Social interaction analysis in captive orcas (Orcinus orca)

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Zoo Biology. 2019;1–11. wileyonlinelibrary.com/journal/zoo © 2019 Wiley Periodicals, Inc. | 1
Received: 29 July 2018 | Revised: 18 April 2019 | Accepted: 24 May 2019
DOI: 10.1002/zoo.21502
R E S EARCH AR T I C L E
Social interaction analysis in captive orcas (Orcinus orca)
Paula Sánchez–Hernández1 | Anastasia Krasheninnikova2,3 | Javier Almunia4 |
Miguel Molina–Borja1
1Grupo de investigación “Etología y Ecología
del Comportamiento”, Fac. Ciencias,
Universidad de La Laguna, Tenerife, Spain
2Max–Planck Comparative Cognition
Research Group, Tenerife, Spain
3Department of Behavioural Neurobiology,
Max–Planck Institute for Ornithology,
Seewiesen, Germany
4Loro Parque Fundación, Tenerife, Spain
Correspondence
Paula Sánchez–Hernández, Asociación
Bienestar Ambiental, C/ Henry Dunant, s/n,
38203 La Laguna, Tenerife, Canary Islands,
Spain.
Email: paula.s.hernandez@gmail.com
Funding information
Loro Parque Fundación
Abstract
The management of socially complex species in captivity is challenging. Research on
their social behavior improves our understanding of interactions in captive animals
and captive‐group management. We conducted a detailed analysis of social
relationships shown by the orcas kept at Loro Parque zoo and their tendency to
reconcile after aggressive episodes. Affiliative interactions were the most frequent
social activities compared to agonistic or sexual interactions. Within affiliative
behaviors, we documented the pattern “gentle tongue bite”, where an animal touches
the other’s tongue with his teeth but does not bite it. Affiliative interactions between
a specific pair of orcas occurred significantly more often than expected by chance,
and together with low levels of agonistic interactions, indicated particular affinity
between some individuals. The most frequently observed low‐level agonistic
relationship was that of the two older males (Tekoa–Keto); however, they also
showed frequent sexual and affiliative interactions. Sexual‐like behaviors (pursuit,
mount, and penis between males) were found in both sexes. Finally, the observed
corrected conciliatory tendency (31.57%) was within the range described for other
primate and cetacean species. This study provides a systematic way to assess social
interactions as well as conflict management strategies in cetaceans housed in zoos
and zoo‐like facilities and may help to improve animal welfare and management of
animals in controlled environments.
K E YWORD S
captivity, conciliatory tendency, ethogram, orcas, social behavior
1 | INTRODUCTION
Keeping animals with a complex social structure in controlled
environments is challenging. The knowledge about individual
behavioral patterns and social interactions among conspecifics is
crucial for optimizing group management and welfare for individuals
living under human care. This is especially the case for marine
mammals such as bottlenose dolphins (Tursiops truncatus) and orcas
(Orcinus orca). In recent decades, there have been a growing number
of studies on behavioral aspects of these species in the wild (Baird &
Dill, 1995, Baird and Whitehead 2000, Foster et al., 2012, Ivkovich
et al., 2010).
However, only a few studies provide detailed descriptions of
behavioral patterns in orcas. The most recent ethograms for this
species date back from 1970s to 1980s (Martinez & Klinghammer,
1978; Salden, 1980). Orcas share several behavioral patterns with
other cetacean relatives; one of the most apparent observed in many
cetaceans, primarily odontocetes, is the strong tendency to move in
groups (Caldwell & Caldwell, 1966). Moreover, sometimes orcas
perform diving and surfacing synchronously (Christensen, 1978) and
this synchrony in movements and respiration, observed in both wild
and captive individuals, has been suggested to be an indicator of the
affinity among them (Jacobsen, 1986; Ray, Carlson, Carlson, &
Upson, 1986).
mailto:paula.s.hernandez@gmail.com
Studying individual behavioral repertoire as well as social
interactions provides data that might indicate the well‐being status
of animals. For example, it has been shown for dolphins that
performing a wide range of behavioral patterns, including social
interactions as well as swimming without a circular pattern, is a
positive indicator of well‐being (Ugaz, Sánchez, & Galindo, 2009;
Ugaz, Valdez, Romano, & Galindo, 2013). On the contrary, long
periods of inactivity are reactions related to aversive events such as
the death of conspecifics (Ray et al., 1986).
