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First Results of an Underwater 360° HD Audio-Video Device for Etho-Acoustical Studies on Bottlenose Dolphins (Tursiops truncatus)

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Bottlenose dolphins (Tursiops truncatus) are highly social odontocetes that live in a fission-fusion society and demonstrate production of a varied sound repertoire, including clicks, whistles, and burst-pulsed sounds, as well as a diverse behavioral repertoire. To better understand the species’ behavior, it is necessary to compare visual and acoustic observations and link vocalizations to individuals and their specific actions. However, the task of linking sounds to individual dolphins is challenging for human observers because dolphins do not always display specific visual cues when producing a sound, and also because human hearing is not naturally adapted to locate underwater sound sources. To respond to these challenges, a new underwater 360° HD audio-video device, the BaBeL, was designed and built. This device consists of a five-hydrophone array attached to two wide-angle video cameras that together cover a 360° field of vision. Acoustic recordings were analyzed with a customized program to detect and localize sound sources and to identify individual vocalizing dolphins. Data from a population of bottlenose dolphins were collected during 14 boat surveys along the northwest coast of Reunion Island (France) by following a strict pre-established protocol to standardize data collection. A total of 21 min of audio-video were recorded when dolphins were present, and 42 click trains and 42 whistles were detected from these data. Dolphins identified as vocalizers were also present for 17% (n = 7) of emitted click trains and 33% (n = 14) of emitted whistles on the videos. Therefore, an analysis of three video sequences as examples of the scope of this methodology is presented. The results show that when the observers stayed ahead and avoided the direct path of groups of five to nine dolphins, only one animal emitted click trains while swimming towards the observers or after turning its rostrum in the humans’ direction, and this dolphin was never the one leading the group. The benefits of using this audio-video device for underwater observations of dolphins in clear water with good visibility are discussed.
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Aquatic Mammals 2017, 43(2), 162-176, DOI 10.1578/AM.43.2.2017.162
First Results of an Underwater 360° HD
Audio-Video Device for Etho-Acoustical Studies on
Bottlenose Dolphins (Tursiops truncatus)
Juliana Lopez-Marulanda,1 Olivier Adam,1, 2 Torea Blanchard,1, 3 Marie Vallée,4
Dorian Cazau,5 and Fabienne Delfour3, 6
1Institute of Neurosciences Paris Saclay, CNRS UMR 9197, University Paris Sud, Orsay, France
E-mail: juliana.lopez-marulanda@u-psud.fr
2Sorbonne Universités, UPMC Univ Paris 06, CNRS UMR 7190, Institut Jean Le Rond d’Alembert, F-75005 Paris, France
3Parc Astérix, Plailly, France
4Association Abyss, La Réunion, France
5ENSTA Bretagne Lab-STICC, CNRS UMR 6285, Université Européenne de Bretagne, Brest, France
6Laboratoire d’Ethologie Expérimentale et Comparée EA 4443 (LEEC), Université Paris 13,
Sorbonne Paris Cité, F-93430 Villetaneuse, France
Abstract presented. The results show that when the observers
stayed ahead and avoided the direct path of groups
Bottlenose dolphins (Tursiops truncatus) are highly of five to nine dolphins, only one animal emitted
social odontocetes that live in a fission-fusion soci-click trains while swimming towards the observers
ety and demonstrate production of a varied sound or after turning its rostrum in the humans’ direc-
repertoire, including clicks, whistles, and burst- tion, and this dolphin was never the one leading
pulsed sounds, as well as a diverse behavioral the group. The benefits of using this audio-video
repertoire. To better understand the species’ behav-device for underwater observations of dolphins in
ior, it is necessary to compare visual and acoustic clear water with good visibility are discussed.
observations and link vocalizations to individuals
and their specific actions. However, the task of Key Words: behavior, acoustics, hydrophone
linking sounds to individual dolphins is challeng-array, acoustic localization, bottlenose dolphin,
ing for human observers because dolphins do not Tursiops truncatus
always display specific visual cues when producing
a sound, and also because human hearing is not nat-Introduction
urally adapted to locate underwater sound sources.
To respond to these challenges, a new underwa-Bottlenose dolphins (Tursiops truncatus) are
ter 360° HD audio-video device, the BaBeL, was highly social odontocetes with a fission-fusion
designed and built. This device consists of a five- social structure (Connor et al., 2000; Mann et al.,
hydrophone array attached to two wide-angle video 2000; Gibson & Mann, 2008; Tsai & Mann, 2013).
cameras that together cover a 360° field of vision. Group members may travel very short or very
Acoustic recordings were analyzed with a custom-long distances within a habitat of limited visibil-
ized program to detect and localize sound sources ity (Connor et al., 1998). As such, communication
and to identify individual vocalizing dolphins. Data via acoustic signals is the most effective strategy
from a population of bottlenose dolphins were col-for sharing information under water (Janik, 1999).
lected during 14 boat surveys along the northwest Bottlenose dolphins display a complex and exten-
coast of Reunion Island (France) by following a sive repertoire of sounds such as clicks or pulsed
strict pre-established protocol to standardize data sounds (Au, 1993; Au & Fay, 2012), burst-pulsed
collection. A total of 21 min of audio-video were sounds (Lopez & Bernal-Shirai, 2009), and whis-
recorded when dolphins were present, and 42 click tles or tonal sounds (reviewed in Janik, 2009).
