Refinement and Environmental Enrichment for Primates: Enrichment 4

Bibliographyon Refinement and Environmental Enrichment for Primates. Enrichment4

(4) PromotingForaging and Food Processing Behavior

(4,1) ForagingDevices

Bayne K, Dexter SL, Mainzer H, McCully C, Campbell G, YamadaF 1992. Theuse of artificial turf as a foraging substrate for individuallyhoused rhesus monkeys (Macaca mulatta). Animal Welfare1, 39-53
Subjects spent on average 15.7 minutes per 30 minute-observationsessions foraging from the device. "An increasing trend intime spent foraging with a concomitant decline in aberrant behaviourover a time period of six months was particularly noteworthy."

Bayne K, Mainzer H, Dexter SL, Campbell G, Yamada F, SuomiSJ 1991. The reduction of abnormal behaviors in individually housedrhesus monkeys (Macaca mulatta) with a foraging/groomingboard. American Journal of Primatology 23, 23-35
All of the single-housed "animals foraged from the boardto the point that a significant reduction in the level of abnormalbehavior was noted." Subjects spent on average 12.1 minutesforaging 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 increasedforaging, and there was a trend of reduced scratching and grooming."

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

Bertrand F, Seguin Y, Chauvier F, Blanquié JP 1999.Influence of two different kinds of foraging devices on feedingbehaviour of rhesus macaques (Macaca mulatta). FoliaPrimatologica 70, 207
A foraging device fitted on the ceiling of the cage (H), anda foraging device fitted on the front of the cage (V) and filledwith pellets were tested in 12 individually housed animals. "Theanimals moved the pellets from the reserve to a hopper. ... Wefound that the amount of waste food was up to 17 times lower inthe V foraging device than in the control feeder and that thefeeding time was much longer with the foraging device than withthe control feeder. Over 90% of the food was eaten within thefirst 15 minutes with the control feeder, whereas it took 60 or75 minutes to reach this percentage using the foraging device,whether it was a V or an H one. Each puzzle required specificskills. Whichever the feeding device, the subjects ate their wholedaily ration and their weight remained stable."

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

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

Brent L, Eichberg JW 1991. Primate puzzleboard: A simple environmentalenrichment device for captive chimpanzees. Zoo Biology10, 353-360
Treat-loaded transparent board with finger holes is attachedto the top of the cage. Mean 'puzzle use' during four 60-minutetrials was 17%.

Brent L, Long KE 1995. The behavioral response of individuallycaged baboons to feeding enrichment and the standard diet: A preliminaryreport. Contemporary Topics in Laboratory Animal Science34(2), 65-69
PVC pipe with finger holes, filled with a mixture of peanutbutter and seeds. The mean amount of feeder use was 51 minutesper 60 minute observation sessions. "Increasing foragingopportunities 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 presentedto six captive chimpanzees housed in pairs. The task successfullyreduced inactivity by about 52%, increased foraging opportunityfrom 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 Enrichment6(2), 9-10
A food puzzle was constructed and modified several times totake into account the subject's high level of intelligence. "Theresults were everything I could have hoped for. Not only did hemaneuver the [food] items through the maze, he also did it withremarkable speed and concentration."

Crockett CM, Bellanca RU, Heffernan KS, Ronan DA, Bonn WF 2001.PuzzleBall foraging device for laboratory monkeys. LaboratoryPrimate Newsletter 40(1), 4-7
"Puzzle Balls are attached outside of the cage. .. Eachanimal was observed for 10 minutes after six pieces of cerealwere placed in the ball. .. Overall, the subjects manipulatedthe Puzzle Ball during 69.5% of the scan samples. ... Four ofthe seven subjects were able to successfully empty (eat plus spill)at least one type of Puzzle Ball in less than 10 minutes. (Mostspilled about as much as they ate.) For the successful animals,it took an average of five minutes to empty the puzzle. ...Eventhough the Puzzle Balls were empty during observations [four ofseven cases], the subjects manipulate them, although an averageof only 1.6% of the time. During the same observations (PuzzleBall present), the subjects manipulated their portable cage toys(at least one per cage) an average of only 0.9% of the time. (Eightof 17 manipulated neither Puzzle nor toy.) .. We were pleasedthat the empty Puzzle Balls were associated with a reduction [approximately60%] in abnormal behavior."

