Ruppe Et Al 2015 PNAS

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Environmental constraints drive the partitioning of the

soundscape in fishes
Laëtitia Ruppéa, Gaël Clémentb, Anthony Herrelc,d, Laurent Ballestae, Thierry Décampsc, Loïc Kévera,
and Eric Parmentiera,1
a
Laboratory of Functional and Evolutionary Morphology, Applied and Fundamental Fish Research Center, Campus du Sart Tilman Bâtiment B6c, University
of Liège, 4000 Liège 1, Belgium; bCentre de Recherches sur la Paléobiodiversité et les Paléoenvironnements (UMR 7207, CR2P), Sorbonne Universités,
Muséum National d’Histoire Naturelle (MNHN)/CNRS/UPMC-Paris6, MNHN 75231 Paris Cedex 05, France; cMécanismes adaptatifs et évolution (UMR 7179,
MECADEV), MNHN/CNRS, MNHN de Paris, 75231 Paris Cedex 05, France; dEvolutionary Morphology of Vertebrates, Ghent University, B-9000 Ghent,
Belgium; and eAndromède Océanologie, 34280 Carnon-Plage, France

Edited by James H. Brown, University of New Mexico, Albuquerque, NM, and approved March 16, 2015 (received for review December 23, 2014)

The underwater environment is more and more being depicted that signal overlap is avoided (11–15). Moreover, theory predicts
as particularly noisy, and the inventory of calling fishes is con- that the competition for acoustic space should result in signal
tinuously increasing. However, it currently remains unknown how divergence, which would increase signal distinctiveness and op-
species share the soundscape and are able to communicate without portunities for correct signal discrimination (14, 15) and lead to
misinterpreting the messages. Different mechanisms of interference the avoidance of frequency overlap. This strategy predicts that
avoidance have been documented in birds, mammals, and frogs, but signals produced at a given time and in a given place can be
little is known about interference avoidance in fishes. How fish thus distinguished by their frequency. The frequency partitioning of
partition the soundscape underwater remains unknown, as acoustic the acoustic environment was first demonstrated for birds and,
communication and its organization have never been studied at the more recently, also for frogs (2, 16).
level of fish communities. In this study, passive acoustic recordings To date, there is little direct evidence of mechanisms of

ECOLOGY
were used to inventory sounds produced in a fish community signal interference avoidance in fish. At best, it has been shown
(120 m depth) in an attempt to understand how different species that calls of nearby toadfish, Opsanus beta, do not overlap.
partition the acoustic environment. We uncovered an important However, this pertains to specimens of the same species (17).
diversity of fish sounds, and 16 of the 37 different sounds recorded Moreover, O. beta increases its call rate and changes its call
were sufficiently abundant to use in a quantitative analysis. We duration during the twilight period (17). Despite the array
show that sonic activity allows a clear distinction between a diurnal of behaviors associated with sound production, fish sounds
and a nocturnal group of fishes. Moreover, frequencies of signals are mainly used during reproduction (courtship, spawning,
made during the day overlap, whereas there is a clear distinction male competition) or during behaviors related to territoriality
between the different representatives of the nocturnal callers (warning, chase, nest defense, fight). During courtship, calls
because of a lack of overlap in sound frequency. This first demon- can be used by females to assess species identity and the quality
stration, to our knowledge, of interference avoidance in a fish of potential sexual partners (18–21). During agonistic behav-
community can be understood by the way sounds are used. In iors, sound features enable the receiver to assess the fighting
diurnal species, sounds are mostly used to support visual display, capacity of the opponent because acoustic parameters can
whereas nocturnal species are generally deprived of visual cues, provide information on the size, the social status, the motiva-
resulting in acoustic constraints being more important. tion, or the physiological state of the emitter (22–25). However,
how fish sounds are organized at the level of the community
|
acoustic communication signal interference | passive acoustic recordings | remains unknown.
|
diversity of sounds frequency partitioning Passive acoustic recording methods have been developed in
recent years (26) and allow not only the detection of a larger