Another crucial issue regarding animal welfare in controlled
environments is the management of social conflicts of animal groups
under human care. Social conflict is inevitable in highly social species,
but may compromise the benefits of group living, especially when it
escalates into aggression. In wild primates, for example, aggression
may even force the loser of the conflict to leave the group (Janson,
1992). In a controlled environment, where it is not possible to avoid a
potential escalation of a conflict (unless the animals are separated in
different environments), this might lead to the increased stress level,
cause injuries, and impact the well‐being of an animal. It is thus
crucial to have an objective and measurable understanding of specific
relationships among members of a social group to take management
decisions and minimize the stress and damage to the group.
Cetaceans housed in zoo settings may experience social stressors
from inappropriate groupings, social changes, and subordinations (Waples
& Gales, 2002). Indeed, studies revealed that conflicts among bottlenose
dolphins in zoo settings appear to be related to dominance relationships
resulting from instability in social interactions (Yamamoto et al., 2015).
Previous work indicates that adult males were consistently dominant to
adult females, whereas the dominance relationships among adult males
were more unstable (Samuels & Gifford, 1997). Similar social stressors
are likely to be a factor for an increased conflict potential in killer whales
under human care as well. Also, aggressive behavior in both species
appears to be associated with consistent vocal pattern (Herzing, 1996;
Graham & Noonan, 2010). In addition, the study of natural behavioral
mechanisms for conflict management is of paramount importance, not
only for captive management but to understand the group structure of
long‐lived species with stable social groups. A strategy to repair and
maintain the integrity of social relationships damaged as a result of a
conflict between social partners in reconciliation behavior (van Schaik,
1989). This mechanism of conflict resolution occurs after aggressive
escalation, especially in form of affiliative postconflict (PC) reunions
between former opponents (Aureli & de Waal, 2000). Most of the
systematic research on reconciliation behavior has been done in non‐
human primates (see de Waal, 2000 for a review), but in the past
decades, it has been extended to various non‐primate species (Cools, van
Hout, & Nelissen, 2008; Cordoni & Palagi, 2008; Cozzi, Sighieri, Gazzano,
Nicol, & Baragli, 2010; Fraser & Bugnyar, 2011; Schino, 1998; Seed,
Clayton, & Emery, 2007; Wahaj, Guse, & Holekamp, 2001), and more
recently to bottlenose dolphins (Tamaki et al., 2006; Weaver, 2003;
Yamamoto et al., 2015). However, to our knowledge, no reconciliation
behavior in an orca group has been described yet.
Therefore, taking all the above into account, the aims of the present
study were (a) To conduct a detailed analysis (description and
quantification) of social behaviors shown by the orcas kept in pools at
Loro Parque, (b) to analyze agonistic, affiliative, and sexual relationships
among the group members, (c) to investigate PC reconciliation behavior
in the study group.
2 | MATERIALS AND METHODS
2.1 | Animal subjects
Six orcas, three females and three males, were observed at Loro
Parque Zoo (in Tenerife, Spain), during a 3‐month studyperiod in
2013. All of them, except one female, were captive‐bred, the
background of the individuals included in the present study is
summarized in Table 1. The youngest male (Adán, hand‐reared) was
being introduced into the group at the time of the study, and it was
not yet in contact with the oldest male. Consequently, there were
few observations of him interacting with the entire group, and his
data was not included. Animals in the group did not have any know
pathologies that might affect their behavior, except Morgan, a young
female rescued from the Wadden sea in 2010 that was integrated in
the group 1 year before the study, and later diagnosed with a severe
hearing loss (Lucke, Finneran, Almunia, & Houser, 2016).
