Amanda Shyne a & Martin Block b a Department of Psychology, Bridgewater State. College b Department of Psychology, Northeastern

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1 This article was downloaded by: [Dr Kenneth Shapiro] On: 09 June 2015, At: 08:36 Publisher: Routledge Informa Ltd Registered in England and Wales Registered Number: Registered office: Mortimer House, Mortimer Street, London W1T 3JH, UK Journal of Applied Animal Welfare Science Publication details, including instructions for authors and subscription information: The Effects of Husbandry Training on Stereotypic Pacing in Captive African Wild Dogs (Lycaon pictus) Amanda Shyne a & Martin Block b a Department of Psychology, Bridgewater State College b Department of Psychology, Northeastern University Published online: 16 Dec To cite this article: Amanda Shyne & Martin Block (2010) The Effects of Husbandry Training on Stereotypic Pacing in Captive African Wild Dogs (Lycaon pictus), Journal of Applied Animal Welfare Science, 13:1, 56-65, DOI: / To link to this article: PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the Content ) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or

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3 JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 13:56 65, 2010 Copyright Taylor & Francis Group, LLC ISSN: print/ online DOI: / The Effects of Husbandry Training on Stereotypic Pacing in Captive African Wild Dogs (Lycaon pictus) Amanda Shyne 1 and Martin Block 2 1 Department of Psychology, Bridgewater State College 2 Department of Psychology, Northeastern University To examine the effects of operant conditioning on stereotypic pacing in 3 female African wild dogs located at the Franklin Park Zoo in Boston, this study made recordings of pacing behavior immediately following individual sessions of husbandry training and 2 no-training conditions. The study found significant differences in the percentage of observations spent in stereotypic pacing behaviors for all 3 dogs among the 3 different conditions. The authors discuss the data in terms of the contribution of motivated tasks to the effects and the role of food deprivation in the expression of stereotypic pacing. The study suggests that even short periods of training may improve the African wild dogs welfare by reducing stereotypic pacing following the conditioning sessions. The use of operant conditioning with positive reinforcement in captive nonhuman animals in the zoo is increasing. Zoo training programs are often implemented in order to alleviate stresses correlated with living in a captive environment (Colahan & Breder, 2003; Laule, Bloomsmith, & Schapiro, 2003; Savastano, Hanson, & McCann, 2003; Scott, Pearce, Fairhall, Muggleton, & Smith, 2003). These stresses include veterinarian visits, introductions of new animals, the inability of the animals to control their environment, movement from one location to another, and routine husbandry procedures. To reduce these stresses, many captive animals are trained, using positive reinforcement, to engage in husbandry Correspondence should be sent to Amanda Shyne, Department of Psychology, Bridgewater State College, 321 Hart Hall, 131 Summer Street, Bridgewater, MA amanda.shyne@ bridgew.edu 56

4 EFFECTS OF HUSBANDRY TRAINING 57 behaviors such as going into a crate or standing on a scale. In this way, training allows zoo personnel to reward the animals for engaging in behaviors that are sources of stress for the animals. After the animals learn the new contingencies, for example, the distress responses associated with moving from one holding area to another area to obtain a desired food item are usually reduced if not eliminated. Research interest in these training procedures has focused primarily on improvements in the specific terminal behaviors being trained (McKinley, Buchanan- Smith, Bassett, & Morris, 2003; Young, 2002; Young & Cipreste, 2004). For example, Bloomsmith, Stone, and Laule (1998) demonstrated how chimpanzees could be trained to move voluntarily into specific parts of their enclosures. Weiss and Wilson (2003) trained Aldabra tortoises to stretch and hold for venipuncture, and Reinhardt (2003) also successfully trained macaques to present a leg and accept venipuncture. In addition to training specific behaviors, Reinhardt collected data on the macaques cortisol concentrations (an indicator of stress) and found that the animals in the restraint condition had much higher levels of cortisol than the animals in the cooperation (training) condition. These studies provide evidence that conditioning the animals to engage in these behaviors can enhance behavioral management and may improve the welfare of the zoo species while engaged in such training programs (Bloomsmith, Laule, Alford, & Thurston, 1994). Although this kind of research on positive reinforcement training clearly demonstrates some of the advantages of training, it does not assess the possible effects of training on behaviors occurring after the training sessions. It is possible, for example, that operant conditioning has enriching benefits to the captive animal s welfare beyond its role in husbandry care (Mellen & MacPhee, 2001; Shyne, 2006). Training is often assumed to have general enriching attributes such as reducing stereotypic behavior and encouraging species-appropriate behavior (Colahan & Breder, 2003). However, very few studies have systematically observed these effects after training (Schapiro, Bloomsmith, & Laule, 2003). Thus, although zoo personnel may be observing broad positive behavioral effects following training sessions, there is little published data that directly test the nonhusbandry effects of operant conditioning. Paradoxically, it is also possible that training could have some negative behavioral effects such as reducing species-typical behavior or increasing negative stereotypic behaviors. Clearly there is a very real need for empirical research to analyze the various possible effects of positive reinforcement training objectively (Melfi & Thomas, 2005; Schapiro et al., 2003). In one of the few systematic studies in the literature that investigated training s effects on nontrained behaviors, Kastelein and Wiepkema (1988) found that a group of captive sea lions spent 7.2% of their time participating in stereotypic swimming during baseline (no-training) days and spent 0.5% of their time in