trains and 42 whistles were detected from these Dolphin sound production is enriched by non-
data. Dolphins identified as vocalizers were also acoustic communication signals during social
present for 17% (n = 7) of emitted click trains and interactions when individuals are within visual
33% (n = 14) of emitted whistles on the videos. range of one another. These animals display vari-
Therefore, an analysis of three video sequences ous body postures (Pryor, 1990), contacts (Sakai
as examples of the scope of this methodology is et al., 2006; Dudzinski et al., 2009), and bubble
163360° HD Audio-Video Device to Observe Dolphins
emissions (Marten et al., 1996). Several dolphin dolphin. Four hydrophones are needed to local-
vocalizations are associated with behavioral con-ize a moving dolphin in 3D (Watkins & Schevill,
texts; for example, burst-pulsed sounds (squawks 1972; Wahlberg et al., 2001)
and whines) have been associated with agonistic Mobile arrays of two (Dudzinski et al., 1995),
behaviors (Herzing, 1996), and low-frequency four (Au & Herzing, 2003; Schotten et al., 2004),
bray calls are related to feeding (Janik, 2000; and 16 (Ball & Buck, 2005) hydrophones have
King & Janik, 2015). been used to study dolphin vocalizations and
Studies of dolphin social behavior and commu-their associated underwater behaviors, but they,
nication rely on simultaneous descriptions of both too, presented several disadvantages. Dudzinski
visual and acoustic signals (Thomas et al., 2002). et al.’s (1995) system did not allow localization in
However, the main obstacle associated with com-the vertical axis, and the systems with four hydro-
pleting these descriptions is the difficulty in iden-phones were used only for localization of click
tifying which dolphin in a group is the vocalizer. emitters (Au & Herzing, 2003; Schotten et al.,
This challenge is caused by two factors: (1) human 2004). The 16-hydrophone array had elements
hearing is not adapted to localize to sound sources separated by 3.2 cm (Ball & Buck, 2005) but did
underwater; and (2) dolphins do not show visible, not allow the confirmation of the emitter’s iden-
regular signs when emitting sounds, like opening tity if animals were located outside of the narrow
their mouths or displaying external clues (Janik, angle of the video camera.
2009). To overcome these obstacles, several meth-As part of this study, an audio-video system
odologies have been developed. Animals have been that was non-intrusive and compact enough to be
isolated (Caldwell et al., 1990; Sayigh et al., 1990) deployed from a small boat was developed. This
or tagged (Tyack, 1991; Nowacek et al., 1998); underwater device includes five hydrophones and
however, these approaches can be considered inva-a 360° HD video recording system with a lim-
sive and might lead to modification of the subjects’ ited blind spot that allows localization of sounds
behaviors and vocalizations. Emission of bubble to free-swimming, vocalizing dolphins coming
streams concurrent with vocalizations has been from almost every direction. In this article, details
used to identify a vocal animal because sometimes about this system’s design and the software devel-
dolphins emit bubbles while whistling (McCowan oped to localize to sounds and to link them to indi-
& Reiss, 1995; Herzing, 1996); however, whistles vidually identified dolphins are provided. Three
with bubble streams are not representative of the audio-video sequences of free-ranging bottlenose
entire whistle repertoire of bottlenose dolphins dolphins have been analyzed to illustrate the ben-
(Fripp, 2005, 2006). efits of this system in dolphin ethological and
As a non-intrusive method to identify the acoustical research.
vocalizing animal, different hydrophone arrays
have been designed. These arrays allow for pro-Methods
cessing of the differences in time of arrival of the
sound to each hydrophone to determine where Recording Device
the call originated. The position of the sound Simultaneous audio and video recordings were
source is linked to the video recordings to con-collected using a waterproof audio-video system
firm which animal is in the same position as the named BaBeL (BioAcoustique, Bien Être et
sound source, thereby identifying the vocalizer. Langage) (Figure 1). The acoustic set-up was
Fixed arrays using two (López-Rivas & Bazuá- comprised of five calibrated Aquarian H2a-XLR
Durán, 2010), three (Watkins & Schevill, 1974), hydrophones connected and synchronized to a
four (Brensing et al., 2001; Quick et al., 2008), ZOOM H6 digital audio recorder. Audio record-
and eight (Thomas et al., 2002) hydrophones have ings were made at a 96-kHz sampling frequency
been used to link audio recordings to behavioral and coded on 24 bits. The recorder was placed in
observations or video recordings; however, fixed a waterproof housing rated to 60 m depth. The
arrays are not well adapted to study highly mobile, architectural design of the hydrophone array was
free-ranging dolphins, and the video recordings a compromise between a large aperture between
were often obtained from a fixed point at the sur-hydrophones and maneuverability since the
face. The main problem with acquiring behavioral system needed to be deployed from small boats
information from the surface is that the docu-with limited space and to be controllable by one
mented behaviors could possibly represent only a observer when submerged. The synchronized
very small percentage of an animal’s behavioral hydrophones were positioned to obtain the time
activity (Janik, 2009). Moreover, an array with delay of arrival to provide the 3D estimations of
two hydrophones (Lopez-Rivas & Bazuá-Durán, dolphin positions.
2010) allows data to be obtained only on the angle The video portion of the BaBel system was
of arrival and not the real position of the emitting comprised of two Kodak SP360 video cameras
164 Lopez-Marulanda et al.
both with a wide-angle field of view (214°); the method used the spatial distribution of hydro-
cameras were placed opposite of each other to the phones, the acoustic properties of the source
left and the right to allow for 360° field of vision (e.g., propagation speed and spherical propaga-
for the system. These cameras were positioned tion model), and the measure of the time differ-
below the waterproof housing of the acoustic ences of arrival (TDOA) of the acoustic wave
recorder (Figure 2). Video and audio files were from the source to the different hydrophones
stored for a posteriori analysis. (Alameda-Pineda & Horaud, 2014). The aim
was to estimate the differences in time of arrival
Custom-Made Program for Data Analysis of emitted sounds; the cross-correlation function
A geometrical localization method was used to method for whistle detection (Van Lancker, 2001)
estimate the position of an acoustic source. This and the threshold time energy for click detection
Figure 1. BaBeL (BioAcoustique, Bien Être et Langage) device: (a) Diagram and orientation of hydrophones (H); and
(b) picture of the device with 360º cameras unattached—five hydrophones installed on five deployable arms and plugged to
a ZOOM H6 (inside the adapted waterproof case).
165360° HD Audio-Video Device to Observe Dolphins
(Blanchard, 2015) were used. To display the esti-
mated position of the acoustic source in the video
image, a conversion position-pixel that took into
account the deformations of the image because
of the spherical curved lens of the Kodak SP360
video cameras was used. With these consider-
ations, a customized program to analyze data
obtained with the BaBeL system was created in
MATLAB®, Version 2013a (Mathworks, Natick,
MA, USA) to synchronize the video and audio
recordings and then to estimate the localization(s)
of each vocalizing dolphin (Blanchard, 2015)
(Figure 3). After identifying the location of the
vocalizing dolphin, video analysis allowed for the
identification of the dolphin based on recogniz-
able scars and marks.