Evans HL, Taylor JD, Ernst J, Graefe JF 1989. Methods to evaluatethe well-being of laboratory primates. Comparison of macaquesand 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 raisinfrom the pickup board [miniature ice cube tray attached to frontof cage]. Experienced macaques emptied the commercial puzzle filledwith the standard food pellet ration within 20 minutes. "Aftera few days experience with the puzzle, macaques ate from bothsources [puzzle feeder and conventional food cup] at the sametime, showing no clear preference for either source. This indicatesa motivation other than taste or caloric need for performing thepuzzle. The puzzle was not adaptable for tamarins since they displayedlittle or no appetite for any hard food items which could be pushedthrough the puzzle. Soft foods, such as grapes, raisins, marshmallowsor marmoset diet were squeezed out through the small holes ratherthan being pushed through the maze of the puzzle."

Fekete JM, Norcross JL, Newman JD 2000. Artificial turf foragingboards as environmental enrichment for pair-housed female squirrelmonkeys. Contemporary Topics in Laboratory Animal Science 39(2),22-26
"Five groups of pair-housed female squirrel monkeys werevideotaped the week prior to, the week following, and for 2 weeksduring the enrichment phase, when treat-enhanced boards were providedfor 2 h daily. During the first 30 min of daily enrichment, inactivitydeclined 35.3%, locomotion increased 3.8%, and board-related behavioroccupied 36.3% of the activity budget; these changes were notevident after 1.5 h." Behavioral disorders were not alteredby the foraging opportunity.

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

*Glenn AS, WatsonJ 2007. Novel nonhuman primate puzzle feeder reduces food wastageand provides environmental enrichment. AALAS [American Associationfor Laboratory Animal Science] 58th National Meeting OfficialProgram , 45

"The feeder dispenses monkey chow and fits on nonhumanprimate group four quad rack cages. .. The original feeders dispensed18 to 20 biscuits. At feeding time, the macaques removed all thebiscuits within 3 min, and those that were not eaten or storedin cheek pouches were pushed back through the feeder onto theroom floor or dropped through the cage floor grid. .. Each feedertook 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, anddecreased clean-up time."

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

Kinsey JH, Jorgensen MJ, Platt DM, Hazen TJ 1996. Food puzzlefeeders: Effects on self-biting and stereotypy in individuallyhoused monkeys. XVIth Congress of the International PrimatologicalSociety/XIXth Conference of the American Society of Primatologists,Abstract No. 683
Subjects were "observed not only when the food puzzlefeeder had just been filled in the early morning but at severalother time points throughout the day. ... There was no effecton self-aggression; however, a reduction in active stereotypicbehavior was noted but only in the first hour of each daily exposure."

Lam K, Rupniak NMJ, Iversen SD 1991. Useof a grooming and foraging substrate to reduce cage stereotypiesin macaques. Journal of Medical Primatology 20, 104-109
"Monkeys given fleece sprinkled with morsels of food didnot groom the fleece, but foraged for long periods (up to 27 min/h).Stereotyped behaviours were reduced by up to 73% by use of thefleece pad both alone and with foraging crumbles."

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

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

Lutz CK, Farrow RA 1996. Foraging device for singly housedlongtailed macaques does not reduce stereotypies. ContemporaryTopics in Laboratory Animal Science 35(3), 75-78
"All [ten] subjects manipulated the foraging boards, butstereotyped behaviors and activity levels were not significantlyaffected 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 dayor on repeated presentation, indicating that there was no noveltyeffect or reduction in motivation."

