Refinement and Environmental Enrichment for Primates: Enrichment 4

Bibliography on Refinement and Environmental Enrichment for Primates. Enrichment 4

(4) Promoting Foraging and Food Processing Behavior

(4,1) Foraging Devices

Bayne K, Dexter SL, Mainzer H, McCully C, Campbell G, Yamada F 1992. The use of artificial turf as a foraging substrate for individually housed rhesus monkeys (Macaca mulatta). Animal Welfare 1, 39-53
Subjects spent on average 15.7 minutes per 30 minute-observation sessions foraging from the device. "An increasing trend in time spent foraging with a concomitant decline in aberrant behaviour over a time period of six months was particularly noteworthy."

Bayne K, Mainzer H, Dexter SL, Campbell G, Yamada F, Suomi SJ 1991. The reduction of abnormal behaviors in individually housed rhesus monkeys (Macaca mulatta) with a foraging/grooming board. American Journal of Primatology 23, 23-35
All of the single-housed "animals foraged from the board to the point that a significant reduction in the level of abnormal behavior was noted." Subjects spent on average 12.1 minutes foraging from the board per 30 minute-observation sessions.

Bjone SJ, Price IR, McGreevy PD 2006. Food distribution effects on the behaviour of captive common marmosets, Callithrix jacchus. Animal Welfare 15, 131-140
"Both the cluster and dispersed feeder distributions increased foraging, and there was a trend of reduced scratching and grooming."

Blanchard M, Gruver S, Kirk P, McLain V, Zebrun M 2005. Look what's hanging around! Foraging feeder cup puzzles for cynomolgus macaques. Tech Talk 10(3), 3
Foraging device is described and demonstrated. It is used by pair-housed cynos to retrieve their daily biscuit ration. No changes in body weights were noticed.

Bertrand F, Seguin Y, Chauvier F, Blanquié JP 1999. Influence of two different kinds of foraging devices on feeding behaviour of rhesus macaques (Macaca mulatta). Folia Primatologica 70, 207
A foraging device fitted on the ceiling of the cage (H), and a foraging device fitted on the front of the cage (V) and filled with pellets were tested in 12 individually housed animals. "The animals moved the pellets from the reserve to a hopper. ... We found that the amount of waste food was up to 17 times lower in the V foraging device than in the control feeder and that the feeding time was much longer with the foraging device than with the control feeder. Over 90% of the food was eaten within the first 15 minutes with the control feeder, whereas it took 60 or 75 minutes to reach this percentage using the foraging device, whether it was a V or an H one. Each puzzle required specific skills. Whichever the feeding device, the subjects ate their whole daily ration and their weight remained stable."

Bloom KR, Cook M 1989. Environmental enrichment: Behavioral responses of rhesus to puzzle feeders. Lab Animal 18(5), 25,27,29,31
A commercial puzzle feeder loaded with 10 whole peanuts is tested in two single-housed adult males. Average time spent foraging from the feeder was about 15 minutes.

Bloomstrand M, Riddle K, Alford PL, Maple TL 1986. Objective evaluation of a behavioral enrichment device for captive chimpanzees (Pan troglodytes). Zoo Biology 5, 293-300
Group-housed individuals spent on average 13 minutes per 120 minute-observation sessions "contacting" the puzzle box. "The most dominant males displayed the highest levels of overall use of this enrichment device. It may be desirable to use this device in groups of animals with relatively stable relationships and/or to increase the number of puzzles available to the group."

Brent L, Eichberg JW 1991. Primate puzzleboard: A simple environmental enrichment device for captive chimpanzees. Zoo Biology 10, 353-360
Treat-loaded transparent board with finger holes is attached to the top of the cage. Mean 'puzzle use' during four 60-minute trials was 17%.

Brent L, Long KE 1995. The behavioral response of individually caged baboons to feeding enrichment and the standard diet: A preliminary report. Contemporary Topics in Laboratory Animal Science 34(2), 65-69
PVC pipe with finger holes, filled with a mixture of peanut butter and seeds. The mean amount of feeder use was 51 minutes per 60 minute observation sessions. "Increasing foraging opportunities in this study reduced abnormal behaviors from 16.4% of the data points in the baseline condition to 4.9% and 5.7% in the chow [normal feeding condition] and feeder condition, respectively."

Celli ML, Tomonagaa M, Udonob T, Teramotob M, Naganob K 2003. Tool use task as environmental enrichment for captive chimpanzees . Applied Animal Behaviour Science 81, 171-182
"A device–honey in a bottle to be "fished" with artificial materials–that elicits tool use was presented to six captive chimpanzees housed in pairs. The task successfully reduced inactivity by about 52%, increased foraging opportunity from 0 to around 31% and elicited tool use and manipulation. ... There was no statistical evidence of habituation to the device."

Corleto J 1997. A-mazing orangutans. The Shape of Enrichment 6(2), 9-10
A food puzzle was constructed and modified several times to take into account the subject's high level of intelligence. "The results were everything I could have hoped for. Not only did he maneuver the [food] items through the maze, he also did it with remarkable speed and concentration."

