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The active space of a signal is an important concept in acoustic communication as it has implications on the function and evolution of acoustic signals. However, it remains mostly unknown for fish since it has been measured in only a restricted number of species. We combined physiological and sound propagation approaches to estimate the communication range of the Lusitanian toadfish's (Halobatrachus didactylus) advertisement sound, the boatwhistle (BW). We recorded BWs at different distances from vocalizing fish in a natural nesting site at circa 2-3 m depth. We measured the representation of these increasingly attenuated BWs in the auditory pathway through the auditory evoked potentials technique (AEP). These measurements point to a communication range ranging between 6 to 13 m, depending on the spectral characteristics of the BW. A similar communication range (circa 8 m) was derived from comparing sound attenuation at selected frequencies with auditory sensitivity. This is one of the few studies that combines auditory measurements with sound propagation to estimate the active space of acoustic signals in fish. We emphasize the need for studies to consider that active space estimates should take informational masking into account.
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Assessing acoustic communication active space in the Lusitanian
Daniel Alves
*, M. Clara P. Amorim
and Paulo J. Fonseca
The active space of a signal is an important concept in acoustic
communication as it has implications for the function and evolution of
acoustic signals. However, it remains mostly unknown for fish as it
has been measured in only a restricted number of species. We
combined physiological and sound propagation approaches to
estimate the communication range of the Lusitanian toadfishs
(Halobatrachus didactylus) advertisement sound, the boatwhistle
(BW). We recorded BWs at different distances from vocalizing fish
in a natural nesting site at ca. 23 m depth. We measured the
representation of these increasingly attenuated BWs in the auditory
pathway through the auditory evoked potential (AEP) technique.
These measurements point to a communication range of between 6
and 13 m, depending on the spectral characteristics of the BW. A
similar communication range (ca. 8 m) was derived from comparing
sound attenuation at selected frequencies with auditory sensitivity.
This is one of the few studies to combine auditory measurements with
sound propagation to estimate the active space of acoustic signals in
fish. We emphasize the need in future studies for estimates of active
space to take informational masking into account.
KEY WORDS: Information masking, Fish, Communication range,
AEP technique, Auditory evoked potential, Boatwhistle
Acoustic communication is a widespread phenomenon across
vertebrates (Bradbury and Vehrencamp, 1998), as well as other
taxa (e.g. insects; Hedwig, 2014) and it is used in a great variety of
contexts such as advertisement, courtship, spawning, agonistic
interactions, competitive feeding or disturbance (Bradbury and
Vehrencamp, 1998; Hedwig, 2014). To be effective, acoustic
signals produced by the sender must be correctly perceived by the
receiver (Bradbury and Vehrencamp, 1998).
In some behavioural contexts, such as mate attraction, it is
advantageous for the emitter to maximize its communication range,
i.e. the area/volume around an individual where communication
with conspecifics can occur (Clark et al., 2009). However, in close-
range interactions, acoustic signals with decreased active space may
also evolve (e.g. Reichard and Anderson, 2015). Independently
of sound source characteristics (e.g. amplitude level), the
communication range of an acoustic signal will be limited by the
environmental sound propagation properties and ambient noise
conditions that will act as an acoustic filter(Fine and Lenhardt,
1983). Therefore, the effective communication distance has
important implications for the evolution and function of
acoustically mediated behaviour (Bradbury and Vehrencamp,
1998). This parameter has been studied in a variety of terrestrial
animals (e.g. insects Kostarakos and Römer, 2010; anurans
Kuczynski et al., 2010; birds Brenowitz, 1982; reptiles Todd,
2007; mammals de La Torre and Snowdon, 2002) but poorly
addressed in aquatic animals such as fish (e.g. Radford et al., 2015).
In general, underwater acoustic communication has received less
attention than terrestrial acoustic communication, probably due to
technical difficulties. Most studies on the communication range of
aquatic animals have been carried out with cetaceans (e.g. Janik,
2000; Sirovićet al., 2007; Tervo et al., 2012). Although teleost fish
are considered the largest group of vocal vertebrates (Ladich, 2004),
communication range estimation in this group is so far restricted to a
small number of species in shallow water conditions (e.g. Fine and
Lenhardt, 1983; Myrberg et al., 1986; Mann and Lobel, 1997; Lugli
and Fine, 2003; Locascio and Mann, 2011; Ghahramani et al., 2014;
Holt and Johnston, 2015; Radford et al., 2015). Sound propagation
is reduced in shallow waters, where low frequency sounds, such as
most fish vocalizations (Amorim, 2006), are strongly attenuated
with distance (Bass and Clark, 2003; Mann, 2006). Depending on
the species, estimated ranges vary from a few centimetres to tens of
metres (Amorim et al., 2015).
The Lusitanian toadfish Halobatrachus didactylus (Bloch and
Schneider 1801) is a member of the family Batrachoididae that
inhabits coastal waters and estuaries (Roux, 1986). It is a benthic
species with an unusually rich vocal repertoire (Amorim et al., 2008)
that produces sounds in both reproductive and agonistic contexts
(dos Santos et al., 2000; Vasconcelos et al., 2010). During the
breeding season, males aggregate in nesting areas close to the
substrate and produce advertisement calls the boatwhistle (BW)
to attract mates (Jordão et al., 2012; Vasconcelos et al., 2012). The
BW is the most commonly produced acoustic signal in this species
throughout the year (Amorim et al., 2006, 2008, 2010).
Halobatrachus didactylus has been used in both behavioural (e.g.
Vasconcelos et al., 2010; Ramos et al., 2012; Conti et al., 2015) and
physiological (e.g. Vasconcelos and Ladich, 2008; Vasconcelos
et al., 2011a,b) studies, making it an excellent model species for the
assessment of active space of acoustic signals in fish. Here, we aimed
to estimate the communication range in the Lusitanian toadfish using
complementary physiological and sound propagation approaches.
Auditory evoked potential (AEP) technique
Test subjects
Lusitanian toadfish were collected in the Tagus estuary (Portugal)
from trawling by local fishermen during the months of December
2013 to February 2014. After collection, fish were transported to the
laboratory at the University of Lisbon (Portugal), where they were
kept in aerated 80 l stock tanks equipped with protein skimmers,
Received 18 November 2015; Accepted 4 February 2016
Departamento de Biologia Animal and cE3c - Centre for Ecology, Evolution
and Environmental Changes, Faculdade de Ciências, Universidade de Lisboa,
Lisbon 1749-016, Portugal.
MARE Marine and Environmental Sciences Centre,
ISPA-Instituto Universitário, Lisbon 1149-041, Portugal.
*Author for correspondence (
© 2016. Published by The Company of Biologists Ltd
Journal of Experimental Biology (2016) 219, 1122-1129 doi:10.1242/jeb.134981
Journal of Experimental Biology
under a 12 h:12 h light:d ark cycle, and fed with shrimp once a week.
Water temperature ranged between 15 and 17°C, falling within
natural values. We used a total of 13 adult fish (8 males and 5
females), with an average standard length of 26.8 cm (range 16.3
37.9 cm), and an average body mass of 590 g (range 1101450 g).
All experiments were performed in accordance with local
Measuring AEPs in response to conspecific sounds
Fish were anaesthetized in a 0.01% ethyl p-aminobenzoate (Alfa
Aesar, Karlsruhe, Germany) saltwater bath and then immobilized
by an intramuscular injection of gallamine triethiodide (10
15 µg kg
; Sigma-Aldrich, Saint-Louis, MO, USA). Test
subjects were positioned just below the water surface, except for
the uppermost part of the head where the recording electrode was
placed, in the middle of a round plastic experimental tank (diameter
36 cm, water depth ca. 18 cm), with the otolithic endorgans kept at
about 7 cm above the vibrating disc of the sound-generating device.
The tank was placed on a vibration isolation table inside a Faraday
cage. All recording and sound-generating equipment were kept
outside the Faraday cage. Fish gills were perfused with saltwater
through a T-split tube positioned in the mouth using a simple
temperature-controlled (21±1°C) gravity-fed water system.
