INTRODUCTION A PVC Treat Dispenser and Feeding Enrichment for Pet Capuchin Monkeys In 1985, the Animal Welfare Act (AWA) of 1966 was amended requiring regulated facilities to provide environmental enhancement to promote the psychological well-being of non-human primates (PL 99-198). The Library of Congress defines environmental enrichment as enhancing the environment of confined animals in order to encourage natural behaviors and improve their quality of life (Kreger, 1999).Designing an enrichment program for non-human primates is a challenging and rewarding experience. Enrichment not only includes manipulating an environment to be more stimulating, but also to provide a challenging and interesting feeding program. “Allowing captive non-human primates to actively express food gathering and food processing behaviours counteracts lack of stimulation and hence promotes the animals’ behavioural health and general well-being” (Reinhardt & Roberts 1997, Conclusion section, ¶ 5). Many primates in their natural environment will spend the greater part of their day in search of food; research by Terborgh as well as Robinson and Janson discuss that “a great deal of the capuchin monkeys diet is fruits, but they devote 30-60 % of their daytime hours locating scattered food items” (as cited in Di Bitetti, & Janson 2001, p. 48). A goal of feeding enrichment is to encourage the primate to work for its food rather than merely providing it in a food dish, as discussed by Honess and Marin (2006):In captivity the animals’ time and energy allocation to feeding can be very low as food may be presented in a processed form (e.g. pellets) and in a temporally and spatially clumped manner, removing the need for animals to search for their food or to spend significant time processing it.Puzzle type feeders are a good way to encourage the primate to work for food or treats; they also have other benefits as discussed by Murchison (1992) in that the manipulation of objects delivering a novel and desired food reward can support the cognitive and manipulative needs of monkeys through the exercise of their foraging skills. New ideas and devices to encourage the primate to work for its food are always in demand as the primate may become bored with existing devices. In a short-term evaluation of a foraging device for non-human primates, the researchers suggested that changing to a novel food re-kindled interest in the device and reduced the extinguishing effect (Holmes, Riley, Juneau, Pyne, & Hofing 1994). A good feeding enrichment program should not only rotate existing devices and vary in rewards but also incorporate new ideas. If an enrichment program becomes a monotonous routine of using the same device and food reward day in and day out, it is no longer serving its purpose of enriching the non-human primates’ lives, it merely becomes an anticipated part of the daily schedule. A quality enrichment program should strive to continually challenge the mind and stimulate activity. Ideally, the feeding enrichment device should reflect naturalistic settings and promote naturalistic foraging behaviors as would be encountered in the wild, but this may not always be possible, and for sanitation purposes this may not always be practical. With some creativity, many sufficient items can easily be fabricated out of synthetic materials that are not so naturalistic but equally challenging. Lutz and Novak (2005) discuss that “Although these methods do not necessarily replicate foraging in the wild, they do simulate the process of working for food” (p.182). A great deal of captive pet primates (like those used in this study) live in spacious highly enriched enclosures as opposed to those living in the limited environment of the research setting which makes it difficult to evaluate a program of using enrichment to reduce abnormal stereotypic behaviors often seen in many research primates. Many pet primate owners also provide their pets with vastly enriched enclosures usually that of toys designed for children, additionally they also interact with their primates frequently, but they too continually strive to provide stimulating activities to occupy the time of their primates while they are in their enclosures. Often, feeding enrichment other than that of food variety is overlooked and feeding is usually done by simply putting the food in a dish leaving the primate with little opportunity to forage or put any effort into food gathering. The main purpose of this study is to examine a method of providing a stimulating snack treat feeding activity by using a puzzle-type treat feeding dispenser to encourage the primates to work for their treat rewards and to increase the time spent collecting them. Additionally, this study will examine handedness; observing which hand is used to operate the apparatus and which hand is predominately used in treat retrieval. This study will also observe if prior instruction invokes greater interest in the apparatus.
Participants consisted of 20 healthy pet capuchin monkeys (15 Cebus apella, 3 Cebus capucinus and 2 Cebus olivaceus). Ten males and 10 females ranging from 1–38 years of age (mean = 11.05). Two of the primates were between 1 and 4 years of age and the remaining 18 ranged from 5 to 38 years. The primate participants were solicited from individuals who own pet primates legally in the United States. The treatment of the participants conformed to the guidelines set forth by the American Psychological Association (APA). The primates’ owners acted as observers and recorded the behaviors of their primates.
