9

© 2009 Universities Federation for Animal Welfare Animal Welfare 2009, 18: 9-19
The Old School, Brewhouse Hill, Wheathampstead, ISSN 0962-7286
Hertfordshire AL4 8AN, UK

Benefits of training/playing therapy in a group of captive lowland gorillas

(Gorilla gorilla gorilla)
L Carrasco*†, M Colell†, M Calvo‡, MT Abelló§, M Velasco§ and S Posada†
†
Department of Psychiatry and Clinical Psychobiology, Faculty of Psychology, University of Barcelona, Campus de la Vall d’Hebron,
Edifici de Ponent, Passeig de la Vall d’Hebron 171, 08035 Barcelona, Spain
‡
Department of Statistics, Faculty of Biology, University of Barcelona, Diagonal 645, 02028, Barcelona, Spain
§
Barcelona Zoo, Parc de la Ciutadella s/n 08003, Barcelona, Spain
* Contact for correspondence and requests for reprints: laracarrascopesquera@hotmail.com

Abstract

Animal well-being and enrichment continue to gain importance in the maintenance of primates living in captivity. Positive rein-
forcement training (PRT) and/or playing interaction have been shown to be effective in improving the well-being of several species
of primates. This research study evaluated the effects of applying a combination of these two techniques (training/playing therapy)
on a group of lowland gorillas (Gorilla gorilla gorilla). The effects of this combination on the behaviour of captive primates have
been given very little attention to date. The behaviour of a group of seven females was recorded in two different phases at
Barcelona Zoo: before (periods 1 and 2) and after (periods 3 and 4) a series of changes were made to the composition of this
social group. In each period, two phases were distinguished: i) baseline condition, after the subjects became used to the researcher,
focal recordings were made of the group’s regular behaviour and, ii) experimental condition, the training and playing sessions
(‘gorilla play’) with two specific subjects began one hour before the group went to the outdoor facility. The frequency and duration
of the behaviour observed in each of the recording conditions were compared. The results showed positive changes in the gorillas’
behaviour: stereotypies, interactions with the public, aggression between subjects and inactivity were all reduced, while affiliative
behaviour and individual and social play-related behaviour increased. Moreover, the benefits of this therapy were observed in
trained individuals and the rest of the gorillas in the group, which would seem to indicate that training/playing can be used to
create a more relaxed atmosphere, reducing social tension and improving the well-being of all the subjects involved.

Keywords: animal welfare, gorilla, human interaction, play, training, well-being

Introduction primates, abnormal behaviour has been used traditionally as

In recent years there have been many improvements in the
way in which captive animals are managed. It is now widely
accepted that enrichment should play an essential role in
caring for wild animals in captivity (Bloomsmith et al 1991;
Bloomsmith 1992); the idea being to maximise individuals’
well-being and mitigate any of the negative effects of
captivity on their behaviour. Animal well-being can be
defined as “the status of full physical and mental health in
which the individual is in harmony with and adapted to the
environment in which it lives and its specific physical and
psychological needs are met” (Duncan & Dawkins 1983;
Broom 1991; Fraser 1993), thus allowing the individual to
perform the species’ natural behaviour. To improve animal
well-being, the objective of all enrichment is to promote the
species typical behaviour in the wild, achieve greater behav-
ioural diversity among subjects and prevent or reduce the
appearance of anomalous behaviour (stereotypic, self-
injurious behaviour; see also Table 1). In fact, in the case of
an indicator of stress and poor mental health (Bloomsmith
et al 1991; Laule 1992; McCormick 2003). Numerous
articles have evaluated the effects of changes in the social
and/or physical environment on the well-being of these
species, but very few have evaluated the repercussions of
variables such as the quantity/quality of human interaction
with a caregiver or researcher. Despite the lack of such
analysis, many experts consider positive reinforcement
training (PRT) to be a new enrichment alternative
(Whittaker et al 2001). This technique is based on rein-
forcing specific behaviour by rewarding the individuals
exhibiting this behaviour and involves establishing closer
contact between keepers and animals. This primate-
management and care tool gained wider acceptance when
many of its benefits were demonstrated through different
studies with chimpanzees (Pan troglodytes) (Baker 1997,
2004; Bloomsmith et al 1997, 1999; Baker et al 2003),
rhesus macaques (Macaca rhesus) (Bayne et al 1993;

Universities Federation for Animal Welfare Science in the Service of Animal Welfare
10 Carrasco et al

Table 1(a) Study ethogram showing individual behaviours (IB) and social behaviours (SB).

Category Individual behaviour Social behaviour

Neutral behaviour
Positive/desirable behaviour
Negative/undesirable behaviour
* Deficit behaviours (DF) are shown below in Table 1(b).
Inactivity (R)
Locomotion (D)
Feeding (Alim)
Self grooming (AA)
Acrobatic play (JA) Locomotion (+D)
Instrumental play (JI) Feeding (+A)
Social play (+J)
Social grooming (+AS)
Affiliative behaviours (+AF)
Deficit behaviours (DF)* Threatening behaviours (+AM)
Interaction with the public (PU) Agonistic behaviour (+AN)

Table 1(b) Study ethogram showing deficit behaviours (DF).