2.2 | Facility and recording equipment
The orcas were housed in a multipool facility with 22.500 m3 of
total volume (Figure 1). The main pool (A) was 12 m depth, and
half of its surface was covered with a white canopy supported by
a curved central beam reaching 25 m of height above water level
at its central point. At the highest point of the central beam, a
remotely operated high‐resolution camera (AXIS® 232D DOMO)
gives a full view of the pool A with a zenithal perspective, and
oblique views of pool B (full), C (partial), and the medical (full)
pool. Other four cameras (AXIS® Q1755) give orthogonal
underwater perspectives of pool A, though they do not cover
the whole basin. The zenithal camera could rotate on a Domo
housing and zoom in to follow specific animals in detail. Its
placement allowed observations either on the surface and
underwater, minimizing reflections. It was manually operated
TABLE 1 Birth dates, sex, body lengths, and weights of the six
animals at the time of the study
Birth Date Sex
Body
length (m) Weight (kg)
Keto 17 June 1995 Male 6.0 3,454
Tekoa 8 November 2000 Male 5.6 2,223
Kohana 3 May 2002 Female 5.2 1,814
Skyla 2 February 2004 Female 5.2 1,798
Morgan Unknown
(2002–2008)*
Female 4.7 1,488
Adán 11 October 2010 Male 3.8 717
*Morgan’s birth date range was estimated from her length at the rescue in
2012 when she arrived at Loro Parque.
2 | SÁNCHEZ–HERNÁNDEZ ET AL.
with a joystick (Remote Control Unit RM‐BR300; SONY®) from a
control booth located in the center of the amphitheater, with a
full view over the facilities and equipped with three monitors that
could be connected to different channels (cameras) through a
digital production switcher (Synergy 100; ROSS®). All the outputs
from the cameras and the control board were continuously
recorded and time tagged in an 8 channel VDR (PEGASO‐H960‐
08; IPTecno®) and automatically stored in a hard drive for 15
days. One of the researchers operated the joystick and the
control board to follow a focal animal (Altmann, 1974) during
observation periods that were approximately 15 min in length; he
selected the most appropriate camera in each situation and sent
the resulting footage to the output channel of the control board.
The Digital Video Recorder stored each channel in 1 hr video
files, and the video files from the output channel covering the
observation time were downloaded and stored in DVDs daily.
The number of observational periods and time analyzed by the focal
animal (see Table 2).
2.3 | Ethical consideration
The protocol and procedures used were ethically reviewed and approved,
agree to Directive 2010/63/EU. As we video‐recorded the individuals
through the installation’s cameras, our investigation did not influence the
everyday normal dynamic of the animals. Moreover, we did not use any
intervention procedure which could affect the normal activities of the
studied animals.
2.4 | Enrichment program
The enrichment program for the marine mammals used in Loro
Parque aimed to improve animal’s welfare by promoting natural
behaviors and stimulating them physically and mentally. The
enrichment included different types of activities and consisted of
the following categories:
(a) Social: involving changes in the social dynamics of individuals to
enhance cooperation, interaction, or communication skills
between the animals and even the trainers.
(b) Sensory: which stimulates animals’ senses—visual, olfactory,
auditory, tactile, and so forth.
(c) Food: dietary changes, both at the variety of food and in terms of
the presentation to promote foraging behaviors as they would in
the wild and increase feeding time.
(d) Environmental/Structural: to enhance the animals’ habitat with
opportunities that change or add complexity to their environ-
ment.
(e) Cognitive: to enhance the development of cognitive abilities of
animals, by promoting thinking and problem‐solving activities or
F IGURE 1 Orca pool disposition,
measurements, and identification in the
facility of Loro Parque, Tenerife. (a) Main
pool: 12m depth; maximum horizontal
width, 24,5 m; maximum horizontal length,
50.8. Med pool: 4.2 m depth; maximum
horizontal width, 7.1 m; maximum
horizontal length, 12.4. (b) Holding pool:
18.1 m depth, maxim horizontal width,
30.5 m; maximum horizontal length, 44.8.