Acoustic stimuli (BWs), generated by a PC, were fed via the D/A
output of an Edirol UA-25EX (Roland Corporation, Tokyo, Japan;
48 kHz, 16 bit), amplified (custom-built amplifier) and delivered,
with alternated phase, through a custom-made underwater sound-
generating device. This device, centred within the tank, was
composed of an immersed Plexiglas disc (8 cm diameter, 8 mm
thick) attached to a rod, which was driven by a damped mechanical
wave driver (SF9324, PASCO, Roseville, CA, USA) kept below the
experimental tank. Because the mechanical wave driver is
uncoupled from the experimental tank, it does not transmit
extraneous mechanical noise to it. The rod crossed the tank
bottom through a water-restraining flexible device, which not only
prevented water drainage but also kept the rod vertically aligned.
Before each experiment, auditory stimuli were calibrated using a
precision hydrophone (8104 Bruël & Kjaer, Naerum, Denmark;
sensitivity 205 dB re. 1 V µPa
) with its acoustic centre located
7 cm above the disc, the same position occupied by the fishs
hearing organs during the recordings. The hydrophone was
connected to a sound level meter (Mediator, 2238, Bruël & Kjaer)
and the acoustic signal was digitized (Edirol UA-25EX, Roland
Corporation; 48 kHz, 16 bit) and then monitored by a laptop
running Adobe Audition 3.0 (Adobe Systems Inc., CA, USA). This
allowed us to verify, and if needed to adjust, the amplitudes of the
auditory stimuli.
The recording electrode was pressed against the skin of the fishs
head directly above the hindbrain, while the ground electrode was
placed between the eyes. The AEPs were amplified (Grass CP511,
Grass Instruments, USA; gain 20,000×, high pass 10 Hz, low pass
1000 Hz), digitized with the A/D input of the same Edirol device
(48 kHz sampling frequency) and recorded with the same PC
running Adobe Audition 3.0. The auditory stimuli and the AEP
recordings were continuously monitored with an oscilloscope.
Sound stimuli
We made synchronous recordings of BWs produced by breeding
territorial males in the natural nesting habitat (Air Force Base 6,
Montijo, Portugal; 38°42N, 8°58W). BWs were registered at
different distances from the sound-producing fish (0.1, 2.5, 5, 7.5,
10, 12.5 and 15 m; hydrophones kept at 0.1 m above the substrate).
These recordings were made with equalized hydrophones (High
Tech 94 SSQ, High Tech Inc., Gulfport, MS, USA; frequency
response: 30 Hz to 6 kHz ±1 dB; voltage sensitivity: 165 dB re.
) connected to a multichannel recording device (M-Audio
Fast Track Ultra 8R, M-Audio, Irwindale, CA, USA; 8 kHz, 16 bit)
controlled by a laptop computer running Adobe Audition 3.0. All
BWs were recorded with water levels ranging from 2.2 to 2.6 m. The
recording obtained at 0.1 m was adjusted to a playback amplitude of
140 dB sound pressure level (SPL; re, 1 µPa), corresponding to the
amplitude of BWs produced by a vocalizing nesting male
(Vasconcelos and Ladich, 2008). The sounds recorded at the
other distances were modified by the same factor in order to
preserve the amplitude gradient measured in the nesting habitat with
distance. These BWs were then played back to the subject fish and
the AEP responses recorded. Each stimulus was presented 500 times
at opposite polarities, with intervals between presentations equal to
50% of the stimulus duration.
To represent the variability of the Lusitanian toadfish BW
(Amorim and Vasconcelos, 2008), four different BWs were used as
stimuli (Fig. 1), differing in duration (4181006 ms) and dominant
frequency [ca. 50150 Hz; fast Fourier transform (FFT) 8192
points, Hamming window]. Each experimental subject was tested
with two different BWs.
Amplitude modulation representation
We used the protocol described in Vasconcelos et al. (2011a) to
estimate the maximum distance at which each fish correctly
represented the features of a BW. In brief, we compared the
envelope (amplitude modulation) of the BW recorded at 0.1 m with
the envelope of the AEP responses to the same BW recorded at
various distances (both positive and negative envelopes). Stimuli
and response envelopes were extracted with a moving average
(7 ms) of maximum amplitude values of a waveform. The variations
of envelopes of stimulus and AEP response were compared using
Pearsons correlation. Response thresholds were estimated with
Pearsons correlations between the envelopes of the stimulus BW
and the AEP response to silence in all the experimental trials
(hereafter called the threshold criteria). The threshold was defined as
the average plus twice the standard deviation of the values of these
correlation coefficients. The longest distance at which the Pearsons
correlation coefficient between the envelopes of BW and respective
averaged AEP was above threshold was considered the maximum
distance at which the BW was correctly perceived.
Signal averaging was performed with custom-written software
(P.J.F. and M. Vieira). This software is available from the authors.
The Pearsons correlation analysis was performed with Statistica
12.0 (StatSoft, Inc., USA).
Sound propagation
To measure sound attenuation in the natural breeding habitat, we
compared recordings of BWs of nesting fish registered at 0.1 m with
simultaneous recordings of the same BWs obtained at different
distances (see above).
We further compared played back sounds recorded with a
hydrophone (High Tech 94 SSQ) positioned at doubling distances
(0.5, 1, 2, 4, 8, 16 m) from an underwater speaker (Clark AQ339,
Lubell Labs, Whitehall, OH, USA), using as a reference the recording
of a similar hydrophone kept at 0.1 m from the speaker. These
measurements were conducted at Air Force Base 6 (Montijo,
Portugal) with a 2- and 5-m-high water column. The sea had very
small waves on an almost windless day. The sounds, fed to the
loudspeaker through an amplifier (Blaupunkt GTA 260, Hildesheim,
RESEARCH ARTICLE Journal of Experimental Biology (2016) 219, 1122-1129 doi:10.1242/jeb.134981
Journal of Experimental Biology
Germany), were produced with a multifunction I/O USB device (NI
USB 6521, National Instruments, Austin, TX, USA) controlled by
software custom-written (P.J.F.) in LabView (v8.2, National
Instruments), and consisted of frequency sweeps (0.01 to 1000 Hz)
with a 500 ms duration, repeated 25 times with 100 ms pauses. The
output of both the reference and testing hydrophones was
simultaneously recorded with the same multifunction board.
Comparisons of the reference sound with attenuated sounds were
made by computing with the same LabView software the averaged
transfer function spectra and the coherence function of the distant
hydrophone relative to the reference hydrophone. The sound
sampling was delayed relative to the recording of the hydrophone
close to the speaker to take into account the sound propagation delay
from the speaker to the distant hydrophone. The hydrophone
recordings were calibrated by comparison with a Bruël & Kjaer type
8104 hydrophone conditioned by a Sound Level Meter (Mediator
2238) with a linear frequency weighting and set on fast measuring
mode. The coherence function is a normalized measure of the
degree of causality (or degree of relationship) between two signals
(here, the voltage signals measured by both hydrophones) and
varies between 0 and 1. High values indicate that the recorded sound
is highly related to the stimulus sound. We only considered data
with coherence values above 0.9. Hence, we selected 120, 240 and
540 Hz as these are multiples of 60 Hz, a common fundamental
frequency in this species (Vasconcelos et al., 2010). Notice that we
excluded 120 Hz at 2 m depth and 16 m distance, and 540 Hz at 5 m
depth and 16 m distance because they did not meet the coherence
value criterion. Moreover, we could not measure the attenuation
around the fundamental frequency because the loudspeaker was not
able to transmit such frequencies with enough power.
BW propagation loss
The BWs (BW14) recorded in shallow waters of the natural
toadfish breeding habitat suffered strong attenuation with distance
(Figs 2 and 3A). When compared with the measurements of the
reference hydrophone (0.1 m), the attenuation averaged 17 dB in the
first 2.5 m. An additional 7 dB attenuation was found 5 m away
from the vocal fish, and the progressive loss of sound energy was to
about 35 dB at a distance of 15 m. From 5 m onward, the
attenuation was almost constant, with an average of 2.12.7 dB per
2.5 m. As expected, the attenuation varied throughout the frequency
range of the BW, with lower frequencies exhibiting a stronger
attenuation with increasing distance (Fig. 3B,C). As different fish
produce BWs with different spectral energy distributions (BW14;
Fig. 1), they suffered different attenuations. BW1 and BW2 were
more severely attenuated than BW3 and BW4 (cf. Fig. 2), as the
100 ms
0 100 200 300 400
Frequency (Hz)
Relative amplitude (dB)
Fig. 1. Oscillograms and power spectra for the four boatwhistles (BWs) that were used as stimuli. The boatwhistles were recorded in the field 0.1 m
away from the vocal male. Power spectra [fast Fourier transform (FFT), 8192 points, Hamming window] are shown as relative amplitude. The dashed line
highlights the typical fundamental frequency of the BWs.