T he number of studies concerning the soundscape or, more


precisely, studies stressing the need for investigations of the
soundscape in different environments is growing because the
Significance

effect of anthropogenic noise is thought to be problematic for More and more studies stress the potential deleterious effect
many species (1–5). The main reason for this call to action is the of anthropogenic sounds on fish acoustic communication.
crucial role of sound communication in the regulation of dif- Paradoxically, how the communication between fishes in a
ferent kinds of social relationships, as has been demonstrated in community is organized remains extremely poorly known, as
numerous taxa. However, most studies with fish tend to consider studies using passive acoustic recordings are typically restricted
species in isolation, and there is a lack of data addressing to one or two species. At a single site, we were able to follow
acoustic communication of fishes living in natural communities 16 different vertebrate sounds for 15 days. We demonstrate
(6). As a consequence, how species share the soundscape with that the fish population can be distributed into two groups:
other species living in the same habitat remains unknown. This one diurnal and one nocturnal. Most interestingly, fish calling
topic has received much more attention in the air, where many at night do not show overlap at the level of the main calling
mechanisms that animals use to deal with this problem are frequency, in contrast to fish calling during the day. This shows
known (Fig. 1). The Lombard effect, for example, corresponds to that at night, in the absence of visual cues, sound communi-
an increase in signal amplitude. It was first described for humans, cation is more important.
and subsequently in birds, mammals, and fish (5, 7). However,
an increase in signal amplitude is a limited solution when the Author contributions: A.H. and E.P. designed research; L.R., G.C., L.B., T.D., and L.K. per-
background noise level is important. As a consequence, some formed research; L.R. and E.P. analyzed data; and L.R., A.H., and E.P. wrote the paper.
frogs, birds, and mammals also increase the call duration, or call The authors declare no conflict of interest.
rate, to increase the likelihood of being heard (8–10). In complex This article is a PNAS Direct Submission.
acoustic environments, such as animal communities character- 1
To whom correspondence should be addressed. Email: [email protected].
ized by an important quantity of signals, vocalizing animals cope This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
with background noise by inserting their signals in such a way 1073/pnas.1424667112/-/DCSupplemental.

www.pnas.org/cgi/doi/10.1073/pnas.1424667112 PNAS Early Edition | 1 of 6


monitoring, migration studies, and so on. However, most of the
passive acoustic studies have restricted their investigations to the
monitoring of one or two aquatic species or to the description
of acoustic characteristics. The biological sound environment
(soundscape) and its partitioning have rarely been studied in
fish communities, although some studies have reported that fish
share the acoustic space (6, 30–32). As such, the mechanisms
of signal interference avoidance remain unknown and will be
addressed in the present study. In other words, we here ask
ourselves whether fish sound production is a cacophony, or
whether there is an organization of sound production in the
marine environment.
In spring 2013, an autonomous recording device was placed in
a cave at a depth of 120 m off the coast of South Africa that was
sheltering a great species diversity. A census performed in 2006
revealed 70 vertebrate groups including 136 teleost species, the
coelacanth Latimeria chalumnae, and 19 chondrichthyan species
(33). The goal of the present study was to categorize the sounds
Fig. 1. Mechanisms to ensure the signal transfer in the soundscape on land.
to understand how the different species share the acoustic
environment.
number of individuals than by the use of visual methods but Results and Discussion
also a continuous day and night monitoring. Moreover, passive
Description of Sounds. The present analysis concerned 2,793
acoustic recording methods can be used at depths not accessible
sounds. These sounds were divided into 17 groups on the basis of
to humans, independent of weather conditions, and for a long- the similarity in their characteristics (Table 1 and Fig. S1). These
term period (27, 28). These methods are based on the deploy- 17 groups were composed of 25–398 sounds. All the sounds of
ment of one or more hydrophones scheduled to record sounds each group were analyzed, but the inequality between groups
during various periods in the natural habitat. These methods makes the statistical analysis of these data complex. Thus, a ran-
have been successfully used to demonstrate temporal partition- dom sample of 10 sounds for each group was taken and analyzed.
ing by several cooccurring species (29). Passive acoustic methods The acoustic features of each sample and its corresponding group
have many applications in the field of conservation, population were statistically compared, and no significant differences for any