A PVC treat dispenser as shown in Figure 1 was made for and provided to all participants. Bio-Serv of Frenchtown, NJ provided Supreme Mini-Treats™, Pina-Colada and Very Berry Flavored to be used in the treat dispenser (For nutritional content and ingredients see Appendix A). Due to diet variances and calorie restrictions, the primate owners were afforded the option to use their own treat choice as long as it was of a comparable size to the Supreme Mini-treats .45 in (1.14cm). A Hose clamp or cable ties was used to attach the dispenser to the inside of the primates’ cages. Data sheets to record each primate’s identifying information were provided to the primate’s owners (See Appendix B), included on this data sheet is a table to record observations (See Table B1). Data charts as shown in Figure 2 were created to record hand preference used to retrieve treats and to record hand preference in operation of the treat feeder apparatus.
Each condition was observed for a maximum of five minutes per day over a course of 10 days. On days 1-5, ten treats a day were placed in the primate’s regular feeding dish; the observers recorded time spent collecting treats and which hand was used to retrieve them. The primate participants were split into two groups; Group A was the control group and group B was the experimental group. The monkeys in the control group (Group A) had no instruction (were not shown how the apparatus works), the experimental group (Group B) was shown by the owner that the lifting of the metal rod produces a treat. The owners of group B were instructed to show their primate how to use the apparatus on the beginning of day six when the dispenser was first attached to the cage. On days 6-10 the treat dispenser was filled with 10 treats each day before being attached to an inside wall of the caging material approximately 18 in (45.72 cm) from the cage floor. The primate owners began their observations and data collection immediately after filling and hanging the treat dispenser for a period of five minutes. Non-human primates are extremely curious and keenly aware of any changes to their environments and they instantaneously explore any change. For this reason, the observation period immediately followed the placement and filling of the treat dispenser apparatus. Also, to not disrupt the primate participants regular feeding schedule or diet the treat dispenser was provided between regular feeding schedules and utilized as a between meal snack or treat feeding activity.
RESULTSA paired-samples t test was calculated to compare the mean time spent retrieving treats from the food dish to the mean time spent retrieving treats from the treat dispenser. The mean time spent at the food dish was 122.36 seconds (sd = 64.88), and the mean time spent at the dispenser was 159.71 seconds (sd = 86.85). A significant difference between dish retrieval and dispenser retrieval was found (t(19) = 2.274, p =.035).An independent-samples t test was calculated comparing the mean amount of time using the dispenser with the primates who were shown (instruction) or not shown (no instruction) how the dispenser works. A non-significant trend was found (t(18) = 1.811, p = .087). The mean amount of time in seconds for instruction (m = 192.94, sd = 66.47) was not significantly different from the mean amount of time in seconds for no instruction (m = 126.48, sd = 95.14). An independent-samples t test was calculated comparing the mean time spent collecting treats from the dispenser with the primate’s gender. No significant difference between gender was found (t(18) = .521, p > .05). The mean amount of time in seconds that the males used the dispenser (m = 170.02, sd =75.4) was not significantly different from the mean amount of time in seconds that the females used the dispenser (m = 149.40, sd = 100.01).A paired-samples t test was calculated to compare handedness on the task of treat retrieval from the food dish. The mean percent of time the right hand was used was 47.80 (sd =31.32), and the mean percent of time the left hand was used was 52.20 (sd = 31.32). No significant difference between right hand and left hand preference of treat retrieval from the food dish was found (t(19)=.314, p=.757).A paired-sample t test was calculated to compare handedness on the bimanual task of treat retrieval from the treat dispenser. The mean percent of time for right-handed treat retrieval was 69.00 (sd = 41.04), and the mean percent of time for left-handed treat retrieval was 14.45 (sd = 29.13). A significant difference for hand preference on the bimanual task of treat retrieval was found (t(19)=3.98, p = .001).A paired-sample t test was calculated to compare handedness on the bimanual task of operating the treat dispenser by lifting the metal rod to produce treats. The mean percent of time for right-handed operation of the treat dispenser was 13.50 (sd = 26.99), and the mean percent of time for left-handed operation of the treat dispenser was 70.10 (sd = 42.25). A significant difference for hand preference on the bimanual task of operation of the dispenser was found (t(19)=4.16, p = .001).
