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Modulation of whistle production related to training sessions in bottlenose dolphins ( Tursiops truncatus ) under human care: Whistle Emission Rate in Bottlenose Dolphins Under Human Care

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Bottlenose dolphins are highly social cetaceans with an extensive sound production including clicks, burst-pulsed sounds, and whistles. Some whistles, known as signature whistles, are individually specific. These acoustic signatures are commonly described as being emitted in contexts of stress during forced isolation and as group cohesion calls. Interactions between humans and captive dolphins is largely based on positive reinforcement conditioning within several training/feeding sessions per day. Vocal behavior of dolphins during these interactions might vary. To investigate this, we recorded 10 bottlenose dolphins of Parc Asterix dolphinarium (France) before, during and after 10 training sessions for a total duration of 7 hr and 32 min. We detected 3,272 whistles with 2,884 presenting a quality good enough to be categorized. We created a catalog of whistle types by visual categorization verified by five naive judges (Fleiss’ Kappa Test). We then applied the SIGID method to identify the signatures whistles present in our recordings. We found 279 whistles belonging to one of the four identified signature whistle types. The remaining 2,605 were classified as non-signature whistles. The non-signature whistles emission rate was higher during and after the training sessions than before. Emission rate of three signature whistles types significantly increased afterwards as compared to before the training sessions. We suggest that dolphins use their signature whistles when they return to their intraspecific social interactions succeeding scheduled and human-organized training sessions. More observations are needed to make conclusions about the function of signature whistles in relation to training sessions.
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RESEARCH ARTICLE
Modulation of Whistle Production Related to Training
Sessions in Bottlenose Dolphins (Tursiops truncatus)
Under Human Care
Juliana Lopez Marulanda,
1
* Olivier Adam,
1,2
and Fabienne Delfour
3
1
Institute of Neurosciences Paris Saclay, Universit
e Paris Sud, CNRS UMR 9197Orsay, France
2
Institut Jean Le Rond dAlembert, Sorbonne Universit
es, UPMC Univ Paris 06, CNRS UMR 7190Paris, France
3
Laboratoire dEthologie Exp
erimentale et Compar
ee E.A. 4443 (LEEC), Universit
e Paris 13, Sorbonne Paris
Cit
eVilletaneuse, France
Bottlenose dolphins are highly social cetaceans with an extensive sound production including clicks, burst-pulsed
sounds, and whistles. Some whistles, known as signature whistles, are individually specic. These acoustic signatures
are commonly described as being emitted in contexts of stress during forced isolation and as group cohesion calls.
Interactions between humans and captive dolphins is largely based on positive reinforcement conditioning within
several training/feeding sessions per day. Vocal behavior of dolphins during these interactions might vary. To
investigate this, we recorded 10 bottlenose dolphins of Parc Asterix dolphinarium (France) before, during and after 10
training sessions for a total duration of 7 hr and 32 min. We detected 3,272 whistles with 2,884 presenting a quality
good enough to be categorized. We created a catalog of whistle types by visual categorization veried by ve naive
judges (FleissKappa Test). We then applied the SIGID method to identify the signatures whistles present in our
recordings. We found 279 whistles belonging to one of the four identied signature whistle types. The remaining 2,605
were classied as non-signature whistles. The non-signature whistles emission rate was higher during and after the
training sessions than before. Emission rate of three signature whistles types signicantly increased afterwards as
compared to before the training sessions. We suggest that dolphins use their signature whistles when they return to
their intraspecic social interactions succeeding scheduled and human-organized training sessions. More observations
are needed to make conclusions about the function of signaturewhistlesinrelationtotrainingsessions.ZooBiol.XX:
XXXX, 2016. © 2016 Wiley Periodicals, Inc.
Keywords: signature whistle; whistle; communication; dolphinarium
INTRODUCTION
Bottlenose dolphins (Tursiops truncatus) are highly
social cetaceans that live in a ssionfusion society where
individuals associate in small groups that can vary in
composition according to age, sex, reproductive status, and
activity [Connor et al., 2000; Mann et al., 2000; Gibson and
Mann, 2008; Tsai and Mann, 2013]. In this extremely mobile
species, group members can be separated by hundreds of
meters within a habitat with limited visibility [Connor et al.,
1998]. Interactions based on the use of acoustic signals seem
to be the most effective communication strategy under these
conditions [Janik, 1999a,b].
Consequently, bottlenose dolphins display an
extensive sound production including clicks or pulsed
sounds [Au, 1993; Au and Fay, 2012], burst-pulsed sounds
[L
opez and Shirai, 2009], and whistles or tonal sounds
(reviewed in Janik, 2009). The term whistleis used to refer
to a unit of one continuous contour (loop), two or more
Correspondence to: Juliana Lopez Marulanda, Institute of Neuro-
sciences Paris Saclay, University Paris Sud, CNRS UMR 9197, Orsay
91405, France. E-mail: juliana.lopez-marulanda@u-psud.fr
Received 13 April 2016; Revised 05 September 2016; Accepted 20
September 2016
DOI: 10.1002/zoo.21328
Published online XX Month Year in Wiley Online Library
(wileyonlinelibrary.com).
© 2016 Wiley Periodicals, Inc.
Zoo Biology 9999 : 110 (2016)
repeated contours (multiloops) that can be connected or
separated by a period of silence lasting between 0.03 and
0.25 sec in duration (disconnected multi-loop whistle) [Esch
et al., 2009a]. The term whistle typedescribes all whistles
showing specic frequency modulations as determined by
visual categorization [Kriesell et al., 2014].
Some individually specic whistles are called
signature whistles[Caldwell and Caldwell, 1965].