5 58 SHYNE AND BLOCK stereotypic behavior on days when they were engaged in a training program. This finding reflects a positive change in the animals behavioral time budget following the training sessions. Because stereotypic behavior is often understood as an indicator of poor welfare (Mason & Latham, 2004), the reduction of stereotypic behavior observed in the training condition suggests that the animals welfare improved in a general way due to the training. A second study found that common marmosets who were involved in a training program performed less self-scratching (a negative behavioral measure of stress) than did their nontrained counterparts (Bassett, Buchanan-Smith, McKinley, & Smith, 2003). These preliminary studies suggest that training programs may have additional benefits beyond improving husbandry skills and that the training may broadly improve the animals welfare. This study systematically recorded the effects of operant conditioning on the pacing behavior of three captive African wild dogs following short training sessions. The zoo s primary goal for the operant conditioning program was to train the animals to present themselves for veterinary exams. For example, the dogs were trained to open their mouths so the veterinarians could examine their teeth. Although cooperation with routine husbandry tasks are important to everyone concerned with the animals welfare, our specific interest as researchers was focused on the general effects that the husbandry training program had on the behavioral time budget of the dogs. In particular, we compared the amount of time the African wild dogs spent in stereotypic pacing, a common indicator of poor welfare (Mason & Latham, 2004), following operant training periods to nontraining periods. The prediction was the husbandry training would significantly reduce the frequency of pacing. Subjects and Habitat METHOD The subjects of the study are 3 adult African wild dogs located at Franklin Park Zoo in Boston. The dogs are female littermates who were born and parent-reared in the Oklahoma City Zoological Park in They arrived at the Franklin Park Zoo in Their outdoor enclosure is a large naturalistic habitat with much vegetation (trees, tall grasses, various shrubs, and plants) that provides the animals with a number of places to hide. While not on exhibit, the dogs are kept together in a holding facility. The holding area consists of three adjacent stalls, which normally remain open so that the dogs have access to the whole area. When the doors are open, the holding area is 11.8 m long and 2.7 m wide. The dogs are kept in holding every night and during days when the temperature is below 30 ı F.

6 EFFECTS OF HUSBANDRY TRAINING 59 Experimental Conditions The study took place over two winters from January 16, 2004, to March 3, 2005, in the holding area. There were three different observation conditions: (a) training with food, (b) no training without food, and (c) no training with food. Due to the restrictive nature of the holding area, only one experimenter, Amanda Shyne, collected data. All three conditions were intermixed to avoid order variables and regression artifacts. The daily decision as to which observational condition to run was made by the wild dog trainer, Christina Demetrio. This decision was dependent on her schedule; therefore, our ability to control for all possible order confounds was limited. During the training condition with food (T), the dogs were trained using standard operant conditioning methods; the animals daily diet was used as a positive reinforcer during the training sessions. To evaluate the effects of this husbandry training, we compared the dogs behaviors under two additional conditions: a no-training without food condition (NT) and no-training with food condition (NTF). During the NT condition, the dogs were not fed or trained during the observation period, and the dogs diet was given following the data-collection session at approximately their normal feeding time. During the NTF condition, the dogs were fed their daily diet before the observation session when data collection took place. The NTF condition was used because of the large number of studies that indicate a relationship between feeding and stereotypic behavior. Past research, for example, suggests that food restrictions increase the incidence of stereotypes in animals such as poultry (Savory, Seawright, & Watson, 1992) and pigs (Terlouw, Lawrence, & Illius, 1991). Although these dogs were not food deprived, they did not have free access to food and were fed only once a day. This feeding routine could motivate the animals to participate in anticipatory appetitive behaviors prior to the scheduled mealtimes. The NTF condition allowed us to examine the possible contribution of the feeding routine to the behavioral effects observed during the T condition. Training (T) Condition A zookeeper trained the dogs to perform simple husbandry procedures using operant conditioning methods that involved the sound of a metal whistle and the presentation of a food reward. During training, approximations to the desired behavior were followed by a short blast of the whistle and then a piece of raw meat (about the size of a lemon). The animals entire daily diet was fed during each training session. All training sessions took place through a fence in the holding area and therefore did not require any physical contact between the trainer and the wild dogs. Some of the husbandry behaviors trained during the data collection sessions were opening the mouth, putting a paw outside of the

