Cage Toys Reduce Abnormal Behavior in Individually Housed Pigtail Macaques Amy L. Kessel & Linda Brent Published online: 04 Jun 2010.

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1 This article was downloaded by: [Dr Kenneth Shapiro] On: 08 June 2015, At: 07:50 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: Cage Toys Reduce Abnormal Behavior in Individually Housed Pigtail Macaques Amy L. Kessel & Linda Brent Published online: 04 Jun To cite this article: Amy L. Kessel & Linda Brent (1998) Cage Toys Reduce Abnormal Behavior in Individually Housed Pigtail Macaques, Journal of Applied Animal Welfare Science, 1:3, , DOI: /s jaws0103_3 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 indirectly in connection with, in relation to or arising out of the use of the Content.

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3 JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 1(3), Copyright O 1998, Lawrence Erlbaum Associates, Inc. Cage Toys Reduce Abnormal Behavior in Individually Housed Pigtail Macaques Amy L. Kessel and Linda Brent Department of laboratory Animal Medicine Southwest Foundation for Biomedical Research As part of a behavioral intervention program that identifies and treats individual nonhuman primates exhibiting abnormal behavior, five individually housed pigtail macaques (Macaca nemestrum) were provided with multiple cage toys in an effort to reduce high levels of abnormal behavior. Ten 30-min observations of each subject were conducted during the baseline condition and again after novel toys were presented, both loose inside the cage and attached to the outside of the cage. The new toys were used during 27% of the observation time. Kong ToysTM were used most consistently by the macaques during the 5-week observation period. Significant decreases in abnormal behavior and cage-directed behavior, as well as significantly increased enrichment use, were evident after the toys were added. Several of the toys were destroyed quickly, and individual differences were evident in the levels of enrichment use and abnormal behavior. Providing multiple manipulable toys as enrichment for pigtail macaques was effective in reducing abnormal behavior and was an important part of an environmental enrichment program for monkeys who could not be housed socially. Federal regulations require the identification of nonhuman primates showing signs of psychological distress. The Code of Federal Regulations states that "special consideration" must be given to nonhuman primates who "show signs of being in psychological distress through behavior or appearance" (Animals and Animal Products, (~)(2), 1991). To improve our animal care program, provide individualized attention, and comply with these regulations, the Southwest Foundation for Biomedical Research in San Antonio, Texas, has developed a program called the "behavioral intervention program," which identifies and treats animals showing signs of psychological distress. The program encompasses a variety of species of nonhuman primates housed at the facility and begins with the training of the care staff to identify abnormal behavior. Requests for reprints should be sent to Linda Brent, Department of Laboratory Animal Medicine, Southwest Foundation for Biomedical Research, P.O. Box , San Antonio, TX

4 228 KESSEL AND BRENT Once abnormal behavior is identified, a report is made to the behavioral staff. The appropriate veterinarian, supervisor, and caregiver are consulted by the behavioral staff to discuss the case and any related physical symptoms. Baseline observations are then conducted to determine potential causes and durations of abnormal behavior. At that time, the behavioral staff also reviews the animal's records, including rearing history, location history, and any reports of previous problems. Baseline data are analyzed and recommendations are made for various "interventions," which typically consist of enrichment strategies such as physical, feeding, sensory, or social enrichment, that have proved successful in similar situations. When the intervention is implemented, data again are collected and analyzed to ascertain whether the abnormal behavior has been reduced. Follow-up observations are conducted, and if one intervention is unsuccessful, different methods of intervention are implemented and evaluated. As part of this behavioral intervention program, a group of five male, individually caged pigtail macaques (Macaca nemestrina) were reported to be exhibiting abnormal behavior. Baseline observations were conducted to determine the type and severity of the problem, and information on enrichment strategies for pigtail macaques was compiled. Our first concern was to address the social needs of the monkeys. Federal regulations suggest that naturally socially living primates be housed in compatible social groups in captivity (Animals and Animal Products, (a), 1991). Information on pigtail macaque introductions indicated that isosexual pairs often were successful (Reinhardt, Liss, & Stevens, 1995), but that in group formation, 58% of the animals did not survive (Messeri & Giacoma, 1987). In another stable pigtail group, both the alpha male and the highest ranking female were killed during a period of changes in the social structure (Bernstein, 1969). Besides the potential for aggression, injury, and death, other problems encountered with social enrichment include disease transmission and dominance issues. According to Oi (1990), wild adult male pigtail macaques interact little with one another. In our study group, pair or group housing was recommended but was deemed too risky because of the differing infectious status of each individual and the possibility that cross-infection might compromise an ongoing, long-term research project at that time. It was decided that nonsocial enrichment options be initiated immediately and that social enrichment be evaluated later. Baseline observations suggested that the pigtails utilized their existing enrichment "toys" often and for long periods of time. Therefore, additional manipulable items were considered as environmental enrichment for this group. Enrichment devices have been reported to have beneficial effects in a number of primate species (Schapiro, Brent, Bloomsmith, & Satterfield, 1991). Previous studies on enrichment for pigtail macaques included physical enrichment with a videotape task and feeding enrichment in the form of a natural foraging task (Boccia, 1989; Lincoln, Andrews, & Rosenblum, 1995). Multiple enrichment devices have been shown to be valuable in group settings by allowing all group members the opportunity to use the enrichment (Lincoln, Andrews, & Rosenblum,