Relative amplitude (dB)
Distance (m)
Fig. 2. Relative amplitude of each of the four BWs used in this study as a
function of the distance from the sound-producing fish in the natural
habitat. Amplitudes (total root mean square power) are shown relative to the
intensity registered at 0.1 m from the vocal male. The line indicates the mean.
See Materials and methods for recording conditions.
RESEARCH ARTICLE Journal of Experimental Biology (2016) 219, 1122-1129 doi:10.1242/jeb.134981
Journal of Experimental Biology
former BWs presented stronger lower frequency components than
the latter (note differences in the fundamental frequency around
50 Hz; Fig. 1), which attenuate faster in shallow waters.
Single frequency propagation
We measured the attenuation close to the substrate of selected
frequencies corresponding to the first and third harmonics of the
BWs in the same toadfish breeding habitat and at different water-
column heights. The use of single frequencies allows the reduction of
confounding effects caused by non-linearities of the loudspeakers,
and also the detection of possible anomalies in the sound
propagation caused, for instance, by acoustic interactions or filter
properties of the environment (e.g. effect of substrate and surface).
Fig. 4 depicts the propagation loss for sound at three different
frequencies (120, 240 and 540 Hz). At 2 m depth, these
measurements exhibit stronger attenuation than BWs produced by
a vocalizing fish (cf. Fig. 2). For example, while BWs attenuated
1519 dB and 3038 dB at 2 and 15 m from the source,
respectively, these frequencies decreased 1529 dB and 37
44 dB, at 2 and 16 m, respectively. Propagation at 120 Hz was
strongly affected by depth; attenuation was greater at 2 m than at 5 m
depth for 120 Hz at all tested distances (e.g. 13 dB versus 29 dB at
1 m distance; 26 dB versus 38 dB at 4 m distance; Fig. 4A). While
the 540 Hz tone seemed to follow this trend (although the pattern
was less obvious than with 120 Hz), this seemed to be reversed for
the 240 Hz tone up to 1012 m from the source (Fig. 4B). At the
distance corresponding to the average communication range (8 m),
the attenuation varied between 30 and 45 dB. In addition to these
selected frequencies, we investigated the propagation loss of the
fundamental and the third harmonic of the BWs used in our study
(Fig. 3C). Attenuation for 60 and 180 Hz followed a similar pattern
to that for 120 and 240 Hz and at ca. 8 m (7.5 m) the average
attenuation was comparable, varying between 27 and 37 dB.
In general, propagation loss fell between the ranges predicted by
spherical and cylindrical propagation models. The only exception
was the 120 Hz tone with the lower 2 m water column, which
attenuated stronger than the predictions of the spherical propagation
model (Fig. 4A).
AEP response to natural sounds
To estimate the distance at which the receivers auditory pathway
can represent a BW, we compared the envelopes of the AEP
responses with the envelope of the stimulus BW recorded at 0.1 m
from the vocal fish, using both the upper and lower AEP envelopes
for the Pearsons correlation. Fig. 5 shows an example of AEP
responses to a BW (BW2) recorded at different distances from the
source and the corresponding averaged AEP. Additionally, Fig. 5A
depicts the positive amplitude envelopes for the more intense sound
and its corresponding AEP.
Amplitude fluctuations of BWs recorded at 0.1 m from the fish
were well represented in the AEP response (Fig. 5A). The responses
to the 5 m-attenuated stimuli (Fig. 5B) showed lower amplitude as
expected (compare the amplitude scales in Fig. 5). Nevertheless,
amplitude fluctuations were still partly preserved. The AEP
response to the same BW recorded at 10 m (Fig. 5C) no longer
represented the envelope of the original sound.
0.1 m
5 m
10 m
100 ms
0.1 m
5 m
10 m
60 Hz
180 Hz
0 2 4 6 8 10121416
Distance (m)
0 100 200 300 400 500
Frequency (Hz)
Relative amplitude (dB)
Fig. 3. Representation of attenuation of BWs in the natural environment. (A) Oscillograms of BW2 recorded at different distances from the vocal fish.
(B) Power spectra (FFT, 8192 points, Hamming window) obtained for BW2 at the same distances as in A. (C) Average propagation loss at 60 and 180 Hz of the
BWs used in our study for all recorded distances. Values are relative to the intensity registered at 0.1 m from the vocal male (error bars represent s.d.).
RESEARCH ARTICLE Journal of Experimental Biology (2016) 219, 1122-1129 doi:10.1242/jeb.134981
Journal of Experimental Biology
Table 1 shows an estimation based on threshold criteria of the
maximum distance at which the amplitude fluctuations of each BW
were still represented in the AEPs and thus probably perceived by
each fish. The mean maximum distance varied between 6.4 m
(BW2) and 13.2 m (BW4). Table 1 also shows differences in
putative detection distances for the four BWs.
In this study, we estimated the communication range of the
Lusitanian toadfish advertisement BW, the most commonly
produced sound in this species (Amorim et al., 2006, 2008). We
used two different methods to provide an estimate for the
communication range of the BW: a sound-propagation experiment
in the natural environment and a physiological evaluation of hearing
ability for BWs recorded in the field.
BW propagation in the natural environment
BWs suffered strong attenuation with distance in the natural toadfish
breeding habitat as expected for shallow water. Low-frequency
sounds with wavelengths longer than the height of the water column
are strongly attenuated in natural environments (Bass and Clark,
2003; Mann, 2006). Because BWs have fundamental frequencies of
ca. 5060 Hz (sound wavelength λ2530 m), water depth at
our breeding study site (<5 m) will impact sound propagation.
Indeed, frequency components corresponding to a wavelength
approximately four times longer than the water depth are below the
cut-off frequency dictated by the high-pass filter properties of the
medium and their propagation will be strongly hampered (Mann,
In addition, the radiation pattern of the sound source should also
influence sound attenuation. For example, the sound-producing
swimbladder in the oyster toadfish, Opsanus tau, was described as a
complex mixed-sound radiator with monopole, dipole and
quadrupole components (Fine et al., 2001). The acoustic near-
field of such a source (usually up to λ/2πmetres) can be quite
complex with acceleration, velocity, net fluid displacement and
sound pressure decreasing faster than expected for a geometric
spreading model (6 dB per doubling distance, which is the
attenuation in the far-field; Bass and Clark, 2003). Although the
swimbladder of the Lusitanian toadfish presents a different
morphology, a complex radiation pattern should also be expected.
This may explain why the attenuation of the BWs in the natural
environment was very high close to the sound-producing fish, with a
steep slope in the first few metres. At greater distances, the
attenuation was lower and became more uniform (Fig. 2).
Amorim and Vasconcelos (2008) reported an attenuation of
21 dB from 0.5 to 4 m for BWs emitted from a speaker. Although
the depth was not mentioned, these values are in accordance
with our findings. Other Batrachoidids present similar attenuation
sounds in the natural environment. For example, in the plainfin
midshipman, Porichthys notatus, the advertisement hum attenuated
–50 024681012141618
Distance (m)
120 Hz, 5 m
120 Hz, 2 m
240 Hz, 5 m
240 Hz, 2 m
540 Hz, 5 m
540 Hz, 2 m
Relative amplitude (dB)
Fig. 4. Propagation loss of selected frequencies at a breeding site of
Lusitanian toadfish (Tagus estuary) at different water-column heights
(2 and 5 m). Frequencies: 120 Hz (A); 240 and 540 Hz (B). Amplitudes are
shown relative to the intensity registered 0.1 m away from the loudspeaker.