Table 1. Mean values of measured acoustic parameters for the 17 groups


Pulse Pulse period,
Group Total duration, s Peak frequency, Hz number pulse·s−1 General pattern

1 0.33 ± 0.12 490 ± 281 6.80 ± 2.25 23.11 ± 11.67 One pulse followed by a train of around six pulses
(pulse period: 50 ms). Sometimes, the previous pulse is absent
2 0.65 ± 0.09 480 ± 227 28.82 ± 4.49 44.75 ± 6.79 Two parts. The first one is composed of around 20–25 pulses
(pulse period: 10–15 ms). The second part is around five pulses
(pulse period: 30–35 ms)
3 0.07 ± 0.02 2,803 ± 277 2.20 ± 0.42 33.72 ± 7.83 Two or three clear pulses separated by 45–50 ms
4 0.16 ± 0.03 66 ± 5 1.00 ± 0 — Isolated boom
5 0.08 ± 0.05 158 ± 69 1.00 ± 0 — Isolated pulse
6 1.16 ± 0,31 274 ± 137 4.10 ± 0.74 3.65 ± 0.68 Coarse pulses with a small growl at the front of the pulse
(pulse period: around 200 ms)
7 0.78 ± 0.25 762 ± 122 4.50 ± 0.97 6.04 ± 1.26 Long pulse. High-frequency whistle.
8 1.14 ± 0.36 1,630 ± 401 10.30 ± 3.33 9.27 ± 1.71 Three or four groups of pulses separated by around 250 ms.
The first one is often composed of one pulse, and the next
groups of three to four pulses (pulse period: around 10–15 ms)
9 1.08 ± 0.64 2,641 ± 257 6.70 ± 3.27 6.38 ± 0.60 Clear pulses, regular
10 0.51 ± 0.12 162 ± 102 4.70 ± 1.16 9.33 ± 1.55 Coarse pulses grouped with a number of pulses, increasing
for the next one
11 0.82 ± 0.35 429 ± 267 19.80 ± 7.76 25.16 ± 6.29 Pulses separated by around 50 ms. Amplitude relative variation:
increase then decrease
12 0.35 ± 0.15 446 ± 299 16.82 ± 4.96 52.87 ± 15.44 One large pulse followed by smaller pulses with an increasing
pulse period
13 1.49 ± 0.70 1,088 ± 214 5.10 ± 2.18 3.58 ± 0.60 Series of grunts
14 1.30 ± 0.23 263 ± 114 Tonal — Long tonal sound with an increasing of the intensity.
At the end, some more isolated pulses are observable
15 0.49 ± 0.08 290 ± 198 6.90 ± 1.20 14.26 ± 2.35 One or two pulses grouped following by a train of around
eight pulses. Sometimes the first group of pulses is
absent
16 1.65 ± 0.74 427 ± 204 4.1 ± 1.20 2.75 ± 0.93 Clear pulses
17 0.24 ± 0.13 1,056 ± 151 6.4 ± 3.37 27.13 ± 2.53 Coarse pulses in regular series

Values are mean ± SD. An oscillogram is presented in Fig. S1 for each group.