Tests with Artificial Sounds
Two simulated whistles to test this approach with
different signal-to-noise ratios (SNRs) (Figure 4)
were created. The objective of this test was to
confirm performance of the time correlation
for acoustic signals deteriorated by underwater
acoustic propagation or when ambient noise is
present in the marine area. To verify our local-
ization method, the system was tested in a 3.1 ×
8.2 m² rectangular freshwater swimming pool.
The BaBeL was immersed in the center of the
Figure 2. Disposition of two Kodak SP360 video cameras.
Each camera has a 360° (N-S-E-W) plus 214° angle of
view. As both cameras are placed opposite to each other,
there is a 34° overlap in the images and a 50-cm blind
spot between the cameras.
Figure 4. Simulated whistles with two signal-to-noise ratios (SNRs): (a) +20 dB and (b) -10 dB.
166 Lopez-Marulanda et al.
pool at 2.5 m from the edge. Percussive sounds Bottlenose Dolphin Data Collection
were generated by knocking together two steel
Acoustic and video data were collected on free-
bars from nine different known places in the hori-
ranging bottlenose dolphins along the northwest
zontal plane of the deviceʼs gravity center. Using
coast off Reunion Island, a French territory in the
the position-pixel conversion, the position of each
Mascarene Islands in the Southwest Indian Ocean.
percussive sound source in the video image was
The species is observed in this location through-
estimated and compared to the location estimated
out the year in groups of 10 to 100 individuals (48
by the custom program.
individuals on average) and occurs in deeper water
Figure 4. Screen display to track dolphins by videos and passive acoustics. On the bottom left, estimations of the angles from
the successive clicks (in blue) and the whistle (in red). On the right, the red cross points to the emitter dolphin.
Figure 5. Disposition of BaBeL device in the water; the whole system is controlled by Observer 1. The vision range of the
camera depends on water clarity. For the Reunion Island, it is ≈10 m. The real scales are not represented in the figure.
167360° HD Audio-Video Device to Observe Dolphins
(425.6 m on average) and further offshore (1.2 to
Audio-Video Analysis
6 km from the coast) than other cetacean species in
The claps at the beginning of each recording ses-
this area (Dulau-Drouot et al., 2008).
sion were used to manually synchronize acoustic
Fourteen boat surveys were conducted from and video data with video editing software (Final
21-29 May 2015 and from 6-18 June 2015 to Cut Pro X, Version 10.1.3©, Apple Inc.). A single
search for bottlenose dolphins and collect etho- video file was created displaying the videos of
acoustical data. When a group of dolphins was the two Kodak SP360 video cameras in the same
sighted, a strict pre-established protocol was fol-window, as well as one of the five audio tracks and
lowed (see Agreement on the Conservation of its corresponding turning spectrogram (FFT size:
Cetaceans in the Black Sea Mediterranean Sea 1,024, overlap 50%, Hanning window) obtained
and Contiguous Atlantic Area [ACCOBAMS], with Audacity, Version 2.0.6 (GNU General
Resolution 4.18) to decide if observers would Public License). We chose only one track in the
enter the water to start a recording session. First, video as a referent since the five audio tracks were
the boat was positioned parallel to the animals’ used for our custom-made acoustical analysis in
travel direction at a distance of more than 50 m. MATLAB® (Blanchard, 2015).
The behavioral response of the dolphin group was The location of the vocalizing dolphin was
recorded into one of three categories: (1) “avoid-noted as “visible” when our program was able to
ance,” (2) “indifference,” and (3) “oncoming” point out one of the dolphins in the video, “ambig-
(see ACCOBAMS for definitions). If the behav-uous” when the program pointed out two dolphins
ioral response was cataloged as “indifference” that were close to each other or in the same direc-
or “oncoming,” the boat was slowly positioned tion, and “not visible” when the program pointed
100 m ahead of the first animal of the group, never to another direction indicating that the emitter
interfering with the travel direction of the animals. dolphin was far outside the range of vision of the
Once in this position, two observers slipped into video cameras, estimated at further than 10 m
the water. away in all directions but also dependent on the
Procedure in Water—One observer swam with wide-angle lens (reduces the size of objects) and
the BaBeL device submerged below the sea sur- water clarity.
face (≈1 m under the surface) (Figure 5), while the To conduct our etho-analysis, the sequences in
other observer recorded the animals on a backup which we could locate with no doubt at least one
SONY HDR-GW66 video camera. Date and time vocalizing dolphin were selected (see Appendix 2,
on all video cameras were synchronized for a pos-Figure 1); a focal-animal sampling technique was
teriori analysis. Since BaBeL was being operated used to note occurrence and duration of body
for the first time, the intent was to document all postures, tactile contacts, and other behaviors
the events. The backup video sequences might be displayed during intraspecific interactions and
used later to confirm what was observed on the during interactions towards humans in video
BaBeL wide-angle cameras, and the recorded sequences (Altmann, 1974; Mann, 1999). Since
sequences might be replayed to document the all sightings were mainly “swim by” wherein
BaBeL operator’s position and behavior in the the dolphins did not remain near the observers
water. for long, individual dolphins in each sequence
At the beginning of the recording session, two were listed in order of appearance in the video.
successive claps were made—one in front of each The “all occurrences” recording sampling method
camera in order to synchronize both videos with focused on frequencies, and durations of occur-
audio recordings during the a posteriori analysis. ring behaviors was used (Martin et al., 1993).