5 CAGE TOYS AND PIGTAIL MACAQUES ). Choice is also considered to be a factor in determining the value of enrichment items, and multiple devices given to a single animal provide that animal with choices. Manipulable objects have been used successfully with macaques on both a long- and a short-term basis, and they helped to avert the development of abnormal behavior during single caging (Brinkman, 1996). The pigtails were provided with multiple new enrichment toys in an effort to reduce high levels of abnormal behavior. METHOD Subjects Subjects were 5 male pigtail macaques (Macaca nemestrina) who averaged 7.4 years of age. All subjects had been housed in 8 ft2 (0.74 m2) single cages equipped with perches for the past 5 years, while engaged in a research project. Subjects had visual, olfactory, and auditory access to each other. Subjects were fed and cages were cleaned twice daily and fruit was given three times per week. Enrichment was available during the baseline condition in the form of a Plaque AttackerTM and a piece of hard oak wood about 1 ft (30 cm) long and 2.5 in (6 cm) in diameter. Observations Observations were conducted using a video camera recorder, focused on an individual macaque, taken at various times of day (0800 to 1700 hr) so as not to interfere with feeding and cleaning schedules. The videotapes were later coded by the first author using a Tandy 102 portable computer and the DATAC program (Paterson, 1992). Baseline observations were recorded during a 6-week period and included ten 30-min observations on each animal. During the intervention stage of the study, the pigtails were provided with multiple commercially available enrichment toys that consisted of a rawhide baseball, a large Kong ToyTM, and a hard rubber ball loose in their cages, and a nylon bone and a hard rubber ring that were attached to the outside of their cages with chain. The wood and the Plaque AttackersT" also continued to be available (see Figure 1). The toys cost between $2 and $6 each (U.S.), with the exception of the wood, which had no cost, and all the toys pictured in Figure 1 cost about $28 (U.S.). During the intervention stage, or toy condition, ten 30-min observations of each subject were videotaped during a 5-week period. The first author then coded the tapes q in the baseline condition, for a total of 25 hr of observation in each condition. Behaviors recorded in both phases of the study were grouped into the

6 230 KESSEL AND BRENT FIGURE 1 Toys evaluated in this study. At top is the nylon bone and ring hung from a chain, and from left to right is the KongTM Toy, the rawhide ball, the wood, Plaque AttackerTM, and rubber ball. following contexts: active behaviors, such as walking or jumping; cage-directed behaviors, such as manipulation of the cage or lock; enrichment-directed, such as manipulation of enrichment objects; fdforage; rest; self-directed, such as grooming or scratching; social, such as threats, lip-smacking, or other behaviors directed at another animal; vocalize; other, such as human- or observer-directed activities. Abnormal behaviors, defined as those qualitatively or quantitatively different from that found in the wild (Erwin & Deni, 1979), included feces painting, hair pulling, and pacing (see Capitanio, 1986, for abnormal behaviors common in macaques). Analysis Behaviors were collapsed into contexts, and repeated measures analysis of variance tests were conducted using Systat for Windows (Evanston, IL) to determine differences between the baseline and the toy conditions. Pearson correlations were conducted to determine if any relations existed between the levels of cage-directed,