Behaviour Description
Licking the glass Individuals stick their tongue out and move it along the glass
Licking up the vomit of others Individuals lick up the vomit left by conspecific
Regurgitating and licking up one’s own vomit Individuals force themselves to vomit and then lick it up
Hugging oneself Individuals wrap themselves around their own shoulders
Yawning Individuals open their mouths with no apparent intention of having anyone see it or
react to it
Self stimulation Repeated contact of one part of the body with another part or with an object; Hitting
a part of the body repeatedly and with low intensity with the fist or open hand
Performing repetitive, low-intensity movements (ie rocking back and forth) so that one
part of the body (usually the back) hits the wall
Coprophagy Eating their own faeces or those of conspecific
Stereotypic behaviours with wrists and arms Individuals shake their wrists and arms for no apparent reason, usually when sitting
with their hands open
Biting nails Individuals put their hands in their mouth and bite their fingertips
Sucking fingers Individuals stick their finger in their mouth and suck it, usually the thumb
Blowing kisses Individuals place the palm of their hand on their mouth and blow kisses into the air
Sticking the tongue out Individuals stick out their tongue and move it from side-to-side with the mouth open

Schapiro et al 2001; Bloomsmith et al 2005) and marmosets
(Callithrix jacchus) (Basset et al 2003; McKinley et al
2003; McKinley & Buchanan-Smith 2003). The uses and
benefits of PRT include the following (Laule et al 1993;
Buchanan-Smith 2003; Prescott & Buchanan-Smith 2003;
Schapiro et al 2003): i) An improvement in veterinary
care;:the subject’s co-operation with certain medical proce-
dures makes it possible to reduce the use of anaesthesia and
the stress level of the treated subject (Seiver et al 2001;
Bassett et al 2003; Scott et al 2003); ii) Individual manage-
ment becomes easier, as do transfers from one facility to
another for cleaning purposes (McKinley et al 2003); iii)
Mothers are encouraged to care for their own young: since
the young remain with their mothers in the group, it is not
necessary to raise them by hand (Abelló 2007); iv) Deficit
and unwanted behaviours are reduced (problems of aggres-
sion while eating [Bloomsmith et al 1994]), as well as other
agonistic behaviours that provoke stress, fights, etc
(examples of deficit behaviours can be found in Table 1); v)
When keepers initiate playing behaviour with subjects, they
promote positive social interaction among group members
(Desmond & Laule 1994; Schapiro et al 2001) that favours
a more peaceful and relaxed environment and, vi) Finally,
because PRT makes it necessary to spend additional time
with each animal, which results in closer, individualised
contact, relations between keepers and the animals they are
responsible for seem to improve (Bayne et al 1993;
Bloomsmith et al 1997; McKinley et al 2003). In fact, the
results were similar to studies in which the only change the
animals were subject to was an increase in positive human