Maki S, Alford PL, Bloomsmith MA, Franklin J 1989. Food puzzledevice simulating termite fishing for captive chimpanzees (Pantroglodytes). American Journal of Primatology 19(Supplement1), 71-78
"Significant reductions of abnormal behavior and significantincreases in activity occurred with the pipe feeder's availability.Species-typical tool-using activity occurred, and the use of thepipe feeder increased subjects' foraging and feeding activitytoward more species-normative levels." In the corral-housedgroups of nine to 12 animals, competetion for use of the singlepipe feeder appeared to induce aggression, with 47 attacks recordedin the groups when the filled feeder was present and none recorded.. prior to the use of the feeder. ... Multiple puzzle devicesshould be available to group-housed animals to preclude undesirableaggression arising from competition."

Maloney MA, Meiers ST, White J, RomanoMA 2006 . Effects of three food enrichment items on the behaviorof 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 affectedby the food enrichment item that required the most manipulation."

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

Mentz I, Perret K 1999. Environmental enrichment bei Flachlandgorillas(Gorilla g. gorilla) - Beobachtungen zur Nahrungsaufnahmeund zum Manipulationsverhalten. (Environmental enrichment forlowland gorillas - observations of foraging and manipulation behavior)[German text with English summary]. Der Zoologische Garten69, 1-15
"Behavioural enrichment possibilities include greaterdispersal of food as well as the providing of food boxes or raisinsticks. 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 captivecallitrichid primates: Behavioral time budgets and foraging skills.In Housing, Care and Psychological Wellbeing of Captive andLaboratory Primates Segal EF (ed), 89-101. Noyes Publications,Park Ridge
The group-housed animals had to hang from above, or sit onthe covered bowl to obtain raisins that were mixed with groundcorn cob. "The device reduced foraging yield and increasedforaging effort to levels similar to those observed in free-rangingpopulations. These dramatic changes in behavioral profiles wereproduced even though the foraging device was supplemental to,rather than a replacement for, standard provisioning."

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

Murchison MA 1994. Primaryforage feeder for singly-caged macaques. Laboratory PrimateNewsletter 33(1), 7-8
Perforated feeder box requires the single-housed subject touse the fingers to maneuver biscuits to access holes at differentlevels. "Apparently the animals consumed nearly all the foodretrieved from the forage feeders, leaving less on the cage floorto become contaminated. The animals spent significantly more timeforaging with the forage feeder than the standard feeder."

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

Murphy DE 1976. Enrichmentand 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 holesin the cylinder allowed access to the inside. A short sectionof a rubber hose was chained near one hole in the cylinder. Thechimps were able to use the hose as a tool in a manner similarto fishing for termites or opening a beehive in the wild. Thechimpanzees rapidly emptied the container of their morning mealwith ingenious manipulation and intense interest. .... Chimpsand orangs manipulated their feeders even though ample food wasavailable. On days when the device could be operated by the orangutans, they were observed climbing in the structure about thirtyper cent more often than when the device was not operating. Therewas an apparent increase in general activity. The most encouragingresult was a reduction in the female's stereotyped pacing. Theenvironmental enrichment of the chimp exhibit has resulted ina decrease in observable coprophagy, a diversification of theactivities, and a probable improvement in the physical and psychologicalcondition of the animals."

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

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

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

Perret K, Büchner S, Adler HJ 1998. Beschäftigungsprogrammefür Schimpansen (Pan troglodytes) im Zoo. (Environmentalenrichment program for chimpanzees in zoos) [German text withEnglish summary]. Der Zoologische Garten 68, 95-111
An effective feeding enrichment program for group-housed chimpanzeesis described and assessed. The program resulted in a more thantwo-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 environmentalenrichment strategies in captive common marmosets (Callithrixjacchus). Primate Report 42, 24-25
"Access to the puzzles was accompanied by increase insocial 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 scientificexperimentation with conventional housing: A pilot study withrhesus monkeys. American Journal of Primatology 14, 223-234
"The testing apparatus ... was connected to a computerthat controlled the test and the distribution of regular monkeychow as reward." Manipulatory activity required by the apparatusreduced motor stereotypies but not self-biting in single-housedsubjects.