Crockett CM, Bellanca RU, Heffernan KS, Ronan DA, Bonn WF 2001. Puzzle Ball foraging device for laboratory monkeys. Laboratory Primate Newsletter 40(1), 4-7
"Puzzle Balls are attached outside of the cage. .. Each animal was observed for 10 minutes after six pieces of cereal were placed in the ball. .. Overall, the subjects manipulated the Puzzle Ball during 69.5% of the scan samples. ... Four of the seven subjects were able to successfully empty (eat plus spill) at least one type of Puzzle Ball in less than 10 minutes. (Most spilled about as much as they ate.) For the successful animals, it took an average of five minutes to empty the puzzle. ...Even though the Puzzle Balls were empty during observations [four of seven cases], the subjects manipulate them, although an average of only 1.6% of the time. During the same observations (Puzzle Ball present), the subjects manipulated their portable cage toys (at least one per cage) an average of only 0.9% of the time. (Eight of 17 manipulated neither Puzzle nor toy.) .. We were pleased that the empty Puzzle Balls were associated with a reduction [approximately 60%] in abnormal behavior."

Evans HL, Taylor JD, Ernst J, Graefe JF 1989. Methods to evaluate the well-being of laboratory primates. Comparison of macaques and tamarins. Laboratory Animal Science 39, 318-323
Single-caged long-tailed macaques took on average 8.7 seconds, paired tamarins took on average 15 seconds to retrieve one raisin from the pickup board [miniature ice cube tray attached to front of cage]. Experienced macaques emptied the commercial puzzle filled with the standard food pellet ration within 20 minutes. "After a few days experience with the puzzle, macaques ate from both sources [puzzle feeder and conventional food cup] at the same time, showing no clear preference for either source. This indicates a motivation other than taste or caloric need for performing the puzzle. The puzzle was not adaptable for tamarins since they displayed little or no appetite for any hard food items which could be pushed through the puzzle. Soft foods, such as grapes, raisins, marshmallows or marmoset diet were squeezed out through the small holes rather than being pushed through the maze of the puzzle."

Fekete JM, Norcross JL, Newman JD 2000. Artificial turf foraging boards as environmental enrichment for pair-housed female squirrel monkeys. Contemporary Topics in Laboratory Animal Science 39(2), 22-26
"Five groups of pair-housed female squirrel monkeys were videotaped the week prior to, the week following, and for 2 weeks during the enrichment phase, when treat-enhanced boards were provided for 2 h daily. During the first 30 min of daily enrichment, inactivity declined 35.3%, locomotion increased 3.8%, and board-related behavior occupied 36.3% of the activity budget; these changes were not evident after 1.5 h." Behavioral disorders were not altered by the foraging opportunity.

Gilloux I, Gurnell J, Shepherdson D 1992. An enrichment device for great apes. Animal Welfare 1, 279-289
The animals could manipulate food items to the end of the pipe by poking sticks through holes drilled along the side of the pipe facing them. When the food items reached the end of the pipe, the animals could reach them with their fingers through the welded mesh. No habituation to the feeder was observed during 12 trials. Average time spent in 'feeder-oriented behaviour' during 30 minute trials was approximately 8 minutes for [pair-housed] orangutans and [group-housed] chimpanzees and 5 minutes for [group-housed] gorillas.

*Glenn AS, Watson J 2007. Novel nonhuman primate puzzle feeder reduces food wastage and provides environmental enrichment. AALAS [American Association for Laboratory Animal Science] 58th National Meeting Official Program , 45

"The feeder dispenses monkey chow and fits on nonhuman primate group four quad rack cages. .. The original feeders dispensed 18 to 20 biscuits. At feeding time, the macaques removed all the biscuits within 3 min, and those that were not eaten or stored in cheek pouches were pushed back through the feeder onto the room floor or dropped through the cage floor grid. .. Each feeder took approximately 1 h to make and cost approximately $60 in materials. .. Puzzle feeder implementation increased time spent foraging (approximately 20 min per biscuit), reduced food wastage, and decreased clean-up time."

Goodwin J 1997. The application, use, and effects of training and enrichment variables with Japanese snow macaques (Macaca fuscata) at the Central Park Wildlife Center. American Zoo and Aquarium Association (AZA) Regional Conference Proceedings, 510-515
"Although the [commercial] primate puzzles proved to be a learning success, they were best used sporadically to prevent the macaques from becoming bored with the puzzles."

Kinsey JH, Jorgensen MJ, Platt DM, Hazen TJ 1996. Food puzzle feeders: Effects on self-biting and stereotypy in individually housed monkeys. XVIth Congress of the International Primatological Society/XIXth Conference of the American Society of Primatologists, Abstract No. 683
Subjects were "observed not only when the food puzzle feeder had just been filled in the early morning but at several other time points throughout the day. ... There was no effect on self-aggression; however, a reduction in active stereotypic behavior was noted but only in the first hour of each daily exposure."

Lam K, Rupniak NMJ, Iversen SD 1991. Use of a grooming and foraging substrate to reduce cage stereotypies in macaques. Journal of Medical Primatology 20, 104-109
"Monkeys given fleece sprinkled with morsels of food did not groom the fleece, but foraged for long periods (up to 27 min/h). Stereotyped behaviours were reduced by up to 73% by use of the fleece pad both alone and with foraging crumbles."

LeBlanc D 1993. A simple device for stimulating gummivory in tamarins (Saguinus). American Zoo and Aquarium Association (AZA) Regional Conference Proceedings, 212-219
A simple, custom-made gum-tree was tested. "The artificial gum-tree was hung vertically from the top of the cage with two screw hooks, and placed ideally two or more feet from existing branches and cage walls. All tamarins under 3.5 years in the study utilized the artificial gum-tree. Older tamarins in general ignored this device, but did take gum arabic and diluted maple syrup from a small food bowl."