100 ms
10 µv
0.5 µv
0.5 µv
Fig. 5. Example oscillograms of stimuli and respective auditory evoked
potential responses, as well as the amplitude modulations (envelopes)
obtained in each case for a fish responding to BW2. Stimuli (upper traces)
recorded at 0.1 m (A), 5 m (B) and 10 m (C) together with the respective
auditory evoked potentials (AEPs; lower traces). To estimate the distance at
which the receivers auditory pathway can represent a BW, we compared the
envelopes of the AEP responses with the envelope of the stimulus BW
recorded at 0.1 m from the vocal fish, using both the upper and lowerenvelopes
for the Pearsons correlation. Although only the upper trace is depicted, both
the upper and lower envelopes were used. Note that the scale bars to the right
of the oscillograms represent the same amplitude because the amplitude of the
stimulus in A is much larger than that in the other panels.
RESEARCH ARTICLE Journal of Experimental Biology (2016) 219, 1122-1129 doi:10.1242/jeb.134981
Journal of Experimental Biology
close to 20 dB from 0.5 to 3 m (5 m depth) from a vocal male (Bass
and Clark, 2003). The advertisement BW in O. tau was reduced by
17 dB between 1 and 5 m distance (0.751.2 m depth) from the
male (Fine and Lenhardt, 1983), while in the Gulf toadfish,
Opsanus beta, it was attenuated by approximately 22 dB between
0.1 and 2.5 m distance (1 m depth) (Remage-Healey and Bass,
2005). For fish of other families, the attenuation described has been
lower (e.g. 79 dB attenuation from 1 to 3 m from the vocal male, 1
4 m depth, in the Hawaiian sergeant damselfish, Abudefduf
abdominalis; Maruska et al., 2007), and the model for sound
degradation in the black drum, Pogonias cromis (7 m depth),
predicts much lower attenuations (Locascio and Mann, 2011).
Single frequency propagation
Water-column height had an important effect in the propagation of
the selected frequencies as there were significant differences in
sound attenuation at distances above 0.5 m between 2 and 5 m water
depth (Fig. 2).
At 2 m depth, the 120 Hz tone (a frequency strongly represented
in many BWs; see Fig. 1) had an amplitude loss around 45 dB 8 m
away from the speaker (see Fig. 4). Considering a level of 140 dB re.
1 µPa at 0.1 m (Vasconcelos and Ladich, 2008), a loss of 45 dB
would mean that the 120 Hz frequency is close to the hearing
threshold for the BW of ca. 98 dB measured with the AEP technique
(Vasconcelos et al., 2011a). Note that the attenuation for the
60 Hz component of the BW had a similar value (ca. 40 dB at a
distance of 7.5 m; see Fig. 3C). Therefore, a receiver would have
very little energy available to listen to a conspecific at around 8 m
The remaining studied frequencies, while still within the
hearing range of this species (Vasconcelos et al., 2011b), have a
smaller contribution for the overall BW energy (Fig. 1). These
frequencies were also attenuated at 8 m from the speaker to
amplitude values that were close to the 98 dB hearing threshold
(Vasconcelos et al., 2011a). Thus, 8 m seems to be a reasonable
approximation for the maximum communication range estimated
with this method.
The propagation of almost all the selected frequencies fell
between a spherical and a cylindrical propagation model (Fig. 4; for
a review of these models, see Bass and Clark, 2003; Mann, 2006).
However, the attenuation of the 120 Hz tone with a 2 m water
column was even greater than for the spherical propagation model.
Using eqn 8 in Mann (2006) with the velocity for sound propagation
in a sandy substrate (1600 m s
), we obtain a cut-off frequency of
539 Hz for a 2 m water column and a cut-off frequency of 216 Hz
for a 5 m column. As 120 Hz is below these cut-off frequencies, as
well as most BW energy, this probably contributes to further limit its
propagation. This intense attenuation of low-frequency sounds in
the breeding environment should restrain the communication range
in this habitat. Moreover, propagation of these frequencies in such
shallow waters is a very complex phenomenon where reflection and
refraction play an important role (Bass and Clark, 2003; Mann,
2006). However, these factors are hard to model because they
generate very complex sound fields and the properties of the
substrate have also to be taken into account. All these factors may
explain why the models do not accurately account for our
propagation data. These factors could also be a possible
explanation for the fact that the 240 Hz tone suffered less
attenuation with a 2 m than with a 5 m water column (Fig. 4).
In summary, the water-column height seems to play a very
important role in shaping the communication range in this species,
as expected. Although we did not register or test the propagation of
BWs at 5 m or deeper waters, we expect that at these depths the
attenuation of low frequencies should be less intense (Fig. 4) and,
because the BWs have more energy at low frequencies (Fig. 1), the
structure of the BWs should be maintained at larger distances.
Congruently, tide level has been shown to influence the number of
BWs produced by nesting males and the characteristics of these
BWs. Males calling from nests in the upper infralitoral zone
exhibited a marked circatidal rhythm, with a higher BW production
in the high tide (Amorim et al., 2011). These changes in vocal
behaviour probably reflect a strategy to minimize vocal activity
costs, i.e. the relationship between the vocal effort and
communication range.
AEP response to natural sounds
Our results indicate that the BWs can be detected up to a distance of
613 m (Table 1). This difference seems to depend mostly on the
spectral content of the sound and not on redundancy conferred by
longer duration. BW2 and BW3 have similar durations but differ by
about 4 m in maximum detection distance, while BW1 and BW2
present similar maximum detection distances but have a 300 ms
duration difference. However, spectral characteristics affect sound
attenuation (see above) and hence its detection by fish. BWs with
more energy in the lower frequency components (BW1 and BW2)
propagated less and presented shorter detection distances as
estimated by AEPs (7 and 6 m) than BWs (BW3 and BW4) with
more energy at higher frequencies (10 and 13 m). The expected
communication ranges for the different BWs estimated with AEPs
are in agreement with the estimations using sound propagation
methods. These distances are slightly longer than the ones reported
for other Batrachoidids such as P. notatus (Ibara et al., 1983) and
O. tau (Fine and Lenhardt, 1983). However, both of these studies
were conducted with lower water-column heights. Communication
range estimations in fish of other families have varied from tens of
centimetres in the Padanian goby, Padogobius bonelli (Lugli and
Fine, 2003), to tens of metres in Pogonias cromis (Locascio and
Mann, 2011). Direct comparisons should be made with caution as
Table 1. Estimated maximum distance at which the fish is able to correctly encode the amplitude modulations of the stimulus boatwhistle
Fish Detection distance (m) Fish Detection distance (m) Fish Detection distance (m) Fish Detection distance (m)
2 7.5 2 10 1 12.5 1 15
6 10 3 7.5 4 7.5 3 7.5
7 5 5 5 6 10 4 12.5
85 85 910 515
10 10 9 7.5 10 12.5 7 15
11 5 11 5 12 10 12 15
13 5 13 12.5
Mean 7.1 Mean 6.4 Mean 10.4 Mean 13.2
Fish are grouped by the different boatwhistles (BWs) used as a stimulus (see Materials and methods).
RESEARCH ARTICLE Journal of Experimental Biology (2016) 219, 1122-1129 doi:10.1242/jeb.134981
Journal of Experimental Biology
differences in the environmental conditions of the experiments,
such as water-column height or distance from the emitter fish to the
substrate, will influence these estimations.
The present study points to the Lusitanian toadfish
communication range being more limited by audition than
affected by the background noise in the studied habitat. Most
experimental fish stopped perceiving the BWs correctly at distances
where the amplitudes registered were well above the hearing
threshold described for this species. Using the attenuation values in
Fig. 2, at 10 m from the sound-producing fish, the BW would have
an amplitude close to 110 dB, considering a source level of 140 dB
re. 1 µPa at 10 cm (Vasconcelos and Ladich, 2008). This value is
over 10 dB above the described threshold for this species (ca.
98 dB) (Vasconcelos et al., 2011a). This contrasts with what
Locascio and Mann (2011) have reported for P. cromis. In their
work, they compared the propagation of calls in the natural
environment with the hearing capabilities of one fish. They
concluded that the limiting factor for communication is
environmental noise because environmental noise is higher than
the hearing threshold. Most other studies that have estimated the
acoustic communication range of fish have either determined
the maximum distance for signals to become indistinguishable from
the background noise (Fine and Lenhardt, 1983; Mann and Lobel,
1997; Lugli and Fine, 2003) or assumed that the limiting factor for
the communication range is environmental noise (Radford et al.,
2015). Notably, thresholds in our study are not based on the
presence of a biological response in the auditory pathway but on a
correct representation of the acoustic signal envelope. Therefore, we
are testing informational masking of acoustic signals and not
energetic masking (Clark et al., 2009). Signal degradation should
make signals lose their informational content before its energy is
undetectable from background noise. Therefore, animals may have
trouble retrieving information from acoustic signals in the
environment at the communication ranges estimated through
energetic masking that characterize many studies.