(c) Holding pool 28.1 m depth; maximum
horizontal width, 20.5 m; and maximum
horizontal length, 36.5
TABLE 2 Number of focal periods and total time by animal
Number of focal periods Total focal time HH:MM
Keto 60 17:11
Tekoa 77 18:18
Kohana 63 15:54
Skyla 74 20:46
Morgan 67 18:57
Adán 37 10:08
SÁNCHEZ–HERNÁNDEZ ET AL. | 3
facilitating animals to regain a certain control over their
environment to mentally stimulate them.
(f) Physical: aimed to increase the amount of physical exercise
performed by the animals.
Depending on the time schedule, the trainers combined the
different enrichment categories and adapted them to ensure
variability in the daily enrichment plans to avoid that the animals
get used to and expect a specific enrichment activity.
2.5 | Behavioral observations
From the recorded videos, one observer (P.S.H.) followed each focal
orca and noted each behavior pattern performed in a database
(Filemaker®). Every behavioral record included a time tag, the
location (pool), the identity of the focal animal and the other animals
in the pool, the behavior performed and for social behaviors the
individuals directing and receiving the behavior. To establish the
behavior patterns to be considered, we used an ethogram based on
Martinez and Klinghammer (1978) and Salden (1980) and our own
previous observations. To avoid human interference, the recordings
were only performed when animals not being trained by the staff. To
check if animal behavior could be modified by the trainers walking
around in nontraining periods, the recordings were classified into two
types: those with potential human presence (PHP; time slots when
animals were left at their own will, between training or feeding
sessions, public presentations, etc., when staff could be present in the
area but they did not interact with the animals) and those with no
human presence (NHP; after the trainers left the facility at 18:00 hr
and before they came in the next day at 08:00 hr). A total of 100 hr
and 30min of behavioral observations were analyzed: 50 hr for the
period “PHP” and 50.5 hr for the period “NHP”. All observations took
place only during the daylight.
Moreover, to establish social relationships among every pair of
orcas, behavior patterns were classified into three general categories
(see ethogram): affiliative, sexual, and agonistic. However, some of
the behavior patterns were categorized differently depending on the
behavioral context; for example “rub” could be sexual if any other
sexual pattern appeared, or affiliative if not. We considered as
affiliative behaviors all activities that individuals performed close
together, except those judged to be agonistic. Agonistic behaviors
were those that appeared to be aggressive or defensive patterns.
Sexual behaviors were those previously described in the literature
and others involved in that context (pursuit or rub). Allother
behavior patterns shown by the orcas were classified as “nonsocial”
(see ethogram in Section 3).
2.6 | Data analysis
Behaviors were initially quantified calculating percentages of time all
orcas showed each category (see Figure 2); Afterward, the relative
frequencies were calculated for each behavior pattern by dividing
their number by the total recorded time for each orca. These relative
frequencies for each individual and from each behavioral category
were initially used to compare PHP vs NHP periods. As significant
differences were not found between these two periods for any
behavioral category (Wilcoxon test, Affiliative: Z = −1.066, p = .286;
Sexual: Z = –1.53, p = .249; and Agonistic: Z = −0.943, p = .219), the
complete data set was used for all subsequent statistical analyses.
Moreover, for social interactions as all individuals were not
present in all the observations, and stayed together different
times, we calculated for every behavior pattern within each
categories relative frequency dividing the number of occurrences
by the time together of every dyad (combination of two animals
in social interaction). To determine the more probable type of
social interaction between pairs of individuals, and as individuals
were not grouped all together in all the observations, for each
dyad and the behavioral category we calculated relative fre-
quency dividing the number of occurrences of all behavior
patterns by the total time each dyad were together. These
fractions were then multiplied by a constant (100) to avoid
numbers close to zero that can affect the precision of the test.
