Anthropogenic Noise Affects Behavior across Sensory Modalities
Kunc, H. P., Lyons, G. N., Sigwart, J. D., McLaughlin, K. E., & Houghton, J. D. R. (2014). Anthropogenic Noise
Affects Behavior across Sensory Modalities.
American Naturalist
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184
(4), E93-100.
https://doi.org/10.1086/677545
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Anthropogenic Noise Affects Behavior across Sensory Modalities.
Author(s): Hansjoerg P. Kunc, Gillian N. Lyons, Julia D. Sigwart, Kirsty E. McLaughlin, and
Jonathan D. R. Houghton
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The American Naturalist,
Vol. 184, No. 4 (October 2014), pp. E93-E100
Published by: The University of Chicago Press for The American Society of Naturalists
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vol. 184, no. 4 the american naturalist october 2014
E-Article
Anthropogenic Noise Affects Behavior across
Sensory Modalities
Hansjoerg P. Kunc,* Gillian N. Lyons, Julia D. Sigwart, Kirsty E. McLaughlin, and
Jonathan D. R. Houghton
Institute for Global Food Security, Queen’s University Belfast, School of Biological Sciences, Medical Biology Centre, 97 Lisburn Road,
Belfast BT9 7BL, United Kingdom; and Queen’s University Marine Laboratory, 12-13 The Strand, Portaferry, County Down BT22 1PF,
United Kingdom
Submitted July 5, 2013; Accepted March 19, 2014; Electronically published July 30, 2014
Dryad data: http://dx.doi.org/10.5061/dryad.c6011.
abstract: Many species are currently experiencing anthropogen-
ically driven environmental changes. Among these changes, increas-
ing noise levels are specifically a problem for species using acoustic
signals (i.e., species relying on signals that use the same sensory
modality as anthropogenic noise). Yet many species use other sensory
modalities, such as visual and olfactory signals, to communicate.
However, we have only little understanding of whether changes in
the acoustic environment affect species that use sensory modalities
other than acoustic signals. We studied the impact of anthropogenic
noise on the common cuttlefish Sepia officinalis, which uses highly
complex visual signals. We showed that cuttlefish adjusted their visual
displays by changing their color more frequently during a playback
of anthropogenic noise, compared with before and after the playback.
Our results provide experimental evidence that anthropogenic noise
has a marked effect on the behavior of species that are not reliant
on acoustic communication. Thus, interference in one sensory chan-
nel, in this case the acoustic one, affects signaling in other sensory
channels. By considering sensory channels in isolation, we risk over-
looking the broader implications of environmental changes for the
behavior of animals.
Keywords: animal communication, noise pollution, environmental
change, phenotypic plasticity, Sepia officinalis.
Introduction
Animal communication plays a crucial role for many spe-
cies, because it is used in different contexts (e.g., sexual
selection, parental care, and predator-prey interactions;
Bradbury and Vehrencamp 2011). Communication in its
simplest form involves a sender producing a signal that
conveys information and a receiver making a decision on
how to respond to that signal (Bradbury and Vehrencamp
* Corresponding author; e-mail: kunc@gmx.at.
Am. Nat. 2014. Vol. 184, pp. E93–E100. 䉷 2014 by The University of Chicago.
0003-0147/2014/18404-54793$15.00. All rights reserved.
DOI: 10.1086/677545
2011). Thus, for an individual, it is vital that the signal is
transmitted effectively across the environment to the
receiver. To maintain signal efficiency, species use a variety
of different sensory modalities to communicate, depending
on the environment they inhabit. However, many species
are currently experiencing anthropogenically driven
environmental changes, including noise altering acoustic
environments in both aquatic and terrestrial ecosystems
(Malakoff 2010; Slabbekoorn et al. 2010).
Changes in the acoustic environment are a specific prob-
lem faced by species that use acoustic signals (i.e., those
that rely on signals that use the same sensory modality as
anthropogenic noise). For example, anura and birds adjust
their acoustic signals when experimentally exposed to
increased noise levels (e.g., Halfwerk and Slabbekoorn
2009; Cunnington and Fahrig 2010; Gross et al. 2010; Ver-
zijden et al. 2010). In these cases, animals modify their
acoustic signals in response to changes in the acoustic
environment within one sensory modality. Yet many spe-
cies use other sensory modalities, such as visual and ol-
factory signals, to communicate (Bradbury and Vehren-
camp 2011). However, whether changes in the acoustic
environment affect species that use sensory modalities
other than acoustic signals is still unknown.