Signature whistles may be composed of a single or multiple
loops [Caldwell et al., 1990]. The number of loops produced
in a signature whistle varies according to the behavioral
context and it increases with age [Caldwell et al., 1990]. It
can also depend of whether it is produced by its owner or
copied by another individual [King et al., 2013]. Signature
whistles have been detected in dolphins as young as 1 or
2 years old [Fripp et al., 2005; Sayigh et al., 1990] and their
frequency modulation pattern remains stable during the
entire life of the individuals [Sayigh et al., 1990]. However,
malessignature whistles can vary throughout life as a
consequence of changing social relationships [Watwood
et al., 2004]. Young males may use signature whistles similar
to their mother while young females are more likely to
choose different frequency modulation patterns [Sayigh
et al., 1990, 1995]. Signature whistles are emitted in context
of forced isolation [Caldwell and Caldwell, 1965; Sayigh
et al., 1990, 1995; Janik et al., 1994; Watwood et al.,
2005] and as a contact or cohesion call between mothers and
calves [Smolker et al., 1993] and between members of the
same group [Janik and Slater, 1998]. During social
interactions, signature whistles are more frequently emitted
than during other behavioral contexts such as feeding or
travelling [Cook et al., 2004]. These signals can also be
copied [Janik, 2000; Tyack, 1986] by other individuals of the
group, possibly to label a particular individual [Janik, 2000].
It has been suggested that signature whistle mimicry might
be afliative [King et al., 2014]. Finally, an increase of the
signature whistle emission rate has been reported during
capture-release procedures with free-ranging bottlenose
dolphins, suggesting that signature whistle emission rate
could be considered as a potential indicator of stress in
dolphins [Esch et al., 2009b].
The management of dolphins in captivity is largely
based on positive reinforcement training [Brando, 2010;
Laule, 2003], and often several training/feeding sessions are
held per day during which caregivers promote desired
behaviors to facilitate husbandry and medical care and build
a bond with the animals [Brando, 2010]. In the daily life of
captive dolphins, training/feeding sessions could represent
remarkable events that involve the development of cognitive
skills and the modulation of the animalsbehaviors. In the
case of Parc Asterix delphinarium, the dolphins are separated
into sub-groups during each training session and each sub-
group performs different exercises. Under these conditions,
it is possible that the dolphinsvocal repertoire and behavior
may vary. For example, it has been reported that the number
of whistle emissions in captive bottlenose dolphins increases
during interactions with people [Akiyama and Ohta, 2007].
Another study on a captive group of false killer whales
(Pseudorca crassidens) reported that the highest vocaliza-
tion rate was registered when animals were fed [Platto et al.,
2015]. However, according to our knowledge, it remains
unknown how the scheduled training/feeding sessions in
bottlenose dolphins under human care modulate the emission
rate of different whistles types (e.g., signature whistles).
This study aims to describe the possible effects that
training/feeding sessions, have on the emission rate of non-
signature and signature whistles, in a group of captive
bottlenose dolphins.
METHODS
Study Subjects
The study was conducted in November 2014 and
May 2015 at the Parc Asterix dolphinarium (Plailly, France).
At the time of the study, the dolphinarium was closed to the
public. The complex was rst inhabited in November by nine
Atlantic bottlenose dolphins (T. truncatus), four females
aged 41, 34, 20, and 15 and years, and ve males aged 32, 5,
4, 4, and 3 years. In January 2015, two males (4 and 5 years
old) were transferred to another facility and one adult male
(31 years old) arrived. Thus, the recordings in May were
conducted on a group of eight individuals. All dolphins
are subject to the same management schedule based on
positive reinforcement training methods. Every day dolphins
take part in at least ve training sessions approximately at the
same time during which their trainers feed them after they
perform several exercises aimed to facilitate the husbandry
and medical care procedures and to prepare for presentations
to the public. Each dolphin knows around 100 behaviors to
perform upon trainerscommand plus the new behaviors
they are learning. Their sequence, their frequency and their
duration change every day in every session. It could be
underwater/aerial behaviors and solitary/group behaviors.
Before and after the training sessions the trainers mainly
stayed in the ofce and food preparation area and remained
not visible but audible by the dolphins. At the beginning of
each training session the trainers went out of the food
preparation area at the same time carrying sh buckets and
place themselves at the edge of the pool. During training
sessions, the trainers divide the animals into sub-groups of
the same two or three individuals. Each sub-group stays with
one trainer and performs different exercises during the
session which lasts around 15 min. This separation is never
forced and it is achieved because animals are reinforced
positively when they stay together in their assigned group.
The trainers start and end their working day by feeding the
dolphins ad-libitum without asking them to perform any kind
of exercises.
Overall, this facility consists of one outdoor and two
indoor pools not acoustically isolated. The outdoor pool has a
volume of 3,246 m
3
and a depth that varies from 2.5 m at the
2Lopez Marulanda et al.
Zoo Biology
shallowest point to 4.5 m at its deepest. The indoor part of the
complex, divided into two sections, has a total volume of
550 m
3
and a depth of 2.5 m. The dolphins have free access
between the pools at all times.
Whistle Recordings
Whistles were recorded approximately 15 min before,
during and 15 min after ten training sessions that took place
on 6 days: ve recording sessions were conducted over
4 days in November 2014 and ve more over 2 days in
May 2015. The recordings were carried out using a CRT
hydrophone C54XRS (frequency response: 0.01644 kHz
3 dB) plugged in to a TASCAM HDP2 recorder at the
acquisition rate of 96 kHz and samples were coded on 24 bits.
In order to prevent the dolphins touching and grabbing the
hydrophone, it was placed in a exible oating tube inside an
18.9 L polycarbonate bottle with multiple perforations. The
apparatus was xed to a wooden stick at a distance of 50 cm
from the edge of the pool and 50 cm deep near the small
beach area (Fig. 1).