7 enrichment-directed, and abnormal behavior over time. Significance was defined as p <.05 for all tests. RESULTS During baseline observations, the pigtails spent an average of 24% of the observation time in abnormal behavior, with individual abnormal behavior ranging from 16% to 35% of the observation time. The existing toys were used 7% of the observation time during the baseline condition. During the toy condition, the macaques used their enrichment toys for an average of 27% of the observation time. The Kong Toym was used the most, at 8% of the observation time, followed closely by the rubber ball at 7%. The rawhide baseball was used 6% of the time, and the bone and ring were used 5%. The wood and the Plaque AttackerTM, which were both present during the baseline condition, were used at much lower levels during the intervention condition (wood: 0.76%; Plaque AttackerTM: 0.50%) than were the newer toys. The use of the toys was reduced over time and began to approach baseline levels during the last few observations (see Figure 2). The Kong ToyTM was used most consistently throughout. However, some of the toys were destroyed and not available after the first few observations. The peak in the use of the rubber ball during Observation 8 resulted from the return of a piece of the ball that had been thrown out of the cage of one pigtail. The addition of the multiple cage toys resulted in a significant decrease in abnormal behavior (F = , p <.0001) and cage-directed behavior (F = 14.91, p <.018), and anhment use (F = , p <.001). Other behavior patterns were not significantly altered when the toys were provided (see Figure 3). O-D Kong Toy t-t M a Baseball Observation Number FIGURE 2 Pigtail macaques' use of novel toys during a 5-week period.

8 232 KESSEL AND BRENT E % n!?o 30 a p 20 c Ė g '0 al a : Baseline Toys FIGURE 3 The levels of behaviors significantly changed after the addition of multiple novel cage toys. The negative correlation between abnormal behavior and enrichment use is illustrated. TABLE 1 Individual Differences in Enrichment Use and Abnormal Behavior (Percentages) IdentiBcation Enrichment Use Abnormal Behavior Abnormal Behavior Number (Toy Condition) (Baseline Condition) (Toy Condition) There was a negative correlation between abnormal behavior and enrichment use (r = , p <.005); abnormal behavior decreased as enrichment use increased after the new toys were provided (see Figure 3). When the abnormal behavior of each individual was reviewed, individual differences were apparent, both before and after the provision of the toys. The macaques who used their enrichment toys the most also had the greatest decreases in the percentage of time they engaged in abnormal behavior (see Table 1). DISCUSSION The provision of multiple cage toys had significant and lasting effects on the behavior of the pigtail macaques in this study. Our goal of reducing abnormal

9 CAGE TOYS AND PIGTAIL MACAQUES 233 behavior was reached, and the pigtails continued to use the toys over the 5-week study period. Although the provision of toys did not totally eliminate the abnormal behaviors of the subjects, this study showed that manipulable objects were highly effective in providing alternative activities to pigtail macaques. Such enrichment techniques should be considered, especially when social enrichment options are limited. Toys were the chosen form of enrichment after baseline observations demonstrated that the pigtails used their existing toys for a large percentage of the observation time. The macaques were very manipulative, and one individual would consistently throw toys out of the cage. When there were no toys in the cage, he would often find other items to manipulate, such as the hose to the water lixit or pieces of the cage, creating husbandry problems for the staff. This macaque used his enrichment toys the most-for an average of 38% of the observation time. In addition to individual difference, there may also be subspecies differences in enrichment use. The pigtailed macaques used their toys for an average of 27% of the observation time, which is probably higher than reports for toy use in other macaque species, although this is difficult to evaluate due to methodological differences between studies. Some researchers have reported the use of inanimate enrichment objects by macaques and their usefulness in reducing abnormal behavior (Bayne, 1989; Bayne, Hurst, & Dexter, 1992; Reinhardt, 1990), but others have found that toys are used very little after a few days of habituation (Line& Morgan, 1991). Our study provided data on the fairly high-level use of enrichment toys by Macaca nemestrina, including both novel toys and those that had been present in the cage for many months. Problems encountered during the study included the rapid destruction of some of the toys. The rawhide balls were destroyed in approximately 24 hr. The hard rubber balls and rings also were destroyed quickly. The longest-lasting of the cage toys were the hard nylon bones, the Kong Toysm, the Plaque Attackersm, and the wood. The Kong ToysTM were used the most and also lasted the longest, suggesting that this may be a cost-effective option as an enrichment toy. Our results support the findings of an earlier study, which found that baboons who were group-housed used Kong Toysm significantly more than Plaque AttackersTM (Brent & Belik, 1997). The baboons in that study used the Kong ToysTM for 12.4% of the observation time, and continued to prefer the Kong Toysm over time. The construction of the cage and the health status of the animals should also be considered when designing enrichment programs. In this study, no health problems attributed to the swallowing of toy pieces was reported. Animals with infectious diseases may have to be handled differently from other animals. For example, regular replacement of toys to increase novelty may increase safety risks. Attaching cage toys to the outside of the cage with chain may eliminate direct contact with the animals, but in this study, loose cage toys were used more frequently than those attached to the cage. This was in contrast to a study by Bayne, Dexter, Hurst,

