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Training success in group-housed long-tailed macaques (Macaca fascicularis) is better explained by personality than by social rank
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Training success in group-housed long-tailed macaques (Macaca fascicularis) is better explained by personality than by social rank Eva-Marie Wergård a,b,∗ , Karolina Westlund a , Mats Spångberg a , Helene Fredlund a , Björn Forkman c a
Department of Comparative Medicine, Karolinska Institutet, SE-171 77 Stockholm, Sweden Department of Zoology, Stockholm University, SE-106 91 Stockholm, Sweden c Department of Large Animal Science, Faculty of Health and Medical Sciences, University of Copenhagen, DK-1870 Frederiksberg C, Denmark b
a r t i c l e
i n f o
Article history: Received 16 December 2014 Received in revised form 9 December 2015 Accepted 19 January 2016 Available online xxx Keywords: Long-tailed macaque Primate Personality Social rank Training Refinement
a b s t r a c t Using training to prepare laboratory animals for biomedical research is one important behavior management task. With increased knowledge about factors influencing training success, training programs may be optimized, resulting in a refinement of primate husbandry. Even when animals are trained under the same conditions there are individual differences in how they respond to training. The current paper focuses on two of the factors potentially influencing training success: social rank and personality. Five observers rated the personality and the social rank of 34 long-tailed macaques (Macaca fascicularis) in an observer trait rating survey. Training success was measured in 22 of these individuals and from four of their shaping protocols; hand-feeding, target training, presenting hands and presenting feet. From the factor analysis four personality traits could be identified: ‘Emotionality’, ‘Activity’, ‘Sociability’, and ‘Tolerance’. A Multiple linear regressions with backward elimination showed that the personality trait ‘Activity’ was associated with training success (adj.R2 = 0.71, p < 0.0005), and unexpectedly, social rank had less influence (adj.R2 = 0.30, p = 0.005) on training success in group-housed long-tailed macaques. We propose that training success can be conceptualized as consisting of two components: access to the trainer and problem solving. In the case of personality, the two components combine to promote training success: curious animals gain access to trainers, and playful animals are good problem solvers; both these adjectives were present in the trait ‘Activity’. In contrast, with regards to rank, qualities that increase access to the trainer (dominance) and traits that promote problem solving (subordinance) counteract one another, potentially explaining why in this study, training was better explained by personality than by rank. We discuss the importance of successfully training different types of personalities in order for the selection of animals in biomedical research to remain random and non-biased, rather than excluding those that do not respond well to training. © 2016 Elsevier B.V. All rights reserved.
1. Introduction Using training to prepare laboratory animals for biomedical research is one important part of animal behavior management (Laule et al., 2003; Prescott and Buchanan-Smith, 2003; Bloomsmith et al., 2006). Training has the potential of enriching the environment and improving the welfare of animals (Westlund, 2014), but can also be a time-consuming activity. Even when animals are trained under the same conditions there are individual
∗ Corresponding author at: Department of Comparative Medicine, Karolinska Institutet, SE-171 77 Stockholm, Sweden. Fax: +46 8 524 278519. E-mail address: [email protected] (E.-M. Wergård).
differences in how they respond to training; while some are easily trained others remain unengaged and can sometimes appear untrainable (Coleman, 2012). We find it vital that the selection of animals within biomedical research remain non-biased, meaning that all animals need to get the opportunity to be successfully trained. This could be managed with tailored behavior management programs, as Coleman (2012) suggests. Therefore, in order to improve training success across all individuals, more knowledge of factors influencing training is needed. The current paper focuses on two of these: social rank and personality. The social rank of animals affect their access to resources, for example in baboons (Papio anubis) (Barton and Whiten, 1993) and starlings (Sturnus vulgaris) (Boogert et al., 2006), where lower
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ranked individuals have reduced access to high quality food. In the case of training the resources are the rewards and thereby the trainer may also be considered a resource. Prescott and Buchanan-Smith (2003) proposed that achievement in training can be influenced by the social rank of the monkey, but do not further develop that reasoning. Schapiro et al. (2003) further report that dominant rhesus monkeys trained in big groups tended to leave their stations to attempt stealing food from subordinates, whose strategies rather involved sitting still at their respective stations. Furthermore, Veeder et al. (2009) found subordinate sooty mangabeys (Cercocebus atys atys) were less compliant when trained to shift between enclosures. These results together suggest that dominant individuals tend to monopolize the training situation. Conversely, Reader and Laland (2001) reviewed primates’ ability to process new information and create new behavior patterns in relation to social status, and found such innovation was more prevalent among low ranking individuals compared to higher ranking animals. In long-tailed macaques (Macaca fascicularis) these results were supported by Bunnell and Perkins (1980), who found that low ranking individuals made fewer errors than high-ranking animals. It is noteworthy that the monkeys performed these learning tasks alone, separated from their social group, since Drea and Wallen (1999) have shown that low ranked rhesus macaques (Macaca mulatta) expressed their knowledge well in a learned task only when out of sight of high ranked group mates. To summarize, high problem-solving abilities thus seem to correlate to low rank, however subordinate individuals are typically inhibited to perform when a dominant individual is present. We consider long-tailed macaques to be a suitable subject when studying the influence of social rank and personality on training success. This species lives in social groups with dominance hierarchies and a despotic dominant style (Else and Lee, 1986); the social rank of the individual monkey may therefore very well influence its success in training when being trained within its social context. To our knowledge there are no studies on how the social rank of monkeys is associated with training success in the context of formal operant training sessions with animals remaining in small social groups. Variations in training success between individuals may also be due to differences in personality, here defined as individual differences in behavior, maintained over time and situations (Freeman and Gosling, 2010). Primate personality, also labelled temperament, has been reported in hundreds of articles, where the main methods to assess personality are through behavioral coding and/or observer trait rating (see the critical review by Freeman et al., 2011). In a study on singly-housed female rhesus macaques, Coleman et al. (2005) labelled monkeys as a function of their latency to approach a novel object as ‘inhibited’, ‘moderate’ or ‘exploratory’. They found that after 12 sessions of training, 75% of the ‘moderate’ and 85% of the ‘exploratory’ monkeys learned the behavior “touch the target”, while only 22% of the ‘inhibited’ monkeys learned the behavior. Although the reaction to a novel object may be related to a specific personality trait, a single test might not give a complete picture of the personality (see Uher and Asendorpf, 2008). An effective personality assessment can be performed through the use of observer trait ratings (Freeman and Gosling, 2010). When performed by observers who know the animals well observer trait rating has been shown to be useful and reliable in a large number of species of primates, e.g., rhesus macaques (Stevenson-Hinde and Zunz, 1978), chimpanzees (Pan troglodytes) (Buirski et al., 1978), olive baboons (P. anubis) (Buirski et al., 1973) and pig-tailed macaques (Macaca nemestrina) (Caine et al., 1983) (see also Freeman and Gosling, 2010 for a review). Observer trait ratings correlate well to assessments based on behavioral coding; they are generally reliable across raters and have been shown to predict long-term behavioral and physiological patterns in subjects. Observer trait ratings are