Both observers remained floating at the surface The analyzed sequences allowed the researchers
with their bodies oriented perpendicular to the to create a behavioral catalog (Tinbergen, 1963),
group’s travel direction, avoiding the direct path which included nonsocial and social (intraspecific
of the dolphins and letting the animals choose at and human-dolphin interactions) behaviors and
what speed and distance they approached. When sounds produced (Table 1).
dolphins slowly moved along the observers,
they swam calmly in parallel with the animals. Results
Depending on whether the dolphins stayed around
the observers or departed, recording sessions Tests with Artificial Sounds
were repeated several times on the same group by As this study is dedicated to the analysis of behav-
carefully re-orienting the boat and by informing iors, only situations when at least one dolphin was
the observers each time the dolphins swam by. A visible in the videos, at a distance of less than
recording session finished when dolphins were 10 m, were taken into account. If this dolphin
not visible for 5 min or when weather conditions emitted clicks and/or whistles during a period
prevented continued observations. with no underwater noise, then the SNR ratio
168 Lopez-Marulanda et al.
was higher than 20 dB. If the dolphin vocalizes one bottlenose dolphin body length. For distances
further away, SNR decreased and could be nega-from the device, the error of the custom program
tive. We performed our approach for positive and was 1.1 to 3.9 m (Table 3).
negative SNR (Table 2). The time differences of
arrival (TDOAs) were still correctly estimated for Data Description
SNR larger than -10 dB, which is acceptable for During 14 boat surveys, dolphins were sighted
our study because underwater noise was low com-four times, allowing collection of 21.03 min of
pared to dolphin sounds. (SNR was always posi-360° HD audio-video data with dolphins pres-
tive in our acoustic recordings.) ent. Recordings allowed the detection of 42 click
Results of the first test comparing estimations of trains and 42 whistles. The vocalizing dolphin
positions in video and audio show that differences was localized and visible on the video for seven
in estimation for azimuthal localizations are less click trains (17%). The vocalizer was not visible
than 12° except for in positions 3 and 4 (Table 3). for 25 click trains (59%); and for 10 click trains
For elevation localizations, the difference is less (24%), localization of the vocalizer was ambigu-
than 10°, except for in position 8. Positions 3, 4, ous. For whistles, localization analysis was not
and 8 can only be seen right on the edge of the possible for five whistles (12%) because of a low
image, making estimations more difficult due to SNR ratio. The vocalizing dolphin was visible on
image compression. Taking into account that the the video for 14 whistles (33%), the vocalizer was
maximal vision range of the BaBeL is estimated to not visible on the video for 18 whistles (43%), and
be 10 m depending on water clarity, a 10° differ-the localization of the vocalizer was ambiguous
ence in estimations from video and audio means for five whistles (12%).
that localization at 10 m from the BaBeL can have Three recording sessions (24 May at 0937
a maximum difference of 1.7 m from the posi-and 0949 h, and 27 May at 1316 h) were chosen
tion of the source in the video, which is less than during which it was possible to localize the
Table 1. Behavioral catalog of the dolphins observed while swimming by observers and documented with the BaBeL device
Behaviors Code Definition
Pectoral rubbing PR The dolphin touches another dolphin.
Synchronized swimming SyS Dolphins swim in synchronous manner within one body length of another dolphin,
showing parallel movements and body axes.
Swim upside down SUD The dolphin swims with its belly turned up.
Swim upside down
underneath
SUDU The dolphin swims with its belly turned up underneath a conspecific.
Side swimming SS The dolphin swims with its belly turned to the right or the left next to a conspecific.
Approach APP The dolphin approaches the observers by leaving the direction axis of its group.
Swim towards observers STO The dolphin swims towards the BaBeL device and the observers.
Turn rostrum TR The dolphin turns its rostrum in the direction of an observer.
Leave L The dolphin stops swimming towards the observers and starts to move away.
Whistle W The dolphin whistles.
Click train C The dolphin emits a click train.
Table 2. Accuracy of the time correlation on simulated signals
Simulated signal Features SNR = 20 dB SNR = -10 dB
Whistle #1 Duration: 0.1 s
Fundamental: 11 kHz
ΔTDOA = 0 ΔTDOA = 1.8 ms
Whistle #2 Duration: 0.5 s
Fundamental frequency 11 kHz
switch to 16 kHz at 0.35 s
ΔTDOA = 0 ΔTDOA = 0
169360° HD Audio-Video Device to Observe Dolphins
dolphin vocalizing to facilitate completion of neutral buoyancy, maneuverability, and simplic-
detailed analyses of dolphin behavior according to ity of deployment simultaneously. The BaBeL
the behavioral catalog (Table 1; see Appendix 1). is relatively easy to deploy from small boats to
Results show that the first animal of the group record behavior and acoustic data on free-ranging
to approach the observers did not produce click dolphins and can also be used with delphinids
trains. A click train was made after an approach under human care. Contrary to other hydrophone
and/or movement of the rostrum towards the arrays, the BaBeL system can be used to detect,
device: in the first observation, the click train was locate, and track dolphins emitting sounds in a 3D
emitted by the second individual after it turned space. The hydrophone arrays of Au & Herzing
its rostrum towards the device (see Appendix 1, (2003), Schotten et al. (2004), and Ball & Buck
Figure 1). In the second observation, the click (2005) all present hydrophones in the same plane,
train was emitted by the last individual after it making it impossible to discriminate from the
approached the device (see Appendix 1, Figure 2; audio recording if the emitter dolphin was in front
video available on the Aquatic Mammals web-of or behind the device. The design of our system
site:
www.aquaticmammalsjournal.org/index.php?
places hydrophones in different planes, allow-
option=com_content&view=article&id=10&
ing us to determine the position of the vocalizing
Itemid=147
). In the third observation, the click dolphin regardless of its direction of approach to
train was emitted by the second individual after it the observers, and the wide-angle HD 360° video
approached the device (see Appendix 1, Figure 3). cameras provide information to localize to an
The same individual produced the four whistles identified vocalizing dolphin visually. When ani-
presented in our second sequence; the first whistle mals are in the visual range of the camera, this
was emitted before the approach, and the three 360° audio-video system could greatly increase
others were emitted after leaving. This animal the number of vocalizations that can be attributed
produced no whistles while swimming towards to an individual dolphin.
the observers. Simultaneous visual and acoustic recordings
are necessary for localizing to a vocalizing dol-
Discussion phin. This system is mainly limited by visual
detection, which depends not only on water clar-
The results with the BaBeL system are promis-ity but also on the wide-angle video cameras.