© 2009 Universities Federation for Animal Welfare


contact with keepers, even though interaction was less
structured than with PRT: the behaviour and well-being of
the primates improved and they displayed less anomalous
behaviour (Bayne et al 1993; Baker et al 1997). To try to
distinguish between the effects of simple positive human
interaction and PRT, Bloomsmith et al (1999) compared
two groups of chimpanzees. One was systematically
trained, while the keepers’ positive contact with the other
group was increased through less structured
playing/grooming/feeding sessions. In both groups, a
general improvement in behaviour was observed. However,
differences were recorded between the groups, depending
on the type of interaction. The PRT seemed to benefit social
behaviour (social playing increased), whereas the less struc-
tured interaction (playing) helped reduce stereotypy and
anxious behaviour. In similar studies that compared the two
management techniques on other primate species, such as
marmosets (McKinley et al 2003) and rhesus macaques
(Bloomsmith et al 2005), no significant differences were
found, which suggests that the benefits and/or repercussions
of training differ depending on the species of primate.
Another important consequence of this increased contact is
that the animals lose their fear of humans. After training, a
colony of New World primates at the Bronx Zoo, New York,
USA changed their attitude toward the keeper (Savastano
et al 2003): they no longer fled or issued calls of alarm and,
as they stayed in front of the glass for longer periods of
time, were more visible to visitors.
However, the presence of humans (visitors, keepers, veteri-
narians, etc) can also have a detrimental effect on the well-
being of captive primates (Lambeth et al 1997; Hosey 2000;
Keane & Marples 2003; Jones & Wehnelt 2003). Group
dynamics in chimpanzees and other primates seem to be
altered by the presence of visitors, in that less affiliative
behaviour and more aggressive conduct have been observed
during the periods when the greatest numbers of visitors are
viewing the animals (Lambeth et al 1997; Hosey 2000).
Therefore, although PRT is apparently beneficial for these
primate communities, it is important to carefully evaluate and
limit interaction with caregivers as a form of enrichment. It
should not be assumed that this type of human contact will be
positive without first carrying out an evaluation.
To assess whether moderate interaction with the animals
(short-term and occasional contact) is a useful handling tool
to increase the well-being of captive primates, a study was
carried out with one of the groups of lowland gorillas at
Barcelona Zoo. Daily training/playing sessions were held
with two members. The objectives were as follows: i) to
evaluate how the behaviour of these individuals in partic-
ular and the group in general was affected by human inter-
action and, ii) to compare the different individual and social
behaviours with the aim of evaluating any differences
before and after interaction with the trainer.
Materials and methods
This study was carried out on a group of seven lowland
female gorillas (Gorilla gorilla gorilla) at Barcelona Zoo
(see Table 2). Two of them, Batanga and Muni, formed part
Benefits of training/playing therapy in gorillas 11
Table 2 Subjects involved in both the first (periods 1 and
2) and second (periods 3 and 4) studies.
Name Study participated in Date of birth Raised
Machinda First 15/1/1978 By hand
Kena First 11/7/1981 By hand
Nimba First and second 31/1/1999 By hand
Batanga First and second 8/2/1999 By hand
Muni First and second 19/2/2000 By hand
Coco Second 1994* By parent
and hand
Yangu Second 2/7/1996 By parent
* Born in the wild, therefore exact date of birth not known.
of a parallel study on the imitation skills of large apes that
included training sessions. Two different recording seasons
were held as the group composition changed while the study
was being carried out. In the first season (called periods 1
and 2), the group could be considered socially stable. For
the second season, several subjects were added to the group
and it consisted of two new females along with three of the
previous females (see Table 2). Following the same method-
ology, data were recorded for the corresponding new
baseline and experimental conditions (called periods 3
and 4). The gorilla enclosure consisted of three different
spaces: five interconnected indoor bedrooms measuring
5 × 5 × 3 m (length × breadth × height) and two outdoor
areas that were exposed to the public. The 90 m2 vestibule
was a covered area with radiant floor heating and platforms
and tree trunks arranged at different levels that led into the
345 m2 outdoor area, designed as a natural setting. During
training and play interaction, the individuals were given free
access to different objects, such as bowls, buckets, ropes,
sticks and clothing. A Sony HC 40E digital video camera
(Tokyo, Japan) was used to record the sessions.
In both cases, the procedure was divided into two phases.
The first phase recorded the baseline condition; from
October to December 2004, the subjects became accus-
tomed to the trainer (habituation) to establish affective ties
between the researcher and the individuals in the study. The
trainer went to the gorilla enclosure each day and encour-
aged the gorillas to play by rewarding them with food,
objects, sticks and clothing. At the same time, record-taking
of group behaviour began with the aim of designing an
ethogram (see Table 1). This information revealed the level
of psychological well-being and social interaction between
the members of this group of gorillas prior to the onset of
playing sessions with humans. To prepare this baseline
condition, focal observations were carried out on each indi-
vidual for 10 min from 1000 to 1400h until a total of 10 h
had been recorded for each individual.
The second phase consisted of the experimental condition;
after the first phase was completed, the training/playing
sessions were started with Batanga and Muni, one hour
Animal Welfare 2009, 18: 9-19
12 Carrasco et al
prior to the animals entering the outdoor area. Whenever
possible, work was carried out with these two subjects indi-
vidually. They were encouraged to come away from the
rest of the group to begin the training session. The other
individuals stayed in the adjacent bedrooms which gave
them visual access to the subjects performing the different
training tasks. After different objects were placed in the
cages, the gorillas were rewarded for copying certain
actions within the context of play. After training, the indi-
viduals joined the group and, for a few minutes, were
encouraged to play with each other and the trainer. The aim
of this less-structured interaction was to create a playful
atmosphere among the gorillas. Following this, they
relocated to the outdoor area and the group’s behaviour was
recorded as part of the experimental condition (period 2).
Once again, 10 min focal recordings were made for each
individual in the group, during the morning, until a total of
10 h observation had been recorded for each individual.
After the changes took place in the study group (November
2005), record-taking, using the same procedure, began in what
was now referred to as periods 3 and 4. Here, the first phase
involved ensuring the new individuals became accustomed to
the trainer and recording the group’s behaviour without prior
human interaction (period 3). Following this, data were
gathered for the corresponding experimental condition
(period 4) after beginning the training/playing sessions.
Our research was carried out at Barcelona Zoo with the permis-
sion of the management and following the guidelines on the
ethical treatment of animals, in accordance with Spanish law
on the protection of animals (Royal Decree 223/1998).
Data analysis
In order to analyse the frequency and duration of the different
types of behaviour and the frequency with which behaviour
occurred, slightly different statistical procedures were
required. Bearing in mind the experimental design, the three
types of variables were observed in two different experi-
ments. The first one corresponded to periods 1 and 2, and the
second to periods 3 and 4. Both had an identical experimental
structure: two groups of different subjects were observed in
two different periods: before and after receiving training.
Within each period, several observations were made of each
individual over time. Therefore, each element in the data
matrix can be understood to be the result of the possible
influence of four sources of variation: (i) the individual; (ii)
the experimental group; (iii) the period and (iv) the time that
passed since the beginning of the period. At this raw data
level, the probabilistic nature of the variables differs: duration
is a time measurement and therefore continuous. However,
the two frequencies are discrete counts.
It would obviously have been better to analyse all the data
with a full model that included the four sources of vari-
ability. However, some of the behaviours were actually not
detected in many of the short 10-min intervals during the
© 2009 Universities Federation for Animal Welfare
experiment. The number of null observations was particu-
larly high for the frequency that individuals commenced
specific behaviours.
With such a sparse data matrix that includes so many zero
counts, it is difficult to obtain suitable inferences of the full
model. This can be solved by grouping observations
together. We propose two alternative procedures: (i) adding
all the values compiled in the same period to obtain a single
measurement for each subject per period or, (ii) making
inferences with the group means over longer time intervals
(with a minimum of four grouped times), thus making it
possible to analyse the time effect within the period. In the
first grouping method, the possibility of detecting the effect
of time within each period is lost, whereas in the second, it
is not possible to detect the effect of the subject. Even when
these criteria are used to group the data, some of the behav-
iours are very infrequent. In such cases, we have added up
the values of similar kinds of behaviours, which are
therefore represented with generic variables.
The two alternative ways of grouping and simplifying the
experimental design provide complementary information,
therefore we analysed our data following the corresponding
linear models. The first grouping procedure has only one
measure per subject and period. In terms of analysis of
variance, the equation of the model should include the
following factors: ‘group’ completely crossed with ‘period’,
while ‘individual’ is nested within the group, thus defining
a hierarchical linear model. Because it can be reasonably
assumed that the residuals were normal for the durations,
we analysed the durations with a normal linear model (ie
classic ANOVA analysis). However, a general linear model
(GLM) was used for the frequencies of commencement,
with the negative binomial distribution as the link function.
The negative binomial is a more flexible probabilistic
model for count data than the Poisson model because it
captures any overdispersion of the analysed frequencies
(Venables & Ripley 2002).
For the second grouping method, where the values of all the
individuals of the group were averaged, the ‘group’ and
‘period’ factors were also crossed, while the ‘time’ since the
beginning of the period was additional information for each
grouped measure. In statistical terminology, it defines a
two-way ANOVA factorial design, with time acting as a
covariate. With this second linear model, we once again
analysed the durations and frequencies of the behaviours.
We assumed the residuals of the frequencies were normal by
virtue of the central limit theorem, because each data value
was an average of several counts with high observed values.
Finally, descriptive statistics were carried out for the set of
variables for which there were insufficient observations.
The computations of all the analyses described above were
done with the freeware package R (R Development Core
Team 2007), with the MASS package added (Venables &
Ripley 2002) to solve the GLM contrasts analysis.