thus suitable for measuring personality in primates without necessarily having to use behavioral coding to validate personality scores (Freeman and Gosling, 2010). Although individual differences in long-tailed macaque personality have been reported in a few articles (Clarke and Mason, 1988; Welker et al., 1992; Sussman et al., 2012), observer trait ratings have, to our knowledge, not been used in this species. The aim of this study on group-housed long-tailed macaques was to investigate the association between training success and social rank versus personality traits determined by observer trait ratings. We predicted that social rank would influence the success in training to a higher extent than the personality of the monkeys, since the animals were trained within their social group in their home environment. 2. Materials and methods This study was completed alongside and did not interfere with the primates’ regular biomedical experiments. The Stockholm North Ethical Committee on Animal Experiments approved the study (no. N103/13). 2.1. Animals and housing A total of 34 long-tailed macaques, five males and 29 females, were used. All the monkeys were at least F2 purpose-bred in China. Their ages ranged between 6 and 12 years with a mean and median age of nine years at the time of the personality evaluation. From the age of four years they had been housed and trained at Karolinska Institutet, Astrid Fagraeus Laboratory (AFL). All monkeys had their own individual name and number for identification. The monkeys were housed in six uni-sexual groups, ranging in size from four to seven individuals, in an animal biosafety level1 environment. They had access to both indoor (15–17.5 m3 ) and outdoor cages (25–33 m3 ), structurally furnished with branches, swings, ladders, grooming platforms and visual barriers. The monkeys were given pellets (Special Diet Services (NDS), UK) in the morning, and fruits and vegetables in the afternoon. All were similarly enriched according to the facility’s normal enrichment schedule with e.g., tennis balls, treat puzzles and fir cones. All indoor cages also had bedding material on the floor consisting of a mix of straw and sawdust. After arrival to Sweden and AFL, all monkeys were regularly exposed to AFL’s training program through positive reinforcement training, involving habituation and husbandry behaviors (Ramirez, 1999) such as target training, stationing to a specific location, allowing handling of hands and feet, opening the mouth for inspection and presenting reliably for injection. Animals were not separated during training but remained within their group. All trainers had undergone AFL’s animal trainer education and had the same theoretical background. 2.2. Design and procedure The trainers had several years of experience working with long-tailed macaques, and trainers had been training their respective groups for the last two to four years—each group had been assigned only trainer. Each group’s trainers, from here on called the observers, conducted the ratings. Assessments and ratings were performed in connection to this study. Furthermore all observers were familiar with their targeted groups of monkeys in different contexts, such as training, cage furnishing, capture and handling as well as behavioral observation and everyday care including cage cleaning, feeding and provisioning of environmental enrichment. We suggest that this diverse history of interaction limited the risk of training experience influencing the trait rating. By observing the
Please cite this article in press as: Wergård, E.-M., et al., Training success in group-housed long-tailed macaques (Macaca fascicularis) is better explained by personality than by social rank. Appl. Anim. Behav. Sci. (2016), http://dx.doi.org/10.1016/j.applanim.2016.01.017
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Tense Confident Insecure Fearful Strong Apprehensive Anxious Equable Subordinate Sociable Opportunistic Curious Popular Playful Motherly Positive Permissive Aggressive Protective Understanding Solitary Effective Eccentric Gentle Excitable Active Irritable Slow
Factor 1
Factor 2
Factor 3
Factor 4
Emotionality
Activity
Sociability
Tolerance
−0.923 0.906 −0.898 −0.865 0.832 −0.826 −0.716 0.704 −0.655 0.574 0.557 0.552 0.495 0.445 0.440 0.340 0.260 0.256 0.243 0.174 −0.145 0.127 0.09 0.074 0.058 0.056 0.012 0.007
−0.065 0.312 0.074 −0.207 0.398 0.047 −0.194 0.175 −0.463 0.522 0.564 0.526 0.488 0.685 0.123 0.665 0.467 −0.17 0.456 0.215 0.155 0.533 0.893 −0.156 0.454 0.656 0.452 −0.022
−0.078 0.022 −0.17 −0.21 0.108 −0.276 0.018 0.363 −0.163 0.426 0.086 0.281 0.592 0.078 0.633 0.490 −0.026 0.019 0.657 0.119 −0.844 0.19 −0.16 0.308 0.042 −0.071 −0.565 0.151
0.016 −0.063 0.073 −0.104 −0.034 −0.051 −0.018 0.449 −0.003 0.174 0.091 0.169 0.226 0.025 0.166 0.221 0.643 −0.546 0.055 0.806 0.194 0.338 0.046 0.268 −0.680 0.017 −0.295 0.284
Values displayed are factor loadings from Varimax rotation, values above 0.4 and below −0.4 are indicated in bold.
animals in many different contexts more aspects of personality can be evaluated than if they had only been studied in a training situation. Two of the groups had three observers, two groups had two observers and two others had a sole observer. When multiple observers rated a group, the mean of the observers’ rating was used in the analysis. 2.3. Social rank assessment The observers had learned how to assess rank in macaques, for instance by gauging the priority of access to resources and the display of submissive and supplant behaviors. For each group, the observers estimated the social rank of each monkey. The dominant monkey was scored as “one” and the others in ascending order according to their perceived relative ranks. All observers were familiar to the monkeys they rated, either being the animal technician or the trainer of the individuals. Assessments were thus gained from the everyday interaction and experience with the monkeys within their social group and home environment for several years. According to the data obtained the social rank was linear. All 34 monkeys were used in the assessment of the association between personality and social rank. 2.4. Personality assessment A survey consisting of a battery of 28 adjectives (Table 1) (Stevenson-Hinde and Zunz, 1978; Capitanio, 1999) was used to rate each monkey’s individual personality. The adjectives were translated into Swedish, which was the first language of all observers. The rating was done using a visual analog scale (VAS), where a 7 cm long line followed each adjective. On the lines each observer marked their subjective experience of how well they thought the adjectives described the personality of the monkey; from “not at all” to “very well”. For each animal, observer and
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adjective, the placement of the mark was measured in millimeters from the left end of the line to the observer’s mark, and the value entered as the data point. As the observers are working daily with the monkeys, the ranking was assessed from the observers’ everyday interaction and experience of the monkeys. In order not to influence the results, the observers were asked not to discuss their ratings with each other. As a tool for rating subjective experience, VASs have been described as both reliable and sensitive (McCormack et al., 1988). 2.5. Training success Twenty two of the 34 monkeys were used to evaluate training success. These 22 monkeys were all female and located in the same department at AFL. All monkeys had been trained according to prewritten shaping protocols detailing the training and the procedures to obtain different behaviors. Each protocol comprised the gradual approximation steps needed for the behavior trained. Since training time varied between the groups, where two groups had been trained for two years longer than the other two groups, we chose to examine four behaviors that were trained early during our training program (hand-feeding, target training, presenting hands and feet), so that all monkeys would have had the chance to learn them if they responded well to training. We thus believe that elapsed time in the training program was not a confounding factor determining the animals’ learning. To score the actual training success for each monkey we summarized the approximation step from the shaping protocols at the time the personality of the monkey was rated. This gave each monkey a score of how far they had reached in their training; a higher score indicating higher success in training. For example, one monkey had a training success score of 15 (hand-feeding: 6, target training: 4, presenting hands: 3 and presenting feet: 2) while another had a higher training success score of 24 (hand-feeding: 6, target training: 4, presenting hands: 7 and presenting feet: 7). 2.6. Statistical analysis A factor analysis with Varimax rotation was used to uncover the personality traits of the long-tailed macaques. To find the higherorder factor loadings we used both the scree plot (Fig. 1) and the Eigenvalue, above 1, for each factor loading (Cattell, 1966). These were then analysed separately, where values greater than 0.4 or below −0.4 of the adjectives’ primary factor loadings were chosen to characterize the personality trait. The statistical package used was IBM SPSS statistics 21. Multiple linear regressions with backward elimination was used for all correlation analyses, with either training success or social rank as the dependent variable, and the four personality traits entered on a single step as predictors. 3. Results Four factors reached the criteria for a scree plot test (Fig. 1), had an Eigenvalue above 1 and accounted for 76.1% of the total variance in the 34 monkeys. The factors were rotated according to Varimax with Kaizer Normalization and labeled ‘Emotionality’, ‘Activity’, ‘Sociability’ and ‘Tolerance’. Table 1 lists the factor loadings for the Varimax rotated solutions; values above 0.4 and below −0.4 were chosen. To investigate if there was a correlation between training success and the social rank of the monkey we performed a regression analysis on “training success” and “social rank”. This revealed that 30% of the variation found in training success could be explained by the social rank of the monkey (adj.R2 = 0.30, p = 0.005; n = 22) (Fig. 2).