Line SW, Markowitz H, Morgan KN, Strong S 1989. Evaluation of attempts to enrich the environment of single-caged non-human primates. In Animal Care and Use in Behavioral Research: Regulation, Issues, and Applications Driscoll JW (ed), 103-117. Animal Welfare Information Center, Beltsville
"Rhesus macaques removed monkey biscuits from a puzzle feeder "despite the fact that the same kind of food was available free-choice at the twice-daily feedings."

Lutz CK, Farrow RA 1996. Foraging device for singly housed longtailed macaques does not reduce stereotypies. Contemporary Topics in Laboratory Animal Science 35(3), 75-78
"All [ten] subjects manipulated the foraging boards, but stereotyped behaviors and activity levels were not significantly affected by the presence of the boards." Subjects "used" the boards approximately 2 minutes per 30 minute-observation sessions. "No reduction in board usage was observed over time of day or on repeated presentation, indicating that there was no novelty effect or reduction in motivation."

Maki S, Alford PL, Bloomsmith MA, Franklin J 1989. Food puzzle device simulating termite fishing for captive chimpanzees (Pan troglodytes). American Journal of Primatology 19(Supplement 1), 71-78
"Significant reductions of abnormal behavior and significant increases in activity occurred with the pipe feeder's availability. Species-typical tool-using activity occurred, and the use of the pipe feeder increased subjects' foraging and feeding activity toward more species-normative levels." In the corral-housed groups of nine to 12 animals, competetion for use of the single pipe feeder appeared to induce aggression, with 47 attacks recorded in the groups when the filled feeder was present and none recorded .. prior to the use of the feeder. ... Multiple puzzle devices should be available to group-housed animals to preclude undesirable aggression arising from competition."

Maloney MA, Meiers ST, White J, Romano MA 2006 . Effects of three food enrichment items on the behavior of black lemurs (Eulemur macaco macaco) and ringtail lemurs (Lemur catta) ath the Henson Robinson Zoo, Springfield, Illinois. Journal of Applied Animal Welfare Science 9, 111-127
"The lemurs' behavior appeared [sic] to be most affected by the food enrichment item that required the most manipulation."

Markowitz H 1979. Environmental enrichment and behavioral engineering for captive primates. In Captivity and Behavior Erwin J, Maple T, Mitchell G (eds), 217-238. Van Nostrand Reinhold, New York
Food dispensing apparatuses were developed and successfully implemented as feeding enrichment options for group-housed gibbons, siamangs and diana monkeys. "Frequently, often with free food in their hands, they [gibbons] attempted to get the lights and levers to respond" and missed the opportunity to 'produce' food.
"The problem of excess food lying around and decaying on the floor had been reduced to a minimum."

Mentz I, Perret K 1999. Environmental enrichment bei Flachlandgorillas (Gorilla g. gorilla) - Beobachtungen zur Nahrungsaufnahme und zum Manipulationsverhalten. (Environmental enrichment for lowland gorillas - observations of foraging and manipulation behavior) [German text with English summary]. Der Zoologische Garten 69, 1-15
"Behavioural enrichment possibilities include greater dispersal of food as well as the providing of food boxes or raisin sticks. Each gorilla was engaged intensively with the raisin sticks [5.8% of day], but were especially responsive to the food boxes [15,2% of day]."

Molzen EM, French JA 1989. The problem of foraging in captive callitrichid primates: Behavioral time budgets and foraging skills. In Housing, Care and Psychological Wellbeing of Captive and Laboratory Primates Segal EF (ed), 89-101. Noyes Publications, Park Ridge
The group-housed animals had to hang from above, or sit on the covered bowl to obtain raisins that were mixed with ground corn cob. "The device reduced foraging yield and increased foraging effort to levels similar to those observed in free-ranging populations. These dramatic changes in behavioral profiles were produced even though the foraging device was supplemental to, rather than a replacement for, standard provisioning."

Murchison MA 1992. Task-oriented feeding device for singly caged primates. Laboratory Primate Newsletter 31(1), 9-11
A perforated hard plastic ball loaded with peanuts was attached to the outside of the cage. "The animals spent most of their time sitting on their cage perches. Manipulating the foraging device was the second most time-consuming activity [males 22%, females 8%]."

Murchison MA 1994. Primary forage feeder for singly-caged macaques. Laboratory Primate Newsletter 33(1), 7-8
Perforated feeder box requires the single-housed subject to use the fingers to maneuver biscuits to access holes at different levels. "Apparently the animals consumed nearly all the food retrieved from the forage feeders, leaving less on the cage floor to become contaminated. The animals spent significantly more time foraging with the forage feeder than the standard feeder."

Murchison MA 1995. Forage feeder box for single animal cages. Laboratory Primate Newsletter 34(1), 1-2
Standard feeder with small access holes rather than one big access hole. Time spent foraging during the first hour after biscuit distribution increased from 51 seconds when 40 biscuits were presented in the standard feeder [one large access hole] to 400 seconds when 40 biscuits were presented in the forage feeder [four small access holes]. "There were no differences between the standard and forage feeders in number of biscuits fed and consumed." More biscuits fell on the cage floor and beneath the cage on the floor of the room in the standard feeder situation than in the forage feeder situation.