Results
Significance levels for all analyses were fixed at 5% and
only P-values lower than 0.05 are reported below.
Period 1 and 2: Results according to the linear
model with individuals
This statistical analysis model was used to compare the
durations of behaviours recorded in the two phases, ie in
period 1 (phase prior to human interaction) and period 2
(after human interaction), and some significant differences
were observed. In the case of deficit behaviours (P = 0.032)
and behaviours directed at the public (P = 0.013), the mean
duration was lower. There was also a significant drop in the
durations of agonistic behaviours (P = 0.048). However,
social play (P = 0.049) increased between the group
members after the training/playing sessions with humans. If
all the individual behaviours were considered as a whole,
significant differences were observed between the two
groups in the two recording situations (P = 0.001). In the
case of subjects worked with directly, an increase occurred
in the duration of these behaviours, whereas there was a
drop in these behaviours in the other group.
Results according to the linear model with times
grouping individuals
(i) Period 1–2, durations
Overall differences were detected between the two
recording periods in the group of trained subjects and in the
group of untrained subjects, in that the duration of variables
such as locomotion (D) (P = 0.005) and interaction with the
public (PU) (P = 0.003) dropped in period 2. There was a
drop in inactivity behaviours (R) (P = 0.001), whereas those
related to feeding (Alim) increased (P = 0.003) and the same
change in trend occurred in both groups over time between
periods 1 and 2. The case of affiliative social behaviour
(+AF) is worth noting, given that significance was detected
in all factors: there were changes in the common curve over
time (P = 0.036) between the two periods (the trend over
time was different in period 1 and period 2), there were also
differences in the evolution depending on the group in
question (P = 0.001), and the overall profile of group 1 was
different from that of group 2 (P = 0.011).
(ii) Period 1–2, frequencies
For Alim (P = 0.001), PU (P = 0.040), +AF (P = 0.027),
overall individual behaviours (P = 0.046) and all social
behaviours (P = 0.007), there were differences in the overall
means of the two recording periods. In the case of inactivity
and locomotion, the trend (curve) over time was different in
each period, ie the behaviours evolved differently over time
in each period, but in the same direction for each group.
General linear model 1 and 2
This last analysis assessed the possible differences between
the number of times the group members worked with indi-
vidually-commenced social behaviours (group 2: Batanga
and Muni) with the other three gorillas (group 1), to see
whether the training had basically affected the behaviour of
the subjects directly involved, or that of all the gorillas in
Benefits of training/playing therapy in gorillas 13
Figure 1
Frequencies of the recorded behaviour categories in periods 1 and 2.
the group. In the case of periods 1 and 2, no significant
differences were detected in the frequency of commencing
such behaviours. Therefore, Batanga and Muni were not the
only ones to commence this type of behaviour after the
sessions with the humans; all the members of the group
increased their positive social interactions.
Qualitative assessment of periods 1 and 2
Despite the fact that in some instances an insufficient number
of observations were obtained to carry out statistical inference,
we feel it is of interest to highlight a few of the situations
described below.
When we grouped the different behaviours included in the
ethogram into four blocks (individual behaviours, deficit
behaviours, interaction with the public and social behaviours),
we obtained the results as seen in Figure 1 for the two periods
in the first recording period. There was a drop in deficit behav-
iours and behaviours directed at the public after the playing
sessions began, whereas there was an increase in individual
behaviours and social behaviours.
If each of these blocks is analysed for each individual, we can
see that, as in the case of group analysis, there was an increase
in individual and social behaviours and a drop in deficit
behaviours and behaviours directed at the public, in all the
subjects in the study (Table 3).
One of the main aims of this study was to assess the effects of
the subjects’ playful interaction with humans on their playing
behaviour with the rest of the group. An increase in these
behaviours could be considered a reflection of increased well-
being. When we analysed individual and social play for each
individual, we found a sharp increase in social play (Table 4).
As previously mentioned, no statistical differences were
found between the groups of gorillas we worked with and the
group we did not work with, in terms of which commenced
Animal Welfare 2009, 18: 9-19
14 Carrasco et al