ing for the study of dolphin behavior. Its accu-Wide-angle lenses affect the perspective by exag-
racy using simulated underwater sounds in a gerating the distance between objects. They make
pool was validated. The BaBeL design during subjects at moderate and far distances seem fur-
field testing was verified: the device achieved ther away than they really are. Consequently, only
Table 3. Localization performance of our custom-made program using the sound produced by two bars of steel during tests
in a pool
Position estimated from the videos
Position estimated from
the acoustic recordings Difference in estimation
Position Azimuth
(°)
Elevation
(°)
Distance
(m)
Azimuth
(°)
Elevation
(°)
Distance
(m)
Azimuth
(°)
Elevation
(°)
Distance
(m)
133.0 5.3 4.7 21.4 3.4 6.3 11.6 1.9 -1.6
25.7 1.2 4.5 6.2 -2.6 0.8 -0.5 3.8 3.7
3328.8 3.5 4.7 349.6 1.1 0.8 -20.8 2.4 3.9
4315 3.1 3.3 349.3 -3.1 1.5 -34.3 6.2 1.8
58.0 -6.1 3.0 2.9 -7.9 0.8 5.1 1.8 2.2
643.6 2.3 3.3 36.3 4.2 1.3 7.3 -1.9 2.0
761.6 5.6 2.1 55.4 -2.8 0.7 6.2 8.4 1.4
86.8 0.7 1.5 0.6 12.5 0.4 6.2 -11.8 1.1
9304.4 -0.7 2.1 303.1 -7.7 0.5 1.3 7.0 1.6
Mean -2.0 2.0 1.8
SD 15.2 6.0 1.6
170 Lopez-Marulanda et al.
dolphins vocalizing near BaBeL (within 10 m) Acknowledgments
were visually and acoustically detected. As previ-
ously demonstrated by Watkins & Shevill (1974), FD’s contribution was partially funded by
the accuracy of this acoustic localization system Focused on Nature. Parc Asterix funded previ-
should decrease as the distance of dolphins from ous preliminary fieldwork of FD and JLM and
the device increases. To improve accuracy, the dis-funded TB’s work. Materials and fieldwork were
tance between the hydrophones can be increased, financed by the CERECAR project from Abyss
but this would reduce system maneuverability. Foundation (La Réunion, France). We are very
Therefore, it is recommended that this device only grateful to the Parc Asterix Dolphinarium curator,
be used in clear water and preferably with dolphin Birgitta Mercera, and her trainers for their help
populations habituated to the presence of human in testing previous versions of our device within
swimmers, or with dolphins under human care. their group of dolphins. We would like to thank
The five possible situations that observers Abyss Foundation volunteers and Emmanuel
might encounter while using BaBeL are sum-Antongiorgi for their support in collecting
marized in Appendix 2. Contrary to using a regu-data, and Isabelle Charrier and the Bioacoustic
lar camera, an observer using such a 360° video Communication Team of NeuroPSI for her con-
system increases the possibility of capturing structive comments during the development of
ongoing behaviors regardless of his position with this work. We thank Isabella Clegg for revising
respect to the animals and his concentration level, the English of this manuscript. Finally, we would
thus reducing human error. In 59% of the detected like to give special thanks to editor Dr. Kathleen
click trains and in 43% of detected whistles, this Dudzinski for her advice and encouragement to
device could acoustically and visually detect dol-improve this manuscript.
phins, but the customized program did not point to
one of the dolphins present on the video, meaning Literature Cited
that the dolphin emitting the sound was out of our
range or vision. Therefore, in these cases, assign-Agreement on the Conservation of Cetaceans in the Black
ing the recorded sound to any of the dolphins Sea Mediterranean Sea and Contiguous Atlantic Area
present on the video would have been a mistake, (ACCOBAMS), Resolution 4.18. (n.d.). Guidelines on
demonstrating the necessity of the use of hydro-the granting of exceptions to Article II, paragraph 1, for
phone arrays to aid in interpreting dolphins’ vocal the purpose of non-lethal in situ research in the agree-
behavior location to avoid erroneous assump-ment area. Retrieved from www.accobams.org
tions about the identity of the vocalizer. When Alameda-Pineda, X., & Horaud, R. (2014). A geometric
dolphins were detected visually and acoustically, approach to sound source localization from time-delay
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Sakai, M., Hishii, T., Takeda, S., & Konshima, S. (2006).
First Observation—In this sequence (34 s),
Flipper rubbing behaviors in wild bottlenose dolphins
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(Ind1 to Ind9) and one calf (Ind10) (Figure 1).
978. https://doi.org/10.1111/j.1748-7692.2006.00082.x
The first dolphin (Ind1) approached and swam
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towards the BaBeL for 15 s; and at 7 and 9 s,
S. (2010). Fine-scale analysis of synchronous breathing
Ind1 turned its rostrum towards the BaBel and
in wild Indo-Pacific bottlenose dolphins (Tursiops adun-
continued swimming towards the observers for
cus). Behavioural Processes, 83(1), 48-53. https://doi.
6 s more before leaving. Ind2 approached and
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the device. Ind4 swam upside down underneath
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247-260. https://doi.org/10.1007/BF00178318
nously for 14 s above Ind4 and then moved to a
Schotten, M., Au, W. W. L., Lammers, M. O., & Aubauer,
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R. (2004). Echolocation recordings and localization of
synchronized swimming below Ind4. Ind6 swam
wild spinner dolphins (Stenella longirostris) and pan-
synchronously below Ind7 for 14 s; at 11 s, Ind6
tropical spotted dolphins (S. attenuata) using a four-
turned its head to observers and continued swim-
hydrophone array. In J. A. Thomas, C. F. Moss, & M.
ming synchronously below Ind7. At 19 s, Ind6
Vater (Eds.), Echolocation in bats and dolphins (pp.
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393-399). Chicago: The University of Chicago Press.
