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

Abstract

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.

Full text

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 d’Alembert, Sorbonne Universit
es, UPMC Univ Paris 06, CNRS UMR 7190Paris, France
3
Laboratoire d’Ethologie 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 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 signaturewhistlesinrelationtotrainingsessions.ZooBiol.XX:
XX–XX, 2016. © 2016 Wiley Periodicals, Inc.
Keywords: signature whistle; whistle; communication; dolphinarium
INTRODUCTION
Bottlenose dolphins (Tursiops truncatus) are highly
social cetaceans that live in a fission–fusion 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 “whistle”is 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 : 1–10 (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 type”describes all whistles
showing specific frequency modulations as determined by
visual categorization [Kriesell et al., 2014].
Some individually specific 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,
males’signature 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 affiliative [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 animals’behaviors. 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 dolphins’vocal 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 first inhabited in November by nine
Atlantic bottlenose dolphins (T. truncatus), four females
aged 41, 34, 20, and 15 and years, and five 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 five 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 trainers’command 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 office 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 fish 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: five recording sessions were conducted over
4 days in November 2014 and five more over 2 days in
May 2015. The recordings were carried out using a CRT
hydrophone C54XRS (frequency response: 0.016–44 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 flexible floating tube inside an
18.9 L polycarbonate bottle with multiple perforations. The
apparatus was fixed 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 influenced 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: firstly, 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
1–10 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 classification method,
five experts, all affiliated to the acoustic communication team
of NeuroPSI laboratory (Orsay, France) and working on
bioacoustics in classification of birds or cetacean sounds,
performed two visual classification tasks using the identified
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 classified
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 first 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 Fleiss’Kappa statistic [Siegel and Castellan,
1988] to determine inter-observer agreement in whistle
classification 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 authors’classifications). When experts are in
complete agreement Fleiss’Kappa 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 identified: 309 (9.44%) were classified as having too
low signal-to-noise ratio whistles to be considered in this
study and 79 (2.41%) were classified as overlapping
whistles, the remaining 2,884 (88.14%) were classified in
signature or non-signature whistle types. Most of the
identified whistles were recorded during the first five
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 five
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 identified belonging to four different signature
whistles types (Fig. 2). The remaining 2,605 (90.32%)
were classified as non-signature whistle types. The four
signature whistles were present in the first five recording
sessions in November with nine individuals and in the last
five recording sessions in May with eight individuals. We
detected the occurrence of 210 signature whistles during
the first recording sessions and the occurrence of 69 signature
whistles during the last recording sessions.
The two visual classification tasks tested reliability of
identifying whistle types. The first task showed a low inter-
observer agreement (Fleiss’kappa 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 first task as the most
similar whistle to the template category. The inter-observer
agreement was high in the second task (Fleiss’kappa
statistic: k¼0.956, z¼28.7, P¼0.00001). These results
show that clearly defined 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 significantly 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 significance level of
P<0.0167) than before the training sessions. No significant
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 significance 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 first five recording sessions were carried out with the first social group (nine animals) and the last five 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
significantly before, during and after training sessions
(Friedman Rank Test: x
2
¼12.2, df ¼2, P¼0.0022):
dolphins emitted significantly more signature whistles
afterwards than before the training sessions (Wilcoxon
signed Rank Test: V¼0, P¼0.0019 with Bonferroni-
adjusted significance level of P<0.0167), but the animals’
signature whistle emission rate before and during the training
sessions did not show any significant variation (Wilcoxon
signed Rank Test: V¼30, P¼0.8457 with Bonferroni-
adjusted significance level of P<0.0167) nor between
periods during and after the training sessions (Wilcoxon
signed Rank Test: V¼0, P¼0.0195 with Bonferroni-
adjusted significance 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 identified 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 identified as variably loopy based on
the final 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 dolphins’whistle (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 dolphins’overall whistle emission
rate did not significantly 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 significantly 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 first
five 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 first
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. Mother–offspring 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
intraspecific social interactions conducted within the groups
might have influenced the number of whistles and signature
whistles recorded. We suggest that the presence of young
dolphins might have increased the number of affiliative, 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 specific [Caldwell et al., 1990] we could
Fig. 4. Boxplot of bottlenose dolphins’non-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 dolphins’signature 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 find nine signature whistles in the first 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 identified 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 influenced 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 find
the signature whistle for each member of the group.
The first classification task allows our study to be
comparable to previous studies that use visual categorization
of bottlenose dolphins’whistles as Janik [2000] and Kriesell
et al. [2014]. The low inter observer agreement obtained on
the first classification 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 fine
and leads to subjectivity. In fact when one of the authors
redid the first classification task several months later, the
inter observer agreement with herself was low (K¼0.133
z¼1.9, P¼0.0581). However, the second classification task
that asked the judges to choose the most similar whistles
showed a high inter observer agreement, which supports the
author’s visual categorization of the data set.
When we compared signature and non-signature
whistles, the total emission rate did not significantly change
before, during and after the training sessions. Our results
differ from previous findings 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 animals’free-time
without the presence of people, and during interactions
with people on a float 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
five 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 trainers’arrival [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.
Dolphins’behaviors and vocalizations can be modu-
lated by trainings [Kuczaj and Xitco, 2002]. Since no
information could be found about the influence 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 Ohta’s [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
Ohta’s [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 significantly 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 dolphins’signature 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 affiliative, 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 influence 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
influence 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
affiliative 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
specific [Caldwell et al., 1990], so it is highly probable
that the four signature whistles identified 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; Highfill and Kuczaj, 2007] that
leads to individual variation in vocal activity. Since group
composition and behavioral contexts influence 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 animals’behaviors 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 prolificvocal
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 2–3 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 classification
tasks and Isabella Clegg for revising the English of this
manuscript.
8Lopez Marulanda et al.
Zoo Biology

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