These data were used to fill matrices for every behavioral
category (affiliative, sexual, and agonistic) thus reflecting the
relative frequency of interactions for all possible combinations of
individuals. The matrices were then used to study independence
in the behavior between the dyads using a row‐wise matrix
correlation. With this calculation, we use an iterative procedure
F IGURE 2 Percentage of cases that each behavioral category was
shown by the study subjects within each period. NHP, no human
presence; PHP, potential human presence
4 | SÁNCHEZ–HERNÁNDEZ ET AL.
to calculate impute variable of the empty diagonal cells. These
imputed values are equal to the expected values calculated in the
full matrix. This procedure allows computing the expected values
and residuals for all cells of the matrix. As the residuals of the
diagonal cells are equal to zero they do not contribute to the χ2
value of the matrix (van der Heijden et al., 1990). The adjusted
residuals greater or less than 1.96 can be considered significantly
greater than expected by chance (Haberman, 1973). Therefore,
within each of the agonistic, sexual, or affiliative categories,
positive or negative residuals indicate those dyads that inter-
acted more or less frequently than expected by chance. There-
fore, within each of the agonistic, sexual, or affiliative categories,
positive or negative residuals indicate those dyads that inter-
acted more or less frequently than expected by chance.
Reconciliation analysis was based on the hypothesis that the
probability of social contacts with opponents was affected after
conflicts and checked using the PC/matched‐control or PCMC
model (De Waal & Yoshihara, 1983). Description of conflict in
dolphins (Holobinko & Waring, 2010; Weaver, 2003) was used to
determine this type of situations in the group of orcas. We
defined conflict when at least two consecutive agonistic patterns
occurred between two animals and one of them involved physical
contact (push or tail kick, principally); in this way, we avoided the
inclusion of isolated and instantaneous behaviors (adaptation of
Weaver, 2003). Conflicting situations were thus identified and
located in the database to establish the conflict (C) and PC
periods; if the conflict was resumed within 5 minutes it was
considered unfinished, and the onset of the PC period postponed.
This criterion ensured that PC contacts were only considered
when the conflict was finished.
To obtain a baseline for the affiliative behaviors out of a PC
period we set up matched‐control observations (MCs). These
MCs were done during the study period out of PC periods with
the same animals and time corrected to ensure that the control
data had the same distribution over the group members. We then
compared latency times to the first‐affiliative pattern during PC
and MC periods. Pairs in which the affiliative latency PC was
lower than during the control periods were labeled as “Trend to
reconciliation” and were marked with (a), when the affiliative
latency during PC was greater than the average, pairs were
labeled as “No trend to reconciliation” (b), and when opponents
showed the same latency to making contact in both PC and MC
periods or did not make contact in none of them, they were
classified as “neutral pairs” (c).
Following the standard primate behavior research methods,
these results were used to calculate a corrected conciliatory
tendency (CCT; adapted from Veenema, Das, & Aureli, 1994) with
the formula: a − b/(a + b + c). We calculated a CCT index to
understand any increase in affiliative behaviors (Veenema, Das, &
Aureli, 1994). This CCT reflects the increase in affiliative interactions
due to the preceding conflict over the baseline levels. Finally, we
applied a Wilcoxon test to compare latency times between MC and
PC periods.
3 | RESULTS
3.1 | Behavioral analysis
A detailed description of all registered behavior is presented in Table
2. The main behaviors analyzed in each category were:
Affiliative behaviors: swimming together “swimming”, sometimes
including synchronized swimming “Synchro”, exploring the holes
“holes”, exploring the water jet “water jet”, staying close to the gates
between the pools “door”, playing in group “social play” sometimes
including “gentle tongue bite” and resting together “rest”.
Common sexual behaviors consisted of “genital”, “mount”, “penis”,
“ventral‐ventral”, “pursuit”, and sexual “rub”.
The behavioral patterns observed within an agonistic context were
“chase”, “dip push”, “bite”, “rake”, “ram”, and “tail kick”. A description of a
typical behavioral sequence within each category will be provided in
results.
The analysis of the recordings revealed 29,818 behavioral patterns,
the vast majority of them being non‐social activities (85% of cases for
PHP and 90% for NHP; Figure 2). The most frequent social activities
were affiliative behaviors, amounting to 12% during the PHP period and
9% during the NHP period, respectively. The animals showed sexual
patterns in 1% in both periods. Furthermore, agonistic behaviors were
observed in 2% of the time or cases recorded when the staff was
potentially present, but less than 1% in the period “NHP”.