Prist P., Pizzutto CS, Hashimoto C2004. Wovenvine balls and baskets as feeding enrichment for howler monkeys.Shape of Enrichment 14(2), 1-2
"Our results showed that the animals spent more timeforaging when the feeder balls were used [compared to the baskets],since it was more difficult to reach the leaves. The monkeys alsoexplored each of the baskets and stopped spending most of theirtime on the floor. We concluded that these two enrichment ideasincreased the animals' activity through play and exploration,and also increased their use of vertical space and reduced theirtime on the floor. These behaviors are more species-typical andappropriate for arboreal monkeys."

Reinhardt V 1992. Foragingfor commercial chow. Laboratory Primate Newsletter31(2), 10
"While sitting on swings, platforms or other elevatedstructures, or clinging to the mesh, individual animals seizea piece of chow [fruit, vegetable or bread] and retrieve a piece[through the mesh of the ceiling]. This simple 'food puzzle' notonly promotes non-injurious foraging skills but also keeps thefloor relatively clean by avoiding undue spoilage of food. Theanimals only work for food that they actually eat."

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

Reinhardt V 1993. Evaluationof an inexpensive custom-made food puzzle used as primary feederfor pair-housed rhesus macaques. Laboratory Primate Newsletter32(3), 7-8
"Working for their standard food rather than collectingit from freely accessible food boxes did not impair the [pair-housed]animals' body weight maintenance, suggesting that their generalhealth was not impaired by the new feeding technique."

Reinhardt V 1993. Promoting increased foraging behaviour incaged 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-foldincrease in total time engaged in [biscuit ration] food-retrievingactivities."

Reinhardt V 1993. Usingthe mesh ceiling as a food puzzle to encourage foraging behaviourin caged rhesus macaque (Macaca mulatta). AnimalWelfare 2, 165-172
"Daily commercial dry food rations consisting of 33 bar-shapedor 16 star-shaped biscuits per animal were placed on the meshceiling of the cages instead of in the feed-boxes. This inducedan 80-fold increase and 289-fold increase, respectively, in foragingtime" in the pair-housed males.

Reinhardt V 1994. Cagedrhesus macaques voluntarily work for ordinary food. Primates35, 95-98
Individuals spent on average 32 sec retrieving biscuits fromthe ordinary food box, and 673 sec retrieving biscuits from thefood puzzle. "It was inferred that the animals voluntarilyworked for ordinary food, with the expression of foraging activitiesserving as its own reward."

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

Schapiro SJ, Suarez SA, Porter LM, Bloomsmith MA 1996. Theeffects of different types of feeding enhancements on the behaviourof single-caged, yearling rhesus macaques. Animal Welfare5, 129-138
"Enrichment use" in minutes/observation hour wasas 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 providessome combination of stimulating devices and foods that are noveland require processing, can have a very positive impact on thebehaviour of captive primates."

Spector M, Kowalczky MA, Fortman JD, Bennett BT 1994. Designand implementation of a primate foraging tray. ContemporaryTopics in Laboratory Animal Science 33(5), 54-55
"Excreta trays have been modified to include [small] foragingtrays. The trays are placed under the cages. Videotape observationof [single-housed] 24 animals indicates the trays provide from30 to over 120 min of foraging activity."

(4,2) Substrates

Anderson JR, Chamove AS 1984. Allowingcaptive primates to forage. In Standards in LaboratoryAnimal Management. Proceedings of a Symposium 253-256. TheUniversities Federation For Animal Welfare, Potters Bar
A woodchip litter substrate reduces abnormal behaviours, primarilyself-aggression, and encourages foraging, even in the absenceof grain.