Murphy DE 1976. Enrichment and occupational devices for orang utans and chimpanzees. International Zoo News 137(23.5), 24-26
"A heavy metal cylinder, 60 cm long and 45 cm in diameter, was capped on each end and bolted to a platform. Three 8 cm holes in the cylinder allowed access to the inside. A short section of a rubber hose was chained near one hole in the cylinder. The chimps were able to use the hose as a tool in a manner similar to fishing for termites or opening a beehive in the wild. The chimpanzees rapidly emptied the container of their morning meal with ingenious manipulation and intense interest. .... Chimps and orangs manipulated their feeders even though ample food was available. On days when the device could be operated by the orang utans, they were observed climbing in the structure about thirty per cent more often than when the device was not operating. There was an apparent increase in general activity. The most encouraging result was a reduction in the female's stereotyped pacing. The environmental enrichment of the chimp exhibit has resulted in a decrease in observable coprophagy, a diversification of the activities, and a probable improvement in the physical and psychological condition of the animals."

Novak MA, Kinsey JH, Jorgensen MJ, Hazen TJ 1998. Effects of puzzle feeders on pathological behavior in individually housed rhesus monkeys. American Journal of Primatology 46, 213-227
"Manipulation of the puzzle feeder was associated with a reduction in pacing and rocking in all subjects; but this effect was transient, occurring only during the first hour after the puzzle feeder was filled with treats. Puzzle feeder manipulation had no effect on self-injurious behavior; in fact, some monkeys with this disorder actually bit themselves while extracting peanuts."

Nishimura S 2006. Owl monkey enrichment ideas. Tech Talk 11(1)
"One enrichment item we use is a small suet basket. We place pieces of fresh fruits, dried fruits, nuts, and ice cubes inside the basket and hang it inside the cages and kennels. The holes in the suet basket are too small for the Aotus to reach through, so they spend a good amount of time trying to manipulate the food pieces with their fingers and teeth.
Another form of enrichment used is a small plastic baskets filled with hay, pine shavings, or Sani Chips to which we add a few nuts, cereal pieces, or mealworms." These two items increase foraging time.

O'Connor E, Reinhardt V 1994. Caged stumptailed macaques voluntarily work for ordinary food. In Touch 1(1), 10-11
"Dan spent 286 seconds retrieving 12 biscuits from the food puzzle after leaving 21 freely available dish-biscuits untouched."

Perret K, Büchner S, Adler HJ 1998. Beschäftigungsprogramme für Schimpansen (Pan troglodytes) im Zoo. (Environmental enrichment program for chimpanzees in zoos) [German text with English summary]. Der Zoologische Garten 68, 95-111
An effective feeding enrichment program for group-housed chimpanzees is described and assessed. The program resulted in a more than two-fold increase in time spent foraging (23.6% per day vs. 57.4% per day).

Poffe A, Melotto S, Gerrard PA 1995. Comparison of four environmental enrichment strategies in captive common marmosets (Callithrix jacchus). Primate Report 42, 24-25
"Access to the puzzles was accompanied by increase in social interaction and activity and decrease in stereotypic behaviour. This behavioural profile was also observed, to a lesser extent, in animals exposed to the 'gum tree'. ... Novel objects alone [toys] failed to significantly alter behaviour."

Preilowski B, Reger M, Engele H 1988. Combining scientific experimentation with conventional housing: A pilot study with rhesus monkeys. American Journal of Primatology 14, 223-234
"The testing apparatus ... was connected to a computer that controlled the test and the distribution of regular monkey chow as reward." Manipulatory activity required by the apparatus reduced motor stereotypies but not self-biting in single-housed subjects.

Prist P., Pizzutto CS, Hashimoto C 2004. Woven vine balls and baskets as feeding enrichment for howler monkeys. Shape of Enrichment 14(2), 1-2
"Our results showed that the animals spent more time foraging when the feeder balls were used [compared to the baskets], since it was more difficult to reach the leaves. The monkeys also explored each of the baskets and stopped spending most of their time on the floor. We concluded that these two enrichment ideas increased the animals' activity through play and exploration, and also increased their use of vertical space and reduced their time on the floor. These behaviors are more species-typical and appropriate for arboreal monkeys."

Reinhardt V 1992. Foraging for commercial chow. Laboratory Primate Newsletter 31(2), 10
"While sitting on swings, platforms or other elevated structures, or clinging to the mesh, individual animals seize a piece of chow [fruit, vegetable or bread] and retrieve a piece [through the mesh of the ceiling]. This simple 'food puzzle' not only promotes non-injurious foraging skills but also keeps the floor relatively clean by avoiding undue spoilage of food. The animals only work for food that they actually eat."

Reinhardt V 1993. Enticing nonhuman primates to forage for their standard biscuit ration. Zoo Biology 12, 307-312
Ordinary feeder-boxes were converted into food puzzles by remounting them onto the mesh of the front of the cages, away from original access holes. The total amount of time [pair-housed] adult male rhesus macaques engaged in gathering the standard biscuit ration was 141 times higher at food puzzles [42.2 min] than at feeder-boxes [0.3 min].

Reinhardt V 1993. Evaluation of an inexpensive custom-made food puzzle used as primary feeder for pair-housed rhesus macaques. Laboratory Primate Newsletter 32(3), 7-8
"Working for their standard food rather than collecting it from freely accessible food boxes did not impair the [pair-housed] animals' body weight maintenance, suggesting that their general health was not impaired by the new feeding technique."

Reinhardt V 1993. Promoting increased foraging behaviour in caged stumptailed macaques. Folia Primatologica 61, 47-51
"Simply remounting the food box [of single-housed subjects] a few centimeters away from the access hole resulted in a 69-fold increase in total time engaged in [biscuit ration] food-retrieving activities."