Within the affiliative category, the most common behavior was
“swimming together”, that also included “synchro” in the same plot
section (see Figure 3). The next most common group activity was
“social play”. Among play behaviors, we documented the behavioral
pattern “gentle tongue bite”, gently conducted among females and
young (see Figure 4), which was previously described by Martinez
and Klinghammer (1978). The rest of the affiliative activities
consisted of group interactions with elements of the pool or a group
of orcas which observed other individuals who were in a different
pool or rested together. (Figures 5 and 6).
F IGURE 3 Percentages of cases each behavior pattern occurred
within the affiliative category
SÁNCHEZ–HERNÁNDEZ ET AL. | 5
The behavioral patterns observed within an agonistic context
were “chase, dip push, bite, rake, ram, and tail kick” (see Table 2).
Individuals who received those agonistic behaviors could react
with avoidance, “escape”, “roll over”, and sometimes with “beach”
behavior. The most common behavioral pattern in an agonistic
context was “push”, and the typical sequenceconsisted of
approaches followed by several short pushes. Biting and
scratching with the teeth occurred rarely, and never caused
injuries (no bleeding or fresh wounds could be detected in the
video recordings); These behavioral patterns occurred not only
within a typical agonistic sequence (after threats, intense chases,
or evasion), but were also observed rather isolated within other
behavioral contexts, for example, during social play, or while two
animals were observing the trainers (neither the recipient animal
fled nor continued an aggressive sequence). In a single case, a
female showed this type of behavior toward another one that was
not interacting with her but with a male in a sexual context.
A common sexual sequence consisted of “genital, mount,
penis, ventral–ventral, and pursuit”. A typical sexual behavioral
sequence often began with a “rub”, which is one of the most
frequent behavioral patterns in the sexual context. Usually, one
of the individuals followed the other slowly and when eventually
above him/her continued swimming in a “mount” position with or
without visible penis or performed the “genital” behavioral
pattern. When the recipient of sexual behaviors reacted eva-
sively, high‐speed chases “pursuit”, were frequently observed.
The receiver sometimes performed aggressive behaviors as a
response to sexual interest from the former.
3.2 | Relationships among individuals
The comparisons of observed and expected values for the matrix
of individual interactions within each behavioral category
showed there were significant differences in each (Agonistic:
χ2 = 9245, df = 19; Sexual: χ2 = 3567.6, df = 11; Affiliative: χ2 = 313,
df=19; p4.1 | Behavioral patterns
The repertoire of sexual and affiliative patterns found in our group of
orcas is similar to the descriptions in Martinez and Klinghammer (1978).
Bain (1986) also mentioned a pattern similar to “gentle tongue bite”
described in this study, although in their observations the animals did not
bite the tongue, both tongues made contact.
The agonistic patterns found in our work were similar to those
described by Norris (1967). However, we did not find the aggressive
display characterized by chasing with open mouth directed at tail fluke
and genital region of the orca being pursued, as described by Psarakos,
Herzing., and Marten (2003). We also found some differences to the
“intense aggressive chase” described by Graham and Noonan (2010).
Intense aggressive chase was described as apparent bite attempts, very
rapid swimming, and unmistakable evasive maneuvers on the part of the
male”. In our observations, the intensive chase ended with pushing but
never with bites. Also, in the group studied by Graham and Noonan, all
agonistic displays came from a female that chased a male (the study was
made on mating partners with a young calf), whereas different
combinations of agonistic interactions between males, or females were
found in the present study.
4.2 | Relationships in the dyads
Analyzing the sign of the adjusted residuals in the three social matrices
suggests the kind of relationship or compatibility between specific orca
dyads. Thus, for example, a negative residual in the agonistic matrix
(indicating that these kinds of behaviors were significantly less frequent
than expected by chance) together with a positive residual in the
affiliative and or sexual matrix (indicating that category was more
frequent than expected) suggest compatibility between a pair. This was
the case of the dyads: Kohana–Morgan, Kohana–Adán, and Tekoa–Skyla.