Demonstration of the communication distance at which fish are
capable of extracting relevant information from conspecific sounds is
probably only possible with behavioural experiments. To the best of
our knowledge, there are no studies that measure the communication
range in the field based on information criteria. For instance,
Myrberg et al. (1986) report that females are attracted to playbacks of
male sounds up to 10 m away from the speaker and that they show
preference for the sound of a larger male. However, because no other
sounds were tested, it remains to be clarified whether the phonotaxis
range described was due to information extraction from the sound or
simply triggered by cues such as frequency or energy.
In summary, we show that the communication range of the
Lusitanian toadfish advertisement BW varies on average between 6
and 13 m, an estimation that is corroborated by comparing the
attenuation of selected frequencies measured in the natural habitat
with the hearing sensitivity of the fish. We highlight the importance
of estimating communication active space by taking into account the
perception of the information content in acoustic signals and not just
energy detection.
We thank Air Force Base No. 6of Montijo (Portugal) for allowing us to conduct sound
recordings of toadfish adults in their military establishment. We would also like to
thank Andreia Ramos for her help with the fieldwork and Manuel Vieira for help with
the averaging software.
Competing interests
The authors declare no competing or financial interests.
Author contributions
D.A. conceived the experimental design, carried out the AEP experiments and
analysed their results, and drafted the article. M.C.P.A. helped design the
experiments, supervised the experimental work and critically reviewed the article.
P.J.F. conceived the experimental design, supervised the experimental work,
carried out the sound propagation experiments and analysed their results, and
critically reviewed the manuscript.
This study was funded by the Science and Technology Foundation, Portugal [ grant
SFRH/BD/48015/2008 to D.A. and pluriannual programme UI&D 331/94 and UI&D
329, and the strategic projects UID/MAR/04292/2013 and UID/BIA/00329/2013
granted to MARE (M.C.P.A.) and to cE3c (P.J.F.)].
Data availability
Custom-written software (P.J.F. and M. Vieira) for signal averaging is available on
request from the authors.
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... The protocol for AEP recordings followed Kenyon et al. (1998), adapted by Wysocki and Ladich (Wysocki and Ladich, 2001;Wysocki and Ladich, 2003), and used by Alves et al. (2016). In short, each juvenile fish was mildly anesthetized with MS-222 (ethyl 3-aminobenzoate methanesulfonic acid salt, ACROS Organics, Geel, Belgium) to be immobilized in a soft sponge, with the opercula free but with the head movements restricted by pieces of plastic soft tubing in both sides of the snout and jaw. ...
... Acoustic stimuli (see below) were fed via an Edirol UA-25EX to an amplifier and delivered through an underwater sound generating device (described in Vasconcelos et al., 2011 andin Alves et al., 2016). The sound pressure levels of the stimuli used were calibrated with a hydrophone (8104, Brüel & Kjaer, Naerum, Denmark; sensitivity -205 dB re. 1 V μPa − 1 ; frequency response from 0.1 Hz to 180 kHz) positioned in the place later occupied by the fish inner ears and connected to a sound level meter (Bruël & Kjaer 2238 Mediator, Naerum, Denmark). ...
... To obtain the thresholds of the AEP response to conspecific calls (short grunt) without or with the presence of boat noise we adapted the protocol described by Vasconcelos et al. (2011) and Alves et al. (2016) to estimate the minimum stimulus amplitude at which each fish correctly represented the features of a short grunt without and with boat noise. In brief, we computed Pearson correlations between the averaged AEP response to the short grunt stimulus presented at the higher amplitude and the AEP responses to the same grunt recorded at the various decreasing amplitudes. ...
Aquatic noise has increased in last decades imposing new constraints on aquatic animals' acoustic communication. Meagre (Argyrosomus regius) produce loud choruses during the breeding season, likely facilitating ag-gregations and mating, and are thus amenable to being impacted by anthropogenic noise. We assessed the impact of boat noise on this species acoustic communication by: evaluating possible masking effects of boat noise on hearing using Auditory Evoked Potentials (AEP) and inspecting changes in chorus sound levels from free ranging fish upon boat passages. Our results point to a significant masking effect of anthropogenic noise since we observed a reduction of ca. 20 dB on the ability to discriminate conspecific calls when exposed to boat noise. Furthermore, we verified a reduction in chorus energy during ferryboat passages, a behavioural effect that might ultimately impact spawning. This study is one of few addressing the effects of boat noise by combining different methodologies both in the lab and with free ranging animals.
... After preliminary visualization of the rose-plots produced by each pair, we decided to aggregate the phase angles according to distance between males -separated by ≤5 m or > 5 m, since in more distant pairs phase angles consistently presented a higher variability (see examples in Fig. S2). The distance threshold was selected in accordance with the communication active space reported for the Lusitanian toadfish by Alves et al. (2016) that estimated maximum distance with correct perception of conspecific's BWs to be from 5 up to 13 m, using BWs recorded during nearly high tide (water levels 2.2-2.6 m). The dividing distance of 5 m (the lower range of found correct perception distance) was chosen as BW propagation is highly depth dependent (Alves et al., 2016). ...
... The distance threshold was selected in accordance with the communication active space reported for the Lusitanian toadfish by Alves et al. (2016) that estimated maximum distance with correct perception of conspecific's BWs to be from 5 up to 13 m, using BWs recorded during nearly high tide (water levels 2.2-2.6 m). The dividing distance of 5 m (the lower range of found correct perception distance) was chosen as BW propagation is highly depth dependent (Alves et al., 2016). To extract the relevant interactions among fish while using the pool of calls produced by the 16 fish, we only considered the occurrences when a single male's BW was between the BWs of another male. ...
... This interaction pattern was less clear at larger distances when BWs tend to attenuate to background levels. The 5 m distance threshold used here is consistent with the estimated communication range of up to 5-13 m in the shallow water breeding area of the Tagus estuary (Alves et al., 2016). ...
Males of several fish species aggregate and vocalize together, increasing the detection range of the sounds and their chances of mating. In the Lusitanian toadfish (Halobatrachus didactylus), breeding males build nests under rocks in close proximity and produce hundreds of boatwhistles (BW) an hour to attract females to lay their demersal eggs on their nest. Chorusing behaviour includes fine-scale interactions between individuals, a behavioural dynamic worth investigating in this highly vocal fish. Here we present a study to further investigate this species' vocal temporal patterns on a fine (individual rhythms and male-male interactions) and large (chorus daily patterns) scales. Several datasets recorded in the Tagus estuary were labelled with the support of an automatic recognition system based on hidden Markov models. Fine-scale vocal temporal patterns exhibit high variability between and within individuals, varying from an almost isochronous to an apparent aperiodic pattern. When in a chorus, males exhibited alternation or synchrony calling patterns, possibly depending on motivation and social context (mating or male-male competition). When engaged in sustained calling, males usually alternated vocalizations with their close neighbours thus avoiding superposition of calls. Synchrony was observed mostly in fish with lower mean calling rate. Interaction patterns were less obvious in more distanced males. Daily choruses showed periods with several active calling males and periods of low activity with no significant diel patterns in shallower intertidal waters. Here, chorusing activity was mainly affected by tide level. In contrast, at a deeper location, tide level did not significantly influence calling and there was a higher calling rate at night. These data show that photoperiod and tide levels can influence broad patterns of Lusitanian toadfish calling activity as in other shallow-water fishes, but fine temporal patterns in acoustic interactions among nesting males is more complex than previously known for fishes.