Cephalopods use complex visual signals, including the
alteration of body coloration and patterning (Tinbergen
1939; Hanlon and Messenger 1988, 1996). Additionally,
they use a mechanosensory receptor system of epidermal
head and arm lines, which allows them to detect local water
movements, including those caused by sound waves trans-
mitted underwater (Sundermann 1983; Budelmann and
Bleckmann 1988). The perception of local water move-
ments can be enhanced by raising their first pair of arms,
and there is no evidence that cephalopods communicate
by sound (Budelmann et al. 1991; Hanlon and Messenger
1996; Vermeij 2010). If species that do not rely on acoustic
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E94 The American Naturalist
communication respond to anthropogenic changes in their
acoustic environment, noise pollution could have far-
reaching consequences by affecting not only species that
use acoustic signals but also those that communicate by
other means.
To test whether anthropogenic noise affects animals that
do not rely on acoustic communication, we exposed com-
mon cuttlefish (Sepia officinalis) to an experimental noise-
polluted environment. We examined whether cuttlefish
changed their visual and tactile behavior in response to
changes in their acoustic environment by exposing them
to anthropogenic noise. To exclude the possibility that the
presence of the loudspeaker alone or any other acoustic
stimuli elicits the same behavioral response, we exposed
the same individuals to a control playback consisting of
waves breaking in the surf zone. We predicted that indi-
viduals exposed to anthropogenic noise should adjust their
behavior to changes in their acoustic environment. Fur-
thermore, if individuals responded more strongly to an-
thropogenic noise than to the control playback, we could
conclude that anthropogenic noise, and not merely any
change in the acoustic environment, affects behavior.
Material and Methods
Study Species and Housing
Sepia officinalis eggs were collected from lobster pot lines
off Weymouth, England; transported to aquarium facilities
in Portaferry, Northern Ireland; and reared under standard
laboratory conditions for 4–6 weeks after hatching (e.g.,
Forsythe et al. 1991, 1994). Animals were fed live mysid
shrimps ad lib., with food supplies checked and topped
up twice daily. Cuttlefish were exposed to only common
aquarium noises until the start of the playback experi-
ments. One week before experimentation, 30 cuttlefish
were placed singly in isolated tanks (22 cm # 31 cm #
22 cm) supplied with flow-through seawater at local am-
bient temperature. To prevent sound from playbacks being
transmitted to other tanks, all tanks rested on a 10-cm
thick Styrofoam base, and each tank was isolated visually
from neighboring tanks by 5-cm Styrofoam.
Playback Stimuli and Experimental Setup
First, we tested whether cuttlefish adjusted their behavior
to anthropogenic noise, and second, whether the exposure
to anthropogenic noise and a control sound led to different
behavioral responses (cf. Gross et al. 2010). To avoid pseu-
doreplication, a new set of acoustic stimuli was created
for each individual (Kunc et al. 2007a, 2007b; McMullen
et al. 2014). The control playback consisted of recordings
of waves breaking in the surf zone, and the anthropogenic
noise playback consisted of underwater engine noise from
a small car ferry (MV Portaferry II, 312 gross tonnage).
We chose ship noise, because it is the most common source
of anthropogenic noise in the aquatic environment (Vas-
concelos et al. 2007), and because most other anthropo-
genic noise is biased toward the lower frequency band
(Hildebrand 2009). Therefore, ship noise represents a suit-
able stimulus to test the impact of anthropogenic noise
on animals in the aquatic environment. Recordings of both
types of stimuli were made with a hydrophone (HTI-96-
MIN with preamplifier; manufacturer-calibrated sensitiv-
ity, ⫺165 dB re: 1 v/mPa; frequency range, 2 Hz to 30
kHz) connected to a Marantz PMD660 recorder. The hy-
drophone and recorder were calibrated using a signal of
known amplitude (for method, see Purser and Radford
2011). Averaged power spectra (fig. 1) were generated in
AVISOFT SASLab (R. Specht, Berlin) using fast Fourier
transform (FFT) analysis (FFT size 1,024; Hann evaluation
window; spectrum level units normalized to 1 Hz band-
width; 50% overlap, averaged from 5-s segments of mul-
tiple recordings).