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

*Baumans V, CokeC, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A,Reinhardt V, Van Loo P 2007 Making Lives Easier for Animalsin Research Labs - Chapter4.3. Feeding Enrichment. Washington, DC: Animal WelfareInstitute
"Wood shavings in the catch pans provide an ideal substrateto foster foraging activities. On days when we change the pansthree times a week we sprinkle sunflower seeds on the shavings.Our rhesus and squirrel monkeys then search with their fingersthrough the litter and pull the seeds through the floor grids,eat them or store them in their cheek pouches. Since we changethe pans, rather than dump the bedding, we don't have any drainageproblems in the rooms. This feeding enrichment technique doesn'trequire undue extra work time in our colony of approximately 130monkeys. I'd say the benefit of being able to provide even a briefperiod of "natural" foraging behavior for our cagedprimates is worth the little additional time it takes to put thebedding in the pans and add a handful of seeds."

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

Boccia ML 1989. Long-termeffects of a natural foraging task on aggression and stereotypiesin socially housed pigtail macaques. Laboratory PrimateNewsletter 28(2), 18-19
"A supplementary feeding of approximately one cup of sunflowerseeds were dispersed throughout the cage in the woodchip beddingin the middle of the afternoons, 4-6 hours after the group wasfed their daily ration of chow and fruit. ... Two months followingthe introduction of the foraging task .. stereotypies remaineddepressed, and hairpulling remained rare. In addition, beddingexploration and other types of exploration remained elevated,and agonistic behaviors remained low."

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

Bryant CE, Rupniak NMJ, Iversen SD 1988. Effectsof different environmental enrichment devices on cage stereotypiesand autoaggression in captive cynomolgus monkeys. Journalof Medical Primatology 17, 257-269
"Of the many activities available in the playpen, thosethat 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 belowthe grid floor of the cage]."

Burt DA, Plant M 1990. Observationson a caging system for housing stump-tailed macaques. AnimalTechnology 41, 175-179
"The removal of metal grids at the bottom of the cageand the introduction of direct access to a substrate mixed withcereals and seeds, had a beneficial effect on the psychologicalwell-being of the [single-housed] macaques by allowing foragingand, in our experience, up to 60% of our macaques' day is nowspent in this pursuit."

Byrne GD, Suomi SJ 1991. Effects of woodchips and buried foodon behavior patterns and psychological well-being of captive rhesusmonkeys. American Journal of Primatology 23, 141-151
The addition of woodchips increased exploration and feedinglevels. Burial of regular monkey chow in woodchips had littleeffect on behavior beyond that of the woodchips alone, increasingexploration and decreasing passivity. The addition of sunflowerseeds to the woodchips encouraged increased feeding and explorationand led to decreases in passivity and social interaction. No effecton abnormal behavior.

Chamove AS 2001. Floor-coveringresearch benefits primates. Australian Primatology14(3), 16-19
"Many zoos, labs, and people keep animals on concreteor in wire cages. It is believed to be hygienic, efficient, andadequate for the needs of the animals. ... We tested a varietyof floor-coverings-wood-chips, wood-wool, peat, straw, hay, sawdust,and shredded paper from the cigarette industry. The sawdust didnot dry out easily; the paper, wood-wool, hay, and straw did notabsorb urine very well; the peat appeared messy with black dusteverywhere. Peat was the preferred substrate for those gardenerswho worked in the primate unit, and is now enriching some of theflower beds around Stirling Castle. For more practical reasons,we did most of our remaining studies using wood-chips. ... Thebasic study involved scattering the smallest food items we couldfind either onto the bare floor or into some substrate... Aggressionwas reduced. .. Food intake was more evenly distributed. .. Naïvehuman "smellers" rated the small daily from 1 to 4 --none, slight, strong, very strong. A bare pen cleaned daily ratedjust over 1 (slight) on average but received 5 strong and 5 moderateratings. A pen with chips after 4-8 weeks of no cleaning ratedunder 0.6 (none-slight), and only a single moderate rating. ...Monkeyspreferred to sit on a substrate-covered floor to a bare one. Thewalls and viewing windows remained cleaner with a floor-coveringin place. Monkeys used the floor ten times as much as when itwas bare. ... Mature litter is more inhibitory to may diseaseorganisms as well as to yeasts and moulds than fresh litter. ...Wefound NO bad effects ... The monkeys were foraging 14% of thetime through the wood-chips looking for and eating grain eventhough that same grain was available from hoppers full of thestuff nearby."