Please cite this article in press as: Wergård, E.-M., et al., Training success in group-housed long-tailed macaques (Macaca fascicularis) is better explained by personality than by social rank. Appl. Anim. Behav. Sci. (2016), http://dx.doi.org/10.1016/j.applanim.2016.01.017
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Fig. 3. Illustration of the relationship between factor 2 ‘Activity’ and the actual training success for each monkey. Table 3 Model summary of the correlation between social rank, rated by five observers familiar to the monkeys, and the factor loadings representing the personality traits of the monkeys. Social rank was best explained by factor 1 ‘Emotionality’.
Fig. 1. Scree plot from the factor ‘Analysis’ of the 34 long-tailed macaques, used to identify the chosen factors to represent the personality of the monkeys. The four factors before the characteristic elbow were chosen, all above Eigenvalue 1.
Model R
Adjusted R-square Std. error of the estimate Predictors (constant)
1 2 3 4
0.610 0.614 0.615 0.600
0.811 0.806 0.799 0.782
1.075 1.068 1.067 1.088
Factor 4,2,3,1 Factor 4,3,1 Factor 3,1 Factor 1
success. Also with the use of this model training success was best explained by factor 2 ‘Activity’ (adj.R2 = 0.71, p < 0.0005; n = 22). In order to investigate if there was an association between personality and social rank in the monkeys a Multiple Regression with Backward elimination was performed. This analysis showed that factor loading 1 ‘Emotionality’ could explain 60% of the social rank of the monkey (adj.R2 = 0.60, p < 0.0005; n = 34) (Table 3). 4. Discussion We propose that the personality trait ‘Activity’ has a major influence on the training success of group-housed long-tailed macaques. Social rank, as assessed by the observers, was not significantly correlated to the trait ‘Activity’. Rank also influenced training success, but to a lesser degree than did personality. Fig. 2. Individual training success and social rank for the four groups (A–D). Number 1 represents the dominant monkey in each group, and the others in ascending order according to their perceived relative ranks. Group size ranged from four to seven animals. In group B, two animals received the same assessment of their rank position.
Table 2 Model summary of the correlation between training success, measured from previous results of the training of four different behaviours, and the factor loadings representing the personality traits of the monkeys. Training success was best explained by factor 2 ‘Activity’. Model R
Adjusted R-square Std. error of the estimate Predictors (constant)
1 2 3 4
0.734 0.725 0.726 0.707
0.886 0.874 0.867 0.849
34.375 34.913 34.827 36.028
Factor 4,2,3,1 Factor 4,2,1 Factor 4,2 Factor 2
We tested whether the monkeys’ training success correlated with their personality. A Multiple Regression with Backward elimination showed that factor loading 2 ‘Activity’ could explain 71% of the variation in the training success of the monkey (adj.R2 = 0.71, p < 0.0005; n = 22) (Table 2; Fig. 3). We then performed a Multiple Linear Regression with factor 2 ‘Activity’ and social rank as simultaneous predictors of training
4.1. Personality traits and training success In addition to the present study with group-housed long-tailed macaques, a few previous studies have shown that there is a correlation between personality and training success in primates; Coleman et al. (2005)—singly housed rhesus macaques, and Reamer et al. (2014)—group-housed chimpanzees. These studies used two different methods to assess personality: a Novel Object test in Coleman et al. (2005) and observer trait rating in Reamer et al. (2014) and the present study. The explorative trait examined in Coleman et al. (2005) and the adjectives ‘active, curious, excitable, opportunistic, playful’ in the personality trait ‘Activity’ identified in this study have similar characteristics. Furthermore, in a study on chimpanzees (Freeman et al., 2013), the personality trait ‘Openness’ loaded onto adjectives such as ‘active, inquisitive/curious, inventive, intelligent, playful’. Although even closely related species such as rhesus and long-tailed macaques show different personality traits (Clarke and Mason, 1988), it seems as if there is a common denominator in what personality traits affect training success in laboratory primates. Indeed, similar results generalize to a wide range of taxa, for example guppie (Poecilia reticulate) (Budaev, 1997), hyena (Crocuta crocuta) (Gosling, 1998) and octopus (Octopus rubescens) (Mather and Anderson, 1993).
