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Behavior and salivary cortisol of captive dolphins (Tursiops truncatus)
kept in open and closed facilities
Cristian Ugaz
a
, Ricardo A. Valdez
b
, Marta C. Romano
b
, Francisco Galindo
a
,
*
a
Departamento de EtologÍa y Fauna Silvestre, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México, Ciudad Universitaria,
México D.F., México
b
Departamento de FisiologÍa, BiofÍsica y Neurociencias, CINVESTAV, México D.F., México
article info
Article history:
Received 10 May 2012
Received in revised form 8 August 2012
Accepted 25 October 2012
Available online 27 December 2012
keywords:
dolphins
behavior
salivary cortisol
welfare
abstract
Few studies have been carried out on the welfare of captive bottlenose dolphins (Tursiops
truncatus). Of these, most include information on animals kept in closed facilities or pools.
The aim of this study was to assess the welfare of captive bottlenose dolphins in open and
closed facilities by measuring states of individual behavior and salivary cortisol concen-
trations. A total of 23 bottlenose dolphins were studied in 4 different dolphinaria. Dol-
phinaria A and B have closed facilities, whereas dolphinaria C and D have open facilities. A
total of 152 hours of behavioral observations were analyzed using a combination of
behavior and scan sampling to obtain information on individual time budgets. Salivary
cortisol concentrations were measured using radioimmunoassay in 96 and 180 saliva
samples of dolphins kept in closed and open facilities, respectively. In general, the results
found that dolphins kept in open facilities spent less time floating (P<0.05) and swim-
ming in circular patterns than linear ones (P<0.05) compared with dolphins in closed
facilities. Dolphins kept in open facilities also had lower salivary cortisol concentrations
than dolphins kept in closed facilities (P<0.05). For this reason, we suggest that further
research should include other welfare indicators such as reproductive function and health
measurements to know more about the relationships between the design of pools and
dolphin welfare.
Ó2013 Elsevier Inc. All rights reserved.
Introduction
The behavior of any wild species is the result of many
generations of natural selection and adaptation to the
environment. The ability to cope with changes in the
environment such as those related to captivity depends on
a complex interplay of biological factors (Mason, 1990;
Shepherdson, 1994;Carlstead, 1996;Poole, 1998). The
welfare of many species of terrestrial mammals has been
studied (Carlstead, 1996), but little information is available
on marine mammals in captivity (Pedernera-Romano et al.,
2006;Luna, 2008). Bottlenose dolphins (Tursiops truncatus)
in captivity are still used for entertainment and assisted
therapy in several countries. It is known that these animals
have to adapt to changes in their physical and social envi-
ronments as a result of the design of the enclosures where
they are kept, changes in food presentation, and also
because of changes in their social structure (Pedernera-
Romano et al., 2006).
It is well known that stress induces behavioral changes
(Fowler, 1986;Dierauf, 1990;Waples and Gales, 2000) that
could be related to prolonged adrenalactivity and long-term
welfare and health problems (Moberg, 1985;Broom and
Johnson, 1993;Fowler, 1995;Chrousos et al., 1998;
Sapolsky et al., 2000;Reeder and Kramer, 2005).
*Address for reprint requests and correspondence: Francisco Galindo,
PhD, Departamento de Etologia y Fauna Silvestre, Facultad de Medicina
Veterinaria y Zootecnia, Universidad Nacional Autónoma de México,
Ciudad Universitaria, 04510 México D.F, México. Tel: þ52-56225941; Fax:
þ52-56225942 or þ52-55508697.
E-mail address: galindof@unam.mx (F. Galindo).