Combette C, Anderson JR 1991. Réponses à deuxtechniques d'enrichissement environmental chez deux espècesde primates en laboratoire (Cebus apella, Lemur macaco). [Responseto two environmental enrichment techniques in two primate species(Cebus apella, Lemur macaco) in the laboratory setting.(French text with English summary)] . Cahiers d'Ethologie11, 1-16
"Locomotion almost doubled in the lemurs when small fooditems were added to the litter, but only the [group-housed] capuchinsengaged in foraging activities to any extent."

Grief L, Fritz J, Maki S 1992. Alternativeforage types for captive chimpanzees. Laboratory PrimateNewsletter 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 chimpanzeesstill foraging late in the day for these small kernels. In addition,for subjects such as our blind animal, who had one of the highestforaging scores in our study, this [inexpensive] enrichment cannotbe overemphasized."

Lutz CK, Novak MA 1995. Use of foraging racks and shavingsas enrichment tools for groups of rhesus monkeys (Macaca mulatta).Zoo Biology 14, 463-474
Antagonism decreased when the animals had to search for foodin 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. "Wefill the trays with wood chips or other types of bedding scatteredwith crushed maize, rice, or raisins, and attach them to the undersideof the cage floors with bungie cords, thereby providing the animalswith hours of searching activity."

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

Stegenga L 1993. Modifying spider monkey behavior with theuse of environmental variables. The Shape of Enrichment2(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 theleaves were added to the enclosure, playtime was more significant."

(4,3) Produce

*Baumans V, CokeC, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A,Reinhardt V, Van Loo P 2007 Making Lives Easier for Animalsin Research Labs - Chapter4.4. Coconuts. Washington, DC: Animal Welfare Institute
"Rhesus don't care much about coconuts, but stump-tailedmacaques 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 injuredwhile processing a nut.
I give whole coconuts to our individually caged cynos. More thananything, they like them for grooming purposes. It gives themsomething else to do besides bite themselves. I also had a femalewho carried her coconut around as if it was a baby, constantlyclutching it to her chest, and lip smacking to it, grooming it,etc. She was a chronic alopecia case. The coconut alleviated someunfortunately not all of her stereotypical hair pulling behavior."

*
Baumans V, Coke C,Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, ReinhardtV, Van Loo P 2007 Making Lives Easier for Animals in ResearchLabs - Chapter4.3. Feeding Enrichment. Washington, DC: Animal WelfareInstitute
"I have given whole watermelons to group-housed rhesus,cynos, bonnet and stump-tailed macaques for several years withoutnoticeable adverse effects. It would be a waste of time to cutthe melons into small pieces. The monkeys first gnaw a hole intothe rind and then "dig" into the soft and juicy part.They really like this and are kept busy until the last morselhas been eaten. They usually discard the rind, but before theydo so they thoroughly remove any soft material and eat it. Thisusually 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- andgroup-housed environments. I would say that this is one of themost 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-housedrhesus and baboons. They love it, and I enjoy observing them "peeland eat," leaving a big mess after they have finished. Theygnaw the cob into little pieces that finally fall through thegrid floor on the pans. I cannot say whether they actually alsoeat pieces of the cob, but we have never encountered any health-relatedproblem. 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 andeating the corn. They typically pick the kennels both with theirhands and their teeth. When they are done, they proceed gnawingon 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. Threeinexpensive environmental enrichment options for group-housedMacaca mulatta. Laboratory Primate Newsletter31(1), 7-8
"We distributed the following enrichment materials onthe floor once a week, each on a different day: (1) 1 kg roastedpeanuts in their shells; (2) 32 ears of hard corn; (3) one non-corrugatedcardboard box. ... After a habituation period of 8 weeks, [2-hour]behavioral observations were made. ...The corn was the most effectiveeliciter of foraging activity, engaging the animals about 77%of the time. Next in effectiveness was the box (65%) and finallythe peanuts (47%)."