Visual Categorization Process
To create a whistle catalogue, spectrograms (FFT size:
1024, overlap 50%, Hanning window) of the recorded
whistles were analyzed using Audacity 2.06 software (GNU
General Public License, The Audacity Team, Pittsburg,
PA). Graphs with standardized x-andy-axes (1 sec long,
with a frequency range of 0 Hz to 48 kHz) of the frequency
modulation of each whistle were used to prevent distortion
of whistles caused by axes differing in length as this
would have inuenced the visual categorization process.
Whistles with a negative signal-to-noise ratio or overlapping
with other whistles were registered but not included in the
categorization. Once each whistle spectrogram was regis-
tered, a visual categorization of whistle types was carried out.
We applied the SIGID method [Janik et al., 2013] to identify
signature whistles within our catalog of whistle types based on
two criteria: rstly, signature whistles were whistle types
repeated at least four times in a recording session, and
secondly, at least on one occasion the whistles were produced
in a sequence in which 75% or more repetitions occur within
110 sec of one other. The whistle types that were not
cataloged as signature whistle types using this method were
cataloged as non-signature whistle types.
To verify the reliability of our classication method,
ve experts, all afliated to the acoustic communication team
of NeuroPSI laboratory (Orsay, France) and working on
bioacoustics in classication of birds or cetacean sounds,
performed two visual classication tasks using the identied
signature whistles of our dataset [see Kriesell et al., 2014].
For each signature whistle type, six whistle repetitions were
randomly selected: 1 to act as a template and 5 to be classied
by the experts. Each signature whistle repetition was
surrounded by the signature whistle templates and was
presented to each expert on a Microsoft Power Point slide. In
the rst task, the experts were asked to compare each whistle
repetition with each template and to rate the similarity in a
scale from 1 (very different) to 5 (very similar). The second
task was to assign to each whistle repetition the most similar
template category. The ratings were compared between
experts using FleissKappa statistic [Siegel and Castellan,
1988] to determine inter-observer agreement in whistle
classication and consistency in categorization (with and
Fig. 1. Position of the recording set-up in the pool. Not to scale.
Whistle Emission Rate in Bottlenose Dolphins Under Human Care 3
Zoo Biology
without authorsclassications). When experts are in
complete agreement FleissKappa statistics (k) is equal to
1 [Landis and Koch, 1977]. If agreement between experts is
the same as expected by chance, then kis equal to 0.
Whistle Emission Analysis
Statistical tests were conducted using R statistical
software version 3.02 [R Core Team, 2013]. Mean values of
whistles emission rate and signature whistle emission rate
per minute were calculated for the recordings before, during
and after each training session. The Friedman Rank Test was
used to compare the non-signature whistle emission rate and
the signature whistle emission rate before, during and after
each training session. Post hoc tests were performed to
examine the variation in the tested variables.
RESULTS
A total of 7 hr 32 min (Table 1) were recorded among
the ten training sessions (154 min before, 147 min during
training sessions and 152 min after) in which 3,272 whistles
were identied: 309 (9.44%) were classied as having too
low signal-to-noise ratio whistles to be considered in this
study and 79 (2.41%) were classied as overlapping
whistles, the remaining 2,884 (88.14%) were classied in
signature or non-signature whistle types. Most of the
identied whistles were recorded during the rst ve
recording sessions with nine individuals (n¼1,946; before
training: 288, during training: 743, and after training: 915)
while less of half of whistles was recorded during the last ve
recording sessions with eight individuals (n¼938; before
training: 192; during training: 329, and after training: 417).
According to SIGID method, 279 (9.67%) signature
whistles were identied belonging to four different signature
whistles types (Fig. 2). The remaining 2,605 (90.32%)
were classied as non-signature whistle types. The four
signature whistles were present in the rst ve recording
sessions in November with nine individuals and in the last
ve recording sessions in May with eight individuals. We
detected the occurrence of 210 signature whistles during
the rst recording sessions and the occurrence of 69 signature
whistles during the last recording sessions.
The two visual classication tasks tested reliability of
identifying whistle types. The rst task showed a low inter-
observer agreement (Fleisskappa statistic without author as
judge: k¼0.388, njudges ¼5, z¼18.7, P¼0.00001; with
author as judge: k¼0.408, njudges ¼6, z¼24.2,
P¼0.00001). During the second task, the experts repeatedly
chose the highest similarity rating for the rst task as the most
similar whistle to the template category. The inter-observer
agreement was high in the second task (Fleisskappa
statistic: k¼0.956, z¼28.7, P¼0.00001). These results
show that clearly dened whistle types exist in the repertoire
of Parc Asterix bottlenose dolphins and support the authors
visual categorization of the dataset.
The overall whistle emission rate during our recordings
was 7.48 whistles per minute. We calculated this rate
(including signature and non-signature whistles) by averaging
the ten sessions before, during and after the training sessions.
The rate did not change signicantly from 4.72 3.32
whistles per minute before the training sessions, to
8.14 2.74 whistles per minute during the training sessions
and 9.84 7.44 whistles per minute after the training sessions
(Friedman Rank Test: x
2
¼2.6, df ¼2, P¼0.2725) (Fig. 3).
When comparing non-signature and signature whistles
separately, we found that dolphins emitted more non-
signature whistles during and afterwards (respectively
Wilcoxon signed Rank Test: V¼4, P¼0.0137 and V¼2,
P¼0.0058 with Bonferroni-adjusted signicance level of
P<0.0167) than before the training sessions. No signicant
differences were found between the non-signature whistle
emission rate during and after the training sessions (Wilcoxon
signed Rank Test: V¼25, P¼0.8457 with Bonferroni-
adjusted signicance level of P<0.0167) (Fig. 4).