Reinhardt V 1993. Using the mesh ceiling as a food puzzle to encourage foraging behaviour in caged rhesus macaque (Macaca mulatta). Animal Welfare 2, 165-172
"Daily commercial dry food rations consisting of 33 bar-shaped or 16 star-shaped biscuits per animal were placed on the mesh ceiling of the cages instead of in the feed-boxes. This induced an 80-fold increase and 289-fold increase, respectively, in foraging time" in the pair-housed males.

Reinhardt V 1994. Caged rhesus macaques voluntarily work for ordinary food. Primates 35, 95-98
Individuals spent on average 32 sec retrieving biscuits from the ordinary food box, and 673 sec retrieving biscuits from the food puzzle. "It was inferred that the animals voluntarily worked for ordinary food, with the expression of foraging activities serving as its own reward."

Riviello MC 1995. The use of feeding board as an environmental enrichment device for tufted capuchin monkeys (Cebus apella). Primate Report 42, 23-24
"Results show that the feeding board [on which seeds were scattered] were almost always in use [during 30-minute observations]. ... There was no evidence that the position in which the feeding board was placed [high vs low] influenced its use" by the group-housed animals.

Schapiro SJ, Suarez SA, Porter LM, Bloomsmith MA 1996. The effects of different types of feeding enhancements on the behaviour of single-caged, yearling rhesus macaques. Animal Welfare 5, 129-138
"Enrichment use" in minutes/observation hour was as follows: Turf mats 25.8 minutes; Acrylic puzzles 22.1 minutes; Produce 17.4 minutes; Frozen juice 14.6 minutes.
"We feel that a feeding enrichment program ... that provides some combination of stimulating devices and foods that are novel and require processing, can have a very positive impact on the behaviour of captive primates."

Spector M, Kowalczky MA, Fortman JD, Bennett BT 1994. Design and implementation of a primate foraging tray. Contemporary Topics in Laboratory Animal Science 33(5), 54-55
"Excreta trays have been modified to include [small] foraging trays. The trays are placed under the cages. Videotape observation of [single-housed] 24 animals indicates the trays provide from 30 to over 120 min of foraging activity."

(4,2) Substrates

Anderson JR, Chamove AS 1984. Allowing captive primates to forage. In Standards in Laboratory Animal Management. Proceedings of a Symposium 253-256. The Universities Federation For Animal Welfare, Potters Bar
A woodchip litter substrate reduces abnormal behaviours, primarily self-aggression, and encourages foraging, even in the absence of grain.

Baker KC 1997. Straw and forage material ameliorate abnormal behaviors in adult chimpanzees. Zoo Biology 16, 225-236
"In an [successful] effort to reduce abnormal behaviors, especially regurgitation and reingestion, and promote higher activity levels [locomoting and playing], straw and scattered forage material were added to the enclosures of 13 indoor-housed chimpanzees living in pairs and trios."

*Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, Reinhardt V, Van Loo P 2007 Making Lives Easier for Animals in Research Labs - Chapter 4.3. Feeding Enrichment. Washington, DC: Animal Welfare Institute
"Wood shavings in the catch pans provide an ideal substrate to foster foraging activities. On days when we change the pans three times a week we sprinkle sunflower seeds on the shavings. Our rhesus and squirrel monkeys then search with their fingers through the litter and pull the seeds through the floor grids, eat them or store them in their cheek pouches. Since we change the pans, rather than dump the bedding, we don't have any drainage problems in the rooms. This feeding enrichment technique doesn't require undue extra work time in our colony of approximately 130 monkeys. I'd say the benefit of being able to provide even a brief period of "natural" foraging behavior for our caged primates is worth the little additional time it takes to put the bedding in the pans and add a handful of seeds."

Blois-Heulin C, Jubin R 2004. Influence of the presence of seeds and litter on the behaviour of captive red-capped mangabeys Cercocebus torquatus torquatus. Applied Animal Behaviour Science 85, 340-362
"The addition of both litter and seeds induced a significant decline in self-directed activities and a significant increase in search for food. The presence of litter, with or without seeds, induced diversification of occupation of space."

Boccia ML 1989. Long-term effects of a natural foraging task on aggression and stereotypies in socially housed pigtail macaques. Laboratory Primate Newsletter 28(2), 18-19
"A supplementary feeding of approximately one cup of sunflower seeds were dispersed throughout the cage in the woodchip bedding in the middle of the afternoons, 4-6 hours after the group was fed their daily ration of chow and fruit. ... Two months following the introduction of the foraging task .. stereotypies remained depressed, and hairpulling remained rare. In addition, bedding exploration and other types of exploration remained elevated, and agonistic behaviors remained low."

Brown DL, Gold KC 1997. Effects of straw bedding on non-social and abnormal behavior of captive lowland gorillas (Gorilla gorilla gorilla). In Proceedings on the 2nd International Conference on Environmental Enrichment Holst B (ed), 27-35. Copenhagen Zoo, Frederiksberg
"Two individuals were frequently observed to hold their ears or head while the exhibit was in an unbedded condition. This behavior virtually disappeared in the enriched condition. ... Of the eight individuals found to engage in coprophagy, five individuals were observed to exhibit this behavior in solely the unbedded condition." Individuals who engaged in regurgitation-reingestion demonstrated lower levels of this behavior in the bedded condition.

Bryant CE, Rupniak NMJ, Iversen SD 1988. Effects of different environmental enrichment devices on cage stereotypies and autoaggression in captive cynomolgus monkeys. Journal of Medical Primatology 17, 257-269
"Of the many activities available in the playpen, those that consistently captured the attention of all the [single-housed] animals throughout the 3-week observation period were foraging [in woodchip litter scattered with sunflower seeds placed below the grid floor of the cage]."