... PAM is already used for a multitude of biological applications. Examples include monitoring, characterizing and delineating underwater soundscapes, and investigating aquatic communities (e.g., Desjonquères et al., 2015;Erbe et al., 2015;Menze et al., 2017;Mooney et al., 2020;Stanley et al., 2021); documenting the distribution and migration patterns of the great whales (e.g., Risch et al., 2014;Tsujii et al., 2016;Davis et al., 2020;Warren et al., 2021); characterizing the spatial and temporal responses of fish choruses to environmental drivers like temperature, salinity, lunar phase, tide, and time of sunset (e.g., Barrios, 2004;Rountree et al., 2006;Parsons, 2010;Straight et al., 2015;Rice et al., 2016;McWilliam et al., 2017;Parsons et al., 2016;Karaconstantis et al., 2020;Linke et al., 2020); understanding how animals change their behavior and distribution in response to climate change (Gordon et al., 2018), anthropogenic noise sources (e.g., Thompson et al., 2013;Cerchio et al., 2014;Erbe et al., 2019;Meekan et al., 2021), algal blooms (e.g., Rycyk et al., 2020) and extreme weather events like hurricanes (e.g., Locascio and Mann, 2005;Fandel et al., 2020;Boyd et al., 2021;Schall et al., 2021); understanding how prey change their sound production rates or behaviors with the presence of predators (e.g., Luczkovich and Keusenkothen, 2007;Hughes et al., 2014;Bailey et al., 2019;Burnham and Duffus, 2019); and how noise and propagation conditions can affect communication spaces (e.g., Alves et al., 2016;McKenna et al., 2021). This wide range of uses for PAM is expanding with developments in technology, providing a great volume of easily accessible data on aquatic life. ...
... Sound production between similar species within a taxonomic family can also be compared, such as those of mulloway (Argyrosomus japonicus) and black jewfish (Protonibea diacanthus) in Australia (Parsons et al., 2012(Parsons et al., , 2013b(Parsons et al., , 2016 with those of French meagre (A. regius) in Europe (Lagardère and Mariani, 2006;Bolgan et al., 2020b), or those of various species of toadfishes in the Pacific, Indian, and Atlantic oceans (Thorson and Fine, 2002;Rice and Bass, 2009;Mosharo and Lobel, 2012;Alves et al., 2016;Staaterman et al., 2018;Pyć et al., 2021), to better understand the variation within families. ...
Full-text available
Aquatic environments encompass the world’s most extensive habitats, rich with sounds produced by a diversity of animals. Passive acoustic monitoring (PAM) is an increasingly accessible remote sensing technology that uses hydrophones to listen to the underwater world and represents an unprecedented, non-invasive method to monitor underwater environments. This information can assist in the delineation of biologically important areas via detection of sound-producing species or characterization of ecosystem type and condition, inferred from the acoustic properties of the local soundscape. At a time when worldwide biodiversity is in significant decline and underwater soundscapes are being altered as a result of anthropogenic impacts, there is a need to document, quantify, and understand biotic sound sources–potentially before they disappear. A significant step toward these goals is the development of a web-based, open-access platform that provides: (1) a reference library of known and unknown biological sound sources (by integrating and expanding existing libraries around the world); (2) a data repository portal for annotated and unannotated audio recordings of single sources and of soundscapes; (3) a training platform for artificial intelligence algorithms for signal detection and classification; and (4) a citizen science-based application for public users. Although individually, these resources are often met on regional and taxa-specific scales, many are not sustained and, collectively, an enduring global database with an integrated platform has not been realized. We discuss the benefits such a program can provide, previous calls for global data-sharing and reference libraries, and the challenges that need to be overcome to bring together bio- and ecoacousticians, bioinformaticians, propagation experts, web engineers, and signal processing specialists (e.g., artificial intelligence) with the necessary support and funding to build a sustainable and scalable platform that could address the needs of all contributors and stakeholders into the future.
... The sensitivity analysis revealed that cod stock is dominantly influenced by its habitat condition and by factors altering it (Fig. 2F), since juvenile cod requires bottom habitats of structural complexity for survival (Tupper and Boutilier, 1995). Further, adult cod show avoidance behavior towards suspension (Westerberg et al., 1996) and furthermore, noise pollution from leisure boating activities was shown to severely impede communication across different fish species, potentially resulting in a limitation of reproduction and survival (Slabbekoorn et al., 2010;Alves et al., 2016). ...
Global climate change and related land use changes are expected to impose unprecedented pressures on coastal biodiversity and ecosystem processes. To sustainably manage coastal ecosystems, it is crucial to predict the consequences of human activities for coastal ecosystems and identify areas for directed abatement measures. Empirical data together with expert knowledge and evidence from the literature were integrated into a Bayesian Belief Network (BBN) for a marine protected area, the Kosterhavet National Park off the Swedish west coast. The variability and interactions of anthropogenic pressures and two key ecosystem components, eelgrass meadows and northern shrimp stock, were tested under four storylines of environmental change. The results show that of the influential drivers of environmental change, only three variables (bottom trawling, leisure boating and aquaculture) are manageable within the national park itself. Scenario analysis suggested that notable gains of both ecosystem components were most likely under a storyline of sustainable development, assuming a radiative forcing of 4.5 W/m² by 2100 in concert with a preventive cooperation among neighboring countries and a tighter restriction of commercial and recreational uses in the park area. The findings suggest that the sustainable management of eelgrass meadows and northern shrimp stock in Kosterhavet National Park requires both local measures at the scale of the park's water bodies and, to a greater part, also regional measures, e.g., to reduce nutrient influx from adjacent water bodies. In conclusion, this approach can help practitioners to make more informed management decisions and foresee the effects of routes of socio-economic development.
... A detrimental effect in calling activity has been found in other batrachoidids namely the oyster toadfish (Krahforst, 2017;Mackiewicz et al., 2021) and the plainfin midshipman (Brown et al., 2021), in sciaenids such as the black drum Pogonias courbina (Ceraulo et al., 2021) and the meagre Argyrosomus regius (Vieira et al., 2021c), and in two gobies, Gobiusculus flavescens and P. pictus (de Jong et al., 2018a). Besides from decreasing calling activity, which is essential to attract and court mates in several fish species (Amorim et al., 2015), reproduction may be further impaired by the reduction in the communication active space (Alves et al., 2016), by masking (Alves et al., 2021;Pine et al., 2021) or changing the receivers' physiology by causing stress and/or distraction (Simpson et al., 2016;Butler and Maruska, 2021). Interestingly, some species compensate for communication loss by increasing vocalization rates (such as the brown meagre Sciaena umbra; Picciulin et al., 2012), by changing the frequency and/or amplitude of their vocalizations (Brown et al., 2021), or by shifting to other sensory modalities (de Jong et al., 2018b). ...
Anthropogenic noise is a growing threat to marine organisms, including fish. Yet very few studies have addressed the impact of anthropogenic noise on fish reproduction, especially in situ. In this study, we investigated the impacts of boat noise exposure in the reproductive success of wild Lusitanian toadfish (Halobatrachus didactylus), a species that relies on advertisement calls for mate attraction, using behavioural, physiological and reproductive endpoints. Two sets of artificial nests were deployed in the Tagus estuary and exposed to either ambient sound or boat noise during their breeding season. Toadfish males spontaneously used these nests to breed. We inspected nests for occupation and the presence of eggs in six spring low tides (in two years) and assessed male vocal activity and stress responses. Boat noise did not affect nest occupation by males but impacted reproductive success by decreasing the likelihood of receiving eggs, decreasing the number of live eggs and increasing the number of dead eggs, compared to control males. Treatment males also showed depressed vocal activity and slightly higher cortisol levels. The assessment of oxidative stress and energy metabolism-related biomarkers revealed no oxidative damage in noise exposed males despite having lower antioxidant responses and pointed towards a decrease in the activity levels of energy metabolism-related biomarkers. These results suggest that males exposed to boat noise depressed their metabolism and their activity (such as parental care and mate attraction) to cope with an acoustic stressor, consistent with a freezing defensive response/behaviour. Together, our study demonstrates that boat noise has severe impacts on reproductive fitness in Lusitanian toadfish. We argue that, at least fishes that cannot easily avoid noise sources due to their dependence on specific spawning sites, may incur in significant direct fitness costs due to chronic noise exposure.