TABLE 1. Time of recording of the 10 sessions: Before, during and after the training
Duration (hh:mm:ss)
Session and social grouping Before During After Total
1st social grouping, session 1 00:02:09 00:24:21 00:14:32 00:41:02
2 00:04:17 00:20:42 00:15:59 00:40:58
3 00:06:49 00:17:50 00:14:26 00:39:05
4 00:16:23 00:13:18 00:14:29 00:44:10
5 00:15:00 00:11:08 00:16:33 00:42:41
Sub-total 00:44:38 01:27:19 01:15:59 03:27:56
2nd social grouping, session 1 00:30:07 00:13:29 00:15:00 00:58:36
2 00:35:39 00:15:33 00:15:08 01:06:20
3 00:14:58 00:11:18 00:15:00 00:41:16
4 00:12:38 00:11:30 00:15:00 00:39:08
5 00:16:01 00:08:13 00:15:00 00:39:14
Sub-total 01:49:23 01:00:03 01:15:08 04:04:34
Total 02:34:01 02:27:22 02:32:07 07:32:30
The rst ve recording sessions were carried out with the rst social group (nine animals) and the last ve recording sessions were carried
out with a second social group (eight animals).
4Lopez Marulanda et al.
Zoo Biology
When we pooled the four types of signature whistles,
we found that signature whistle emission rate varied
signicantly before, during and after training sessions
(Friedman Rank Test: x
2
¼12.2, df ¼2, P¼0.0022):
dolphins emitted signicantly more signature whistles
afterwards than before the training sessions (Wilcoxon
signed Rank Test: V¼0, P¼0.0019 with Bonferroni-
adjusted signicance level of P<0.0167), but the animals
signature whistle emission rate before and during the training
sessions did not show any signicant variation (Wilcoxon
signed Rank Test: V¼30, P¼0.8457 with Bonferroni-
adjusted signicance level of P<0.0167) nor between
periods during and after the training sessions (Wilcoxon
signed Rank Test: V¼0, P¼0.0195 with Bonferroni-
adjusted signicance level of P<0.0167) (Fig. 5).
The four different signature whistle types were not
present in all the recording sessions making it impossible to
statistically compare the whistle emission rate of each kind of
Fig. 2. Three randomly chosen spectrograms of each of the identied signature whistles emitted by Parc Ast
erix bottlenose dolphins
(Plailly, France): (a) Signature whistle type 1 (SW1); (b) Signature whistle type 2 (SW2) which can be identied as variably loopy based on
the nal loop which is consistent from whistle to whistle; (c) Signature whistle type 3 (SW3); (d) Signature whistle type 4 (SW4). The
numbers in the right are the total occurrences of the whistle type found in the acoustic recordings (n¼293 signature whistles).
Spectrograms are all presented in the same scaling. Frequency (kHz) is on the y-axis and ranges from 0 to 48 kHz. Time (s) is on the x-axis.
FFT 1,024, Hanning window, overlap 50%.
Fig. 3. Boxplot of bottlenose dolphinswhistle (all types)
emission rate before, during and after training sessions (n¼10).
Friedman Rank Test: x
2
¼2.6, df ¼2, P>0.05.
Whistle Emission Rate in Bottlenose Dolphins Under Human Care 5
Zoo Biology
signature whistle between the sessions. However, we
calculated the emission rate of each signature whistle type
for the 10 sessions before, during and after the training.
Whistle rate increased after the training sessions for
signatures whistles type 1 (SW1), type 2 (SW2), and type
3 (SW3). The whistle emission rate of the signature whistle
type 4 (SW4) was higher before than after the training
sessions (Fig. 6).
To summarize, the dolphinsoverall whistle emission
rate did not signicantly change before, during and after
the training sessions. However, the non-signature emission
rate was higher during and afterwards than before the
training sessions and the signature whistle emission rate
was signicantly higher after than before the training
sessions. The emission rate varied between the different
signatures whistles types, increasing for types 1, 2, and 3
and decreasing for type 4.
DISCUSSION
Dolphin whistle emission rate is highly variable and
depends on several parameters: groups size [Jones and
Sayigh, 2002; Cook et al., 2004; Quick and Janik, 2008],
group composition [Hawkins and Gartside, 2010] and
behavioral context [Dos Santos et al., 1990; Jacobs et al.,
1993; Acevedo-Guti
errez and Stienessen, 2004; Cook et al.,
2004]. Most of the whistles detected occurred during the rst
ve recording sessions: in November the nine dolphins
whistled and produced signature whistles two times more
frequently than the eight individuals in May. It is
comprehensible to have more whistles and signature whistles
produced when the group size increases [Van Parijs et al.,
2002], but here, the difference in occurrence of whistles was
not proportional to the number of individuals. Instead, it is
possible that the group composition impacted the dolphins
vocal productions, and in particular the age of the individuals
might also have been an important variable. The rst
recording sessions in November were carried out in a group
with four young dolphins out of nine individuals while the
second set of recordings in May occurred in a group of two
young dolphins and six adults. Motheroffspring interactions
include various behaviors (i.e., teaching behaviors) [Bender
et al., 2009] and involve vocalizations (i.e., during periods of
separation) [Smolker et al., 1993]. The nature of the
intraspecic social interactions conducted within the groups
might have inuenced the number of whistles and signature
whistles recorded. We suggest that the presence of young
dolphins might have increased the number of afliative, play
and discipline behaviors within the group and these
behaviors could be correlated to a high production of
whistles.
The SIGID method [Janik et al., 2013] allowed us to
identify four signature whistles within the bottlenose
dolphins at Parc Asterix dolphinarium. If signature whistles
are individually specic [Caldwell et al., 1990] we could
Fig. 4. Boxplot of bottlenose dolphinsnon-signature whistle
emission rate before, during and after training sessions (n¼10).
Wilcoxon signed Rank Test: V¼2, P<0.0167 (with Bonferroni
correction). Wilcoxon signed Rank Test: V¼4, P<0.0167 (with
Bonferroni correction).