2 of 6 | www.pnas.org/cgi/doi/10.1073/pnas.1424667112 Ruppé et al.


number of pulses: χ2 = 149.6; df = 16; P < 0.001; peak fre-
quency: χ2 = 141.2; df = 16; P < 0.001; sound duration: χ2 =
144.7; df = 16; P < 0.001). The results of the honest significant
difference (HSD) Tukey post hoc tests show that, in most cases,
groups are distinguishable by their acoustic parameters (Table
S1). However, a minority of groups are not distinct (such as 1
and 15 or 6 and 16).
A discriminant function analysis was then performed to
complement the principal component analysis. A mean cross-
validation matrix was calculated after 1,000 cross-validation
tests. In addition, the discriminant function analysis was per-
formed on random groups (all sounds were mixed, and 17
groups created randomly). After the cross-validation test, 70%
of sounds were correctly assigned to their group (Table S2),
which is significantly greater than expected by chance (χ2 test:
χ2 = 51.11; df = 16; P < 0.001). Fig. 2 represents the confu-
sion matrix obtained from the result of the cross-validation
tests. The confusion matrix diagonal is well discerned (>50%
of correct assignment) with the exception of groups 1, 6, 13,
and 16. For these latter groups, the acoustic parameters are
not sufficient to distinguish the sounds. However, sound
description is not only restricted to the data used in the analysis;
Fig. 2. Confusion matrix summarizing the result of the cross-validation it appears other features allow support of group validity. Groups
discriminant function analysis test. The horizontal axis represents the actual 1 and 15 were confused by the model; for these two groups, the

ECOLOGY
group to which the sound belongs, and the vertical axis represents the as- general pattern of sound (oscillogram shape) is similar, but the
signment of a sound to a group by the model. The more yellow the color, the hours of activity are opposed (sounds of group 1 occur mainly
higher the proportion of correct assignments (Table S2).
during the day, whereas sounds of group 15 occur mainly at
night). Two hypotheses can be proposed: these sounds are pro-
of the acoustic parameters were found (Wilcoxon test, P > 0.05 in duced by two different species, one diurnal and one nocturnal,
all cases), showing each sampling is representative and does not thus avoiding acoustic interference, or these sounds are pro-
duced by a single species with a large activity period. At this
influence the results. Statistical analyses were performed to
point, we cannot distinguish between these two possibilities.
estimate the validity and consistency of these groups. In a prin-
Some sounds belonging to group 6 were assigned to group 16
cipal component analysis, ∼71.1% of the variability is explained by the model. The general pattern of these two groups is, how-
by the first two principal components (43.2% by principal com- ever, different. Sounds belonging to group 6 show long pulses
ponent 1 and 27.9% by principal component 2). Principal com- with small growls, whereas sounds belonging to group 16 are
ponent 1 describes the pulse period and the number of pulses. composed of clear and short pulses (Table 1 and Fig. S1). These
The second component describes the sound duration and the sounds cannot be produced by an identical mechanism, and thus
peak frequency. All groups are homogeneous, and Kruskal not by the same species. The same holds for group 13 (sounds of
Wallis tests were significant for each acoustic parameter be- “grunt” type), from which some sounds were assigned to group 7
tween groups (pulse period: χ2 = 161.2; df = 16; P < 0.001; (sounds of “whistle” type).

Fig. 3. Distribution of the different groups during the day. Daytime was between 05:00 and 16:30. Each group is represented by its relative percentage of
presence per hour. The longer the rectangle, the more likely the presence of the group at this hour is.