DISCUSSIONThe treat dispenser significantly increased time spent gathering treats; many primates actively manipulated the rod in an up and down motion to produce the treats, and some figured out that by holding the rod to maintain its upright position they could continue to remove treats. One primate owner reported that on the first day that the treat dispenser was introduced the monkey initially attempted to unscrew the threaded cap to gain access to the treats, after which the monkey immediately began actively manipulating the feeder. Several of the primates continued to manipulate it with no treats remaining. However, further research may reveal an extinguishing effect as the novelty of the apparatus diminishes. Three of the 20 primates had little to no interest in the dispenser and did not operate it or retrieve any treats. In comparing instruction, though a significant difference was not found, the results indicated that instruction approached significance in the monkeys that were shown how to operate the dispenser. The data revealed a non-significant trend compared with those who were not shown how to operate it. Future research with a larger sample size may reveal a higher success rate with instruction. There was not a significant difference between males and females in regard to time spent using the treat dispenser. Handedness observations revealed no significant hand preference in retrieving treats from an open dish. However, a significant difference was found in the bimanual task in which the task required the primate to lift the metal rod with one hand to produce the treat and to use the other hand to grasp the treat as shown in Figure 3. Some primates used their mouth to lift the rod; the use of mouth only to rod observations were not recorded unless it was immediately followed by using a hand to complete the action of holding the rod. Some primates also lifted the rod with one hand and retrieved the treat with their mouth; the mouth only retrievals were not calculated. If a treat fell from the dispenser to the floor it was recorded as to which hand was used to retrieve the treat. The bimanual task revealed a significant preference for use of the left hand to lift the rod and a right hand preference for treat retrieval. These findings are consistent with research of a bimanual tube task in which a sticky substance food reward was placed inside a suspended tube. The researchers found that 73 % of the monkeys held the tube with their left hand and removed the food with their right hand (Spinozzi, Castorina, & Truppa 1998). Conversely, research done by Westergaard and Suomi (1996) compared hand preference of capuchins and macaques with baited tubes placed on the cage floor, they found a right hand bias in macaques but no bias toward the use of either hand in capuchins. Limitations of this study include multiple observers recording observations; individual interpretation of instructions and data recording may have been inconsistent across observers. Variance in cage size and amount of existing enrichment may also elicit a differential response in relation to use of the feeder. Future research should also take into consideration the primate’s posture when retrieving treats. Previous research on posture in relation to handedness and reaching has revealed a significant shift of hand preference use from quadrupedal to bipedal posture (Spinozzi et al., 1998; Westergaard, Wagner, & Suomi 1999). The mixed species sample in this study may also have had an effect as noted in research done by Westergaard et al. in which they have found there to be differences between Cebus albifrons and Cebus apella in that both have shown a right hand preference in bipedal reaching but differ in quadrupedal reaching (1999).
REFERENCESAnimal Welfare Act, Pub. L. No. 99-198 (1985).Di Bitetti, M., & Janson, C. (2001). Social foraging and the finder`s share in capuchin monkeys, Cebus apella. Animal Behaviour, 62, 47-56.Holmes, S. N., Riley, J. M., Juneau, P., Pyne, D., Hofing, G. L. (1994). Short-term evaluation of a foraging device for non-human primates. Laboratory Animals, 29, 364-369.Honess, P. E., Marin, C. M. (2006). Enrichment and aggression in primates. Neuroscience and Biobehavioral Reviews, 30, 413-346.Kreger, M. D. (1999). Environmental Enrichment for Nonhuman Primates Resource Guide. Retrieved October 10, 2006, from http://www.nal.usda.gov/awic/pubs/primates/primate1.htm#toc15Lutz, C. K., Novak, M. (2005). Environmental enrichment for nonhuman primates: Theory and application. ILAR [Institute for Laboratory Animal Research] Journal 46, 178-191.Murchison, M. A. (1992, January) Task-oriented feeding device for singly caged primates. Laboratory Primate Newsletter, 31, 9-11.Reinhardt, V., & Roberts, A. (1997). Effective feeding enrichment for non-human primates. A brief review. Animal Welfare, 6, 265-272. Retrieved September 13, 2006, from http://www.awionline.org/Lab_animals/biblio/aw2feed.htmSpinozzi, G., Castorina, M. G., & Truppa, V. (1998). Hand preference in unimanual and coordinated-bimanual tasks by tufted capuchin monkeys (Cebus apella). Journal of Comparative Psychology, 112, 183-191Westergaard, G. C., & Suomi, S. J., (1996). Hand preference for a bimanual task in tufted capuchins (Cebus apella) and rhesus macaques (Macaca mulatta). Journal of Comparative Psychology, 110, 406-411Westergaard, G. C., Wagner, J. L., & Suomi, S. J., (1999). Manipulative tendencies of captive Cebus albifrons. International Journal of Primatology, 20, 751-759
APPENDIX ANutrition content and ingredients of Supreme Mini-treatsTypical nutrition content: Protein 19.8%, Fiber 11.7%, Moisture < 10.0%, Fat 6.1%, Ash 4.2%, Carbohydrate 52.0%, Calories: 3.42 kcal/treat, Encapsulated Vitamin C: 1.08 mg/each, Vitamin D3: 2.1 IU/each. Ingredients: Casein, Dextrose, Sucrose, Cellulose, Starch, Corn Oil, Corn Syrup, Choline Bitartrate, Mineral Mix, Vitamin Mix, L-Cystine, Ascorbic Acid, Flavoring Agents, Flowing Agents and Coloring Agents (Very Berry Flavor Only).