Table 3 Absolute frequencies and percentages of observed behaviours during periods 1 and 2.

Experiment Individual Ind % Def % Publ % Social %

Period 1 Nimba 337 64 16 3 39 7.5 129 24
Batanga 378 68 23 4.1 31 5.6 119 21
Muni 371 57 37 5.7 43 6.6 197 30
Kena 266 59 82 18 22 4.9 76 17
Machinda 340 77 66 15 9 2 23 5.2
Period 2 Nimba 404 59 19 2.7 9 1.3 247 36
Batanga 410 64 11 1.7 6 0.9 210 33
Muni 414 55 22 2.9 18 2.3 298 38
Kena 312 57 60 11 9 1.6 160 29
Machinda 440 85 42 8.1 1 0.2 33 6.4

Ind: Individual behaviours; Def: Deficit behaviours; Publ: Interactions with the public; Social: Social behaviours.

Table 4 Frequencies of individual play for each subject during periods 1–4.

Individual Period 1 Period 2 Period 3 Period 4

JA JI +J JA JI +J JA JI +J JA JI +J
Nimba 12 18 50 22 25 92 0 3 0 4 23 4
Batanga 40 42 46 52 44 94 6 1 15 62 43 127
Muni 35 44 89 73 53 160 3 2 15 74 61 112
Kena 5 13 28 4 1 68 – – – – – –
Machinda 0 1 1 0 3 2 – – – – – –
Yangu – – – – – – 0 0 0 3 12 27
Coco – – – – – – 0 0 34 5 16 166

JA: Acrobatic play; JI: Instrumental play; +J: Social play.

Table 5 Frequencies and percentages of commencing behaviours during social interaction with members of the group
for periods 1–4.

Individual Period 1 Period 2 Period 3 Period 4

FSI %CSI FSI %CSI FSI %CSI FSI %CSI
Nimba 63 90 155 86 8 75 81 98.7
Batanga 81 90 143 93 52 76 362 98.6
Muni 143 96.5 213 96.7 26 80 191 98
Kena 57 59.6 133 80.5 – – – –
Machinda 18 22.2 20 70 – – – –
Yangu – – – – 21 66 197 92
Coco – – – – 42 76 287 95

FSI: Frequency of social interaction; %CSI: Percentage commencing social interaction.

social behaviours. However, in terms of the percentage of
positive social behaviours compared to total social behav-
iours (Table 5), an increase was observed in the number of
times the subjects commenced positive social behaviours,
with the exception of Nimba. In other words, the
training/playing sessions seem to have modified the social
behaviour of all the group members, not simply the subjects
which participated most actively in the study. This change
was more pronounced in the case of Kena and Machinda, the
two adult females which, surprisingly, were the subjects that
interacted least with the other members of the group, prior to
the start of the training/playing sessions.