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There are a number of limitations in the current study, most notably the relatively small number of animals compared to the number of variables included as well as the same observers not being able to observe all the groups. Despite these limitations however the personality traits found in the study are similar to the ones reported earlier (see above). Below, we focus on two subsets of the identified adjectives that may impact training success in different ways: curiosity/exploration and playfulness. Laboratory primates are not domesticated and in our case they are not tame on arrival to our facility. We might expect that a crucial step in early training is overcoming fear of humans—if this is not achieved, further learning of operant tasks during formal training sessions will be difficult. This corresponds to step1, “encountering new situations” in processes involving learning, where exploratory animals may appear better at problem solving, not because they are better at learning the task, but because they are quicker to encounter and perform the task (Sih and Del Giudice, 2012). We speculate that the inclination to explore and being curious can help the animal overcome fear and provide the motivation to participate in the training session, as illustrated by Coleman et al. (2005). In contrast, in domestic species such as dogs, overcoming fear of human handlers is probably less of a problem with regard to training success, provided that they have had adequate socialization and are tame. However, boldness, a broad personality trait which includes non-social fear, has been found to improve performance in working dogs (Canis familiaris) (Svartberg, 2002). Playfulness could indicate that the animal is in a positive affective state and willing to interact positively with other (Boissy et al., 2007). However, in dogs, playfulness is also correlated with trainability in several studies, e.g., Draper (1995) and it is also an important part of the shyness-boldness factor of Svartberg (2002). Furthermore, Panksepp (1998) has shown that rats that do not play have reduced problem-solving abilities. We suggest that the animal is required to problem solve as it learns the next approximation step during shaping when using positive reinforcement training. Thus, playfulness may help the animal understand the training contingency and improve progress in the sessions. In Coleman et al. (2005), more than half the inhibited monkeys, being non-explorative, never took treats from the trainer, and were consequently not target trained at all—their problem solving abilities were never assessed. We submit that curiosity and exploration are prerequisites to initiate operant training. For long-term best results, the animal must also be able to problem-solve in order to advance quickly during training. It would seem that playfulness plays an important role here, although curiosity has also been found to affect practical problem solving in bushbabies (Otolemur garnettii) learning to solve a latch-box problem (Watson and Ward, 1996). 4.2. Social rank and training success It has earlier been suggested that the structure of the social group might impact what can be achieved when training monkeys in groups (Prescott and Buchanan-Smith, 2003; Schapiro et al., 2003). Our study corroborated this notion: in addition to personality, social rank also influenced training success. In our facility, higher ranked monkeys exhibited higher training success, replicating the findings of Veeder et al. (2009) in sooty mangabeys (C. atys atys). However, according to Bunnell and Perkins (1980) and Reader and Laland (2001), low-ranking individuals out-perform high ranking primates when tested singly but “play dumb” in a social setting (Drea and Wallen, 1999). We observed in our data that if a rank effect occurred, there was a tendency for it to occur somewhere between the third and fifth ranking animal in the groups. Within the highest-ranking cohort in the groups, there was no clear rank effect on training success after several years of training. In addition, accumulated training
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time might be another important element. In our experience, initial training progresses mainly with the dominant individual, who monopolizes access to the trainer and through intimidation prevents the lower ranking animals from approaching. The effect of social rank affecting trainer access may therefore be strongest in the beginning of the training period. Once the hierarchy is established and everyone knows what to do, the signs of dominance/subordination are usually subtle. A potential explanation of our results would be if a correlation exists between personality and the social rank of the monkeys. However, the personality trait ‘Emotionality’ explained 60% of the variation found regarding social rank, whereas training success was best explained by ‘Activity’. This suggests that, while there is a correlation between social rank and personality, training success and social rank are explained by different personality traits. In addition, as outlined above, training success can be conceptualized as consisting of two components: access to the trainer, and problem solving abilities. If the former is not achieved, the latter does not matter. In the case of personality, we argue that traits that increase access to the trainer (curiosity) and problem solving abilities (playfulness) combine to promote training success. In contrast, with regard to social rank, qualities that increase access to the trainer (dominance), and traits that promote problem solving (subordinance), counteract one another with regard to training success. From a theoretical perspective, it is thus not surprising that training success is more influenced by personality than by social rank. In studies where authors have found better problem solving in subordinate animals, they were always tested alone where “access to the trainer” was a non-issue (Bunnel and Perkins, 1980; Reader and Laland, 2001). This reasoning would also explain why ‘Emotionality’ did not correlate with training success to the same extent as ‘Activity’: it involves traits connected to rank which influence training success in opposing ways. 4.3. Methods to increase training success Knowing more about individual differences can be of help when planning animal behavioral management and customize it to promote the welfare of each individual. Several authors have suggested that individual differences in temperament should be taken into account (Boccia et al., 1995; Coleman et al., 2012; Herrelko et al., 2012), by e.g., allocating time differently between animals, as individuals vary in their reaction to the same event and thereby need different efforts. Starling et al. (2013) discuss that individuals are responsive to learning at different arousal levels. Furthermore, Duberstein and Gilkeson (2010) suggest that the gender of the horse could influence what method to choose, i.e., it could beneficial to train geldings differently from mares to obtain optimal training results. In dogs, different evaluation methods have been used to predict if the individual is suited for the proposed line of work (Slabbert and Odendaal, 1999; Serpell and Hsu, 2001). However, in biomedical research such selection may be very inappropriate (Morton et al., 2013), since personality traits also correlates with physiological traits (Capitanio et al., 1999). In order for the selection of animals in biomedical research to remain random and nonbiased, it is vital to find ways to successfully train different types of personalities, instead of excluding those that do not respond well to training. Obtaining access to the animal is the first obstacle when training laboratory non-human primates. Difficulties in doing so may be due to fear (influenced by personality), or social dynamics (influenced by rank). With regard to fear, different kinds of desensitization techniques, where the goal is to change the monkey’s perception of an event to a more neutral one (Hurly and Holmes, 1998), could be used. Counterconditioning (Pearce and Dickinson, 1975) and systematic desensitization (Rachman, 1967), alone or
Please cite this article in press as: Wergård, E.-M., et al., Training success in group-housed long-tailed macaques (Macaca fascicularis) is better explained by personality than by social rank. Appl. Anim. Behav. Sci. (2016), http://dx.doi.org/10.1016/j.applanim.2016.01.017
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in combination, are examples of such techniques. Several studies have shown that these techniques successfully decrease fear responses in monkeys (Goldstein, 1969; Bloomsmith et al., 2006; Clay et al., 2009). Further, in cheetas (Acinonyx jubatus), Baker and Pullen (2013) have showed that ‘Keeper-directed Sociability’ could be improved through an increase of the everyday interaction with humans. One goal of training is to improve Human–AnimalRelationships (Bayne, 2002; Westlund, 2014)—perhaps the reverse, the Human–Animal-Relationship influencing training success, is also true. Concerning social dynamics and animal access, recent guidelines in the Council of Europe suggest the abolition of single housing (Appendix A, of the European Convention for Protection of Vertebrate Animals used for Experimental and other Scientific Purposes, ETS No. 123). Since subordinates succeed better outside the group context (Drea and Wallen, 1999), one solution might be to conduct training sessions in a setting where subordinates are undisturbed—e.g., temporarily separated from their group (Colahan and Breder, 2003). When training several individuals simultaneously, one method to get access to them all is to use cooperation and stationing training (Ramirez, 1999; Colahan and Breder, 2003; McKinley et al., 2003; Schapiro et al., 2003). Another approach is to use multiple trainers simultaneously in big groups, thus reducing the effective group size per trainer (Wergård, unpublished data). Once the animal reliably comes up to the trainer, learning is influenced by problem solving abilities, where one of the key traits is suggested to be playfulness (Montgomery, 2014; Panksepp, 1998). If playfulness influences trainability, it might be important to ensure that animals are housed in conditions that promote play behavior, including an adequate social group (Poirier and Smith, 1974), and provided with suitable structures and enrichment (Morley-Fletcher et al., 2003). Perhaps in doing so, even dominant individuals’ problem solving skills may be improved without having to expose them to the same social environment as subordinates. 5. Conclusion The social structure of the group has been suggested to impact animal training. This study, however, revealed the unexpected result that social rank had less influence than personality when group-housed long-tailed macaques were being trained. Furthermore, we showed that social rank and personality were correlated, but that the personality trait ‘Activity’ was associated with training success, whereas ‘Emotionality’ was associated with the social rank of the monkey. We highlight the importance of successfully training different types of personalities in order for the selection of animals in biomedical research to remain random and non-biased, rather than excluding those that do not respond well to training. Acknowledgements We thank The Swedish Research Council (521-2010-3820) for funding. Mikaela Sandbacka, Maria Valsjö and Jenny Werner at Astrid Fagræus Laboratory, who gave valuable assistance throughout the experiments. References Baker, K., Pullen, K., 2013. The Impact of housing and husbandry on the personality of cheetah (Acinonyx jubatus). J. Zoo Aqua. Res. 1, 35–40. Barton, R.A., Whiten, A., 1993. Feeding competition among female olive baboons (Papio anubis). Anim. Behav. 46, 777–789, http://dx.doi.org/10.1006/anbe. 1993.1255. Bayne, K., 2002. Development of the human-research animal bond and its impact on animal well-being. ILAR J. 43, 4–9, http://dx.doi.org/10.1093/ilar.43.1.4. Bloomsmith, M.A., Schapiro, S.J., Strobert, E.A., 2006. Preparing chimpanzees for laboratory research. ILAR J. 47, 316–325, http://dx.doi.org/10.1093/i.
