification 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 floor 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 fiddler 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 profiles 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
individuals’feeding regimes may not be replicated naturally. From
an acoustics perspective, playbacks cannot perfectly replicate nat-
ural sound sources and the sound field in a tank is complex
(Parvulescu 1964,1967;Okumura et al. 2002). However, our pri-
mary aim was to determine for the first 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
reflections.
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 first 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 floor (as per Jensen et al. 2002). In the food search
experiment, the playback track was first 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 find 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 first
removed and the crab allowed to find 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 first 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 classified 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 O’Brien & Dunlap 1975). The crab was held in this
position for 15 s, since pinning for 30 s or longer can trigger an
immobility response (O’Brien & 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 fitted 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; final 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 findings, 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 significantly in their likelihood of finding 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 find 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
significantly 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 find 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 significant 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 significantly in the type of initial reaction (chi-square test:
c
2
1
¼2:03, P¼0.154) or in their time to find 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
significant 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 significantly 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
significant 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 significantly 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
find a food source, (b) mean SE time taken to find 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 fish behaviour (e.g. Purser & Radford 2011;
Bracciali et al. 2012;Bruintjes & Radford 2013). However, our
findings represent the first 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 beneficial, 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 (O’Brien & 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 fish 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 find 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 confines of the tank may
have made finding 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 fisheries), 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 fields 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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