The most likely agonistic relationship was that of the two older males
(Tekoa–Keto); however, they also showed frequent sexual and affiliative
relationships. This could have happened because Keto frequently
followed Tekoa attempting sexual interactions with him; same‐sex sexual
contact has been described as important in the social life of free orcas
(Bahemihl, 1999). The female dyadMorgan–Kohana had some similarities
with Keto–Tekoa but, in this case, the sexual behaviors happened in both
directions (initiated from both individuals). These two orcas also have
significantly adjusted residuals in the three categories but their sexual
behavior was less clear because only two patterns (“mount” and “genital”)
were shown. As sexual behaviors have not been reported between
female orcas, these patterns may have another social function. Morgan
was the more recent member incorporated to the group and Kohana is
the oldest and bigger female. For that reason, presumably the relation-
ship between both animals was building up and the observed interactions
could be the result of that process. This may give some clues about
different types of conflicts and reconciliation. On the other hand, the
analysis of dyad relationships could be used to take management
decisions. For example, the agonistic relationship between Skyla and
Morgan suggest a lack of compatibility and could be the target of actions
to avoid more serious conflicts.
4.3 | Conflict resolution
Our results show that the group of orcas studied showed a CCT of
31.57%, which is close to the range between 31.7% and 44% reported in
dolphins (Weaver, 2003; Yamamoto et al., 2015). First‐affiliative
behaviors occurred earlier after aggressions (on average within the first
3min) than in control periods. Similarly, conciliations reported in ravens
(Corvus corax), red‐necked wallabies (Macropus rufogriseus), and spotted
TABLE 4 Adjusted residuals for the interactions within each
behavioral category and each pair of individuals (emitter in the first
column and receiver in the second column) that were performed
more (positive sign) or less (negative sign) frequently than expected
by chance
Dyads Agonistic Sexual Affiliative
Kohana– Skyla −14.12 – –
Morgan −22.66 13.20 5.10
Tekoa 55.51 −8.38 −6.03
Adán −6.77 – 5.69
Keto −9.43 −3.27 –
Skyla– Kohana −21.01 14.32 –
Morgan 31.48 – –
Keto −14.86 – −2.60
Tekoa −23.37 – 3.25
Keto– Kohana −6.79 −38.28 –
Tekoa 22.55 30.66 5.15
Morgan −5.9 – 3.01
Skyla −7.19 −9.93 −2.60
Tekoa– Kohana −3.98 – –6.03
Skyla – 14.64 3.25
Keto 62.06 – 5.15
Adán 6.41 – 1.98
Morgan −25.51 −2.46 –6.20
Morgan– Kohana 24.16 47.99 5.10
Skyla 13.57 −4.50 –
Keto −2.03 2.81 3.01
Tekoa −30.13 −35.49 –
Adán −2.32 – –
Adán– Kohana −3.88 – 5.69
Skyla ‐4.11 – –
Tekoa 15.71 – 1.98
Morgan −4.71 – –
Note: As affiliative behaviors were reciprocal, the same residual appears
in both dyads of every pair. Dashes represent residuals lower than 1.96.
8 | SÁNCHEZ–HERNÁNDEZ ET AL.
hyenas (Crocuta crocuta) occurred within the first 2–5min after a conflict
(Cordoni & Norscia, 2014; Fraser & Bugnyar, 2011;Wahaj et al., 2001). In
a group of captive bottlenose dolphins, the affiliation between former
opponents occurred mostly within 1min after aggression (Yamamoto
et al., 2015).
For non‐human primates, the reported ranges for the CCT are
between 7% and 54% (Aureli & de Waal, 2000). In a captive
wallaby colony, the only marsupial mammal reported showing
reconciliation, the CCT was 27.4% (Cordoni & Norscia, 2014), and
in a permanent group of horses 26.5% (Cozzi et al., 2010). Similar
to the CCT found in these two last studies, our current finding
can be placed in between the minimum of 3.1% found in Japanese
macaques (Chaffin, Friedlen, & de Waal, 1995) and the maximum
of 51.4% in crested macaques (Petit, Abegg, & Thierry, 1997).