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Training success in group-housed long-tailed macaques (Macaca fascicularis) is better explained by personality than by social rank Eva-Marie Wergård a,b,∗ , Karolina Westlund a , Mats Spångberg a , Helene Fredlund a , Björn Forkman c a
Department of Comparative Medicine, Karolinska Institutet, SE-171 77 Stockholm, Sweden Department of Zoology, Stockholm University, SE-106 91 Stockholm, Sweden c Department of Large Animal Science, Faculty of Health and Medical Sciences, University of Copenhagen, DK-1870 Frederiksberg C, Denmark b
a r t i c l e
i n f o
Article history: Received 16 December 2014 Received in revised form 9 December 2015 Accepted 19 January 2016 Available online xxx Keywords: Long-tailed macaque Primate Personality Social rank Training Refinement
a b s t r a c t Using training to prepare laboratory animals for biomedical research is one important behavior management task. With increased knowledge about factors influencing training success, training programs may be optimized, resulting in a refinement of primate husbandry. Even when animals are trained under the same conditions there are individual differences in how they respond to training. The current paper focuses on two of the factors potentially influencing training success: social rank and personality. Five observers rated the personality and the social rank of 34 long-tailed macaques (Macaca fascicularis) in an observer trait rating survey. Training success was measured in 22 of these individuals and from four of their shaping protocols; hand-feeding, target training, presenting hands and presenting feet. From the factor analysis four personality traits could be identified: ‘Emotionality’, ‘Activity’, ‘Sociability’, and ‘Tolerance’. A Multiple linear regressions with backward elimination showed that the personality trait ‘Activity’ was associated with training success (adj.R2 = 0.71, p < 0.0005), and unexpectedly, social rank had less influence (adj.R2 = 0.30, p = 0.005) on training success in group-housed long-tailed macaques. We propose that training success can be conceptualized as consisting of two components: access to the trainer and problem solving. In the case of personality, the two components combine to promote training success: curious animals gain access to trainers, and playful animals are good problem solvers; both these adjectives were present in the trait ‘Activity’. In contrast, with regards to rank, qualities that increase access to the trainer (dominance) and traits that promote problem solving (subordinance) counteract one another, potentially explaining why in this study, training was better explained by personality than by rank. We discuss the importance of successfully training different types of personalities in order for the selection of animals in biomedical research to remain random and non-biased, rather than excluding those that do not respond well to training. © 2016 Elsevier B.V. All rights reserved.
1. Introduction Using training to prepare laboratory animals for biomedical research is one important part of animal behavior management (Laule et al., 2003; Prescott and Buchanan-Smith, 2003; Bloomsmith et al., 2006). Training has the potential of enriching the environment and improving the welfare of animals (Westlund, 2014), but can also be a time-consuming activity. Even when animals are trained under the same conditions there are individual
∗ Corresponding author at: Department of Comparative Medicine, Karolinska Institutet, SE-171 77 Stockholm, Sweden. Fax: +46 8 524 278519. E-mail address: [email protected] (E.-M. Wergård).
differences in how they respond to training; while some are easily trained others remain unengaged and can sometimes appear untrainable (Coleman, 2012). We find it vital that the selection of animals within biomedical research remain non-biased, meaning that all animals need to get the opportunity to be successfully trained. This could be managed with tailored behavior management programs, as Coleman (2012) suggests. Therefore, in order to improve training success across all individuals, more knowledge of factors influencing training is needed. The current paper focuses on two of these: social rank and personality. The social rank of animals affect their access to resources, for example in baboons (Papio anubis) (Barton and Whiten, 1993) and starlings (Sturnus vulgaris) (Boogert et al., 2006), where lower
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ranked individuals have reduced access to high quality food. In the case of training the resources are the rewards and thereby the trainer may also be considered a resource. Prescott and Buchanan-Smith (2003) proposed that achievement in training can be influenced by the social rank of the monkey, but do not further develop that reasoning. Schapiro et al. (2003) further report that dominant rhesus monkeys trained in big groups tended to leave their stations to attempt stealing food from subordinates, whose strategies rather involved sitting still at their respective stations. Furthermore, Veeder et al. (2009) found subordinate sooty mangabeys (Cercocebus atys atys) were less compliant when trained to shift between enclosures. These results together suggest that dominant individuals tend to monopolize the training situation. Conversely, Reader and Laland (2001) reviewed primates’ ability to process new information and create new behavior patterns in relation to social status, and found such innovation was more prevalent among low ranking individuals compared to higher ranking animals. In long-tailed macaques (Macaca fascicularis) these results were supported by Bunnell and Perkins (1980), who found that low ranking individuals made fewer errors than high-ranking animals. It is noteworthy that the monkeys performed these learning tasks alone, separated from their social group, since Drea and Wallen (1999) have shown that low ranked rhesus macaques (Macaca mulatta) expressed their knowledge well in a learned task only when out of sight of high ranked group mates. To summarize, high problem-solving abilities thus seem to correlate to low rank, however subordinate individuals are typically inhibited to perform when a dominant individual is present. We consider long-tailed macaques to be a suitable subject when studying the influence of social rank and personality on training success. This species lives in social groups with dominance hierarchies and a despotic dominant style (Else and Lee, 1986); the social rank of the individual monkey may therefore very well influence its success in training when being trained within its social context. To our knowledge there are no studies on how the social rank of monkeys is associated with training success in the context of formal operant training sessions with animals remaining in small social groups. Variations in training success between individuals may also be due to differences in personality, here defined as individual differences in behavior, maintained over time and situations (Freeman and Gosling, 2010). Primate personality, also labelled temperament, has been reported in hundreds of articles, where the main methods to assess personality are through behavioral coding and/or observer trait rating (see the critical review by Freeman et al., 2011). In a study on singly-housed female rhesus macaques, Coleman et al. (2005) labelled monkeys as a function of their latency to approach a novel object as ‘inhibited’, ‘moderate’ or ‘exploratory’. They found that after 12 sessions of training, 75% of the ‘moderate’ and 85% of the ‘exploratory’ monkeys learned the behavior “touch the target”, while only 22% of the ‘inhibited’ monkeys learned the behavior. Although the reaction to a novel object may be related to a specific personality trait, a single test might not give a complete picture of the personality (see Uher and Asendorpf, 2008). An effective personality assessment can be performed through the use of observer trait ratings (Freeman and Gosling, 2010). When performed by observers who know the animals well observer trait rating has been shown to be useful and reliable in a large number of species of primates, e.g., rhesus macaques (Stevenson-Hinde and Zunz, 1978), chimpanzees (Pan troglodytes) (Buirski et al., 1978), olive baboons (P. anubis) (Buirski et al., 1973) and pig-tailed macaques (Macaca nemestrina) (Caine et al., 1983) (see also Freeman and Gosling, 2010 for a review). Observer trait ratings correlate well to assessments based on behavioral coding; they are generally reliable across raters and have been shown to predict long-term behavioral and physiological patterns in subjects. Observer trait ratings are