7 60 SHYNE AND BLOCK fence, and touching a target with their nose. During the training process the dogs were separated into three stalls and remained separate until each dog finished the training. On training days, the experimenter would arrive at the holding area at 1:50 in the afternoon to acclimate the dogs to an observer. The holding area was relatively active, so the dogs were accustomed to people moving around and watching them in holding. In addition, the experimenter had watched the dogs in this area for several days during preliminary observation periods. At approximately 2:00 p.m., the zookeeper/dog trainer would arrive, separate the dogs, train them individually, and then release the animals together in holding. The average time spent training the individual dogs was 2.02 min; the longest training session lasted 2.58 min, and the shortest was 1.30 min. The animals were reinforced approximately times during each training session. Data collection for this condition began as soon as the trainer left the immediate vicinity surrounding the dogs enclosure and continued during the hour following the training. Nine days of data were collected in this condition. No-Training (NT) Condition On days when the wild dogs were kept in holding but not trained or yet fed, the experimenter arrived approximately 10 min before 2:00 p.m. for acclimation. Data were collected from 2:00 until 3:00 p.m. On these days, the dogs were separated and fed their daily diet after 3:00 p.m., following data collection. Typically, the dogs were fed at random times between 2:00 and 3:30 p.m. Eight days of behavioral data were collected in this NT condition. No-Training With Food (NTF) Condition During this condition, the experimenter arrived approximately 10 min before 2:00 p.m. The trainer separated the dogs and fed them the same amount of food they received in the other two conditions before releasing the animals together into the holding area. The average time spent feeding each dog was 35 s. Data collection began as soon as the keeper left the immediate vicinity of the dogs holding area and continued for the hour following the feeding. Five days of feeding data were collected under this condition. Behavioral Data and Analyses Preliminary observations showed that the dogs tended to engage in high levels of stereotypic pacing in the holding area; therefore, we focused on whether the training had observable effects on their stereotypic pacing. Any reductions

8 EFFECTS OF HUSBANDRY TRAINING 61 observed in time spent in this behavior during the T condition compared with the NT or NTF conditions would reflect training s effects and suggest an improvement in welfare. The pacing behavior of the dogs was recorded using instantaneous time sampling at 30-s intervals. The nonparametric Friedman Test was used to analyze the differences in the rank order of the relative frequencies of pacing in each of the three conditions. The alpha level was set at.05. Because of the small n, no post hoc test (e.g., the Wilcoxon signed-rank test) could be used for comparing differences between conditions. However, the effect size r was found for each comparison to provide an estimate of the effects of the different conditions. RESULTS After the NT condition, the 3 individual dogs engaged in stereotypic pacing in 36%, 49%, and 49% of the observations, respectively. After the NTF condition, the 3 dogs engaged in stereotypic pacing in 21%, 20%, and 28% of the observations, respectively. After the T condition, the individual dogs engaged in stereotypic pacing 6%, 6%, and 8% of the observations, respectively. See Figure 1 for the average percentage of pacing for the three conditions. The Friedman test showed a significant overall difference across the three conditions (F r (2) D 6.0, p <.05). When the effect size was calculated between the conditions, it was found that the r for each of the three different comparisons (NT-NTF, NT-T, and NTF-T) was the same, namely, r D.71. These equivalent effect sizes are due to the fact that the data were rank ordered for this calculation, FIGURE 1 Average percentage of observations spent in stereotypic behavior following training and no-training conditions.