Burt DA, Plant M 1990. Observations on a caging system for housing stump-tailed macaques. Animal Technology 41, 175-179
"The removal of metal grids at the bottom of the cage and the introduction of direct access to a substrate mixed with cereals and seeds, had a beneficial effect on the psychological well-being of the [single-housed] macaques by allowing foraging and, in our experience, up to 60% of our macaques' day is now spent in this pursuit."

Byrne GD, Suomi SJ 1991. Effects of woodchips and buried food on behavior patterns and psychological well-being of captive rhesus monkeys. American Journal of Primatology 23, 141-151
The addition of woodchips increased exploration and feeding levels. Burial of regular monkey chow in woodchips had little effect on behavior beyond that of the woodchips alone, increasing exploration and decreasing passivity. The addition of sunflower seeds to the woodchips encouraged increased feeding and exploration and led to decreases in passivity and social interaction. No effect on abnormal behavior.

Chamove AS 2001. Floor-covering research benefits primates. Australian Primatology 14(3), 16-19
"Many zoos, labs, and people keep animals on concrete or in wire cages. It is believed to be hygienic, efficient, and adequate for the needs of the animals. ... We tested a variety of floor-coverings-wood-chips, wood-wool, peat, straw, hay, sawdust, and shredded paper from the cigarette industry. The sawdust did not dry out easily; the paper, wood-wool, hay, and straw did not absorb urine very well; the peat appeared messy with black dust everywhere. Peat was the preferred substrate for those gardeners who worked in the primate unit, and is now enriching some of the flower beds around Stirling Castle. For more practical reasons, we did most of our remaining studies using wood-chips. ... The basic study involved scattering the smallest food items we could find either onto the bare floor or into some substrate... Aggression was reduced. .. Food intake was more evenly distributed. .. Naïve human "smellers" rated the small daily from 1 to 4 -- none, slight, strong, very strong. A bare pen cleaned daily rated just over 1 (slight) on average but received 5 strong and 5 moderate ratings. A pen with chips after 4-8 weeks of no cleaning rated under 0.6 (none-slight), and only a single moderate rating. ...Monkeys preferred to sit on a substrate-covered floor to a bare one. The walls and viewing windows remained cleaner with a floor-covering in place. Monkeys used the floor ten times as much as when it was bare. ... Mature litter is more inhibitory to may disease organisms as well as to yeasts and moulds than fresh litter. ...We found NO bad effects ... The monkeys were foraging 14% of the time through the wood-chips looking for and eating grain even though that same grain was available from hoppers full of the stuff nearby."

Combette C, Anderson JR 1991. Réponses à deux techniques d'enrichissement environmental chez deux espèces de primates en laboratoire (Cebus apella, Lemur macaco). [Response to two environmental enrichment techniques in two primate species (Cebus apella, Lemur macaco) in the laboratory setting. (French text with English summary)] . Cahiers d'Ethologie 11, 1-16
"Locomotion almost doubled in the lemurs when small food items were added to the litter, but only the [group-housed] capuchins engaged in foraging activities to any extent."

Grief L, Fritz J, Maki S 1992. Alternative forage types for captive chimpanzees. Laboratory Primate Newsletter 31(2), 11-13
"Chicken scratch, because it is small and harder to find [in the litter], elicited the most foraging of the three foods ['sweet feed', popcorn]. It is very encouraging to see the chimpanzees still foraging late in the day for these small kernels. In addition, for subjects such as our blind animal, who had one of the highest foraging scores in our study, this [inexpensive] enrichment cannot be overemphasized."

Lutz CK, Novak MA 1995. Use of foraging racks and shavings as enrichment tools for groups of rhesus monkeys (Macaca mulatta). Zoo Biology 14, 463-474
Antagonism decreased when the animals had to search for food in wood shavings.

Mahoney CJ 1992. Some thoughts on psychological enrichment. Lab Animal 21(5), 27,29,32-37
Pans from rabbit cages can be used as foraging trays. "We fill the trays with wood chips or other types of bedding scattered with crushed maize, rice, or raisins, and attach them to the underside of the cage floors with bungie cords, thereby providing the animals with hours of searching activity."

Stegenga L 1993. Modifying spider monkey behavior with the use of environmental variables. The Shape of Enrichment 2(3), 3-4
"During baseline observations, the monkeys spent 7.3% of the time feeding, but when leaves were added to the enclosure, feeding activities increased to 13.1% of the time. ... When the leaves were added to the enclosure, playtime was more significant."

(4,3) Produce

*Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, Reinhardt V, Van Loo P 2007 Making Lives Easier for Animals in Research Labs - Chapter 4.4. Coconuts. Washington, DC: Animal Welfare Institute
"Rhesus don't care much about coconuts, but stump-tailed macaques are fascinated by them and do not get tired "working" on them until the last morsel has disappeared in the drop pan. It never occurred that one of the monkeys somehow became injured while processing a nut.
I give whole coconuts to our individually caged cynos. More than anything, they like them for grooming purposes. It gives them something else to do besides bite themselves. I also had a female who carried her coconut around as if it was a baby, constantly clutching it to her chest, and lip smacking to it, grooming it, etc. She was a chronic alopecia case. The coconut alleviated some unfortunately not all of her stereotypical hair pulling behavior."

*Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, Reinhardt V, Van Loo P 2007 Making Lives Easier for Animals in Research Labs - Chapter 4.3. Feeding Enrichment. Washington, DC: Animal Welfare Institute
"I have given whole watermelons to group-housed rhesus, cynos, bonnet and stump-tailed macaques for several years without noticeable adverse effects. It would be a waste of time to cut the melons into small pieces. The monkeys first gnaw a hole into the rind and then "dig" into the soft and juicy part. They really like this and are kept busy until the last morsel has been eaten. They usually discard the rind, but before they do so they thoroughly remove any soft material and eat it. This usually creates quite a mess, but I don't mind cleaning it up, because the animals enjoy this type of feeding enrichment so much.
We give whole pumpkins to rhesus and cynos in both single- and group-housed environments. I would say that this is one of the most effective foraging device we have ever given our animals. All of them spent hours processing their pumpkin!
I give whole corn with the husk to our pair- and group-housed rhesus and baboons. They love it, and I enjoy observing them "peel and eat," leaving a big mess after they have finished. They gnaw the cob into little pieces that finally fall through the grid floor on the pans. I cannot say whether they actually also eat pieces of the cob, but we have never encountered any health-related problem. I don't mind cleaning up the mess; its worth the treat!
We use corn on the cob for all our caged cynos, rhesus and vervets. The animals give the impression that they love processing and eating the corn. They typically pick the kennels both with their hands and their teeth. When they are done, they proceed gnawing on the cob. I don't know if they actually ingest pieces of it. Even if they do, we have never encountered any clinical problems."

Beirise JH, Reinhardt V 1992. Three inexpensive environmental enrichment options for group-housed Macaca mulatta. Laboratory Primate Newsletter 31(1), 7-8
"We distributed the following enrichment materials on the floor once a week, each on a different day: (1) 1 kg roasted peanuts in their shells; (2) 32 ears of hard corn; (3) one non-corrugated cardboard box. ... After a habituation period of 8 weeks, [2-hour] behavioral observations were made. ...The corn was the most effective eliciter of foraging activity, engaging the animals about 77% of the time. Next in effectiveness was the box (65%) and finally the peanuts (47%)."

Bennett BT, Spector MR 1989. The use of naturally occurring manipulanda to improve the psychological well-being of singly housed baboons. Journal of the American Veterinary Medical Association 194, 1782
The single-housed animals demonstrated a marked reduction of cage stereotypy during the time they had the corn to manipulate.

Nadler RD, Herndon JG, Metz B, Ferrer AC, Erwin J 1992. Environmental enrichment by varied feeding strategies for individually caged young chimpanzees. In Chimpanzee Conservation and Public Health: Environments for the Future Erwin J, Landon JC (eds), 137-145. Diagnon/Bioqual, Rockville
Providing an ear of unhusked corn daily or on alternate days, in addition to laboratory chow, resulted in more time spent contacting food [primarily the corn] an hour after feeding [34% & 55%] than feeding laboratory chow alone [8% & 5%]. Seven of eight [single-housed] animals exhibited less stereotypy on the days they received the ear of corn. Stereotypical behavior, which occurs at relatively low frequencies under natural conditions, was reduced somewhat when the animals were fed three [rather than one] meals."

Waugh C 2002. Coconuts as enrichment item for macaques. Wisconsin Primate Research Center, University of Wisconsin-Madison, Primate Enrichment Forum (electronic discussion group), October 24, 2002
"I give whole coconuts, and have had them last a long time (days/ weeks), until we exchange them with new ones (they are really durable). I have had one male cyno break one open by throwing it around his cage for a few days in a row, and even then it just cracked - he loved the milk and continued to amuse himself by trying to get to the fleshy part inside until we eventually had to take it away from him because it got kind of gross! More than anything, I think they like them for grooming purposes - it gives them something else to do besides bite themselves. I also had a female cyno who carried her coconut around like it was a baby, constantly clutching it to her chest, and lip smacking to it, grooming it, etc. She was a chronic alopecia case, and the coconut aided in her problem somewhat also. In my experience, it is a cheap, quite helpful, and interesting alternative!

(4,4) Ice and Water

Anderson JR, Peignot P, Adelbrecht C 1992. Task-directed and recreational underwater swimming in captive rhesus monkeys (Macaca mulatta). Laboratory Primate Newsletter 31(4), 1-4
"Facilitating thermoregulation and increasing [solitary and social] play are two reasons to consider a swimming facility to be a cheap and clean environmental enrichment."

Anonymous 2006. Is a swimming pool safe for macaques? A discussion. Laboratory Primate Newsletter 45(3), 13
Experience suggest that the provision of a shallow swimming pool provides aneffective, safe environmental enrichment option for macaques.

*Baumans V, Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, Reinhardt V, Van Loo P 2007 Making Lives Easier for Animals in Research Labs - Chapter 8.7. Swimming Pools for Macaques. Washington, DC: Animal Welfare Institute
"We give our pair-housed cynos "bathtubs," filled with 30 to 40 cm deep warm water, a few times a week, and have never encountered any problems other than a lot of splashing. Some monkeys take luxurious baths, others climb a perch and jump into the water, others sit on the side walls and drag their hands in the water, and others wash their fruit in the water. Usually the monkeys make a real mess within the first half hour, and yes they do urinate/defecate in the water. We empty the tubs after about two hours, if the monkeys haven't done it already themselves which is often the case.
There are a few published articles on the use of swimming pools for rhesus, long-tailed and Japanese macaques. None of these papers mention any safety or hygienic problems."