Ruppé et al. PNAS Early Edition | 3 of 6


between 05:00 and 17:00. During our recording, the sun rose
around 06:30, and sunset was around 17:30. This is compatible
with our result because many species deploy peaks of activities
around these periods of the day, and there is not a strict limit (40,
41). The diurnal group is composed of calls 1, 3, 5, 10, 11, 12, 13,
and 16. At 17:00, there is a drastic change in the acoustic envi-
ronment. Between 17:00 and 05:00, a nocturnal group of callers
is being established and is composed of calls 6, 7, 8, 9, 14, and 15.
Calls 2, 4, and 17 occur during both night and day, but call 2
presents its maximal activity during the daytime, whereas the
maximal activity of call 4 is during the nighttime. Call 17 shows
only a restricted activity at sunrise.
The division of the calls into two distinct groups can be re-
lated to environmental constraints and the need for different
kinds of strategies to avoid species misidentification by the
receiver. To study the sound overlap between calls within each
group, different analyses were performed, using the calls that
are most representative: calls 1, 2, 3, 10, 11, and 12 for the
diurnal group and calls 4, 6, 7, 8, 9, and 15 for the nocturnal
group. These calls represent 90% of the total vocal activity.
Data pertaining to frequency and pulse periods were used be-
cause these characters are usually involved in the coding of
information (42, 43). Within the diurnal group, sounds pro-
duced by different species overlap at the level of the pulse
period and frequency (Fig. 4). In this group, only call 3 con-
stitutes an exception, showing high pulse periods and high peak
frequencies, which are acoustic characters known from ceta-
ceans. In contrast, these acoustic parameters allow a clear
distinction between the different representatives of the noc-
turnal group (Fig. 4). This distinction is mostly a result of dif-
Fig. 4. Overlap analysis on the diurnal community (Upper) and the noc- ferences in peak frequencies, as there is little overlap between
turnal community (Lower) in terms of peak frequency and pulse period. Note sounds produced by nocturnal species (Fig. 5).
that whereas sound characteristics overlap strongly during the day, calls are In diurnal fishes, sounds are often associated with a particular
clearly separated by frequency and pulse period at night. behavior to reinforce visual stimuli. For example, courtship in
Dascyllus (Pomacentridae) species is characterized by consecu-
tive dances (called dips) performed by the courting male and by
In summary, 17 groups of sounds can be clearly distinguished, modifications of the color pattern. The male rises first in the
and each would therefore at best represent a sound-producing water column and then falls off, rapidly emitting a pulsed sound
marine species. Note, however, that some species are able to (42, 44). In gobiids, the sound can be accompanied by nodding
produce different kinds of sounds (34). Fish sounds are mainly movements (45). In contrast, visual stimuli cannot be used to
characterized by low frequencies (<1,000 Hz), are limited in transfer information in nocturnal fishes. This implies greater
intensity, and are pulsed and produced routinely for long periods constraints on the acoustic channel, with the need to be able to
of time during the day (27). All groups have the characteristics of distinguish species on the basis of sound only. The use of dif-
fish sounds with the exception of group 3. This group presents a ferent frequencies should allow the fish to identify conspecifics
very fast pulse rate and a high frequency (>2,500 Hz). These and allows for the simultaneous presence of the calls of different
characteristics are reminiscent of cetacean clicks. Calls of group species without generating crosstalk.
9 also have high frequencies (>2,500 Hz). However, these calls
were recorded continuously from 17h00 to 04h00, highlighting Conclusion
that they were produced by sedentary species living permanently The use of passive recording methods highlighted an important
in or around the cave. These data indicate it cannot be cetacean diversity of sounds produced by fishes at a depth of 120 m off the
clicks, the sound emission of which is more sporadic. Therefore, coast of Sodwana Bay, southeastern South Africa. Sixteen dif-
the acoustic analysis allowed us to identify 16 different fish-like ferent fish sounds were described. The analysis of the temporal
sounds and one cetacean-like sound (group 3). The important occurrence of these sounds shows the partitioning of the acoustic
number of different sounds obtained here highlights the incred- window with a diurnal and a nocturnal pattern. During the day,
ible diversity of sounds produced in the aquatic environment, the different sounds overlap at the level of the pulse period and
particularly in a relatively deep-water habitat. The fact that frequency. In contrast, there is a clear distinction between the
sounds were recorded at a depth of 120 m explains why it was different representatives that call at night, where species do not
impossible to visually identify the calling species, and additional overlap in frequency characteristics. This call partitioning at
studies are required to identify the species producing the calls.
night could help prevent signal interference and likely compen-
Comparisons of our acoustic data with the literature suggest
sates for the lack of visibility.
groups 2 and 14 could belong to Batrachoididae (35–37), groups
1 and 15 to Holocentridae (38), and group 4 to the serranid Materials and Methods
genus Epinephelus (39). Study Site. The study was conducted at Sodwana Bay, KwaZulu Natal Province,
Ezemvelo Nature Reserve, Isimangaliso Wetland Park, southeastern South
Frequency Partitioning of the Acoustic Environment. For each group, Africa. Twelve large and many small submarine canyons running along a stretch
the probability of its presence in the recording files was calcu- of coastline ∼78 km in length characterize this area. The canyons are oriented
lated. Two distinct groups could thus be highlighted (Fig. 3): a perpendicularly to the shoreline and can reach more than 700 m in depth (46).
nocturnal group and a diurnal group. The diurnal group is active The specificity of these canyons is the presence of numerous moderate-sized