9 62 SHYNE AND BLOCK and each dog was observed engaging in the same relative amount of pacing after the three conditions: NT > NTF > T. DISCUSSION The results of this study suggest that training sessions can have a greater impact on an individual animal s welfare state than just the husbandry behaviors being trained, as indicated by the marked reduction in pacing immediately following the training condition (Kastelein & Wiepkema, 1988). All three animals exhibited far less stereotypic pacing following training sessions (T) than following either of the two other conditions, NT or NTF. The large reduction in the stereotypic behavior in the T condition requires an explanation that includes more than just the fact that the dogs had been fed. The artificial appetitive behaviors (lifting paw and opening mouth) that the dogs engaged in to acquire a desirable functional consequence (food reinforcement) during training may have substituted for a natural functional appetitive behavior and subsequently fulfilled a behavioral need to control access to their food. A model proposed by Hughes and Duncan (1988) suggests that when an animal s appetitive behaviors are never rewarded with a functional consequence, appetitive behaviors can become close-looped and mutate into abnormal behaviors such as stereotypes. In this situation, some captive animals may learn that their appetitive behaviors are ineffective in controlling certain important aspects of their environment, such as access to food. In this study, the wild dogs learned that specific behavioral responses (lifting paw) to environmental stimuli (cues given by the trainer) could result in a predictable functional outcome. In the Hughes and Duncan (1988) model, these contingencies, set in place with the training, broke the loop of unrewarded appetitive behaviors; provided the dogs with an aspect of control over their environment; and, as a result, could have contributed to the reduction in pacing behavior that occurred following the training sessions. In line with this suggestion, an additional study we have conducted with these dogs while on exhibit indicates that giving them an opportunity to engage in natural foraging-like behaviors by hiding their food in the habitat also had a similar significant effect on reducing the amount of pacing (Shyne, 2005). Another aspect of the results indicates that pacing in the wild dog habitat may be a form of food-related stereotype. The regular provision of meat to the wild dogs every afternoon may be inducing prefeeding stereotypes that are similar to terminal stereotypes observed in other species. Terminal stereotypes are behaviors that can be experimentally induced by delivering food at regular time intervals. The terminal stereotypic behavior is observed at the end of the fasting period immediately before the next meal (Staddon & Simmelhag, 1971).

10 EFFECTS OF HUSBANDRY TRAINING 63 The NTF condition in the present study led to a marked decrease in pacing immediately following the provision of food, strongly suggesting that some of the stereotypic pacing observed in the NT condition was caused by anticipatory frustrations. This type of food-related stereotype has been observed in a number of species including golden hamsters, pigs, sheep, and poultry (Anderson & Shettleworth, 1977; Marsden & Wood-Gush, 1986; Savory et al., 1992; Terlouw et al., 1991), but this is the first study to document the phenomenon in African wild dogs. The care and management of captive populations has been dramatically improved by the use of operant conditioning using positive reinforcement techniques. As mentioned previously, there are many benefits of husbandry training that include, for example, better coping mechanisms for routine stressors (Bassett et al., 2003), voluntary movement from one enclosure to another (Bloomsmith et al., 1998; Bloomsmith et al., 2003), and cooperation during veterinary care (Reinhardt, 2003; Reinhardt & Cowley, 1990; Turkkan, 1990; Vertein & Reinhardt, 1989; Weiss & Wilson, 2003). Our research suggests that operant training, in addition to helping with husbandry care, can more broadly improve welfare. The reduction in stereotypic behavior exhibited by the African wild dogs after the training condition provides direct evidence that the training has the potential to improve the animals general psychological health. The results of this study provide zoo personnel with quantitative evidence of how a common and easily applied behavioral technique can be used to improve a captive animal s well being. ACKNOWLEDGMENTS We thank Zoo New England for their cooperation in conducting this study and, in particular, Christina Demetrio, the African wild dog trainer. We also thank Dr. Judith Hall and Dr. Perrin Cohen for comments on the article. REFERENCES Anderson, M. C., & Shettleworth, S. J. (1977). Behavioural adaptation to fixed-interval and fixedtime food delivery in golden hamsters. Journal of the Experimental Analysis of Behaviour, 25, Bassett, L., Buchanan-Smith, H., McKinley, J., & Smith, T. E. (2003). Effects of training on stressrelated behavior of the common marmoset (Callithrix jacchus) in relation to coping with routine husbandry procedures. Journal of Applied Animal Welfare Science, 6, Bloomsmith, M. A., Jones, M. L., Snyder, R. J., Singer, R. A., Gardner, W. A., Liu, S. C., et al. (2003). Positive reinforcement training to elicit voluntary movement of two giant pandas throughout their enclosure. Zoo Biology, 22,

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