thus suitable for measuring personality in primates without necessarily having to use behavioral coding to validate personality scores (Freeman and Gosling, 2010). Although individual differences in long-tailed macaque personality have been reported in a few articles (Clarke and Mason, 1988; Welker et al., 1992; Sussman et al., 2012), observer trait ratings have, to our knowledge, not been used in this species. The aim of this study on group-housed long-tailed macaques was to investigate the association between training success and social rank versus personality traits determined by observer trait ratings. We predicted that social rank would influence the success in training to a higher extent than the personality of the monkeys, since the animals were trained within their social group in their home environment. 2. Materials and methods This study was completed alongside and did not interfere with the primates’ regular biomedical experiments. The Stockholm North Ethical Committee on Animal Experiments approved the study (no. N103/13). 2.1. Animals and housing A total of 34 long-tailed macaques, five males and 29 females, were used. All the monkeys were at least F2 purpose-bred in China. Their ages ranged between 6 and 12 years with a mean and median age of nine years at the time of the personality evaluation. From the age of four years they had been housed and trained at Karolinska Institutet, Astrid Fagraeus Laboratory (AFL). All monkeys had their own individual name and number for identification. The monkeys were housed in six uni-sexual groups, ranging in size from four to seven individuals, in an animal biosafety level1 environment. They had access to both indoor (15–17.5 m3 ) and outdoor cages (25–33 m3 ), structurally furnished with branches, swings, ladders, grooming platforms and visual barriers. The monkeys were given pellets (Special Diet Services (NDS), UK) in the morning, and fruits and vegetables in the afternoon. All were similarly enriched according to the facility’s normal enrichment schedule with e.g., tennis balls, treat puzzles and fir cones. All indoor cages also had bedding material on the floor consisting of a mix of straw and sawdust. After arrival to Sweden and AFL, all monkeys were regularly exposed to AFL’s training program through positive reinforcement training, involving habituation and husbandry behaviors (Ramirez, 1999) such as target training, stationing to a specific location, allowing handling of hands and feet, opening the mouth for inspection and presenting reliably for injection. Animals were not separated during training but remained within their group. All trainers had undergone AFL’s animal trainer education and had the same theoretical background. 2.2. Design and procedure The trainers had several years of experience working with long-tailed macaques, and trainers had been training their respective groups for the last two to four years—each group had been assigned only trainer. Each group’s trainers, from here on called the observers, conducted the ratings. Assessments and ratings were performed in connection to this study. Furthermore all observers were familiar with their targeted groups of monkeys in different contexts, such as training, cage furnishing, capture and handling as well as behavioral observation and everyday care including cage cleaning, feeding and provisioning of environmental enrichment. We suggest that this diverse history of interaction limited the risk of training experience influencing the trait rating. By observing the
Please cite this article in press as: Wergård, E.-M., et al., Training success in group-housed long-tailed macaques (Macaca fascicularis) is better explained by personality than by social rank. Appl. Anim. Behav. Sci. (2016), http://dx.doi.org/10.1016/j.applanim.2016.01.017
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Tense Confident Insecure Fearful Strong Apprehensive Anxious Equable Subordinate Sociable Opportunistic Curious Popular Playful Motherly Positive Permissive Aggressive Protective Understanding Solitary Effective Eccentric Gentle Excitable Active Irritable Slow
Factor 1
Factor 2
Factor 3
Factor 4
Emotionality
Activity
Sociability
Tolerance
−0.923 0.906 −0.898 −0.865 0.832 −0.826 −0.716 0.704 −0.655 0.574 0.557 0.552 0.495 0.445 0.440 0.340 0.260 0.256 0.243 0.174 −0.145 0.127 0.09 0.074 0.058 0.056 0.012 0.007
−0.065 0.312 0.074 −0.207 0.398 0.047 −0.194 0.175 −0.463 0.522 0.564 0.526 0.488 0.685 0.123 0.665 0.467 −0.17 0.456 0.215 0.155 0.533 0.893 −0.156 0.454 0.656 0.452 −0.022
−0.078 0.022 −0.17 −0.21 0.108 −0.276 0.018 0.363 −0.163 0.426 0.086 0.281 0.592 0.078 0.633 0.490 −0.026 0.019 0.657 0.119 −0.844 0.19 −0.16 0.308 0.042 −0.071 −0.565 0.151
0.016 −0.063 0.073 −0.104 −0.034 −0.051 −0.018 0.449 −0.003 0.174 0.091 0.169 0.226 0.025 0.166 0.221 0.643 −0.546 0.055 0.806 0.194 0.338 0.046 0.268 −0.680 0.017 −0.295 0.284
Values displayed are factor loadings from Varimax rotation, values above 0.4 and below −0.4 are indicated in bold.
animals in many different contexts more aspects of personality can be evaluated than if they had only been studied in a training situation. Two of the groups had three observers, two groups had two observers and two others had a sole observer. When multiple observers rated a group, the mean of the observers’ rating was used in the analysis. 2.3. Social rank assessment The observers had learned how to assess rank in macaques, for instance by gauging the priority of access to resources and the display of submissive and supplant behaviors. For each group, the observers estimated the social rank of each monkey. The dominant monkey was scored as “one” and the others in ascending order according to their perceived relative ranks. All observers were familiar to the monkeys they rated, either being the animal technician or the trainer of the individuals. Assessments were thus gained from the everyday interaction and experience with the monkeys within their social group and home environment for several years. According to the data obtained the social rank was linear. All 34 monkeys were used in the assessment of the association between personality and social rank. 2.4. Personality assessment A survey consisting of a battery of 28 adjectives (Table 1) (Stevenson-Hinde and Zunz, 1978; Capitanio, 1999) was used to rate each monkey’s individual personality. The adjectives were translated into Swedish, which was the first language of all observers. The rating was done using a visual analog scale (VAS), where a 7 cm long line followed each adjective. On the lines each observer marked their subjective experience of how well they thought the adjectives described the personality of the monkey; from “not at all” to “very well”. For each animal, observer and
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adjective, the placement of the mark was measured in millimeters from the left end of the line to the observer’s mark, and the value entered as the data point. As the observers are working daily with the monkeys, the ranking was assessed from the observers’ everyday interaction and experience of the monkeys. In order not to influence the results, the observers were asked not to discuss their ratings with each other. As a tool for rating subjective experience, VASs have been described as both reliable and sensitive (McCormack et al., 1988). 2.5. Training success Twenty two of the 34 monkeys were used to evaluate training success. These 22 monkeys were all female and located in the same department at AFL. All monkeys had been trained according to prewritten shaping protocols detailing the training and the procedures to obtain different behaviors. Each protocol comprised the gradual approximation steps needed for the behavior trained. Since training time varied between the groups, where two groups had been trained for two years longer than the other two groups, we chose to examine four behaviors that were trained early during our training program (hand-feeding, target training, presenting hands and feet), so that all monkeys would have had the chance to learn them if they responded well to training. We thus believe that elapsed time in the training program was not a confounding factor determining the animals’ learning. To score the actual training success for each monkey we summarized the approximation step from the shaping protocols at the time the personality of the monkey was rated. This gave each monkey a score of how far they had reached in their training; a higher score indicating higher success in training. For example, one monkey had a training success score of 15 (hand-feeding: 6, target training: 4, presenting hands: 3 and presenting feet: 2) while another had a higher training success score of 24 (hand-feeding: 6, target training: 4, presenting hands: 7 and presenting feet: 7). 2.6. Statistical analysis A factor analysis with Varimax rotation was used to uncover the personality traits of the long-tailed macaques. To find the higherorder factor loadings we used both the scree plot (Fig. 1) and the Eigenvalue, above 1, for each factor loading (Cattell, 1966). These were then analysed separately, where values greater than 0.4 or below −0.4 of the adjectives’ primary factor loadings were chosen to characterize the personality trait. The statistical package used was IBM SPSS statistics 21. Multiple linear regressions with backward elimination was used for all correlation analyses, with either training success or social rank as the dependent variable, and the four personality traits entered on a single step as predictors. 3. Results Four factors reached the criteria for a scree plot test (Fig. 1), had an Eigenvalue above 1 and accounted for 76.1% of the total variance in the 34 monkeys. The factors were rotated according to Varimax with Kaizer Normalization and labeled ‘Emotionality’, ‘Activity’, ‘Sociability’ and ‘Tolerance’. Table 1 lists the factor loadings for the Varimax rotated solutions; values above 0.4 and below −0.4 were chosen. To investigate if there was a correlation between training success and the social rank of the monkey we performed a regression analysis on “training success” and “social rank”. This revealed that 30% of the variation found in training success could be explained by the social rank of the monkey (adj.R2 = 0.30, p = 0.005; n = 22) (Fig. 2).