Fig. 5. Boxplot of bottlenose dolphinssignature whistle (all
types) emission rate before, during and after training sessions
(n¼10). Wilcoxon signed Rank Test: V¼0, P<0.0167 (with
Bonferroni correction).
Fig. 6. Signature whistle emission rate for each type of signature
whistle (SW) before, during and after the training sessions.
6Lopez Marulanda et al.
Zoo Biology
expect to nd nine signature whistles in the rst half of our
recording sessions and eight in the second half. However, the
SIGID method was conceived to be very conservative so that
false positives were eliminated. This precaution means
the SIGID method did not consider about half of the signature
whistles present in the sample [Janik et al., 2013].
We recorded a total of 7 hr and 32 min. It is probable that
signature whistles of all the individuals were present in our
samples but we only identied less than 50% of them using the
SIGID method. In this case, some of the non-signature
whistles that were used in our analyses are signature whistles
that were not detected by the method and in this terms the
results we obtained on the non-signature whistle emission rate
are inuenced by the signature whistle emission rate.
However, the emission of signature whistles in captivity is
very scarce and for some individuals can be less than 1% of
whistle emission rate [Janik and Slater, 1998]. Thus, it is
highly probable that signature whistles of all the individuals
were not present in our acoustic recordings. It would be
necessary to record the animals during forced [Esch et al.,
2009a] or voluntary isolation [Janik and Slater, 1998] or using
a hydrophone array [L
opez-Rivas and Baz
ua-Dur
an, 2010], to
link the whistle emission to individual dolphins in order to nd
the signature whistle for each member of the group.
The rst classication task allows our study to be
comparable to previous studies that use visual categorization
of bottlenose dolphinswhistles as Janik [2000] and Kriesell
et al. [2014]. The low inter observer agreement obtained on
the rst classication task has also been reported by these
authors and might be due to the fact that we asked judges to
classify whistles on a scale of discrimination that is too ne
and leads to subjectivity. In fact when one of the authors
redid the rst classication task several months later, the
inter observer agreement with herself was low (K¼0.133
z¼1.9, P¼0.0581). However, the second classication task
that asked the judges to choose the most similar whistles
showed a high inter observer agreement, which supports the
authors visual categorization of the data set.
When we compared signature and non-signature
whistles, the total emission rate did not signicantly change
before, during and after the training sessions. Our results
differ from previous ndings on other groups of cetaceans
under human care: for instance, bottlenose dolphins
increased whistle production during interactions with
humans [Akiyama and Ohta, 2007; Therrien et al., 2012].
Akiyama and Ohta [2007] measured the number of whistles
emitted by three captive bottlenose dolphins (one male and
two females, all less than 8 years old) during several
situations in a facility in Muroto (Japan): immediately before
feeding, during feeding, during the animalsfree-time
without the presence of people, and during interactions
with people on a oat and in the water. They found that most
of the whistles were emitted during the period preceding
feeding (which is analog to the period before trainings in our
study), and whistle emission was higher during various
interactions with humans (including feeding) than during
their free-time in absence of people (which is analog to the
period after training session in our study). Therrien et al.
[2012] measured the whistle production of a group of eight
bottlenose dolphins (four adult females, two adult males, and
two young males) and found increased whistle production to
coincide with increased interactions with humans during
feeding/training sessions. Recently, a study carried out on
ve captive false killer whales (P. crassidens) (three adult
females, one adult male, and one male calf) also found an
increase in their acoustic emissions (including whistles)
upon trainersarrival [Platto et al., 2015]. The high rate was
maintained during feeding sessions and reduced immediately
after the animals were fed. In contrast, we found that non-
signature whistles increased during the training sessions but
their rate was higher afterwards, and signature whistle rate
was higher after the training sessions compared to before.
Dolphinsbehaviors and vocalizations can be modu-
lated by trainings [Kuczaj and Xitco, 2002]. Since no
information could be found about the inuence of the nature
and content of trainings in the related papers, we cannot
comment on the impact they have on whistle emission rate.
Moreover, in Akiyama and Ohtas [2007] study, dolphins
spent less than 2 years under human care; this is in contrast to
Parc Ast
erix dolphins, where six out of nine dolphins are
born in the dolphinarium and the other three have been in
captivity for over 2 decades. It has been shown that free-
ranging dolphins increase their whistle emission rate during
feedings probably to recruit more members to the group
[Acevedo-Guti
errez and Stienessen, 2004], and this behavior
is likely not necessary, or less present, in captivity where
feeding is less cooperative than in the wild. In Akiyama and
Ohtas [2007] study, the dolphins might interact (e.g., to
cooperate) while feeding. Unfortunately, Therrien et al.
[2012] and Platto et al. [2015] do not specify for how long
their studied animals have been in captivity.
Our study shows that overall, signature whistle
emission signicantly increased after the training sessions.
However this was not the case for all the signature whistles
types we detected, suggesting that depending upon the
situation dolphinssignature whistles production varies, and
consequently they might be used for various functions.
Context of emissions of signature whistles varies from stress
calls during forced isolation [Esch et al., 2009a] to cohesion
calls [Smolker et al., 1993; Janik and Slater, 1998; Quick and
Janik, 2012]. In Parc Asterix, during training sessions the
trainers divide the animals into groups of the same two or
three individuals. Each sub-group remains with one trainer
and performs different exercises during the session. This
division is never forced and it is achieved by using positive
reinforcement. The training session by itself can be
considered as rewarding for the animals [Laule and
Desmond, 1998], since they are positively reinforced when
they perform exercises. A previous study conducted in this
facility measured the breathing rate of animals before and
after the training sessions [Jensen et al., 2013] as a possible
indicator of stress [Broom and Johnson, 1993; Dierauf,
Whistle Emission Rate in Bottlenose Dolphins Under Human Care 7
Zoo Biology
2001]. The results showed that the animals maintained the
same breathing rate before and after the sessions [Jensen
et al., 2013], indicating that the exercises they were asked to
perform did not affect their level of stress. The increase in
signature and non-signature whistle emission rates therefore
is not likely to be explained by the animals being stressed
during the training sessions. We suggest that the increase in
non-signature and some signature whistle emission after
training sessions is due to an augmentation of social
behaviors. Before training sessions, dolphins can freely
interact displaying afliative, agonistic, and sexual behav-
iors [Herzing, 1996; Samuels and Gifford, 1997]. Since
training sessions occur consistently approximately at the
same hour, dolphins can perform anticipatory behaviors
[Jensen et al., 2013] which could have an inuence in their
vocal production as has been found in captive false killer
whales (P. crassidens) [Platto et al., 2015] and bottlenose
dolphins in other facilities [Akiyama and Ohta, 2007].