Bennett BT, Spector MR 1989. The use of naturally occurringmanipulanda to improve the psychological well-being of singlyhoused baboons. Journal of the American Veterinary MedicalAssociation 194, 1782
The single-housed animals demonstrated a marked reduction ofcage stereotypy during the time they had the corn to manipulate.

Nadler RD, Herndon JG, Metz B, Ferrer AC, Erwin J 1992. Environmentalenrichment by varied feeding strategies for individually cagedyoung 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 contactingfood [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 daysthey received the ear of corn. Stereotypical behavior, which occursat relatively low frequencies under natural conditions, was reducedsomewhat when the animals were fed three [rather than one] meals."

Waugh C 2002. Coconutsas enrichment item for macaques.Wisconsin Primate Research Center, University of Wisconsin-Madison,Primate Enrichment Forum (electronic discussion group), October24, 2002
"I give whole coconuts, and have had them last a longtime (days/ weeks), until we exchange them with new ones (theyare really durable). I have had one male cyno break one open bythrowing it around his cage for a few days in a row, and eventhen it just cracked - he loved the milk and continued to amusehimself by trying to get to the fleshy part inside until we eventuallyhad to take it away from him because it got kind of gross! Morethan anything, I think they like them for grooming purposes -it gives them something else to do besides bite themselves. Ialso had a female cyno who carried her coconut around like itwas a baby, constantly clutching it to her chest, and lip smackingto it, grooming it, etc. She was a chronic alopecia case, andthe 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-directedand recreational underwater swimming in captive rhesus monkeys(Macaca mulatta). Laboratory Primate Newsletter31(4), 1-4
"Facilitating thermoregulation and increasing [solitaryand social] play are two reasons to consider a swimming facilityto be a cheap and clean environmental enrichment."

Anonymous 2006. Isa swimming pool safe for macaques? A discussion. LaboratoryPrimate Newsletter 45(3), 13
Experience suggest that the provision of a shallow swimmingpool provides aneffective, safe environmental enrichment optionfor macaques.

*Baumans V, CokeC, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A,Reinhardt V, Van Loo P 2007 Making Lives Easier for Animalsin Research Labs - Chapter8.7. Swimming Pools for Macaques. Washington, DC: AnimalWelfare Institute
"We give our pair-housed cynos "bathtubs," filledwith 30 to 40 cm deep warm water, a few times a week, and havenever encountered any problems other than a lot of splashing.Some monkeys take luxurious baths, others climb a perch and jumpinto the water, others sit on the side walls and drag their handsin the water, and others wash their fruit in the water. Usuallythe monkeys make a real mess within the first half hour, and yesthey do urinate/defecate in the water. We empty the tubs afterabout two hours, if the monkeys haven't done it already themselveswhich is often the case.
There are a few published articles on the use of swimming poolsfor rhesus, long-tailed and Japanese macaques. None of these papersmention any safety or hygienic problems."