Fritz J, Howell S 1993. The disappearing ice cube. Laboratory Primate Newsletter 32(1), 8
Ice "cubes are distributed across the floor, hidden in high plastic barrels (we call these igloos), tucked into corners of the cages, etc. As the animals come out, the excitement of the hunt starts and continues until the last ice cube is found. Hoarders clutch them to their chests, ... others fill their mouths and carry the cubes to the top of the cage, where they lay them down and watch carefully as the cubes get smaller and smaller. Still others have learned to skate through the puddles, making mad dashes in order to slide further and further." No detrimental effects have been found of providing the ice cubes.

Gilbert SG, Wrenshall E 1989. Environmental enrichment for monkeys used in behavioral toxicology studies. In Housing, Care and Psychological Wellbeing of Captive and Laboratory Primates Segal EF (ed), 244-254. Noyes Publications, Park Ridge
"The pools [stainless-steel frame with 3/8" Plexiglas sides] have been a tremendous success with the younger [cynomolgus] monkeys, who adapt easily to water and are instinctively good swimmers. They will swim under water with their eyes open looking for the raisins and playing with each other."

Hazlewood SJ 2001. From beagles to marmosets - The development of a marmoset breeding cage. Animal Technology 52, 149-152
"The provision of water bath was found to be of little interest to the marmosets, other than to use it as a toilet!"

McNulty J 1993. Enrichment for primates in a toxicology facility. Laboratory Primate Newsletter 32(2), 16
Ice cubes have "been given to hundreds of [probably single-housed] monkeys, and we found no ill effects (e.g., broken teeth)."

Parks KA, Novak MA 1993. Observations of increased activity and tool use in captive rhesus monkeys exposed to troughs of water. American Journal of Primatology 29, 13-25
"These results suggest that exposure to water sources may elicit a broad spectrum of species-typical activity and may be a simple and inexpensive way to enrich the environment of captive [group-housed] rhesus monkeys. ... Standing water was more effective than running water in increasing exploration and object manipulation."

Poulsen E 1994. Monkeys on ice. The Shape of Enrichment 3(1), 7
"I spent an hour or so shoveling fresh, clean new snow into a huge plastic bin and dumped the lot on the floors of each small primate and prosimian indoor enclosure... The event was a tremendous success"

Rademacher A 1997. Gorilla treats served poolside. The Shape of Enrichment 6(3), 11
"Initially, [Rocky, the gorilla], was hesitant and seemed a bit irritated at this presentation of food [floating on the pool's surface], but eventually he waded into the water and retrieved the treats. Rocky will now wade into the pool when food items are tossed in; we no longer need to float them on the surface. He even makes use of the pool occasionally during our hot Arkansas summers, sitting on the bottom, with his arms stretched along the pool's edge."

Schafer J 2005. Primate popsicles. Tech Talk 10(3), 4
"When the frozen enrichment treats were first provided to our rhesus macaques, they showed a great deal of interest and worked steadily at removing the food from the ice. After several months of using this enrichment, the primates still enjoy their frozen treats."

Steele TL, Butler NA, Segar MT, Olson SM 1995. Preferences for food location and foraging requirements in white-handed gibbons. American Zoo and Aquarium Association (AZA) Regional Conference Proceedings, 151-158
"Mixing ice with the food [in buckets] reduced eating time slightly but substantially increased foraging time. Foraging was much more extensive from the top bucket and significantly more food was gathered from this source than from the bottom bucket. The dominance of the male during feeding suggests that more than one food source should be available for multiple animals."

(4,5) Food Preparation and Feeding Schedule

Fritz J, Howell S 1993. The disappearing ice cube. Laboratory Primate Newsletter 32(1), 8
Ice "cubes are distributed across the floor, hidden in high plastic barrels (we call these igloos), tucked into corners of the cages, etc. As the animals come out, the excitement of the hunt starts and continues until the last ice cube is found. Hoarders clutch them to their chests, ... others fill their mouths and carry the cubes to the top of the cage, where they lay them down and watch carefully as the cubes get smaller and smaller. Still others have learned to skate through the puddles, making mad dashes in order to slide further and further." No detrimental effects have been found of providing the ice cubes.

Kerridge FJ 2005. Environmental enrichment to address behavioral differences between wild and captive balck-and-white ruffed lemurs (Varecia variegata). American Journal of Primatology 66, 71-84
"Behavioral enrichment experiments were carried out in which whole rather than chopped fruit was provided and presented in a more naturalistic manner [whole fruit suspended by sisal or jute from wooden polses]. ... Manual manipulation of dietary items increased. Time spent feeding also increased significantly. .. The novel feeding method successfully stimulated the animals to use their hands to obtain and process fruit. It also necessitated bipedal and tripedal suspension. .. The enrichment increased the time spent feeding to levels similar to those seen in the wild.".

Potratz KR, Boettcher C 2006. Rhesus diet smoothies. Tech Talk 11(4), 5
There are a number of situations in which non-human primates need a special diet to provide additional calories. The receipe for a Chow Smoothie for Rhesus macaques is described and consists in incorporating the animal's regular food, tailoring the smoothie to the individual animal's needs, and adding specific supplements, medications, and different flavors. The smoothie was tested on 40 Rhesus macaques ranging in age from 2 to 25 years.

Rademacher A 1997. Gorilla treats served poolside. The Shape of Enrichment 6(3), 11
"Initially, Rocky was hesitant and seemed a bit irritated at this presentation of food [floating on the pool's surface], but eventually he waded into the water and retrieved the treats. Rocky will now wade into the pool when food items are tossed in; we no longer need to float them on the surface. He even makes use of the pool occasionally during our hot Arkansas summers, sitting on the bottom, with his arms stretched along the pool's edge"

(5) Promoting Arboreal Behavior

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