© 2009 Universities Federation for Animal Welfare


Figure 2
Frequencies of the categories of recorded
behaviours in periods 3 and 4.
Periods 3 and 4: Results according to the linear
model with individuals
The results of this second period of record-taking showed
an increase in period 4 in the duration of individual behav-
iours, such as inactivity (P = 0.015), locomotion (P = 0.005)
and deficit behaviours (P = 0.010). Among social behav-
iours, there was a sharp increase in affiliative behaviours
(+AF) (P = 0.018) and a drop in threatening behaviours
(P = 0.008). When all social behaviours were assessed
together, significant differences were observed between the
two periods (P = 0.012), in that the subjects spent far more
time on social behaviours in period 4 than in period 3 (mean
in period 3 = 1,020 and period 4 = 8,755), before playful
interaction with humans began. When the specific case of
individual and social play was analysed (P = 0.012), it was
once again seen to increase in duration in period 4.
Results according to the linear model with times,
grouping individuals
(i) Period 3-4, durations
Inactivity (P = 0.000) and locomotion (P = 0.001) increased
in period 4; in the case of locomotion, the trend over time in
period 4 was different than in period 3 (P = 0.014). There
was an increase in social behaviours related to feeding (such
as sharing food, asking for food; P = 0.026) and, in keeping
with the previous model, there was a very sharp increase in
affiliative behaviours (mean duration in period 3 = 2,065,
period 4 = 22,076; P = 0.008).
(ii) Periods 3 and 4, frequencies
In period 4, there was an increase in the frequency of behav-
iours such as feeding (P = 0.005), self-grooming
(P = 0.025), affiliative behaviours (P = 0.037) and all social
behaviours as a group (mean frequency in period 3 = 27,
period 4 = 220). When all individual behaviours were
considered at the same time, differences in frequencies were
observed (P = 0.039), and the evolution over time and for
each group was different in period 3, compared to period 4.
Benefits of training/playing therapy in gorillas 15
General linear model: periods 3 and 4
This statistical model was used to assess the effects of our
handling system on the behaviour of trained and untrained
gorillas in periods 3 and 4. Once again, as occurred in
periods 1 and 2, no significant differences were observed
between the two groups.
Qualitative assessment of periods 3 and 4
When we arranged the different group behaviours in the
four blocks mentioned above (individual behaviours, deficit
behaviours, interaction with the public and social behav-
iours), we obtained the results seen in Figure 2, which show
a sharp increase in individual and social behaviours. Social
behaviours can be positive (playing, grooming, seeking
contact, etc) or negative (threatening behaviours, fighting,
avoiding contact, etc) but, when the percentage of social
behaviours was analysed, we found that they increased by
77% in period 3 and by 96.5% in period 4. When these cate-
gories were compared for each individual (see Table 6), we
observed that, for all subjects, the same trend occurred as
for the group in general, ie there was a sharp increase in
both individual and social behaviours. For all the subjects in
the group, there was an increase in the frequency of indi-
vidual play that was even more pronounced in the case of
social play (see Table 4). It would appear therefore that the
individuals played with each other more after the
training/playing sessions with humans.
As in the previous section, periods 3 and 4 were compared
to determine whether Batanga and Muni were the main
subjects who commenced the positive social behaviours or
whether differences were observed in all the group
members (see Table 5). In this second record-taking
period, the group of gorillas was presumably less socially
stable due to the changes in make-up. However, all the
individuals were seen to be very socially active, which
indicated that they interacted positively with each other. In
fact, it was the new individuals in the group (Yangu and
Coco) which tended to commence positive social behav-
iours with the other members of the group.
Animal Welfare 2009, 18: 9-19
16 Carrasco et al

Table 6 Absolute frequencies and percentages of observed behaviours during periods 3 and 4.

Experiment Individual Ind % Def % Publ % Social %

Period 3 Nimba 250 90 12 4.3 2 0.7 12 4.3
Batanga 271 77 15 4.2 0 5.60 65 18.4
Muni 289 77 31 8.2 6 1.6 48 12.8
Yangu 248 87 10 3.5 1 0.3 26 9.1
Cocu 294 78 2 0.5 26 6.8 57 15
Period 4 Nimba 606 79 11 1.4 0 0 151 20
Batanga 763 62 16 1.3 0 0 444 36
Muni 864 73 33 2.8 3 2.8 276 23
Yangu 248 63 16 1.8 0 0 310 35
Cocu 294 65 4 0.3 26 2.1 385 32

Ind: Individual behaviours; Def: Deficit behaviours; Publ: Interactions with the public; Social: Social behaviours.