10 234 KESSEL AND BRENT Strange, and Hill (1993), which found no differences in use between loose Kong ToysTM or those secured to the cage. When designing our behavioral intervention program, we decided to focus on individual animals displaying behavioral problems. This study illustrates that a variety of factors, such as individual and species differences, need to be considered when developing a comprehensive enrichment program, and our behavioral intervention program offers a unique method of accomplishing that goal. REFERENCES Bayne, K. A. L. (1989). Nylon balls re-visited. Laboratory Primate Newsletter, 28, 5-6. Bayne, K. A. L., Dexter, S. L., Hurst, J. K., Strange, G. M., & Hill, E. E. (1993). Kong ToysThi for laboratory primates: Are they really an enrichment or just fomites? Laboratory Animal Science, 43, Bayne, K. A. L., Hurst, J. K., & Dexter, S. L. (1992). Evaluation of the preference to and behavioral effects of an enriched environment on male rhesus monkeys. Laboratory Animal Science, 42,3845. Bernstein, I. S. (1969). Stability of the status hierarchy in apigtail monkey group (Macaca nemestrina). Aninlal Behaviour, 17, Boccia, M. L. (1989). Preliminary repoit on the use of a natural foraging task to reduce aggression and stereotypies in socially housed pigtail macaques. Laboratory Primate Newsletter, 28, 3-4. Brent, L., & Belik, M. (1997). The response of group-housed baboons to three enrichment toys. Laboratory Animals, 31, Brinkman, C. (1996). Toys for the boys: Environmental enrichment for singly housed adult male macaques (Macaca fascicularis). Laboratoql Primate Newsletter, Capitanio, J. P. (1986). Behavioral pathology. In G. Mitchell (Ed.), Comparative primate biology: Vol. 2, Part A. Behavior, corzservation and ). New York: Alan R. Liss. Animals and Animal Products, Pt. 1,9 C.F.R (1991). Erwin, J., & Deni, R. (1979). Strangers in a stmnge land: Abnormal behaviors or abnormal environments? In J. Erwin, T. L. Maple, & G. Mitchell (Eds.), Captivity and behavior, primates in breeding colonies, laboratories and zoos (pp. 1-28). New York: Van Nostrand Reinhold. Lincoln, H., 111, Andrews, M. W., & Rosenblum, L. A. (1994). Environmental structure influences use of multiple video-task devices by socially housed pigtail macaques. Applied Animal Behmiour Science, 41, Lincoln, H., 111, Andrews, M. W., & Rosenblum, L. A. (1995). Pigtail macaque performance on a challenging joystick task has important implications for enrichment and anxiety within a captive environment. Laboratory Animal Science. 45, Line, S. W., &Morgan, K. N. (1991). The effects of two novel objects on the behavior of singly caged adult rhesus macaques. Laboratory Animal Science, Messeri, P., & Giacoma, C. (1987). Variables affecting symmetric interactions in a new-formed group of pigtail macaques. Primate Report, 18, Oi, T. (1990). Patterns of dominance and affiliation in wild pig-tailed macaques (Macaca nemestrina) in West Sumatra. International Journal of Primatology, 11, Paterson, J. D. (1992). Primate behavior. An exercise workbook. Prospect Heights, n: Waveland. Reinhardt, V. (1990). Environmental enrichment program for caged stumptailed macaques (Macaca arctoides). Laboratory Primate Newsletter. 29, 1CL11. Reinhardt, V., Liss, C., & Stevens, C. (1995). Social housing of previously single-caged macaques: What are the options and the risks?animal Welfare, 4, Schapiro, S. J., Brent, L., Bloomsmith, M. A,, & Satterfield, W. C. (1991). Enrichment devices for nonhuman primates. Lab Animal, 20,22-28.