Training sessions occur consistently approximately at the
same hour and before these dolphins can perform anticipa-
tory behaviors [Jensen et al., 2013] which could have an
inuence in their vocal production as has been found in
captive false killer whales (P. crassidens) [Platto et al.,
2015] and bottlenose dolphins in other facilities [Akiyama
and Ohta, 2007]. During training sessions, the groups are
subdivided and dolphins are asked to perform several
exercises, where these activities modulate social interactions
between animals. Finally, after the training sessions
individuals are free to regroup as they want and the signature
whistles might then be used as cohesion calls and copied as
afliative signals [King et al., 2014].
When comparing the emission rate of signature
whistles before and after the training sessions we found
that SW1, SW2, and SW3 emission rates increased after the
training session and SW4 emission rate decreased after the
training session. Signature whistles are individually
specic [Caldwell et al., 1990], so it is highly probable
that the four signature whistles identied were mostly
emitted by four particular individuals with the exception of
the cases where the signature whistles are copied [Janik,
2000; Tyack, 1986]. If this is the case, the signature
whistles detected are not from the three males that were
transferred between facilities because they are present
before and after the transfer. One of the signature whistles
(SW2) consists of several connected loops. Since the
number of loops increases with the age of the individual
[Caldwell et al., 1990], we suggest that SW2 probably
belongs to one of the oldest animals in the group.
The differences found between the emission rates of
each signature whistle type might be due to individual
differences, meaning that the three individuals that emitted
more signature whistles after the training sessions were
probably seeking group cohesion or at least looking for social
interactions. In contrast, one individual emitted more
signature whistles before the training sessions probably
looking for social interactions in a different moment.
These individual differences could be explained
by the presence of different personalities in dolphins
[Birgersson et al., 2014; Highll and Kuczaj, 2007] that
leads to individual variation in vocal activity. Since group
composition and behavioral contexts inuence dolphins
vocalization rate [Dos Santos et al., 1990; Jacobs et al.,
1993; Cook et al., 2004; Hawkins and Gartside 2010], it
would be necessary to identify the vocalizing dolphins and
to observe the animalsbehaviors during signature whistles
emissions to explain the particular behavioral context that
caused these individual differences. As a hypothesis, we
suggest that non-signature whistles are intended to give
information to listener dolphins, while signature whistles
are used to give information about the emitter. The copy of
signature whistles might play a role in spreading the
information and letting the emitter know that the
information has correctly been received. Vocal mimicry
is an important part of communication in all species of
mammals, but this is higher for cetacean species, in
particular for toothed whales. These prolicvocal
exchanges might probably be due to the development of
their personalities, the features of their social structure and
also the large diversity of their sound emissions.
In conclusion, our study shows that non-signature
and particular signature whistle emission rate increases
after scheduled training sessions in Parc Asterix dolphi-
narium. We suggest that animals might have been seeking
social interactions after the sessions. We suppose that
before the sessions, animals are free to interact, or not
interact, with the partner(s) they choose, during the training
sessions the group structure changes due to human
intervention (trainers regroup particular dolphins into
groups of 23 individuals), and after the training sessions
dolphins freely regroup using signature whistles as
cohesion calls. However, in order to validate this
hypothesis, it is necessary to directly observe the animals
behaviors and to link the patterns of group association with
whistle emissions. Moreover, during training sessions the
trainers ask the dolphins to perform solitary and coordi-
nated exercises, and their vocalization rate might also
depend on the task the trainers ask them to perform. We
can expect higher sound production rates during coordi-
nated exercises and cooperative tasks [Eskelinen et al.,
2016]. Linking whistle emissions to particular behaviors
will be the next step to better understand how dolphins
under human care communicate.
ACKNOWLEDGMENTS
We are very grateful to the Parc Asterix Dolphinarium
curator, Birgitta Mercera, and her trainers for their help
during the recording sessions. We would like to thank to the
acoustic communication team (NeuroPsi) members for their
constructive comments and for carrying out the classication
tasks and Isabella Clegg for revising the English of this
manuscript.
8Lopez Marulanda et al.
Zoo Biology
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10 Lopez Marulanda et al.
Zoo Biology
... Dibble et al., 2016;Herzing, 2000) and thus could be invaluable to welfare studies, but so far we know relatively little about which emotions certain vocalisations might indicate due to problems with identifying the sound-emitting dolphin (Herzing, 1996). Fortunately, new technology and etho-acoustical approaches are actively addressing this issue and the first results look promising in terms of discovering the meaning behind dolphin vocalisations (Lopez Marulanda et al., 2016. ...
... Therefore our results of slowclose synchronous swimming is likely to reflect the formation and/or maintenance of social bonds in the group, and may be seen more frequently following the sessions since the dolphins are reunited after a human-controlled period of separation. A recent study at Parc Astérix showed that the emission rate of signature whistles increased after the training sessions, and the authors postulated that they function as cohesion calls and affiliative signals: this concurs strongly with the behavioral results in our study (Lopez Marulanda et al., 2016). Examples can also be found in other species: working donkeys (Equus africanus asinus) gathered together to socially interact immediately after finishing their working period, even if they were fatigued and dehydrated, and water and food were available (Swann, 2006). ...