Cozzi et al. (2010) suggested that such an intermediate position
of the CCT may be due to the controlled living environment, in
which motivation to reconcile after a conflict could be high
considering the need for mandatory sharing of space, but not as
high as in situations where the risk of predators and possible lack
of resources would require even greater cohesion. However, the
CCT found in a captive group of bottlenose dolphins was much
closer to those found in crested macaques, even though this
group was also kept in a controlled environment. On the contrary,
Yamamoto et al. (2015) suggested that dolphins living in
controlled environments might conduct PC affiliation more
frequently compared to their wild counterparts. This supports
the view that the need for conflict management might be higher
in a limited environment and restricted social grouping where
former opponents cannot reduce the possibility of resumption of
aggression just by separating from each other. Although little is
known about reconciliation tendencies in wild dolphins, this
assumption is supported by the findings from wild and captive
chimpanzees showing slightly higher reconciliation tendency in
captive compared to wild populations: 17.25% versus 14.4%,
respectively (Fuentes, Malone, Sanzm, Matheson, & Vaughan,
2002; Kutsukake & Castles, 2004). The present study provides
the first assessment of orca behavioral reconciliation patterns.
However, it is important to note that the value of the CCT found
in the present study must be considered with caution due to the
small number of PC–MC observations compared to other studies,
which used more than 100 pairs of PC–MC observations for the
analysis of reconciliation tendencies (e.g., Cordoni & Norscia,
2014; Cozzi et al., 2010; Palagi, Paoli, & Tarli, 2004).
Early findings reporting the occurrence of reconciliation in chimpan-
zees were interpreted as an indication that great apes might have more
sophisticated cognitive abilities than other primates (for review, see
Aureli, Cords, & van Schaik, 2002). Since then, however, reconciliation
behavior has been found in a wide range of other primates, non‐primate
mammals and even birds showing that this capacityis not restricted to
“higher” apes. Nevertheless, reconciliation in non‐human primates is
thought to be associated with some specific cognitive characteristics
important for managing social interactions in complex groups such as
memory and individual recognition (deWaal & Yoshihara, 1983). This link
appears to be present in bottlenose dolphins as well as they possess both
elaborate levels of visual and spatial memory and individual recognition
of their conspecifics (see for a review, Marino et al., 2007) and
do reconciliate at least in controlled environments (Yamamoto et al.,
2015). The present study reports reconciliation in another delphinid
species which is well known for its behavioral flexibility and complexity
(for a review, see de Bruyn, Tosh, & Terauds, 2013; Riesch, Barrett‐
Lennard, Ellis, Ford, & Deecke, 2012). The findings provide further
evidence for convergent evolution of higher cognitive skills in the
suborders of Odontoceti, some members of the orders of Psittaciformes,
the family of Corvidae, and the family of Hominidae (Güntürkün, 2014,
Marino, 2002).
Minimizing social stress should be an important goal in zoo animal
management. Waples and Gales (2002) proposed that stress, resulting
from social instability and ensuing aggressive interactions,
is likely to affect negatively the health of bottlenose dolphins in zoo
settings. Thus monitoring the social behavior and dominance interactions
are crucial in identifying the potential for such social stressors (Waples &
Gales, 2002). The present study provides a systematic way to assess
social individual associations and interactions as well as conflict manage-
ment in cetaceans housed in zoos and zoo‐like facilities and may
contribute to improvements in animal welfare and management of
animals in controlled environments.
ACKNOWLEDGMENT
We thank Loro Parque Foundation and employees at Loro Parque zoo for
allowing us to carry out the study and for all practical support. We also
thank Fernando Rosa for help in the systematization of the big amount of
behavioral data obtained in this study and Antonio Cabello for his
assistance during the initial revision of the videos. During the study, P. S.‐
H was granted by Loro Parque Fundación.
CONFLICT OF INTERESTS
The authors declare that there are no conflict of interests.
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How to cite this article: Sánchez–Hernández P,
Krasheninnikova A, Almunia J, Molina–Borja M. Social
interaction analysis in captive orcas (Orcinus orca). Zoo Biology.
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https://doi.org/10.1002/zoo.21502