Contents lists available at SciVerse ScienceDirect
Journal of Veterinary Behavior
journal homepage: www.journalvetbehavior.com
1558-7878/$ –see front matter Ó2013 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.jveb.2012.10.006
Journal of Veterinary Behavior 8 (2013) 285–290
Some studies carried out with bottlenose dolphins have
been useful for understanding general aspects of their
maintenance behaviors in captivity (Gygax, 1993;Sobel
et al., 1994;Small and DeMaster, 1995;Bassos and Wells,
1996;Galhardo et al., 1996;St. Aubin and Dierauf, 2001;
Sekiguchi and Kohshima, 2003;Ugaz et al., 2009). Fewer
studies, however, have assessed adrenal function through
measurements of plasma, serum, and salivary cortisol
(Thomson and Geraci, 1986;St. Aubin, 1996;Ortiz and
Worthy, 2000;St. Aubin, 2001;Suzuki et al., 2003;
Pedernera-Romano et al., 2006;Noda et al., 2007). Salivary
cortisol of dolphins has proven to be a noninvasive proce-
dure of great value when repeated sampling is necessary as
its collection is potentially stress free and practical
(Pedernera-Romano et al., 2006). So far, most of this
information has been obtained from dolphins kept in dol-
phinaria with closed pools. A recent study that compared
the behavior of 10 dolphins that were kept in pools
and moved to open sea enclosures showed that the
behavior of dolphins varies according to the type of facili-
ties (Ugaz et al., 2009). The results show that when
dolphins were kept in closed facilities they spent less time
swimming and more time floating than when in open
facilities. Dolphins in closed facilities tend to swim in
circles, whereas those in open facilities spend more time
swimming in linear patterns. Furthermore, dolphins kept in
closed facilities spent more time interacting socially than
those in open facilities. For these reasons, the aim of this
study was to compare individual and social behaviors, as
well as salivary cortisol, of different groups of captive bot-
tlenose dolphins kept in open and closed facilities. This
information can enhance our knowledge of how the char-
acteristics of open facilities for captive dolphins may
influence their behavior and adrenal activity in comparison
to closed pools.
Methods
Locations and animals
A total of 23 bottlenose dolphins were studied in 4
different dolphinaria.
Dolphinaria A and B have closed facilities, whereas
dolphinaria C and D have open facilities (Table 1). A closed
facility was defined as a pool with no access to the sea and
with treated water, whereas an open facility was defined as
a pen, usually designed as a dock, with access to the sea and
seawater and contained within a fence.
The average age of the dolphins studied was 16.3 years
old (age range, from 11 to 24 years) with 6 males and 17
females (Table 1). All individuals were adults andhealthy at
the time of the study. All were captured in the Gulf of
Mexico, and they had an average of 9.5 years in captivity
(range, from 8 to 15 years). All dolphins, both in closed and
open facilities, were fed with the same species of fish:
capelin (Mallotus villosus), Atlantic Herring (Clupea hare-
ngus), and squid (Loligo patagonica,Loligo gahi,orLoligo
vulgaris). The aquariums were opened to the public and
regularly hosted interactive swimming sessions. The 4
dolphinaria had 5 interactive sessions per day, each lasting
40 minutes to every 80 minutes. The first interactive
program is at 9:30
AM
and the last one at 15:00. The
observations were not conducted during an interaction or
performance session.
Closed facilities
Dolphinarium A is a round pool with a conical bottom
reaching a maximum depth of 5 m and with a capacity of
196 4 m
3
. It is located in Mexico City at 2240 m above sea
level. Dolphinarium B is a rectangular pool, with an average
depth of 4 m, subdivided into a main area of 60 20 m and
4 small (5 10 m) holdings or pens, 2 at each end. It has
total capacity of 5600 m
3
and is located on the Pacific coast
of central Mexico.
Open facilities
Dolphinarium C is located on the east coast of the
Yucatan Peninsula. It is an artificial breakwater with access
to the sea allowing the exchange of seawater and small fish
and other marine species. It has a maximum depth of 3.5 m,
a total volume of 6074 m
3
, and is subdivided into 2 areas of
equal size with a dock separation and an oval rubble quay.
Dolphinarium D is located in the north coast of the Yucatan
Peninsula. It has 3 holdings or pens each of 33 10 m,
separated by an open fence and with access to a central
area of 100 35 m, with a maximum depth of 4 m, and an
estimated total water capacity of 26,250 m
3
(Table 2).