... The exact definition used throughout this thesis is where two or more animals swim within one body length of another, corresponding their movements and body axes, with 0-2 seconds delay between each individual surfacing for breathing (based on Connor et al., 2006a;Harvey et al., 2017;Holobinko and Waring, 2010). The review paper (Paper 1) at the start of the project briefly highlighted synchronous swimming as a possible indicator of positive welfare states, and therefore it was included in the suite of behaviours studied in relation to timing of training sessions in Paper 2. In addition, in this paper we went a step further and delineated the behaviour by speed and distance to partner which resulted in four (Lopez Marulanda et al., 2016). ...
Thesis
Welfare science is now an established discipline which enables objective measurements of animal welfare to be made. Bottlenose dolphins (Tursiops truncatus) are a common cetacean species kept in captivity, and although questions are arising over their quality of life in this environment, very few studies have focussed on objectively measuring their welfare. This thesis aimed to address this lack of data by developing animal-based indicators of bottlenose dolphin welfare. An initial review identified potential dolphin welfare measures, before selected behavioural indicators were measured in relation to training sessions. A judgement bias test was then adapted to dolphins, where optimistic biases were significantly linked to higher frequencies of synchronous swimming in their ‘free-time’ and lower frequencies of anticipatory behaviour before training sessions, (concurring with there ward-sensitivity theory). A penultimate study showed that anticipatory behaviour predicted participation in the upcoming event, and positive Human-Animal Interactions were anticipated more than access to toys. A final, on-going experiment has developed and applied a standardised protocol for measuring dolphins’motivation during training sessions in relation to social and health-related welfare problems. Although overall welfare is still difficult to measure, this thesis has proposed some first measures of dolphin emotions and affective states. Synchronous swimming is a likely indicator of positive emotions and social support, although more research should investigate variability between contexts. Anticipatory behaviour seemed to indicate motivation for events, and we suggest it reflects reward sensitivity as in other animals : further work into frequency thresholds would render it a valuable welfare indicator. A major objective of the thesis is to stimulate more research on welfare measures for bottlenose dolphins and other cetacean species in captivity.
... time prior to training sessions the animals invest more time in actively communicating and interacting socially than after the training sessions that could be devoted to rest. This result contrast with what has been found in other facility, in which dolphins produce more non-signature whistles in the period after than before the training sessions(Lopez-Marulanda et al., 2016). Several factors could explain these differences in the vocal activity: differences in group composition(Hawkins and Gartside, 2010; Heiler et al., 2016), different personalities of the animals(Bigersson et al., 2014;Highfill and Kuczaj, 2007), and differences in management between both facilities. ...
... In fact, both facilities differ in the procedure during the training sessions. In Boudewjin SeaPark, the animals are separated in different pools during each training, while in Parc Asterix (France), the animals are never isolated(Lopez- Marulanda et al., 2016). The isolation of animals might increase the production of whistles ...
Thesis
Full-text available
Bottlenose dolphins are highly social cetaceans that strongly rely on acoustic communication and signaling. The diversity of sounds emitted by the species has been structurally classified in whistles, clicks and burst-pulsed sounds, with some whistles called « signature whistles » that are used as cohesion calls. During this thesis, we developed an easily deployable system that identifies the animal producing sound and allows simultaneous underwater behavioral observations. We tested this methodology with bottlenose dolphins infreedom and in captivity. The present doctoral thesis aims to better understand the communication of bottlenose dolphins within their social group. First, I developed two studies to describe how the signature and non-signature whistle rate of captive dolphins varies in relation to behavior and interaction with humans. Secondly, I present the design and implementation of an innovative methodology (BaBeL system) that allows the localization of vocalizing dolphins in a three-dimensional environment, and which can be used in captivity and with free-range dolphins. Finally, I present two applications of this location methodology to address research questions regarding the exploratory behavior of a young dolphin and the use of vocalizations for coordinated movements in bottlenose dolphins.
... Yangtze finless porpoises produced more clicks during training/feeding sessions than outside of such sessions. This pattern has already been reported in other captive odontocetes with an increase in all types of underwater sounds during training/feeding/public presentations (bottlenose dolphins [42,[72][73][74][75]; belugas, Delphinapterus leucas [76]; Pacific white-sided dolphins, Lagenorhynchus obliquidens [77]). Such routine events might have caused an increased level of excitement or anticipation [72,73]. ...
Article
Full-text available
Yangtze finless porpoises use high-frequency clicks to navigate, forage, and communicate. The way in which click production may vary depending on social or environmental context has never been investigated. A group of five captive Yangtze finless porpoises was monitored for one year, and 107 h of audio recordings was collected under different conditions. Using a MATLAB-generated interface, we extracted click density (i.e., number of clicks per minute) from these recordings and analyzed its variation depending on the context. As expected, click density increased as the number of animals present increased. The click density did not exhibit diurnal variations but did have seasonal variations, with click density being highest in summer and fall. Yangtze finless porpoises produced more clicks when socially separated than when not (136% more), during training/feeding sessions than outside of such sessions (312% more), when enrichment was provided (265% more on average), and when noisy events occurred rather than when no unusual event occurred (22% more). The click density decreased when many visitors were present in the facility (up to 35% less). These results show that Yangtze finless porpoises modulate their click production depending on the context and suggest that their echolocation activity and their emotional state may be linked to these changes. Such context-dependent variations also indicate the potential usefulness of monitoring acoustical activity as part of a welfare assessment tool in this species. Additionally, the click density variation found in captivity could be useful for understanding click rate variations of wild populations that are hardly visible.