Discussion these individuals. Several social behaviours were also

According to our results, an effective way of improving the
well-being and social dynamics of primates in captivity is to
combine training with relatively unstructured playing
sessions. In these playing sessions, the trainer or keeper
encourages specific playing behaviours (‘gorilla play:
striking the chest with half-closed eyes; running from one
place to another; pinching oneself’) similar to those that
gorillas engage in with individuals of the same species. A
drop in anomalous and negative behaviour was observed
and these playing sessions seemed to favour activity models
similar to those typically found in the wild, given that
positive social behaviours increased. An undesirable effect
of human/animal interaction is human imprinting on non-
human primates as this can disrupt the attention of the
species from members of its own species. This moderate
human interaction (short duration and occasional contact
with animals) helped focus their interest on conspecifics
while preserving their rules of social behaviour. As with
other studies on enrichment, behavioural recordings began
before the trainer/keeper was present. In these studies, the
benefits of enrichment were only observed during and
immediately after it had began (Bryant et al 1988; Bayne &
Dexter 1992). However, in our case, record-taking during
the entire morning (in the hours after the training/playing
sessions were held) still reflected the effects of these
sessions, in that the animals showed a change in attitude,
and were less tense and less reactive.
When the recordings taken in periods 1 and 2 were
compared using the first statistical model (linear model with
individuals), a sharp drop was observed in the mean
duration of deficit behaviours (DF) after the
training/playing sessions began. Given that such
anomalous, self-directed, stereotypic behaviours have been
used as indicators of stress and poor mental health in
animals in captivity (Bloomsmith et al 1991; Laule 1992;
McCormick 2003), a drop in such behaviours can be consid-
ered an improvement to the psychological well-being of
modified and there was an increase in species-typical
behaviours, which is one of the chief objectives of all
enrichment systems (Bloomsmith 1992). The drop in behav-
iours directed at the public (PU) (striking the glass,
clapping) reflects a loss of interest in visitors, and could
favour greater interaction with the members of the group.
Likewise, the duration of agonistic behaviours (submissive
behaviours, avoiding social contact and watching another
individual) in period 2 was lower, which could reflect less
intragroup tension. When we consider the positive behav-
iours whose duration increased after playful interaction with
humans, it is especially interesting to note the case of play-
related behaviours. Some studies have shown that playing
only occurs when individuals’ vital necessities are satisfied
and there is a lack of stress (Rensch 1973). Moreover, social
play has an important role in group cohesion and, in periods
of great tension, can relax the atmosphere (Palagi et al
2004). Therefore, the significant increase observed in social
play allows us to affirm that these training/playing sessions
with humans conferred many benefits to the members of the
gorilla group. The second statistical model (linear model
with times) allowed us to complete our analysis and
contributed some new data. It was detected that periods of
inactivity lasted for less time but were more frequent, ie the
gorillas rested more often but for shorter periods of time,
which meant they had a higher rate of activity, which could
also explain the increase in feed-related behaviours. These
results agree with those obtained with chimpanzees in
previous studies (Baker 1997; Bloomsmith et al 1997).
There was a significant increase in the duration and
frequency of affiliative social behaviours. These behaviours
denote an affinity between two or more individuals and their
purpose is to establish, maintain or re-establish ties,
strengthen social ties and promote group cohesion.
Therefore, the fact that they increased in period 2 shows,
once again, increased interaction between the different
members of the group. In short, the subjects seemed to be
less stressed, interacted more and spent more time playing.