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Fig. 3. Illustration of the relationship between factor 2 ‘Activity’ and the actual training success for each monkey. Table 3 Model summary of the correlation between social rank, rated by five observers familiar to the monkeys, and the factor loadings representing the personality traits of the monkeys. Social rank was best explained by factor 1 ‘Emotionality’.
Fig. 1. Scree plot from the factor ‘Analysis’ of the 34 long-tailed macaques, used to identify the chosen factors to represent the personality of the monkeys. The four factors before the characteristic elbow were chosen, all above Eigenvalue 1.
Model R
Adjusted R-square Std. error of the estimate Predictors (constant)
1 2 3 4
0.610 0.614 0.615 0.600
0.811 0.806 0.799 0.782
1.075 1.068 1.067 1.088
Factor 4,2,3,1 Factor 4,3,1 Factor 3,1 Factor 1
success. Also with the use of this model training success was best explained by factor 2 ‘Activity’ (adj.R2 = 0.71, p < 0.0005; n = 22). In order to investigate if there was an association between personality and social rank in the monkeys a Multiple Regression with Backward elimination was performed. This analysis showed that factor loading 1 ‘Emotionality’ could explain 60% of the social rank of the monkey (adj.R2 = 0.60, p < 0.0005; n = 34) (Table 3). 4. Discussion We propose that the personality trait ‘Activity’ has a major influence on the training success of group-housed long-tailed macaques. Social rank, as assessed by the observers, was not significantly correlated to the trait ‘Activity’. Rank also influenced training success, but to a lesser degree than did personality. Fig. 2. Individual training success and social rank for the four groups (A–D). Number 1 represents the dominant monkey in each group, and the others in ascending order according to their perceived relative ranks. Group size ranged from four to seven animals. In group B, two animals received the same assessment of their rank position.
Table 2 Model summary of the correlation between training success, measured from previous results of the training of four different behaviours, and the factor loadings representing the personality traits of the monkeys. Training success was best explained by factor 2 ‘Activity’. Model R
Adjusted R-square Std. error of the estimate Predictors (constant)
1 2 3 4
0.734 0.725 0.726 0.707
0.886 0.874 0.867 0.849
34.375 34.913 34.827 36.028
Factor 4,2,3,1 Factor 4,2,1 Factor 4,2 Factor 2
We tested whether the monkeys’ training success correlated with their personality. A Multiple Regression with Backward elimination showed that factor loading 2 ‘Activity’ could explain 71% of the variation in the training success of the monkey (adj.R2 = 0.71, p < 0.0005; n = 22) (Table 2; Fig. 3). We then performed a Multiple Linear Regression with factor 2 ‘Activity’ and social rank as simultaneous predictors of training
4.1. Personality traits and training success In addition to the present study with group-housed long-tailed macaques, a few previous studies have shown that there is a correlation between personality and training success in primates; Coleman et al. (2005)—singly housed rhesus macaques, and Reamer et al. (2014)—group-housed chimpanzees. These studies used two different methods to assess personality: a Novel Object test in Coleman et al. (2005) and observer trait rating in Reamer et al. (2014) and the present study. The explorative trait examined in Coleman et al. (2005) and the adjectives ‘active, curious, excitable, opportunistic, playful’ in the personality trait ‘Activity’ identified in this study have similar characteristics. Furthermore, in a study on chimpanzees (Freeman et al., 2013), the personality trait ‘Openness’ loaded onto adjectives such as ‘active, inquisitive/curious, inventive, intelligent, playful’. Although even closely related species such as rhesus and long-tailed macaques show different personality traits (Clarke and Mason, 1988), it seems as if there is a common denominator in what personality traits affect training success in laboratory primates. Indeed, similar results generalize to a wide range of taxa, for example guppie (Poecilia reticulate) (Budaev, 1997), hyena (Crocuta crocuta) (Gosling, 1998) and octopus (Octopus rubescens) (Mather and Anderson, 1993).
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There are a number of limitations in the current study, most notably the relatively small number of animals compared to the number of variables included as well as the same observers not being able to observe all the groups. Despite these limitations however the personality traits found in the study are similar to the ones reported earlier (see above). Below, we focus on two subsets of the identified adjectives that may impact training success in different ways: curiosity/exploration and playfulness. Laboratory primates are not domesticated and in our case they are not tame on arrival to our facility. We might expect that a crucial step in early training is overcoming fear of humans—if this is not achieved, further learning of operant tasks during formal training sessions will be difficult. This corresponds to step1, “encountering new situations” in processes involving learning, where exploratory animals may appear better at problem solving, not because they are better at learning the task, but because they are quicker to encounter and perform the task (Sih and Del Giudice, 2012). We speculate that the inclination to explore and being curious can help the animal overcome fear and provide the motivation to participate in the training session, as illustrated by Coleman et al. (2005). In contrast, in domestic species such as dogs, overcoming fear of human handlers is probably less of a problem with regard to training success, provided that they have had adequate socialization and are tame. However, boldness, a broad personality trait which includes non-social fear, has been found to improve performance in working dogs (Canis familiaris) (Svartberg, 2002). Playfulness could indicate that the animal is in a positive affective state and willing to interact positively with other (Boissy et al., 2007). However, in dogs, playfulness is also correlated with trainability in several studies, e.g., Draper (1995) and it is also an important part of the shyness-boldness factor of Svartberg (2002). Furthermore, Panksepp (1998) has shown that rats that do not play have reduced problem-solving abilities. We suggest that the animal is required to problem solve as it learns the next approximation step during shaping when using positive reinforcement training. Thus, playfulness may help the animal understand the training contingency and improve progress in the sessions. In Coleman et al. (2005), more than half the inhibited monkeys, being non-explorative, never took treats from the trainer, and were consequently not target trained at all—their problem solving abilities were never assessed. We submit that curiosity and exploration are prerequisites to initiate operant training. For long-term best results, the animal must also be able to problem-solve in order to advance quickly during training. It would seem that playfulness plays an important role here, although curiosity has also been found to affect practical problem solving in bushbabies (Otolemur garnettii) learning to solve a latch-box problem (Watson and Ward, 1996). 4.2. Social rank and training success It has earlier been suggested that the structure of the social group might impact what can be achieved when training monkeys in groups (Prescott and Buchanan-Smith, 2003; Schapiro et al., 2003). Our study corroborated this notion: in addition to personality, social rank also influenced training success. In our facility, higher ranked monkeys exhibited higher training success, replicating the findings of Veeder et al. (2009) in sooty mangabeys (C. atys atys). However, according to Bunnell and Perkins (1980) and Reader and Laland (2001), low-ranking individuals out-perform high ranking primates when tested singly but “play dumb” in a social setting (Drea and Wallen, 1999). We observed in our data that if a rank effect occurred, there was a tendency for it to occur somewhere between the third and fifth ranking animal in the groups. Within the highest-ranking cohort in the groups, there was no clear rank effect on training success after several years of training. In addition, accumulated training