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Ind7 for 7 s. At 27 s, Ind6 continued swimming
Linking the sounds of dolphins to their locations and
synchronously below Ind7, and Ind7 swam syn-
behavior using video and multichannel acoustic record-
chronously with Ind6 and touched Ind6 with its
ings. The Journal of the Acoustical Society of America,
pectoral fin on two occasions for 2 s at 14 s on the
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swam by the observers. Finally, Ind9 and Ind10
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swam synchronously by the BaBel next to each
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other.
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Second Observation—In the second sequence
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towards the observers for 4 s, pointed its rostrum
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towards the recording system with no sound
Van Lancker, E. (2002). Acoustic goniometry: A spatio-
being detected, and left. Ind2 also swam towards
temporal approach (Doctoral dissertation). Faculté
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the observers with no sound being detected, and
Wahlberg, M., Mohl, B., & Madsen, P. (2001). Estimating
left. Following behind the first two dolphins,
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Ind3 whistled, swam towards the observers for 2
phone array for bioacoustics. The Journal of the
s, and left. After leaving, Ind3 emitted three more
173360° HD Audio-Video Device to Observe Dolphins
whistles before disappearing out of the range of
Third Observation—In this 22 s sequence, six
vision of the video system. Ind4 swam by the
adult dolphins passed from left to right in front
BaBel, while Ind5 approached and swam towards
of the BaBeL (Figure 8). Ind1 swam less than 50
the observers for 4 s, emitted a click train, and
cm distance above Ind2. Ind2 swam upside down
continued swimming towards the observers for 5 s underneath Ind1 for 16 s; at 3 s, Ind2 turned its
before leaving (Figure 2). rostrum towards the observers and, at 8 s, emitted
Figure 1. First observation: (a) Screenshot of the location of the clicking dolphin (Ind2) in 360° video and backup video with
the red cross pointing to the source of the sound emission; and (b) timelines for ten individuals.
174 Lopez-Marulanda et al.
Figure 2. Second observation: (a) Screenshot of the location of the whistling dolphin (Ind3) in 360° video and backup video
with the red cross pointing to the source of the sound emission; (b) screenshot of the location of the clicking dolphin (Ind5)
in 360° video and backup video; and (c) timelines for five individuals (Ind1 to Ind5).
175360° HD Audio-Video Device to Observe Dolphins
a click train. At 11 s, Ind2 rubbed Ind1’s belly upside down underneath Ind4 for 4 s and then con-
with its pectoral fin for 8 s. At 19 s, Ind2 stopped tinued swimming synchronously with Ind4. Ind4
its contact with Ind1 and swam synchronously pectoral fin rubbed Ind5’s belly for 1 s at 3 s and
above it until the end of the sequence. then continued swimming synchronously with Ind5
Ind3 swam by the BaBel, and Ind4 synchro-and Ind6 (Figure 3).
nously swam next to Ind5 and Ind6. Ind5 swam
Figure 3. Third observation: (a) Screenshot of the location of the clicking dolphin (Ind3) in 360° video and backup video
with the red cross pointing to the source of the sound emission; and (b) timelines for six individuals.
176 Lopez-Marulanda et al.
Figure 1. Use of focal-animal sampling technique. Top left: No sound detected and dolphins out of the cameraʼs visual
range; Top middle: Sound detected but dolphins out of the cameraʼs visual range; Top right: No sound detected but dolphins
in the visual range of the camera; Bottom left: Dolphin in the visual range of the camera and sound detected, but the dolphin
vocalizing is not present in the video; and Bottom right: Dolphin in the visual range of the camera, with the sound detected
and the vocalizing dolphin present in the video.
Appendix 2
The five possible situations observers could encounter while operating the BaBeL.
... In this paper, we applied a 360° acoustic localization method (López-Marulanda et al., 2017) to analyze the acoustic exploratory behavior of a calf aged from 39 to 169 days for the first time. This method involves combining the spatial distribution of hydrophones, the acoustic properties of the acoustic source (propagation speed and spherical propagation model), and the evaluation of the time differences of arrival (TDOA) of acoustic waves from the source to each hydrophone (Alameda-Pineda & Horaud, 2014). ...
... Simultaneous audio and video recordings were collected using a waterproof 360° audio-video system named BaBeL (BioAcoustique, Bien-Être et Langage) (López-Marulanda, Adam & Delfour, 2017). Video data were collected using two Kodak SP360 video cameras (wide angle of 214°), one on each side of BaBel to allow a 360° view. ...
... Audio recordings were conducted at a 96-kHz sampling frequency and coded on 24 bits. All details about the geometry of the hydrophone array are described in López-Marulanda et al. (2017). ...
Article
Full-text available
Exploratory behaviour includes all the actions that an animal performs to obtain information about a new object, environment or individual through using its different senses of perception. Here, we studied the development of the exploratory behaviour of a bottlenose dolphin (Tursiops truncatus) calf aged from 39 to 169 days, by investigating its acoustic productions in relation to an immerged object handled by a familiar human without isolation from its original social group. The study was conducted between July 2015 and January 2016 at Parc Asterix dolphinarium (Plailly, France). Simultaneous audio and video recordings were collected using a waterproof 360° audio-video system named BaBeL which allows localization of the dolphin that is producing sounds. During 32 recordings sessions, for a total duration of 6 hours 55 minutes of audio-video recordings, 46 click trains were attached to individual dolphins: 18 times to the calf, 11 times to its mother and 17 times to another dolphin in the pool. When comparing the calf’s acoustical production to its mother’s, no significant differences were found in their click rate, mean click duration, or mean interclick interval (ICI). However, linear regression showed that calf’s click rate increased with age and mean ICI decreased with age, probably due to an increase in its arousal. This non-intrusive methodology allows the description and analysis of acoustic signal parameters and acoustic exploratory behaviour of a dolphin calf within its social group.
... Physiological and health-related welfare parameters such as stress hormones [86,89,90], blood profiles [91,92], and pulmonary function [93] have also been examined in captive animals. The controlled environment of the captive setting has also aided in the development of certain hydrophone-video arrays aiming to match cetacean vocalisations to behaviours, thereby decoding their meaning, which would be a critical step in evaluating cetacean welfare [94,95]. However, much is still unknown about the utility of captive welfare findings to wild marine mammals. ...