... 6 social bonds in the group, and may be seen more frequently following the sessions because the dolphins are reunited after a human-controlled period of separation. A recent study at Parc Astérix showed that the emission rate of signature whistles increased after the training sessions, and the authors postulated that they function as cohesion calls and affiliative signals: This concurs strongly with the behavioral results in our study (Lopez Marulanda, Adam, & Delfour, 2016). Examples can also be found in other species: Working donkeys (Equus africanus asinus) gathered together to socially interact immediately after finishing their working period, even if they were fatigued and dehydrated, and water and food were available (Swann, 2006). ...
Article
Behavioral patterns are established in response to predictable environmental cues. Animals under human care frequently experience predictable, human-controlled events each day, but very few studies have questioned exactly how behavioral patterns are affected by such activities. Bottlenose dolphins (Tursiops truncatus) maintained for public display are good models to study such patterns since they experience multiple daily human-controlled periods (e.g., shows, training for shows, medical training). Thus, we investigated the effect of training session schedule on their "free-time" behavior, studying 29 individuals within 4 groups from 3 European facilities. Our initial time budget analyses revealed that among the behaviors studied, dolphins spent the most time engaged in synchronous swimming, and within this category swam most at slow speeds and in close proximity to each other. "Slow-close" synchronous swimming peaked shortly after training sessions and was low shortly before the next session. Play behavior had significantly higher frequencies in juveniles than in adults, but the effect was only seen during the in-between session period (interval neither shortly before nor after sessions). Anticipatory behavior toward sessions was significantly higher shortly before sessions and lower afterward. We conclude that dolphin behaviors unconnected to the human-controlled periods were modulated by them: slow-close synchronous swimming and age-dependent play, which have important social dimensions and links to welfare. We discuss potential parallels to human-controlled periods in other species, including humans themselves. Our findings could be taken into account when designing welfare assessments, and aid in the provision of enrichment and maintaining effective schedules beneficial to animals themselves. (PsycINFO Database Record
... In addition, the observations were only achieved in the main pool but no camera recorded the behaviors of the dolphins in the back-pools, engendering a lack of data. A recent study pointed out that bottlenose dolphins tend to produce more whistles after versus before training (Lopez-Marulanda, Adam, & Delfour, 2016). Further studies would benefit to include acoustic analysis when focusing on dolphins' social behaviors. ...
Article
Social play varies among species and individuals and changes in frequency and duration during ontogeny. This type of play is modulated by environmental changes (e.g., resource availability). In captivity, cetaceans and their environment are managed by humans, and training sessions and/or public presentations punctuate the day as well as other frequent or occasional events. There is a lack of research on the effects of environmental events that occur in captivity and might affect dolphins' behavior. We studied the context in which nine bottlenose dolphins (Tursiops truncatus) played socially and the events that could potentially impact this social interaction. The dolphins' social play behavior was significantly more frequent and lasted longer in the morning than in the afternoon and was present before and after interactions with their trainers with a non-significant tendency to be more frequent before and after a training session than a public presentation. In an experimental paradigm using familiar environmental enrichment, our results demonstrated that environmental enrichment tended to increase social play duration whereas temporary noisy construction work around the pool and display of agonistic behaviors by members of the group significantly decreased it. These results contribute to better understand the social play distribution in captive bottlenose dolphins and the impact of different events within their daily lives. Since play decreases or disappears when animals are facing unfavorable conditions, the evaluation of social play may relate to the animals' current well-being. We suggest that social play has potential to become an indicator of bottlenose dolphins' current welfare state.
Article
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.
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Although many species have proven capable of cooperating to achieve common goals, the role of communication in cooperation has received relatively little attention. Analysis of communication between partners is vital in determining whether actions are truly cooperative rather than serendipitous or learned via trial and error (Chalmeau and Gallo in Behav Process 35:101-111, 1996a. doi: 10.1016/0376-6357(95)00049-6 , Primates 37:39-47, 1996b. doi: 10.1007/BF02382918 ). Wild cetaceans often produce sounds during cooperative foraging, playing, and mating, but the role of these sounds in cooperative events is largely unknown. Here, we investigated acoustic communication between two male bottlenose dolphins while they cooperatively opened a container (Kuczaj et al. in Anim Cogn 18:543-550, 2015b. doi: 10.1007/s10071-014-0822-4 ). Analyses of whistles, burst pulses, and bi-phonations that occurred during four contexts (i.e., no container, no animals interacting with container, one animal interacting with container, and two animals interacting with container) revealed that overall sound production rate significantly increased during container interactions. Sound production rates were also significantly higher during cooperative successes than solo successes, suggesting that the coordination of efforts rather than the apparatus itself was responsible for the phonation increase. The most common sound type during cooperative successes was burst pulse signals, similar to past recordings of cooperative events in bottlenose dolphins (Bastian in Animal sonar systems. Laboratoire de Physiologie Acoustique, Jouy-en Josas, pp 803-873, 1967; Connor and Smolker 1996).
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The sonar of dolphins has undergone evolutionary re-finement for millions of years and has evolved to be the premier sonar system for short range applications. It far surpasses the capability of technological sonar, i.e. the only sonar system the US Navy has to detect buried mines is a dolphin system. Echolocation experiments with captive animals have revealed much of the basic parameters of the dolphin sonar. Features such as signal characteristics, transmission and reception beam patterns, hearing and internal filtering properties will be discussed. Sonar detection range and discrimination capabilities will also be included. Recent measurements of echolocation signals used by wild dolphins have expanded our understanding of their sonar system and their utilization in the field. A capability to perform time-varying gain has been recently uncovered which is very different than that of a technological sonar. A model of killer whale foraging on Chinook salmon will be examined in order to gain an understanding of the effectiveness of the sonar system in nature. The model will examine foraging in both quiet and noisy environments and will show that the echo levels are more than sufficient for prey detection at relatively long ranges.