... Thus, we can conclude that the communication distances are much shorter than the detection ranges. On the specific dataset studied here, assuming that the animals are sensitive to frequencies below 1 kHz, the communication distances would be no more than 10 m (see Figure 20), which is consistent with what is known for fish (Mann and Lobel 1997, Alves et al. 2016, Locascio and Mann 2011. ...
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Le rôle écologique des sons chez les crustacés est mal défini comparé aux mammifères marins et aux poissons. Or, comprendre l’importance des sons pour la biologie d’une espèce est crucial lorsque les impacts des bruits anthropiques sont recherchés. Par ailleurs, l’écologie cherche encore à développer de nouveaux outils de suivi par acoustique passive (PAM). L’enjeu principal de cette thèse était d’étudier la bioacoustique de deux espèces de crustacés à fort intérêt commercial et patrimonial en Europe : le homard Européen Homarus gammarus, et la langouste rouge Palinurus elephas. En tenant compte de l’effet physique des cuves sur les sons, nous avons mis en évidence la forte production de buzz entre homards mâles lors de rencontres agonistiques pour établir des statuts de dominance. Une approche neurophysiologique nous a ensuite permis de caractériser les capacités sensorielles des homards qui détectent les sons dans la même bande de fréquence que les buzz qu’ils émettent, renforçant l’hypothèse d’une communication acoustique. La deuxième partie de cette thèse présente comment, chez la langouste, leurs rasps d’antennes pourraient être utilisés avec du PAM par les biologistes et les halieutes. En effet, après avoir quantifié leur propagation in situ, nous avons mis en évidence que ces sons peuvent être détectés à l’échelle du kilomètre, et que leurs caractéristiques dépendent de la taille des individus. Nous avons également montré que ces rasps d’antennes sont largement énergétiques dans les basses fréquences (< 1 kHz), ce qui permet aussi de poser l’hypothèse de leur utilisation pour une communication acoustique. Les résultats de ce travail de thèse ouvrent des perspectives importantes sur l’impact potentiel des bruits anthropiques et le développement du PAM pour la gestion et conservation des crustacés.
... In shallow waters, the energy of sounds attenuated sharply with increasing distance, and propagation can be theoretically predicted by cylindrical (transmission loss equal to 10 log r) and spherical (20 log r) spreading loss models (Bass & Clark, 2003). The experiments of playback of 120 Hz tones showed an attenuation of ~ 30 dB from 0.1 to 10 m (5 m depth), falling between ranges of cylindrical and spherical loss models (Alves et al., 2016). Due to the limitations of safety regulations imposed by the wind farm company, we were not allowed to measure the underwater noise levels close to the vicinity of the turbine foundations. ...
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Environmental assessments of underwater noise on marine species must be based on species‐specific hearing abilities. This study was to assess the potential impact of underwater noise from the East China Sea Bridge wind farm on the acoustic communication of the marbled rockfish. Here, the 1/3 octave frequency band of underwater noise was 125 Hz with the level range of 78–96 dB re 1 μPa, recorded at distances between 15‐20m from the foundation at wind speed of 3–5 m/s. Auditory evoked potential (AEP) and passive acoustic techniques were used to determine the hearing abilities and sound production of the fish. The resultes showed the lowest auditory threshold of Sebastiscus marmoratus was 70 dB at 150 Hz matching the disturbance sound ranging 140–180 Hz, which indicating the acoustic communication used in this species. However, the frequency and level of turbine underwater noise overlapped the auditory sensitivity and vocalization of Sebastiscus marmoratus. The wind turbine noise could be detected by fish and may have a masking effect on their acoustic communication. This result can be applied for further to the assessent of fish species released into offshore wind farm marine ranch.
... Our results represent a conservative estimate based in part on hypothetical estimates of sound production and perception and therefore may not entirely reflect the natural abilities of grasshopper mice. Nevertheless, estimating the maximum distance that vocalizations function in nature not only informs the ecological context of species-specific signalling but provides a metric to compare across diverse taxa (Brenowitz, 1982;Brown, 1989;Gerhardt & Huber, 2002;Alves et al., 2016;Taylor et al., 2019;Römer, 2020) to facilitate our understanding of how acoustic communication systems evolve. Due to extreme variation in rodent social systems, space use, and acoustic signalling (Janik, 2000;Wolff & Sherman, 2007;Miller & Engstrom, 2007Pasch et al., 2011Pasch et al., , 2017, their continued study promises to provide important insights. ...
The efficacy of animal acoustic communication depends on signal transmission through an oft-cluttered environment. Anthropogenic-induced changes in vegetation may affect sound propagation and thus habitat quality, but few studies have explored this hypothesis. In the southwestern United States, fire suppression and cattle grazing have facilitated displacement of grasslands by pinyon-juniper woodlands. Northern grasshopper mice (Onychomys leucogaster) inhabit regions impacted by juniper encroachment and produce long-distance vocalizations to advertise their presence to conspecifics. In this study, we coupled acoustic recordings and electrophysiological measurements of hearing sensitivity from wild mice in the laboratory with sound transmission experiments of synthesized calls in the field to estimate the active space (maximum distance that stimuli are detected) of grasshopper mouse vocalizations. We found that mice can detect loud (85 dB SPL at 1 m) 11.6 kHz vocalizations at 28 dB SPL. Sound transmission experiments revealed that signal active space is approximately 50 m. However, we found no effect of woody plant encroachment on call propagation because juniper and woody plant density were inversely associated and both present barriers to a 9 cm mouse advertising at ground level. Our data indicate that woody plant encroachment does not directly impact the efficacy of grasshopper mouse communication, but vegetation shifts may negatively impact mice via alternative mechanisms. Identifying the maximum distance that vocalizations function provides an important metric to understand the ecological context of species-specific signaling and potential responses to environmental change.
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As an Arctic gateway, the Norwegian Sea sustains a rich diversity of seasonal and resident species of soniferous animals, vulnerable to the effects of climate change and anthropogenic activities. We show the occurrence of seasonal patterns of acoustic signals in a small canyon off Northern Norway, and investigate cetacean vocal behavior, human-made noise, and climatic contributions to underwater sound between January and May 2018. Mostly median sound levels ranged between 68.3 and 96.31 dB re 1 μPa2 across 1/3 octave bands (13 Hz–16 kHz), with peaks in February and March. Frequencies under 2 kHz were dominated by sounds from baleen whales with highest rates of occurrence during winter and early spring. During late-spring non-biological sounds were predominant at higher frequencies that were linked mainly to ship traffic. Seismic pulses were also recorded during spring. We observed a significant effect of wind speed and ship sailing time on received sound levels across multiple distance ranges. Our results provide a new assessment of high-latitude continental soundscapes in the East Atlantic Ocean, useful for management strategies in areas where anthropogenic pressure is increasing. Based on the current status of the local soundscape, we propose considerations for acoustic monitoring to be included in future management plans.
Anthropogenic noise is considered a major underwater pollutant as increasing ocean background noise due to human activities is impacting aquatic organisms. One of the most prevalent anthropogenic sounds is boat noise. Although motorboat traffic has increased in the past few decades, its impact on the communication of fish is still poorly known. The highly vocal Lusitanian toadfish (Halobatrachus didactylus) is an excellent model to test the impact of this anthropogenic stressor as it relies on acoustic communication to attract mates. Here, we performed two experiments to test the impact of boat noise on the acoustic communication of the Lusitanian toadfish. Using the auditory evoked potential (AEP) technique, we first compared the maximum distance a fish can perceive a boatwhistle (BW), the mate attraction acoustic signal, before and after embedding it in boat noise. Noises from a small motorboat and from a ferryboat reduced the active space from a control value of 6.4–10.4 m to 1.7–2.5 m and 6.3–6.7 m, respectively. In the second experiment we monitored the acoustic behaviour of breeding males exposed to boat noise playbacks and we observed an increase in the inter-onset interval of BWs and a disruption of the usual vocal interactions between singing males. These results demonstrate that boat noise can severely reduce the acoustic active space and affect the chorusing behaviour in this species, which may have consequences in breeding success for individuals and could thus affect fitness.