Fritz J, Howell S 1993. Thedisappearing ice cube. Laboratory Primate Newsletter32(1), 8
Ice "cubes are distributed across the floor, hidden inhigh plastic barrels (we call these igloos), tucked into cornersof the cages, etc. As the animals come out, the excitement ofthe hunt starts and continues until the last ice cube is found.Hoarders clutch them to their chests, ... others fill their mouthsand carry the cubes to the top of the cage, where they lay themdown and watch carefully as the cubes get smaller and smaller.Still others have learned to skate through the puddles, makingmad dashes in order to slide further and further." No detrimentaleffects have been found of providing the ice cubes.

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

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

McNulty J 1993. Enrichmentfor primates in a toxicology facility. Laboratory PrimateNewsletter 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 activityand 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 sourcesmay elicit a broad spectrum of species-typical activity and maybe a simple and inexpensive way to enrich the environment of captive[group-housed] rhesus monkeys. ... Standing water was more effectivethan running water in increasing exploration and object manipulation."

Poulsen E 1994. Monkeys on ice. The Shape of Enrichment3(1), 7
"I spent an hour or so shoveling fresh, clean new snowinto a huge plastic bin and dumped the lot on the floors of eachsmall primate and prosimian indoor enclosure... The event wasa tremendous success"

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

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

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

(4,5) Food Preparation and Feeding Schedule

Fritz J, Howell S 1993. Thedisappearing ice cube. Laboratory Primate Newsletter32(1), 8
Ice "cubes are distributed across the floor, hidden inhigh plastic barrels (we call these igloos), tucked into cornersof the cages, etc. As the animals come out, the excitement ofthe hunt starts and continues until the last ice cube is found.Hoarders clutch them to their chests, ... others fill their mouthsand carry the cubes to the top of the cage, where they lay themdown and watch carefully as the cubes get smaller and smaller.Still others have learned to skate through the puddles, makingmad dashes in order to slide further and further." No detrimentaleffects have been found of providing the ice cubes.

Kerridge FJ 2005. Environmental enrichmentto address behavioral differences between wild and captive balck-and-whiteruffed lemurs (Varecia variegata). American Journalof Primatology 66, 71-84
"Behavioral enrichment experiments were carried out inwhich whole rather than chopped fruit was provided and presentedin a more naturalistic manner [whole fruit suspended by sisalor jute from wooden polses]. ... Manual manipulation of dietaryitems increased. Time spent feeding also increased significantly... The novel feeding method successfully stimulated the animalsto use their hands to obtain and process fruit. It also necessitatedbipedal and tripedal suspension. .. The enrichment increased thetime spent feeding to levels similar to those seen in the wild.".

McNulty J 1993. Enrichmentfor primates in a toxicology facility. Laboratory PrimateNewsletter 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 activityand 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 sourcesmay elicit a broad spectrum of species-typical activity and maybe a simple and inexpensive way to enrich the environment of captive[group-housed] rhesus monkeys. ... Standing water was more effectivethan running water in increasing exploration and object manipulation."

Potratz KR, Boettcher C 2006. Rhesusdiet smoothies. Tech Talk 11(4), 5
There are a number of situations in which non-human primatesneed a special diet to provide additional calories. The receipefor a Chow Smoothie for Rhesus macaques is described and consistsin incorporating the animal's regular food, tailoring the smoothieto the individual animal's needs, and adding specific supplements,medications, and different flavors. The smoothie was tested on40 Rhesus macaques ranging in age from 2 to 25 years.

Poulsen E 1994. Monkeys on ice. The Shape of Enrichment3(1), 7
"I spent an hour or so shoveling fresh, clean new snowinto a huge plastic bin and dumped the lot on the floors of eachsmall primate and prosimian indoor enclosure... The event wasa tremendous success"

Rademacher A 1997. Gorilla treats served poolside. The Shapeof Enrichment 6(3), 11
"Initially, Rocky was hesitant and seemed a bit irritatedat 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 makesuse of the pool occasionally during our hot Arkansas summers,sitting on the bottom, with his arms stretched along the pool'sedge"

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

(5) PromotingArboreal Behavior


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