The original recording of the ship noise, which was used
as the anthropogenic noise stimuli, had a higher sound
pressure level (SPL) than the waves breaking the surf zone,
which was used as a control treatment (fig. 1). Therefore,
to mitigate the difference in SPL, we standardized the stim-
uli to the peak amplitude using the “normalize” function
in Audacity 1.2.6. (sample frequency: 44.1 kHz; sample
format: 32-bit float). Rerecordings of the two stimuli in
the tank showed that this successfully reduced the differ-
ence in SPL between the two stimuli (fig. 1; difference
between original recordings: 48 dB; difference between
tank rerecordings: 20 dB). The remaining differences in
the recordings of the different stimuli are based on the
spectral characteristics of the stimuli, which show similar
patterns to the original recordings (frequency quartiles for
the original anthropogenic recording: 25% p 417 Hz,
50% p 812 Hz, 75% p 22,358 Hz; frequency quartiles
for the anthropogenic noise recorded in tank: 25% p 270
Hz, 50% p 656 Hz, 75% p 6434 Hz; frequency quartiles
for the original control recording: 25% p 80 Hz, 50% p
370 Hz, 75% p 2,488 Hz; frequency quartiles for the
control recorded in tank: 25% p 80 Hz, 50% p 140 Hz,
75% p 235 Hz).
The aim of our study was to test whether changes in
one sensory channel (the acoustic channel, which was af-
fected by adding anthropogenic noise) affect behavior in
other sensory channels (the tactile and the visual chan-
nels). To rule out the possibility that individuals might
respond to any change in their acoustic environment in a
uniform manner, we compared the response to anthro-
pogenic noise with response to the control treatment.
Playbacks were conducted on 30 individuals in a ran-
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Anthropogenic Noise Affects Behavior E95
Freq (Hz)
0 5000 10000 15000 20000
Sound Pressure Level (Spectral density dB/Hz re 1uPa)
60
80
100
120
140
160
180
Anthropogenic noise recorded in tank
Control recorded in tank
Original anthropogenic recording
Original control recording
Figure 1: Averaged power spectra for anthropogenic noise (ferry noise) and biological control (waves breaking in the surf zone) recorded
in the wild and recorded in the experimental tank (fast Fourier transform size p 1,024; Hann evaluation window; spectrum level units
normalized to 1 Hz bandwidth; 50% overlap; averaged from 5-s recordings). Freq p frequency.
domized order, and the two treatments were separated by
24 h to minimize habituation effects. Stimuli were played
back through a UW30 underwater speaker (Lubell Labs)
from a compact disk player connected to an amplifier
(EAGLE TPA 30V). The speaker was mounted in a cus-
tomized tank lid that allowed it to sit below the water line
while keeping disturbance to a minimum.
Experimental Protocol
For each playback, individuals were observed for 210 s
before the playback started (silence), which provided an
individual’s baseline level. Playback duration was 210 s,
and we continued to observe subjects for another 210 s
after playback (silence). For the first 30 s of the playback
period, the noise level was increased gradually to avoid
startling the cuttlefish. During each of the 210-s periods,
we noted (i) the frequency of color changes, as a measure
of visual signaling; (ii) the frequency of time individuals
had their first pair of arms raised, as a measure of tactile
signaling (cf. Hanlon and Messenger 1988); and (iii) the
time spent swimming (in seconds), as a measure of
activity.
Statistical Analyses
Statistical analyses were performed in IBM SPSS 19. To
test whether cuttlefish changed their behavior during the
anthropogenic noise playbacks, we used repeated measures
ANOVA. To fulfill the assumptions of sphericity, the three
behavioral measurements were transformed using root
squared ( ). Data shown in the figures are raw datax ⫹ 10
and are available in the Dryad Digital Repository: http://
datadryad.org/resource/doi:10.5061/dryad.c6011 (Kunc et
al. 2014). Treatment order had no significant effect on each
of the behavioral responses and thus was excluded from
the final models. To test whether cuttlefish changed their
behavior differently from the baseline control observations
to the two treatment observations, we calculated the dif-
ferences of the transformed data in the frequency of color
changes, in the time swimming, and in the frequency of
arms raised per cuttlefish per interval and tested these
values against each other using paired t-tests (cf. Gross et
al. 2010). All tests were two-tailed.
Results
Cuttlefish changed their behavior in response to anthro-
pogenic noise, and their response also differed between
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