4 of 6 | www.pnas.org/cgi/doi/10.1073/pnas.1424667112 Ruppé et al.


ECOLOGY
Fig. 5. Mean peak frequency distribution between the nocturnal community and diurnal community at each hour. The center of the rectangles represents
the mean peak frequency of the group. The SD is represented by the vertical extent of rectangles. In the legend, the name of the group is associated with
letters representing the significant difference. Two groups sharing a letter have no significant difference in peak frequency. A difference is considered
significant when P < 0.05.

caves sheltering many species, including coelacanths. The device was placed in Statistical Analyses. A principal component analysis and a discriminant
a submarine cave (called U-cave or cave 2) localized at 113 m in depth at the function analysis were conducted to discriminate and determine the validity
head of the Jesser Canyon, about 4 km from the shoreline. of our sound groups. These tests were coupled to Kruskal Wallis tests, χ2 test,
and Tukey HSD post hoc tests. To study the emission of sounds during
Acoustic Recordings. The Digital SpectroGram Recorder system is an auton- daytime and nighttime, the same tests were used. A nonparametric test on
omous acoustic recording system. It enables users to save acoustic recordings paired data (Wilcoxon test) was used to justify the use of a raw data sample.
on a 32-GB SD memory card and is controlled by an on-board real-time clock.
All these tests were conducted with R i386 3.0.2 software.
In this study, a Digital SpectroGram Recorder system (Loggerhead In-
struments) was positioned in a crevice of the submarine cave wall. Sounds
ACKNOWLEDGMENTS. We thank the team of Gombessa 2013, in particular
were recorded for 9 min every 10 min by the hydrophone (−186 dB re 1V/μPa,
Florian Holon, Tybo Rauby, and Yannick and Cédric Gentil, for the equip-
sample rate of 20 kHz) during a total of 19 nonconsecutive days from April ment and the implementation of the device. We thank Frédéric Bertucci,
through May 2013. Files were automatically saved with temporal data. A total Bruno Frédérich, and Damien Olivier for logistical support and useful discus-
of 2,273 acoustic files were recorded during this study. Given the large number sions. We also thank to Peter Timm, Adele Stegen, and the Triton Experience
of files, only the first 9 min of each hour were analyzed (387 files). Acoustical diving team for their effective assistance during the dives. We are grateful to
analyses were conducted manually with Avisoft-SASLab Pro-5.2.07 software. the scientific teams of the South African Institute for Aquatic Biodiversity
For each distinct sound, the following acoustic parameters were measured: and of the South African National Biodiversity Institute. Thanks are also
total sound duration (s), number of pulses, pulse period (i.e., the ratio between owed to the iSimangaliso Wetland Park Authorities for permission to dive in
the park. This work was supported by the MNHN funding sources via Crédits
the pulse number and the sound duration, in pulses per second), and the peak
Recherche, Soutien pour les Expéditions scientifiques, ATM Formes, and by the
frequency in hertz (i.e., the frequency of greatest amplitude). The temporal CNRS via Labex BCdiv Biological and Cultural diversities. We also thank la
features were measured from oscillograms (44.1 kHz, 16 bit), whereas the Société des Amis du Muséum et du Jardin des Plantes, Association de Retrans-
peak frequency was obtained from the logarithmic power spectra (Hamming mission Télévisuelle Européenne France Télévision, and the Manufacture de
window, FFT Fast Fourier Transform, FFT Length 64, 689-Hz resolution). Haute Horlogerie Blancpain.

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