Benefits of training/playing therapy in a group of captive lowland gorillas (Gorilla gorilla gorilla)

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1 9 The Old School, Brewhouse Hill, Wheathampstead, Hertfordshire AL4 8AN, UK ISSN 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, 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 reinforcement 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 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 behavioural diversity among subjects and prevent or reduce the appearance of anomalous behaviour (stereotypic, selfinjurious behaviour; see also Table 1). In fact, in the case of Universities Federation for Animal Welfare primates, abnormal behaviour has been used traditionally as 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 reinforcing specific behaviour by rewarding the individuals exhibiting this behaviour and involves establishing closer contact between keepers and animals. This primatemanagement 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; Science in the Service of Animal Welfare

2 10 Carrasco et al Table 1(a) Study ethogram showing individual behaviours (IB) and social behaviours (SB). Category Individual behaviour Social behaviour Neutral behaviour Inactivity (R) Locomotion (D) Feeding (Alim) Self grooming (AA) Positive/desirable behaviour Acrobatic play (JA) Locomotion (+D) Instrumental play (JI) Feeding (+A) Social play (+J) Social grooming (+AS) Affiliative behaviours (+AF) Negative/undesirable behaviour Deficit behaviours (DF)* Threatening behaviours (+AM) Interaction with the public (PU) Agonistic behaviour (+AN) * Deficit behaviours (DF) are shown below in Table 1(b). Table 1(b) Study ethogram showing deficit behaviours (DF). Behaviour Licking the glass Licking up the vomit of others Regurgitating and licking up one s own vomit Hugging oneself Yawning Self stimulation Coprophagy Stereotypic behaviours with wrists and arms Biting nails Sucking fingers Blowing kisses Sticking the tongue out Description Individuals stick their tongue out and move it along the glass Individuals lick up the vomit left by conspecific Individuals force themselves to vomit and then lick it up Individuals wrap themselves around their own shoulders Individuals open their mouths with no apparent intention of having anyone see it or react to it 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 Eating their own faeces or those of conspecific Individuals shake their wrists and arms for no apparent reason, usually when sitting with their hands open Individuals put their hands in their mouth and bite their fingertips Individuals stick their finger in their mouth and suck it, usually the thumb Individuals place the palm of their hand on their mouth and blow kisses into the air 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 procedures 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 management 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 aggression 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

3 Benefits of training/playing therapy in gorillas 11 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 structured 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, veterinarians, etc) can also have a detrimental effect on the wellbeing 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 particular and the group in general was affected by human interaction 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 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 methodology, 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 m (length breadth height) and two outdoor areas that were exposed to the public. The 90 m 2 vestibule was a covered area with radiant floor heating and platforms and tree trunks arranged at different levels that led into the 345 m 2 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 accustomed 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 encouraged 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 individual 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

4 12 Carrasco et al prior to the animals entering the outdoor area. Whenever possible, work was carried out with these two subjects individually. 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 individuals 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 permission 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 experiments. 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 variability. However, some of the behaviours were actually not detected in many of the short 10-min intervals during the experiment. The number of null observations was particularly 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 behaviours 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.

5 Benefits of training/playing therapy in gorillas 13 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 individually-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 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 behaviours 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 wellbeing. 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

6 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 Batanga Muni Kena Machinda Period 2 Nimba Batanga Muni Kena Machinda 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 Batanga Muni Kena Machinda Yangu Coco 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 Batanga Muni Kena Machinda Yangu Coco 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 behaviours (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.

7 Benefits of training/playing therapy in gorillas 15 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 behaviours, such as inactivity (P = 0.015), locomotion (P = 0.005) and deficit behaviours (P = 0.010). Among social behaviours, 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 behaviours 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. 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 behaviours), 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 categories 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 individual 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 behaviours with the other members of the group.

8 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 Batanga Muni Yangu Cocu Period 4 Nimba Batanga Muni Yangu Cocu Ind: Individual behaviours; Def: Deficit behaviours; Publ: Interactions with the public; Social: Social behaviours. Discussion 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 nonhuman 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 considered an improvement to the psychological well-being of these individuals. Several social behaviours were also 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 behaviours 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 behaviours whose duration increased after playful interaction with humans, it is especially interesting to note the case of playrelated 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.

9 Benefits of training/playing therapy in gorillas 17 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 adaptation 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 statistical 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 affiliative 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 significant 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 behaviours and all social behaviours, in general. This management 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 hypothesis was that the subjects directly involved would begin the 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 behaviours with greater frequency after the sessions with the trainer began. In period 4, it was even observed that the new individuals (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 predominately 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

10 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 intragroup 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. References Abelló MT 2007 Maternal training program results in two mother-reared infants for the first time. Gorilla Gazette 20(1): 12 Baker KC 1997 Human interaction as enrichment for captive chimpanzees: preliminary report. American Journal of Primatology 42: Baker KC 2004 Benefits of positive human interaction for socially housed chimpanzees. 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