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time might be another important element. In our experience, initial training progresses mainly with the dominant individual, who monopolizes access to the trainer and through intimidation prevents the lower ranking animals from approaching. The effect of social rank affecting trainer access may therefore be strongest in the beginning of the training period. Once the hierarchy is established and everyone knows what to do, the signs of dominance/subordination are usually subtle. A potential explanation of our results would be if a correlation exists between personality and the social rank of the monkeys. However, the personality trait ‘Emotionality’ explained 60% of the variation found regarding social rank, whereas training success was best explained by ‘Activity’. This suggests that, while there is a correlation between social rank and personality, training success and social rank are explained by different personality traits. In addition, as outlined above, training success can be conceptualized as consisting of two components: access to the trainer, and problem solving abilities. If the former is not achieved, the latter does not matter. In the case of personality, we argue that traits that increase access to the trainer (curiosity) and problem solving abilities (playfulness) combine to promote training success. In contrast, with regard to social rank, qualities that increase access to the trainer (dominance), and traits that promote problem solving (subordinance), counteract one another with regard to training success. From a theoretical perspective, it is thus not surprising that training success is more influenced by personality than by social rank. In studies where authors have found better problem solving in subordinate animals, they were always tested alone where “access to the trainer” was a non-issue (Bunnel and Perkins, 1980; Reader and Laland, 2001). This reasoning would also explain why ‘Emotionality’ did not correlate with training success to the same extent as ‘Activity’: it involves traits connected to rank which influence training success in opposing ways. 4.3. Methods to increase training success Knowing more about individual differences can be of help when planning animal behavioral management and customize it to promote the welfare of each individual. Several authors have suggested that individual differences in temperament should be taken into account (Boccia et al., 1995; Coleman et al., 2012; Herrelko et al., 2012), by e.g., allocating time differently between animals, as individuals vary in their reaction to the same event and thereby need different efforts. Starling et al. (2013) discuss that individuals are responsive to learning at different arousal levels. Furthermore, Duberstein and Gilkeson (2010) suggest that the gender of the horse could influence what method to choose, i.e., it could beneficial to train geldings differently from mares to obtain optimal training results. In dogs, different evaluation methods have been used to predict if the individual is suited for the proposed line of work (Slabbert and Odendaal, 1999; Serpell and Hsu, 2001). However, in biomedical research such selection may be very inappropriate (Morton et al., 2013), since personality traits also correlates with physiological traits (Capitanio et al., 1999). In order for the selection of animals in biomedical research to remain random and nonbiased, it is vital to find ways to successfully train different types of personalities, instead of excluding those that do not respond well to training. Obtaining access to the animal is the first obstacle when training laboratory non-human primates. Difficulties in doing so may be due to fear (influenced by personality), or social dynamics (influenced by rank). With regard to fear, different kinds of desensitization techniques, where the goal is to change the monkey’s perception of an event to a more neutral one (Hurly and Holmes, 1998), could be used. Counterconditioning (Pearce and Dickinson, 1975) and systematic desensitization (Rachman, 1967), alone or
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in combination, are examples of such techniques. Several studies have shown that these techniques successfully decrease fear responses in monkeys (Goldstein, 1969; Bloomsmith et al., 2006; Clay et al., 2009). Further, in cheetas (Acinonyx jubatus), Baker and Pullen (2013) have showed that ‘Keeper-directed Sociability’ could be improved through an increase of the everyday interaction with humans. One goal of training is to improve Human–AnimalRelationships (Bayne, 2002; Westlund, 2014)—perhaps the reverse, the Human–Animal-Relationship influencing training success, is also true. Concerning social dynamics and animal access, recent guidelines in the Council of Europe suggest the abolition of single housing (Appendix A, of the European Convention for Protection of Vertebrate Animals used for Experimental and other Scientific Purposes, ETS No. 123). Since subordinates succeed better outside the group context (Drea and Wallen, 1999), one solution might be to conduct training sessions in a setting where subordinates are undisturbed—e.g., temporarily separated from their group (Colahan and Breder, 2003). When training several individuals simultaneously, one method to get access to them all is to use cooperation and stationing training (Ramirez, 1999; Colahan and Breder, 2003; McKinley et al., 2003; Schapiro et al., 2003). Another approach is to use multiple trainers simultaneously in big groups, thus reducing the effective group size per trainer (Wergård, unpublished data). Once the animal reliably comes up to the trainer, learning is influenced by problem solving abilities, where one of the key traits is suggested to be playfulness (Montgomery, 2014; Panksepp, 1998). If playfulness influences trainability, it might be important to ensure that animals are housed in conditions that promote play behavior, including an adequate social group (Poirier and Smith, 1974), and provided with suitable structures and enrichment (Morley-Fletcher et al., 2003). Perhaps in doing so, even dominant individuals’ problem solving skills may be improved without having to expose them to the same social environment as subordinates. 5. Conclusion The social structure of the group has been suggested to impact animal training. This study, however, revealed the unexpected result that social rank had less influence than personality when group-housed long-tailed macaques were being trained. Furthermore, we showed that social rank and personality were correlated, but that the personality trait ‘Activity’ was associated with training success, whereas ‘Emotionality’ was associated with the social rank of the monkey. We highlight the importance of successfully training different types of personalities in order for the selection of animals in biomedical research to remain random and non-biased, rather than excluding those that do not respond well to training. Acknowledgements We thank The Swedish Research Council (521-2010-3820) for funding. Mikaela Sandbacka, Maria Valsjö and Jenny Werner at Astrid Fagræus Laboratory, who gave valuable assistance throughout the experiments. References Baker, K., Pullen, K., 2013. The Impact of housing and husbandry on the personality of cheetah (Acinonyx jubatus). J. Zoo Aqua. Res. 1, 35–40. Barton, R.A., Whiten, A., 1993. Feeding competition among female olive baboons (Papio anubis). Anim. Behav. 46, 777–789, http://dx.doi.org/10.1006/anbe. 1993.1255. Bayne, K., 2002. Development of the human-research animal bond and its impact on animal well-being. ILAR J. 43, 4–9, http://dx.doi.org/10.1093/ilar.43.1.4. Bloomsmith, M.A., Schapiro, S.J., Strobert, E.A., 2006. Preparing chimpanzees for laboratory research. ILAR J. 47, 316–325, http://dx.doi.org/10.1093/i.
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Please cite this article in press as: Wergård, E.-M., et al., Training success in group-housed long-tailed macaques (Macaca fascicularis) is better explained by personality than by social rank. Appl. Anim. Behav. Sci. (2016), http://dx.doi.org/10.1016/j.applanim.2016.01.017