... The applicability of captive animal physiological reference ranges to wild marine mammals remains an ongoing discussion [66]. Some assert that captive research can successfully be adapted to aid wild marine mammal conservation [57,89,[95][96][97], while others advocate that welfare in captivity is compromised to the point that wild-captive comparisons of behaviour, physiology or cognition are invalid [98]. For larger species such as baleen whales and other species not kept in captivity, there is very limited research from a few longer-term rehabilitation efforts that can be used to evaluate its applicability [99,100]. ...
Article
Full-text available
Integrating welfare principles into conservation strategy is an emerging synthesis that encourages consideration of individual animals’ quality of life in research, policies and law. However, these principles have gained limited traction in marine compared to terrestrial animal conservation. This manuscript investigates several factors that may be contributing to this disparity. In order to gauge current understanding of animal welfare science principles by marine mammal researchers and other stakeholders, a “Welfare in the Wild” workshop was convened at the 32nd European Cetacean Society conference (La Spezia, Italy, April 2018). The workshop was attended by 30 participants who completed pre- and post-workshop surveys on animal welfare principles. The survey results highlight a range of different views about exactly what animal welfare science is and how it can be applied to marine mammals. Specifically, participants’ definitions appeared to vary depending on the type of employment or research they engaged in, indicating a need for an interdisciplinary common language. Secondly, we analysed the peer-reviewed literature in order to ascertain where marine mammal publications exploring welfare were being published. From 1950 to July 2020, a total of 299 articles featured both marine mammal taxa (one or more) and the word welfare in the title, abstract or keywords. This represents just 0.96% of the total peer-reviewed published papers on marine mammal taxa (n = 31,221) during the same period. When examining articles published within “Welfare and Ethics” (n = 6133) and “Aquatic-focused” (n = 139,352) journals, just 1.2% (n = 71) and 0.04% (n = 57) of articles, respectively, featured the word welfare when examining marine mammals. With the aim of exploring how explicitly including welfare evaluations in marine mammal research and management can benefit conservation outcomes, we framed our workshop and quantitative literature review findings to provide practical solutions to the language, translation and reception issues of this burgeoning cross-disciplinary collaboration.
... Les antennes dites embarquées, par exemple sur un drone [15], peuventêtre utilisées pour détecter et localiser la présence de sources par mesures acoustiques en vue d'éviter une collision en plein vol [16] ou de localiser des personnes en danger [17]. Les antennes dites portatives sont par exemple utilisées en acoustique sous-marine pour l'identification et le suivi d'invidus acoustiquement actifs au sein d'un groupe d'animaux [18], [19]. L'antenne est directement transportée par l'utilisateur qui suit le groupe d'invidusà la nage. ...
... Le même protocole de traitement est donc utilisé. Les erreurs sur les estimations, obtenues commeétant leś ecarts entre les estimations et la position de référence, sont regroupées par intervalles d'erreurs de 10 • , pour chaque filtrage, conduisant aux histogrammes de la figure 5. 18. Les erreurs sont sensiblement identiquesà celles obtenues en salle anéchoïque, avec toutefois une dégradation plus importante de la localisation lorsqu'un seul harmonique est sélectionné (formation de voies et goniométrie confondues). ...
Thesis
Ces travaux de thèse portent sur l’identification acoustique de drones en vue du dimensionnement d’une antenne avec peu de microphones (jusqu'à 10) et adaptée aux fréquences émises pour la localisation et le suivi de ces appareils. Des mesures de caractérisation ont mis en évidence la structure harmonique inhérente au signal émis par les systèmes de propulsion des drones. Une étape de filtrage précédant la localisation, adaptée à ce type de signal, est proposée. Elle consiste en une détection de la fréquence fondamentale par l'algorithme HPS (Harmonic Product Spectrum) et d'une série de filtres passe-bande pour conserver les harmoniques utiles du signal. Deux méthodes de localisation sont confrontées au travers de simulations numériques et de mesures expérimentales. La première est la formation de voies appliquée dans le domaine temporel. Usuellement employée pour la localisation angulaire de sources, elle est étendue pour une localisation dans l'espace 3D. La seconde, appelée goniométrie acoustique, estime la position angulaire de la cible comme solution d'un problème inverse. Un filtre de Kalman est ensuite utilisé pour assurer le suivi de la cible. Une campagne de mesures expérimentales a permis d'établir une base de données du déplacement d’un petit drone quadrimoteur pour différentes trajectoires. L'analyse des données a montré qu’un faible nombre d'harmoniques (de 3 à 6) dans le spectre du signal de la source à localiser est suffisant pour estimer la position d'une source sans perte significative en précision relativement à une localisation sans traitement. Le choix de cette stratégie se justifie pour la localisation et le suivi en présence de plusieurs drones.
... Since the different parameters (i.e., rate, duration, amplitude, intervocalization interval) of vocal production are easily quantifiable, acoustic monitoring might be an interesting way of measuring emotions in marine mammals. However, tremendous efforts have to be made to precisely identify the emitter of the vocalizations (Lopez-Marulanda et al., 2017) and to understand the situation and the context vocalizations are produced. ...
Article
In the last 30 years, concerns about animal emotions have emerged from the general public but also from animal professionals and scientists. Animals are now considered as sentient beings, capable of experiencing emotions such as fear or pleasure. Understanding animals’ emotions is complex and important if we want to guarantee them the best care, management, and welfare. The main objectives of the paper are, first, to give a brief overview of various and contemporary assessments of emotions in animals, then to focus on particular zoo animals, that is, marine mammals, since they have drawn a lot of attention lately in regards of their life under professional care. We discuss here 1 approach to monitor their emotions by examining their laterality to finally conclude the importance of understanding animal emotion from a holistic welfare approach.
... Simultaneous audio and video recordings were carried out using a waterproof 360°audio-video system known as BaBeL (Lopez-Marulanda et al., 2017). Video data were collected using one wide angle camera (GIROPTIC) consisting of three objectives that allowed a 360°F ig. 1. Top view of the enclosure at the Boudewijn Seapark (Belgium). ...