Table 1
Individual dolphins kept in the 4 dolphinaria studied
Dolphinaria Facilities ID Sex Age (y) Time in captivity (y)
A C 1 Female 12 þ8
A C 2 Male 18 þ15
B C 3 Female 12 þ8
B C 4 Female 14 þ8
B C 5 Female 14 þ8
B C 6 Male 15 þ8
B C 7 Male 18 þ8
B C 8 Male 17 þ8
C O 9 Male 18 þ10
C O 10 Female 14 þ10
C O 11 Female 12 þ9
C O 12 Female 11 þ8
C O 13 Female 16 þ8
D O 14 Male 16 þ10
D O 15 Female 24 þ10
D O 16 Female 18 þ10
D O 17 Female 17 þ10
D O 18 Female 16 þ10
D O 19 Female 18 þ10
D O 20 Female 16 þ10
D O 21 Female 18 þ10
D O 22 Female 18 þ10
D O 23 Female 22 þ10
Facilities are marked as C ¼closed and O ¼opened.
Table 2
Size of the pools in each dolphinarium
Dolphinaria Length
(m)
Width
(m)
Minimum
depth (m)
Maximum
depth (m)
A 25 25 3.5 5
B702044
C 75 30 3 3.5
D 100 45 3.5 4
C. Ugaz et al. / Journal of Veterinary Behavior 8 (2013) 285–290286
Measurements of behavior
A behavioral catalog was adapted from Galhardo et al.
(1996),Miguel (2004), and Singh (2005) using 48 hours
of ad libitum sampling during day and night completing
two 24-hour cycles. During this time, individuals were
identified by their distinctive natural marks. Data were
collected through direct observations using a combination
of behavior and scan sampling (Martin and Bateson, 1993)
over 48 hours divided in 2 cycles of 24 hours, distributed
over 6 days, and divided into 4 hours every day. Observa-
tion periods were divided as follows: day 1, 0800–1200;
day 2, 1200–1600; d ay 3 , 160 0 –2000; day 4, 2000–2400;
day 5, 2400–0400; and day 6, 0400–0800. In total, 152
hours of behavioral observations were analyzed, 58 hours
in closed facilities, and 94 hours in open facilities. This
information was used to obtain individual time budgets.
The behaviors observed and recorded were total time
swimming (TTS) when a dolphin was moving and total time
floating when the dolphin was static. TTS was divided into
linear swimming (LS), when a dolphin swam alone in
different directions covering the entire length of the pool,
without a fixed circular pattern; and circular swimming
(CS), when a dolphin swam in a circular pattern. LS was
subdivided into deep swimming (DS), when animals swam
in different directions with their dorsal fin always under
the water and superficial swimming (SS), when dolphins
swam in different directions with at least one part of the
dorsal fin out of the water.
For each animal, the time spent in behaviors during the
study was expressed as proportion of time calculated as
follows: number of observations of a behavior divided by
total minutes observed. The term time budget was defined
as the summed proportions (total 100%) of these behaviors.
Saliva samples and cortisol analysis
The dolphins that participated in this study were
trained to emerge from the water and open their mouths
voluntarily, thereby assuring a noninvasive procedure to
obtain the samples. Saliva samples were obtained on the
same day that observations were carried out and before the
first meal of the day. This was always between 9:00
AM
and
9:30
AM
, 16 hours after the last activity with the trainer.
Before saliva collection, all cotton swabs were washed with
ether (which evaporated completely before use) to elimi-
nate all organic residues. When taking the sample, the
swab was introduced up to the base of the tongue and
placed in a sterile plastic tube.
The swabs were then centrifuged at 3000 rpm, and the
sample of saliva was stored at 20
C until assayed. In total,
276 saliva samples were collected, 12 from each animal, 96
samples in closed facilities and 180 in open facilities.
Radioimmunoassay kits of iodine-125 (Cort CT2; CIS Bio
International, France) were described by Pedernera-
Romano et al. (2006).