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A previously unreported kind of fish sound, which was produced spontaneously by nesting male Porichthys notatus, was recorded in the field and laboratory. Unlike other fish sounds, this monotonous ‘hum’ continues uninterrupted from a few seconds to over 60 min with a mean length of about 11 min. It has a fundamental frequency between 98–108 Hz. The hum was produced only at night. The hum stimulates male-searching behavior in gravid females and serves as an underwater acoustic beacon for mate localization in this nocturnally active species. Gravid females responded in identical manner to pure tones as to the hum and became most highly excited at ~95 Hz, but also responed actively to pure tones over a range of 85–115 Hz. Spent females, juveniles and ripe males showed little, if any, response to the same pure tones. Gravid females tracked in an 8 m diameter concrete tank oriented to the 95 Hz pure tone by swimming directly 2–3 m to the suspended speaker, or by swimming in a circuitous path to the source, then pausing, turning or stopping under the speaker or swimming up to and butting and nipping the speaker.
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Fish sound characteristics are associated with different sound-generating mechanisms. Sounds produced by swimbladder-related mechanisms usually comprise low-frequency pulses produced at different rates. Fishes emit one to five sound types that do not show such outstanding variability as found in other taxa. However, closely related species show consistent differences in their sounds and in some species even individuality is found. Of particular interest are differences in courtship sounds made by closely related sympatric species that may promote reproductive isolation. Differences between individuals of the same species may in turn play a role in sexual selection through male-male competition and female mate choice. Other known sources of variability are related to context, including motivation and recent social status, season, time of day, ontogenetic changes and sexual dimorphism. Fish sound variability is mainly based on temporal patterning of sounds or pulses within a sound and on frequency variation (sometimes modulation). Such variability has been found to play a role in the social life of fishes.
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Fish acoustic signals associated with mating behaviour are typically low-frequency sounds produced by males when in close proximity to females. However, some species make sounds that serve the function and follow the design of advertisement calls, well known in insects, anurans, and birds. Close-range courtship acoustic signals may be used by females in mate assessment as they contain information of male quality such as size and condition. For example, sound-dominant frequency, amplitude, and fatigue resistance may signal body size whereas pulse period (i.e. muscle contraction rate) and calling activity are related with body condition in some species. Some signal features, such as sound pulse number, may carry multiple messages including size and condition. Playback experiments on mate choice of a restricted number of species suggest that females prefer vocal to silent males and may use sound frequency, amplitude, and mainly calling rate when assessing males. The assessment of males by females becomes more challenging when males engage in choruses or when sounds are otherwise masked by anthropogenic noise but almost nothing is known about how these aspects affect mating decisions and fish reproductive success.
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The function of fish sounds in territorial defence, in particular its influence on the intruder's behaviour during territorial invasions, is poorly known. Breeding Lusitanian toadfish males (Halobatrachus didactylus) use sounds (boatwhistles) to defend nests from intruders. Results from a previous study suggest that boatwhistles function as a 'keep-out signal' during territorial defence. To test this hypothesis we performed territorial intrusion experiments with muted Lusitanian toadfish. Subject males were assigned to three groups: muted, sham and unmanipulated. Males were muted by making a cut and deflating the swimbladder (the sound producing apparatus) under anaesthesia. Sham males suffered the same surgical procedure except the swimbladder cut and deflation. Toadfish nest-holder males reacted to intruders mainly by emitting sounds (sham and unmanipulated) and less frequently with escalated fights. When the nest-holder produced a boatwhistle, the intruder fled more frequently than expected by chance alone. Muted males experienced a higher number of intrusions than the remaining groups probably due to their inability to vocalise. Together, our results show that fish acoustic signals are effective deterrents in nest/territorial intrusions, similar to bird song.
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Fish sounds are an important biological component of the underwater soundscape. Understanding species-specific sounds and their associated behaviour is critical to determine how animals use the biological component of the soundscape. Using both field and laboratory experiments we describe the sound production of a nocturnal planktivore, Pempheris adspersa (New Zealand bigeye) and provide calculations for the potential effective distance of the sound for intraspecific communication. Bigeye vocalisations recorded in the field were confirmed as such by tank recordings. They can be described as popping sounds, with individual pops of short duration (7.9 ± 0.3 ms), and a peak frequency of 405 ± 12 Hz. Sound production varied during a 24 h period with peak vocalisation activity occurring during the night, when the fish are most active. The source level of the bigeye vocalisation was 115.8 ± 0.2 dB re 1µPa @ 1m and is relatively quiet compared to other soniferous fish. Effective calling range, or active space, depended both on season and lunar phase, with maximum calling distance of 31.6 m and minimum of 0.6 m. The bigeyes' nocturnal behaviour, characteristics of their vocalisation, source level and the spatial scale of its active space reported in the current study demonstrate the potential for fish vocalisations to function effectively as contact calls for maintaining school cohesion in darkness.
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Blue catfish Ictalurus furcatus Lesueur, the largest catfish in North America, produces pectoral stridulation sounds (distress calls) when attacked and held. They have both fish and bird predators, and the frequency spectrum of their sounds is better matched to hearing of birds than to that of unspecialized fish predators with low frequency hearing. It is unclear whether their sounds evolved to function in air or water. We categorized the calls and how they change with fish size in air and water and compared developmental changes in call parameters with stridulation motions captured with a high-speed camera. Stridulation sounds consist of a variable series of pulses produced during abduction of the pectoral spine. Pulses are caused by quick rapid spine rotations (jerks) of the pectoral spine that do not change with fish size although larger individuals generate longer, higher amplitude pulses with lower peak frequencies. There are longer pauses between jerks, and therefore fewer jerks and fewer pulses in larger fish that take longer to abduct their spines and therefore produce a longer series of pulses per abduction sweep. Sounds couple more effectively to water (1400 times greater pressure in Pascals at 1m), are more sharply tuned and have lower peak frequencies than in air. Blue catfish stridulation sounds appear to be specialized to produce under-water signals although most of the sound spectrum includes frequencies matched to catfish hearing but largely above the hearing range of unspecialized fishes.
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The relation between acoustic signaling and reproductive success is important to understand the evolution of vocal communi-cation systems and has been well studied in several taxa but never clearly shown in fish. This study aims to investigate whether vocal behavior affects the reproductive success in the Lusitanian toadfish (Halobatrachus didactylus) that relies on acoustic communication to attract mates. We recorded 56 nest-holding (type I) males during the breeding season and analyzed the calling performance and acoustic features of the mate advertising sounds (boatwhistles) exhibited over circa 2 weeks. Hormonal levels of the subjects and the number of eggs (reproductive success) present in the respective nests were quantified. Nesting males attracted both females and other males, namely smaller type I males with significantly lower total length (TL), body condition, sonic muscle mass, gonad mass, and accessory glands mass. Calling rate (CR), calling effort (CE) (% time spent calling), and sound dominant frequency were significantly higher in nesting males with clutches than in those without clutches. Sex steroids (11-ketotestosterone and testosterone) were not correlated with vocal parameters or number of eggs. Maximum CR and CE were the best predictors of the number of eggs. In addition, these vocal variables were best explained by male's TL, condition, and sonic muscle mass. We provide first evidence that vocal behavior significantly determines reproductive success in a vocal fish and show that acoustic signaling at higher and constant rates can operate as an indicator of the male's size and body condition and probably of elevated motivation for reproduction. Key words: acoustic communication, Batrachoididae, mate attraction, reproductive success, toadfish. [Behav Ecol 23:375–383 (2012)] INTRODUCTION
Acoustic signalling is a taxonomically widespread form of animal communication consisting of long-range, high-amplitude signals and short-range, low-amplitude signals. Research on acoustic communication has emphasized high-amplitude signals and often overlooked low-amplitude signals, even though they are produced in behavioural contexts that directly influence fitness. Low-amplitude signals are referred to by a variety of names such as soft songs, courtship songs, whispers, close calls, contact calls, grunts and moans, but all of these signals share a reduced amplitude and an active space that is limited to close-proximity receivers. In this review, we establish a general definition for low-amplitude signals and investigate the similarities and differences between low- and high-amplitude signals with respect to their acoustic structure and function. Then, we critically evaluate some proximate and ultimate evolutionary mechanisms that may explain why these signals are produced at low amplitude using examples from a variety of taxa. We conclude by suggesting priorities for future research on low-amplitude signals and highlighting how studying these signals will lead to a more complete understanding of how and why animals communicate acoustically.