© 2009 Universities Federation for Animal Welfare


In periods 3 and 4, the composition of the group changed
which meant that, unlike the situation in the first period, the
group was not stable and there was greater tension between
members. In fact, two of the members were in the adapta-
tion period when record-taking began in this second period.
It was, therefore, of even greater interest to assess the
effects of human interaction under these circumstances. If
the results for this period once again showed the benefits of
this ‘play therapy’ for the gorillas, it could be considered an
effective way of integrating new members into social
groups or in any other area of behavioural management of
captive primates. The results obtained from the first statis-
tical analysis, which supported this idea, were as follows:
when all the social behaviours were grouped together, it was
observed that the individuals spent eight times more time on
social interaction in period 4 than in period 3. There was a
drop in threatening behaviours and a sharp increase in affil-
iative and playful behaviours, both at the individual and
social levels. This confirms the hypothesis that play has a
key role in regulating tension and preventing conflict. The
training/playing sessions with humans continued to be
beneficial for the members of the group as they promoted
more relaxed interaction among them. However, an increase
in deficit behaviours was also detected, probably as a result
of the tension generated by the changes in the composition
of the social group. Even so, playing behaviours increased
significantly, which reflected the effectiveness of the
therapy, even under adverse initial conditions.
Unfortunately, it is still possible to find subjects in captivity
that show symptoms of poor adaptation to the social group
and/or abnormal behaviours. They are usually individuals
that were raised by hand or traumatically separated from
their natural group and maintained in unsuitable captive
conditions. Therefore, the possibility of recovering some of
these individuals using training/playing therapy, which
incurs minimal cost, is of unquestionable interest and can be
highly useful for centres that house these subjects.
With the linear model with times, we obtained new signifi-
cant differences between periods 3 and 4: there was a sharp
increase in the time spent on affiliative behaviours and the
frequency of self-grooming behaviours, affiliative behav-
iours and all social behaviours, in general. This manage-
ment system can therefore be considered a tool for
providing emotional support to new individuals who have
been rejected or are having difficulties joining the social
group. Using these two types of human interaction (actual
training and less-structured sessions), individuals with
anomalous behaviours can be helped to regain confidence in
themselves and become capable of exhibiting normal social
behaviour and increasing communication with their
conspecifics. Bloomsmith (1992) pointed out that the most
important factor to be studied to improve the life of captive
chimpanzees was their social situation.
Another of our objectives was to assess whether the playing
sessions with humans only modified the frequencies of social
behaviours of the directly-trained subjects or whether it had
an effect on all of the subjects in general. The initial hypoth-
esis was that the subjects directly involved would begin the
Benefits of training/playing therapy in gorillas 17
social behaviours with their conspecifics more often than the
subjects who had not been trained. However, both the general
linear model and the qualitative analysis showed that there
were no significant differences between the trained and
untrained individuals. The training/playing therapy seems
therefore to affect the behaviour of all the individuals and to
provide benefits for the individuals directly involved, as well
as the others. All the subjects commenced positive behav-
iours with greater frequency after the sessions with the trainer
began. In period 4, it was even observed that the new individ-
uals (Yangu and Coco) were the ones who commenced these
positive social interactions the most.
According to our results and those of recent studies
(Buchanan-Smith 2003; Schapiro et al 2003; Baker 2004;
Bloomsmith et al 2005), these interactions not only
improved the well-being and living conditions of primates,
but also affected other environments and benefited keepers
and even visitors: more relaxed relations in the social group
were promoted and the animals reacted less to people. Their
attitude towards the keeper changed from being predomi-
nately aggressive to fundamentally affiliative. In fact, the
subjects lost their fear of the keeper/‘play companion’, who
initiated play and responded to play with them, and they
associated the keeper with positive experiences. They
stopped fleeing from the keeper, issuing calls of alarm and
hiding in their enclosures when the keeper appeared; they
even moved closer to and interacted more with the keeper
(Savastano et al 2003). This suggests that a simple affiliation
between humans and primates should be a component to be
assessed when handling these species because it not only
produces specific changes in behaviour, but also establishes
a closer relationship between keepers and the animals they
are responsible for that is beneficial for both parties (Prescott
& Buchanan-Smith 2003; Baker 2004). Moreover, the lack
of strict rules makes it possible to include a few minutes of
interaction during daily handling tasks, though, for safety
reasons and in the best interests of the subjects, the people
who interact with them should be familiar with the species
and the individuals involved. More employees can also
participate in these tasks. However, different studies have
shown the negative influence visitors can have on group
dynamics in different primate species. Thus, during periods
of high influx of visitors at zoo facilities, more aggression,
fighting and injuries have been observed, and/or a drop in
affiliative behaviours (Lambeth et al 1997; Hosey 2000;
Jones & Wehnelt 2003; Keane & Marples 2003). And yet,
some anecdotal observations have mentioned that actions
that previously agitated the study subjects (visits of strangers
to the building or prolonged activity near the cages) had less
effect after training/playing therapy had been introduced,
thus reducing animal behaviours indicative of anxiety and
stress. Therefore, if the animals are more relaxed than they
were before these positive human interactions, it can be
considered another advantage of this therapy for primate
communities in captivity. However, if a preliminary study
has not been carried out on the potential repercussions of
increased interactions between keepers and the animals they
are responsible for, alternative techniques are recommended
Animal Welfare 2009, 18: 9-19
18 Carrasco et al
to improve animal well-being (Bayne & Dexter 1992;
Bloomsmith 1992; Bloomsmith & Pruetz 1992; Laule 1992;
Bayne et al 1993; Hill & Broom 2003). Another interesting
conclusion is that this therapy could be useful in periods
prior to carrying out research studies on primates in
captivity. The researchers could help ensure subjects became
accustomed to their presence through playing sessions, with
the aim of ensuring the individuals involved are more
relaxed and participate more during the study.
Animal welfare implications
Adding a few minutes of positive human interaction per
animal per week to the management of captive gorillas
resulted in improved well-being in several areas: the drop
in abnormal behaviours, behaviours directed at the public,
inactivity and agonistic behaviours may reflect less intra-
group tension, while affiliative behaviours and individual
and social play-related behaviour increased. These results
confirm that an effective way of improving the well-being
and social dynamics of primates in captivity is to combine
training with relatively unstructured playing sessions.
These aspects should be taken into consideration as part of
behavioural management.
Acknowledgements
This research project was supported by a FI grant from the
Ministry of Education of the Autonomous Government of
Catalonia (2005/08). We are grateful to Barcelona Zoo for
permission to perform the study on the zoo premises and to
the staff of the primate section for their close collaboration.
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