The kits have an affinity of 100% to serum, urine, and
salivary cortisol, and cross-reaction with prednisolone
(42%), fludrocortisone (12.1%), forticosterone (2.8%), pred-
nisone (1.2%), cortisone (0.9%), and less than 1% with other
similar metabolites. The intra- and interassay coefficients of
variation were 9.01% and 10.9%, respectively.
Statistical analysis
Data were analyzed using SAS, version 6.0 (Manufac-
turer SAS Instituted, Cary, North Carolina). Kolmogorov–
Smirnov tests of normality were applied to variables of
behavior, and the results were notsignificant (P>0.05). For
this reason, an analysis of variance test was used to
compare behavior and average salivary cortisol levels
between all facilities.
Results
Behavior
When behaviors were compared between groups,
statistical differences were found (Table 3). The time
swimming was higher, and the time floating was lower, in
dolphinaria C and D (F¼27.37, P<0.001) compared with
dolphinaria A and B (F¼10.83, P<0.001, Table 3),
respectively. There were also differences in the types of
swimming: the time spent in LS was lower in dolphinarium
A(F¼36.31, P<0.0001, Table 3) than in the other 3 groups,
and the time spent in CS was lower in dolphinarium D
(F¼17.46, P<0.001, Table 3). Finally, there were differ-
ences in the time spent in the 2 types of LS: the time in SS
was higher in dolphinarium A (F¼5.45, P<0.01), and the
time in DS was lower compared with dolphinaria B, C, and
D(F¼36.33, P<0.001, Table 3), respectively (Figure 1).
Salivary cortisol
Salivary cortisol levels ranged from 0.0116 to 1.5109
nmol/L with an average value of 0.3293 nmol/L. When the
average salivary cortisol values were compared between
Table 3
Comparison of behaviors and salivary cortisol levels between dolphinaria (average standard error)
Variable Dolphinarium A Dolphinarium B Dolphinarium C Dolphinarium D
TTS (%) 62.87a 13.97 71.76a 7.73 90.95b 2.96 93.98b 1.88
LS 21.73a 5.16 58.10b 10.49 66.39b 17.66 92.77ab 2.06
SS 10.61a 2.81 4.63b 2.72 3.34b 1.58 6.52ab 2.34
DS 11.12a 4.69 53.48b 12.38 63.05b 16.21 86.24ab 3.54
CS 41.14a 24.10 13.66b 5.04 24.56a 15.97 1.21ab 0.70
TTF (%) 37.13a 11.26 28.24a 7.73 9.05b 2.96 6.01b 1.87
Cortisol (nmol/L) 1.40a 1.10 0.65a 0.17 0.30ab 0.10 0.09b 0.02
Different letters (a, b, and ab) in each column represent statistical differences between groups.
TTS, total time swimming; LS, linear swimming; SS, superficial swimming; DS, deep swimming; CS, circular swimming; TTF, total time floating.
C. Ugaz et al. / Journal of Veterinary Behavior 8 (2013) 285–290 287
groups, it was found that dolphins in dolphinaria A and B
had higher values than those kept in dolphinaria C and D
(F¼49.89, P<0.001, Table 3;Figure 2).
Discussion and conclusions
These results demonstrate that the enclosure type
influences the behavior and salivary cortisol concentrations
of captive bottlenose dolphins. Dolphins that were kept in
open facilities were more active and spent more time
swimming in a linear pattern than dolphins that were kept
in closed facilities. Furthermore, dolphins in closed pools
show higher salivary cortisol concentrations than those
individuals housed in open pens.
Previous studies carried out with dolphins housed in
pools or closed facilities have shown that these animals
spent most of the time swimming in a continuous circular
pattern (Gygax, 1993;Galhardo et al., 1996;Singh, 2005).