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Bottlenose dolphins are social cetaceans that strongly rely on acoustic communication and signaling. The diversity of sounds emitted by the species has been structurally classified into whistles, clicks and burst-pulsed sounds. Although click sounds and individually-specific signature whistles have been largely studied, not much is known about non-signature whistles. Most studies that link behavior and whistle production conduct aerial behavioral observations and link the production of whistles to the general category of social interactions. The aim of this study was to determine if there was a correlation between the non-signature whistle production and the underwater behaviors of a group of bottlenose dolphins (Tursiops truncatus) under human care, during their free time in the absence of trainers. To do this we made audio-video recordings 15 minutes before and after 10 training sessions of eight dolphins in Boudewijn Seapark (Belgium). For the behavioral analysis we conducted focal follows on each individual based on six behavioral categories. For the acoustical analysis, carried out at the group level, we used the SIGID method to identify non-signature whistles (N = 661) and we classified them in six categories according to their frequency modulation. The occurrences of the six categories of whistles were highly collinear. Most importantly, non-signature whistle production was positively correlated with the time individuals spent slow swimming alone, and was negatively correlated with the time spent in affiliative body contact. This is the first analysis that links the production of non-signature whistles with particular underwater behaviors in this species.
... Occupant une niche écologique où la lumière s'atténue plus rapidement que dans l'air (Lythgoe 1979 ;Kröger 2008), les néocètes vivent principalement dans un « monde de sons » sous-marin (Ketten 1994(Ketten , 2000Tyack 1999 ;Wartzok & Ketten 1999 ;Mooney et al. 2012 ;Yamato et al. 2014 ;Ary et al. 2016 ;Nummela & Yamato 2018) et possèdent des systèmes de communications sonores très complexes (e.g. Payne & McVay 1971 ;Rendell & Whitehead 2003 ;Eriksen et al. 2005 ;King & Janik 2013 ;Gero et al. 2016 ;López-Marulanda et al. 2017 ;Allen et al. 2018 ;Rossi-Santos 2018 ;Stafford et al. 2018 ;Martin et al. 2019). De plus, les deux groupes de cétacés actuels se distinguent grandement par leurs capacités auditives. ...
Thesis
La mise en évidence par la biologie moléculaire et par les données paléontologiques de l'appartenance des cétacés au groupe des artiodactyles constitue une des avancées majeures de ces 30 dernières années en mammalogie. Il n'y a cependant pas à l'heure actuelle de consensus quant aux relations phylogénétiques basales des artiodactyles fondées sur des caractères morphologiques et l'histoire évolutive du groupe est de fait, ponctuée de nombreux points d'interrogation. Cette thèse explore une source de caractères phylogénétiques prometteuse : la région auditive (os pétreux, bulle auditive, osselets de l'oreille moyenne, oreille interne) à partir notamment des nouvelles perspectives offertes par l'imagerie µCT Scan. Les principaux objectifs de cette thèse sont (1) de déterminer le signal phylogénétique porté par la région auditive chez les artiodactyles afin d’apporter une nouvelle source de caractères aux analyses et (2) d’explorer le signal écologique porté par les différents éléments de cette région sensorielle dédiée à l’audition (oreille externe, moyenne et canal cochléaire du labyrinthe osseux) et à l’équilibrioception (vestibule et canaux semi-circulaires du labyrinthe osseux). La première partie de cette thèse (I) nous emmène au Togo, où de nombreux restes inédits de la région auditive de « baleines à pattes » (Protocetidae Stromer, 1908) ont été récoltés. D’un point de vu anatomique, ces restes fossiles ont permis de documenter et de décrire pour la première fois le stapes, l’incus et le labyrinthe osseux d’un protocète ; des éléments indispensables pour comprendre leur audition. L’analyse morpho-fonctionnelle indique qu’une audition optimale était probablement possible dans l’air et dans l’eau pour ces cétacés semi-aquatiques. De plus, la morphologie de leur cochlée indique que leur capacité auditive était proche de celle de leurs cousins terrestres et que les spécialisations relatives aux capacités auditives remarquables des cétacés modernes (i.e. sensibilité aux infra- ou ultrasons) se sont opérées après la séparation historique entre les mysticètes et les odontocètes.La deuxième partie de ce travail (II) se concentre sur les origines de l’amphibiose au sein des Cetancodonta, à travers l’étude de plusieurs familles fossiles, connues pour leurs liens étroits au milieu aquatique. L’étude de la région auditive des hippopotamoïdes (Anthracotheriidae + Hippopotamidae), révèle que l’adaptation à un mode de vie semi-aquatique est apparue plusieurs fois, de façon convergente, dans son histoire évolutive et semble d’ailleurs indiquer une origine terrestre pour ce groupe. Quant au raoellidé Indohyus, son complexe pétro-tympanique présente une combinaison de caractères suggérant un certain degré d’adaptation au milieu aquatique, mais l’étude fonctionnelle de sa cochlée indique que ce taxon ne pouvait très probablement pas entendre de façon efficace sous l’eau. Pour finir, le dernier point de cette thèse explore également le potentiel phylogénétique de la région auditive à travers une analyse construite sur des caractères morphologiques du pétreux et du labyrinthe osseux à l’échelle des artiodactyles. Pour la première fois, les résultats de notre analyse concordent avec ceux des analyses moléculaires. Parmi les points les plus notables, le clade des Cetancodonta est bien soutenu par la morphologie du pétreux et la position d’Indohyus suggère fortement que les raoellidés sont des cétacés.Ainsi, la région auditive s’avère être un élément essentiel d’un point de vu phylogénétique et morphofonctionnel. En effet, comme nous avons pu le voir tout au long de cette thèse, lorsque la nature complexe et variée de la région auditive est appréhendée dans son ensemble, elle permet d’inférer l’écologie d’un taxon donné et d’en apprendre davantage sur ses relations de parenté. Par conséquent, la région auditive est encore loin d’avoir dit ses derniers mots... et nous n’avons pas encore fini d’en entendre parler.
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Chapter
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