These results, supported by the fact that dolphins housed in
open facilities spent more time swimming in a linear
pattern, suggest that the lack of space and depth in a pool,
compared with an open pen, plays a role in this change of
behavior. It is likely then that the shape and size of the
pools could influence the type and intensity of the swim-
ming patterns (Sobel et al., 1994). In this sense, it would
also be important to further investigate the possible rela-
tionship of this swimming pattern with an abnormal
behavior, as previously suggested (Gygax, 1993).
Figure 1. Average time budgets in the 4 groups of dolphins observed. Total time swimming (F¼27.37, P<0.001), total time floating (F¼10.83, P<0.0 01), linear
swimming (F¼36.31,P<0.0 001), circular swimming (F¼17.46, P<0.001), superficial swimming (F¼5.45, P<0.01), and deep swimming (F¼36.33, P<0.001).
C. Ugaz et al. / Journal of Veterinary Behavior 8 (2013) 285–290288
Although we found that CS was less frequent in open
than in closed facilities, there was also a difference in this
behavior between open facilities. This could be attributed
to one of the dolphins in dolphinaria C that showed this
behavior more frequently close to the medical area,
possibly related to having spent some time there soon
before the start of this study and to the close presence of
the trainers in that section of the pool.
Also, the fact that dolphins in closed facilities were less
active supports previous studies (Bassos and Wells, 1996;
Singh, 2005) that reported that dolphins spent a greater
proportion of time at rest in smaller pools than in bigger
ones. These results suggest that the occurrences of passive
states of behavior in small and closed pools could be related
to the quality of the space and how the animal perceives it.
Several authors have reported a CS pattern of bottlenose
dolphins in captivity (Sobel et al., 1994;Bassos and Wells,
1996;Miguel, 2004;Singh, 2005). To know more about
the implications of these behaviors, it is important to
investigate how they relate to both external and internal
stimuli, such as the design and size of a pool, water
currents, and laterality behaviors (Gygax, 1993;Marino and
Stowe, 1997;Sekiguchi and Kohshima, 2003;Stafne and
Manger, 2004).
Considering the fact that most dolphins sampled for
saliva collection in this study were trained to open their
mouth voluntarily, the hormone concentrations obtained
from the dolphins studied could be considered as non-
stressed cortisol values. The results show, for the first time,
salivary cortisol measurements of dolphins kept in open
facilities with open access to seawater. The values obtained
in this study from dolphins kept in closed facilities are
similar to those found by Pedernera-Romano et al. (2006)
for similar types of pools. However, the values of salivary
cortisol in open facilities were lower. Carlstead (1996)
argues that limited space, and inadequate environmental
stimuli, among other factors, can be stressful. It could be
argued that dolphins kept in open facilities are exposed to
more diverse stimuli related to the space available and to
the fact that these facilities have access to the sea and,
hence, increase swimming in slow linear patterns and have
lower salivary cortisol levels. Although information on
social interactions was not included in this analysis, it is
important to consider in future studies a possible link
between aggression and cortisol levels, especially in closed
facilities.
In summary, this study demonstrates that dolphins kept
in open facilities show different swimming behaviors and
lower salivary cortisol concentrations than those kept in
closed facilities. It should be noted that it is likely that
dolphins in open facilities also have to cope with problems
associated with that type of facilities. To better understand
these relationships, we suggest that further research using
other welfare indicators, apart from behavior and adrenal
activity, could be carried out to assess the welfareof captive
dolphins. Such welfare indicators could include reproduc-
tive function, through measurements of hormonal profiles,
offspring survival, or semen quality, among others; as well
as epidemiological studies, health records, and survival
rates. This could also help to know more about the bio-
logical significance of many of the behavioral changes seen
in this species when they are kept in captivity.
Acknowledgments
The program Programa de Apoyo a los Productos de
Investigación e Innovación Tecnológica de la Universidad
Nacional Autónoma de México IN223106 supported this
study. We are very grateful to the dolphinaria that partici-
pated in this study and acknowledge the support given by
Dirección General de Asuntos del Personal Académico de la
Universidad Nacional Autónoma de México to Dr. Francisco
Galindo to conclude the analysis and writing of this article.
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